Inactivation of miR-34a by aberrant CpG methylation in Kazakh patients with esophageal carcinoma
Identifieur interne : 001132 ( Ncbi/Merge ); précédent : 001131; suivant : 001133Inactivation of miR-34a by aberrant CpG methylation in Kazakh patients with esophageal carcinoma
Auteurs : Xiaobin Cui [République populaire de Chine] ; Zhimin Zhao [République populaire de Chine] ; Dong Liu [République populaire de Chine] ; Tao Guo [République populaire de Chine] ; Su Li [République populaire de Chine] ; Jianming Hu [République populaire de Chine] ; Chunxia Liu [République populaire de Chine] ; Lan Yang [République populaire de Chine] ; Yuwen Cao [République populaire de Chine] ; Jinfang Jiang [République populaire de Chine] ; Weihua Liang [République populaire de Chine] ; Wei Liu [République populaire de Chine] ; Shugang Li [République populaire de Chine] ; Lianghai Wang [République populaire de Chine] ; Lidong Wang [République populaire de Chine] ; Wenyi Gu [Australie] ; Chuanyue Wu [République populaire de Chine, États-Unis] ; Yunzhao Chen [République populaire de Chine] ; Feng Li [République populaire de Chine]Source :
- Journal of Experimental & Clinical Cancer Research : CR [ 0392-9078 ] ; 2014.
Abstract
Esophageal squamous cell carcinoma (ESCC) is an aggressive tumor with dismal prognosis and high incidence and mortality in Kazakh population. MiR-34a, a direct p53 target gene, possesses tumor-suppressive properties as they mediate apoptosis, cell cycle arrest, and senescence. The reduced expression of miR-34a by methylation in various cancers has been reported.
To determine whether aberrant miR-34a methylation occurs in esophageal cancer, the DNA methylation of 23 CpGs sites in the miR-34a promoter was quantitatively analyzed in relation to the translation initiation site by MALDI -TOF mass spectrometry in 59 ESCC tissues and 34 normal tissues from the Kazakh population. Real-time PCR was used to detect the inhibition of miR-34a expression levels and to evaluate their association with methylation.
We found that miR-34a is more frequently methylated in ESCC (0.133 ± 0.040) than in controls (0.066 ± 0.045, P < 0.01). A nearly two-fold increase in miR-34a expression for the hypomethylated promoter was found in normal esophageal tissues than ESCC with hypermethylation (P <0.0001), pointing to a negative relationship between miR-34a CpG sites methylation and expression(r = −0.594, P = 0.042). The hypermethylation of miR-34a CpG_8.9 was associated with the advanced UICC stage III/IV of the esophageal cancers, and the hypermethylation of CpG_8.9 and CpG_5 of miR-34a was significantly correlated with lymph node metastasis.
Our findings suggest that miR-34a is involved in the etiology of ESCC and that hypermethylated miR-34a is a potential biomarker for ESCC diagnosis and prognosis. Moreover, targeting miR-34a methylation by demethylating agents may offer a novel strategy for anticancer therapy of ESCC.
Url:
DOI: 10.1186/1756-9966-33-20
PubMed: 24528540
PubMed Central: 3931274
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<affiliation wicri:level="1"><nlm:aff id="I1">Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002</wicri:regionArea>
<wicri:noRegion>Xinjiang 832002</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Jiang, Jinfang" sort="Jiang, Jinfang" uniqKey="Jiang J" first="Jinfang" last="Jiang">Jinfang Jiang</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002</wicri:regionArea>
<wicri:noRegion>Xinjiang 832002</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Liang, Weihua" sort="Liang, Weihua" uniqKey="Liang W" first="Weihua" last="Liang">Weihua Liang</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002</wicri:regionArea>
<wicri:noRegion>Xinjiang 832002</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Liu, Wei" sort="Liu, Wei" uniqKey="Liu W" first="Wei" last="Liu">Wei Liu</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002</wicri:regionArea>
<wicri:noRegion>Xinjiang 832002</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Li, Shugang" sort="Li, Shugang" uniqKey="Li S" first="Shugang" last="Li">Shugang Li</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002</wicri:regionArea>
<wicri:noRegion>Xinjiang 832002</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Wang, Lianghai" sort="Wang, Lianghai" uniqKey="Wang L" first="Lianghai" last="Wang">Lianghai Wang</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002</wicri:regionArea>
<wicri:noRegion>Xinjiang 832002</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Wang, Lidong" sort="Wang, Lidong" uniqKey="Wang L" first="Lidong" last="Wang">Lidong Wang</name>
<affiliation wicri:level="1"><nlm:aff id="I3">Henan Key Laboratory for Esophageal Cancer, Zhengzhou University School of Medicine, Zhengzhou, Henan 450001, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Henan Key Laboratory for Esophageal Cancer, Zhengzhou University School of Medicine, Zhengzhou, Henan 450001</wicri:regionArea>
<wicri:noRegion>Henan 450001</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Gu, Wenyi" sort="Gu, Wenyi" uniqKey="Gu W" first="Wenyi" last="Gu">Wenyi Gu</name>
<affiliation wicri:level="1"><nlm:aff id="I4">Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane QLD 4072, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane QLD 4072</wicri:regionArea>
<wicri:noRegion>Brisbane QLD 4072</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Wu, Chuanyue" sort="Wu, Chuanyue" uniqKey="Wu C" first="Chuanyue" last="Wu">Chuanyue Wu</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002</wicri:regionArea>
<wicri:noRegion>Xinjiang 832002</wicri:noRegion>
</affiliation>
<affiliation wicri:level="4"><nlm:aff id="I5">Department of Pathology, University of Pittsburgh, Pittsburgh, PA 15261, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Pathology, University of Pittsburgh, Pittsburgh, PA 15261</wicri:regionArea>
<placeName><region type="state">Pennsylvanie</region>
<settlement type="city">Pittsburgh</settlement>
</placeName>
<orgName type="university">Université de Pittsburgh</orgName>
</affiliation>
</author>
<author><name sortKey="Chen, Yunzhao" sort="Chen, Yunzhao" uniqKey="Chen Y" first="Yunzhao" last="Chen">Yunzhao Chen</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002</wicri:regionArea>
<wicri:noRegion>Xinjiang 832002</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Li, Feng" sort="Li, Feng" uniqKey="Li F" first="Feng" last="Li">Feng Li</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002</wicri:regionArea>
<wicri:noRegion>Xinjiang 832002</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="I2">Department of Oncology, Tongji Hospital, Huazhong University of Science and Technology, Wuhan, Hubei 430030, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Oncology, Tongji Hospital, Huazhong University of Science and Technology, Wuhan, Hubei 430030</wicri:regionArea>
<wicri:noRegion>Hubei 430030</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series><title level="j">Journal of Experimental & Clinical Cancer Research : CR</title>
<idno type="ISSN">0392-9078</idno>
<idno type="eISSN">1756-9966</idno>
<imprint><date when="2014">2014</date>
</imprint>
</series>
</biblStruct>
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</teiHeader>
<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>Esophageal squamous cell carcinoma (ESCC) is an aggressive tumor with dismal prognosis and high incidence and mortality in Kazakh population. MiR-34a, a direct p53 target gene, possesses tumor-suppressive properties as they mediate apoptosis, cell cycle arrest, and senescence. The reduced expression of miR-34a by methylation in various cancers has been reported.</p>
</sec>
<sec><title>Methods</title>
<p>To determine whether aberrant miR-34a methylation occurs in esophageal cancer, the DNA methylation of 23 CpGs sites in the miR-34a promoter was quantitatively analyzed in relation to the translation initiation site by MALDI -TOF mass spectrometry in 59 ESCC tissues and 34 normal tissues from the Kazakh population. Real-time PCR was used to detect the inhibition of miR-34a expression levels and to evaluate their association with methylation.</p>
</sec>
<sec><title>Results</title>
<p>We found that miR-34a is more frequently methylated in ESCC (0.133 ± 0.040) than in controls (0.066 ± 0.045, P < 0.01). A nearly two-fold increase in miR-34a expression for the hypomethylated promoter was found in normal esophageal tissues than ESCC with hypermethylation (P <0.0001), pointing to a negative relationship between miR-34a CpG sites methylation and expression(r = −0.594, P = 0.042). The hypermethylation of miR-34a CpG_8.9 was associated with the advanced UICC stage III/IV of the esophageal cancers, and the hypermethylation of CpG_8.9 and CpG_5 of miR-34a was significantly correlated with lymph node metastasis.</p>
</sec>
<sec><title>Conclusions</title>
<p>Our findings suggest that miR-34a is involved in the etiology of ESCC and that hypermethylated miR-34a is a potential biomarker for ESCC diagnosis and prognosis. Moreover, targeting miR-34a methylation by demethylating agents may offer a novel strategy for anticancer therapy of ESCC.</p>
</sec>
</div>
</front>
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<pmc article-type="research-article" xml:lang="en"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Exp Clin Cancer Res</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Exp. Clin. Cancer Res</journal-id>
<journal-title-group><journal-title>Journal of Experimental & Clinical Cancer Research : CR</journal-title>
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<issn pub-type="ppub">0392-9078</issn>
<issn pub-type="epub">1756-9966</issn>
<publisher><publisher-name>BioMed Central</publisher-name>
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<article-meta><article-id pub-id-type="pmid">24528540</article-id>
<article-id pub-id-type="pmc">3931274</article-id>
<article-id pub-id-type="publisher-id">1756-9966-33-20</article-id>
<article-id pub-id-type="doi">10.1186/1756-9966-33-20</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research</subject>
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</article-categories>
<title-group><article-title>Inactivation of miR-34a by aberrant CpG methylation in Kazakh patients with esophageal carcinoma</article-title>
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<contrib-group><contrib contrib-type="author" equal-contrib="yes" id="A1"><name><surname>Cui</surname>
<given-names>Xiaobin</given-names>
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<xref ref-type="aff" rid="I1">1</xref>
<xref ref-type="aff" rid="I2">2</xref>
<email>cuixiaobin4363@foxmail.com</email>
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<contrib contrib-type="author" equal-contrib="yes" id="A2"><name><surname>Zhao</surname>
<given-names>Zhimin</given-names>
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<xref ref-type="aff" rid="I1">1</xref>
<email>674126204@qq.com</email>
</contrib>
<contrib contrib-type="author" id="A3"><name><surname>Liu</surname>
<given-names>Dong</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>2553204405@qq.com</email>
</contrib>
<contrib contrib-type="author" id="A4"><name><surname>Guo</surname>
<given-names>Tao</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>sdmcgt@126.com</email>
</contrib>
<contrib contrib-type="author" id="A5"><name><surname>Li</surname>
<given-names>Su</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>944873356@qq.com</email>
</contrib>
<contrib contrib-type="author" id="A6"><name><surname>Hu</surname>
<given-names>Jianming</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>jianming.120@163.com</email>
</contrib>
<contrib contrib-type="author" id="A7"><name><surname>Liu</surname>
<given-names>Chunxia</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>liuliu2239@sina.com</email>
</contrib>
<contrib contrib-type="author" id="A8"><name><surname>Yang</surname>
<given-names>Lan</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>yl-branda@163.com</email>
</contrib>
<contrib contrib-type="author" id="A9"><name><surname>Cao</surname>
<given-names>Yuwen</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>cywwb2013@126.com</email>
</contrib>
<contrib contrib-type="author" id="A10"><name><surname>Jiang</surname>
<given-names>Jinfang</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>shzjjf@163.com</email>
</contrib>
<contrib contrib-type="author" id="A11"><name><surname>Liang</surname>
<given-names>Weihua</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>727312528@qq.com</email>
</contrib>
<contrib contrib-type="author" id="A12"><name><surname>Liu</surname>
<given-names>Wei</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>27024289@qq.com</email>
</contrib>
<contrib contrib-type="author" id="A13"><name><surname>Li</surname>
<given-names>Shugang</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>251068648@qq.com</email>
</contrib>
<contrib contrib-type="author" id="A14"><name><surname>Wang</surname>
<given-names>Lianghai</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>87550240@qq.com</email>
</contrib>
<contrib contrib-type="author" id="A15"><name><surname>Wang</surname>
<given-names>Lidong</given-names>
</name>
<xref ref-type="aff" rid="I3">3</xref>
<email>ldwang@xxmu.edu.cn</email>
</contrib>
<contrib contrib-type="author" id="A16"><name><surname>Gu</surname>
<given-names>Wenyi</given-names>
</name>
<xref ref-type="aff" rid="I4">4</xref>
<email>w.gu@uq.edu.au</email>
</contrib>
<contrib contrib-type="author" id="A17"><name><surname>Wu</surname>
<given-names>Chuanyue</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<xref ref-type="aff" rid="I5">5</xref>
<email>carywu@pitt.edu</email>
</contrib>
<contrib contrib-type="author" corresp="yes" id="A18"><name><surname>Chen</surname>
<given-names>Yunzhao</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>cyz0515@sina.com</email>
</contrib>
<contrib contrib-type="author" corresp="yes" id="A19"><name><surname>Li</surname>
<given-names>Feng</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<xref ref-type="aff" rid="I2">2</xref>
<email>lifeng7855@126.com</email>
</contrib>
</contrib-group>
<aff id="I1"><label>1</label>
Department of Pathology and Key Laboratory for Xinjiang Endemic and Ethnic Diseases, Shihezi University School of Medicine, North 4th Road, Shihezi, Xinjiang 832002, China</aff>
<aff id="I2"><label>2</label>
Department of Oncology, Tongji Hospital, Huazhong University of Science and Technology, Wuhan, Hubei 430030, China</aff>
<aff id="I3"><label>3</label>
Henan Key Laboratory for Esophageal Cancer, Zhengzhou University School of Medicine, Zhengzhou, Henan 450001, China</aff>
<aff id="I4"><label>4</label>
Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane QLD 4072, Australia</aff>
<aff id="I5"><label>5</label>
Department of Pathology, University of Pittsburgh, Pittsburgh, PA 15261, USA</aff>
<pub-date pub-type="collection"><year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>17</day>
<month>2</month>
<year>2014</year>
</pub-date>
<volume>33</volume>
<issue>1</issue>
<fpage>20</fpage>
<lpage>20</lpage>
<history><date date-type="received"><day>14</day>
<month>12</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>13</day>
<month>2</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2014 Cui et al.; licensee BioMed Central Ltd.</copyright-statement>
<copyright-year>2014</copyright-year>
<copyright-holder>Cui et al.; licensee BioMed Central Ltd.</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/2.0"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/2.0">http://creativecommons.org/licenses/by/2.0</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>
) applies to the data made available in this article, unless otherwise stated.</license-p>
</license>
</permissions>
<self-uri xlink:href="http://www.jeccr.com/content/33/1/20"></self-uri>
<abstract><sec><title>Background</title>
<p>Esophageal squamous cell carcinoma (ESCC) is an aggressive tumor with dismal prognosis and high incidence and mortality in Kazakh population. MiR-34a, a direct p53 target gene, possesses tumor-suppressive properties as they mediate apoptosis, cell cycle arrest, and senescence. The reduced expression of miR-34a by methylation in various cancers has been reported.</p>
</sec>
<sec><title>Methods</title>
<p>To determine whether aberrant miR-34a methylation occurs in esophageal cancer, the DNA methylation of 23 CpGs sites in the miR-34a promoter was quantitatively analyzed in relation to the translation initiation site by MALDI -TOF mass spectrometry in 59 ESCC tissues and 34 normal tissues from the Kazakh population. Real-time PCR was used to detect the inhibition of miR-34a expression levels and to evaluate their association with methylation.</p>
</sec>
<sec><title>Results</title>
<p>We found that miR-34a is more frequently methylated in ESCC (0.133 ± 0.040) than in controls (0.066 ± 0.045, P < 0.01). A nearly two-fold increase in miR-34a expression for the hypomethylated promoter was found in normal esophageal tissues than ESCC with hypermethylation (P <0.0001), pointing to a negative relationship between miR-34a CpG sites methylation and expression(r = −0.594, P = 0.042). The hypermethylation of miR-34a CpG_8.9 was associated with the advanced UICC stage III/IV of the esophageal cancers, and the hypermethylation of CpG_8.9 and CpG_5 of miR-34a was significantly correlated with lymph node metastasis.</p>
</sec>
<sec><title>Conclusions</title>
<p>Our findings suggest that miR-34a is involved in the etiology of ESCC and that hypermethylated miR-34a is a potential biomarker for ESCC diagnosis and prognosis. Moreover, targeting miR-34a methylation by demethylating agents may offer a novel strategy for anticancer therapy of ESCC.</p>
</sec>
</abstract>
<kwd-group><kwd>MiR-34a</kwd>
<kwd>Esophageal squamous cell carcinoma</kwd>
<kwd>Kazakh</kwd>
<kwd>Methylation</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Australie</li>
<li>République populaire de Chine</li>
<li>États-Unis</li>
</country>
<region><li>Pennsylvanie</li>
</region>
<settlement><li>Pittsburgh</li>
</settlement>
<orgName><li>Université de Pittsburgh</li>
</orgName>
</list>
<tree><country name="République populaire de Chine"><noRegion><name sortKey="Cui, Xiaobin" sort="Cui, Xiaobin" uniqKey="Cui X" first="Xiaobin" last="Cui">Xiaobin Cui</name>
</noRegion>
<name sortKey="Cao, Yuwen" sort="Cao, Yuwen" uniqKey="Cao Y" first="Yuwen" last="Cao">Yuwen Cao</name>
<name sortKey="Chen, Yunzhao" sort="Chen, Yunzhao" uniqKey="Chen Y" first="Yunzhao" last="Chen">Yunzhao Chen</name>
<name sortKey="Cui, Xiaobin" sort="Cui, Xiaobin" uniqKey="Cui X" first="Xiaobin" last="Cui">Xiaobin Cui</name>
<name sortKey="Guo, Tao" sort="Guo, Tao" uniqKey="Guo T" first="Tao" last="Guo">Tao Guo</name>
<name sortKey="Hu, Jianming" sort="Hu, Jianming" uniqKey="Hu J" first="Jianming" last="Hu">Jianming Hu</name>
<name sortKey="Jiang, Jinfang" sort="Jiang, Jinfang" uniqKey="Jiang J" first="Jinfang" last="Jiang">Jinfang Jiang</name>
<name sortKey="Li, Feng" sort="Li, Feng" uniqKey="Li F" first="Feng" last="Li">Feng Li</name>
<name sortKey="Li, Feng" sort="Li, Feng" uniqKey="Li F" first="Feng" last="Li">Feng Li</name>
<name sortKey="Li, Shugang" sort="Li, Shugang" uniqKey="Li S" first="Shugang" last="Li">Shugang Li</name>
<name sortKey="Li, Su" sort="Li, Su" uniqKey="Li S" first="Su" last="Li">Su Li</name>
<name sortKey="Liang, Weihua" sort="Liang, Weihua" uniqKey="Liang W" first="Weihua" last="Liang">Weihua Liang</name>
<name sortKey="Liu, Chunxia" sort="Liu, Chunxia" uniqKey="Liu C" first="Chunxia" last="Liu">Chunxia Liu</name>
<name sortKey="Liu, Dong" sort="Liu, Dong" uniqKey="Liu D" first="Dong" last="Liu">Dong Liu</name>
<name sortKey="Liu, Wei" sort="Liu, Wei" uniqKey="Liu W" first="Wei" last="Liu">Wei Liu</name>
<name sortKey="Wang, Lianghai" sort="Wang, Lianghai" uniqKey="Wang L" first="Lianghai" last="Wang">Lianghai Wang</name>
<name sortKey="Wang, Lidong" sort="Wang, Lidong" uniqKey="Wang L" first="Lidong" last="Wang">Lidong Wang</name>
<name sortKey="Wu, Chuanyue" sort="Wu, Chuanyue" uniqKey="Wu C" first="Chuanyue" last="Wu">Chuanyue Wu</name>
<name sortKey="Yang, Lan" sort="Yang, Lan" uniqKey="Yang L" first="Lan" last="Yang">Lan Yang</name>
<name sortKey="Zhao, Zhimin" sort="Zhao, Zhimin" uniqKey="Zhao Z" first="Zhimin" last="Zhao">Zhimin Zhao</name>
</country>
<country name="Australie"><noRegion><name sortKey="Gu, Wenyi" sort="Gu, Wenyi" uniqKey="Gu W" first="Wenyi" last="Gu">Wenyi Gu</name>
</noRegion>
</country>
<country name="États-Unis"><region name="Pennsylvanie"><name sortKey="Wu, Chuanyue" sort="Wu, Chuanyue" uniqKey="Wu C" first="Chuanyue" last="Wu">Chuanyue Wu</name>
</region>
</country>
</tree>
</affiliations>
</record>
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