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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Cyclin D1 overexpression supports stable EBV infection in nasopharyngeal epithelial cells</title>
<author><name sortKey="Tsang, Chi Man" sort="Tsang, Chi Man" uniqKey="Tsang C" first="Chi Man" last="Tsang">Chi Man Tsang</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Yip, Yim Ling" sort="Yip, Yim Ling" uniqKey="Yip Y" first="Yim Ling" last="Yip">Yim Ling Yip</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Lo, Kwok Wai" sort="Lo, Kwok Wai" uniqKey="Lo K" first="Kwok Wai" last="Lo">Kwok Wai Lo</name>
<affiliation><nlm:aff id="aff4">Department of Anatomical and Cellular Pathology,<institution>Chinese University of Hong Kong</institution>
,<country>Hong Kong</country>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Deng, Wen" sort="Deng, Wen" uniqKey="Deng W" first="Wen" last="Deng">Wen Deng</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="To, Ka Fai" sort="To, Ka Fai" uniqKey="To K" first="Ka Fai" last="To">Ka Fai To</name>
<affiliation><nlm:aff id="aff4">Department of Anatomical and Cellular Pathology,<institution>Chinese University of Hong Kong</institution>
,<country>Hong Kong</country>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hau, Pok Man" sort="Hau, Pok Man" uniqKey="Hau P" first="Pok Man" last="Hau">Pok Man Hau</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Lau, Victoria Ming Yi" sort="Lau, Victoria Ming Yi" uniqKey="Lau V" first="Victoria Ming Yi" last="Lau">Victoria Ming Yi Lau</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Takada, Kenzo" sort="Takada, Kenzo" uniqKey="Takada K" first="Kenzo" last="Takada">Kenzo Takada</name>
<affiliation><nlm:aff id="aff5">Institute for Genetic Medicine,<institution>Hokkaido University</institution>
, Sapporo 060-0815,<country>Japan</country>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Lui, Vivian Wai Yan" sort="Lui, Vivian Wai Yan" uniqKey="Lui V" first="Vivian Wai Yan" last="Lui">Vivian Wai Yan Lui</name>
<affiliation><nlm:aff id="aff6">Department of Otolaryngology,<institution>University of Pittsburgh School of Medicine</institution>
, Pittsburgh,<addr-line>PA 15213</addr-line>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Lung, Maria Li" sort="Lung, Maria Li" uniqKey="Lung M" first="Maria Li" last="Lung">Maria Li Lung</name>
<affiliation><nlm:aff wicri:cut=", and" id="aff2">Clinical Oncology</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Chen, Honglin" sort="Chen, Honglin" uniqKey="Chen H" first="Honglin" last="Chen">Honglin Chen</name>
<affiliation><nlm:aff id="aff3">Microbiology, Li Ka Shing Faculty of Medicine, University of Hong Kong, Hong Kong;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zeng, Musheng" sort="Zeng, Musheng" uniqKey="Zeng M" first="Musheng" last="Zeng">Musheng Zeng</name>
<affiliation><nlm:aff wicri:cut="; and" id="aff7">State Key Laboratory of Oncology in Southern China, Cancer Institute,<institution>Sun Yat-sen University</institution>
, Guangzhou 510275,<country>China</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Middeldorp, Jaap Michiel" sort="Middeldorp, Jaap Michiel" uniqKey="Middeldorp J" first="Jaap Michiel" last="Middeldorp">Jaap Michiel Middeldorp</name>
<affiliation><nlm:aff id="aff8">Department of Pathology,<institution>Vrije Universiteit University Medical Center</institution>
, 1081HV, Amsterdam,<country>The Netherlands</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Cheung, Annie Lai Man" sort="Cheung, Annie Lai Man" uniqKey="Cheung A" first="Annie Lai-Man" last="Cheung">Annie Lai-Man Cheung</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Tsao, Sai Wah" sort="Tsao, Sai Wah" uniqKey="Tsao S" first="Sai Wah" last="Tsao">Sai Wah Tsao</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">23161911</idno>
<idno type="pmc">3528537</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3528537</idno>
<idno type="RBID">PMC:3528537</idno>
<idno type="doi">10.1073/pnas.1202637109</idno>
<date when="2012">2012</date>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Cyclin D1 overexpression supports stable EBV infection in nasopharyngeal epithelial cells</title>
<author><name sortKey="Tsang, Chi Man" sort="Tsang, Chi Man" uniqKey="Tsang C" first="Chi Man" last="Tsang">Chi Man Tsang</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Yip, Yim Ling" sort="Yip, Yim Ling" uniqKey="Yip Y" first="Yim Ling" last="Yip">Yim Ling Yip</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Lo, Kwok Wai" sort="Lo, Kwok Wai" uniqKey="Lo K" first="Kwok Wai" last="Lo">Kwok Wai Lo</name>
<affiliation><nlm:aff id="aff4">Department of Anatomical and Cellular Pathology,<institution>Chinese University of Hong Kong</institution>
,<country>Hong Kong</country>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Deng, Wen" sort="Deng, Wen" uniqKey="Deng W" first="Wen" last="Deng">Wen Deng</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="To, Ka Fai" sort="To, Ka Fai" uniqKey="To K" first="Ka Fai" last="To">Ka Fai To</name>
<affiliation><nlm:aff id="aff4">Department of Anatomical and Cellular Pathology,<institution>Chinese University of Hong Kong</institution>
,<country>Hong Kong</country>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hau, Pok Man" sort="Hau, Pok Man" uniqKey="Hau P" first="Pok Man" last="Hau">Pok Man Hau</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Lau, Victoria Ming Yi" sort="Lau, Victoria Ming Yi" uniqKey="Lau V" first="Victoria Ming Yi" last="Lau">Victoria Ming Yi Lau</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Takada, Kenzo" sort="Takada, Kenzo" uniqKey="Takada K" first="Kenzo" last="Takada">Kenzo Takada</name>
<affiliation><nlm:aff id="aff5">Institute for Genetic Medicine,<institution>Hokkaido University</institution>
, Sapporo 060-0815,<country>Japan</country>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Lui, Vivian Wai Yan" sort="Lui, Vivian Wai Yan" uniqKey="Lui V" first="Vivian Wai Yan" last="Lui">Vivian Wai Yan Lui</name>
<affiliation><nlm:aff id="aff6">Department of Otolaryngology,<institution>University of Pittsburgh School of Medicine</institution>
, Pittsburgh,<addr-line>PA 15213</addr-line>
;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Lung, Maria Li" sort="Lung, Maria Li" uniqKey="Lung M" first="Maria Li" last="Lung">Maria Li Lung</name>
<affiliation><nlm:aff wicri:cut=", and" id="aff2">Clinical Oncology</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Chen, Honglin" sort="Chen, Honglin" uniqKey="Chen H" first="Honglin" last="Chen">Honglin Chen</name>
<affiliation><nlm:aff id="aff3">Microbiology, Li Ka Shing Faculty of Medicine, University of Hong Kong, Hong Kong;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zeng, Musheng" sort="Zeng, Musheng" uniqKey="Zeng M" first="Musheng" last="Zeng">Musheng Zeng</name>
<affiliation><nlm:aff wicri:cut="; and" id="aff7">State Key Laboratory of Oncology in Southern China, Cancer Institute,<institution>Sun Yat-sen University</institution>
, Guangzhou 510275,<country>China</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Middeldorp, Jaap Michiel" sort="Middeldorp, Jaap Michiel" uniqKey="Middeldorp J" first="Jaap Michiel" last="Middeldorp">Jaap Michiel Middeldorp</name>
<affiliation><nlm:aff id="aff8">Department of Pathology,<institution>Vrije Universiteit University Medical Center</institution>
, 1081HV, Amsterdam,<country>The Netherlands</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Cheung, Annie Lai Man" sort="Cheung, Annie Lai Man" uniqKey="Cheung A" first="Annie Lai-Man" last="Cheung">Annie Lai-Man Cheung</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
<author><name sortKey="Tsao, Sai Wah" sort="Tsao, Sai Wah" uniqKey="Tsao S" first="Sai Wah" last="Tsao">Sai Wah Tsao</name>
<affiliation><nlm:aff id="aff1"></nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
<idno type="eISSN">1091-6490</idno>
<imprint><date when="2012">2012</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
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<front><div type="abstract" xml:lang="en"><p>Undifferentiated nasopharyngeal carcinomas (NPCs) are commonly present with latent EBV infection. However, events regulating EBV infection at early stages of the disease and the role of EBV in disease pathogenesis are largely undefined. Genetic alterations leading to activation of cyclin D1 signaling in premalignant nasopharyngeal epithelial (NPE) cells have been postulated to predispose cells to EBV infection. We previously reported that loss of p16, a negative regulator of cyclin D1 signaling, is a frequent feature of NPC tumors. Here, we report that early premalignant lesions of nasopharyngeal epithelium overexpress cyclin D1. Furthermore, overexpression of cyclin D1 is closely associated with EBV infection. Therefore we investigated the potential role of cyclin D1 overexpression in dysplastic NPE cells in vitro. In human telomerase reverse transcriptase-immortalized NPE cells, overexpression of cyclin D1 or a p16-resistant form of CDK4 (CDK4<sup>R24C</sup>
) suppressed differentiation. This suppression may have implications for the close association of EBV infection with undifferentiated NPC. In these in vitro models, we found that cellular growth arrest and senescence occurred in EBV-infected cell populations immediately after infection. Nevertheless, overexpression of cyclin D1 or a p16-resistant form of CDK4 or knockdown of p16 in the human telomerase reverse transcriptase-immortalized NPE cell lines could counteract the EBV-induced growth arrest and senescence. We conclude that dysregulated expression of cyclin D1 in NPE cells may contribute to NPC pathogenesis by enabling persistent infection of EBV.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
<journal-id journal-id-type="publisher-id">PNAS</journal-id>
<journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
</journal-title-group>
<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
<publisher><publisher-name>National Academy of Sciences</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">23161911</article-id>
<article-id pub-id-type="pmc">3528537</article-id>
<article-id pub-id-type="publisher-id">201202637</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1202637109</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>PNAS Plus</subject>
</subj-group>
<subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Cell Biology</subject>
</subj-group>
</subj-group>
<series-title>PNAS Plus</series-title>
</article-categories>
<title-group><article-title>Cyclin D1 overexpression supports stable EBV infection in nasopharyngeal epithelial cells</article-title>
<alt-title alt-title-type="short">Cyclin D1 supports EBV infection</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Tsang</surname>
<given-names>Chi Man</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yip</surname>
<given-names>Yim Ling</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lo</surname>
<given-names>Kwok Wai</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Deng</surname>
<given-names>Wen</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>To</surname>
<given-names>Ka Fai</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hau</surname>
<given-names>Pok Man</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lau</surname>
<given-names>Victoria Ming Yi</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Takada</surname>
<given-names>Kenzo</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lui</surname>
<given-names>Vivian Wai Yan</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lung</surname>
<given-names>Maria Li</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chen</surname>
<given-names>Honglin</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zeng</surname>
<given-names>Musheng</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Middeldorp</surname>
<given-names>Jaap Michiel</given-names>
</name>
<xref ref-type="aff" rid="aff8"><sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cheung</surname>
<given-names>Annie Lai-Man</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Tsao</surname>
<given-names>Sai Wah</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<aff id="aff1">Departments of<sup>a</sup>
Anatomy,</aff>
<aff id="aff2"><sup>e</sup>
Clinical Oncology, and</aff>
<aff id="aff3"><sup>f</sup>
Microbiology, Li Ka Shing Faculty of Medicine, University of Hong Kong, Hong Kong;</aff>
<aff id="aff4"><sup>b</sup>
Department of Anatomical and Cellular Pathology,<institution>Chinese University of Hong Kong</institution>
,<country>Hong Kong</country>
;</aff>
<aff id="aff5"><sup>c</sup>
Institute for Genetic Medicine,<institution>Hokkaido University</institution>
, Sapporo 060-0815,<country>Japan</country>
;</aff>
<aff id="aff6"><sup>d</sup>
Department of Otolaryngology,<institution>University of Pittsburgh School of Medicine</institution>
, Pittsburgh,<addr-line>PA 15213</addr-line>
;</aff>
<aff id="aff7"><sup>g</sup>
State Key Laboratory of Oncology in Southern China, Cancer Institute,<institution>Sun Yat-sen University</institution>
, Guangzhou 510275,<country>China</country>
; and</aff>
<aff id="aff8"><sup>h</sup>
Department of Pathology,<institution>Vrije Universiteit University Medical Center</institution>
, 1081HV, Amsterdam,<country>The Netherlands</country>
</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>2</sup>
To whom correspondence should be addressed. E-mail: <email>gswtsao@hku.hk</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Elliott Kieff, Harvard Medical School and Brigham and Women's Hospital, Boston, MA, and approved October 12, 2012 (received for review March 6, 2012)</p>
</fn>
<fn fn-type="con"><p>Author contributions: C.M.T., P.M.H., and S.W.T. designed research; C.M.T., Y.L.Y., K.W.L., W.D., and V.M.Y.L. performed research; K.F.T., K.T., M.Z., J.M.M., and A.L.-M.C. contributed new reagents/analytic tools; C.M.T., K.W.L., W.D., H.C., and S.W.T. analyzed data; and C.M.T., V.W.Y.L., M.L.L., and S.W.T. wrote the paper.</p>
</fn>
<fn id="fn1" fn-type="equal"><p><sup>1</sup>
C.M.T. and Y.L.Y. contributed equally to this work.</p>
</fn>
<fn fn-type="conflict"><p>The authors declare no conflict of interest.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>11</day>
<month>12</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>16</day>
<month>11</month>
<year>2012</year>
</pub-date>
<volume>109</volume>
<issue>50</issue>
<fpage>E3473</fpage>
<lpage>E3482</lpage>
<page-range>E3473–E3482</page-range>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pnas.201202637.pdf"></self-uri>
<self-uri content-type="author-summary-pdf" xlink:type="simple" xlink:href="pnas.201202637_summary.pdf"></self-uri>
<abstract id="d34e299"><p>Undifferentiated nasopharyngeal carcinomas (NPCs) are commonly present with latent EBV infection. However, events regulating EBV infection at early stages of the disease and the role of EBV in disease pathogenesis are largely undefined. Genetic alterations leading to activation of cyclin D1 signaling in premalignant nasopharyngeal epithelial (NPE) cells have been postulated to predispose cells to EBV infection. We previously reported that loss of p16, a negative regulator of cyclin D1 signaling, is a frequent feature of NPC tumors. Here, we report that early premalignant lesions of nasopharyngeal epithelium overexpress cyclin D1. Furthermore, overexpression of cyclin D1 is closely associated with EBV infection. Therefore we investigated the potential role of cyclin D1 overexpression in dysplastic NPE cells in vitro. In human telomerase reverse transcriptase-immortalized NPE cells, overexpression of cyclin D1 or a p16-resistant form of CDK4 (CDK4<sup>R24C</sup>
) suppressed differentiation. This suppression may have implications for the close association of EBV infection with undifferentiated NPC. In these in vitro models, we found that cellular growth arrest and senescence occurred in EBV-infected cell populations immediately after infection. Nevertheless, overexpression of cyclin D1 or a p16-resistant form of CDK4 or knockdown of p16 in the human telomerase reverse transcriptase-immortalized NPE cell lines could counteract the EBV-induced growth arrest and senescence. We conclude that dysregulated expression of cyclin D1 in NPE cells may contribute to NPC pathogenesis by enabling persistent infection of EBV.</p>
</abstract>
<kwd-group><kwd>Epstein-Barr virus</kwd>
<kwd>episome</kwd>
<kwd>viral persistence</kwd>
</kwd-group>
<custom-meta-group><custom-meta><meta-name>author-summary</meta-name>
<meta-value><xref ref-type="other" rid="author-summary"></xref>
</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
</record>
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