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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases</title><author><name sortKey="Kell, Douglas B" sort="Kell, Douglas B" uniqKey="Kell D" first="Douglas B" last="Kell">Douglas B. Kell</name><affiliation><nlm:aff id="I1">School of Chemistry and Manchester Interdisciplinary Biocentre, The University of Manchester, 131 Princess St, Manchester, M1 7DN, UK</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">19133145</idno><idno type="pmc">2672098</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2672098</idno><idno type="RBID">PMC:2672098</idno><idno type="doi">10.1186/1755-8794-2-2</idno><date when="2009">2009</date><idno type="wicri:Area/Pmc/Corpus">000223</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases</title><author><name sortKey="Kell, Douglas B" sort="Kell, Douglas B" uniqKey="Kell D" first="Douglas B" last="Kell">Douglas B. Kell</name><affiliation><nlm:aff id="I1">School of Chemistry and Manchester Interdisciplinary Biocentre, The University of Manchester, 131 Princess St, Manchester, M1 7DN, UK</nlm:aff></affiliation></author></analytic><series><title level="j">BMC Medical Genomics</title><idno type="eISSN">1755-8794</idno><imprint><date when="2009">2009</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>The production of peroxide and superoxide is an inevitable consequence of aerobic metabolism, and while these particular 'reactive oxygen species' (ROSs) can exhibit a number of biological effects, they are not of themselves excessively reactive and thus they are not especially damaging at physiological concentrations. However, their reactions with poorly liganded iron species can lead to the catalytic production of the very reactive and dangerous hydroxyl radical, which is exceptionally damaging, and a major cause of chronic inflammation.</p></sec><sec><title>Review</title><p>We review the considerable and wide-ranging evidence for the involvement of this <underline>combination</underline> of (su)peroxide and poorly liganded iron in a large number of physiological and indeed pathological processes and inflammatory disorders, especially those involving the progressive degradation of cellular and organismal performance. These diseases share a great many similarities and thus might be considered to have a common cause (i.e. iron-catalysed free radical and especially hydroxyl radical generation).</p><p>The studies reviewed include those focused on a series of cardiovascular, metabolic and neurological diseases, where iron can be found at the sites of plaques and lesions, as well as studies showing the significance of iron to aging and longevity. The effective chelation of iron by natural or synthetic ligands is thus of major physiological (and potentially therapeutic) importance. As systems properties, we need to recognise that physiological observables have multiple molecular causes, and studying them in isolation leads to inconsistent patterns of apparent causality when it is the <underline>simultaneous combination</underline> of multiple factors that is responsible.</p><p>This explains, for instance, the decidedly mixed effects of antioxidants that have been observed, since in some circumstances (especially the presence of poorly liganded iron) molecules that are nominally antioxidants can actually act as pro-oxidants. The reduction of redox stress thus requires suitable levels of both antioxidants and effective iron chelators. Some polyphenolic antioxidants may serve both roles.</p><p><underline>Understanding the exact speciation and liganding of iron in all its states is thus crucial to separating its various pro- and anti-inflammatory activities.</underline> Redox stress, innate immunity and pro- (and some anti-)inflammatory cytokines are linked in particular via signalling pathways involving NF-kappaB and p38, with the oxidative roles of iron here seemingly involved upstream of the IkappaB kinase (IKK) reaction. In a number of cases it is possible to identify mechanisms by which ROSs and poorly liganded iron act synergistically and autocatalytically, leading to 'runaway' reactions that are hard to control unless one tackles multiple sites of action simultaneously. Some molecules such as statins and erythropoietin, not traditionally associated with anti-inflammatory activity, do indeed have 'pleiotropic' anti-inflammatory effects that may be of benefit here.</p></sec><sec><title>Conclusion</title><p>Overall we argue, by synthesising a widely dispersed literature, that the role of poorly liganded iron has been rather underappreciated in the past, and that in combination with peroxide and superoxide its activity underpins the behaviour of a great many physiological processes that degrade over time. Understanding these requires an integrative, systems-level approach that may lead to novel therapeutic targets.</p></sec></div></front><back><div1 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article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">BMC Med Genomics</journal-id><journal-title>BMC Medical Genomics</journal-title><issn pub-type="epub">1755-8794</issn><publisher><publisher-name>BioMed Central</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">19133145</article-id><article-id pub-id-type="pmc">2672098</article-id><article-id pub-id-type="publisher-id">1755-8794-2-2</article-id><article-id pub-id-type="doi">10.1186/1755-8794-2-2</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases</article-title></title-group><contrib-group><contrib id="A1" corresp="yes" contrib-type="author"><name><surname>Kell</surname><given-names>Douglas B</given-names></name><xref ref-type="aff" rid="I1">1</xref><email>dbk@manchester.ac.uk</email></contrib></contrib-group><aff id="I1"><label>1</label>School of Chemistry and Manchester Interdisciplinary Biocentre, The University of Manchester, 131 Princess St, Manchester, M1 7DN, UK</aff><pub-date pub-type="collection"><year>2009</year></pub-date><pub-date pub-type="epub"><day>8</day><month>1</month><year>2009</year></pub-date><volume>2</volume><fpage>2</fpage><lpage>2</lpage><ext-link ext-link-type="uri" xlink:href="http://www.biomedcentral.com/1755-8794/2/2"></ext-link><history><date date-type="received"><day>2</day><month>9</month><year>2008</year></date><date date-type="accepted"><day>8</day><month>1</month><year>2009</year></date></history><permissions><copyright-statement>Copyright © 2009 Kell; licensee BioMed Central Ltd.</copyright-statement><copyright-year>2009</copyright-year><copyright-holder>Kell; licensee BioMed Central Ltd.</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/2.0"><p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/2.0"></ext-link>), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</p><pmc-comment>
Kell
B
Douglas
dbk@manchester.ac.uk
Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases
2009 BMC Medical Genomics 2(1): 2-. (2009) 1755-8794(2009)2:1<2> urn:ISSN:1755-8794
</license></permissions><abstract><sec><title>Background</title><p>The production of peroxide and superoxide is an inevitable consequence of aerobic metabolism, and while these particular 'reactive oxygen species' (ROSs) can exhibit a number of biological effects, they are not of themselves excessively reactive and thus they are not especially damaging at physiological concentrations. However, their reactions with poorly liganded iron species can lead to the catalytic production of the very reactive and dangerous hydroxyl radical, which is exceptionally damaging, and a major cause of chronic inflammation.</p></sec><sec><title>Review</title><p>We review the considerable and wide-ranging evidence for the involvement of this <underline>combination</underline> of (su)peroxide and poorly liganded iron in a large number of physiological and indeed pathological processes and inflammatory disorders, especially those involving the progressive degradation of cellular and organismal performance. These diseases share a great many similarities and thus might be considered to have a common cause (i.e. iron-catalysed free radical and especially hydroxyl radical generation).</p><p>The studies reviewed include those focused on a series of cardiovascular, metabolic and neurological diseases, where iron can be found at the sites of plaques and lesions, as well as studies showing the significance of iron to aging and longevity. The effective chelation of iron by natural or synthetic ligands is thus of major physiological (and potentially therapeutic) importance. As systems properties, we need to recognise that physiological observables have multiple molecular causes, and studying them in isolation leads to inconsistent patterns of apparent causality when it is the <underline>simultaneous combination</underline> of multiple factors that is responsible.</p><p>This explains, for instance, the decidedly mixed effects of antioxidants that have been observed, since in some circumstances (especially the presence of poorly liganded iron) molecules that are nominally antioxidants can actually act as pro-oxidants. The reduction of redox stress thus requires suitable levels of both antioxidants and effective iron chelators. Some polyphenolic antioxidants may serve both roles.</p><p><underline>Understanding the exact speciation and liganding of iron in all its states is thus crucial to separating its various pro- and anti-inflammatory activities.</underline> Redox stress, innate immunity and pro- (and some anti-)inflammatory cytokines are linked in particular via signalling pathways involving NF-kappaB and p38, with the oxidative roles of iron here seemingly involved upstream of the IkappaB kinase (IKK) reaction. In a number of cases it is possible to identify mechanisms by which ROSs and poorly liganded iron act synergistically and autocatalytically, leading to 'runaway' reactions that are hard to control unless one tackles multiple sites of action simultaneously. Some molecules such as statins and erythropoietin, not traditionally associated with anti-inflammatory activity, do indeed have 'pleiotropic' anti-inflammatory effects that may be of benefit here.</p></sec><sec><title>Conclusion</title><p>Overall we argue, by synthesising a widely dispersed literature, that the role of poorly liganded iron has been rather underappreciated in the past, and that in combination with peroxide and superoxide its activity underpins the behaviour of a great many physiological processes that degrade over time. Understanding these requires an integrative, systems-level approach that may lead to novel therapeutic targets.</p></sec></abstract></article-meta></front><body><sec><title>Background and preamble</title><p>The 'balkanisation' of the literature is in part due to the amount of it (some 25,000 journals with presently 2.5 million <bold>peer-reviewed</bold> papers per year, i.e. ~5 <bold>per minute </bold>[<xref ref-type="bibr" rid="B1">1</xref>]), with a number <ext-link ext-link-type="uri" xlink:href="http://www.nlm.nih.gov/bsd/medline_cit_counts_yr_pub.html"></ext-link> increasing by something approaching 2 <bold>per minute</bold> at PubMed/Medline alone. In addition, the disconnect between the papers in the literature (usually as pdf files) and the metadata describing them (author, journal, year, pages, etc) is acute and badly needs filling [<xref ref-type="bibr" rid="B2">2</xref>]. Without solving this problem, and without automation of the processes of reading, interpreting and exploiting this literature and its metadata in a digital format, we cannot make use of the existing tools for text mining and natural language processing (e.g. [<xref ref-type="bibr" rid="B3">3</xref>-<xref ref-type="bibr" rid="B5">5</xref>]), for joining disparate concepts [<xref ref-type="bibr" rid="B6">6</xref>], for literature-based discovery (e.g. [<xref ref-type="bibr" rid="B7">7</xref>-<xref ref-type="bibr" rid="B11">11</xref>], and for studies of bibliometrics [<xref ref-type="bibr" rid="B12">12</xref>,<xref ref-type="bibr" rid="B13">13</xref>], literature dynamics [<xref ref-type="bibr" rid="B14">14</xref>], knowledge domains [<xref ref-type="bibr" rid="B15">15</xref>], detecting republication [<xref ref-type="bibr" rid="B16">16</xref>] and so on. Until we recognise these possibilities we are unlikely to seek to realise them.</p><p>The present article (and see [<xref ref-type="bibr" rid="B17">17</xref>] for a preprint) serves to show some of the benefits than can accrue from a more overarching view of the otherwise highly disparate literature in a particular domain (see also [<xref ref-type="bibr" rid="B18">18</xref>]), but was done 'the hard way', i.e. with a few bibliographic and bibliometric tools but without the kind of automation implied above. For the record, the main tools used (see a review in [<xref ref-type="bibr" rid="B2">2</xref>]) were Web of Knowledge and Scopus for literature and citation searching, supplemented by Google Scholar. Some use was also made of ARROWSMITH [<xref ref-type="bibr" rid="B6">6</xref>,<xref ref-type="bibr" rid="B19">19</xref>,<xref ref-type="bibr" rid="B20">20</xref>] and GOPubMed [<xref ref-type="bibr" rid="B21">21</xref>], as well as various workflows in the Taverna environment [<xref ref-type="bibr" rid="B22">22</xref>-<xref ref-type="bibr" rid="B26">26</xref>], including the BioAID_DiseaseDiscovery workflow <ext-link ext-link-type="uri" xlink:href="http://www.myexperiment.org/workflows/72"></ext-link> written by Marco Roos. Citations and attendant metadata were stored in Endnote (latterly version X).</p></sec><sec><title>Introduction</title><p>Even under 'normal' conditions, as well as during ischaemia when tissue oxygenation levels are low, the redox poise of the mitochondrial respiratory chain is such that the normally complete four-electron reduction of dioxygen to water is also accompanied by the production, at considerable rates (ca 1–4% of O<sub>2 </sub>reduced), of partially reduced forms of dioxygen such as hydrogen peroxide and superoxide (e.g. [<xref ref-type="bibr" rid="B27">27</xref>-<xref ref-type="bibr" rid="B45">45</xref>]). These 1- and 2-electron reductions of O<sub>2 </sub>are necessarily exacerbated when the redox poise of the b-type cytochromes is low, for instance when substrate supplies are in excess or when the terminal electron acceptor O<sub>2 </sub>is abnormally low due to hypoxia or ischaemia. Various other oxygenases, oxidases and peroxidases can also lead directly to the production of such 'reduced' forms of dioxygen <italic>in vivo </italic>(e.g. [<xref ref-type="bibr" rid="B46">46</xref>-<xref ref-type="bibr" rid="B48">48</xref>]), with H<sub>2</sub>O<sub>2 </sub>from xanthine oxidase being especially implicated in ischaemia/reperfusion injury (e.g. [<xref ref-type="bibr" rid="B47">47</xref>,<xref ref-type="bibr" rid="B49">49</xref>-<xref ref-type="bibr" rid="B54">54</xref>]). These molecules (peroxide and superoxide) can cause or contribute to various kinds of oxidative stress. However, this is mainly not in fact because they can react directly with tissue components themselves, since they are <underline>comparatively</underline> non-toxic, cells have well-known means of dealing with them [<xref ref-type="bibr" rid="B55">55</xref>], and they are even used in cellular signalling (e.g. [<xref ref-type="bibr" rid="B56">56</xref>-<xref ref-type="bibr" rid="B60">60</xref>]). Much more importantly, it is because they can react with other particular species to create far more reactive and damaging products such as hydroxyl radicals, with all these agents nevertheless being known collectively (and indiscriminately) as reactive oxygen species (ROSs). Possibly the commonest means by which such much more damaging species, in particular the hydroxyl radical, are created is by reaction with unliganded or incompletely liganded iron ions [<xref ref-type="bibr" rid="B61">61</xref>-<xref ref-type="bibr" rid="B63">63</xref>]. <underline><bold>The themes of this review are thus (i) that it is this <italic>combination</italic> of poorly liganded iron species, coupled to the natural production of ROSs, that is especially damaging, (ii) that the role of iron has received far less attention than has the general concept of ROSs, albeit the large literature that we review, and (iii) that this basic combination underpins a great many (and often similar) physiological changes leading to a variety of disease manifestations, and in particular those where the development of the disease is manifestly progressive and degenerative.</bold></underline></p><p>An overview of the structure of the review is given in Fig <xref ref-type="fig" rid="F1">1</xref>, in the form of a 'mind map' [<xref ref-type="bibr" rid="B64">64</xref>]. The main literature review for this meta-analysis was completed on June 30<sup>th</sup>, 2008, with some updates being added following the refereeing process.</p><fig position="float" id="F1"><label>Figure 1</label><caption><p><bold>An overview of this article, set out in the form of a 'mind map' </bold>[<xref ref-type="bibr" rid="B64">64</xref>].</p></caption><graphic xlink:href="1755-8794-2-2-1"></graphic></fig></sec><sec><title>Some relevant chemistry of iron and reduced forms of oxygen</title><p>While superoxide and peroxide are the proximate forms of incomplete O<sub>2 </sub>reduction in biology, a reaction catalysed by the enzyme superoxide dismutase [<xref ref-type="bibr" rid="B65">65</xref>] serves to equilibrate superoxide and peroxide:</p><p><disp-formula id="bmcM1"><label>(1)</label>2O<sub>2</sub><sup>•- </sup>+ 2H<sup>+ </sup>→ H<sub>2</sub>O<sub>2 </sub>+ O<sub>2 </sub></disp-formula></p><p>Arguably the most important reaction of hydrogen peroxide with (free or poorly liganded) Fe(II) is the Fenton reaction [<xref ref-type="bibr" rid="B66">66</xref>], leading to the very reactive and damaging hydroxyl radical (OH<sup>•</sup>)</p><p><disp-formula id="bmcM2"><label>(2)</label>Fe(II) + H<sub>2</sub>O<sub>2 </sub>→ Fe(III) + OH<sup>- </sup>+ OH<sup>•</sup></disp-formula></p><p>Superoxide can also react with ferric iron in the Haber-Weiss reaction [<xref ref-type="bibr" rid="B67">67</xref>] to produce Fe(II) again, thereby effecting redox cycling:</p><p><disp-formula id="bmcM3"><label>(3)</label>O<sub>2</sub><sup>•- </sup>+ Fe(III) → O<sub>2 </sub>+ Fe(II)</disp-formula></p><p>Ascorbate can replace O<sub>2</sub><sup>•- </sup>within the cell for reducing the Fe(III) to Fe(II) [<xref ref-type="bibr" rid="B68">68</xref>]. Further reactions, that are not the real focus here, follow from the ability of hydroxyl radicals and indeed Fe(n) directly to interact with many biological macro- and small molecules, especially including DNA, proteins and unsaturated lipids. Thus [<xref ref-type="bibr" rid="B69">69</xref>-<xref ref-type="bibr" rid="B73">73</xref>], Fe(II) and certain Fe(II) chelates react with lipid hydroperoxides (ROOH), as they do with hydrogen peroxide, splitting the O--O bond. This gives RO<sup>•</sup>, an alkoxyl radical, which can also abstract H<sup>• </sup>from polyunsaturated fatty acids and from hydroperoxides. The resulting peroxyl radicals ROO<sup>• </sup>can continue propagation of lipid peroxidation. Oxidative stress also leads to considerable DNA damage [<xref ref-type="bibr" rid="B74">74</xref>-<xref ref-type="bibr" rid="B76">76</xref>] and to the polymerisation and denaturation of proteins [<xref ref-type="bibr" rid="B77">77</xref>-<xref ref-type="bibr" rid="B79">79</xref>] and proteolipids that can together form insoluble structures typically known as lipofucsin (see e.g. [<xref ref-type="bibr" rid="B80">80</xref>,<xref ref-type="bibr" rid="B81">81</xref>]) or indeed plaques. <bold><italic>Such plaques can also entrap the catalysts of their formation, and thereby point them up</italic></bold>. Some of the evidence for these is described below. Many small molecule metabolic markers for this kind of <bold>oxidative stress </bold>induced by the hydroxyl radical and other 'reactive oxygen species' (ROSs) are known [<xref ref-type="bibr" rid="B43">43</xref>,<xref ref-type="bibr" rid="B82">82</xref>-<xref ref-type="bibr" rid="B89">89</xref>], and include 8-oxo-guanine [<xref ref-type="bibr" rid="B90">90</xref>-<xref ref-type="bibr" rid="B94">94</xref>], 8-hydroxy guanine [<xref ref-type="bibr" rid="B95">95</xref>], 8-hydroxy-2'-deoxy-guanosine [<xref ref-type="bibr" rid="B96">96</xref>,<xref ref-type="bibr" rid="B97">97</xref>], 8-oxo-GTP [<xref ref-type="bibr" rid="B98">98</xref>], 4-hydroxy-2-hexenal [<xref ref-type="bibr" rid="B99">99</xref>], 4-hydroxy-nonenal [<xref ref-type="bibr" rid="B100">100</xref>], 4-hydroperoxy-2-nonenal, various isoprostanes [<xref ref-type="bibr" rid="B101">101</xref>-<xref ref-type="bibr" rid="B107">107</xref>], 7-keto-cholesterol [<xref ref-type="bibr" rid="B108">108</xref>], many other cholesterol derivatives [<xref ref-type="bibr" rid="B109">109</xref>], malondialdehyde [<xref ref-type="bibr" rid="B110">110</xref>], neopterin [<xref ref-type="bibr" rid="B111">111</xref>], nitrotyrosine [<xref ref-type="bibr" rid="B112">112</xref>-<xref ref-type="bibr" rid="B115">115</xref>] and thymidine glycol [<xref ref-type="bibr" rid="B116">116</xref>,<xref ref-type="bibr" rid="B117">117</xref>]. Note that the trivial names in common use for this kind of metabolite are not helpful and may even be ambiguous or misleading, and it is desirable (e.g. [<xref ref-type="bibr" rid="B118">118</xref>]) to refer to such molecules using terminology that relates them either to molecules identified in persistent curated datbases [<xref ref-type="bibr" rid="B119">119</xref>] such as ChEBI [<xref ref-type="bibr" rid="B120">120</xref>] or KEGG [<xref ref-type="bibr" rid="B121">121</xref>], or better to describe them via database-independent encodings such as SMILES [<xref ref-type="bibr" rid="B122">122</xref>] or InChI [<xref ref-type="bibr" rid="B123">123</xref>-<xref ref-type="bibr" rid="B128">128</xref>] strings. (There are other oxidative markers that may be less direct, such as the ratio of 6-keto-prostaglandin F1α to thromboxane B2 [<xref ref-type="bibr" rid="B129">129</xref>], but these are not our focus here.)</p><p>Overall, it is in fact well established that the interactions between 'iron' <italic>sensu lato </italic>and partly reduced forms of oxygen can lead to the production of the very damaging hydroxyl radical (e.g. [<xref ref-type="bibr" rid="B43">43</xref>,<xref ref-type="bibr" rid="B130">130</xref>-<xref ref-type="bibr" rid="B139">139</xref>]), and that <bold>this radical in particular probably underpins or mediates many higher-level manifestations of tissue damage, disease, organ failure and ultimately death</bold>[<xref ref-type="bibr" rid="B36">36</xref>,<xref ref-type="bibr" rid="B137">137</xref>,<xref ref-type="bibr" rid="B140">140</xref>-<xref ref-type="bibr" rid="B143">143</xref>]. While the role of ROSs generally in these processes has been widely discussed, the general recognition of the importance of inadequately liganded iron in each of them has perhaps been less than fully appreciated. One of our tasks here will therefore be to stress this role of 'iron', and to assess the various means of chelating 'iron' such that it does not in fact do this. (Throughout we use 'iron' to refer to forms of Fe(n, n > 0) with unspecified ligands, though we absolutely stress that it is the <underline>exact</underline> speciation and liganding that determines the reactivity of 'iron' in catalysing reactions such as that of hydroxyl radical formation, and indeed its bioavailability generally – inadequate liganding of iron in the required forms can be a cause of anaemia even if the total amount of 'iron' is plentiful.)</p><p>For completeness we note the reactions catalysed by superoxide dismutase</p><p><disp-formula id="bmcM4"><label>(4)</label>2O<sub>2</sub><sup>•- </sup>+ 2H<sup>+ </sup>→ O<sub>2 </sub>+ H<sub>2</sub>O<sub>2 </sub></disp-formula></p><p>and by catalase</p><p><disp-formula id="bmcM5"><label>(5)</label>H<sub>2</sub>O<sub>2 </sub>→ H<sub>2</sub>O + 1/2 O<sub>2 </sub></disp-formula></p><p>These together, were their activity in the relevant locations sufficiently great, might serve to remove (su)peroxide from cells completely.</p><p>In addition to reactive oxygen species there are ions such as the perferryl ion (Fe-O) [<xref ref-type="bibr" rid="B144">144</xref>] and reactive nitrogen species [<xref ref-type="bibr" rid="B60">60</xref>,<xref ref-type="bibr" rid="B145">145</xref>-<xref ref-type="bibr" rid="B147">147</xref>]. These latter are mainly formed from the natural radical NO, an important inflammatory mediator [<xref ref-type="bibr" rid="B148">148</xref>], with peroxynitrite production (from the reaction of NO and superoxide) [<xref ref-type="bibr" rid="B46">46</xref>,<xref ref-type="bibr" rid="B149">149</xref>-<xref ref-type="bibr" rid="B154">154</xref>] leading to nitrotyrosine [<xref ref-type="bibr" rid="B112">112</xref>], or nitro-fatty acid [<xref ref-type="bibr" rid="B155">155</xref>,<xref ref-type="bibr" rid="B156">156</xref>] or protein cystein nitrosylation [<xref ref-type="bibr" rid="B157">157</xref>,<xref ref-type="bibr" rid="B158">158</xref>] being a common means of their detection downstream. Other toxic products of the reactions of NO include NO<sub>2</sub>, N<sub>2</sub>O<sub>3</sub>, and S-nitrosothiols [<xref ref-type="bibr" rid="B159">159</xref>], and the sequelae of some of these may also involve iron [<xref ref-type="bibr" rid="B160">160</xref>].</p><p>Overall, we recognise that these kinds of inflammatory, oxidative stress-related reactions are accumulative and somewhat irreversible [<xref ref-type="bibr" rid="B161">161</xref>], that they are consequently age-related, and (see [<xref ref-type="bibr" rid="B162">162</xref>-<xref ref-type="bibr" rid="B165">165</xref>] and later), and that most diseases and causes of mortality that are prevalent in the developed world are in this sense largely manifestations of this kind of aging.</p></sec><sec><title>Ligands and siderophores</title><p>As well as the reactions described above, ferrous ions will react with oxygen under aerobic conditions to produce ferric ions, and in natural environments there is little to stop this. Consequently, and because these reflect fundamental physicochemical properties of such ions, the problems of both solubility and toxicity were faced by bacteria (and indeed fungi [<xref ref-type="bibr" rid="B166">166</xref>-<xref ref-type="bibr" rid="B169">169</xref>]) long ago in evolution, and were solved by their creation and excretion of (mainly ferric-)iron chelators known as siderophores [<xref ref-type="bibr" rid="B170">170</xref>-<xref ref-type="bibr" rid="B189">189</xref>] (and for haemophores see [<xref ref-type="bibr" rid="B190">190</xref>]). These typically have extremely tight binding constants (K<sub>f </sub>> 10<sup>30 </sup>[<xref ref-type="bibr" rid="B191">191</xref>]) and can solubilise and sequester iron such that it can be internalised via suitable transporter molecules within the bacterial plasma membrane [<xref ref-type="bibr" rid="B192">192</xref>]. Bacterial and fungal siderophores usually form hexadentate octahedral complexes with ferric iron and typically employ hydroxamates, α-hydroxycarboxylates and catechols as extremely effective Fe<sup>3+ </sup>ligands [<xref ref-type="bibr" rid="B182">182</xref>]. Since bacterial growth requires iron, it is unsurprising that siderophores are effectively virulence factors (e.g. [<xref ref-type="bibr" rid="B174">174</xref>,<xref ref-type="bibr" rid="B193">193</xref>-<xref ref-type="bibr" rid="B196">196</xref>]). While upwards of 500 microbial siderophores have been identified [<xref ref-type="bibr" rid="B182">182</xref>], with new ones still appearing (some via genomic analyses, e.g. [<xref ref-type="bibr" rid="B197">197</xref>]), and with the most common one in medical use, desferrioxamine or DFO, being such a bacterial product (see below), it is an astonishing fact that no human siderophore has been chemically identified, even though such activities were detected nearly 30 years ago [<xref ref-type="bibr" rid="B198">198</xref>,<xref ref-type="bibr" rid="B199">199</xref>] (see also [<xref ref-type="bibr" rid="B200">200</xref>-<xref ref-type="bibr" rid="B205">205</xref>]). As noted by Kaplan [<xref ref-type="bibr" rid="B206">206</xref>], "a discovery that mammals produce siderophores would lead to an epochal change in the paradigm of mammalian iron homeostasis." To this end, some recent events have begun to change matters, and our overall knowledge of the regulation of iron metabolism, considerably.</p></sec><sec><title>Mammalian iron metabolism</title><p>The total body iron in an adult male is 3000 to 4000 mg and the daily iron requirement for erythropoiesis, the major 'sink', is about 20 mg [<xref ref-type="bibr" rid="B207">207</xref>]. However, the loss of iron in a typical adult male is very small [<xref ref-type="bibr" rid="B208">208</xref>,<xref ref-type="bibr" rid="B209">209</xref>] and can be met by absorbing just 1 – 2 mg of iron per day [<xref ref-type="bibr" rid="B210">210</xref>,<xref ref-type="bibr" rid="B211">211</xref>]. The careful conservation and recycling of iron – mainly from degrading erythrocytes – is in fact essential because typical human diets contain just enough iron to replace the small losses, although when dietary iron is more abundant, absorption must be (and is) attenuated since higher levels than necessary lead to iron overload and many distressing sequelae contingent on the radical production described above.</p><p>A variety of aspects of mammalian iron metabolism have been reviewed in detail elsewhere (e.g. [<xref ref-type="bibr" rid="B134">134</xref>,<xref ref-type="bibr" rid="B139">139</xref>,<xref ref-type="bibr" rid="B195">195</xref>,<xref ref-type="bibr" rid="B212">212</xref>-<xref ref-type="bibr" rid="B241">241</xref>]), including a series on 'iron imports' [<xref ref-type="bibr" rid="B242">242</xref>-<xref ref-type="bibr" rid="B248">248</xref>], and for our present purposes (Fig <xref ref-type="fig" rid="F2">2</xref>) mainly involves the intestinal (mainly duodenal) uptake of Fe(II) (produced from Fe(III) using a luminal ferrireductase) via a divalent metal ion transporter DMT1/DCT1/NRAMP [<xref ref-type="bibr" rid="B249">249</xref>,<xref ref-type="bibr" rid="B250">250</xref>] and its subsequent binding as Fe(III) to transferrin (Tf). The intestinal uptake of haem (heme) occurs via the heme carrier protein-1 (HCP1) [<xref ref-type="bibr" rid="B251">251</xref>] and it is thereby internalized, while the iron in heme is liberated by heme oxygenase-1 (HO1) [<xref ref-type="bibr" rid="B252">252</xref>-<xref ref-type="bibr" rid="B254">254</xref>]. Haem is synthesised in many tissues, especially liver and erythroid cells [<xref ref-type="bibr" rid="B255">255</xref>]. Vesicular routes of intestinal transfer may also occur [<xref ref-type="bibr" rid="B256">256</xref>,<xref ref-type="bibr" rid="B257">257</xref>]. Low MW cytoplasmic chelators such as citrate can bind iron fairly weakly and thereby contribute to a labile iron pool (LIP) in the cytoplasm and especially the lysosomes and mitochondria (see [<xref ref-type="bibr" rid="B258">258</xref>-<xref ref-type="bibr" rid="B262">262</xref>]), while ferritin [<xref ref-type="bibr" rid="B263">263</xref>] too can bind cytoplasmic iron (via a chaperone [<xref ref-type="bibr" rid="B264">264</xref>]) and is seen as a good overall marker of iron status [<xref ref-type="bibr" rid="B265">265</xref>-<xref ref-type="bibr" rid="B267">267</xref>]. Iron(II) is subsequently exported through the basolateral membrane of the enterocyte by ferroportin-1 (FPN1) [<xref ref-type="bibr" rid="B268">268</xref>-<xref ref-type="bibr" rid="B270">270</xref>]. Ferroportin may also contribute to uptake in enterocytes [<xref ref-type="bibr" rid="B271">271</xref>]. Fe(III) may then be produced by hephaestin (Hp) [<xref ref-type="bibr" rid="B272">272</xref>] before it is bound by transferrin (Tf), which is the main but not sole means of binding Fe(III) when it is transported through the circulation, with major iron storage taking place in the liver. Similar processes occur in the peripheral tissues, with significant transfer of iron from transferrin occurring via the transferrin receptor [<xref ref-type="bibr" rid="B273">273</xref>].</p><fig position="float" id="F2"><label>Figure 2</label><caption><p><bold>Schematic overview of the main elements considered to participate in mammalian iron metabolism</bold>.</p></caption><graphic xlink:href="1755-8794-2-2-2"></graphic></fig><p>'Free' haem appears in the circulation (it may have a signalling role [<xref ref-type="bibr" rid="B274">274</xref>]) and elsewhere largely because of erythrocyte degradation, and it can also greatly amplify the cellular damage caused by ROSs [<xref ref-type="bibr" rid="B275">275</xref>], and its degradation pathway via haem oxygenase [<xref ref-type="bibr" rid="B276">276</xref>,<xref ref-type="bibr" rid="B277">277</xref>] to biliverdin and then using biliverdin reductase to form bilirubin generates 'free' (and potentially redox-active) iron. It would appear, not least because biliverdin has powerful antioxidant properties, that haem oxygenase is more protective than damaging [<xref ref-type="bibr" rid="B253">253</xref>,<xref ref-type="bibr" rid="B278">278</xref>-<xref ref-type="bibr" rid="B282">282</xref>], even though one of the products of its reaction is Fe that must eventually be liganded (or e.g. incorporated into ferritin). (Another product is the gas CO, that has been proposed as a measure of oxidative stress in the lung [<xref ref-type="bibr" rid="B283">283</xref>].)</p><p>All of the above obviously ignores both some important aspects of the speciation and liganding of iron, as well as the tissue distribution of the specific proteins involved – for which latter global information will shortly emerge [<xref ref-type="bibr" rid="B284">284</xref>] (<ext-link ext-link-type="uri" xlink:href="http://www.proteinatlas.org/"></ext-link> and see later). It also ignores any discussion on the genetic regulation of iron metabolism (e.g. [<xref ref-type="bibr" rid="B285">285</xref>-<xref ref-type="bibr" rid="B288">288</xref>]), which is not our main focus.</p><p>However, one molecule in particular, hepcidin, has recently emerged as a 'master regulator' of regulation at the physiological level, and we describe some of these new developments.</p><sec><title>Hepcidin</title><p>In the liver and elsewhere, many aspects of iron metabolism are regulated by a recently discovered 25-amino acid polypeptide called hepcidin [<xref ref-type="bibr" rid="B207">207</xref>,<xref ref-type="bibr" rid="B241">241</xref>,<xref ref-type="bibr" rid="B245">245</xref>,<xref ref-type="bibr" rid="B271">271</xref>,<xref ref-type="bibr" rid="B289">289</xref>-<xref ref-type="bibr" rid="B327">327</xref>] that acts in part as a negative regulator of iron efflux [<xref ref-type="bibr" rid="B328">328</xref>] by causing the internalisation of ferroportin [<xref ref-type="bibr" rid="B329">329</xref>-<xref ref-type="bibr" rid="B333">333</xref>]. Hepcidin is produced, partly under the regulation of a receptor called hemojuvelin (e.g. [<xref ref-type="bibr" rid="B334">334</xref>]), via an 84-aa precursor called pre-pro-hepcidin and a 60 mer called pro-hepcidin [<xref ref-type="bibr" rid="B304">304</xref>,<xref ref-type="bibr" rid="B335">335</xref>,<xref ref-type="bibr" rid="B336">336</xref>] although the active agent is considered to be the 25 mer referred to above, and with the inactive precursors appearing not to be useful markers [<xref ref-type="bibr" rid="B337">337</xref>,<xref ref-type="bibr" rid="B338">338</xref>].</p><p>Strikingly, anaemia and anoxia both suppress hepcidin production [<xref ref-type="bibr" rid="B245">245</xref>,<xref ref-type="bibr" rid="B339">339</xref>,<xref ref-type="bibr" rid="B340">340</xref>] (Fig <xref ref-type="fig" rid="F3">3</xref>), such that just while superoxide production is being enhanced by the anoxia there is more iron being absorbed from the intestine and effluxed into the circulation. In view of the inter-reactivity of superoxide and iron this could be anticipated to enhance free radical formation, leading to a positive feedback loop in which the problems are amplified: ischaemia/anoxia changes Fe(n) distribution leading to differential reactivity with the products of anoxia and thus further free radical production. However, hepcidin is overexpressed in inflammatory disease and is an early inflammatory marker [<xref ref-type="bibr" rid="B245">245</xref>,<xref ref-type="bibr" rid="B341">341</xref>-<xref ref-type="bibr" rid="B345">345</xref>]. Its expression is positively controlled inter alia by SMAD4, and loss of hepatic SMAD4 is thus associated with dramatically decreased expression of hepcidin in liver and increased duodenal expression of a variety of genes involved in intestinal iron absorption, including Dcytb, DMT1 and ferroportin, leading to iron overload [<xref ref-type="bibr" rid="B346">346</xref>]. STAT3 is another positive effector of hepcidin expression [<xref ref-type="bibr" rid="B347">347</xref>,<xref ref-type="bibr" rid="B348">348</xref>], and ROSs inhibit this effect [<xref ref-type="bibr" rid="B349">349</xref>], thereby creating a link between ROSs and Fe metabolism. To understand the exact roles of hepcidin in iron metabolism, it is going to be especially important to understand where it is expressed; fortunately, such studies are beginning to emerge [<xref ref-type="bibr" rid="B350">350</xref>].</p><fig position="float" id="F3"><label>Figure 3</label><caption><p><bold>Some effects of hepcidin, summarizing the fact that hypoxic condition can suppress it and thus lead to hyperferraemia</bold>. Since hypoxic conditions can also lead to ROS production the hypoxia-mediated regulation of hepcidin can have especially damaging effects.</p></caption><graphic xlink:href="1755-8794-2-2-3"></graphic></fig><p>Overall there is a complex interplay between positive and negative regulation and the organismal distribution of iron caused by changes in hepcidin concentration [<xref ref-type="bibr" rid="B351">351</xref>], with in many cases the hypoxic response (decreased hepcidin) seeming to dominate that due to inflammation (increased hepcidin) even when iron levels are high [<xref ref-type="bibr" rid="B352">352</xref>,<xref ref-type="bibr" rid="B353">353</xref>]. Specifically, lowered hepcidin causes hyperferraemia. Hepcidin is also activated by p53 [<xref ref-type="bibr" rid="B354">354</xref>], and may play a role in the degradation of atherosclerotic plaques [<xref ref-type="bibr" rid="B355">355</xref>]. Another recently discovered protein that is crucially involved in human iron metabolism is NGAL or siderocalin, and while there is some evidence for their co-regulation [<xref ref-type="bibr" rid="B356">356</xref>], they have normally been studied separately.</p></sec><sec><title>NGAL (also known as lipocalin-2 or siderocalin)</title><p>Lipocalins [<xref ref-type="bibr" rid="B357">357</xref>] are a diverse group of ligand-binding proteins that share a conserved structure even in the absence of significant sequence conservation. This core structure includes an eight-stranded anti- parallel β barrel that defines a calyx, or cup-shaped structure, enclosing the ligand binding site.</p><p>NGAL – neutrophil gelatinase-associated lipocalin – is a 21 kDal glycoprotein first isolated by Kjeldsen and colleagues in 1993 [<xref ref-type="bibr" rid="B358">358</xref>]. Synonyms include lipocalin 2, siderocalin, Lcn2, α2-microglobulin-related protein or neu-related lipocalin (in rats) [<xref ref-type="bibr" rid="B359">359</xref>,<xref ref-type="bibr" rid="B360">360</xref>] and (in mice) 24p3 or uterocalin [<xref ref-type="bibr" rid="B361">361</xref>]. Although lipocalins are well known to be involved in the sequestration and transport of a variety of ligands, the natural ligand of NGAL (as is the case with many lipocalins) was not initially known even in terms of its chemical class. This changed with the seminal paper of Goetz and colleagues [<xref ref-type="bibr" rid="B362">362</xref>] (and see [<xref ref-type="bibr" rid="B206">206</xref>]) who purified recombinant NGAL from a particular strain of <italic>E. coli </italic>and found that its structure contained a negatively charged ferric siderophore with a subnanomolar dissociation constant that it had extracted from its bacterial host, and that the apo form of this molecule could also act as a potent bacteriostatic agent by sequestering iron (see also [<xref ref-type="bibr" rid="B363">363</xref>-<xref ref-type="bibr" rid="B367">367</xref>]). A companion paper [<xref ref-type="bibr" rid="B368">368</xref>] showed that the iron-delivering activity was expressed in mammalian cells. The structure of NGAL is now known [<xref ref-type="bibr" rid="B369">369</xref>] and one of its interaction partners is a matrix metalloproteinase [<xref ref-type="bibr" rid="B370">370</xref>] to which it can presumably donate a metal ion and in the complex decrease its degradation [<xref ref-type="bibr" rid="B371">371</xref>].</p><p>The finding that NGAL was one of the most highly expressed proteins following ischaemia-reperfusion injury in kidney cells [<xref ref-type="bibr" rid="B372">372</xref>-<xref ref-type="bibr" rid="B374">374</xref>], and prognostic of kidney damage long before the more traditional marker creatinine was raised significantly, has led to considerable interest in this protein, especially as a marker of renal injury [<xref ref-type="bibr" rid="B375">375</xref>-<xref ref-type="bibr" rid="B389">389</xref>], and perhaps as a therapeutic [<xref ref-type="bibr" rid="B375">375</xref>]. Devireddy and colleagues [<xref ref-type="bibr" rid="B390">390</xref>] identified a receptor that internalizes 24p3, and internalization of iron bound to 24p3 prevents apoptosis. In contrast, internalization of the apo form of 24p3 that does not contain iron led to cellular iron efflux and apoptosis via the proapoptotic protein Bim [<xref ref-type="bibr" rid="B391">391</xref>]. In humans the megalin receptor can bind siderocalin (and its siderophore payload) and mediate its intracellular uptake [<xref ref-type="bibr" rid="B392">392</xref>]. Oxidative stress can also induce its expression [<xref ref-type="bibr" rid="B393">393</xref>], and it is protective against it [<xref ref-type="bibr" rid="B394">394</xref>].</p><p>Exogenously administered NGAL also markedly upregulates heme oxygenase-1, a proven multifunctional protective agent in experimental Acute Kidney Injury (AKI) that is thought to work by limiting iron uptake, promoting intracellular iron release, enhancing production of antioxidants such as biliverdin and carbon monoxide, and inducing the cell cycle regulatory protein p21 [<xref ref-type="bibr" rid="B279">279</xref>,<xref ref-type="bibr" rid="B395">395</xref>,<xref ref-type="bibr" rid="B396">396</xref>]. Because of this multifaceted protective action, NGAL has emerged as a prime therapeutic target in ischaemic AKI [<xref ref-type="bibr" rid="B379">379</xref>].</p><p>Structural and direct binding studies have suggested that siderocalin tends (although not exclusively) to bind catecholate-type ligands, rather than hydroxamate- or carboxylate-based siderophores, at least when tested with microbially derived siderophores [<xref ref-type="bibr" rid="B362">362</xref>,<xref ref-type="bibr" rid="B363">363</xref>,<xref ref-type="bibr" rid="B365">365</xref>] (but cf. [<xref ref-type="bibr" rid="B369">369</xref>] for claims, disputed [<xref ref-type="bibr" rid="B360">360</xref>] and not now accepted, as to the binding of bacterially derived formyl peptides!). The role of NGAL, as a siderophore-binding agent, is thus consistent with the widespread recognition that iron-induced radical generation is intimately involved in a variety of renal and other diseases [<xref ref-type="bibr" rid="B397">397</xref>,<xref ref-type="bibr" rid="B398">398</xref>]. However, while it is certainly the case that siderocalin can reduce the virulence of bacteria when it binds the relevant bacterial siderophores [<xref ref-type="bibr" rid="B362">362</xref>-<xref ref-type="bibr" rid="B367">367</xref>] and that bacteria can 'evade' this by synthesising siderophores that siderocalin cannot bind (e.g. [<xref ref-type="bibr" rid="B186">186</xref>,<xref ref-type="bibr" rid="B187">187</xref>,<xref ref-type="bibr" rid="B399">399</xref>-<xref ref-type="bibr" rid="B401">401</xref>]), it is questionable whether the only role of siderocalin lies in fact in its antibacterial activity. Rather we would suggest that its main role is in sequestrating iron via a human siderophore to stop inappropriately liganded iron from producing damaging oxygen radicals. Consistent with this iron-liganding role for human biology is the fact that the tissue most highly expressing NGAL under normal conditions is bone marrow [<xref ref-type="bibr" rid="B360">360</xref>,<xref ref-type="bibr" rid="B402">402</xref>], the site of erythropoiesis. The liganding can be extensive; as Goetz and colleagues [<xref ref-type="bibr" rid="B362">362</xref>] note, "During inflammation, concentrations of NGAL can increase to levels, with concentrations approaching 20–30 nM in the serum [<xref ref-type="bibr" rid="B403">403</xref>], presumably adequate to bind all available iron as ferric siderophore complexes".</p><p>Significant changes in NGAL expression have also been observed, for instance, during kinase-mediated signalling [<xref ref-type="bibr" rid="B404">404</xref>,<xref ref-type="bibr" rid="B405">405</xref>], in cardiovascular disease [<xref ref-type="bibr" rid="B406">406</xref>-<xref ref-type="bibr" rid="B409">409</xref>] and in cancer [<xref ref-type="bibr" rid="B410">410</xref>-<xref ref-type="bibr" rid="B412">412</xref>].</p><p>These findings on the kidney and the role of NGAL, together with the important knowledge that its chief ligand is probably an unknown human siderophore (Figs <xref ref-type="fig" rid="F2">2</xref>, <xref ref-type="fig" rid="F4">4</xref>), thus lead us to consider the role of this system (and unliganded iron generally) in a whole series of other diseases that all share many characteristics of oxidative stress and inflammation (see also [<xref ref-type="bibr" rid="B413">413</xref>]). A similar thesis, albeit with comparatively little stress on iron, is the <italic>leitmotif </italic>of Finch's recent detailed monograph [<xref ref-type="bibr" rid="B163">163</xref>]. The theme of these sections is thus to stress the fact that while the role of ROSs in general in such syndromes has been pointed up previously, that of iron as a major culprit has not so generally yet been stressed, notwithstanding that there is in fact a great deal of pertinent literature that we here highlight as the focus of this review.</p><fig position="float" id="F4"><label>Figure 4</label><caption><p><bold>Overview of the roles of ischaemia, ROSs, poorly liganded iron and the iron metabolism regulators HGAL and hepicidin in effecting inflammation as a physiological level</bold>.</p></caption><graphic xlink:href="1755-8794-2-2-4"></graphic></fig></sec></sec><sec><title>Some disease manifestations in which iron may be implicated</title><sec><title>Preeclampsia (PE)</title><p>Another important disease that shares many of the same properties (or at least sequelae) of renal impairment, and may have the same fundamental aetiology, is pre-eclampsia. This is the most significant cause of morbidity and mortality in pregnant women [<xref ref-type="bibr" rid="B414">414</xref>]. The chief clinical manifestations at time of diagnosis are a raised blood pressure (hypertension) [<xref ref-type="bibr" rid="B415">415</xref>] and proteinuria, together with raised creatinine, consistent with the <underline>reversible</underline> existence (since it is relieved upon delivery of the baby) of renal impairment. However, prognostic markers that might manifest early in pregnancy are lacking, and would be highly desirable. There is widespread agreement [<xref ref-type="bibr" rid="B416">416</xref>] that a poor connection of the placenta to the uterus leads to ischaemia and thus oxidative stress, with a substantial involvement of apoptosis during the placental remodelling [<xref ref-type="bibr" rid="B417">417</xref>-<xref ref-type="bibr" rid="B423">423</xref>]. Since preeclampsia-like syndromes can be induced in pregnant animals by surgical restriction of the uteroplacental blood supply [<xref ref-type="bibr" rid="B424">424</xref>], it is presumed that blood-borne agents arising from the ischaemic placenta are the cause of the generalized endothelial cell damage and inflammatory responses that give rise to the symptoms of hypertension, proteinuria, and sudden oedema characteristic of preeclampsia [<xref ref-type="bibr" rid="B70">70</xref>]. Indeed, many studies implicate oxidative stress as a substantial contributor to this [<xref ref-type="bibr" rid="B425">425</xref>-<xref ref-type="bibr" rid="B489">489</xref>], while some have noted the importance of iron status [<xref ref-type="bibr" rid="B70">70</xref>,<xref ref-type="bibr" rid="B133">133</xref>,<xref ref-type="bibr" rid="B450">450</xref>,<xref ref-type="bibr" rid="B490">490</xref>-<xref ref-type="bibr" rid="B511">511</xref>], and so far as is known the transporters of iron in the placenta are similar to those in other cells [<xref ref-type="bibr" rid="B512">512</xref>]. Oxidative stress of this type is of course inflammatory in nature and inflammation is observed in PE [<xref ref-type="bibr" rid="B472">472</xref>,<xref ref-type="bibr" rid="B476">476</xref>,<xref ref-type="bibr" rid="B484">484</xref>,<xref ref-type="bibr" rid="B486">486</xref>,<xref ref-type="bibr" rid="B513">513</xref>-<xref ref-type="bibr" rid="B519">519</xref>]. We suggest strongly that it is the <underline>combination</underline> of inadequately liganded Fe(II or III) and superoxide/peroxide leading to OH<sup>• </sup>formation that is the chief mechanistic cause of the downstream events that manifest in PE, and that appropriate removal by liganding/chelation or otherwise of these ions would prove of therapeutic benefit. (Iron status has also been implicated in other pregnancy and neonatal disorders [<xref ref-type="bibr" rid="B520">520</xref>-<xref ref-type="bibr" rid="B524">524</xref>].) There is evidence too for the involvement of the radical NO [<xref ref-type="bibr" rid="B456">456</xref>,<xref ref-type="bibr" rid="B525">525</xref>].</p><p>We note that it is quite common nevertheless for iron to be prescribed during pregnancy, especially during its latter stages [<xref ref-type="bibr" rid="B526">526</xref>,<xref ref-type="bibr" rid="B527">527</xref>], and that this does of course lead to oxidative stress [<xref ref-type="bibr" rid="B528">528</xref>,<xref ref-type="bibr" rid="B529">529</xref>].</p><p>Oxidative stress is caused both by the initial rate of production of superoxide and the rate of their conversion into OH<sup>• </sup>radicals. The former can be induced by hypoxic conditions such as occur at high altitude, and one prediction, that is borne out [<xref ref-type="bibr" rid="B487">487</xref>,<xref ref-type="bibr" rid="B530">530</xref>], is that PE should therefore be more prevalent at high altitude. Erythropoietin may be a marker for oxidative stress in pre-eclampsia [<xref ref-type="bibr" rid="B531">531</xref>].</p><p>Regarding the second stage, predictions include that PE should be more common in those suffering from diseases of iron metabolism. Although such mothers are of course less well <italic>a priori</italic>, this prediction is borne out for α-thalassemia [<xref ref-type="bibr" rid="B532">532</xref>,<xref ref-type="bibr" rid="B533">533</xref>] although not, interestingly, for haemochromatosis [<xref ref-type="bibr" rid="B534">534</xref>]. We note in this context that thalassaemia not only predisposes towards PE but is known in general to cause hepcidin to decrease and NGAL to increase [<xref ref-type="bibr" rid="B352">352</xref>,<xref ref-type="bibr" rid="B353">353</xref>,<xref ref-type="bibr" rid="B356">356</xref>,<xref ref-type="bibr" rid="B535">535</xref>], with consequent and inevitable iron dysregulation.</p><p>Another prediction is then that hepcidin should be changed in pre-eclampsia. Although no serum measurements have been reported to date, it is of extreme interest that – while they took it to be an antimicrobial peptide rather than an iron regulator – a recent study by Knox and colleagues of placental gene expression in a mouse model of PE showed that hepcidin expression <underline>increased</underline> by a greater factor than that of any other gene save one [<xref ref-type="bibr" rid="B536">536</xref>], consistent with the view that major changes in the regulation of iron liganding and metabolism underpin PE.</p><p>Finally, we note that NGAL is significantly implicated in pregnancy, and was even named uterocalin in mice to reflect its high expression in the uterus [<xref ref-type="bibr" rid="B361">361</xref>,<xref ref-type="bibr" rid="B537">537</xref>-<xref ref-type="bibr" rid="B539">539</xref>]. A very recent study [<xref ref-type="bibr" rid="B540">540</xref>] suggests that it may be a useful second trimester biomarker for pre-eclampsia.</p></sec><sec><title>Diabetes</title><p>Type 2 diabetes and insulin resistance are known complications of pregnancy (e.g. [<xref ref-type="bibr" rid="B541">541</xref>-<xref ref-type="bibr" rid="B545">545</xref>]), and also predispose towards PE. In a similar vein, various types of pregnancy-related intrauterine growth restriction predispose towards diabetes in later life [<xref ref-type="bibr" rid="B546">546</xref>,<xref ref-type="bibr" rid="B547">547</xref>], pointing up the progressive nature of these syndromes. Metabolic biomarkers for the one can thus be predictive of the other [<xref ref-type="bibr" rid="B548">548</xref>], consistent with a common cause. Certainly ROSs are known to play a substantive role in both insulin resistance [<xref ref-type="bibr" rid="B549">549</xref>-<xref ref-type="bibr" rid="B556">556</xref>] and in a variety of diabetic sequelae [<xref ref-type="bibr" rid="B95">95</xref>,<xref ref-type="bibr" rid="B557">557</xref>-<xref ref-type="bibr" rid="B559">559</xref>], and mitochondrial dysfunction may be an early step in this [<xref ref-type="bibr" rid="B560">560</xref>]. Some anti-diabetic drugs, such as the 'glitazones' that are considered to act on Peroxisome Proliferator Activated Receptor (PPAR)γ, may also act by decreasing ROS production (e.g. [<xref ref-type="bibr" rid="B561">561</xref>-<xref ref-type="bibr" rid="B565">565</xref>]), and are even active aganst cerebral ischaemia and stroke [<xref ref-type="bibr" rid="B566">566</xref>-<xref ref-type="bibr" rid="B569">569</xref>]. As with most if not all of the other diseases we review here, studies of pro-inflammatory markers (such as TNF-α, IL-1 and C-reactive protein [<xref ref-type="bibr" rid="B570">570</xref>]) during the development of diabetes show its aetiology to be inflammatory in nature [<xref ref-type="bibr" rid="B553">553</xref>,<xref ref-type="bibr" rid="B571">571</xref>-<xref ref-type="bibr" rid="B590">590</xref>]. Iron 'excess' is also a known feature of gestational diabetes [<xref ref-type="bibr" rid="B591">591</xref>-<xref ref-type="bibr" rid="B593">593</xref>], and is a clear risk factor for the disease even in 'normal' populations [<xref ref-type="bibr" rid="B594">594</xref>-<xref ref-type="bibr" rid="B603">603</xref>], and indeed diabetes is a classical consequence of iron overloading as seen in hereditary haemochromatosis [<xref ref-type="bibr" rid="B604">604</xref>]. Serum ferritin and body iron stores are strongly associated with diabetes [<xref ref-type="bibr" rid="B603">603</xref>,<xref ref-type="bibr" rid="B605">605</xref>-<xref ref-type="bibr" rid="B609">609</xref>], including prospectively [<xref ref-type="bibr" rid="B610">610</xref>], while changes in visfatin are also intimately involved in changes of iron metabolism (with <underline>pro</underline>-hepcidin being elevated) [<xref ref-type="bibr" rid="B611">611</xref>]. Most importantly, lipocalin 2 (siderocalin/NGAL) is strongly associated with the development of diabetes [<xref ref-type="bibr" rid="B612">612</xref>,<xref ref-type="bibr" rid="B613">613</xref>]. Lowering iron improves insulin sensitivity [<xref ref-type="bibr" rid="B598">598</xref>,<xref ref-type="bibr" rid="B614">614</xref>], and metallothionein is also protective [<xref ref-type="bibr" rid="B615">615</xref>-<xref ref-type="bibr" rid="B619">619</xref>]. There seems little doubt that iron status is a major determinant of the development of type 2 diabetes [<xref ref-type="bibr" rid="B620">620</xref>].</p><p>Non-transferrin-bound iron is also considerably elevated in type 2 diabetes [<xref ref-type="bibr" rid="B621">621</xref>], and this too is exacerbated by vitamin C. Iron metabolism is substantially deranged in type 2 diabetes and the metabolism of glucose (a reducing sugar) interacts significantly with iron metabolism [<xref ref-type="bibr" rid="B598">598</xref>]. Iron is also strongly implicated in non-alcoholic steatohepatitis, considered an early marker of insulin resistance [<xref ref-type="bibr" rid="B622">622</xref>-<xref ref-type="bibr" rid="B624">624</xref>]. Well-known diabetic complications include retinopathies, and it is noteworthy that elevated levels of ferritin can lead to cataract formation [<xref ref-type="bibr" rid="B625">625</xref>,<xref ref-type="bibr" rid="B626">626</xref>].</p></sec><sec><title>The metabolic syndrome</title><p>Although some of its origins may be pre-natal [<xref ref-type="bibr" rid="B547">547</xref>], many of the features of these diseases are also seen in the (so-called) Metabolic Syndrome [<xref ref-type="bibr" rid="B627">627</xref>-<xref ref-type="bibr" rid="B631">631</xref>]. Thus, serum ferritin is also related to insulin resistance [<xref ref-type="bibr" rid="B606">606</xref>,<xref ref-type="bibr" rid="B632">632</xref>,<xref ref-type="bibr" rid="B633">633</xref>] and iron levels are raised [<xref ref-type="bibr" rid="B624">624</xref>,<xref ref-type="bibr" rid="B634">634</xref>,<xref ref-type="bibr" rid="B635">635</xref>]. Of course diabetes and the Metabolic Syndrome are also closely coupled, so it is reasonable that features observed in the one may be observed during the development of the other. The metabolic syndrome is also an independent indicator for chronic kidney disease [<xref ref-type="bibr" rid="B636">636</xref>] and may be related to liver steatosis [<xref ref-type="bibr" rid="B637">637</xref>]. Metabolic disorders of this type too are closely intertwined with inflammation [<xref ref-type="bibr" rid="B575">575</xref>,<xref ref-type="bibr" rid="B581">581</xref>,<xref ref-type="bibr" rid="B587">587</xref>,<xref ref-type="bibr" rid="B638">638</xref>], that is of course stimulated by ROSs whose generation is increased by high-fat diets [<xref ref-type="bibr" rid="B639">639</xref>]. Thus, our role here is to point up the existence of a considerable body of more-than-circumstantial evidence that here too the progressive and damaging nature of these diseases may be caused, in part, by inappropriately chelated iron.</p></sec><sec><title>Obesity</title><p>"As previously pointed out by Booth <italic>et al</italic>. [<xref ref-type="bibr" rid="B640">640</xref>], 100% of the increase in the prevalence of Type 2 diabetes and obesity in the United States during the latter half of the 20th century must be attributed to a changing environment interacting with genes, because 0% of the human genome has changed during this time period." [<xref ref-type="bibr" rid="B629">629</xref>]</p><p>It is well known that there has been a staggering increase in the prevalence of obesity, diabetes, and especially type 2 diabetes, in the last 50 years or so, and that this increase is expected to continue (e.g. [<xref ref-type="bibr" rid="B641">641</xref>-<xref ref-type="bibr" rid="B643">643</xref>] and <ext-link ext-link-type="uri" xlink:href="http://www.who.int/diabetes/"></ext-link>). Equally, it is now well known that obesity, metabolic syndrome, diabetes and cardiovascular diseases are all more or less related to each other [<xref ref-type="bibr" rid="B643">643</xref>], and the question arises here as to whether dysfunctional iron metabolism might be a feature of each of them. In the case of obesity <italic>per se</italic>, however, we see no major evidence as yet for a causative role of deranged iron metabolism or chelation in causing obesity. Indeed, while they are related [<xref ref-type="bibr" rid="B644">644</xref>], what little evidence there is [<xref ref-type="bibr" rid="B645">645</xref>,<xref ref-type="bibr" rid="B646">646</xref>] suggests that the converse may be true, i.e. that changes in iron metabolism might be consequent upon obesity (possibly via peroxide generation [<xref ref-type="bibr" rid="B639">639</xref>]). Importantly, considerable evidence suggests that obesity and inflammation are significantly related [<xref ref-type="bibr" rid="B163">163</xref>,<xref ref-type="bibr" rid="B486">486</xref>,<xref ref-type="bibr" rid="B575">575</xref>,<xref ref-type="bibr" rid="B581">581</xref>,<xref ref-type="bibr" rid="B642">642</xref>,<xref ref-type="bibr" rid="B647">647</xref>-<xref ref-type="bibr" rid="B664">664</xref>], not least because adipocytes produce and release various adipokines including pro-inflammatory cytokines such as IL-6 and TNF-α [<xref ref-type="bibr" rid="B575">575</xref>,<xref ref-type="bibr" rid="B649">649</xref>,<xref ref-type="bibr" rid="B650">650</xref>,<xref ref-type="bibr" rid="B665">665</xref>-<xref ref-type="bibr" rid="B671">671</xref>]. It is likely that it is the <underline>combination</underline> of overfeeding-induced obesity and inflammation (partly induced by the obesity itself [<xref ref-type="bibr" rid="B672">672</xref>]) that leads to diabetes [<xref ref-type="bibr" rid="B673">673</xref>]. Certainly there is evidence for increased ROS production in obese mice, possibly mediated in part via the fatty acid-induced activation of NAPH oxidase [<xref ref-type="bibr" rid="B674">674</xref>], while obesity is linked [<xref ref-type="bibr" rid="B675">675</xref>,<xref ref-type="bibr" rid="B676">676</xref>] to urinary levels of 8-epi-PGF<sub>2α</sub>, a well established marker of oxidative stress (qv). Fig <xref ref-type="fig" rid="F5">5</xref> summarises the above in a manner that stresses the roles of iron, overfeeding and inflammation in the genesis of these processes, and notes that interference in several of these steps is likely to be required to limit their progression to best advantage.</p><fig position="float" id="F5"><label>Figure 5</label><caption><p><bold>Role of inflammation caused by hydroxyl radical formation in the interactive development of obesity, the metabolic syndrome and diabetes</bold>. Intervention at multiple steps is likely to be most beneficial in alleviating this kind of progression.</p></caption><graphic xlink:href="1755-8794-2-2-5"></graphic></fig></sec><sec><title>Hypertension</title><p>As well its significance in pre-eclampsia (see above), hypertension is a well known risk factor for many cardiovascular and related disease (e.g. [<xref ref-type="bibr" rid="B677">677</xref>]), and there is considerable evidence that its underlying cause is inflammatory in nature [<xref ref-type="bibr" rid="B678">678</xref>-<xref ref-type="bibr" rid="B686">686</xref>], is related to the metabolic syndrome and obesity (e.g. [<xref ref-type="bibr" rid="B648">648</xref>,<xref ref-type="bibr" rid="B687">687</xref>-<xref ref-type="bibr" rid="B691">691</xref>]), and may be mediated mainly via ROSs [<xref ref-type="bibr" rid="B692">692</xref>]. There is evidence that some of its sequelae may be mediated via iron [<xref ref-type="bibr" rid="B693">693</xref>,<xref ref-type="bibr" rid="B694">694</xref>].</p></sec><sec><title>Cardiovascular diseases</title><p>It is well known that elevated iron stores can predispose to coronary artery disease and thence myocardial infarction. The 'iron hypothesis' of the benefits of some iron depletion due to menstruation was devised to account for the lowering of heart-disease risk in young women (that disappears in those post-menopause) and was proposed by Jerome Sullivan in 1981 [<xref ref-type="bibr" rid="B695">695</xref>-<xref ref-type="bibr" rid="B698">698</xref>] (and see also [<xref ref-type="bibr" rid="B699">699</xref>,<xref ref-type="bibr" rid="B700">700</xref>]). (In this sense, the lack of menstruation during pregnancy would predispose to a comparative abundance of iron, as is indeed found – see above.) It is of particular interest that the well-known adverse vascular effects of homocysteine (in inhibiting flow-mediated dilatation) are in fact iron-dependent [<xref ref-type="bibr" rid="B701">701</xref>-<xref ref-type="bibr" rid="B703">703</xref>], and that reducing homocysteine (e.g. by folate supplementation) in the absence of lowering iron has shown no clinical benefit to date [<xref ref-type="bibr" rid="B704">704</xref>], thereby suggestion iron mediation. By contrast, iron stores represent an established risk factor for cardiovascular disease [<xref ref-type="bibr" rid="B705">705</xref>].</p><p>Of course many factors such as lipid levels, stress, smoking and so are well-known risk factors for cardiovascular, coronary artery disease and related diseases. Indeed kidney disease is well established as a risk factor for cardiovascular disease [<xref ref-type="bibr" rid="B706">706</xref>-<xref ref-type="bibr" rid="B708">708</xref>] (and indeed stroke [<xref ref-type="bibr" rid="B709">709</xref>]), all consistent with their having in part a common cause – we believe inflammation). Our purpose here, within the spirit of this review, is to indicate the evidence for the involvement of inappropriately chelated iron in cardiovascular diseases too. There is no doubt that the iron-mediated causal chain of ischaemia → (su)peroxide → OH<sup>• </sup>radical formation occurs during the development of heart disease, especially during reperfusion injury [<xref ref-type="bibr" rid="B710">710</xref>-<xref ref-type="bibr" rid="B713">713</xref>], and suitable iron chelators inhibit this [<xref ref-type="bibr" rid="B714">714</xref>,<xref ref-type="bibr" rid="B715">715</xref>] (see also [<xref ref-type="bibr" rid="B716">716</xref>,<xref ref-type="bibr" rid="B717">717</xref>], and for thalassaemia [<xref ref-type="bibr" rid="B718">718</xref>]). Iron is also involved in the protection that can be produced by ischaemic preconditioning [<xref ref-type="bibr" rid="B719">719</xref>,<xref ref-type="bibr" rid="B720">720</xref>]. Erythropoietin, a hormone with multiple effects that may involve iron metabolism, is also protective [<xref ref-type="bibr" rid="B721">721</xref>,<xref ref-type="bibr" rid="B722">722</xref>].</p></sec><sec><title>Heart failure</title><p>The sequelae of heart failure are complex, and involve a <underline>chronic and continuing</underline> worsening of a variety of physiological properties. ROSs are certainly involved here, since allopurinol (a potent inhibitor of xanthine oxidase) improves prognosis considerably [<xref ref-type="bibr" rid="B723">723</xref>], and uric acid is a well known biomarker for heart failure (see e.g. [<xref ref-type="bibr" rid="B724">724</xref>,<xref ref-type="bibr" rid="B725">725</xref>]). Biopyrrins, degradation products of bilirubin and thus markers of oxidative stress are also considerably increased [<xref ref-type="bibr" rid="B726">726</xref>]. Anaemia is a common occurrence (and risk factor) in heart failure [<xref ref-type="bibr" rid="B727">727</xref>-<xref ref-type="bibr" rid="B729">729</xref>], again implying a role for dysregulated iron metabolism and a need to understand the exact speciation of iron in chronic anaemias linked to inflammatory diseases [<xref ref-type="bibr" rid="B730">730</xref>].</p><p>It is next on the formation of atherosclerotic plaques that our attention is here focussed.</p></sec><sec><title>Atherosclerosis</title><p>Atherosclerosis is a progressive <underline>inflammatory disease</underline>[<xref ref-type="bibr" rid="B731">731</xref>-<xref ref-type="bibr" rid="B762">762</xref>] characterized by the accumulation of both oxidised lipids and various fibrous elements in arteries, often as plaques [<xref ref-type="bibr" rid="B763">763</xref>,<xref ref-type="bibr" rid="B764">764</xref>]. Iron and oxidised lipids are both found in atherosclerotic lesions [<xref ref-type="bibr" rid="B141">141</xref>,<xref ref-type="bibr" rid="B765">765</xref>-<xref ref-type="bibr" rid="B777">777</xref>], and iron depletion by dietary or other means delays this [<xref ref-type="bibr" rid="B778">778</xref>-<xref ref-type="bibr" rid="B782">782</xref>]. There is a correlation between iron status and atherosclerosis [<xref ref-type="bibr" rid="B766">766</xref>,<xref ref-type="bibr" rid="B776">776</xref>,<xref ref-type="bibr" rid="B783">783</xref>-<xref ref-type="bibr" rid="B794">794</xref>], evidently caused in part by the known ability of poorly liganded iron to effect lipid [<xref ref-type="bibr" rid="B765">765</xref>,<xref ref-type="bibr" rid="B784">784</xref>] and protein peroxidation, and by the effects of primed neutrophils [<xref ref-type="bibr" rid="B795">795</xref>] and transferrin [<xref ref-type="bibr" rid="B758">758</xref>]. In this context, exogenous ferric iron is deleterious to endothelial function [<xref ref-type="bibr" rid="B796">796</xref>], while iron chelation improves it [<xref ref-type="bibr" rid="B797">797</xref>-<xref ref-type="bibr" rid="B800">800</xref>]. However, phlebotomy provided no clinical benefit here [<xref ref-type="bibr" rid="B801">801</xref>]. Note that iron levels in plaques correlate with the amount of oxidised proteins therein [<xref ref-type="bibr" rid="B771">771</xref>], and that in one study [<xref ref-type="bibr" rid="B767">767</xref>], the EPR-detectable iron (essentially Fe(III)) in atherosclerotic tissue was <underline>seventeen times greater</underline> than that in the equivalent healthy tissue; this is not a small effect. (Iron, as part of the general ROS cascade, has also been implicated in gallstone formation, where melatonin has proved protective [<xref ref-type="bibr" rid="B802">802</xref>,<xref ref-type="bibr" rid="B803">803</xref>].)</p><p>Statins, typically developed on the basis of their ability to inhibit the enzyme HMG-CoA redutase and thus decrease serum cholesterol, are well established to have benefits in terms of decreasing the adverse events of various types of cardiovascular disease [<xref ref-type="bibr" rid="B804">804</xref>], albeit that in many populations (e.g. [<xref ref-type="bibr" rid="B805">805</xref>-<xref ref-type="bibr" rid="B807">807</xref>]) cholesterol alone is a poor predictor of cardiovascular disease, especially in the normal range. However, a known target of statins different from HMGCoA reductase is the β<sub>2</sub>-integrin leukocyte function antigen-1 (LFA-1) [<xref ref-type="bibr" rid="B808">808</xref>,<xref ref-type="bibr" rid="B809">809</xref>] and in this context, it is important to note that the clinical benefits of the statins are certainly <underline>not</underline> due solely to their cholesterol-lowering ability via the inhibition of HMG-CoA reductase (see e.g. [<xref ref-type="bibr" rid="B163">163</xref>,<xref ref-type="bibr" rid="B281">281</xref>,<xref ref-type="bibr" rid="B650">650</xref>,<xref ref-type="bibr" rid="B807">807</xref>,<xref ref-type="bibr" rid="B808">808</xref>,<xref ref-type="bibr" rid="B810">810</xref>-<xref ref-type="bibr" rid="B840">840</xref>]), and different statins can cause a variety of distinct expression profiles [<xref ref-type="bibr" rid="B841">841</xref>] that are inconsistent with a unitary mode of action. The apparent paradox [<xref ref-type="bibr" rid="B842">842</xref>] that lipid-lowering statins do indeed exhibit epidemiological disease-lowering benefit, while having little effect on plaques, is arguably well explained, especially within the context of the present review, via their additional anti-inflammatory effects [<xref ref-type="bibr" rid="B817">817</xref>,<xref ref-type="bibr" rid="B819">819</xref>,<xref ref-type="bibr" rid="B843">843</xref>,<xref ref-type="bibr" rid="B163">163</xref>,<xref ref-type="bibr" rid="B807">807</xref>,<xref ref-type="bibr" rid="B823">823</xref>-<xref ref-type="bibr" rid="B825">825</xref>,<xref ref-type="bibr" rid="B830">830</xref>,<xref ref-type="bibr" rid="B836">836</xref>,<xref ref-type="bibr" rid="B837">837</xref>-<xref ref-type="bibr" rid="B892">892</xref>], acting upstream of the nuclear transcription factor NF-κB (and see later). It is also extremely relevant, for instance, that some statins have metal chelating properties [<xref ref-type="bibr" rid="B893">893</xref>].</p><p>It has been pointed out that many measures of iron stress are inappropriate, since it is only the redox-active form of iron that is likely involved in oxidative stress. Serum ferritin is considered by some to be the most reliable marker of iron status in general [<xref ref-type="bibr" rid="B894">894</xref>], although it is not well correlated with iron distribution in the heart [<xref ref-type="bibr" rid="B895">895</xref>], for instance. What is clear, however, from the above is that deranged iron metabolism is intimately and causally involved in the formation of atherosclerotic lesions, and that appropriate iron chelation can help both to prevent and to reverse this.</p><p>Iron status is also closely involved in other chronic vascular diseases, and in the behaviour of wounds [<xref ref-type="bibr" rid="B896">896</xref>-<xref ref-type="bibr" rid="B899">899</xref>].</p></sec><sec><title>Stroke</title><p>Stroke is caused by ischaemia, leading to inflammation [<xref ref-type="bibr" rid="B900">900</xref>] and to the formation of ROS and other damaging free radicals [<xref ref-type="bibr" rid="B901">901</xref>] in the brain (which is high in metal ions [<xref ref-type="bibr" rid="B902">902</xref>]), and is exacerbated by existing inflammation – see e.g. [<xref ref-type="bibr" rid="B903">903</xref>,<xref ref-type="bibr" rid="B904">904</xref>]. Thus, another prediction is that iron excess should also aggravate the sequelae of stroke, and that appropriate chelation or free radical trapping agents should mitigate these effects. These predictions are indeed borne out [<xref ref-type="bibr" rid="B138">138</xref>,<xref ref-type="bibr" rid="B905">905</xref>-<xref ref-type="bibr" rid="B914">914</xref>]. It is also of considerable interest that plasma NGAL levels are increased in stroke [<xref ref-type="bibr" rid="B406">406</xref>]; it is noteworthy that this can be seen in plasma despite the localised origin of the disease.</p><p>A variety of other studies have shown the beneficial treatments in stroke models of anti-inflammatory and antioxidant treatment, i.e. treatments that lower the amount of ROSs (e.g. [<xref ref-type="bibr" rid="B915">915</xref>-<xref ref-type="bibr" rid="B922">922</xref>]), as well as of preconditioning [<xref ref-type="bibr" rid="B923">923</xref>]. Given its role in iron metabolism, it is of considerable interest that erythropoietin also seems to be very effective in protecting against brain ischaemia/reperfusion injury and stroke [<xref ref-type="bibr" rid="B924">924</xref>-<xref ref-type="bibr" rid="B939">939</xref>], by a mechanism independent of erythropoiesis [<xref ref-type="bibr" rid="B940">940</xref>-<xref ref-type="bibr" rid="B942">942</xref>], and one that appears to involve anti-inflammatory activity [<xref ref-type="bibr" rid="B943">943</xref>].</p></sec><sec><title>Alzheimer's, Parkinson's and other major neurodegenerative diseases</title><p>Oxidative stress and inflammation are early events of neurodegenerative diseases [<xref ref-type="bibr" rid="B920">920</xref>,<xref ref-type="bibr" rid="B944">944</xref>-<xref ref-type="bibr" rid="B957">957</xref>] such as Alzheimer's disease (e.g. [<xref ref-type="bibr" rid="B958">958</xref>-<xref ref-type="bibr" rid="B973">973</xref>]), where plaque formation precedes neurodegeneration [<xref ref-type="bibr" rid="B974">974</xref>]. Iron (and in some cases copper) is also <underline>strongly</underline> implicated in a variety of neurodegenerative diseases [<xref ref-type="bibr" rid="B944">944</xref>,<xref ref-type="bibr" rid="B981">981</xref>,<xref ref-type="bibr" rid="B945">945</xref>,<xref ref-type="bibr" rid="B958">958</xref>,<xref ref-type="bibr" rid="B962">962</xref>,<xref ref-type="bibr" rid="B950">950</xref>,<xref ref-type="bibr" rid="B917">917</xref>,<xref ref-type="bibr" rid="B278">278</xref>,<xref ref-type="bibr" rid="B43">43</xref>,<xref ref-type="bibr" rid="B285">285</xref>,<xref ref-type="bibr" rid="B972">972</xref>,<xref ref-type="bibr" rid="B141">141</xref>,<xref ref-type="bibr" rid="B975">975</xref>-<xref ref-type="bibr" rid="B1087">1087</xref>].</p><p>Indeed Thompson and colleagues comment [<xref ref-type="bibr" rid="B136">136</xref>] that "The underlying pathogenic event in oxidative stress is cellular iron mismanagement" and stress that "Multiple lines of evidence implicate redox-active transition metals, such as iron and copper, as mediators of oxidative stress and ROS production in neurodegenerative diseases". There is also ample evidence for its presence in the plaques characteristic of Alzheimer's disease [<xref ref-type="bibr" rid="B1004">1004</xref>,<xref ref-type="bibr" rid="B1013">1013</xref>,<xref ref-type="bibr" rid="B1027">1027</xref>,<xref ref-type="bibr" rid="B1088">1088</xref>], just as in those of atherosclerosis (see above). Note too that iron can catalyse the oxidation of dopamine to a quinine form that can bind covalently to and then aggregate proteins [<xref ref-type="bibr" rid="B1089">1089</xref>]. Kostoff [<xref ref-type="bibr" rid="B1090">1090</xref>] has used a very interesting literature-based discovery approach to highlight the role of oxidative stress in the development of Parkinson's disease.</p><p>Other papers highlight the role of iron in multiple sclerosis [<xref ref-type="bibr" rid="B899">899</xref>,<xref ref-type="bibr" rid="B991">991</xref>,<xref ref-type="bibr" rid="B1091">1091</xref>-<xref ref-type="bibr" rid="B1098">1098</xref>] and in prion diseases [<xref ref-type="bibr" rid="B967">967</xref>,<xref ref-type="bibr" rid="B1099">1099</xref>,<xref ref-type="bibr" rid="B1100">1100</xref>]. However, a particularly clear example of iron-mediated neurodegeneration is given by the sequelae consequent upon lesions in a protein known as frataxin involved in the disease Friedreich's ataxia (FA).</p></sec><sec><title>Friedreich's ataxia</title><p>A number of repiratory chain components contain non-heme iron, and the question arises as to how they acquire it [<xref ref-type="bibr" rid="B1101">1101</xref>]. Frataxin is a mitochondrial iron chaperone protein [<xref ref-type="bibr" rid="B1102">1102</xref>-<xref ref-type="bibr" rid="B1109">1109</xref>], involved in the safe insertion of Fe(II) during the production of Fe-S centres in the mitochondrial respiratory chain [<xref ref-type="bibr" rid="B1110">1110</xref>]. As are some other aspects of iron metabolism [<xref ref-type="bibr" rid="B1111">1111</xref>], it is highly conserved in eukaryotes from yeast to humans [<xref ref-type="bibr" rid="B1112">1112</xref>,<xref ref-type="bibr" rid="B1113">1113</xref>], a fact that made the unravelling of its function considerably easier [<xref ref-type="bibr" rid="B1114">1114</xref>-<xref ref-type="bibr" rid="B1123">1123</xref>]. Friedreich's ataxia (FA) is a neurodegenerative disorder that arises from a genetic deficit of frataxin activity, whether by a missense mutation or, much more commonly, via the addition of GAA trinucleotide repeats [<xref ref-type="bibr" rid="B1107">1107</xref>,<xref ref-type="bibr" rid="B1124">1124</xref>-<xref ref-type="bibr" rid="B1127">1127</xref>]. As well as the neurodegeneration and measurable iron deposition, clinical symptoms include cardiac hypertrophy [<xref ref-type="bibr" rid="B1128">1128</xref>] and (pre-)diabetes [<xref ref-type="bibr" rid="B1129">1129</xref>], consistent with the general thesis described here that all are in part manifestations of iron dysregulation, and in which suitable chelation may be beneficial [<xref ref-type="bibr" rid="B1130">1130</xref>,<xref ref-type="bibr" rid="B1131">1131</xref>] (but cf. [<xref ref-type="bibr" rid="B1132">1132</xref>]).</p><p>ROSs are undoubtedly involved in FA [<xref ref-type="bibr" rid="B1133">1133</xref>,<xref ref-type="bibr" rid="B1134">1134</xref>], specifically via Fenton chemistry [<xref ref-type="bibr" rid="B1135">1135</xref>,<xref ref-type="bibr" rid="B1136">1136</xref>], since the attenuation of H<sub>2</sub>O<sub>2 </sub>production (but not of superoxide) [<xref ref-type="bibr" rid="B1110">1110</xref>] ameliorates the disease [<xref ref-type="bibr" rid="B1137">1137</xref>]. The deficit in frataxin causes both an increase in ROS (H<sub>2</sub>O<sub>2</sub>) production via the mitochondrial electron transport deficiency [<xref ref-type="bibr" rid="B1138">1138</xref>] as well as a dysregulation in iron metabolism, potentially a very damaging synergistic <underline>combination</underline> (see later). Elements of its (in)activity that are seen as paradoxical [<xref ref-type="bibr" rid="B1139">1139</xref>] are in fact easily explained when one recognises that it is the combination of free iron with H<sub>2</sub>O<sub>2 </sub>that is especially damaging. The neonatally lethal GRACILE syndrome is also caused by a failure of iron chaperoning into mitochondrial complex III due to mutations in the <italic>BCS1L </italic>gene [<xref ref-type="bibr" rid="B1140">1140</xref>,<xref ref-type="bibr" rid="B1141">1141</xref>].</p></sec><sec><title>Amyotrophic lateral sclerosis (ALS) or Lou Gehrig's disease</title><p>ALS is another progressive inflammatory [<xref ref-type="bibr" rid="B1142">1142</xref>] disease in which motor neuron death causes irreversible wasting of skeletal muscles. It has largely defied efforts to uncover the genetic basis of any predisposition [<xref ref-type="bibr" rid="B1143">1143</xref>], save for a very clear association with defects in a Cu/Zn superoxide dismutase [<xref ref-type="bibr" rid="B33">33</xref>,<xref ref-type="bibr" rid="B1144">1144</xref>-<xref ref-type="bibr" rid="B1146">1146</xref>] that can obviously lead to an increase in the steady-state levels of superoxide (and hence hydroxyl radical formation). There is also significant evidence for the involvement of iron [<xref ref-type="bibr" rid="B1147">1147</xref>,<xref ref-type="bibr" rid="B1148">1148</xref>]. Drug therapies have to date shown rather limited benefits, and more in mouse models of Cu/Zn SOD deficiencies than in humans, though iron chelation therapy does not seem to have figured heavily, and it is recognised that combination therapies might offer better prognoses [<xref ref-type="bibr" rid="B1149">1149</xref>].</p></sec><sec><title>Aging</title><p>Aging or senescence is defined as a decline in performance and fitness with advancing age [<xref ref-type="bibr" rid="B1150">1150</xref>]. Iron stores tend to increase with age [<xref ref-type="bibr" rid="B1151">1151</xref>-<xref ref-type="bibr" rid="B1155">1155</xref>], partly due to dietary reasons [<xref ref-type="bibr" rid="B1156">1156</xref>] (and see [<xref ref-type="bibr" rid="B1157">1157</xref>,<xref ref-type="bibr" rid="B1158">1158</xref>]), as does anaemia [<xref ref-type="bibr" rid="B1159">1159</xref>,<xref ref-type="bibr" rid="B1160">1160</xref>]. So too does the expression of NGAL/Lcn2/siderocalin, a process that can be reversed by melatonin [<xref ref-type="bibr" rid="B1161">1161</xref>]. Mainstream theories of aging [<xref ref-type="bibr" rid="B163">163</xref>,<xref ref-type="bibr" rid="B165">165</xref>,<xref ref-type="bibr" rid="B1162">1162</xref>-<xref ref-type="bibr" rid="B1180">1180</xref>] recognise the relationship between progressive inflammation, cellular damage and repair and the higher-level manifestations of the aging process, and ('the free radical theory of aging' [<xref ref-type="bibr" rid="B1163">1163</xref>,<xref ref-type="bibr" rid="B1181">1181</xref>]) ROSs are of course strongly implicated as partial contributors to the aging process (e.g. [<xref ref-type="bibr" rid="B31">31</xref>,<xref ref-type="bibr" rid="B43">43</xref>,<xref ref-type="bibr" rid="B980">980</xref>,<xref ref-type="bibr" rid="B1163">1163</xref>,<xref ref-type="bibr" rid="B1182">1182</xref>-<xref ref-type="bibr" rid="B1206">1206</xref>]). Needless to say, not least because of the low steady-state net rate of generation of the various ROSs [<xref ref-type="bibr" rid="B1207">1207</xref>], few studies have managed to be very specific mechanistically [<xref ref-type="bibr" rid="B1208">1208</xref>], but it should be clear that all ROSs are not created equal and we need here to concentrate mainly on the 'nasty' parts of ROS metabolism, and in particular on the hydroxyl radical as generated via poorly liganded iron and on peroxynitrite, and to have the greatest effects we need to inhibit both their generation and their reactivity (see Systems Biology section, below). The iron content of cells also increases as cells age normally [<xref ref-type="bibr" rid="B1209">1209</xref>]. As many diseases increase with age, probably via mechanisms highlighted herein, treating aging can thereby treat disease [<xref ref-type="bibr" rid="B162">162</xref>], and it is important to recognise that most 'diseases' are in fact consequences of aging (despite the considerably greater historical focus on the former).</p></sec><sec><title>Frailty</title><p>One issue of aging is not that just it happens but that it can manifest in a series of essentially undesirable physiological changes, referred to as frailty [<xref ref-type="bibr" rid="B1210">1210</xref>], in which ROSs have also been strongly implicated. Indeed, there are many parts of physiology and metabolism that lose functionality during aging (e.g. the cardiovascular system [<xref ref-type="bibr" rid="B1211">1211</xref>] and of course cognitive function [<xref ref-type="bibr" rid="B1212">1212</xref>]), and iron metabolism is known to change considerably as humans age [<xref ref-type="bibr" rid="B980">980</xref>,<xref ref-type="bibr" rid="B1213">1213</xref>], with anaemia a typical accompaniment of aging [<xref ref-type="bibr" rid="B1214">1214</xref>]. The question then arises as to how much of this deranged iron metabolism is causal in accelerated aging, and this is not easy to state at this time. However, lowering iron does increase the lifespan of <italic>Drosophila </italic>[<xref ref-type="bibr" rid="B1215">1215</xref>] and yeast [<xref ref-type="bibr" rid="B1105">1105</xref>]. At all events, the purpose of this rather brief section is to point out to researchers in aging, frailty and gerontology generally the relevance of inadequately controlled iron metabolism as a major part of ROS-induced injuries that may accelerate the aging process.</p></sec><sec><title>Longevity</title><p>Although aging and longevity are not of course the same thing, and longevity is not a 'disease', studies of aging are often performed with the intention of improving our understanding of longevity [<xref ref-type="bibr" rid="B1216">1216</xref>], and certainly longevity is linked to age-related disease [<xref ref-type="bibr" rid="B1217">1217</xref>]. However, the longevity of many organisms can be varied by the manipulation of any number of diseases or processes. This said, caloric or dietary restriction is a well-known contributor to longevity (indeed the only reliable one in pretty well all species [<xref ref-type="bibr" rid="B1218">1218</xref>-<xref ref-type="bibr" rid="B1223">1223</xref>] – although possibly not <italic>H. sapiens </italic>[<xref ref-type="bibr" rid="B1180">1180</xref>]), and appears to act at the root of the processes involved [<xref ref-type="bibr" rid="B1224">1224</xref>]. Caloric restriction appears to be associated with a considerably lowered rate of production of ROSs and accrual of ROS-induced damage [<xref ref-type="bibr" rid="B1207">1207</xref>,<xref ref-type="bibr" rid="B1225">1225</xref>-<xref ref-type="bibr" rid="B1228">1228</xref>], and this is to be expected on general grounds in that a restriction of substrate supply will make the redox poise of mitochondria [<xref ref-type="bibr" rid="B1229">1229</xref>] more oxiding and thereby minimise the amount of 1- and 2-electron reductions of O<sub>2 </sub>to form peroxide and superoxide. It is therefore also of great interest that caloric restriction also benefits iron status [<xref ref-type="bibr" rid="B1230">1230</xref>] and that it is this improved iron status that in part promotes longevity [<xref ref-type="bibr" rid="B1231">1231</xref>]. Caloric restriction has also been shown to effect a differential stress response between normal and tumour cells [<xref ref-type="bibr" rid="B1232">1232</xref>], although this study did not look at relative iron status.</p><p>Antioxidants can also influence lifespan. Thus (rather high doses of) melatonin extended the lifespan (and stress resistance) of <italic>Drosophila </italic>[<xref ref-type="bibr" rid="B1191">1191</xref>,<xref ref-type="bibr" rid="B1233">1233</xref>-<xref ref-type="bibr" rid="B1235">1235</xref>] while that of <italic>Caenorhadbitis elegans </italic>could be extended by mimics [<xref ref-type="bibr" rid="B1236">1236</xref>] of SOD and catalase [<xref ref-type="bibr" rid="B1187">1187</xref>], and by a variety of antioxidant and other pharmacological agents [<xref ref-type="bibr" rid="B1237">1237</xref>].</p><p>As an example, let us consider <italic>C. elegans</italic>. Mutants with a decreased activity of the insulin-like growth factor signalling pathway (e.g. <italic>daf2 </italic>mutants that have a greater amount of the DAF16 FOXO-like transcription factor) can live for nearly twice as long as wild types [<xref ref-type="bibr" rid="B1238">1238</xref>,<xref ref-type="bibr" rid="B1239">1239</xref>] and produce more catalase, superoxide dismutase (sod-3) [<xref ref-type="bibr" rid="B1240">1240</xref>] and glutathione-S-transferase.</p><p>Overall, it is the potent combination of oxidative stress, already leading to damaging peroxides and radicals, and its catalysis and further reactions caused by inappropriately chelated iron, that causes a 'double whammy'. Indeed, iron, copper and H<sub>2</sub>O<sub>2 </sub>have been referred to as the 'toxic triad' [<xref ref-type="bibr" rid="B1032">1032</xref>]. While there is comparatively little that we can do about the production of superoxide and peroxide, we can (by pharmacological or dietary means) try and improve the speciation of iron ions.</p></sec><sec><title>Rheumatoid arthritis</title><p>One disease whose aetiology is well known to be bound up with ROSs is rheumatoid arthritis (RA) [<xref ref-type="bibr" rid="B36">36</xref>,<xref ref-type="bibr" rid="B1241">1241</xref>-<xref ref-type="bibr" rid="B1246">1246</xref>]. What is known of the role of iron metabolism? Generally an overall low iron status – anaemia – is a characteristic of rheumatoid arthritis [<xref ref-type="bibr" rid="B1247">1247</xref>-<xref ref-type="bibr" rid="B1251">1251</xref>], whereas by contrast iron is elevated in the synovial fluid of arthritic joints [<xref ref-type="bibr" rid="B1252">1252</xref>-<xref ref-type="bibr" rid="B1255">1255</xref>]. This suggests a significant derangement of iron metabolism in RA as well, and a mechanism [<xref ref-type="bibr" rid="B1256">1256</xref>-<xref ref-type="bibr" rid="B1259">1259</xref>] in which elevated superoxide liberates free iron from ferritin in synovial fluid (and elsewhere [<xref ref-type="bibr" rid="B1260">1260</xref>]), thereby catalysing further the damaging production of hydroxyl radicals. This autocatalytic process (Fig <xref ref-type="fig" rid="F6">6</xref>) is, even in principle, especially destructive (and may account for species differences in sensitivity to iron loading [<xref ref-type="bibr" rid="B1261">1261</xref>]). Note that erythrocytes when oxidized can also release free iron [<xref ref-type="bibr" rid="B524">524</xref>]. Natural antioxidants such as vitamin E are also lowered [<xref ref-type="bibr" rid="B1262">1262</xref>]. There is some evidence that appropriate iron chelators can ameliorate the symptoms of RA [<xref ref-type="bibr" rid="B1263">1263</xref>], though membrane-impermeant chelators such as desferroxamine cannot [<xref ref-type="bibr" rid="B1264">1264</xref>].</p><fig position="float" id="F6"><label>Figure 6</label><caption><p><bold>Catalysis and autocatalysis in the Haber-Weiss and Fenton reactions leading to the production of the hydroxyl radical, including the liberation by superoxide of free iron from ferritin</bold>.</p></caption><graphic xlink:href="1755-8794-2-2-6"></graphic></fig><p>One interesting feature of RA is that in 75% of women it is strongly ameliorated during pregnancy [<xref ref-type="bibr" rid="B1265">1265</xref>-<xref ref-type="bibr" rid="B1267">1267</xref>]; although the multifactorial nature of this observation has made a mechanistic interpretation difficult, from everything that we have seen so far it would be surprising if changes in iron metabolism were not strongly involved.</p><p>An interesting related feature is the 'restless legs syndrome' [<xref ref-type="bibr" rid="B1268">1268</xref>-<xref ref-type="bibr" rid="B1270">1270</xref>], that is often associated with iron deficiency and pregnancy. Serum transferrin receptor seems to be a rather sensitive measure of this iron deficiency [<xref ref-type="bibr" rid="B273">273</xref>,<xref ref-type="bibr" rid="B1271">1271</xref>,<xref ref-type="bibr" rid="B1272">1272</xref>]. There are relationships with other syndromes that we discuss here, such as cardiovascular disease [<xref ref-type="bibr" rid="B1273">1273</xref>], but in the present review it is of especial interest that a dysregulation of iron metabolism appears to play a significant role [<xref ref-type="bibr" rid="B1274">1274</xref>]</p></sec><sec><title>Lupus (Systemic Lupus Erythematosus)</title><p>Lupus, or Systemic Lupus Erythematosus (SLE) [<xref ref-type="bibr" rid="B1275">1275</xref>,<xref ref-type="bibr" rid="B1276">1276</xref>] describes a syndrome, somewhat related to arthritis and rheumatism, of broadly auto-immunological or inflammatory origin, and with a large variety of manifestations (e.g. [<xref ref-type="bibr" rid="B1277">1277</xref>-<xref ref-type="bibr" rid="B1285">1285</xref>]), but characterised in particular by fatigue [<xref ref-type="bibr" rid="B1286">1286</xref>], often as a result of anaemia. This of course points to a certain level of iron dysregulation (of any number of causes), and there is certain some evidence for this [<xref ref-type="bibr" rid="B1274">1274</xref>,<xref ref-type="bibr" rid="B1287">1287</xref>]. Thus, while anaemia is a feature of the disease, serum ferritin may be raised in SLE [<xref ref-type="bibr" rid="B1288">1288</xref>], and some of the usual lipid markers of oxidative stress (that can be a result of hydroxyl radical production catalysed by poorly liganded iron) are also present [<xref ref-type="bibr" rid="B1289">1289</xref>].</p><p>There is also a very interesting linkage between SLE and vitamin D metabolism [<xref ref-type="bibr" rid="B1290">1290</xref>], something that has also come up in relation to the statins and atherosclerosis ([<xref ref-type="bibr" rid="B832">832</xref>,<xref ref-type="bibr" rid="B1291">1291</xref>], but cf. [<xref ref-type="bibr" rid="B1292">1292</xref>]), and indeed it there is evidence that statins may be of benefit in the treatment and even reversal of lupus [<xref ref-type="bibr" rid="B1293">1293</xref>,<xref ref-type="bibr" rid="B1294">1294</xref>]. Indeed, from a much more general point of view, there is precedent for these kinds of linkages being used to uncover unknown mediators in disease states that may be worth pursuing (e.g. [<xref ref-type="bibr" rid="B6">6</xref>,<xref ref-type="bibr" rid="B19">19</xref>,<xref ref-type="bibr" rid="B20">20</xref>,<xref ref-type="bibr" rid="B1295">1295</xref>,<xref ref-type="bibr" rid="B1296">1296</xref>]).</p></sec><sec><title>Asthma</title><p>Asthma is a well-known inflammatory disease, and has been linked with ROS generation [<xref ref-type="bibr" rid="B1297">1297</xref>] catalysed by iron [<xref ref-type="bibr" rid="B276">276</xref>,<xref ref-type="bibr" rid="B1298">1298</xref>-<xref ref-type="bibr" rid="B1300">1300</xref>].</p></sec><sec><title>Inflammatory bowel diseases (IBD)</title><p>By definition, IBD such as Crohn's disease and ulcerative colitis are inflammatory diseases, and while the inflammation and ROS production are well established here, their origins are somewhat uncertain [<xref ref-type="bibr" rid="B1301">1301</xref>-<xref ref-type="bibr" rid="B1304">1304</xref>]. They are frequently accompanied by anaemia, implying a derangement in iron absorption and/or metabolism [<xref ref-type="bibr" rid="B1305">1305</xref>,<xref ref-type="bibr" rid="B1306">1306</xref>], and very probably absorption [<xref ref-type="bibr" rid="B1307">1307</xref>,<xref ref-type="bibr" rid="B1308">1308</xref>]. The anaemia may be monitored by ferritin and transferrin receptor levels, and its correction is possible by iron supplementation plus erythropoietin [<xref ref-type="bibr" rid="B1309">1309</xref>-<xref ref-type="bibr" rid="B1315">1315</xref>]. One may suppose that some of the issues here relate to iron speciation, that is usually not measured in these studies.</p></sec><sec><title>Age-related macular degeneration</title><p>Age-related macular degeneration (AMD) [<xref ref-type="bibr" rid="B1316">1316</xref>] is now the leading cause of blindness and visual disability in the elderly in developed countries [<xref ref-type="bibr" rid="B1317">1317</xref>-<xref ref-type="bibr" rid="B1320">1320</xref>]. Many components of atherosclerotic plaques have also been demonstrated in drusen [<xref ref-type="bibr" rid="B1321">1321</xref>], a characteristic of AMD and, as here, it is reasonable to propose a common mechanism of pathogenesis between AMD and atherosclerosis. Retinal iron levels increase with age [<xref ref-type="bibr" rid="B1322">1322</xref>], iron is significantly implicated in AMD [<xref ref-type="bibr" rid="B1323">1323</xref>-<xref ref-type="bibr" rid="B1329">1329</xref>], and iron chelation may help to reverse the process [<xref ref-type="bibr" rid="B1330">1330</xref>]. Dietary antioxidants are also protective [<xref ref-type="bibr" rid="B1331">1331</xref>]. The source of the iron appears to be excess angiogenesis and leakage from blood vessels catalysed by VEGF, and a PEGylated aptamer [<xref ref-type="bibr" rid="B1332">1332</xref>-<xref ref-type="bibr" rid="B1334">1334</xref>] against VEGF (pegaptanib) or a monoclonal antibody (ranibizumab) have shown significant promise in the treatment of macular degeneration [<xref ref-type="bibr" rid="B1335">1335</xref>-<xref ref-type="bibr" rid="B1340">1340</xref>]. Plausibly a combination therapy with one of these plus a suitable iron chelator might be even more effective.</p></sec><sec><title>Psoriasis</title><p>Psoriasis is an anflammatory disease in which the production of free radicals and ROSs are strongly implicated [<xref ref-type="bibr" rid="B1341">1341</xref>-<xref ref-type="bibr" rid="B1343">1343</xref>]. Here too there is clear evidence for the involvement of a deranged iron metabolism [<xref ref-type="bibr" rid="B1343">1343</xref>-<xref ref-type="bibr" rid="B1345">1345</xref>]. Early attempts at therapy with a series of unusual iron chelators (that unfortunately had side effects) [<xref ref-type="bibr" rid="B1346">1346</xref>] do not seem to have been followed up.</p></sec><sec><title>Gout</title><p>Gout is another important inflammatory disease, characterised by the accumulation of uric acid [<xref ref-type="bibr" rid="B1347">1347</xref>]. There is considerable evidence that this too is a disease of iron overload, and that uric acid accumulation – as both an antioxidant and an iron chelator [<xref ref-type="bibr" rid="B1348">1348</xref>] – is in response to the iron overload [<xref ref-type="bibr" rid="B1349">1349</xref>,<xref ref-type="bibr" rid="B1350">1350</xref>] and with highly beneficial remission of gouty symptoms occurring on depletion of iron by phlebotomy [<xref ref-type="bibr" rid="B1351">1351</xref>].</p></sec><sec><title>Alcoholic and other forms of liver disease</title><p>It is known that with chronic excess, either iron or alcohol alone may individually injure the liver and other organs, and that in combination, each exaggerates the adverse effects of the other. Specifically, in alcoholic liver disease, both iron and alcohol contribute to the production of hepatic fibrosis [<xref ref-type="bibr" rid="B1352">1352</xref>-<xref ref-type="bibr" rid="B1358">1358</xref>]. Iron overload is well known to lead to hepatotoxicity [<xref ref-type="bibr" rid="B1359">1359</xref>-<xref ref-type="bibr" rid="B1362">1362</xref>] and liver cancer [<xref ref-type="bibr" rid="B1363">1363</xref>,<xref ref-type="bibr" rid="B1364">1364</xref>], and lowering or chelating it is protective [<xref ref-type="bibr" rid="B1365">1365</xref>,<xref ref-type="bibr" rid="B1366">1366</xref>]. Hepcidin may be involved here [<xref ref-type="bibr" rid="B1367">1367</xref>].</p></sec><sec><title>Chronic obstructive pulmonary disorder (COPD) and related lung diseases</title><p>Chronic obstructive pulmonary disease (COPD) is a progressive and chronic disease which is characterised by an apparently inexorable decline in respiratory function, exercise capacity, and health status. It is also characterised by periods in which the symptoms are considerably exacerbated [<xref ref-type="bibr" rid="B1368">1368</xref>-<xref ref-type="bibr" rid="B1371">1371</xref>]. Such an acute exacerbation of COPD (AECOPD) is defined [<xref ref-type="bibr" rid="B1372">1372</xref>] as "a sustained worsening of the patient's condition from the stable state and beyond normal day to day variations, that is acute in onset and necessitates a change in regular medication in a patient with underlying COPD". Smoking is a major source of free radicals (and indeed metals [<xref ref-type="bibr" rid="B1373">1373</xref>]), and is a major cause of COPD. Consequently, there is considerable evidence for the evidence for the involvement of inflammation and ROSs in both the 'stable' and 'exacerbated' stages [<xref ref-type="bibr" rid="B1374">1374</xref>-<xref ref-type="bibr" rid="B1381">1381</xref>].</p><p>Needless to say, there is also considerable evidence for the significance of exposure to iron [<xref ref-type="bibr" rid="B1382">1382</xref>] (as well as exposure to other toxic metals [<xref ref-type="bibr" rid="B1383">1383</xref>]) in the development of COPD and other lung diseases [<xref ref-type="bibr" rid="B1384">1384</xref>]. Haem oxygenase also appears to be a significant culprit [<xref ref-type="bibr" rid="B280">280</xref>], and lung (lavage) iron is increased [<xref ref-type="bibr" rid="B1385">1385</xref>] while transferrin levels can be considerably lower [<xref ref-type="bibr" rid="B1386">1386</xref>].</p><p>Other lung diseases in which ROS and iron have been implicated include Adult Respiratory Distress Syndrome [<xref ref-type="bibr" rid="B1387">1387</xref>-<xref ref-type="bibr" rid="B1390">1390</xref>] and cystic fibrosis [<xref ref-type="bibr" rid="B1391">1391</xref>].</p></sec><sec><title>Smoking</title><p>Tobacco smoke contains many unpleasant and carcinogenic compounds, and that tobacco smoking is a leading cause of carcinoma of the lung and indeed of other organs has become well known since the pioneering epidemiological studies of Doll, Peto and colleagues (e.g. [<xref ref-type="bibr" rid="B1392">1392</xref>-<xref ref-type="bibr" rid="B1395">1395</xref>]). Our purpose here is to point out that many of the particles associated with smoking (and also ingested from other sources) are heavily laden with micro-particulate iron, which, as a major catalyst of hydroxyl radical production, undoubtedly is a substantial contributor as well (see e.g. [<xref ref-type="bibr" rid="B1373">1373</xref>,<xref ref-type="bibr" rid="B1384">1384</xref>,<xref ref-type="bibr" rid="B1396">1396</xref>-<xref ref-type="bibr" rid="B1400">1400</xref>]).</p></sec><sec><title>Cancer and oncology</title><p>In addition to the issues of smoking, the development of cancer can certainly contain an inflammatory component (e.g. [<xref ref-type="bibr" rid="B1401">1401</xref>-<xref ref-type="bibr" rid="B1425">1425</xref>]), and indeed the long-term use of prophylactic anti-inflammatory aspirin lowers colon cancer incidence by 40% (age-adjusted relative risk = 0.6) [<xref ref-type="bibr" rid="B1426">1426</xref>] (though note that this may have other side-effects [<xref ref-type="bibr" rid="B1427">1427</xref>]). (The well-known association between infectious agents such as <italic>H. pylori </italic>[<xref ref-type="bibr" rid="B1428">1428</xref>-<xref ref-type="bibr" rid="B1430">1430</xref>] and e.g. bowel cancer is probably initiated by chronic inflammation.) Given that cells require iron, restricting its supply can also limit the growth of cells, including tumour cells [<xref ref-type="bibr" rid="B1431">1431</xref>-<xref ref-type="bibr" rid="B1442">1442</xref>]. Conversely the iron carrier NGAL is overexpressed in tumours [<xref ref-type="bibr" rid="B410">410</xref>,<xref ref-type="bibr" rid="B411">411</xref>,<xref ref-type="bibr" rid="B1443">1443</xref>], a process mediated via NF-κB [<xref ref-type="bibr" rid="B1444">1444</xref>] (and see later). Further, the roles of iron, not least in the mutagenic effects of metal-catalysed Fenton chemistry, are also of significance in promoting oncogenesis [<xref ref-type="bibr" rid="B1445">1445</xref>-<xref ref-type="bibr" rid="B1461">1461</xref>]. Iron chelators [<xref ref-type="bibr" rid="B1438">1438</xref>,<xref ref-type="bibr" rid="B1462">1462</xref>] are thus a doubly attractive component of anti-cancer therapeutics. The mutagenic, carcinogenic and disease-causing actions of asbestos and related fibres may also be due in significant measure to the ability of the Fe(n) that they contain to catalyse hydroxyl radical production [<xref ref-type="bibr" rid="B1463">1463</xref>-<xref ref-type="bibr" rid="B1475">1475</xref>], while there seem to be complex relations between the likelihood of apoptosis and the differential concentrations of superoxide and H<sub>2</sub>O<sub>2 </sub>[<xref ref-type="bibr" rid="B1476">1476</xref>,<xref ref-type="bibr" rid="B1477">1477</xref>]. Overall, it is becoming increasingly widely recognised that anti-inflammatory agents have a role to play in the treatment of cancers; we would suggest that iron chelation may be a useful component of such treatments.</p></sec><sec><title>Malaria</title><p>Just as do tumour cells, the malarial parasite <italic>Plasmodium falciparum </italic>requires considerable iron for growth, and there is evidence that lowering the amount of available iron provides a promising route to antimalarials (e.g. [<xref ref-type="bibr" rid="B1478">1478</xref>-<xref ref-type="bibr" rid="B1494">1494</xref>], but cf. [<xref ref-type="bibr" rid="B1495">1495</xref>]). Note in this context that iron-catalysed radical formation is also significantly involved in the antimalarial (i.e. cytotoxic) mode of action of artemisinin [<xref ref-type="bibr" rid="B1494">1494</xref>,<xref ref-type="bibr" rid="B1496">1496</xref>-<xref ref-type="bibr" rid="B1504">1504</xref>], and this reaction is in fact inhibited by iron chelators [<xref ref-type="bibr" rid="B1505">1505</xref>] such that <underline>a combined artemisinin-chelator therapy would be <bold>contraindicated</bold></underline>.</p></sec><sec><title>Antimicrobials</title><p>Lower down the evolutionary scale, and as presaged earlier in the section on bacterial siderophores, microbes require iron for growth, its presence may be limiting even at the scale of global CO<sub>2 </sub>fixation [<xref ref-type="bibr" rid="B1506">1506</xref>-<xref ref-type="bibr" rid="B1509">1509</xref>], its excess can in some circumstances [<xref ref-type="bibr" rid="B1510">1510</xref>] correlate with infectivity or virulence (see above and e.g. [<xref ref-type="bibr" rid="B180">180</xref>,<xref ref-type="bibr" rid="B193">193</xref>,<xref ref-type="bibr" rid="B1493">1493</xref>,<xref ref-type="bibr" rid="B1511">1511</xref>-<xref ref-type="bibr" rid="B1531">1531</xref>]), and its chelation in a form not available to bacteria offers a route to at least a bacteriostatic kind of antibiotic or to novel therapies based on the lowering of iron available to microbes by using hepcidin [<xref ref-type="bibr" rid="B1532">1532</xref>] or NGAL [<xref ref-type="bibr" rid="B1533">1533</xref>]. Iron chelators are also inhibitory to trypanosomes [<xref ref-type="bibr" rid="B1534">1534</xref>,<xref ref-type="bibr" rid="B1535">1535</xref>], and changes in iron metabolism are also associated with viral infections [<xref ref-type="bibr" rid="B1536">1536</xref>].</p></sec><sec><title>Sepsis leading to organ failure and death: severe inflammatory response syndrome</title><p>It is well known that one consequence of bacterial infection (sepsis) can be septic shock, that this can be mimicked by the Gram-negative bacterial outer membrane component LPS (lipopolysaccharide), and that in the worst cases this leads via multiple organ failure to death. However, whatever LPS does it is quite independent of the present of viable (i.e. growing or culturable – see [<xref ref-type="bibr" rid="B1537">1537</xref>,<xref ref-type="bibr" rid="B1538">1538</xref>]) bacteria as the same phenomena leading to multiple organ failure (MOF) are seen without infection [<xref ref-type="bibr" rid="B1539">1539</xref>,<xref ref-type="bibr" rid="B1540">1540</xref>]. Consequently, the recognition of a series of symptoms contingent on this initial inflammatory response has led to the development of the idea of a Systemic Inflammatory Response Syndrome (SIRS) [<xref ref-type="bibr" rid="B1541">1541</xref>-<xref ref-type="bibr" rid="B1551">1551</xref>] that leads to the MOF, both via apoptosis [<xref ref-type="bibr" rid="B1552">1552</xref>] and necrosis [<xref ref-type="bibr" rid="B1553">1553</xref>,<xref ref-type="bibr" rid="B1554">1554</xref>]. There is by now little doubt that these phenomena too are associated with the hyperproduction of ROSs [<xref ref-type="bibr" rid="B1546">1546</xref>,<xref ref-type="bibr" rid="B1551">1551</xref>,<xref ref-type="bibr" rid="B1555">1555</xref>-<xref ref-type="bibr" rid="B1570">1570</xref>]. Circulating free iron is raised in sepsis and related conditions [<xref ref-type="bibr" rid="B1400">1400</xref>,<xref ref-type="bibr" rid="B1571">1571</xref>-<xref ref-type="bibr" rid="B1573">1573</xref>]. Direct assays of oxidant induced cell death indicate that most 'free' iron is concentrated in lysosomes [<xref ref-type="bibr" rid="B1574">1574</xref>-<xref ref-type="bibr" rid="B1577">1577</xref>], that its decompartmentation is substantially involved [<xref ref-type="bibr" rid="B1570">1570</xref>], and that its chelation can thus prevent cell death [<xref ref-type="bibr" rid="B1578">1578</xref>-<xref ref-type="bibr" rid="B1581">1581</xref>].</p><p>Many circulating inflammatory factors have been identified as important in the development of septic shock, including cytokines such as Tissue Necrosis Factor (TNF) [<xref ref-type="bibr" rid="B1582">1582</xref>], and cellular responses via the Toll-Like Receptor are clearly involved in this process [<xref ref-type="bibr" rid="B1583">1583</xref>,<xref ref-type="bibr" rid="B1584">1584</xref>]. However, we would argue that since antibodies against TNF do not inhibit the sequelae of septic shock such as multiple organ failure, the truly damaging agents are caused elsewhere and are likely to involve the iron-mediated production of damaging hydroxyl radicals (see also [<xref ref-type="bibr" rid="B1563">1563</xref>]).</p><p>In this regard, it is especially interesting that the antioxidant melatonin is particularly effective in preventing septic shock [<xref ref-type="bibr" rid="B1585">1585</xref>-<xref ref-type="bibr" rid="B1587">1587</xref>], and a variety of suitable antioxidants have shown potential here [<xref ref-type="bibr" rid="B1573">1573</xref>,<xref ref-type="bibr" rid="B1588">1588</xref>-<xref ref-type="bibr" rid="B1591">1591</xref>], notably in combination with iron chelators [<xref ref-type="bibr" rid="B1592">1592</xref>,<xref ref-type="bibr" rid="B1593">1593</xref>] (and see also [<xref ref-type="bibr" rid="B1594">1594</xref>,<xref ref-type="bibr" rid="B1595">1595</xref>]). As with quite a number of the indications given above, a further link with Fe metabolism is seen in the protective effects of erythropoietin [<xref ref-type="bibr" rid="B1596">1596</xref>,<xref ref-type="bibr" rid="B1597">1597</xref>].</p></sec></sec><sec><title>Pro- and anti-oxidants and their contributions to cellular physiology</title><p>A very great many cellular metabolites are redox active within the range of redox potentials realistically accessible to biology (including some molecules such as proline [<xref ref-type="bibr" rid="B1598">1598</xref>] that are not commonly considered to be redox-active), and it is not our purpose here to list them extensively. Not only their redox potential and status but even their absolute amounts can have profound effects on metabolism [<xref ref-type="bibr" rid="B1599">1599</xref>]). Our chief point here is that it is the intersection of iron metabolism and oxygen <underline>reduction</underline> that needs to be the focus, with the 'iron'-catalysed production of hydroxyl radical being the nexus, with the standard redox potential of a redox couple <italic>per se </italic>being less significant in absolute terms, and the redox potential that a particular redox couple 'feels' being dependent in a complex manner on a variety of thermodynamic and kinetic factors [<xref ref-type="bibr" rid="B1229">1229</xref>]. Thus, although ascorbate is 'reducing' and an 'antioxidant', its reaction with O<sub>2</sub>, especially when catalysed by Fe(II), produces superoxide and thence OH<sup>• </sup>radicals that may be pro-oxidant. It is this kind of stepwise multi-electron-transfer phenomenon that explains the otherwise possibly puzzling observation of the oxidant-induced reduction of respiratory chain components (see e.g. [<xref ref-type="bibr" rid="B1600">1600</xref>,<xref ref-type="bibr" rid="B1601">1601</xref>]). Consequently, it is extremely unwise to make pronouncements on the role of 'ROSs' without being quite explicit about which ones are meant.</p><p>Thus anything – even an antioxidant – that e.g. by reaction with O<sub>2 </sub>produces superoxide, peroxide and hydroxyl radicals will turn out to be a pro-oxidant if the flux to superoxide and in particular to hydroxyl radicals is stimulated. Thermodynamically, the 1-electron reduction by ascorbate of dioxygen is disfavoured, with the 2-electron reduction to peroxide being the thermodynamically preferred route. However, such reactions are heavily restricted kinetically in the absence of any catalysts [<xref ref-type="bibr" rid="B130">130</xref>]. It is an unfortunate fact that the oxygen-mediated "autoxidation" of ascorbate does in fact occur at considerable rates when it is accelerated by the presence of iron or other transition metal ions [<xref ref-type="bibr" rid="B130">130</xref>,<xref ref-type="bibr" rid="B1602">1602</xref>-<xref ref-type="bibr" rid="B1606">1606</xref>]. In a similar vein, 'free' or inadequately liganded Fe(II) catalyses the production of hydroxyl radicals from oxygen plus a variety of natural biomolecules, including adrenaline (epinephrine) [<xref ref-type="bibr" rid="B1607">1607</xref>], haemin [<xref ref-type="bibr" rid="B1608">1608</xref>], and even peptides such as the amyloid-β involved in the development of Alzheimer's disease [<xref ref-type="bibr" rid="B1009">1009</xref>,<xref ref-type="bibr" rid="B1027">1027</xref>]. Dietary antioxidants (see below) can therefore act in complex and synergistic ways depending on iron status [<xref ref-type="bibr" rid="B1609">1609</xref>]. In this regard, the idea of using elemental iron plus ascorbate in food supplements [<xref ref-type="bibr" rid="B1610">1610</xref>] does not seem a good one.</p><p>It should be noted that there are also occasions, e.g. in the decomposition of refractory polymers such as lignin, where such radical production is involved beneficially [<xref ref-type="bibr" rid="B1611">1611</xref>].</p><p>Finally, a variety of molecules can trap hydroxyl radicals, including hippurate [<xref ref-type="bibr" rid="B1612">1612</xref>], melatonin [<xref ref-type="bibr" rid="B1233">1233</xref>,<xref ref-type="bibr" rid="B1585">1585</xref>,<xref ref-type="bibr" rid="B1586">1586</xref>,<xref ref-type="bibr" rid="B1613">1613</xref>-<xref ref-type="bibr" rid="B1631">1631</xref>] and salicylate [<xref ref-type="bibr" rid="B1632">1632</xref>].</p></sec><sec><title>Antioxidants as therapeutic agents? Should we be including iron chelators in such clinical trials?</title><p>Given the wide recognition of the importance of ROSs in a variety of diseases as described above, many investigators have considered the use of known antioxidants such as vitamins C (ascorbate) and E (α-tocopherol) in preventative therapy. Although there have been some successes (e.g. [<xref ref-type="bibr" rid="B1633">1633</xref>]), the results have generally been decidedly mixed, with little clinical benefit (or even actual disbenefit) following from their administration [<xref ref-type="bibr" rid="B692">692</xref>,<xref ref-type="bibr" rid="B1588">1588</xref>,<xref ref-type="bibr" rid="B1634">1634</xref>-<xref ref-type="bibr" rid="B1639">1639</xref>], e.g. for ALS [<xref ref-type="bibr" rid="B1640">1640</xref>], atherosclerosis [<xref ref-type="bibr" rid="B106">106</xref>,<xref ref-type="bibr" rid="B764">764</xref>], cardiovascular disease [<xref ref-type="bibr" rid="B1641">1641</xref>-<xref ref-type="bibr" rid="B1645">1645</xref>], neuroprotection [<xref ref-type="bibr" rid="B1646">1646</xref>], macular degeneration [<xref ref-type="bibr" rid="B1647">1647</xref>], pre-eclampsia [<xref ref-type="bibr" rid="B1648">1648</xref>-<xref ref-type="bibr" rid="B1652">1652</xref>], critical care medicine [<xref ref-type="bibr" rid="B1653">1653</xref>], aging [<xref ref-type="bibr" rid="B1165">1165</xref>,<xref ref-type="bibr" rid="B1168">1168</xref>,<xref ref-type="bibr" rid="B1654">1654</xref>,<xref ref-type="bibr" rid="B1655">1655</xref>], lung disease [<xref ref-type="bibr" rid="B1656">1656</xref>], elective surgery involving ischaemia-reperfusion [<xref ref-type="bibr" rid="B1657">1657</xref>], all-cause mortality [<xref ref-type="bibr" rid="B1637">1637</xref>,<xref ref-type="bibr" rid="B1658">1658</xref>], etc. One interpretation for these disappointing results, that is consistent with the general theme of this review, involves the recognition that a variety of <underline>anti</underline>oxidants can in fact act as <underline>pro</underline>-oxidants and thus actually <underline>promote</underline> the production of OH<sup>• </sup>radicals in the presence of inappropriately or inadequately liganded Fe(II) [<xref ref-type="bibr" rid="B130">130</xref>,<xref ref-type="bibr" rid="B528">528</xref>,<xref ref-type="bibr" rid="B1602">1602</xref>,<xref ref-type="bibr" rid="B1604">1604</xref>,<xref ref-type="bibr" rid="B1659">1659</xref>,<xref ref-type="bibr" rid="B1660">1660</xref>]. (One might also comment that the intracellular location of the <underline>anti</underline>oxidants may be an issue, and that the view that targeting them to mitochondria may well have considerable merit [<xref ref-type="bibr" rid="B1661">1661</xref>-<xref ref-type="bibr" rid="B1663">1663</xref>].) Thus any predictions about the utility or otherwise of <underline>anti</underline>oxidants need to take into account the amount of 'free' iron present. <bold>In particular, we would suggest that future trials of this type might beneficially include appropriate iron chelators, whether alone or with <underline>anti</underline>oxidants.</bold></p></sec><sec><title>Liganding and reactivity of Fe(n)</title><p>Given the damage that iron-mediated OH<sup>• </sup>radical can create, the question arises as to whether appropriate chelators can inhibit this by inhibiting the production of OH<sup>•</sup>, and while the answer is 'yes' the interpretation of the relevant experiments is not always as clear cut as one would wish [<xref ref-type="bibr" rid="B43">43</xref>]. This is because the OH<sup>• </sup>radical is so reactive that its production is normally assessed by addition of the putative chelator and observation of its effect on the rate of reaction of a target molecule such as salicylate with the OH<sup>• </sup>generated. The ability of a chelator to inhibit such a reaction can then occur not only via a reduction in the rate of OH<sup>• </sup>production but by trapping the OH<sup>• </sup>itself, as well as by other mechanisms [<xref ref-type="bibr" rid="B1664">1664</xref>]. This said, there is little doubt that iron chelators can be highly protective, and it is many ways very surprising that their use is not more widespread.</p><p>We begin by noting that the reactivity of iron does vary greatly depending upon its liganding environment [<xref ref-type="bibr" rid="B71">71</xref>]. Cheng <italic>et al</italic>. state [<xref ref-type="bibr" rid="B72">72</xref>] "Oxygen ligands prefer Fe(III); thus, the reduction potential of the iron is decreased. Conversely, nitrogen and sulfur ligands stabilize Fe(II); thus, the reduction potential of the iron is increased. Therefore, chelators with oxygen ligands, such as citrate, promote the oxidation of Fe(II) to Fe(III), while chelators that contain nitrogen ligands, such as phenanthroline, inhibit the oxidation of Fe(II). Many chelators, such as EDTA and Desferal (DFO), will bind both Fe(II) and Fe- (III); however, the stability constants are much greater for the Fe(III)-chelator complexes. Therefore, these chelators will bind Fe(II) and subsequently promote the oxidation of the Fe(II) to Fe(III) with the concomitant reduction of molecular oxygen to partially reduced oxygen species. Since the maximal coordination number of iron is six, the hexadentate chelators can provide more consistently inert complexes due to their ability to completely saturate the coordination sphere of the iron atom and, consequently, deactivate the "free iron" completely. For example, DFO is a very effective antioxidant in clinical application because of its potential to markedly decrease the redox activity of iron [<xref ref-type="bibr" rid="B137">137</xref>]." However, it is not easy to make hexadentate ligands orally active [<xref ref-type="bibr" rid="B1665">1665</xref>].</p><p>Iron typically can coordinate 6 ligands in an octahedral arrangement. Preferential chelation of the Fe(II) or the Fe(III) form necessarily changes its redox potential as a result of Le Chatelier's principle, and from Marcus theory [<xref ref-type="bibr" rid="B1666">1666</xref>-<xref ref-type="bibr" rid="B1669">1669</xref>] the rate of outer-sphere electron transfer reactions is typically related to differences in the free energy change, i.e. the differences in redox potentials of the interacting partners. In addition, it widely recognised that [<xref ref-type="bibr" rid="B137">137</xref>] "The tight binding of low molecular {weight} chelators via coordinating ligands such as O, N, S to iron blocks the iron's ability to catalyze redox reactions. Since the maximal coordination number of iron is six, it is often argued that the hexadentate chelators can provide more consistently inert complexes due to their ability to completely saturate the coordination sphere of the Fe atom. Consequently, a chelator molecule that binds to all six sites of the Fe ion completely deactivates the "free iron". Such chelators are termed "hexidentate" {sic}, of which desferrioxamine is an example. There are many Fe chelators that inhibit the reactions of Fe, oxygen, and their metabolites. For example, desferrioxamine ... (DFO) markedly decreases the redox activity of Fe(III) and is a very effective antioxidant through its ability to bind Fe."</p><p>By contrast, bidentate or tridentate chelators that bind to only 2 or 3 of the available iron chelation sites, especially when they bind to both Fe(II) and Fe(III), can in fact catalyse redox cycling and thereby promote free radical generation [<xref ref-type="bibr" rid="B1437">1437</xref>,<xref ref-type="bibr" rid="B1665">1665</xref>,<xref ref-type="bibr" rid="B1670">1670</xref>,<xref ref-type="bibr" rid="B1671">1671</xref>]. Thus, the most potent iron chelators will normally be hexadentate (but may consequently strip iron from iron-containing enzyme and thereby have deleterious side effects). Bi- or tri-dentate ligands should therefore be at saturating concentrations for maximum effect.</p><p>Generally, the harder ligands that favour Fe(III) involve O whereas softer ligands that bind Fe(II) involve N and S. The type of ligand also influences the absorption spectrum of the ferric form of the chelator, such that conclusions can be drawn about the types of group involved in the complex. These charge transfer bands that appear on ligand binding are at around 340 nm for carboxylates, around 425 nm for trishydroxamates, 470 nm for bis-hydroxamates, 515 nm for monohydroxamates, around 480 nm for tris-catecholates, 560 nm for bis-catecholates and 680 nm for mono-catecholates [<xref ref-type="bibr" rid="B173">173</xref>]. In addition, for tris-bidentate complexes the complex can, on an octahedral arrangement, have two different configurations, a left-handed propeller, termed the Λ-configuration, and a righthanded propeller, the Δ-configuration [<xref ref-type="bibr" rid="B173">173</xref>].</p><sec><title>Iron chelators – those approved and used clinically</title><p>A number of reviews (e.g. [<xref ref-type="bibr" rid="B1437">1437</xref>,<xref ref-type="bibr" rid="B1438">1438</xref>,<xref ref-type="bibr" rid="B1672">1672</xref>-<xref ref-type="bibr" rid="B1678">1678</xref>]) cover aspects of iron chelators that have had or may have utility clinically.</p><p>Whitnall and Richardson [<xref ref-type="bibr" rid="B1062">1062</xref>] list a number of useful features of an experimentally (and clinically) useful iron chelator. Thus, "A compound suitable for the treatment of neurodegenerative disease should possess a number of qualities, namely (1) strong affinity for FeIII, (2) low molecular weight, (3) lipophilicity high enough to accommodate permeation of cell membranes and the BBB, (4) oral activity, and (5) minimal toxicity [<xref ref-type="bibr" rid="B1062">1062</xref>]. Also, partly because there are few trivalent ions other than Fe(III) that the body actually needs, the major synthetic focus has been on the design of FeIII-selective chelators which feature "hard" oxygen donor atoms. Additionally, under aerobic conditions, high-affinity FeIII chelators will tend to chelate FeII to facilitate autoxidation, such that high-affinity FeIII-selective compounds will beneficially bind both FeIII and FeII under most physiological conditions" [<xref ref-type="bibr" rid="B1062">1062</xref>]. (Note that liophilicity <italic>per se </italic>may not be relevant, as drugs require carriers to cross membranes [<xref ref-type="bibr" rid="B18">18</xref>], and promiscuity and off-target effects increase with lipophilicity [<xref ref-type="bibr" rid="B1679">1679</xref>].)</p><p>Desferrioxamines are nonpeptide hydroxamate siderophores composed of alternating dicarboxylic acid and diamine units. linked by amide bonds. They are produced by many <italic>Streptomyces </italic>species [<xref ref-type="bibr" rid="B1680">1680</xref>]. Desferrioxamine B is a linear (acyclic) substance produced (industrially) by the actinobacterium <italic>Streptomyces pilosus </italic>[<xref ref-type="bibr" rid="B1681">1681</xref>], and is widely used as an iron chelator for the prevention and treatment of the effects of iron overload. It is commercially available as desferal (desferrioxamine methane sulphonate), also known as deferoxamine in the USA. It has been very effective in the treatment of a number of diseases, leading to the view that such molecules should have considerable therapeutic potential. A significant disadvantage of DFO is that it does not seem to cross the intestine intact (despite the rather catholic substrate specificity of intestinal peptide transporters [<xref ref-type="bibr" rid="B1682">1682</xref>-<xref ref-type="bibr" rid="B1685">1685</xref>]) and must therefore be given intravenously or subcutaneously. By contrast, another chelator known as Deferriprone or L1 does appear to cross cell membranes, but it is only bidentate.</p><p>Those with approval for clinical use are few in number and we deal with them first. Table <xref ref-type="table" rid="T1">1</xref> compares them with the 'ideal' properties of a clinically useful iron chelator, while Fig <xref ref-type="fig" rid="F7">7</xref> gives the structure of the three most common, viz. desferal (deferoxamine), ferriprox (L1 or deferiprone) and exjade (ICL670 or deferasirox). (Dexrazoxane, a hexadentate chelator, is also marketed [<xref ref-type="bibr" rid="B1686">1686</xref>].)</p><fig position="float" id="F7"><label>Figure 7</label><caption><p><bold>Some iron chelators that are in clinical use (left hand side) or that have been proposed</bold>.</p></caption><graphic xlink:href="1755-8794-2-2-7"></graphic></fig><table-wrap position="float" id="T1"><label>Table 1</label><caption><p>Comparison of the main available iron chelators to an ideal chelation drug (modified from [<xref ref-type="bibr" rid="B2469">2469</xref>])</p></caption><table frame="hsides" rules="groups"><thead><tr><td></td><td align="center"><bold>"Ideal chelator"</bold></td><td align="center"><bold>Deferoxamine</bold></td><td align="center"><bold>Deferiprone</bold></td><td align="center"><bold>Deferasirox</bold></td></tr></thead><tbody><tr><td align="left">Route of administration</td><td align="left">Oral</td><td align="left">Parenteral, usually subcutaneous or intravenous</td><td align="left">Oral</td><td align="left">Oral</td></tr><tr><td align="left">Plasma half-life</td><td align="left">Long enough to give constant protection from labile plasma iron</td><td align="left">Short (minutes); requires constant delivery</td><td align="left">Moderate (< 2 hours). Requires at least 3-times-per-day dosing</td><td align="left">Long, 8–16 hours; remains in plasma at 24 h</td></tr><tr><td align="left">Therapeutic index</td><td align="left">High</td><td align="left">High at moderate doses in iron-overloaded subjects</td><td align="left">Idiosyncratic side effects are most important</td><td align="left">Probably high in iron overloaded subjects*</td></tr><tr><td align="left">Molar iron chelating efficiency; charge of iron (III) complex</td><td align="left">High, uncharged</td><td align="left">High (hexadentate); charged</td><td align="left">Low (bidentate); uncharged</td><td align="left">Moderate (tridentate); uncharged</td></tr><tr><td align="left">Important side effects</td><td align="left">None or only in iron-depleted subjects</td><td align="left">Auditory and retinal toxicity; effects on bones and growth; potential lung toxicity, all at high doses; local skin reactions at infusion sites</td><td align="left">Rare but severe agranulocytosis; mild neutropenia; common abdominal discomfort; erosive arthritis</td><td align="left">Abdominal discomfort; rash or mild diarrhoea upon initiation of therapy; mild increased creatinine level</td></tr><tr><td align="left">Ability to chelate intracellular cardiac and other tissue iron in humans</td><td align="left">High</td><td align="left">Probably lower than deferiprone and deferasirox (it is not clear why)</td><td align="left">High in clinical and in <italic>in vitro </italic>studies</td><td align="left">Insufficient clinical data available; promising in laboratory studies</td></tr></tbody></table><table-wrap-foot><p>*Nephrotoxicity that has been observed in non-iron-loaded animals has been minimal in iron-overloaded humans, but effectiveness is demonstrated only at higher end of tested doses, as discussed in [<xref ref-type="bibr" rid="B1693">1693</xref>].</p></table-wrap-foot></table-wrap><p>Desferal (deferoxamine) is the most used chelator for historical reasons. It is hexadentate but is not orally bioavailable. Ferriprox (deferiprone) is a bidentate ligand (1,2-dimethyl, 3-hydroxypyridin-4-one). It is orally bioavailable although comparatively high doses are required, and it postdates desferal. "Deferiprone has high affinity for iron and interacts with almost all the iron pools at the molecular, cellular, tissue and organ levels. Doses of 50–120 mg/kg/day appear to be effective in bringing patients to negative iron balance" [<xref ref-type="bibr" rid="B1687">1687</xref>]. It can have somewhat better properties than desferal [<xref ref-type="bibr" rid="B1688">1688</xref>]. Finally, Exjade (ICL670) (deferasirox) [<xref ref-type="bibr" rid="B1689">1689</xref>-<xref ref-type="bibr" rid="B1702">1702</xref>] is the most recent chelator approved for clinical use, and is tridentate. It is orally active, and there is a large bibliography at <ext-link ext-link-type="uri" xlink:href="http://www.exjade.com/utils/bibliography.jsp?disclaimer=Y"></ext-link>. The recommended initial daily dose of Exjade is 20 mg/kg body weight.</p><p>It is clear from Table <xref ref-type="table" rid="T1">1</xref> that in the time evolution from deferoxamine through deferiprone to deferasirox there has been a noticeable improvement in the general properties of iron chelators, although there are few published data on the quantitative structure-activity relationships of candidate molecules that might allow one to design future ones rationally. What is certainly clear is that there is a trade-off in properties, and that appropriate chelators will keep iron levels intermediate, i.e. not too low and not too high (a 'Goldilocks' strategy, if you will), and that hexadentate molecules may correspondingly be too tightly binding and strip iron from important molecules that need it. What is particularly important, as well as a good plasma half-life, is the ability to cross cell membranes, as this is necessary both for oral administration and for ensuring that the chelator in question actually accesses the intracellular 'free' iron pools of interest. Which carriers are used for this in humans <italic>in vivo </italic>is presently uncertain [<xref ref-type="bibr" rid="B18">18</xref>,<xref ref-type="bibr" rid="B1703">1703</xref>].</p></sec><sec><title>Drugs that have been approved for clinical use for other purposes, but that also happen to be iron chelators</title><p>The high investment of time, money and intellectual activity necessary to get a drug approved clinically has led to a number of strategies to exploit those that already have been approved and are thus considered 'safe'. One such strategy is the combination therapy of approved drugs that can yet serve for novel indications (e.g. [<xref ref-type="bibr" rid="B1704">1704</xref>-<xref ref-type="bibr" rid="B1708">1708</xref>]). Another strategy is to look for antioxidant or iron-binding chemical motifs in drugs that have already been approved for other purposes [<xref ref-type="bibr" rid="B1709">1709</xref>] (or to measure such properties directly).</p><p>Clioquinol (CQ) [<xref ref-type="bibr" rid="B1062">1062</xref>,<xref ref-type="bibr" rid="B1674">1674</xref>,<xref ref-type="bibr" rid="B1710">1710</xref>,<xref ref-type="bibr" rid="B1711">1711</xref>] (Fig <xref ref-type="fig" rid="F7">7</xref>) is one existing (anti-parasitic) drug that has been proposed for use as an iron chelator, as it contains the known iron-chelating 8-hydroxyquinoline moiety. It has indeed enjoyed some success in this role. However, clioquinol toxicity has been reported if it is used over an extended period [<xref ref-type="bibr" rid="B1712">1712</xref>] and this may be due to the formation of a Zn-clioquinol chelate [<xref ref-type="bibr" rid="B1713">1713</xref>].</p><p>A particular attraction of such existing drugs is that they are likely to have favourable pharmacokinetics and pharmacodynamics, and in particular are likely to be cell-permeable. Note that despite a widespread assumption that lipophilicity or log P is sufficient to account for drug distribution this is not in fact the case, as there are hundreds of natural transporters that drugs can use (e.g. [<xref ref-type="bibr" rid="B18">18</xref>,<xref ref-type="bibr" rid="B1714">1714</xref>]). For instance, the iron-chelating 8-hydroxy quinoline motif contained in molecules such as clioquinol is also present in the tryptophan catabolite xanthurenic acid (Fig <xref ref-type="fig" rid="F7">7</xref>), and it is likely that transmembrane transport of the synthetic drug molecule occurs via natural carriers whose 'normal' role is to transport endogenous but structurally related molecules [<xref ref-type="bibr" rid="B18">18</xref>,<xref ref-type="bibr" rid="B1703">1703</xref>].</p></sec><sec><title>Iron chelators that have been studied but not yet approved</title><p>Given the importance of the field, many academic investigators have sought to develop their own iron chelators that might exhibit the desirable properties listed above. One class of molecule includes isonicotinylhydrazones. Thus, pyridoxal isonicotinyl hydrazone (PIH) [<xref ref-type="bibr" rid="B1672">1672</xref>,<xref ref-type="bibr" rid="B1715">1715</xref>-<xref ref-type="bibr" rid="B1720">1720</xref>] is a promising molecule (also proposed in anti-cancer therapy), although it is hydrolysed both <italic>in vivo </italic>and <italic>in vitro </italic>[<xref ref-type="bibr" rid="B1721">1721</xref>]. Other analogues include salicylaldehyde (SIH) [<xref ref-type="bibr" rid="B1722">1722</xref>] and 2-hydroxy-1-napthylaldehyde (NIH) isonicotinyl hydrazones. PIH was disclosed before being patented, and is thus seen as having no pharmaceutical (company) interest. Various other derivatives are therefore being considered [<xref ref-type="bibr" rid="B1035">1035</xref>,<xref ref-type="bibr" rid="B1462">1462</xref>], including pyrazinylketone isonicotinoyl hydrazones [<xref ref-type="bibr" rid="B1723">1723</xref>].</p><p>A variety of 8-hydroxyquinolines (8HQs) [<xref ref-type="bibr" rid="B1724">1724</xref>] have been considered, although as with other bidentate and tridentate ligands that cannot necessarily effect complete liganding of iron there is always a danger that inadequate concentrations might be pro-oxidant (e.g. [<xref ref-type="bibr" rid="B1725">1725</xref>,<xref ref-type="bibr" rid="B1726">1726</xref>]). One molecule, VK-28, combines various pertinent moieties and has shown some promise in the treatment of neurological disorders [<xref ref-type="bibr" rid="B1727">1727</xref>-<xref ref-type="bibr" rid="B1730">1730</xref>]. This strategy of combining drug elements that can hit multiple targets ('polypharmacology' [<xref ref-type="bibr" rid="B807">807</xref>,<xref ref-type="bibr" rid="B1731">1731</xref>-<xref ref-type="bibr" rid="B1734">1734</xref>]) has much to commend it, including on theoretical grounds, and we discuss these in the section on systems biology below. Another 8HQ that has elicited interest is O-trensox [<xref ref-type="bibr" rid="B1431">1431</xref>,<xref ref-type="bibr" rid="B1735">1735</xref>-<xref ref-type="bibr" rid="B1742">1742</xref>].</p><p>Other ligands or motifs that might be considered include di-2-pyridylketone-4,4,-dimethyl-3-thiosemicarbazone (Dp44mT), that has been shown to be effective against tumours [<xref ref-type="bibr" rid="B1743">1743</xref>], 2,2'-dipyridyl, 1,10-phenanthroline [<xref ref-type="bibr" rid="B1744">1744</xref>,<xref ref-type="bibr" rid="B1745">1745</xref>], 2-benzoylpyridine thiosemicarbazones [<xref ref-type="bibr" rid="B1746">1746</xref>] and thiohydrazones [<xref ref-type="bibr" rid="B1747">1747</xref>]. HBED (Fig <xref ref-type="fig" rid="F7">7</xref>) (N,N'-bis-(2-hydroxybenzyl)ethylenediamine-N,N'-diacetic acid) forms a 1:1 complex with Fe(III) but is probably only tetradentate [<xref ref-type="bibr" rid="B1748">1748</xref>]. It seems not to be very orally active [<xref ref-type="bibr" rid="B1749">1749</xref>] but may be more effective than is DFO [<xref ref-type="bibr" rid="B1750">1750</xref>-<xref ref-type="bibr" rid="B1752">1752</xref>]. Poly-hydroxylated 1,4-naphthoquinones occur as sea urchin pigments and have shown protective effects [<xref ref-type="bibr" rid="B1753">1753</xref>].</p><p>Continuing the theme of polypharmacology, R-(α)-lipoic acid [<xref ref-type="bibr" rid="B1754">1754</xref>-<xref ref-type="bibr" rid="B1757">1757</xref>] is also an antioxidant, that may in addition act by stimulating other anti-oxidant pathways [<xref ref-type="bibr" rid="B1758">1758</xref>]. Finally, one interesting area is that of prochelators (e.g. [<xref ref-type="bibr" rid="B1759">1759</xref>]) in which the oxidant itself triggers the formation of a chelator able to inhibit the Fenton reaction.</p></sec></sec><sec><title>Utility of iron chelators in disease amelioration</title><p>Therapeutic uses of iron chelators have been widely and usefully reviewed (e.g. [<xref ref-type="bibr" rid="B1437">1437</xref>,<xref ref-type="bibr" rid="B1489">1489</xref>,<xref ref-type="bibr" rid="B1676">1676</xref>,<xref ref-type="bibr" rid="B1760">1760</xref>-<xref ref-type="bibr" rid="B1767">1767</xref>]). Many problems remain, such as bioavailability, mis-dosing [<xref ref-type="bibr" rid="B1768">1768</xref>] (too little iron as well as too much of it can be bad), toxicity, selectivity and so on, and their design is consequently highly non-trivial [<xref ref-type="bibr" rid="B1665">1665</xref>,<xref ref-type="bibr" rid="B1670">1670</xref>]. Nevertheless, iron chelators have demonstrated therapeutic benefits in Alzheimer's [<xref ref-type="bibr" rid="B1674">1674</xref>,<xref ref-type="bibr" rid="B1710">1710</xref>,<xref ref-type="bibr" rid="B1769">1769</xref>-<xref ref-type="bibr" rid="B1771">1771</xref>], Parkinson's [<xref ref-type="bibr" rid="B1037">1037</xref>,<xref ref-type="bibr" rid="B1729">1729</xref>,<xref ref-type="bibr" rid="B1772">1772</xref>], cold-induced brain injury [<xref ref-type="bibr" rid="B1773">1773</xref>,<xref ref-type="bibr" rid="B1774">1774</xref>], coronary disease [<xref ref-type="bibr" rid="B714">714</xref>,<xref ref-type="bibr" rid="B797">797</xref>], renal diseases [<xref ref-type="bibr" rid="B1775">1775</xref>], various kinds of infection [<xref ref-type="bibr" rid="B1763">1763</xref>] and of course in iron overload diseases [<xref ref-type="bibr" rid="B1762">1762</xref>,<xref ref-type="bibr" rid="B1767">1767</xref>].</p><p>As mentioned above, one interesting strategy is to devise chelators that are only activated by oxidative stress [<xref ref-type="bibr" rid="B1760">1760</xref>,<xref ref-type="bibr" rid="B1776">1776</xref>-<xref ref-type="bibr" rid="B1779">1779</xref>]. Another is to seek to combine different kinds of functionality in the same molecule. To this end, Youdim and colleagues in particular have developed a series of multifunctional 8-hydroxyquinoline [<xref ref-type="bibr" rid="B1740">1740</xref>] derivatives that are effective bidentate iron chelators and that seem to show considerable promise in the treatment of a variety of neurodegenerative diseases [<xref ref-type="bibr" rid="B1037">1037</xref>,<xref ref-type="bibr" rid="B1727">1727</xref>-<xref ref-type="bibr" rid="B1729">1729</xref>,<xref ref-type="bibr" rid="B1780">1780</xref>-<xref ref-type="bibr" rid="B1784">1784</xref>] (see also US Patent 20060234927). In this case the antioxidative mechanism is clearly via chelation since such (8-hydroxyquinoline) molecules are poor scavengers of radicals directly [<xref ref-type="bibr" rid="B1785">1785</xref>], a fact that also makes them useful scientific tools. As bidentate ligands they cross both cell membranes and the BBB fairly easily (though lipophilicity <italic>per se </italic>seems not to be important for the biological activity of 8-hydroxyquinoline chelators [<xref ref-type="bibr" rid="B1737">1737</xref>,<xref ref-type="bibr" rid="B1739">1739</xref>]). Importantly, the comparatively weak bidentate binders seem not to have major long-term effects if used carefully [<xref ref-type="bibr" rid="B1483">1483</xref>,<xref ref-type="bibr" rid="B1762">1762</xref>,<xref ref-type="bibr" rid="B1786">1786</xref>,<xref ref-type="bibr" rid="B1787">1787</xref>]</p></sec><sec><title>Interaction of xenobiotics with iron metabolism</title><p>As Cherny and colleagues point out [<xref ref-type="bibr" rid="B1710">1710</xref>], there are many US Pharmacopaeia-registered drugs that, while not being termed chelators, do in fact have both chelating properties and favourable toxicity profiles. Thus we need to recognise potentially both positive and negative interactions between drugs in general and iron metabolism. Any drug that can bind iron can also catalyse the formation of free radicals. Thus, gentamicin can form a gentamicin-iron complex that can lead to toxic symptoms such as hearing loss; this is reversed by iron chelators [<xref ref-type="bibr" rid="B1788">1788</xref>,<xref ref-type="bibr" rid="B1789">1789</xref>]. Existing drugs other than iron chelators may also have effects on iron metabolism [<xref ref-type="bibr" rid="B1790">1790</xref>], and iron can catalyse their oxidation [<xref ref-type="bibr" rid="B1791">1791</xref>]. It is not, of course, news that drugs have multiple effects. In this context, we reiterate that some statins, for instance, have chelating properties [<xref ref-type="bibr" rid="B893">893</xref>].</p><p>Other toxicants might also mediate their damaging effects through iron-catalysed radical formation [<xref ref-type="bibr" rid="B1792">1792</xref>,<xref ref-type="bibr" rid="B1793">1793</xref>]. This in addition to the well-known iron-catalysed, radical-mediated mechanism of toxicity of the viologens such as diquat and paraquat [<xref ref-type="bibr" rid="B1794">1794</xref>-<xref ref-type="bibr" rid="B1799">1799</xref>] (whose herbicidal activity is in fact inhibited by iron chelators [<xref ref-type="bibr" rid="B1800">1800</xref>]) and of adriamycin [<xref ref-type="bibr" rid="B1801">1801</xref>,<xref ref-type="bibr" rid="B1802">1802</xref>]. As mentioned above, the carcinogenic action of asbestos may also be due to the ability of the Fe(n) that it contains to catalyse hydroxyl radical production [<xref ref-type="bibr" rid="B1469">1469</xref>,<xref ref-type="bibr" rid="B1475">1475</xref>], while carcinogenic mycotoxins such as aflatoxin may interact synergistically with iron [<xref ref-type="bibr" rid="B1803">1803</xref>].</p><sec><title>Dietary sources of iron chelators</title><p>There is also a considerable and positive role for nutrients in terms of their chelation of iron. Indeed, polyphenolic compounds, many of which have known health benefits [<xref ref-type="bibr" rid="B1804">1804</xref>-<xref ref-type="bibr" rid="B1813">1813</xref>], are widely used as food antioxidants [<xref ref-type="bibr" rid="B1814">1814</xref>,<xref ref-type="bibr" rid="B1815">1815</xref>]. There is of course considerable epidemiological evidence for the benefits of consuming fruit and vegetables that are likely to contain such antioxidants (e.g. [<xref ref-type="bibr" rid="B1816">1816</xref>-<xref ref-type="bibr" rid="B1819">1819</xref>]), and – although possibly a minimum – this has been popularised as the 'five a day' message (e.g. <ext-link ext-link-type="uri" xlink:href="http://www.fruitsandveggiesmatter.gov/"></ext-link> and <ext-link ext-link-type="uri" xlink:href="http://www.5aday.nhs.uk/"></ext-link>). Even though elements of the 'Mediterranean' diet that are considered to be beneficial are usually assumed to be so on the basis of their antioxidant capabilities (but cf. [<xref ref-type="bibr" rid="B1820">1820</xref>]), many of the polyphenolic compounds (e.g. flavones, isoflavones, stilbenes, flavanones, catechins (flavan-3-ols), chalcones, tannins and anthocyanidins) [<xref ref-type="bibr" rid="B1821">1821</xref>-<xref ref-type="bibr" rid="B1828">1828</xref>] so implicated may also act to chelate iron as well [<xref ref-type="bibr" rid="B1073">1073</xref>,<xref ref-type="bibr" rid="B1829">1829</xref>-<xref ref-type="bibr" rid="B1843">1843</xref>]. This is reasonable given that many of these polyphenols and flavonoid compounds [<xref ref-type="bibr" rid="B1821">1821</xref>,<xref ref-type="bibr" rid="B1844">1844</xref>-<xref ref-type="bibr" rid="B1853">1853</xref>] have groups such as the catechol moiety that are part of the known iron-binding elements of microbial siderophores. Examples include flavones such as quercetin [<xref ref-type="bibr" rid="B914">914</xref>,<xref ref-type="bibr" rid="B1813">1813</xref>,<xref ref-type="bibr" rid="B1829">1829</xref>,<xref ref-type="bibr" rid="B1854">1854</xref>-<xref ref-type="bibr" rid="B1864">1864</xref>], rutin [<xref ref-type="bibr" rid="B1829">1829</xref>,<xref ref-type="bibr" rid="B1857">1857</xref>,<xref ref-type="bibr" rid="B1858">1858</xref>,<xref ref-type="bibr" rid="B1865">1865</xref>,<xref ref-type="bibr" rid="B1866">1866</xref>], baicalin [<xref ref-type="bibr" rid="B1860">1860</xref>,<xref ref-type="bibr" rid="B1867">1867</xref>], curcumin [<xref ref-type="bibr" rid="B1813">1813</xref>,<xref ref-type="bibr" rid="B1868">1868</xref>-<xref ref-type="bibr" rid="B1872">1872</xref>], kolaviron [<xref ref-type="bibr" rid="B1873">1873</xref>], flavonol [<xref ref-type="bibr" rid="B1874">1874</xref>], floranol [<xref ref-type="bibr" rid="B1875">1875</xref>], xanthones such as mangiferin [<xref ref-type="bibr" rid="B1876">1876</xref>-<xref ref-type="bibr" rid="B1879">1879</xref>], morin [<xref ref-type="bibr" rid="B1876">1876</xref>], catechins [<xref ref-type="bibr" rid="B1073">1073</xref>,<xref ref-type="bibr" rid="B1807">1807</xref>,<xref ref-type="bibr" rid="B1838">1838</xref>,<xref ref-type="bibr" rid="B1854">1854</xref>,<xref ref-type="bibr" rid="B1880">1880</xref>,<xref ref-type="bibr" rid="B1881">1881</xref>] and theaflavins [<xref ref-type="bibr" rid="B1882">1882</xref>], as well as procyanidins [<xref ref-type="bibr" rid="B1835">1835</xref>,<xref ref-type="bibr" rid="B1883">1883</xref>] and melatonin [<xref ref-type="bibr" rid="B1628">1628</xref>,<xref ref-type="bibr" rid="B1884">1884</xref>-<xref ref-type="bibr" rid="B1887">1887</xref>]. However, the celebrated (<italic>trans</italic>-)-resveratrol molecule [<xref ref-type="bibr" rid="B1888">1888</xref>-<xref ref-type="bibr" rid="B1902">1902</xref>] may act mainly via other pathways.</p><p>A considerable number of studies with <underline>non-purified</underline> dietary constituents containing the above polyphenolic components have also shown promise in inhibiting diseases in which oxidative stress is implicated [<xref ref-type="bibr" rid="B1825">1825</xref>,<xref ref-type="bibr" rid="B1903">1903</xref>-<xref ref-type="bibr" rid="B1906">1906</xref>]. For instance in stroke and related neuronal aging and stress conditions, preventative activity can be found in blueberries [<xref ref-type="bibr" rid="B1907">1907</xref>-<xref ref-type="bibr" rid="B1913">1913</xref>] (and see [<xref ref-type="bibr" rid="B1914">1914</xref>]), <italic>Ginkgo biloba </italic>extract (EGb 761) [<xref ref-type="bibr" rid="B1910">1910</xref>,<xref ref-type="bibr" rid="B1915">1915</xref>,<xref ref-type="bibr" rid="B1916">1916</xref>], grapes [<xref ref-type="bibr" rid="B1917">1917</xref>], green tea [<xref ref-type="bibr" rid="B1807">1807</xref>,<xref ref-type="bibr" rid="B1918">1918</xref>-<xref ref-type="bibr" rid="B1921">1921</xref>], <italic>Mangifera indica </italic>extract [<xref ref-type="bibr" rid="B1879">1879</xref>], strawberries [<xref ref-type="bibr" rid="B1907">1907</xref>], spinach [<xref ref-type="bibr" rid="B1907">1907</xref>] and <italic>Crataegus </italic>[<xref ref-type="bibr" rid="B922">922</xref>], while combinations of some these components ('protandim') have been claimed to reduce ROS levels by stimulating the production of catalase and SOD [<xref ref-type="bibr" rid="B1922">1922</xref>]. As with pharmaceutical drugs [<xref ref-type="bibr" rid="B18">18</xref>,<xref ref-type="bibr" rid="B1923">1923</xref>-<xref ref-type="bibr" rid="B1925">1925</xref>], there are significant problems with bioavailability [<xref ref-type="bibr" rid="B1926">1926</xref>,<xref ref-type="bibr" rid="B1927">1927</xref>], although the necessary measurements are starting to come forward [<xref ref-type="bibr" rid="B1804">1804</xref>,<xref ref-type="bibr" rid="B1809">1809</xref>,<xref ref-type="bibr" rid="B1926">1926</xref>-<xref ref-type="bibr" rid="B1932">1932</xref>]. There is now increasing evidence for the mechanisms with which these dietary components and related natural products and derivatives (often with anti-inflammatory, anti-mutagenic or anti-carcinogenic properties) interact with well recognised cellular signalling pathways (e.g. [<xref ref-type="bibr" rid="B1402">1402</xref>,<xref ref-type="bibr" rid="B1935">1935</xref>,<xref ref-type="bibr" rid="B1895">1895</xref>,<xref ref-type="bibr" rid="B1896">1896</xref>,<xref ref-type="bibr" rid="B1410">1410</xref>,<xref ref-type="bibr" rid="B1413">1413</xref>,<xref ref-type="bibr" rid="B1913">1913</xref>,<xref ref-type="bibr" rid="B1900">1900</xref>,<xref ref-type="bibr" rid="B1933">1933</xref>-<xref ref-type="bibr" rid="B1990">1990</xref>]).</p></sec></sec><sec><title>Role of iron-generated ROSs in cellular signalling and oxidative stress</title><p>Thus, although this is not the focus of the present more physiologically based review, we recognise that many of relationships between ROSs and oxidative stress and overt progressive diseases may be mediated via the inflammatory signalling pathways involved in 'innate immunity' [<xref ref-type="bibr" rid="B900">900</xref>,<xref ref-type="bibr" rid="B1991">1991</xref>-<xref ref-type="bibr" rid="B1993">1993</xref>]. NF-κB is an important transcription factor, and the NF-κB system is intimately involved in this signalling [<xref ref-type="bibr" rid="B588">588</xref>,<xref ref-type="bibr" rid="B672">672</xref>,<xref ref-type="bibr" rid="B719">719</xref>,<xref ref-type="bibr" rid="B1408">1408</xref>,<xref ref-type="bibr" rid="B1409">1409</xref>,<xref ref-type="bibr" rid="B1454">1454</xref>,<xref ref-type="bibr" rid="B1994">1994</xref>-<xref ref-type="bibr" rid="B2019">2019</xref>].</p><p>In the NF-κB system (e.g. [<xref ref-type="bibr" rid="B2020">2020</xref>-<xref ref-type="bibr" rid="B2024">2024</xref>]) (Fig <xref ref-type="fig" rid="F8">8</xref>), NF-κB is normally held inactive in the cytoplasm by binding to an inhibitor IκB (often IκBα). Pro-inflammatory cytokines such as TNF-α, LPS [<xref ref-type="bibr" rid="B2025">2025</xref>-<xref ref-type="bibr" rid="B2030">2030</xref>] and IL-1 [<xref ref-type="bibr" rid="B2031">2031</xref>] act by binding to receptors at the cell surface and initiating signalling pathways that lead to the activation of a particular kinase, IκB kinase or IKK. This kinase phosphorylates the IκB causing it to be released (and ubiquitinated and degraded by the proteasome), allowing the NF-κB to be translocated to the nucleus where it can activate as many as 300 genes. Simple models of the NF-κB system show the main control elements [<xref ref-type="bibr" rid="B2032">2032</xref>,<xref ref-type="bibr" rid="B2033">2033</xref>] and their synergistic interaction [<xref ref-type="bibr" rid="B2034">2034</xref>]. The NF-κB system is implicated in apoptosis [<xref ref-type="bibr" rid="B2035">2035</xref>,<xref ref-type="bibr" rid="B2036">2036</xref>], aging [<xref ref-type="bibr" rid="B1199">1199</xref>], and in diseases such as cancer [<xref ref-type="bibr" rid="B1405">1405</xref>,<xref ref-type="bibr" rid="B1444">1444</xref>,<xref ref-type="bibr" rid="B1454">1454</xref>,<xref ref-type="bibr" rid="B1808">1808</xref>,<xref ref-type="bibr" rid="B2037">2037</xref>-<xref ref-type="bibr" rid="B2040">2040</xref>], arthritis [<xref ref-type="bibr" rid="B2040">2040</xref>-<xref ref-type="bibr" rid="B2043">2043</xref>] and a variety of other diseases [<xref ref-type="bibr" rid="B2044">2044</xref>]. Antioxidants such as vitamin E [<xref ref-type="bibr" rid="B552">552</xref>,<xref ref-type="bibr" rid="B2017">2017</xref>] and melatonin [<xref ref-type="bibr" rid="B2045">2045</xref>-<xref ref-type="bibr" rid="B2049">2049</xref>] are at least partially protective. Oxidative stress seems to act upstream of IKK [<xref ref-type="bibr" rid="B2014">2014</xref>], on IκBα directly [<xref ref-type="bibr" rid="B2050">2050</xref>] and in the p38 MAP kinase pathway [<xref ref-type="bibr" rid="B1993">1993</xref>,<xref ref-type="bibr" rid="B2014">2014</xref>,<xref ref-type="bibr" rid="B2051">2051</xref>], and there is also evidence that at least some of the statins act on the PI3K-akt and NF-κB pathways too [<xref ref-type="bibr" rid="B819">819</xref>,<xref ref-type="bibr" rid="B883">883</xref>,<xref ref-type="bibr" rid="B2052">2052</xref>-<xref ref-type="bibr" rid="B2060">2060</xref>]. A considerable number of inhibitors of the NF-κB system exist [<xref ref-type="bibr" rid="B2055">2055</xref>], many exhibiting cross-reactivity [<xref ref-type="bibr" rid="B1734">1734</xref>].</p><fig position="float" id="F8"><label>Figure 8</label><caption><p><bold>An overview of cellular signaling using the NF-κB and p38 systems</bold>. Note that some of the extracellular effectors that mediate NF-κB activation are themselves produced and secreted as a result of the activation, potentially creating an autocatalytic system.</p></caption><graphic xlink:href="1755-8794-2-2-8"></graphic></fig><p>The induction of NF-κB by ROSs appears to involve a coupling via the glutathione system [<xref ref-type="bibr" rid="B2007">2007</xref>,<xref ref-type="bibr" rid="B2035">2035</xref>,<xref ref-type="bibr" rid="B2036">2036</xref>,<xref ref-type="bibr" rid="B2061">2061</xref>-<xref ref-type="bibr" rid="B2078">2078</xref>] (and see also [<xref ref-type="bibr" rid="B2079">2079</xref>,<xref ref-type="bibr" rid="B2080">2080</xref>]).</p><p>A variety of studies have shown that iron is involved in these signalling processes [<xref ref-type="bibr" rid="B1839">1839</xref>,<xref ref-type="bibr" rid="B1996">1996</xref>,<xref ref-type="bibr" rid="B2015">2015</xref>,<xref ref-type="bibr" rid="B2081">2081</xref>-<xref ref-type="bibr" rid="B2085">2085</xref>], probably again acting upstream of the IKK [<xref ref-type="bibr" rid="B557">557</xref>,<xref ref-type="bibr" rid="B2083">2083</xref>,<xref ref-type="bibr" rid="B2086">2086</xref>,<xref ref-type="bibr" rid="B2087">2087</xref>].</p><p>Interestingly, there is interplay between the NF-κB pathway and the regulation of NGAL [<xref ref-type="bibr" rid="B404">404</xref>,<xref ref-type="bibr" rid="B405">405</xref>,<xref ref-type="bibr" rid="B2088">2088</xref>,<xref ref-type="bibr" rid="B2089">2089</xref>], ferritin [<xref ref-type="bibr" rid="B2030">2030</xref>] and hepcidin [<xref ref-type="bibr" rid="B2090">2090</xref>], presumably acting as a negative feedback as the cell tries to control and ligand its free Fe(n) in the face of oxidative stress caused by the release of free iron [<xref ref-type="bibr" rid="B2091">2091</xref>].</p></sec><sec><title>The systems biology of ROS generation and activity</title><p>It is not news that most major changes in physiological states have multigenic or multifactorial origins (e.g. [<xref ref-type="bibr" rid="B2092">2092</xref>,<xref ref-type="bibr" rid="B2093">2093</xref>]). This means, as an inevitable consequence, that we need to recognize that their observation requires a systems approach, and that most diseases are therefore in fact to be seen as systems or network diseases [<xref ref-type="bibr" rid="B631">631</xref>,<xref ref-type="bibr" rid="B2094">2094</xref>-<xref ref-type="bibr" rid="B2102">2102</xref>]. Changes in individual reaction steps (or even single manipulations) can change the levels of scores or hundreds of transcripts [<xref ref-type="bibr" rid="B2103">2103</xref>], proteins [<xref ref-type="bibr" rid="B2104">2104</xref>] or metabolites [<xref ref-type="bibr" rid="B725">725</xref>]. In this regard, small molecule (metabolomics) measurements have especial advantages for capturing network organisation, including on theoretical grounds [<xref ref-type="bibr" rid="B2105">2105</xref>-<xref ref-type="bibr" rid="B2112">2112</xref>].</p><p>If we consider just one variable of present relevance, the quantity of hydroxyl radical, the amount that is able to react with proteins, lipids and DNA is clearly determined by a huge number of reactions, whether directly or otherwise – not only the concentrations of reagents and enzyme that directly catalyse its formation and destruction but by everything else that affects <underline>their</underline> concentration and activity, and so on. This is of course well established in biology in the formalism of metabolic control analysis (MCA) (see e.g. [<xref ref-type="bibr" rid="B2113">2113</xref>-<xref ref-type="bibr" rid="B2120">2120</xref>]), and was recognized over 30 years ago in Morris' prescient review on anaerobes [<xref ref-type="bibr" rid="B2121">2121</xref>]. Modern systems theories of aging (e.g. [<xref ref-type="bibr" rid="B1175">1175</xref>,<xref ref-type="bibr" rid="B1180">1180</xref>,<xref ref-type="bibr" rid="B2120">2120</xref>,<xref ref-type="bibr" rid="B2122">2122</xref>] and above) (Fig <xref ref-type="fig" rid="F9">9</xref>) also recognize physiological progression as being determined in terms of a balance between 'good' and 'bad' factors. MCA and related formalisms can be seen as theories of sensitivity analysis, which in many cases can be normalized such that an overall output function can be described <underline>quantitatively</underline> in terms of the relative contributions of each of its component steps (e.g. [<xref ref-type="bibr" rid="B2123">2123</xref>-<xref ref-type="bibr" rid="B2127">2127</xref>]). In MCA the normalized local sensitivities are known as control coefficients, and the sum of the concentration-control coefficients = 0, in other words in the steady state the rate of production and consumption of a particular entity is in balance and <underline>all</underline> reactions can contribute to it to some degree. The concentration-control coefficient describes this degree quantitatively. It is now possible to produce appropriate quantitative representations of metabolic networks using quite sparse kinds of information (in fact just the stoichiometry and network structure [<xref ref-type="bibr" rid="B2128">2128</xref>]), and thereby provide initial estimates for more sophisticated fitting algorithms (e.g. [<xref ref-type="bibr" rid="B2129">2129</xref>-<xref ref-type="bibr" rid="B2132">2132</xref>]. Indeed, the analysis of the properties and behaviour of networks is at the core of modern systems biology (e.g. [<xref ref-type="bibr" rid="B2095">2095</xref>,<xref ref-type="bibr" rid="B2133">2133</xref>-<xref ref-type="bibr" rid="B2140">2140</xref>]).</p><fig position="float" id="F9"><label>Figure 9</label><caption><p><bold>General view of the role of iron, antioxidants and ROSs in aging and degenerative processes</bold>. Some of the decay may be ameliorated by lifestyle and dietary means. Based in part on [<xref ref-type="bibr" rid="B1175">1175</xref>].</p></caption><graphic xlink:href="1755-8794-2-2-9"></graphic></fig><p>A corollary of such considerations is that to decrease the amount of damage caused by OH<sup>• </sup>(or any other) radicals we need both to decrease their production and increase their removal to harmless substances [<xref ref-type="bibr" rid="B2141">2141</xref>], and that on general grounds [<xref ref-type="bibr" rid="B1706">1706</xref>-<xref ref-type="bibr" rid="B1708">1708</xref>,<xref ref-type="bibr" rid="B2142">2142</xref>] such a strategy (for instance of combining a cell-permeable iron chelator with a cell-permeable antioxidant) might be expected to give a synergistic response. Even determining the means of cell permeability and tissue distribution turns out to be a systems biology problem in which we need to know the nature and activity of all the carriers that are involved [<xref ref-type="bibr" rid="B18">18</xref>,<xref ref-type="bibr" rid="B1703">1703</xref>,<xref ref-type="bibr" rid="B1714">1714</xref>,<xref ref-type="bibr" rid="B2143">2143</xref>]. At all events, it is undoubtedly the case that the steady-state rate of production of a molecule such as the hydroxyl radical is controlled or affected by a considerable number of steps. These minimally include the multiple reactions of the mitochondrial respiratory chain and the various oxidases producing superoxide and peroxide, the activities of catalase and SOD enzymes that together can remove them, protective reactions such as heat-shock proteins, and most pertinently to the present review a large number of reactions involved in the metabolism and safe liganding of iron that help determine the rate at which OH<sup>• </sup>is produced.</p><p>It is also pertinent to enquire as to why we are now seeing so many of these progressive diseases, and as to what may be their causes. Undoubtedly the simple fact of improved longevity is one [<xref ref-type="bibr" rid="B165">165</xref>] as damage accumulates. However, we note that anything that decreases the amount of unliganded iron, such as decreasing the total dietary iron intake e.g. from red meat, must be helpful [<xref ref-type="bibr" rid="B1156">1156</xref>,<xref ref-type="bibr" rid="B2144">2144</xref>].</p><sec><title>Anti-inflammatory cytokines; the example of erythropoietin</title><p>We have above adduced considerable evidence that decreasing the amount of hydroxyl radical by any means is valuable, whether by removing initially generated ROSs such as superoxide and peroxide or by chelating poorly liganded iron in a way that stops these ROSs forming the hydroxyl radical. While pro-inflammatory cytokines can themselves increase ROS production and modulate the activities of signaling pathways such as NF-κB and p38, there are also anti-inflammatory cytokines. A particularly interesting example is that of erythropoietin (also discussed above as being protective in a number of iron-mediated diseases).</p><p>Erythropoietin was originally recognized via its role in erythropoiesis [<xref ref-type="bibr" rid="B2145">2145</xref>-<xref ref-type="bibr" rid="B2147">2147</xref>] (hence its name, of course), but it has become evident that it has many other roles, and in particular it is observed phenomenologically that erythropoietin (and non-erthyropoetic derivatives) is protective in a number of inflammatory conditions that accompany many diseases such as those listed above [<xref ref-type="bibr" rid="B940">940</xref>,<xref ref-type="bibr" rid="B942">942</xref>,<xref ref-type="bibr" rid="B2148">2148</xref>-<xref ref-type="bibr" rid="B2155">2155</xref>]. These included cardiovascular disease [<xref ref-type="bibr" rid="B721">721</xref>,<xref ref-type="bibr" rid="B722">722</xref>,<xref ref-type="bibr" rid="B2156">2156</xref>-<xref ref-type="bibr" rid="B2175">2175</xref>], stroke and other related neurological diseases [<xref ref-type="bibr" rid="B924">924</xref>-<xref ref-type="bibr" rid="B926">926</xref>,<xref ref-type="bibr" rid="B928">928</xref>,<xref ref-type="bibr" rid="B929">929</xref>,<xref ref-type="bibr" rid="B933">933</xref>,<xref ref-type="bibr" rid="B937">937</xref>,<xref ref-type="bibr" rid="B938">938</xref>,<xref ref-type="bibr" rid="B2155">2155</xref>,<xref ref-type="bibr" rid="B2176">2176</xref>-<xref ref-type="bibr" rid="B2204">2204</xref>], diabetic neuropathy [<xref ref-type="bibr" rid="B2205">2205</xref>], kidney injury [<xref ref-type="bibr" rid="B2173">2173</xref>,<xref ref-type="bibr" rid="B2206">2206</xref>-<xref ref-type="bibr" rid="B2212">2212</xref>], intestinal injury [<xref ref-type="bibr" rid="B2213">2213</xref>] and shock (both septic and non-septic) [<xref ref-type="bibr" rid="B1596">1596</xref>,<xref ref-type="bibr" rid="B1597">1597</xref>,<xref ref-type="bibr" rid="B2214">2214</xref>].</p><p>The question then arises as to how it is doing this mechanistically, and the proximate answer is that it (and other anti-inflammatory agents, e.g. [<xref ref-type="bibr" rid="B1808">1808</xref>,<xref ref-type="bibr" rid="B2215">2215</xref>,<xref ref-type="bibr" rid="B2216">2216</xref>]) seem to act via many of the same signalling pathways as do inflammatory agents [<xref ref-type="bibr" rid="B943">943</xref>,<xref ref-type="bibr" rid="B2150">2150</xref>,<xref ref-type="bibr" rid="B2217">2217</xref>-<xref ref-type="bibr" rid="B2226">2226</xref>]. There is evidence that it can help maintain superoxide dismutase activity [<xref ref-type="bibr" rid="B2214">2214</xref>,<xref ref-type="bibr" rid="B2227">2227</xref>], invoke haem oxygenase [<xref ref-type="bibr" rid="B2228">2228</xref>], and in particular – from the perspective of this review – that it may remove poorly liganded iron [<xref ref-type="bibr" rid="B2229">2229</xref>] and interact with hydroxyl radical directly [<xref ref-type="bibr" rid="B2230">2230</xref>-<xref ref-type="bibr" rid="B2233">2233</xref>].</p><p>It is notable that appropriate levels of erythropoietin appear not only to be efficacious but to be safe, even in pregnancy [<xref ref-type="bibr" rid="B2234">2234</xref>-<xref ref-type="bibr" rid="B2241">2241</xref>]. Erythropoietin may itself be a marker of hypoxia and oxidative stress in pregnancy [<xref ref-type="bibr" rid="B531">531</xref>,<xref ref-type="bibr" rid="B2242">2242</xref>-<xref ref-type="bibr" rid="B2245">2245</xref>], consistent with a view that the body is attempting to deal with these problems by creating anti-inflammatory cytokines.</p></sec></sec><sec><title>Hypoxia-inducible factor (HIF)</title><p>Although I am mainly not concentrating on genetic regulatory aspects in this review, the HIF [<xref ref-type="bibr" rid="B2246">2246</xref>,<xref ref-type="bibr" rid="B2247">2247</xref>] does deserve some mention, since many of the syndromes described above are accompanied by hypoxia, and this causes levels of the HIF to increase. HIF is a transcription factor that can activate a considerable number of genes, including VEGF [<xref ref-type="bibr" rid="B1951">1951</xref>,<xref ref-type="bibr" rid="B2246">2246</xref>-<xref ref-type="bibr" rid="B2250">2250</xref>]. In contrast to the constitutive expression of HIF-1α, HIF-1β protein levels are regulated in response to the cellular oxygen concentration [<xref ref-type="bibr" rid="B2251">2251</xref>]. The active HIF is the HIF-1αβ heterodimer [<xref ref-type="bibr" rid="B2252">2252</xref>]. HIF couples anoxia to innate immunity via the NF-κB system [<xref ref-type="bibr" rid="B2253">2253</xref>]. In particular, HIF effects (via hepcidin) the mobilisation or iron and can cause the expression of inflammatory cytokines such as IL-1, IL-6 and TNF-α [<xref ref-type="bibr" rid="B2254">2254</xref>-<xref ref-type="bibr" rid="B2256">2256</xref>] under conditions (hypoxia) where superoxide and peroxide production are likely to be increased, and consequently increases sepsis (in that HIF-knockout mice are resistant to LPS-induced sepsis [<xref ref-type="bibr" rid="B2254">2254</xref>,<xref ref-type="bibr" rid="B2255">2255</xref>]). By contrast, induction of HIF (and the genes that it activates) can effect neuroprotection [<xref ref-type="bibr" rid="B2252">2252</xref>,<xref ref-type="bibr" rid="B2257">2257</xref>]. HIF also appears to have a significant role in placental development, and defective HIF expression may be involved in pre-eclampsia and intra-uterine growth retardation [<xref ref-type="bibr" rid="B435">435</xref>,<xref ref-type="bibr" rid="B2246">2246</xref>,<xref ref-type="bibr" rid="B2258">2258</xref>]. Qutub and colleagues provide useful models [<xref ref-type="bibr" rid="B2259">2259</xref>,<xref ref-type="bibr" rid="B2260">2260</xref>] of HIF activation under a variety of conditions of iron, O<sub>2</sub>, 2-oxoglutarate and other factors.</p><sec><title>Autocatalysis, positive feedback and Systems Biology</title><p>What has emerged in recent years is a recognition that the structure (i.e. topology) of the modules of metabolic and signalling networks, somewhat independent of the individual activities of their components, can have a profound controlling influence on their behaviour (e.g. [<xref ref-type="bibr" rid="B2107">2107</xref>,<xref ref-type="bibr" rid="B2134">2134</xref>,<xref ref-type="bibr" rid="B2135">2135</xref>,<xref ref-type="bibr" rid="B2261">2261</xref>,<xref ref-type="bibr" rid="B2262">2262</xref>]). Classically, negative feedback structures are considered to confer stability, while positive feedbacks tend to have the opposite effect. However, negative feedbacks with delay loops can cause oscillations [<xref ref-type="bibr" rid="B2022">2022</xref>,<xref ref-type="bibr" rid="B2109">2109</xref>] while some kinds of positive feedback loops can confer stability [<xref ref-type="bibr" rid="B2262">2262</xref>,<xref ref-type="bibr" rid="B2263">2263</xref>]. However, there is no doubt that structures in which a damaging agent causes the production of a second damaging agent that itself catalyses the production of the first or a separate damaging agent can exhibit a runaway kind of damage. This is <underline>exactly</underline> what can happen with iron and superoxide since Fe(n) can be liberated from ferritin by superoxide radicals and then catalyse the production of further hydroxyl radical by increasing the amount of free iron (Fig <xref ref-type="fig" rid="F6">6</xref>). A similar effect can occur with Fe-S proteins in SOD-deficiency [<xref ref-type="bibr" rid="B1148">1148</xref>], with the degradation of mitochondria by radical damage leading to further production of radicals [<xref ref-type="bibr" rid="B28">28</xref>,<xref ref-type="bibr" rid="B30">30</xref>,<xref ref-type="bibr" rid="B2264">2264</xref>], and the effects of oxidative stress on iron storage [<xref ref-type="bibr" rid="B2265">2265</xref>]. This again illustrates the importance of acting at multiple points in a network to control these kinds of damage. Exactly the same is true of the IL-1 and TNF-α systems in which IL-1 or TNF-α (oxidative stress) acting on one cell can effect the secretion of further IL-1/TNF-α that can act on adjacent cells (Fig <xref ref-type="fig" rid="F8">8</xref>), of the hypoxia-dependent increase in both ROSs and serum iron mediated by hepcidin (Fig <xref ref-type="fig" rid="F3">3</xref>), the autocatalytic synergy between overfeeding, inflammation and (pre-)diabetes, and of the peroxide/iron pair that are liberated when frataxin is deficient (see above). It is these kinds of synergistic effects and <underline>autocatalytic cycles</underline> that are the hallmark of the major and progressive effects on human physiology that are seen in these kinds of system. Indeed, one might comment that such multi-site and autocatalytic effects are required to overwhelm normal defences precisely because human metabolic and signalling systems are 'robust' systems that have evolved topologies that are resistant or robust to parameter changes (see e.g. [<xref ref-type="bibr" rid="B2266">2266</xref>-<xref ref-type="bibr" rid="B2291">2291</xref>]).</p></sec></sec><sec><title>Predictive biology</title><p>It is often considered (e.g. [<xref ref-type="bibr" rid="B2292">2292</xref>,<xref ref-type="bibr" rid="B2293">2293</xref>]) that a desirable feature of a scientific idea is its ability to make useful predictions, and while this is not in fact a particularly well founded philosophical principle, it probably is of value to set out a couple of 'predictions' that follow from the present analysis. One prominent feature of the above is the primacy of the iron-catalysed production of the damaging hydroxyl radical, and thus a test of the involvement of these kinds of reactions in the various physiological and pathological states to which we allude is the prediction that they should be accompanied by markers of oxidative stress characteristic of reactions of endogenous metabolites with the hydroxyl radical. While it is not that easy to disentangle the complex reactions of ROSs with biomolecules [<xref ref-type="bibr" rid="B43">43</xref>,<xref ref-type="bibr" rid="B1055">1055</xref>], at least the following appear to be a result of reactions involving OH<sup>• </sup>[<xref ref-type="bibr" rid="B2294">2294</xref>,<xref ref-type="bibr" rid="B2295">2295</xref>]: 8-oxo-2'-deoxyguanosine (oxo<sup>8</sup>dG) [<xref ref-type="bibr" rid="B98">98</xref>,<xref ref-type="bibr" rid="B2296">2296</xref>,<xref ref-type="bibr" rid="B2297">2297</xref>], 8-oxo-7,8- dihydro-2'-deoxyguanosine [<xref ref-type="bibr" rid="B90">90</xref>,<xref ref-type="bibr" rid="B92">92</xref>] and thymine glycol [<xref ref-type="bibr" rid="B92">92</xref>,<xref ref-type="bibr" rid="B2294">2294</xref>].</p><p>Another set of predictions from the systems biology perspective [<xref ref-type="bibr" rid="B1704">1704</xref>-<xref ref-type="bibr" rid="B1708">1708</xref>,<xref ref-type="bibr" rid="B1731">1731</xref>,<xref ref-type="bibr" rid="B2138">2138</xref>,<xref ref-type="bibr" rid="B2291">2291</xref>,<xref ref-type="bibr" rid="B2298">2298</xref>-<xref ref-type="bibr" rid="B2310">2310</xref>] is that combinations of chemical agents (or manipulations such as those of transcription factors that affect multiple steps in a pathway [<xref ref-type="bibr" rid="B1906">1906</xref>] or modulation of multiple gene products [<xref ref-type="bibr" rid="B2311">2311</xref>], or both [<xref ref-type="bibr" rid="B2312">2312</xref>,<xref ref-type="bibr" rid="B2313">2313</xref>]) will be far more efficacious, for instance in modulating iron-catalysed oxidative stress and its sequelae, than will be the use of 'magic bullet' single agents. Such combinations of 'causes' do not have to be guessed <italic>a priori </italic>but can be obtained via inferencing techniques (e.g. [<xref ref-type="bibr" rid="B2314">2314</xref>-<xref ref-type="bibr" rid="B2320">2320</xref>]) – for a recent example see [<xref ref-type="bibr" rid="B2321">2321</xref>]. The nonlinear behaviour of biochemical networks also serves to explain the bell-shaped dose-response curves underpinning the hormesis [<xref ref-type="bibr" rid="B2322">2322</xref>-<xref ref-type="bibr" rid="B2326">2326</xref>] often observed.</p><p>Iron-mediated oxidative stress is arguably the cause of much of the inflammation typically observed in biological systems, often further mediated via pro-inflammatory cytokines. Another major prediction that comes from the above then is that molecules that are anti-inflammatory, whether widely recognised as such or not, should have beneficial effects in syndromes for which they have not necessarily been tested. An obvious set of candidates in this regard are to be found among the statins, since it is now clear that they have important anti-inflammatory properties (see above). Thus, there are already indications that as well as their established benefits in cardiovascular disease (e.g. [<xref ref-type="bibr" rid="B804">804</xref>,<xref ref-type="bibr" rid="B2327">2327</xref>]) they may exert benefit in a huge variety of syndromes [<xref ref-type="bibr" rid="B838">838</xref>], including sepsis [<xref ref-type="bibr" rid="B839">839</xref>,<xref ref-type="bibr" rid="B2060">2060</xref>,<xref ref-type="bibr" rid="B2328">2328</xref>-<xref ref-type="bibr" rid="B2340">2340</xref>], heart failure [<xref ref-type="bibr" rid="B2341">2341</xref>], pain perception [<xref ref-type="bibr" rid="B2342">2342</xref>], lupus and related diseases [<xref ref-type="bibr" rid="B1293">1293</xref>,<xref ref-type="bibr" rid="B2343">2343</xref>], diabetes [<xref ref-type="bibr" rid="B877">877</xref>,<xref ref-type="bibr" rid="B2344">2344</xref>], rheumatoid arthritis [<xref ref-type="bibr" rid="B866">866</xref>,<xref ref-type="bibr" rid="B869">869</xref>,<xref ref-type="bibr" rid="B890">890</xref>,<xref ref-type="bibr" rid="B2345">2345</xref>-<xref ref-type="bibr" rid="B2350">2350</xref>], kidney disease [<xref ref-type="bibr" rid="B2351">2351</xref>-<xref ref-type="bibr" rid="B2353">2353</xref>], inflammatory skin disease [<xref ref-type="bibr" rid="B2354">2354</xref>], emphysema [<xref ref-type="bibr" rid="B2355">2355</xref>], ischaemia-reperfusion injury [<xref ref-type="bibr" rid="B2356">2356</xref>], stroke [<xref ref-type="bibr" rid="B864">864</xref>,<xref ref-type="bibr" rid="B872">872</xref>,<xref ref-type="bibr" rid="B2357">2357</xref>-<xref ref-type="bibr" rid="B2364">2364</xref>], traumatic brain injury [<xref ref-type="bibr" rid="B2365">2365</xref>-<xref ref-type="bibr" rid="B2367">2367</xref>], neurodegenerative diseases [<xref ref-type="bibr" rid="B860">860</xref>-<xref ref-type="bibr" rid="B862">862</xref>,<xref ref-type="bibr" rid="B920">920</xref>,<xref ref-type="bibr" rid="B1294">1294</xref>,<xref ref-type="bibr" rid="B2059">2059</xref>,<xref ref-type="bibr" rid="B2368">2368</xref>-<xref ref-type="bibr" rid="B2384">2384</xref>], neurotoxicity [<xref ref-type="bibr" rid="B2385">2385</xref>] and cancer [<xref ref-type="bibr" rid="B2386">2386</xref>-<xref ref-type="bibr" rid="B2400">2400</xref>].</p></sec><sec><title>Concluding remarks and quo vadis</title><p>"Actually, the orgy of fact extraction in which everybody is currently engaged has, like most consumer economies, accumulated a vast debt. This is a debt of theory and some of us are soon going to have an exciting time paying it back – with interest, I hope." [<xref ref-type="bibr" rid="B2401">2401</xref>].</p><p>"But one thing is certain: to understand the whole you must look at the whole" [<xref ref-type="bibr" rid="B2402">2402</xref>]</p><p>"If you are not thinking about your experiments on a whole-genome level you are going to be a dinosaur". J. Stamatoyannopoulos, quoted in [<xref ref-type="bibr" rid="B2403">2403</xref>].</p><p>While it is less common for scientists to publish 'negative' results ('there was no effect of some agent on some process'), and there has been a tendency to seek to falsify specific hypotheses rather than to paint a big picture [<xref ref-type="bibr" rid="B2404">2404</xref>], there is no doubt that the sheer weight of positive evidence can be persuasive in leading one to a view. As Bertrand Russell put it [<xref ref-type="bibr" rid="B2405">2405</xref>], "When one admits that nothing is certain one must, I think, also admit that some things are much more nearly certain than others." However, as mentioned above, the huge volume of scientific activity has in many ways led to a 'balkanisation' of the literature [<xref ref-type="bibr" rid="B2406">2406</xref>] in which scientists deal with the problem of the deluge of published papers by necessarily ignoring most of them. This is no longer realistic (nor necessary) in an age of post-genomics, the internet, Web 2.0 and systems biology, and when we are starting to move to integrative (if distributed) models of organisms (including humans) at a whole organ, genome or whole organism scale [<xref ref-type="bibr" rid="B118">118</xref>,<xref ref-type="bibr" rid="B2135">2135</xref>,<xref ref-type="bibr" rid="B2407">2407</xref>-<xref ref-type="bibr" rid="B2416">2416</xref>]. The 'digital human' is thus an important research goal [<xref ref-type="bibr" rid="B2410">2410</xref>,<xref ref-type="bibr" rid="B2415">2415</xref>-<xref ref-type="bibr" rid="B2417">2417</xref>]. Expression profiling atlases are becoming increasingly widespread (e.g. [<xref ref-type="bibr" rid="B2418">2418</xref>-<xref ref-type="bibr" rid="B2423">2423</xref>]), and one can anticipate using these straightforwardly to extend these 'generalised' (sub)cellular network models in a tissue-specific manner [<xref ref-type="bibr" rid="B2424">2424</xref>]. With the ability to exchange models of biochemical networks in a principled way [<xref ref-type="bibr" rid="B2425">2425</xref>-<xref ref-type="bibr" rid="B2428">2428</xref>], when they are marked up appropriately (e.g. [<xref ref-type="bibr" rid="B3">3</xref>,<xref ref-type="bibr" rid="B4">4</xref>]), we can expect to begin to reason about them automatically [<xref ref-type="bibr" rid="B118">118</xref>,<xref ref-type="bibr" rid="B2429">2429</xref>], such that we may soon look forward to an era in which we can recognise the commonalities across a variety of different subfields – a specific message of the present overview. Thus, while iron and metabolism should be considered in the context of other processes that may be contributing to the disorders discussed, and it is evident that they are intimately involved in many disease processes, therapies derived for one of the inflammatory diseases listed above may well have benefit in some of the others where their underlying 'causes' are the same. The 'mass collaboration' agenda (e.g. [<xref ref-type="bibr" rid="B2430">2430</xref>-<xref ref-type="bibr" rid="B2435">2435</xref>]), in which dispersed agents contribute their different skills to the solution of a complex problem, may well help this happen effectively. Developments in distributed workflow technology, such as the Taverna [<xref ref-type="bibr" rid="B22">22</xref>-<xref ref-type="bibr" rid="B26">26</xref>,<xref ref-type="bibr" rid="B2436">2436</xref>,<xref ref-type="bibr" rid="B2437">2437</xref>]<ext-link ext-link-type="uri" xlink:href="http://taverna.sourceforge.net/"></ext-link> and the myExperiment [<xref ref-type="bibr" rid="B2438">2438</xref>]<ext-link ext-link-type="uri" xlink:href="http://www.myexperiment.org/"></ext-link> environments, represent an intellectually important approach. Important too to this endeavour will be Open Access initiatives [<xref ref-type="bibr" rid="B1">1</xref>,<xref ref-type="bibr" rid="B2439">2439</xref>,<xref ref-type="bibr" rid="B2440">2440</xref>] and institutional and other repositories [<xref ref-type="bibr" rid="B2441">2441</xref>,<xref ref-type="bibr" rid="B2442">2442</xref>] of full-text papers. This will help to build an accurate picture of the biochemical networks operating in both normal and diseased states (and see [<xref ref-type="bibr" rid="B2443">2443</xref>]), preferably marked up semantically as in [<xref ref-type="bibr" rid="B118">118</xref>], and hence, by modelling them [<xref ref-type="bibr" rid="B2263">2263</xref>], where best to consider interventions. In order to develop and exploit this distributed approach, it will also be necessary for those generating them to make their data and metadata available (preferably in a semantically marked up way), probably as Web Services (e.g. [<xref ref-type="bibr" rid="B24">24</xref>,<xref ref-type="bibr" rid="B2444">2444</xref>-<xref ref-type="bibr" rid="B2452">2452</xref>]), and to give greater scientific weight to those involved in bio-curation [<xref ref-type="bibr" rid="B119">119</xref>] as they will be an increasingly important part of the scientific landscape. Modern sequencing instruments, for instance (e.g. [<xref ref-type="bibr" rid="B2453">2453</xref>-<xref ref-type="bibr" rid="B2457">2457</xref>]) are generating quality data at truly enormous rates [<xref ref-type="bibr" rid="B2458">2458</xref>], and innovative but computationally demanding algorithms are required to deal with them (e.g. [<xref ref-type="bibr" rid="B2459">2459</xref>]). In particular, however, we need tools for manipulating and visualising biochemical models [<xref ref-type="bibr" rid="B2110">2110</xref>,<xref ref-type="bibr" rid="B2410">2410</xref>,<xref ref-type="bibr" rid="B2429">2429</xref>,<xref ref-type="bibr" rid="B2460">2460</xref>]. As well as storing these models (e.g. as SBML or CellML [<xref ref-type="bibr" rid="B2461">2461</xref>]) in a file format, it is also convenient to store them in a database format, such as the B-net database developed by Mendes and colleagues [<xref ref-type="bibr" rid="B118">118</xref>,<xref ref-type="bibr" rid="B2462">2462</xref>]. Federated annotation protocols such as the Distributed Annotaton Scheme (see e.g. [<xref ref-type="bibr" rid="B2463">2463</xref>]) allow data from heterogeneous sources to be combined, while other integrative/distributed architectures such as ONDEX [<xref ref-type="bibr" rid="B2464">2464</xref>] and Utopia [<xref ref-type="bibr" rid="B2465">2465</xref>-<xref ref-type="bibr" rid="B2468">2468</xref>] are similarly showing considerable promise for integrative systems biology.</p><p>Given the widely dispersed communities that have been referenced herein, and the future requirement for integrating knowledge generated throughput the world, a programme for understanding the combinatorial roles of poorly liganded iron and reactive oxygen species in the aetiology of many diseases, as set out in the above, appears to be prototypical for the kinds of new approaches to doing science that we may anticipate in the eras of Web 2.0 and the Semantic Web.</p></sec><sec><title>Abbreviations</title><p>AECOPD: Acute Exacerbation of Chronic Obstructive Pulmonary Disorder; AKI: Acute Kidney Injury; ALS: Amyotrophic Lateral Sclerosis; AMD: Age-related Macular Degeneration; BBB: Blood-brain barrier; ChEBI: Chemical Entities of Biological Interest; CQ: Clioquinol; COPD: Chronic Obstructive Pulmonary Disorder; DFO: Desferrioxamine; Dp44mT: di-2-pyridylketone-4,4,-dimethyl-3-thiosemicarbazone; EDTA: Ethylenediamine-tetraacetic Acid; FA: Friedrich's ataxia; FPN1: Ferroportin-1; HBED: N,N'-bis-(2-hydroxybenzyl)ethylenediamine-N,N'-diacetic acid; HCP1: Heme Carrier Protein-1; HIF: Hypoxia-Inducible Factor; HO1: Heme Oxygenase-1; HMG-CoA: Hydroxymethyl glutaryl Coenzyme A; Hp: Hephaestin; 8HQs: A variety of 8-hydroxyquinolines; IBD: Inflammatory Bowel Disease; InChI: International Chemical Identifier; IKK: IκB kinase; KEGG: Kyoto Encyclopedia of Genes and Genomes; L1: Deferriprone; LFA-1: Leukocyte Function Antigen-1; LIP: Labile Iron Pool; LIPID: Long-Term Intervention with Pravastatin in Ischaemic Disease; LPS: Lipopolysaccharide; MOF: Multiple organ failure; NF-κB: Nuclear Factor κB; NGAL: Neutrophil Gelatinase-Associated Lipocalin (Also known as lipocalin-2 or siderocalin); NIH: 2-hydroxy-1-napthylaldehyde isonicotinyl hydrazone; PE: Pre-eclampsia; PIH: Pyridoxal isonicotinyl hydrazone; PPAR: Peroxisome Proliferator Activated Receptor; RA: Rheumatoid Arthritis; ROS: Reactive Oxygen Species; SBML: Systems Biology Markup Language; SIH: Salicylaldehyde isonicotinyl hydrazone; SIRS: Systemic Inflammatory Response Syndrome; SLE: Systemic Lupus Erythematosus; SMILES: Simplified Molecular Input Line Entry Specification; SOD: Superoxide Dismutase; Tf: Transferrin; TNF: Tissue Necrosis Factor; VEGF: Vascular Endothelial Growth Factor.</p></sec><sec><title>Competing interests</title><p>The author declares that he has no competing interests.</p></sec><sec><title>Pre-publication history</title><p>The pre-publication history for this paper can be accessed here:</p><p><ext-link ext-link-type="uri" xlink:href="http://www.biomedcentral.com/1755-8794/2/2/prepub"></ext-link></p></sec></body><back><ack><sec><title>Acknowledgements</title><p>I thank Jon Barasch (Columbia University) for drawing my attention to the role of NGAL in human physiology, and Phil Baker, David Brough and Louise Kenny for many further useful and enjoyable discussions. I thank Katya Tarasova for considerable assistance with literature gathering and Julie Cowley for assistance with the proofs. Much of my work when this was written has been supported by the UK BBSRC and EPSRC, for which I am most grateful, and I am also a recipient of funding from the British Heart Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. 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