Regulation of the host immune system by helminth parasites
Identifieur interne : 000630 ( Pmc/Checkpoint ); précédent : 000629; suivant : 000631Regulation of the host immune system by helminth parasites
Auteurs : Rick M. Maizels [Royaume-Uni] ; Henry J. Mcsorley [Royaume-Uni]Source :
- The Journal of Allergy and Clinical Immunology [ 0091-6749 ] ; 2016.
Abstract
Helminth parasite infections are associated with a battery of immunomodulatory mechanisms that affect all facets of the host immune response to ensure their persistence within the host. This broad-spectrum modulation of host immunity has intended and unintended consequences, both advantageous and disadvantageous. Thus the host can benefit from suppression of collateral damage during parasite infection and from reduced allergic, autoimmune, and inflammatory reactions. However, helminth infection can also be detrimental in reducing vaccine responses, increasing susceptibility to coinfection and potentially reducing tumor immunosurveillance. In this review we will summarize the panoply of immunomodulatory mechanisms used by helminths, their potential utility in human disease, and prospective areas of future research.
Url:
DOI: 10.1016/j.jaci.2016.07.007
PubMed: 27476889
PubMed Central: 5010150
Affiliations:
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<front><div type="abstract" xml:lang="en"><p>Helminth parasite infections are associated with a battery of immunomodulatory mechanisms that affect all facets of the host immune response to ensure their persistence within the host. This broad-spectrum modulation of host immunity has intended and unintended consequences, both advantageous and disadvantageous. Thus the host can benefit from suppression of collateral damage during parasite infection and from reduced allergic, autoimmune, and inflammatory reactions. However, helminth infection can also be detrimental in reducing vaccine responses, increasing susceptibility to coinfection and potentially reducing tumor immunosurveillance. In this review we will summarize the panoply of immunomodulatory mechanisms used by helminths, their potential utility in human disease, and prospective areas of future research.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Allergy Clin Immunol</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Allergy Clin. Immunol</journal-id>
<journal-title-group><journal-title>The Journal of Allergy and Clinical Immunology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0091-6749</issn>
<issn pub-type="epub">1097-6825</issn>
<publisher><publisher-name>Mosby</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27476889</article-id>
<article-id pub-id-type="pmc">5010150</article-id>
<article-id pub-id-type="publisher-id">S0091-6749(16)30725-4</article-id>
<article-id pub-id-type="doi">10.1016/j.jaci.2016.07.007</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Reviews and Feature Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Regulation of the host immune system by helminth parasites</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Maizels</surname>
<given-names>Rick M.</given-names>
</name>
<degrees>PhD</degrees>
<email>rick.maizels@glasgow.ac.uk</email>
<xref rid="aff1" ref-type="aff">a</xref>
<xref rid="cor1" ref-type="corresp">∗</xref>
</contrib>
<contrib contrib-type="author"><name><surname>McSorley</surname>
<given-names>Henry J.</given-names>
</name>
<degrees>PhD</degrees>
<xref rid="aff2" ref-type="aff">b</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>a</label>
Wellcome Trust Centre for Molecular Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, United Kingdom</aff>
<aff id="aff2"><label>b</label>
Centre for Inflammation Research, University of Edinburgh, Queen's Medical Research Institute, Edinburgh, United Kingdom</aff>
<author-notes><corresp id="cor1"><label>∗</label>
Corresponding author: Rick M. Maizels, PhD, Wellcome Trust Centre for Molecular Parasitology, Institute of Infection, Immunity and Inflammation, University of Glasgow, 120 University Place, Glasgow G12 8TA, United Kingdom.Wellcome Trust Centre for Molecular ParasitologyInstitute of Infection, Immunity and InflammationUniversity of Glasgow120 University PlaceGlasgowG12 8TAUnited Kingdom <email>rick.maizels@glasgow.ac.uk</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release"><day>1</day>
<month>9</month>
<year>2016</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>9</month>
<year>2016</year>
</pub-date>
<volume>138</volume>
<issue>3</issue>
<fpage>666</fpage>
<lpage>675</lpage>
<history><date date-type="received"><day>7</day>
<month>7</month>
<year>2016</year>
</date>
<date date-type="rev-recd"><day>25</day>
<month>7</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>25</day>
<month>7</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>© 2016 The Authors</copyright-statement>
<copyright-year>2016</copyright-year>
<license license-type="CC BY" xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).</license-p>
</license>
</permissions>
<abstract id="abs0010"><p>Helminth parasite infections are associated with a battery of immunomodulatory mechanisms that affect all facets of the host immune response to ensure their persistence within the host. This broad-spectrum modulation of host immunity has intended and unintended consequences, both advantageous and disadvantageous. Thus the host can benefit from suppression of collateral damage during parasite infection and from reduced allergic, autoimmune, and inflammatory reactions. However, helminth infection can also be detrimental in reducing vaccine responses, increasing susceptibility to coinfection and potentially reducing tumor immunosurveillance. In this review we will summarize the panoply of immunomodulatory mechanisms used by helminths, their potential utility in human disease, and prospective areas of future research.</p>
</abstract>
<kwd-group id="kwrds0010"><title>Key words</title>
<kwd>Allergy</kwd>
<kwd>infection</kwd>
<kwd>pathology</kwd>
<kwd>therapy</kwd>
<kwd>tolerance</kwd>
</kwd-group>
<kwd-group id="kwrds0015"><title>Abbreviations used</title>
<kwd>Breg, Regulatory B</kwd>
<kwd>DC, Dendritic cell</kwd>
<kwd>Foxp3, Forkhead box protein 3</kwd>
<kwd>Treg, Regulatory T</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="fig1"><label>Fig 1</label>
<caption><p>Immune system–parasite interactions during helminth infections. <bold>A,</bold>
Blockade of innate sensing and alarmin production, such as inhibiting Toll-like receptor <italic>(TLR)</italic>
responses of dendritic cells, thereby impairing inflammatory T<sub>H</sub>
1/T<sub>H</sub>
17 development, and abrogating epithelial cell production of IL-33, thereby pre-empting the type 2 response. <italic>ILC2</italic>
, Type 2 innate lymphoid cell. <bold>B,</bold>
Modulation of the adaptive immune response, promoting Treg cell differentiation either directly through production of TGF-β–like mimics <italic>(TGM)</italic>
or indirectly by inducing host TGF-β and retinoic acid <italic>(RA)</italic>
from DCs and macrophages. <bold>C,</bold>
Modification of bystander immune responses in the infected host.</p>
</caption>
<graphic xlink:href="gr1"></graphic>
</fig>
<table-wrap id="tbl1" position="float"><label>Table I</label>
<caption><p>Selected parasite-derived molecules with activity in immune-mediated diseases</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th>Immune modulatory effect</th>
<th>Example parasite product</th>
<th>Mechanism of action</th>
<th>Disease models in which efficacy is shown</th>
<th>References</th>
</tr>
</thead>
<tbody><tr><td>Suppression of innate and adaptive immune cell activation</td>
<td><italic>A viteae</italic>
ES-62</td>
<td>Nonconventional signaling through TLR4, leading to sequestration of PKC-α</td>
<td>Asthma, atopic dermatitis, SLE, and arthritis</td>
<td><xref rid="bib106" ref-type="bibr">106</xref>
, <xref rid="bib107" ref-type="bibr">107</xref>
, <xref rid="bib108" ref-type="bibr">108</xref>
</td>
</tr>
<tr><td>Suppression of antigen presentation</td>
<td><italic>S mansoni</italic>
ω-1</td>
<td>Degradation of DC mRNA, preventing IL-12 secretion</td>
<td>NOD diabetes, metabolic homeostasis</td>
<td><xref rid="bib73" ref-type="bibr">73</xref>
, <xref rid="bib105" ref-type="bibr">105</xref>
, <xref rid="bib109" ref-type="bibr">109</xref>
</td>
</tr>
<tr><td></td>
<td><italic>F hepatica</italic>
FhHDM-1</td>
<td>Inhibition of vacuolar ATPase resulting in reduced endolysosomal acidification</td>
<td>Sepsis</td>
<td><xref rid="bib110" ref-type="bibr">110</xref>
, <xref rid="bib111" ref-type="bibr">111</xref>
</td>
</tr>
<tr><td></td>
<td>Cystatins:<break></break>
<italic>A viteae</italic>
Av17 (AvCystatin),<break></break>
<italic>B malayi</italic>
Bm-CPI-2,<break></break>
<italic>N brasiliensis</italic>
Nippocystatin</td>
<td>Inhibition of cysteine proteases required for antigen presentation; induction of IL-10 through signaling events downstream of an unknown receptor (Av17)</td>
<td>Asthma, colitis</td>
<td><xref rid="bib104" ref-type="bibr">104</xref>
, <xref rid="bib112" ref-type="bibr">112</xref>
, <xref rid="bib113" ref-type="bibr">113</xref>
, <xref rid="bib114" ref-type="bibr">114</xref>
, <xref rid="bib115" ref-type="bibr">115</xref>
</td>
</tr>
<tr><td>Suppression of ILC2 responses</td>
<td><italic>H polygyrus</italic>
HES</td>
<td>Suppression of ILC2-inducing IL-33 responses</td>
<td>Asthma</td>
<td><xref rid="bib103" ref-type="bibr">103</xref>
</td>
</tr>
<tr><td>Induction of Treg cells</td>
<td><italic>H polygyrus</italic>
HES</td>
<td>Secreted TGF-β mimic ligates host TGF-β receptor</td>
<td>Asthma</td>
<td><xref rid="bib45" ref-type="bibr">45</xref>
</td>
</tr>
<tr><td></td>
<td><italic>S mansoni</italic>
SEA/ω-1</td>
<td>Induction of tolerogenic DCs, which produce TGF-β and RA</td>
<td>Type I diabetes</td>
<td><xref rid="bib46" ref-type="bibr">46</xref>
, <xref rid="bib109" ref-type="bibr">109</xref>
</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p><italic>Bm-CPI-2</italic>
, <italic>Brugia malayi</italic>
cysteine protease inhibitor 2; <italic>FhHDM-1</italic>
, <italic>Fasciola hepatica</italic>
helminth defense molecule 1; <italic>HES</italic>
, <italic>H polygyrus</italic>
excretory secretory products; <italic>Hp-CPI</italic>
, <italic>H polygyrus</italic>
cysteine protease inhibitor; <italic>ILC2</italic>
, type 2 innate lymphoid cell; <italic>PKC</italic>
, protein kinase C; <italic>RA</italic>
, retinoic acid; <italic>SEA</italic>
, <italic>Schistosoma mansoni</italic>
soluble egg antigen; <italic>SLE</italic>
, systemic lupus erythematosus; <italic>TLR</italic>
, Toll-like receptor.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list><country><li>Royaume-Uni</li>
</country>
<region><li>Écosse</li>
</region>
<settlement><li>Glasgow</li>
<li>Édimbourg</li>
</settlement>
<orgName><li>Université d'Édimbourg</li>
<li>Université de Glasgow</li>
</orgName>
</list>
<tree><country name="Royaume-Uni"><region name="Écosse"><name sortKey="Maizels, Rick M" sort="Maizels, Rick M" uniqKey="Maizels R" first="Rick M." last="Maizels">Rick M. Maizels</name>
</region>
<name sortKey="Mcsorley, Henry J" sort="Mcsorley, Henry J" uniqKey="Mcsorley H" first="Henry J." last="Mcsorley">Henry J. Mcsorley</name>
</country>
</tree>
</affiliations>
</record>
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