A New and Integral Approach to the Etiopathogenesis and Treatment of Breast Cancer Based upon Its Hydrogen Ion Dynamics
Identifieur interne : 000A32 ( Pmc/Curation ); précédent : 000A31; suivant : 000A33A New and Integral Approach to the Etiopathogenesis and Treatment of Breast Cancer Based upon Its Hydrogen Ion Dynamics
Auteurs : Salvador Harguindey ; Khalid Alfarouk ; Julián Polo Orozco ; Kévin Hardonnière ; Daniel Stanciu ; Stefano Fais ; Jesús DevesaSource :
- International Journal of Molecular Sciences [ 1422-0067 ] ; 2020.
Abstract
Despite all efforts, the treatment of breast cancer (BC) cannot be considered to be a success story. The advances in surgery, chemotherapy and radiotherapy have not been sufficient at all. Indeed, the accumulated experience clearly indicates that new perspectives and non-main stream approaches are needed to better characterize the etiopathogenesis and treatment of this disease. This contribution deals with how the new pH-centric anticancer paradigm plays a fundamental role in reaching a more integral understanding of the etiology, pathogenesis, and treatment of this multifactorial disease. For the first time, the armamentarium available for the treatment of the different types and phases of BC is approached here from a Unitarian perspective-based upon the hydrogen ion dynamics of cancer. The wide-ranged pH-related molecular, biochemical and metabolic model is able to embrace most of the fields and subfields of breast cancer etiopathogenesis and treatment. This single and integrated approach allows advancing towards a unidirectional, concerted and synergistic program of treatment. Further efforts in this line are likely to first improve the therapeutics of each subtype of this tumor and every individual patient in every phase of the disease.
Url:
DOI: 10.3390/ijms21031110
PubMed: 32046158
PubMed Central: 7036897
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<front><div type="abstract" xml:lang="en"><p>Despite all efforts, the treatment of breast cancer (BC) cannot be considered to be a success story. The advances in surgery, chemotherapy and radiotherapy have not been sufficient at all. Indeed, the accumulated experience clearly indicates that new perspectives and non-main stream approaches are needed to better characterize the etiopathogenesis and treatment of this disease. This contribution deals with how the new pH-centric anticancer paradigm plays a fundamental role in reaching a more integral understanding of the etiology, pathogenesis, and treatment of this multifactorial disease. For the first time, the armamentarium available for the treatment of the different types and phases of BC is approached here from a Unitarian perspective-based upon the hydrogen ion dynamics of cancer. The wide-ranged pH-related molecular, biochemical and metabolic model is able to embrace most of the fields and subfields of breast cancer etiopathogenesis and treatment. This single and integrated approach allows advancing towards a unidirectional, concerted and synergistic program of treatment. Further efforts in this line are likely to first improve the therapeutics of each subtype of this tumor and every individual patient in every phase of the disease.</p>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Mol Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Int J Mol Sci</journal-id>
<journal-id journal-id-type="publisher-id">ijms</journal-id>
<journal-title-group><journal-title>International Journal of Molecular Sciences</journal-title>
</journal-title-group>
<issn pub-type="epub">1422-0067</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
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<article-meta><article-id pub-id-type="pmid">32046158</article-id>
<article-id pub-id-type="pmc">7036897</article-id>
<article-id pub-id-type="doi">10.3390/ijms21031110</article-id>
<article-id pub-id-type="publisher-id">ijms-21-01110</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>A New and Integral Approach to the Etiopathogenesis and Treatment of Breast Cancer Based upon Its Hydrogen Ion Dynamics</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-1725-757X</contrib-id>
<name><surname>Harguindey</surname>
<given-names>Salvador</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-21-01110">1</xref>
<xref rid="c1-ijms-21-01110" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Alfarouk</surname>
<given-names>Khalid</given-names>
</name>
<xref ref-type="aff" rid="af2-ijms-21-01110">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Polo Orozco</surname>
<given-names>Julián</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-21-01110">1</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-4866-8937</contrib-id>
<name><surname>Hardonnière</surname>
<given-names>Kévin</given-names>
</name>
<xref ref-type="aff" rid="af3-ijms-21-01110">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Stanciu</surname>
<given-names>Daniel</given-names>
</name>
<xref ref-type="aff" rid="af4-ijms-21-01110">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fais</surname>
<given-names>Stefano</given-names>
</name>
<xref ref-type="aff" rid="af5-ijms-21-01110">5</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-4153-2543</contrib-id>
<name><surname>Devesa</surname>
<given-names>Jesús</given-names>
</name>
<xref ref-type="aff" rid="af6-ijms-21-01110">6</xref>
</contrib>
</contrib-group>
<aff id="af1-ijms-21-01110"><label>1</label>
Institute of Clinical Biology and Metabolism, Postas 13, 01004 Vitoria, Spain;<email>polorozco@gmail.com</email>
</aff>
<aff id="af2-ijms-21-01110"><label>2</label>
Al-Ghad International Colleges for Applied Medical Sciences, Al-Madinah Al-Munawarah, Saudi Arabia and Alfarouk Biomedical Research LLC, Tampa, FL 33617, USA;<email>khaliomer@gmail.com</email>
</aff>
<aff id="af3-ijms-21-01110"><label>3</label>
Université Paris-Saclay, Inserm, Inflammation, Microbiome and Immunosurveillance, 92290 Châtenay-Malabry, France;<email>kevin.hardonniere@u-psud.fr</email>
</aff>
<aff id="af4-ijms-21-01110"><label>4</label>
Scientific Direction, MCS Foundation For Life, 5623KR Eindhoven, The Netherlands;<email>cd.stanciu@gmail.com</email>
</aff>
<aff id="af5-ijms-21-01110"><label>5</label>
Department of Oncology and Molecular Medicine, Istituto Superiore di Sanità (National Institute of Health), Viale Regina Elena, 299, 00161 Rome, Italy;<email>Stefano.fais@iss.it</email>
</aff>
<aff id="af6-ijms-21-01110"><label>6</label>
Scientific Direction, Foltra Medical Centre, Travesía de Montouto 24, 15886 Teo, Spain;<email>devesa.jesus@gmail.com</email>
</aff>
<author-notes><corresp id="c1-ijms-21-01110"><label>*</label>
Correspondence: <email>salvaszh@telefonica.net</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>07</day>
<month>2</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="collection"><month>2</month>
<year>2020</year>
</pub-date>
<volume>21</volume>
<issue>3</issue>
<elocation-id>1110</elocation-id>
<history><date date-type="received"><day>21</day>
<month>1</month>
<year>2020</year>
</date>
<date date-type="accepted"><day>06</day>
<month>2</month>
<year>2020</year>
</date>
</history>
<permissions><copyright-statement>© 2020 by the authors.</copyright-statement>
<copyright-year>2020</copyright-year>
<license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract><p>Despite all efforts, the treatment of breast cancer (BC) cannot be considered to be a success story. The advances in surgery, chemotherapy and radiotherapy have not been sufficient at all. Indeed, the accumulated experience clearly indicates that new perspectives and non-main stream approaches are needed to better characterize the etiopathogenesis and treatment of this disease. This contribution deals with how the new pH-centric anticancer paradigm plays a fundamental role in reaching a more integral understanding of the etiology, pathogenesis, and treatment of this multifactorial disease. For the first time, the armamentarium available for the treatment of the different types and phases of BC is approached here from a Unitarian perspective-based upon the hydrogen ion dynamics of cancer. The wide-ranged pH-related molecular, biochemical and metabolic model is able to embrace most of the fields and subfields of breast cancer etiopathogenesis and treatment. This single and integrated approach allows advancing towards a unidirectional, concerted and synergistic program of treatment. Further efforts in this line are likely to first improve the therapeutics of each subtype of this tumor and every individual patient in every phase of the disease.</p>
</abstract>
<kwd-group><kwd>pH and breast cancer</kwd>
<kwd>breast cancer etiology</kwd>
<kwd>breast cancer pathogenesis</kwd>
<kwd>breast cancer treatment</kwd>
<kwd>pH-centric anticancer paradigm</kwd>
<kwd>hydrogen ion dynamics of cancer</kwd>
<kwd>cancer proton reversal</kwd>
<kwd>multiple drug resistance (MDR) integral approach</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="ijms-21-01110-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Proton transporters and proton pumps involved in the carcinogenicity of breast cancer and other malignant tumors. pHi: intracellular pH; CT: cell transformation; pHe: extracellular pH; PTs: proton transporters; PPs: Proton pumps; NHE-1: Na<sup>+</sup>
/H<sup>+</sup>
antiporter; H<sup>+</sup>
: hydrogen ion; CAs: carbonic anhydrases; MCT: monocarboxylate transporters; P-gp: P-glycoprotein; V-H<sup>+</sup>
-ATPase: Vacuolar ATPase; MDR: Multiple drug resistance. Blue arrows: Induction. Black arrows: Result. Yellow color: intracellular space of a tumor cell.</p>
</caption>
<graphic xlink:href="ijms-21-01110-g001"></graphic>
</fig>
<table-wrap id="ijms-21-01110-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">ijms-21-01110-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>pH-related and -unrelated mechanisms in the etiopathogenesis and progression of breast cancer. BC: Breast cancer; TME: Tumor microenvironment; MDR: Multidrug resistance; NHE: Na<sup>+</sup>
/H<sup>+</sup>
antiporter: CAs: Carbonic anhydrases; ER-: Estrogen negative cells; PTIs: Proton transport inhibitors; PPIs; Proton pump inhibitors.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Mechanisms</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Summary</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">H<sup>+</sup>
extrusion and/or elevated pHi</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">H<sup>+</sup>
extrusion from cells is sufficient to induce transformation, growth and invasion in BC and other tumors. NHE-mediated H<sup>+</sup>
extrusion by itself has a carcinogenic effect on breast cells and increases MDR.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B8-ijms-21-01110" ref-type="bibr">8</xref>
,<xref rid="B23-ijms-21-01110" ref-type="bibr">23</xref>
,<xref rid="B25-ijms-21-01110" ref-type="bibr">25</xref>
,<xref rid="B37-ijms-21-01110" ref-type="bibr">37</xref>
,<xref rid="B38-ijms-21-01110" ref-type="bibr">38</xref>
,<xref rid="B39-ijms-21-01110" ref-type="bibr">39</xref>
,<xref rid="B40-ijms-21-01110" ref-type="bibr">40</xref>
,<xref rid="B41-ijms-21-01110" ref-type="bibr">41</xref>
,<xref rid="B42-ijms-21-01110" ref-type="bibr">42</xref>
,<xref rid="B43-ijms-21-01110" ref-type="bibr">43</xref>
,<xref rid="B44-ijms-21-01110" ref-type="bibr">44</xref>
,<xref rid="B48-ijms-21-01110" ref-type="bibr">48</xref>
,<xref rid="B54-ijms-21-01110" ref-type="bibr">54</xref>
,<xref rid="B59-ijms-21-01110" ref-type="bibr">59</xref>
,<xref rid="B122-ijms-21-01110" ref-type="bibr">122</xref>
,<xref rid="B123-ijms-21-01110" ref-type="bibr">123</xref>
,<xref rid="B124-ijms-21-01110" ref-type="bibr">124</xref>
,<xref rid="B125-ijms-21-01110" ref-type="bibr">125</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Tumor micro-environmental (TME) acidosis, immunity and MDR</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Acidity of the TME disrupts the body immune defense mechanisms towards malignant tumors, locally and systemically. This allows a relentless and uncontrolled tumor progression. TME also has an essential role in the progression of inflammatory BC. Thus, TME is a novel therapeutic target in BC. TME acidity also induces MDR.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B20-ijms-21-01110" ref-type="bibr">20</xref>
,<xref rid="B21-ijms-21-01110" ref-type="bibr">21</xref>
,<xref rid="B22-ijms-21-01110" ref-type="bibr">22</xref>
,<xref rid="B47-ijms-21-01110" ref-type="bibr">47</xref>
,<xref rid="B49-ijms-21-01110" ref-type="bibr">49</xref>
,<xref rid="B50-ijms-21-01110" ref-type="bibr">50</xref>
,<xref rid="B51-ijms-21-01110" ref-type="bibr">51</xref>
,<xref rid="B78-ijms-21-01110" ref-type="bibr">78</xref>
,<xref rid="B79-ijms-21-01110" ref-type="bibr">79</xref>
,<xref rid="B84-ijms-21-01110" ref-type="bibr">84</xref>
,<xref rid="B87-ijms-21-01110" ref-type="bibr">87</xref>
,<xref rid="B116-ijms-21-01110" ref-type="bibr">116</xref>
,<xref rid="B120-ijms-21-01110" ref-type="bibr">120</xref>
,<xref rid="B126-ijms-21-01110" ref-type="bibr">126</xref>
,<xref rid="B127-ijms-21-01110" ref-type="bibr">127</xref>
,<xref rid="B128-ijms-21-01110" ref-type="bibr">128</xref>
,<xref rid="B129-ijms-21-01110" ref-type="bibr">129</xref>
,<xref rid="B130-ijms-21-01110" ref-type="bibr">130</xref>
,<xref rid="B131-ijms-21-01110" ref-type="bibr">131</xref>
,<xref rid="B132-ijms-21-01110" ref-type="bibr">132</xref>
,<xref rid="B133-ijms-21-01110" ref-type="bibr">133</xref>
,<xref rid="B134-ijms-21-01110" ref-type="bibr">134</xref>
,<xref rid="B135-ijms-21-01110" ref-type="bibr">135</xref>
,<xref rid="B136-ijms-21-01110" ref-type="bibr">136</xref>
,<xref rid="B137-ijms-21-01110" ref-type="bibr">137</xref>
,<xref rid="B138-ijms-21-01110" ref-type="bibr">138</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Insulin (INS) and insulin-like growth factor-1 (IGF-1)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">INS and INS-resistance have a direct effect in raising pHi and are associated with breast cancer carcinogenicity and progression. Over-expression of insulin/insulin-like growth factor-1 is associated with a decrease in the life span of women with BC.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B3-ijms-21-01110" ref-type="bibr">3</xref>
,<xref rid="B35-ijms-21-01110" ref-type="bibr">35</xref>
,<xref rid="B39-ijms-21-01110" ref-type="bibr">39</xref>
,<xref rid="B139-ijms-21-01110" ref-type="bibr">139</xref>
,<xref rid="B140-ijms-21-01110" ref-type="bibr">140</xref>
,<xref rid="B141-ijms-21-01110" ref-type="bibr">141</xref>
,<xref rid="B142-ijms-21-01110" ref-type="bibr">142</xref>
,<xref rid="B143-ijms-21-01110" ref-type="bibr">143</xref>
,<xref rid="B144-ijms-21-01110" ref-type="bibr">144</xref>
,<xref rid="B145-ijms-21-01110" ref-type="bibr">145</xref>
,<xref rid="B146-ijms-21-01110" ref-type="bibr">146</xref>
,<xref rid="B147-ijms-21-01110" ref-type="bibr">147</xref>
,<xref rid="B148-ijms-21-01110" ref-type="bibr">148</xref>
,<xref rid="B149-ijms-21-01110" ref-type="bibr">149</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Prolactin (PRL)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PRL stimulates growth, motility and invasiveness of BC cells through NHE1 activation. In this way contributes to the metastatic process of human BC and becomes another therapeutic target.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B150-ijms-21-01110" ref-type="bibr">150</xref>
,<xref rid="B151-ijms-21-01110" ref-type="bibr">151</xref>
,<xref rid="B152-ijms-21-01110" ref-type="bibr">152</xref>
,<xref rid="B153-ijms-21-01110" ref-type="bibr">153</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Estrogens</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Estrogens play a crucial role in breast tumorigenesis by promoting cell proliferation and decreasing apoptosis. ER-cells are considered to have a higher expression of NHE activity and are preferably associated with CA-IX over CA-XII. Inhibition of CA-IX improves the prognosis of the disease.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B4-ijms-21-01110" ref-type="bibr">4</xref>
,<xref rid="B154-ijms-21-01110" ref-type="bibr">154</xref>
,<xref rid="B155-ijms-21-01110" ref-type="bibr">155</xref>
,<xref rid="B156-ijms-21-01110" ref-type="bibr">156</xref>
,<xref rid="B157-ijms-21-01110" ref-type="bibr">157</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Ion channels</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NaV1.5-Na<sup>+</sup>
channels associated with NHE-1 are overexpressed in BC, stimulating the formation of invadopodia, facilitating local growth and the metastatic process.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B8-ijms-21-01110" ref-type="bibr">8</xref>
,<xref rid="B72-ijms-21-01110" ref-type="bibr">72</xref>
,<xref rid="B73-ijms-21-01110" ref-type="bibr">73</xref>
,<xref rid="B75-ijms-21-01110" ref-type="bibr">75</xref>
,<xref rid="B76-ijms-21-01110" ref-type="bibr">76</xref>
,<xref rid="B77-ijms-21-01110" ref-type="bibr">77</xref>
,<xref rid="B148-ijms-21-01110" ref-type="bibr">148</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PTs, PPs, and Growth factors</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NHE1-overexpression is stimulated by a myriad of factors, which alone or in combination induce a carcinogenic elevation of pHi as the oncogenic response of normal cells of different origins and locations. Carbonic anhydrases (CAs) also have an important role in the pathogenesis of BC, mainly in hypoxic conditions. NHE1 levels are significantly higher in BC tissue than in adjacent normal tissue, and also in resistant BC cells when compared to sensitive cells.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B8-ijms-21-01110" ref-type="bibr">8</xref>
,<xref rid="B25-ijms-21-01110" ref-type="bibr">25</xref>
,<xref rid="B41-ijms-21-01110" ref-type="bibr">41</xref>
,<xref rid="B55-ijms-21-01110" ref-type="bibr">55</xref>
,<xref rid="B56-ijms-21-01110" ref-type="bibr">56</xref>
,<xref rid="B57-ijms-21-01110" ref-type="bibr">57</xref>
,<xref rid="B58-ijms-21-01110" ref-type="bibr">58</xref>
,<xref rid="B59-ijms-21-01110" ref-type="bibr">59</xref>
,<xref rid="B60-ijms-21-01110" ref-type="bibr">60</xref>
,<xref rid="B61-ijms-21-01110" ref-type="bibr">61</xref>
,<xref rid="B62-ijms-21-01110" ref-type="bibr">62</xref>
,<xref rid="B63-ijms-21-01110" ref-type="bibr">63</xref>
,<xref rid="B64-ijms-21-01110" ref-type="bibr">64</xref>
,<xref rid="B65-ijms-21-01110" ref-type="bibr">65</xref>
,<xref rid="B66-ijms-21-01110" ref-type="bibr">66</xref>
,<xref rid="B67-ijms-21-01110" ref-type="bibr">67</xref>
,<xref rid="B68-ijms-21-01110" ref-type="bibr">68</xref>
,<xref rid="B69-ijms-21-01110" ref-type="bibr">69</xref>
,<xref rid="B70-ijms-21-01110" ref-type="bibr">70</xref>
,<xref rid="B71-ijms-21-01110" ref-type="bibr">71</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="ijms-21-01110-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">ijms-21-01110-t002_Table 2</object-id>
<label>Table 2</label>
<caption><p>pH-related drugs with present and potential benefit in the treatment of breast cancer. BC: Breast cancer; NHE: Na<sup>+</sup>
/H<sup>+</sup>
antiporter; MDR: Multiple drug resistance; P-gp: P-glycoprotein; CAs: Carbonic anhydrases; ER<sup>+</sup>
: Estrogen positive cells; ER-: Estrogen negative cells; PTIs: Proton transport inhibitors; PPIs; Proton pump inhibitors. TME: tumor microenvironment.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Drug</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Summary</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Amiloride (AM) (and/or liposomal amiloride), proton transport inhibitors (PTIs) and intracellular (IC) acidifiers</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AM is a non-specific NHE inhibitor first introduced for human use as a K<sup>+</sup>
sparing diuretic. It works as an antiangiogenic agent and has proved to be most effective as an antimetastatic drug in transplanted breast tumors in animals. A positive clinical experience in an occasional patient has been reported with its chronic use when traditional chemotherapy had failed. Also, the many anti-cancer effects of AM have been fully described. However, its utilization has not entered clinical trials in bedside oncology. (For further details, see the text).</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B8-ijms-21-01110" ref-type="bibr">8</xref>
,<xref rid="B16-ijms-21-01110" ref-type="bibr">16</xref>
,<xref rid="B25-ijms-21-01110" ref-type="bibr">25</xref>
,<xref rid="B26-ijms-21-01110" ref-type="bibr">26</xref>
,<xref rid="B32-ijms-21-01110" ref-type="bibr">32</xref>
,<xref rid="B53-ijms-21-01110" ref-type="bibr">53</xref>
,<xref rid="B54-ijms-21-01110" ref-type="bibr">54</xref>
,<xref rid="B60-ijms-21-01110" ref-type="bibr">60</xref>
,<xref rid="B63-ijms-21-01110" ref-type="bibr">63</xref>
,<xref rid="B64-ijms-21-01110" ref-type="bibr">64</xref>
,<xref rid="B67-ijms-21-01110" ref-type="bibr">67</xref>
,<xref rid="B68-ijms-21-01110" ref-type="bibr">68</xref>
,<xref rid="B69-ijms-21-01110" ref-type="bibr">69</xref>
,<xref rid="B79-ijms-21-01110" ref-type="bibr">79</xref>
,<xref rid="B82-ijms-21-01110" ref-type="bibr">82</xref>
,<xref rid="B88-ijms-21-01110" ref-type="bibr">88</xref>
,<xref rid="B101-ijms-21-01110" ref-type="bibr">101</xref>
,<xref rid="B110-ijms-21-01110" ref-type="bibr">110</xref>
,<xref rid="B118-ijms-21-01110" ref-type="bibr">118</xref>
,<xref rid="B129-ijms-21-01110" ref-type="bibr">129</xref>
,<xref rid="B158-ijms-21-01110" ref-type="bibr">158</xref>
,<xref rid="B165-ijms-21-01110" ref-type="bibr">165</xref>
,<xref rid="B170-ijms-21-01110" ref-type="bibr">170</xref>
,<xref rid="B171-ijms-21-01110" ref-type="bibr">171</xref>
,<xref rid="B172-ijms-21-01110" ref-type="bibr">172</xref>
,<xref rid="B173-ijms-21-01110" ref-type="bibr">173</xref>
,<xref rid="B174-ijms-21-01110" ref-type="bibr">174</xref>
,<xref rid="B175-ijms-21-01110" ref-type="bibr">175</xref>
,<xref rid="B176-ijms-21-01110" ref-type="bibr">176</xref>
,<xref rid="B177-ijms-21-01110" ref-type="bibr">177</xref>
,<xref rid="B178-ijms-21-01110" ref-type="bibr">178</xref>
,<xref rid="B179-ijms-21-01110" ref-type="bibr">179</xref>
,<xref rid="B180-ijms-21-01110" ref-type="bibr">180</xref>
,<xref rid="B181-ijms-21-01110" ref-type="bibr">181</xref>
,<xref rid="B182-ijms-21-01110" ref-type="bibr">182</xref>
,<xref rid="B183-ijms-21-01110" ref-type="bibr">183</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Proton pump inhibitors (PPIs) and TME alkalization</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PPIs are useful in the prevention of BC. Besides, the clinical utilization of V-ATPase inhibitors is a novel therapeutic measure to counteract the abnormal proton dynamics of BC and other tumors. PPIs also benefit from the microenvironmental acidity of tumors. Preclinical and clinical studies also support a direct anti-tumor effect of PPIs in BC and other solid tumors.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B22-ijms-21-01110" ref-type="bibr">22</xref>
,<xref rid="B49-ijms-21-01110" ref-type="bibr">49</xref>
,<xref rid="B51-ijms-21-01110" ref-type="bibr">51</xref>
,<xref rid="B67-ijms-21-01110" ref-type="bibr">67</xref>
,<xref rid="B78-ijms-21-01110" ref-type="bibr">78</xref>
,<xref rid="B85-ijms-21-01110" ref-type="bibr">85</xref>
,<xref rid="B128-ijms-21-01110" ref-type="bibr">128</xref>
,<xref rid="B130-ijms-21-01110" ref-type="bibr">130</xref>
,<xref rid="B177-ijms-21-01110" ref-type="bibr">177</xref>
,<xref rid="B184-ijms-21-01110" ref-type="bibr">184</xref>
,<xref rid="B185-ijms-21-01110" ref-type="bibr">185</xref>
,<xref rid="B186-ijms-21-01110" ref-type="bibr">186</xref>
,<xref rid="B187-ijms-21-01110" ref-type="bibr">187</xref>
,<xref rid="B188-ijms-21-01110" ref-type="bibr">188</xref>
,<xref rid="B189-ijms-21-01110" ref-type="bibr">189</xref>
,<xref rid="B190-ijms-21-01110" ref-type="bibr">190</xref>
,<xref rid="B191-ijms-21-01110" ref-type="bibr">191</xref>
,<xref rid="B192-ijms-21-01110" ref-type="bibr">192</xref>
,<xref rid="B193-ijms-21-01110" ref-type="bibr">193</xref>
,<xref rid="B194-ijms-21-01110" ref-type="bibr">194</xref>
,<xref rid="B195-ijms-21-01110" ref-type="bibr">195</xref>
,<xref rid="B196-ijms-21-01110" ref-type="bibr">196</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Monocarboxylate transport (MCT) inhibitors</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Quercetin is a pan-monocarboxylate transporter (MCT) inhibitor and intracellular acidifier. Liposomal quercetin is also available, since gastrointestinal absorption is very limited in the non-liposomal drug form.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B101-ijms-21-01110" ref-type="bibr">101</xref>
,<xref rid="B102-ijms-21-01110" ref-type="bibr">102</xref>
,<xref rid="B137-ijms-21-01110" ref-type="bibr">137</xref>
,<xref rid="B197-ijms-21-01110" ref-type="bibr">197</xref>
,<xref rid="B198-ijms-21-01110" ref-type="bibr">198</xref>
,<xref rid="B199-ijms-21-01110" ref-type="bibr">199</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Acetazolamide (AZM)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AZM is a carbonic anhydrase (CA) pan-inhibitor and cell acidifier. CAIX inhibition significantly reduces invasion of BC cells and represents a most promising drug in the treatment of BC, alone or in combination with different NHE inhibitors.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B63-ijms-21-01110" ref-type="bibr">63</xref>
,<xref rid="B65-ijms-21-01110" ref-type="bibr">65</xref>
,<xref rid="B165-ijms-21-01110" ref-type="bibr">165</xref>
,<xref rid="B183-ijms-21-01110" ref-type="bibr">183</xref>
,<xref rid="B200-ijms-21-01110" ref-type="bibr">200</xref>
,<xref rid="B201-ijms-21-01110" ref-type="bibr">201</xref>
,<xref rid="B202-ijms-21-01110" ref-type="bibr">202</xref>
,<xref rid="B203-ijms-21-01110" ref-type="bibr">203</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Doxorubicin (DOXO)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">There is a progressive increase in resistance to DOXO by increasing elevations of pHi, resistance that is suppressed by P-gp inhibitors, while P-gp also increases pHi. MDR is characterized by a reversal of the pH gradient (cancer proton reversal or CPR) across cancer cell membranes.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B8-ijms-21-01110" ref-type="bibr">8</xref>
,<xref rid="B25-ijms-21-01110" ref-type="bibr">25</xref>
,<xref rid="B84-ijms-21-01110" ref-type="bibr">84</xref>
,<xref rid="B88-ijms-21-01110" ref-type="bibr">88</xref>
,<xref rid="B89-ijms-21-01110" ref-type="bibr">89</xref>
,<xref rid="B90-ijms-21-01110" ref-type="bibr">90</xref>
,<xref rid="B101-ijms-21-01110" ref-type="bibr">101</xref>
,<xref rid="B179-ijms-21-01110" ref-type="bibr">179</xref>
,<xref rid="B204-ijms-21-01110" ref-type="bibr">204</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Paclitaxel</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">The inhibition of NHE1, which is fundamental in the chemotherapy of triple-negative BC metastasis, improves the efficacy of Paclitaxel and mediates in Paclitaxel-induced apoptosis of BC cells.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B40-ijms-21-01110" ref-type="bibr">40</xref>
,<xref rid="B42-ijms-21-01110" ref-type="bibr">42</xref>
,<xref rid="B44-ijms-21-01110" ref-type="bibr">44</xref>
,<xref rid="B179-ijms-21-01110" ref-type="bibr">179</xref>
,<xref rid="B180-ijms-21-01110" ref-type="bibr">180</xref>
,<xref rid="B205-ijms-21-01110" ref-type="bibr">205</xref>
,<xref rid="B206-ijms-21-01110" ref-type="bibr">206</xref>
,<xref rid="B207-ijms-21-01110" ref-type="bibr">207</xref>
,<xref rid="B208-ijms-21-01110" ref-type="bibr">208</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cis-platinum (CDDP)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">The first effect of CDDP is the induction of intracellular acidification by inhibiting H+ extrusion secondary to downregulation of NHE-1. Contrariwise, the activity of NHE-1 and its effect on elevating pHi increases CDDP resistance to treatment.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B206-ijms-21-01110" ref-type="bibr">206</xref>
,<xref rid="B209-ijms-21-01110" ref-type="bibr">209</xref>
,<xref rid="B210-ijms-21-01110" ref-type="bibr">210</xref>
,<xref rid="B211-ijms-21-01110" ref-type="bibr">211</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Antiestrogens</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ER- breast cancer cells have a higher expression of NHE activity and are preferably associated with CA-IX over CA-XII. Inhibition of CA-IX improves the prognosis of the disease. Although the role of Tamoxifen and Letrozole is well established, no further connections among pH dynamics and these antiestrogens have been described.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B4-ijms-21-01110" ref-type="bibr">4</xref>
,<xref rid="B5-ijms-21-01110" ref-type="bibr">5</xref>
,<xref rid="B154-ijms-21-01110" ref-type="bibr">154</xref>
,<xref rid="B155-ijms-21-01110" ref-type="bibr">155</xref>
,<xref rid="B156-ijms-21-01110" ref-type="bibr">156</xref>
,<xref rid="B157-ijms-21-01110" ref-type="bibr">157</xref>
,<xref rid="B200-ijms-21-01110" ref-type="bibr">200</xref>
,<xref rid="B212-ijms-21-01110" ref-type="bibr">212</xref>
,<xref rid="B213-ijms-21-01110" ref-type="bibr">213</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Melatonin (MT)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MT has an antiestrogenic effect and only for this reason it should be contemplated in BC therapy. Treatment with MT modulates tumor aggressiveness and increases apoptosis n BC cell lines. MT also suppresses tumor aerobic metabolism (the Warburg effect) and decreases breast cancer angiogenesis and metastasis.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B214-ijms-21-01110" ref-type="bibr">214</xref>
,<xref rid="B215-ijms-21-01110" ref-type="bibr">215</xref>
,<xref rid="B216-ijms-21-01110" ref-type="bibr">216</xref>
,<xref rid="B217-ijms-21-01110" ref-type="bibr">217</xref>
,<xref rid="B218-ijms-21-01110" ref-type="bibr">218</xref>
,<xref rid="B219-ijms-21-01110" ref-type="bibr">219</xref>
,<xref rid="B220-ijms-21-01110" ref-type="bibr">220</xref>
,<xref rid="B221-ijms-21-01110" ref-type="bibr">221</xref>
,<xref rid="B222-ijms-21-01110" ref-type="bibr">222</xref>
,<xref rid="B223-ijms-21-01110" ref-type="bibr">223</xref>
,<xref rid="B224-ijms-21-01110" ref-type="bibr">224</xref>
,<xref rid="B225-ijms-21-01110" ref-type="bibr">225</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cariporide (CP)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CP (HOE-642) is a powerful NHE1 inhibitor that, unfortunately, is not available for clinical use in bedside oncology. It induces apoptotic cells death in different malignant tumors.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B8-ijms-21-01110" ref-type="bibr">8</xref>
,<xref rid="B25-ijms-21-01110" ref-type="bibr">25</xref>
,<xref rid="B35-ijms-21-01110" ref-type="bibr">35</xref>
,<xref rid="B170-ijms-21-01110" ref-type="bibr">170</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Compound 9t (C9t)<break></break>
(Unavailable)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C9t is 500-fold more potent against NHE1 than cariporide and has a 1400-fold greater selectivity for NHE1 over NHE2. Besides, C9t is orally bioavailable, has low side-effects in mice and it presents a significantly improved safety profile over other NHE1inhibitors.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B8-ijms-21-01110" ref-type="bibr">8</xref>
,<xref rid="B35-ijms-21-01110" ref-type="bibr">35</xref>
,<xref rid="B178-ijms-21-01110" ref-type="bibr">178</xref>
] </td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Phx-3</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Phx-3 is a potent, selective and non-toxic NHE1 inhibitor that triggers apoptosis in a variety of cancer cell lines and is highly effective in some animal tumor models.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B8-ijms-21-01110" ref-type="bibr">8</xref>
,<xref rid="B32-ijms-21-01110" ref-type="bibr">32</xref>
,<xref rid="B182-ijms-21-01110" ref-type="bibr">182</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Repurposed drugs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Phloretin, Lonidamine, Niclosamide, Docosaexaenoic acid, Salinomycin and Simvastatin have been reported to be useful in the treatment of BC because of their pH-related effects. Resveratrol also has a role as an aromatase inhibitor. (For further details, see the text).</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B8-ijms-21-01110" ref-type="bibr">8</xref>
,<xref rid="B103-ijms-21-01110" ref-type="bibr">103</xref>
,<xref rid="B226-ijms-21-01110" ref-type="bibr">226</xref>
,<xref rid="B227-ijms-21-01110" ref-type="bibr">227</xref>
,<xref rid="B228-ijms-21-01110" ref-type="bibr">228</xref>
,<xref rid="B229-ijms-21-01110" ref-type="bibr">229</xref>
,<xref rid="B230-ijms-21-01110" ref-type="bibr">230</xref>
,<xref rid="B231-ijms-21-01110" ref-type="bibr">231</xref>
,<xref rid="B232-ijms-21-01110" ref-type="bibr">232</xref>
,<xref rid="B233-ijms-21-01110" ref-type="bibr">233</xref>
,<xref rid="B234-ijms-21-01110" ref-type="bibr">234</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Metformin (MET)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MET has been introduced as an anticancer agent in BC. It induces intracellular hyperacidification in tumor xenograft models. MET has been reported to inhibit insulin and insulin/IGF-1, HIF-1α, Warburg metabolism, gene expression, angiogenesis, cancer migration, invasion and metastasis, apart from reducing the side effects of doxorubicin. MET has also been reported to act synergistically with chemotherapy and decrease its dosages, thus, its side-effects. It has also been used to target resistant cells in BC and has been considered a radio-sensitizer.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B235-ijms-21-01110" ref-type="bibr">235</xref>
,<xref rid="B236-ijms-21-01110" ref-type="bibr">236</xref>
,<xref rid="B237-ijms-21-01110" ref-type="bibr">237</xref>
,<xref rid="B238-ijms-21-01110" ref-type="bibr">238</xref>
,<xref rid="B239-ijms-21-01110" ref-type="bibr">239</xref>
,<xref rid="B240-ijms-21-01110" ref-type="bibr">240</xref>
,<xref rid="B241-ijms-21-01110" ref-type="bibr">241</xref>
,<xref rid="B242-ijms-21-01110" ref-type="bibr">242</xref>
,<xref rid="B243-ijms-21-01110" ref-type="bibr">243</xref>
,<xref rid="B244-ijms-21-01110" ref-type="bibr">244</xref>
,<xref rid="B245-ijms-21-01110" ref-type="bibr">245</xref>
,<xref rid="B246-ijms-21-01110" ref-type="bibr">246</xref>
,<xref rid="B247-ijms-21-01110" ref-type="bibr">247</xref>
,<xref rid="B248-ijms-21-01110" ref-type="bibr">248</xref>
,<xref rid="B249-ijms-21-01110" ref-type="bibr">249</xref>
,<xref rid="B250-ijms-21-01110" ref-type="bibr">250</xref>
,<xref rid="B251-ijms-21-01110" ref-type="bibr">251</xref>
,<xref rid="B252-ijms-21-01110" ref-type="bibr">252</xref>
,<xref rid="B253-ijms-21-01110" ref-type="bibr">253</xref>
,<xref rid="B254-ijms-21-01110" ref-type="bibr">254</xref>
,<xref rid="B255-ijms-21-01110" ref-type="bibr">255</xref>
]</td>
</tr>
</tbody>
</table>
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