Tumor Cell Dormancy: Threat or Opportunity in the Fight against Cancer
Identifieur interne : 000897 ( Pmc/Curation ); précédent : 000896; suivant : 000898Tumor Cell Dormancy: Threat or Opportunity in the Fight against Cancer
Auteurs : Rana Jahanban-Esfahlan [Iran] ; Khaled Seidi [Iran] ; Masoud H. Manjili [États-Unis] ; Ali Jahanban-Esfahlan [Iran] ; Tahereh Javaheri [Autriche] ; Peyman Zare [Pologne]Source :
- Cancers [ 2072-6694 ] ; 2019.
Abstract
Tumor dormancy, a clinically undetectable state of cancer, makes a major contribution to the development of multidrug resistance (MDR), minimum residual disease (MRD), tumor outgrowth, cancer relapse, and metastasis. Despite its high incidence, the whole picture of dormancy-regulated molecular programs is far from clear. That is, it is unknown when and which dormant cells will resume proliferation causing late relapse, and which will remain asymptomatic and harmless to their hosts. Thus, identification of dormancy-related culprits and understanding their roles can help predict cancer prognosis and may increase the probability of timely therapeutic intervention for the desired outcome. Here, we provide a comprehensive review of the dormancy-dictated molecular mechanisms, including angiogenic switch, immune escape, cancer stem cells, extracellular matrix (ECM) remodeling, metabolic reprogramming, miRNAs, epigenetic modifications, and stress-induced p38 signaling pathways. Further, we analyze the possibility of leveraging these dormancy-related molecular cues to outmaneuver cancer and discuss the implications of such approaches in cancer treatment.
Url:
DOI: 10.3390/cancers11081207
PubMed: 31430951
PubMed Central: 6721805
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Manjili</name><affiliation wicri:level="1"><nlm:aff id="af5-cancers-11-01207">Department of Microbiology & Immunology, VCU School of Medicine, Massey Cancer Center, Richmond, VA 23298, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology & Immunology, VCU School of Medicine, Massey Cancer Center, Richmond, VA 23298</wicri:regionArea></affiliation></author><author><name sortKey="Jahanban Esfahlan, Ali" sort="Jahanban Esfahlan, Ali" uniqKey="Jahanban Esfahlan A" first="Ali" last="Jahanban-Esfahlan">Ali Jahanban-Esfahlan</name><affiliation wicri:level="1"><nlm:aff id="af6-cancers-11-01207">Stem Cell Research Center, Tabriz University of Medical Sciences, Tabriz 9841, Iran</nlm:aff><country xml:lang="fr">Iran</country><wicri:regionArea>Stem Cell Research Center, Tabriz University of Medical Sciences, Tabriz 9841</wicri:regionArea></affiliation></author><author><name sortKey="Javaheri, Tahereh" sort="Javaheri, Tahereh" uniqKey="Javaheri T" first="Tahereh" last="Javaheri">Tahereh Javaheri</name><affiliation wicri:level="1"><nlm:aff id="af7-cancers-11-01207">Ludwig Boltzmann Institute for Cancer Research, 1090 Vienna, Austria</nlm:aff><country xml:lang="fr">Autriche</country><wicri:regionArea>Ludwig Boltzmann Institute for Cancer Research, 1090 Vienna</wicri:regionArea></affiliation></author><author><name sortKey="Zare, Peyman" sort="Zare, Peyman" uniqKey="Zare P" first="Peyman" last="Zare">Peyman Zare</name><affiliation wicri:level="1"><nlm:aff id="af8-cancers-11-01207">Faculty of Medicine, Cardinal Stefan Wyszyński University in Warsaw, 01-938 Warsaw, Poland</nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea>Faculty of Medicine, Cardinal Stefan Wyszyński University in Warsaw, 01-938 Warsaw</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31430951</idno><idno type="pmc">6721805</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6721805</idno><idno type="RBID">PMC:6721805</idno><idno type="doi">10.3390/cancers11081207</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000897</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000897</idno><idno type="wicri:Area/Pmc/Curation">000897</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000897</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Tumor Cell Dormancy: Threat or Opportunity in the Fight against Cancer</title><author><name sortKey="Jahanban Esfahlan, Rana" sort="Jahanban Esfahlan, Rana" uniqKey="Jahanban Esfahlan R" first="Rana" last="Jahanban-Esfahlan">Rana Jahanban-Esfahlan</name><affiliation wicri:level="1"><nlm:aff id="af1-cancers-11-01207">Drug Applied Research Center, Tabriz University of Medical Sciences, Tabriz 9841, Iran</nlm:aff><country xml:lang="fr">Iran</country><wicri:regionArea>Drug Applied Research Center, Tabriz University of Medical Sciences, Tabriz 9841</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-cancers-11-01207">Department of Medical Biotechnology, Faculty of Advanced Medical Sciences, Tabriz University of Medical Sciences, Tabriz 9841, Iran</nlm:aff><country xml:lang="fr">Iran</country><wicri:regionArea>Department of Medical Biotechnology, Faculty of Advanced Medical Sciences, Tabriz University of Medical Sciences, Tabriz 9841</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="af3-cancers-11-01207">Student Research Committee, Tabriz University of Medical Sciences, Tabriz 9841, Iran</nlm:aff><country xml:lang="fr">Iran</country><wicri:regionArea>Student Research Committee, Tabriz University of Medical Sciences, Tabriz 9841</wicri:regionArea></affiliation></author><author><name sortKey="Seidi, Khaled" sort="Seidi, Khaled" uniqKey="Seidi K" first="Khaled" last="Seidi">Khaled Seidi</name><affiliation wicri:level="1"><nlm:aff id="af4-cancers-11-01207">Biotechnology Research Center, Tabriz University of Medical Sciences, Tabriz 9841, Iran</nlm:aff><country xml:lang="fr">Iran</country><wicri:regionArea>Biotechnology Research Center, Tabriz University of Medical Sciences, Tabriz 9841</wicri:regionArea></affiliation></author><author><name sortKey="Manjili, Masoud H" sort="Manjili, Masoud H" uniqKey="Manjili M" first="Masoud H." last="Manjili">Masoud H. Manjili</name><affiliation wicri:level="1"><nlm:aff id="af5-cancers-11-01207">Department of Microbiology & Immunology, VCU School of Medicine, Massey Cancer Center, Richmond, VA 23298, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology & Immunology, VCU School of Medicine, Massey Cancer Center, Richmond, VA 23298</wicri:regionArea></affiliation></author><author><name sortKey="Jahanban Esfahlan, Ali" sort="Jahanban Esfahlan, Ali" uniqKey="Jahanban Esfahlan A" first="Ali" last="Jahanban-Esfahlan">Ali Jahanban-Esfahlan</name><affiliation wicri:level="1"><nlm:aff id="af6-cancers-11-01207">Stem Cell Research Center, Tabriz University of Medical Sciences, Tabriz 9841, Iran</nlm:aff><country xml:lang="fr">Iran</country><wicri:regionArea>Stem Cell Research Center, Tabriz University of Medical Sciences, Tabriz 9841</wicri:regionArea></affiliation></author><author><name sortKey="Javaheri, Tahereh" sort="Javaheri, Tahereh" uniqKey="Javaheri T" first="Tahereh" last="Javaheri">Tahereh Javaheri</name><affiliation wicri:level="1"><nlm:aff id="af7-cancers-11-01207">Ludwig Boltzmann Institute for Cancer Research, 1090 Vienna, Austria</nlm:aff><country xml:lang="fr">Autriche</country><wicri:regionArea>Ludwig Boltzmann Institute for Cancer Research, 1090 Vienna</wicri:regionArea></affiliation></author><author><name sortKey="Zare, Peyman" sort="Zare, Peyman" uniqKey="Zare P" first="Peyman" last="Zare">Peyman Zare</name><affiliation wicri:level="1"><nlm:aff id="af8-cancers-11-01207">Faculty of Medicine, Cardinal Stefan Wyszyński University in Warsaw, 01-938 Warsaw, Poland</nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea>Faculty of Medicine, Cardinal Stefan Wyszyński University in Warsaw, 01-938 Warsaw</wicri:regionArea></affiliation></author></analytic><series><title level="j">Cancers</title><idno type="eISSN">2072-6694</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Tumor dormancy, a clinically undetectable state of cancer, makes a major contribution to the development of multidrug resistance (MDR), minimum residual disease (MRD), tumor outgrowth, cancer relapse, and metastasis. Despite its high incidence, the whole picture of dormancy-regulated molecular programs is far from clear. That is, it is unknown when and which dormant cells will resume proliferation causing late relapse, and which will remain asymptomatic and harmless to their hosts. Thus, identification of dormancy-related culprits and understanding their roles can help predict cancer prognosis and may increase the probability of timely therapeutic intervention for the desired outcome. Here, we provide a comprehensive review of the dormancy-dictated molecular mechanisms, including angiogenic switch, immune escape, cancer stem cells, extracellular matrix (ECM) remodeling, metabolic reprogramming, miRNAs, epigenetic modifications, and stress-induced p38 signaling pathways. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Cancers (Basel)</journal-id><journal-id journal-id-type="iso-abbrev">Cancers (Basel)</journal-id><journal-id journal-id-type="publisher-id">cancers</journal-id><journal-title-group><journal-title>Cancers</journal-title></journal-title-group><issn pub-type="epub">2072-6694</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31430951</article-id><article-id pub-id-type="pmc">6721805</article-id><article-id pub-id-type="doi">10.3390/cancers11081207</article-id><article-id pub-id-type="publisher-id">cancers-11-01207</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Tumor Cell Dormancy: Threat or Opportunity in the Fight against Cancer</article-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-5119-252X</contrib-id><name><surname>Jahanban-Esfahlan</surname><given-names>Rana</given-names></name><xref ref-type="aff" rid="af1-cancers-11-01207">1</xref><xref ref-type="aff" rid="af2-cancers-11-01207">2</xref><xref ref-type="aff" rid="af3-cancers-11-01207">3</xref><xref ref-type="author-notes" rid="fn1-cancers-11-01207">†</xref></contrib><contrib contrib-type="author"><name><surname>Seidi</surname><given-names>Khaled</given-names></name><xref ref-type="aff" rid="af4-cancers-11-01207">4</xref><xref ref-type="author-notes" rid="fn1-cancers-11-01207">†</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-7511-2953</contrib-id><name><surname>Manjili</surname><given-names>Masoud H.</given-names></name><xref ref-type="aff" rid="af5-cancers-11-01207">5</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-8693-3837</contrib-id><name><surname>Jahanban-Esfahlan</surname><given-names>Ali</given-names></name><xref ref-type="aff" rid="af6-cancers-11-01207">6</xref></contrib><contrib contrib-type="author"><name><surname>Javaheri</surname><given-names>Tahereh</given-names></name><xref ref-type="aff" rid="af7-cancers-11-01207">7</xref><xref ref-type="author-notes" rid="fn2-cancers-11-01207">‡</xref><xref rid="c1-cancers-11-01207" ref-type="corresp">*</xref></contrib><contrib contrib-type="author"><name><surname>Zare</surname><given-names>Peyman</given-names></name><xref ref-type="aff" rid="af8-cancers-11-01207">8</xref><xref rid="c1-cancers-11-01207" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-cancers-11-01207"><label>1</label>Drug Applied Research Center, Tabriz University of Medical Sciences, Tabriz 9841, Iran</aff><aff id="af2-cancers-11-01207"><label>2</label>Department of Medical Biotechnology, Faculty of Advanced Medical Sciences, Tabriz University of Medical Sciences, Tabriz 9841, Iran</aff><aff id="af3-cancers-11-01207"><label>3</label>Student Research Committee, Tabriz University of Medical Sciences, Tabriz 9841, Iran</aff><aff id="af4-cancers-11-01207"><label>4</label>Biotechnology Research Center, Tabriz University of Medical Sciences, Tabriz 9841, Iran</aff><aff id="af5-cancers-11-01207"><label>5</label>Department of Microbiology & Immunology, VCU School of Medicine, Massey Cancer Center, Richmond, VA 23298, USA</aff><aff id="af6-cancers-11-01207"><label>6</label>Stem Cell Research Center, Tabriz University of Medical Sciences, Tabriz 9841, Iran</aff><aff id="af7-cancers-11-01207"><label>7</label>Ludwig Boltzmann Institute for Cancer Research, 1090 Vienna, Austria</aff><aff id="af8-cancers-11-01207"><label>8</label>Faculty of Medicine, Cardinal Stefan Wyszyński University in Warsaw, 01-938 Warsaw, Poland</aff><author-notes><corresp id="c1-cancers-11-01207"><label>*</label>Correspondence: <email>Tahereh.Javaheri@lbicr.lbg.ac.at</email> (T.J.); <email>Peymanzare33@gmail.com</email> (P.Z.)</corresp><fn id="fn1-cancers-11-01207"><label>†</label><p>These authors contributed equally.</p></fn><fn id="fn2-cancers-11-01207"><label>‡</label><p>The author is no longer in this institution.</p></fn></author-notes><pub-date pub-type="epub"><day>19</day><month>8</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>8</month><year>2019</year></pub-date><volume>11</volume><issue>8</issue><elocation-id>1207</elocation-id><history><date date-type="received"><day>31</day><month>7</month><year>2019</year></date><date date-type="accepted"><day>13</day><month>8</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 by the authors.</copyright-statement><copyright-year>2019</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>Tumor dormancy, a clinically undetectable state of cancer, makes a major contribution to the development of multidrug resistance (MDR), minimum residual disease (MRD), tumor outgrowth, cancer relapse, and metastasis. Despite its high incidence, the whole picture of dormancy-regulated molecular programs is far from clear. That is, it is unknown when and which dormant cells will resume proliferation causing late relapse, and which will remain asymptomatic and harmless to their hosts. Thus, identification of dormancy-related culprits and understanding their roles can help predict cancer prognosis and may increase the probability of timely therapeutic intervention for the desired outcome. Here, we provide a comprehensive review of the dormancy-dictated molecular mechanisms, including angiogenic switch, immune escape, cancer stem cells, extracellular matrix (ECM) remodeling, metabolic reprogramming, miRNAs, epigenetic modifications, and stress-induced p38 signaling pathways. Further, we analyze the possibility of leveraging these dormancy-related molecular cues to outmaneuver cancer and discuss the implications of such approaches in cancer treatment.</p></abstract><kwd-group><kwd>tumor dormancy</kwd><kwd>tumor relapse</kwd><kwd>tumor escape</kwd><kwd>metastasis</kwd><kwd>cancer therapy</kwd></kwd-group></article-meta></front><floats-group><fig id="cancers-11-01207-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>The implication of the immune system in tumor cell dormancy.</p></caption><graphic xlink:href="cancers-11-01207-g001"></graphic></fig><fig id="cancers-11-01207-f002" orientation="portrait" position="float"><label>Figure 2</label><caption><p>The implication of ECM and p38 signaling in tumor dormancy.</p></caption><graphic xlink:href="cancers-11-01207-g002"></graphic></fig><fig id="cancers-11-01207-f003" orientation="portrait" position="float"><label>Figure 3</label><caption><p>Tumor dormancy as a therapeutic opportunity to fight cancer back.</p></caption><graphic xlink:href="cancers-11-01207-g003"></graphic></fig><table-wrap id="cancers-11-01207-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-11-01207-t001_Table 1</object-id><label>Table 1</label><caption><p>Molecular cues involved in tumor cell dormancy.</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">Dormancy Factor</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Mode</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Major Findings</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref</th></tr></thead><tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Angiostatin</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of angiogenic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Upregulation of Angiostatin drive long-term dormancy of primary tumors, inhibit tumor growth, and reduce cancer metastases.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B31-cancers-11-01207" ref-type="bibr">31</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Thrombospondin-1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of angiogenic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Overexpression of Thrombospondin-1 inhibits melanoma angiogenesis, lung colonization, and spontaneous pulmonary metastasis.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B32-cancers-11-01207" ref-type="bibr">32</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEGF/VPF121</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of angiogenic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Overexpression of VEGF/VPF121 result in tumor growth and escape from dormancy.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B33-cancers-11-01207" ref-type="bibr">33</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">(VEGF(121)<break></break>VEGF(165) overexpression</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of angiogenic dormancy</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">The level and VEGF isoforms determine the fate of aggressive tumor growth vs. nontumorigenic and dormant tumor.</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B34-cancers-11-01207" ref-type="bibr">34</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VEGF(189)<break></break>overexpression</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of angiogenic dormancy</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Thrombospondin-1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of angiogenic dormancy</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Endothelial-derived Thrombospondin-1 induces long-lasting BCC dormancy. This repressive nod is lost in sprouting neovasculature where active TGFβ1 and periostin act as tumor-promoting factors derived from endothelial tip cells.</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B35-cancers-11-01207" ref-type="bibr">35</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TGFβ1, Periostin</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of angiogenic dormancy</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Thrombospondin, Angiomotin, Tropomyosin, TGF-β2, P4HA1, EphA5, H2BK, IGFBP-5</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of angiogenic dormancy</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Dormant tumors undergo a stable genetic reprogramming during their switch to the fast-growing phenotype by downregulation of angiogenesis inhibitors such as Thrombospondin and decreased the sensitivity of angiogenic tumors to angiostatin along with upregulation of angiogenesis-related genes.</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B36-cancers-11-01207" ref-type="bibr">36</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">EGFR-1, IGF-IR, CD73, PI3K, ESM-1, PIK3CB, TIMP-3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of angiogenic dormancy</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MME1(NM23)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of angiogenic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NM23 inhibits EGF-induced cell migration. Increase the expression of metastasis-related genes TIMP-1, E-Cadherin and β-Catenin, reduce the expression of VEGR, CD44V6, and MMP-2 and reduce metastasis.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B37-cancers-11-01207" ref-type="bibr">37</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Kai-1 (CD82)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of angiogenic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Binding of tumor cell surface-expressed Kai1 with endothelial DARC inhibit tumor cell proliferation, induce senescence by modulating the expression of TBX2 and p21 and suppress metastasis.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B38-cancers-11-01207" ref-type="bibr">38</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">BRMS1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of angiogenic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">BRMS1 inhibits angiogenesis through blocking NF/KB activity. It can also reduce metastatic potential but not tumorigenicity.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B39-cancers-11-01207" ref-type="bibr">39</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HSP27</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of angiogenic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Downregulation of HSP27 associated with reduced endothelial cell proliferation and decreased secretion of VEGF-A, VEGF-C, and induction of long-term dormancy.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B40-cancers-11-01207" ref-type="bibr">40</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CTL response, MHC class I, NK cells</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of immunologic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">An activate CTL response can maintain immune equilibrium with metastatic dormant cells. Immune dormancy arrest cancer cell growth and promotes angiogenic control.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B41-cancers-11-01207" ref-type="bibr">41</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">B7-H1 and B7.1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of immunologic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Dormant tumor cells up-regulate B7-H1 and B7.1 and resist CTL-mediated lysis.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B42-cancers-11-01207" ref-type="bibr">42</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Macrophage (MΦs)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor/inducer of immunologic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">By forming gap junctional interactions with CSCs, the M2 MΦs promote cycling quiescence and carboplatin resistance. M1 MΦ-derived exosomes activated NFкB to reverse quiescent BCCs to cycling cells in vivo.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B43-cancers-11-01207" ref-type="bibr">43</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Neutrophils</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of immunologic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">14,15-EET trigger neutrophil infiltration in metastatic lesions by activating STAT3/JNK-hIL-8/mCXCL15 and mir-155 which converts tumor-suppressing function of neutrophils to tumor-promoting in vivo.<break></break>In the presence of G-CSF/IL-6, 14,15-EET enhance STAT3 activation in neutrophils to decrease TRAIL expression and increase MMP-9 expression to induce angiogenesis during dormant micrometastases growth.<break></break>Neutrophil depletion or blocking hIL-8/mCXCL15 abrogate micrometastases induced by 14,15-EET.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B44-cancers-11-01207" ref-type="bibr">44</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Zeb1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of immunologic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inflammation triggers Zeb1 to promote EMT and give rise to metastatic outgrowth.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B45-cancers-11-01207" ref-type="bibr">45</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TNFα, IL-β</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of immunologic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Addition of bone remodeling cytokines, TNFα, and IL-β to dormant cancer cells induce proliferation and occurrence of latent bone metastasis.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B46-cancers-11-01207" ref-type="bibr">46</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SOCS1, IL-3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of immunologic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">T-cell inactivation and resistance to apoptosis are mediated by methylation of SOCS1, deregulation of JAK/STAT and overproduction of IL-3 by dormant cells.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B47-cancers-11-01207" ref-type="bibr">47</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IFN-γ</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of immunologic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IFN-γ signaling triggers differentiated tumor cell apoptosis via STAT1; however, when IDO1 and AhR are overexpressed as in DTCs, IFN-gamma induces p27 via IDO1/AhR and inhibits STAT1 signaling, and favors dormancy state.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B48-cancers-11-01207" ref-type="bibr">48</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">LPS/EGF</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of immunologic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Activated immune/stromal cells stimulate the resident hepatic cells to derive tumor growth.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B9-cancers-11-01207" ref-type="bibr">9</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mitochondrial dysfunction</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of metabolic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VLX600 impairs OXPHOS and drives a HIF-1α-dependent switch to glycolysis, which this metabolic pathway can’t meet the energy demands of tumor cells, thus induction of autophagy is unavoidable. Yet, due to lack of HIF-1α-stabilization and glucose inaccessibility in metabolically stressed environments, shifting to glycolysis mode will be restricted, consequently, tumor cells undergo apoptosis.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B11-cancers-11-01207" ref-type="bibr">11</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">LACTB</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of metabolic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mitochondrial tumor suppressor, LACTB potently inhibits the proliferation of BC cells via altering mitochondrial lipid metabolism and differentiation of BC cells by reduction of the levels of mitochondrial phosphatidylserine decarboxylase, which is involved in the synthesis of mitochondrial phosphatidylethanolamine.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B49-cancers-11-01207" ref-type="bibr">49</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">FA metabolism, ROS, oxidative DNA damage</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of metabolic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Residual cells display altered lipid metabolism, elevated ROS, and increased oxidative DNA damage. Thus, lipid metabolism and ROS are therapeutic targets for reducing tumor recurrence in BC patients.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B50-cancers-11-01207" ref-type="bibr">50</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NR2F1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of hypoxic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Hypoxic HNSCC and breast primary tumor microenvironments display upregulation of key dormancy (NR2F1, DEC2, p27) and hypoxia (GLUT1, HIF1α) genes. Post-hypoxic DTCs were frequently NR2F1<sup>hi</sup>/DEC2<sup>hi</sup>/p27<sup>hi</sup>/TGFβ2<sup>hi</sup>, dormant and chemotherapy-resistant.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B51-cancers-11-01207" ref-type="bibr">51</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">LIFR</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of hypoxic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">In BC patients with bone metastases, low LIFR levels negatively correlate with HIF-1α activity and disease outcome. Hypoxia reduces the LIFR: STAT3: SOCS3 signaling in BC cells. Loss of the LIFR or STAT3 reactivates dormant BC cells to proliferate and to downregulate stem cell-related genes and specifically benefit their bone colonization.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B52-cancers-11-01207" ref-type="bibr">52</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">E6/E7 antigen</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of hypoxic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Human papillomavirus-infected cancer cells can enter into reversible dormancy state, with reducing the synthesis of viral antigen and enhanced therapeutic resistance, and uphold tumor recurrence upon reoxygenation.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B53-cancers-11-01207" ref-type="bibr">53</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Kiss-1, CRSP3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Kiss-1 expression suppresses malignant melanoma metastasis, inhibits motility, chemotaxis, and invasion, perhaps by suppressing the expression of MMP-9. CRSP3 regulate the transcriptional expression of Kiss-1.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B54-cancers-11-01207" ref-type="bibr">54</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Type I collagen (Col-I)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Atypical tetraspanin TM4SF1 as a potent inducer of metastatic recurrence of BC couples DDR1 to PKCα. This kinase activates JAK2. Then, JAK2/STAT3 activates the expression of SOX2 and NANOG, maintain the manifestation of CSC traits, and fuel metastatic recurrence in the bone, lung, and brain.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B55-cancers-11-01207" ref-type="bibr">55</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fibronectin</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fibronectin/β1 Integrin/MLCK axis induces a transition from a quiescent to proliferative, metastatic outgrowth.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B56-cancers-11-01207" ref-type="bibr">56</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Col-I</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Col-I/β1 Integrin/SRC/FAK/ERK/MLCK signaling induce dormant cells to switch to proliferative metastatic lesions.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B57-cancers-11-01207" ref-type="bibr">57</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">u-PAR</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">u-PAR, is an essential molecule in BM disseminated tumor cells for long-standing survival during dormancy by regulation of u-PAR of α5β1 integrins, and signal propagation from Fibronectin through the p38, ERK, and EGF-receptor signaling.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B58-cancers-11-01207" ref-type="bibr">58</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">FAK, Src, MEK1/2 (ERK1/2)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Targeting Src prevents the proliferative response of dormant cells to external stimuli. MEK1/2 inhibition suppresses their survival and eliminates tumor relapse.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B59-cancers-11-01207" ref-type="bibr">59</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">KRAS/C-Myc, IGF1/AKT</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">KRAS/C-Myc negative dormant cells represent an increase in autocrine IGF1/AKT. Inhibition of IGF-1R reduces residual disease burden and cancer recurrence.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B60-cancers-11-01207" ref-type="bibr">60</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TGFB2</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cellular adhesion promotes PC cells to escape from dormancy and lethal metastasis. The mechanism involves downregulation of TGFB2, E2F4, and upregulation of MLCK, CDK6.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B61-cancers-11-01207" ref-type="bibr">61</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DIRAS family GTPase 3 (DIRAS3)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DIRAS3 decrease ERK/AKT signaling and induce autophagy. Addition of VEGF, IGF-1, and IL-8 abrogate sustaining autophagic DIRAS3-induced dormancy. A combination of antibodies targeting VEGF, IGF-1, and IL-8 prevent outgrowth of dormant cells.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B62-cancers-11-01207" ref-type="bibr">62</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Aurora kinase A (AURKA)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Activation of URKA-Erk1/2 signaling pathway induces chemotherapy resistance and promote metastasis of laryngeal squamous cell carcinoma.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B63-cancers-11-01207" ref-type="bibr">63</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fbxw7</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Dormant breast cancer cells overexpress Fbxw7, which acts as the negative control of cell cycle and its disruption avoids entry of dormant cells into the quiescent state, rendering them sensitive to chemotherapy.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B64-cancers-11-01207" ref-type="bibr">64</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Wnt5a</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Wnt5a/ROR2/SIAH2 signaling axis is involved in the induction and maintenance of PCa cells dormancy in the bone.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B65-cancers-11-01207" ref-type="bibr">65</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TGFβ2/ GDF10</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Osteoblast-secreted proteins induce TGFβRIII-p38MAPK-pS249/T252RB pathway to mediate dormancy of metastatic PC in the bone.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B66-cancers-11-01207" ref-type="bibr">66</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Axl, Gas6</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Axl is a tyrosine kinase receptor for growth arrest-specific 6 (Gas6). Axl and Gas6 are required for TGF-β2-induced dormancy of PC cells in the bone marrow.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B67-cancers-11-01207" ref-type="bibr">67</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">E-selectin, SDF-1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Proliferating and dormant BCCs inhabit different regions, whereas E-selectin interactions allow BCC residency in the BM, the SDF-1/CXCR4 binding anchors BCCs to the metastatic niche. Blocking CXCR4 (SDF receptor) and E-selectin eliminates latent micrometastases residing in supportive bone, excising occurrence of relapsed disease.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B68-cancers-11-01207" ref-type="bibr">68</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MED12</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of ECM dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">The lack of MED12 induces tumor cell dormancy. Re-expression of MED12 abrogates tumor cell dormancy by positively controlling EGFR expression.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B69-cancers-11-01207" ref-type="bibr">69</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N-cadherin</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of CSC dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N-cadherin upregulation leads to downregulation of E-cadherin, upregulation of Connexin, EMT, and dormancy.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B70-cancers-11-01207" ref-type="bibr">70</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Notch</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of CSC dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Notch remain activated in dormant residual cells and accelerates tumor recurrence.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B71-cancers-11-01207" ref-type="bibr">71</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD13</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of CSC dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD13 is a cancer stem cell dormancy marker in HCC.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B72-cancers-11-01207" ref-type="bibr">72</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Coco</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of CSC dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Coco enhances cancer stem cell traits and antagonizes TGF-β activity. Coco reactivates dormant BC cells in the lung whereas BMP signaling revives metastasis dormancy in the lung.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B73-cancers-11-01207" ref-type="bibr">73</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">BMP7</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of CSC dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Bone stromal cells-derived BMP7 stimulates senescence in prostate CSCs by activating BMP7-BMPR2/p38/p21/NDRG1 axis.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B74-cancers-11-01207" ref-type="bibr">74</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SPARC</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of CSC dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SPARC demethylation (activation) significantly stimulate the expression of BMP7 in bone marrow stromal cells and is required for BMP7 mediated stemness and senescence of PC cells.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B75-cancers-11-01207" ref-type="bibr">75</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SOX2</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of CSC dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Low level of SOX2 expression is required for DTCs maintenance. SOX2 complete depletion of SOX results in activation of STAT3-p53-caspase axis and induction of cell apoptosis.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B76-cancers-11-01207" ref-type="bibr">76</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HMGA1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of CSC dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HMGA1 reprogram triple-negative BC cells to a stem-like state, driving their metastatic outgrowth. HMGA1 silencing excise cancer stem/initiator cells and prevents oncogenesis.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B77-cancers-11-01207" ref-type="bibr">77</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TBK1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of CSC dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC cells target the HSC niche in mouse bone marrow during metastasis. Interaction with niche osteoblasts activate TBK1 expression and inhibit mTOR in PCa cells. Silencing TBK1 dampen drug resistance and formation of PCa stem-like cells.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B78-cancers-11-01207" ref-type="bibr">78</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">p53, Necdin</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of CSC Dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Necdin-knock out adult HSCs is more proliferative and less quiescent than wild-type HSCs, indicating that Necdin resembles p53 function in supporting HSC dormancy during stable conditions.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B19-cancers-11-01207" ref-type="bibr">19</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PRRX1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of CSC Dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PRRX1 positively controls dormancy through TGF-β and promoting EMT in HNSCC and its activity is correlated with low expression of miR-642b-3p and TGF-β2 and p38.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B79-cancers-11-01207" ref-type="bibr">79</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Zeb1, G9a, SMAD5, SMARCD3,</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of Epigenetic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">These genes control EMT and control dormancy by reversible activation of stem cell-like properties of breast cancer cells in vitro.</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B80-cancers-11-01207" ref-type="bibr">80</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">KAT5, DOT1L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of epigenetic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">These genes are involved in MET, promoting epithelial morphologies and thus reduce invasive properties of breast cancer cells in vitro.</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PCL1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of epigenetic dormancy</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">PCL2 and PCL3 are expressed in proliferative tumor state, whereas PCL1 mainly expressed in dormant cells.</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B81-cancers-11-01207" ref-type="bibr">81</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PCL2,3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of epigenetic dormancy</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NR2F1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of epigenetic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NR2F1 is epigenetically upregulated in tumors and induce dormancy by global chromatin repression.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B82-cancers-11-01207" ref-type="bibr">82</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MSK1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of epigenetic dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MSK1 epigenetically controls the differentiation of cancer cells and its expression promotes metastatic dormancy.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B83-cancers-11-01207" ref-type="bibr">83</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-222/223</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of Dmir dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Promotes quiescence and drug resistance.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B84-cancers-11-01207" ref-type="bibr">84</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-34a, miR-93, miR-200c</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of Dmir dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Loss of DmiRNAs happens during the transition from avascular dormant into angiogenic fast-growing phenotype.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B85-cancers-11-01207" ref-type="bibr">85</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mir16/19, miR-580, 588 or 190</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of Dmir dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Dmirs govern tumor dormancy, especially miR-190 induce long-lasting dormancy in glioblastomas and osteosarcomas.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B17-cancers-11-01207" ref-type="bibr">17</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-100-5p</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of Dmir dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-100-5p inhibition induces apoptosis in dormant PC cells and prevents the emergence of castration-resistant PC.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B86-cancers-11-01207" ref-type="bibr">86</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-200b/200a/429</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of Dmir dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Expression of these Dmirs induce tumor cell dormancy and inhibit lung metastasis of BCCs.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B87-cancers-11-01207" ref-type="bibr">87</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-125b</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of Dmir dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Its expression favors epithelial phenotype, reduces Wnt-associated stem cell signaling and mesenchymal-associated genes and thus reduce metastasis of BCCs to the bone.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B88-cancers-11-01207" ref-type="bibr">88</xref>]</td></tr><tr><td rowspan="10" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">p38 Signaling</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">p38 <sup>Up</sup>, ERK <sup>down</sup> leads to tumor dormancy.</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B89-cancers-11-01207" ref-type="bibr">89</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">p38<sup>down</sup>/ERK<sup>up</sup> leads to mitogenesis.</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">p38/BiP/PERK axis promotes drug resistance and survival of quiescent cells. BiP up-regulation averts Bax activation.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B90-cancers-11-01207" ref-type="bibr">90</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">p38 induces dormancy by expression of p53 and BHLHB3 while inhibiting c-Jun and FoxM1.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B91-cancers-11-01207" ref-type="bibr">91</xref>] </td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MKK6 and p38α/β induce survival by regulating nuclear translocation and transcriptional activation of ATF6α in dormant cancer cells.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B92-cancers-11-01207" ref-type="bibr">92</xref>] </td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TGF-β2-MAPK p38α/β-(ERK/p38) (low)- DEC2/SHARP1, p27, ↓CDK4, and dormancy of malignant DTCs.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B93-cancers-11-01207" ref-type="bibr">93</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">˧MERTK, the ↓ratio of P-Erk1/2 to P-p38, ↑ p27, NR2F1, SOX2, and NANOG, ↑histone H3K9me3 and H3K27me3, G1/G0 arrest and dormancy.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B94-cancers-11-01207" ref-type="bibr">94</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MKK4 activates MAPK, p38 and JNK, up-regulate p21 and induce cancer cell growth arrest.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B95-cancers-11-01207" ref-type="bibr">95</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MKK6 activates MAPK and p38.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B95-cancers-11-01207" ref-type="bibr">95</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inducer of stress-induced dormancy</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MKK7 activates MAPK and JNK.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B96-cancers-11-01207" ref-type="bibr">96</xref>]</td></tr></tbody></table><table-wrap-foot><fn><p><italic>Abbreviations</italic>: N-myc downstream-regulated gene 1 (NDRG1); BMP receptor 2 (BMPR2); indolamine 2,3-dioxygenase 1 (IDO1)-kynurenine (Kyn)-aryl hydrocarbon receptor (AhR) (IDO1/AhR); bone morphogenetic protein 7 (BMP7); N-myc downstream-regulated gene 1 (NDRG1); secreted protein acidic and rich in cysteine (SPARC); high mobility group A1 (HMGA1); polycomb-like proteins 1-3 (PCL1-3); protein kinase-like ER kinase (PERK); urokinase plasminogen activator receptor (uPAR); breast-cancer metastasis suppressor 1 (BRMS1); mammalian target of rapamycin (mTOR); Janus-activated kinase/signal transducers and activators of transcription (JAK/STAT); suppressor of cytokine signaling (SOCS); IL-6 cytokine leukaemia inhibitory factor (LIFR); transforming growth factor β2 (TGF-β2); proline hydroxylase I (P4HA1); Eph receptor A5 (EphA5); histone H2BK; insulin-like growth factor binding protein 5 (IGFBP-5); epithelial growth factor receptor (EGFR)-1; insulin-like growth factor type I receptor (IGF-IR); 5′-Ecto-nucleotidase (CD73); endothelial cell–specific molecule 1 (ESM-1); phosphatidylinositol 3-kinase PI3K (PIK3); tissue inhibitor of metalloproteinase-3 (TIMP-3). The RNA polymerase II transcriptional mediator subunit 12 (MED12). ˧ denotes suppression, ↑ denotes upregulation, ↓ denotes downregulation.</p></fn></table-wrap-foot></table-wrap><table-wrap id="cancers-11-01207-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-11-01207-t002_Table 2</object-id><label>Table 2</label><caption><p>Clinical trials targeting persistent DTCs residing in the protective BM niche.</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">Trial Name</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Phase</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">ClinicalTrials.gov<break></break>Identifier</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Anti- Dormancy Strategy</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Targeting Agent</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">End-Point</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Results</th></tr></thead><tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Secondary adjuvant treatment for patients with isolated tumor cells in bone marrow</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">II</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NCT00248703</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Addition of docetaxel in the adjuvant treatment to reduces the risk of persistent DTCs</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">docetaxel</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Disease-free survival by DTC status; DTC number in BM aspirate</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DTC eradication in 79% of patients; enhanced metastasis-free survival</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CLEVER pilot trial: A phase II pilot trial of hydroxychloroquine, everolimus or the combination for prevention of recurrent breast cancer</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">II</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NCT03032406 </td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Target persistent DTCs following standard of care treatment in breast cancer patients</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">hydroxychloroquine, everolimus or combination</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Number of adverse events; DTC number in BM aspirate</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N/A</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Zoledronic acid in the treatment of breast cancer with minimal residual disease in the bone marrow (MRD-1)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">II</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NCT00172068</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibitor of bone resorption; interrupt dormancy state of DTCs</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">zoledronic acid + calcium/vitamin D</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Reduction of detected tumor cells in BM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N/A</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">A phase Ib/II trial of gedatolisib, hydroxychloroquine or the combination of prevention of recurrent breast cancer (GLACIER)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Ib/II</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CT03400254 </td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Target persistent DTCs following standard of care treatment in breast cancer patients</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">hydroxychloroquine, gedatolisib or combination</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DTC number in BM aspirate</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N/A</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">A pilot study to evaluate the impact of denosumab on disseminated tumor cells in patients with early-stage breast cancer</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">II</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NCT01545648 </td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Interrupt immunological dormancy by blocking RNKL overexpression by DTCs which foster the production of chronic inflammatory cytokines.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">denosumab </td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">DTC number in BM aspirate</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N/A</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">A pilot study of mobilization and treatment of disseminated tumor cells in men with metastatic prostate cancer</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">I</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NCT02478125</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Anti-CXCR4 strategy can be used to mobilize and target persistent DTCs</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">burixafor hydrobromide, G-CSF, docetaxel, or combination</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CTC number in peripheral blood; HSC number in peripheral blood; PSA response, safety</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N/A</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">A pilot study of the combination of 5-azacitidine (5-AZA) and all-trans retinoic acid (ATRA) for prostate cancer (PCa) with PSA only recurrence after definitive local treatment</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">II</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NCT03572387</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Reprogramming therapy in patients with recurrent PCa based on rising PSA only.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Combination of 5-azacitidine and alltrans retinoic acid, and lupron</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Disease progression-free rate, Percentage of adverse events by grade, time to tumor progression, measurement of dormancy markers TGF-β2, BMP7, BMP4, GAS6, retinoic acid and NR2F1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N/A</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Effect of trastuzumab on disease-free survival in early-stage HER2-negative breast cancer patients with ERBB2 expressing disseminated tumor cells</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">II</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NCT01779050</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Targeted trastuzumab therapy to eliminate HER2 expressing disseminated tumor cells in BM. </td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">doxorubicin, trastuzumab, cyclophosphamide, paclitaxel, epirubicin, docetaxel, carboplatin, fluorouracil, and combination</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Elimination of ERBB2-positive DTCs from BM. 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