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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Pathology of Kaposi’s Sarcoma-Associated Herpesvirus Infection</title>
<author><name sortKey="Fukumoto, Hitomi" sort="Fukumoto, Hitomi" uniqKey="Fukumoto H" first="Hitomi" last="Fukumoto">Hitomi Fukumoto</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Pathology, National Institute of Infectious Diseases</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2"><institution>Military Medicine Research Unit, Japan Ground Self Defense Force</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Kanno, Takayuki" sort="Kanno, Takayuki" uniqKey="Kanno T" first="Takayuki" last="Kanno">Takayuki Kanno</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Pathology, National Institute of Infectious Diseases</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hasegawa, Hideki" sort="Hasegawa, Hideki" uniqKey="Hasegawa H" first="Hideki" last="Hasegawa">Hideki Hasegawa</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Pathology, National Institute of Infectious Diseases</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Katano, Harutaka" sort="Katano, Harutaka" uniqKey="Katano H" first="Harutaka" last="Katano">Harutaka Katano</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Pathology, National Institute of Infectious Diseases</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">21904536</idno>
<idno type="pmc">3161246</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3161246</idno>
<idno type="RBID">PMC:3161246</idno>
<idno type="doi">10.3389/fmicb.2011.00175</idno>
<date when="2011">2011</date>
<idno type="wicri:Area/Pmc/Corpus">004A10</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">004A10</idno>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Pathology of Kaposi’s Sarcoma-Associated Herpesvirus Infection</title>
<author><name sortKey="Fukumoto, Hitomi" sort="Fukumoto, Hitomi" uniqKey="Fukumoto H" first="Hitomi" last="Fukumoto">Hitomi Fukumoto</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Pathology, National Institute of Infectious Diseases</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2"><institution>Military Medicine Research Unit, Japan Ground Self Defense Force</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Kanno, Takayuki" sort="Kanno, Takayuki" uniqKey="Kanno T" first="Takayuki" last="Kanno">Takayuki Kanno</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Pathology, National Institute of Infectious Diseases</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hasegawa, Hideki" sort="Hasegawa, Hideki" uniqKey="Hasegawa H" first="Hideki" last="Hasegawa">Hideki Hasegawa</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Pathology, National Institute of Infectious Diseases</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Katano, Harutaka" sort="Katano, Harutaka" uniqKey="Katano H" first="Harutaka" last="Katano">Harutaka Katano</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Pathology, National Institute of Infectious Diseases</institution>
<country>Tokyo, Japan</country>
</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Frontiers in Microbiology</title>
<idno type="eISSN">1664-302X</idno>
<imprint><date when="2011">2011</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
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<front><div type="abstract" xml:lang="en"><p>Kaposi’s sarcoma-associated herpesvirus (KSHV; human herpesvirus 8) is a human herpesvirus, classified as a gamma-herpesvirus. KSHV is detected in Kaposi’s sarcoma (KS), primary effusion lymphoma (PEL), and some cases of multicentric Castleman’s disease (MCD). Similar to other herpes viruses, there are two phases of infection, latent and lytic. In KSHV-associated malignancies such as KS and PEL, KSHV latently infects almost all tumor cells. Quantitative PCR analysis revealed that each tumor cell contains one copy of KSHV in KS lesions. The oncogenesis by KSHV has remained unclear. Latency-associated nuclear antigen (LANA)-1 plays an important role in the pathogenesis of KSHV-associated malignancies through inhibition of apoptosis and maintenance of latency. Because all KSHV-infected cells express LANA-1, LANA-1 immunohistochemistry is a useful tool for diagnosis of KSHV infection. KSHV encodes some homologs of cellular proteins including cell-cycle regulators, cytokines, and chemokines, such as cyclin D, G-protein-coupled protein, interleukin-6, and macrophage inflammatory protein-1 and -2. These viral proteins mimic or disrupt host cytokine signals, resulting in microenvironments amenable to tumor growth. Lytic infection is frequently seen in MCD tissues, suggesting a different pathogenesis from KS and lymphoma.</p>
</div>
</front>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Microbiol</journal-id>
<journal-id journal-id-type="publisher-id">Front. Microbio.</journal-id>
<journal-title-group><journal-title>Frontiers in Microbiology</journal-title>
</journal-title-group>
<issn pub-type="epub">1664-302X</issn>
<publisher><publisher-name>Frontiers Research Foundation</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">21904536</article-id>
<article-id pub-id-type="pmc">3161246</article-id>
<article-id pub-id-type="doi">10.3389/fmicb.2011.00175</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Microbiology</subject>
<subj-group><subject>Review Article</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Pathology of Kaposi’s Sarcoma-Associated Herpesvirus Infection</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Fukumoto</surname>
<given-names>Hitomi</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kanno</surname>
<given-names>Takayuki</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hasegawa</surname>
<given-names>Hideki</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Katano</surname>
<given-names>Harutaka</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">*</xref>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup>
<institution>Department of Pathology, National Institute of Infectious Diseases</institution>
<country>Tokyo, Japan</country>
</aff>
<aff id="aff2"><sup>2</sup>
<institution>Military Medicine Research Unit, Japan Ground Self Defense Force</institution>
<country>Tokyo, Japan</country>
</aff>
<author-notes><fn fn-type="edited-by"><p>Edited by: Keiji Ueda, Osaka University Graduate School of Medicine, Japan</p>
</fn>
<fn fn-type="edited-by"><p>Reviewed by: Hiroki Isomura, Aichi Cancer Center Research Institute, Japan; Keiji Ueda, Osaka University Graduate School of Medicine, Japan</p>
</fn>
<corresp id="fn001">*Correspondence: Harutaka Katano, Department of Pathology, National Institute of Infectious Diseases, 1-23-1 Toyama, Shinjuku-ku, Tokyo 162-8640, Japan. e-mail: <email>katano@nih.go.jp</email>
</corresp>
<fn fn-type="other" id="fn002"><p>This article was submitted to Frontiers in Virology, a specialty of Frontiers in Microbiology.</p>
</fn>
</author-notes>
<pub-date pub-type="epreprint"><day>21</day>
<month>7</month>
<year>2011</year>
</pub-date>
<pub-date pub-type="epub"><day>25</day>
<month>8</month>
<year>2011</year>
</pub-date>
<pub-date pub-type="collection"><year>2011</year>
</pub-date>
<volume>2</volume>
<elocation-id>175</elocation-id>
<history><date date-type="received"><day>30</day>
<month>6</month>
<year>2011</year>
</date>
<date date-type="accepted"><day>09</day>
<month>8</month>
<year>2011</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2011 Fukumoto, Kanno, Hasegawa and Katano.</copyright-statement>
<copyright-year>2011</copyright-year>
<license license-type="open-access" xlink:href="http://www.frontiersin.org/licenseagreement"><license-p>This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.</license-p>
</license>
</permissions>
<abstract><p>Kaposi’s sarcoma-associated herpesvirus (KSHV; human herpesvirus 8) is a human herpesvirus, classified as a gamma-herpesvirus. KSHV is detected in Kaposi’s sarcoma (KS), primary effusion lymphoma (PEL), and some cases of multicentric Castleman’s disease (MCD). Similar to other herpes viruses, there are two phases of infection, latent and lytic. In KSHV-associated malignancies such as KS and PEL, KSHV latently infects almost all tumor cells. Quantitative PCR analysis revealed that each tumor cell contains one copy of KSHV in KS lesions. The oncogenesis by KSHV has remained unclear. Latency-associated nuclear antigen (LANA)-1 plays an important role in the pathogenesis of KSHV-associated malignancies through inhibition of apoptosis and maintenance of latency. Because all KSHV-infected cells express LANA-1, LANA-1 immunohistochemistry is a useful tool for diagnosis of KSHV infection. KSHV encodes some homologs of cellular proteins including cell-cycle regulators, cytokines, and chemokines, such as cyclin D, G-protein-coupled protein, interleukin-6, and macrophage inflammatory protein-1 and -2. These viral proteins mimic or disrupt host cytokine signals, resulting in microenvironments amenable to tumor growth. Lytic infection is frequently seen in MCD tissues, suggesting a different pathogenesis from KS and lymphoma.</p>
</abstract>
<kwd-group><kwd>Kaposi’s sarcoma-associated herpesvirus</kwd>
<kwd>HHV-8</kwd>
<kwd>latency-associated nuclear antigen</kwd>
<kwd>LANA-1</kwd>
<kwd>primary effusion lymphoma</kwd>
</kwd-group>
<counts><fig-count count="1"></fig-count>
<table-count count="3"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="88"></ref-count>
<page-count count="9"></page-count>
<word-count count="8442"></word-count>
</counts>
</article-meta>
</front>
<body><sec sec-type=""><title>Introduction</title>
<p>The 1994 discovery of Kaposi’s sarcoma-associated herpesvirus (KSHV, human herpesvirus 8, HHV-8) in Kaposi’s sarcoma (KS) tissues had a huge impact, not only in the field of virology, but also on bioscience generally (Chang et al., <xref ref-type="bibr" rid="B17">1994</xref>
; Ganem, <xref ref-type="bibr" rid="B29">2005</xref>
). Before the discovery of KSHV, almost all viruses had been identified using conventional virus isolation methods with cell cultures. DNA fragments of KSHV were identified in KS tissues by representational difference analysis, which is a subtraction PCR-based method to purify restriction-endonuclease-digested fragments present in one population of DNA fragments but not in others (Chang et al., <xref ref-type="bibr" rid="B17">1994</xref>
). Thus, KSHV is the first virus whose fragments were identified directly by the PCR method before any cell culture methods. In 1996, KSHV-infected cell lines were established, based on the fragments’ DNA sequences (Renne et al., <xref ref-type="bibr" rid="B67">1996b</xref>
). Herpesvirus-like particles of this virus were found in lymphoma cells by electron microscopic analysis. Finally, KSHV’s full DNA sequence was determined (Russo et al., <xref ref-type="bibr" rid="B69">1996</xref>
). Over the 15-years since the discovery of KSHV, it has been established as a tumor virus (Ganem, <xref ref-type="bibr" rid="B29">2005</xref>
). Some KSHV-encoded genes are homologous to oncogenes or cell-cycle-associated genes (Russo et al., <xref ref-type="bibr" rid="B69">1996</xref>
); some are transformational genes, able to transform human cells (Gao et al., <xref ref-type="bibr" rid="B30">1997</xref>
; Bais et al., <xref ref-type="bibr" rid="B6">1998</xref>
; Lee et al., <xref ref-type="bibr" rid="B46">1998</xref>
; Muralidhar et al., <xref ref-type="bibr" rid="B57">1998</xref>
). However, expression of KSHV-encoded genes is severely restricted; only a few viral genes are expressed in KSHV-infected cells. The KSHV-encoded latency-associated nuclear antigen 1 (LANA-1) is the only protein whose expression is stably detected by immunohistochemistry in KSHV-infected cells (Dupin et al., <xref ref-type="bibr" rid="B23">1999</xref>
; Katano et al., <xref ref-type="bibr" rid="B42">2000b</xref>
). LANA-1 is a multifunctional protein, but has no full transforming activity. In comparison, Epstein–Barr virus (EBV) encodes a full oncogenic protein, latent membrane protein-1 (LMP1), which is expressed in a subset of EBV-latently infected cells (Cohen, <xref ref-type="bibr" rid="B20">2000</xref>
). Thus, KSHV oncogenesis is not simple. Many KSHV-encoded non-transforming proteins apparently collaborate to establish and maintain oncogenesis in KSHV-infected cells. In this review, the pathological aspects of KSHV infection and KSHV-associated diseases are summarized.</p>
</sec>
<sec><title>Virus and Its Gene Expression</title>
<p>Usually, viral particles are not observed in KS samples by electron microscope because of the small number of KSHV copies. However, they can be seen in primary effusion lymphoma (PEL) cell lines stimulated by 12-<italic>O</italic>
-tetradecanoylphorbol-13-acetate (TPA). A complete viral particle of KSHV, consisting of a capsid and an envelope (Renne et al., <xref ref-type="bibr" rid="B67">1996b</xref>
; Said et al., <xref ref-type="bibr" rid="B71">1996</xref>
, <xref ref-type="bibr" rid="B70">1997</xref>
; Orenstein et al., <xref ref-type="bibr" rid="B61">1997</xref>
; Ohtsuki et al., <xref ref-type="bibr" rid="B59">1999</xref>
), is 150–200 nm in diameter, which is similar to other human herpes viruses and indistinguishable from other herpes viruses. The unenveloped capsid is produced in the host nucleus and is 100 nm in diameter. It contains a central DNA core, which appears to have a high electron density. The envelope is derived from the inner nuclear membrane, as viral particles bud into the cytoplasm from the nucleus. The tegument protein fills the space between the nucleocapsid and envelope. This feature of viral particles is apparently quite similar among herpes viruses, but related structures forming in infected cells seem to depend on the type of virus.</p>
<p>The KSHV genome consists of linear, double-stranded DNA of about 170 kbp (Renne et al., <xref ref-type="bibr" rid="B66">1996a</xref>
; Russo et al., <xref ref-type="bibr" rid="B69">1996</xref>
). The KSHV genome consists of a long unique region (LUR) and a terminal repeat (TR) at both termini, which resembles the herpes virus saimiri structure (Russo et al., <xref ref-type="bibr" rid="B69">1996</xref>
). The TRs consist of 801-bp direct repeat units having 84.5% GC content. The number of repeats in TRs may vary. The LUR is 140.5 kbp and has 53.5% GC content. KSHV encodes more than 80 viral proteins on LUR. KSHV also encodes 17 microRNAs (miRNAs), which are derived by processing from 12 pre-miRNAs (Cai et al., <xref ref-type="bibr" rid="B11">2005</xref>
). Kinetics of KSHV-encoded genes were mainly investigated in KSHV-infected PEL cell lines stimulated with phorbol ester such as TPA (Sun et al., <xref ref-type="bibr" rid="B80">1999</xref>
). Like other herpesviruses, viral genes were categorized into lytic and latent genes, and also into immediate-early (IE), early (E), and late (L) genes based on their expressions. The function of each KSHV-encoded gene was summarized in the Table <xref ref-type="table" rid="T1">1</xref>
. Open reading frame 50 (<italic>ORF50</italic>
) is an IE gene that is a homolog of <italic>Rta</italic>
, a transcriptional activator encoded by EBV (Lukac et al., <xref ref-type="bibr" rid="B50">1999</xref>
; Seaman et al., <xref ref-type="bibr" rid="B77">1999</xref>
; Sun et al., <xref ref-type="bibr" rid="B80">1999</xref>
; Zhu et al., <xref ref-type="bibr" rid="B86">1999</xref>
). Transcription of <italic>ORF50</italic>
results in its expression within 4 h after stimulation by TPA. This expression could not be blocked by phosphonoacetic acid (a herpesvirus-DNA polymerase inhibitor) nor cycloheximide (a protein synthesis inhibitor). Transfection of <italic>ORF50</italic>
to KSHV-infected cells resulted in the activation of lytic gene expression (Lukac et al., <xref ref-type="bibr" rid="B50">1999</xref>
). Thus, ORF50 protein is a lytic switch protein. Expression of ORF50 protein is required for expression of many KSHV-encoded lytic genes such as <italic>K3</italic>
, and <italic>K5</italic>
(homologs of the IE gene of <italic>BHV-4</italic>
), viral interleukin-6 (<italic>vIL-6)</italic>
, viral macrophage inflammatory proteins (<italic>vMIP</italic>
s), polyadenylated nuclear RNA (<italic>PAN</italic>
), <italic>vBcl-2</italic>
, <italic>K12</italic>
, viral G-protein-coupled receptor (<italic>vGPCR</italic>
), viral dihydrofolate reductase (<italic>vDHFR</italic>
), DNA replication factors, and thymidylate synthase (Sarid et al., <xref ref-type="bibr" rid="B76">1998</xref>
). ORF50 protein also induces expression of K8 (K-bZIP, a positional homolog of EBV BZLF1) protein, an early protein. K8 protein plays a role as transactivation repressor for ORF50 protein, leading to a negative autoregulation system during lytic infection (Liao et al., <xref ref-type="bibr" rid="B48">2003</xref>
). Late genes, including tegument proteins, and virion-associated protein are then expressed (Table <xref ref-type="table" rid="T1">1</xref>
).</p>
<table-wrap id="T1" position="float"><label>Table 1</label>
<caption><p><bold>Kaposi’s sarcoma-associated herpesvirus genes and their functions</bold>
.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Gene</th>
<th align="left" rowspan="1" colspan="1">Phase</th>
<th align="left" rowspan="1" colspan="1">Functions</th>
</tr>
</thead>
<tbody><tr><td align="left" rowspan="1" colspan="1"><italic>LANA-1</italic>
</td>
<td align="left" rowspan="1" colspan="1">Latent</td>
<td align="left" rowspan="1" colspan="1">Always express in KSHV-infected cells</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Maintain and replicate viral genome during mitotic division by holding KSHV episome at chromosome</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Bind to p53 and inhibit p53-dependent apoptosis</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Bind to Rb and inhibit Rb-E2F pathway</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Bind to GSK-3β, and induce accumulation of β-catenin</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>LANA-2</italic>
</td>
<td align="left" rowspan="1" colspan="1">Latent</td>
<td align="left" rowspan="1" colspan="1">Expressed in only PEL cells, not in KS cells</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Homolog of IRF</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Inhibit p53-dependent apoptosis</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>Kaposin</italic>
</td>
<td align="left" rowspan="1" colspan="1">Latent</td>
<td align="left" rowspan="1" colspan="1">Kaposin A: transformation activity?</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Kaposin B, C: associate with cytokine expression as adaptor protein of MAP kinase-associated protein kinase 2 (MK2)</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>v-cyclin</italic>
</td>
<td align="left" rowspan="1" colspan="1">Latent</td>
<td align="left" rowspan="1" colspan="1">Homolog of cyclin D1</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Inhibit P27Kip1, and induce cell-cycle to S-phase</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>v-FLIP</italic>
</td>
<td align="left" rowspan="1" colspan="1">Latent</td>
<td align="left" rowspan="1" colspan="1">Anti-apoptosis</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>ORF50 (RTA)</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic (IE)</td>
<td align="left" rowspan="1" colspan="1">Lytic switch protein</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Transactivator for K8</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>K1</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic</td>
<td align="left" rowspan="1" colspan="1">Transformation activity</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>K8</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic (early)</td>
<td align="left" rowspan="1" colspan="1">Transcriptional repressor for RTA</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>K3, K5</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic (IE/early)</td>
<td align="left" rowspan="1" colspan="1">Down-regulation of MHC class I expression</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>vIL-6</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic (early)</td>
<td align="left" rowspan="1" colspan="1">Induce VEGF expression</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Induce constitutional activation of Stat3</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Disrupt anti-viral function by IFN-α</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>vIRF-1</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic (early)</td>
<td align="left" rowspan="1" colspan="1">Disrupt IFN signal</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Transformation activity?</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>vMIPs</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic (early)</td>
<td align="left" rowspan="1" colspan="1">Bind to chemokine receptors and induce angiogenesis</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>vBcl-2</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic (early)</td>
<td align="left" rowspan="1" colspan="1">Inhibit apoptosis</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>vGPCR</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic (early)</td>
<td align="left" rowspan="1" colspan="1">Transformation activity</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Bind to IL-8</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1"></td>
<td align="left" rowspan="1" colspan="1">Induce VEGF expression</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>K15</italic>
</td>
<td align="left" rowspan="1" colspan="1">Lytic</td>
<td align="left" rowspan="1" colspan="1">Bind to TRAF family, and induction of NF-κB activation</td>
</tr>
</tbody>
</table>
</table-wrap>
<p>Latent infection is predominant in KSHV infection. KSHV codes a latency-associated gene cluster including <italic>ORF73</italic>
(<italic>LANA-1</italic>
, <italic>LNA</italic>
, or <italic>LNA-1</italic>
), v-cyclin (<italic>ORF72</italic>
), viral FLICE-inhibitory protein (<italic>K13</italic>
, <italic>v-FLIP</italic>
), Kaposin (<italic>K12</italic>
), and viral-encoded miRNAs. LANA-1 is always detected as a dot-like staining pattern in KSHV-infected cells by immunohistochemistry. KSHV-encoded 17 miRNAs, which are derived by processing from 12 pre-miRNAs, are expressed during viral latency (Cai et al., <xref ref-type="bibr" rid="B11">2005</xref>
; Samols et al., <xref ref-type="bibr" rid="B74">2005</xref>
).</p>
</sec>
<sec><title>KSHV Oncogenesis</title>
<p>The first evidence of transformation activity by KSHV came from a report describing that human umbilical vein endothelial cells (HUVEC) were transformed and immortalized by KSHV infection <italic>in vitro</italic>
(Flore et al., <xref ref-type="bibr" rid="B26">1998</xref>
). However, such KSHV-infected HUVEC did not express any KSHV gene, and the immortalization by KSHV infection was not confirmed by any other groups (Gao et al., <xref ref-type="bibr" rid="B31">2003</xref>
; Tang et al., <xref ref-type="bibr" rid="B81">2003</xref>
). KSHV efficiently infects primary cultures of human endothelial cells <italic>in vitro</italic>
(Sakurada et al., <xref ref-type="bibr" rid="B73">2001</xref>
; Gao et al., <xref ref-type="bibr" rid="B31">2003</xref>
). KSHV-infected cells express LANA-1 within several hours after infection. One week after infection, a large portion of culture cells will be infected by KSHV and expressing LANA-1. Interestingly, expression of any lytic proteins encoded by KSHV is not observed at that time. Latent infection is dominant in KSHV-infected cells <italic>in vivo</italic>
and <italic>in vitro</italic>
. Although some KSHV-encoded proteins such as K1 and vGPCR are shown to have a transformation activity on mammalian cells, these transforming proteins are not usually expressed in KSHV-infected cells (Bais et al., <xref ref-type="bibr" rid="B6">1998</xref>
; Lee et al., <xref ref-type="bibr" rid="B46">1998</xref>
; Montaner et al., <xref ref-type="bibr" rid="B55">2003</xref>
). However, LANA-1, a major KSHV-encoded latency protein, is always expressed in KSHV-infected cells both <italic>in vivo</italic>
and <italic>in vitro</italic>
(Dupin et al., <xref ref-type="bibr" rid="B23">1999</xref>
; Katano et al., <xref ref-type="bibr" rid="B40">1999b</xref>
; Kellam et al., <xref ref-type="bibr" rid="B45">1999</xref>
). Moreover, latency is maintained during the presence of KSHV in the cells. Thus, LANA-1 clearly plays an important role in the pathogenesis of KSHV infection, and has been shown to be a multifunctional protein. Probably the most important role of LANA-1 is to establish and maintain the latency in KSHV-infected cells by tethering KSHV DNA to host chromosomes (Ballestas et al., <xref ref-type="bibr" rid="B7">1999</xref>
). LANA-1 binds directly to TR sequences of the KSHV genome, and recruits it to the host chromosome (Figure <xref ref-type="fig" rid="F1">1</xref>
E). The DNA of KSHV is replicated during host cell divisions using host DNA replicative machinery (Sakakibara et al., <xref ref-type="bibr" rid="B72">2004</xref>
). Thus, daughter cells inherit KSHV genome without any virus particle. LANA-1 is also associated with signal transduction in KSHV-infected cells. LANA-1 binds directly to p53, a major tumor repressor and anti-apoptotic factor (Friborg et al., <xref ref-type="bibr" rid="B27">1999</xref>
). Viral infection usually induces p53 expression and p53-dependent apoptosis as self-defense system. Direct interaction with p53 by LANA-1 results in inhibition of p53-dependent apoptosis in KSHV-infected cells. Moreover, LANA-1 stabilizes β-catenin by binding to the negative regulator GSK-3β, promoting cell-cycle induction by nuclear accumulation of GSK-3β (Fujimuro et al., <xref ref-type="bibr" rid="B28">2003</xref>
). Thus, LANA-1 plays a central role in the pathogenesis of KSHV infection, but LANA-1 itself does not have any full transformation activity. Many other factors besides LANA-1 are required to establish KSHV oncogenesis.</p>
<fig id="F1" position="float"><label>Figure 1</label>
<caption><p><bold>Histological analysis on KSHV-associated diseases</bold>
. <bold>(A)</bold>
Nodular stage of KS; HE staining. <bold>(B)</bold>
LANA-1 immunohistochemistry of KS. <bold>(C)</bold>
Giemsa staining of PEL. <bold>(D)</bold>
LANA-1 immunofluorescence staining in mitosis of PEL cells. <bold>(E)</bold>
LANA-1 immunostaining of mitosis of PEL cell line, TY-1. Yellow signals indicate LANA-1. Red is counter staining of chromosome. <bold>(F)</bold>
HE staining of MCD. <bold>(G)</bold>
LANA-1 immunohistochemistry of MCD.</p>
</caption>
<graphic xlink:href="fmicb-02-00175-g001"></graphic>
</fig>
<p>Another important factor in KSHV oncogenesis is that KSHV encodes many homologs of human genes. The viral genes of human gene homologs cooperate to establish suitable growth conditions for KSHV-infected cells. Among them, vIL-6 is the most important factor for KSHV pathogenesis. vIL-6 induces angiogenesis by vascular endothelial cell growth factor (VEGF) expression (Aoki et al., <xref ref-type="bibr" rid="B4">1999</xref>
), and stimulates the constitutive Jak-Stat pathway through the Stat3 signal, resulting in cell growth (Aoki et al., <xref ref-type="bibr" rid="B3">2003</xref>
). In addition, vIL-6 represses the anti-viral function of interferon by binding to a subunit of human IL-6 receptor and suppressing p21 expression (Chatterjee et al., <xref ref-type="bibr" rid="B19">2002</xref>
). KSHV-encoded vMIP-1, vMIP-2, vBcl-2, vIRF-1, v-cyclin D, and v-FLIP mimic their human homologs, and work sometimes as inhibitors and sometimes as mimics, resulting in growth of KSHV-infected cells. Because almost all these mimics are lytic proteins, their expression is not usually observed. However, some cytokines may induce their expression independently to lytic and latent infection as necessary. Thus, KSHV oncogenesis is established by cooperation of many viral proteins such as LANA-1 and by the mimic, rather than the primary functions of oncogenetic transformation genes encoded by the virus.</p>
<p>Recently, miRNA has been shown to affect tumor biology. Several KSHV miRNAs were shown to modulate host gene expression, suggesting some roles for miRNA in the pathogenesis of KSHV-induced malignancies. Thrombospondin 1, a potent inhibitor of angiogenesis that is reportedly downregulated in KS lesions, is targeted by multiple miRNAs (Samols et al., <xref ref-type="bibr" rid="B75">2007</xref>
). The target of miR-K5 is Bcl2-associated factor BCLAF1, which promote apoptosis (Lei et al., <xref ref-type="bibr" rid="B47">2010</xref>
). MiR-K1 targets IκBα, an inhibitor of NF-κB. NF-κB inhibits the activation of lytic viral promoters. By activating NF-κB, miR-K1 suppresses viral lytic replication, maintaining latent infection (Ziegelbauer et al., <xref ref-type="bibr" rid="B87">2009</xref>
). So far, miRNAs’ roles in viral infection and replication remain unclear.</p>
</sec>
<sec><title>Epidemiology</title>
<p>Serological studies have revealed that KSHV-infected individuals are found all over the world. Serum antibody to KSHV is detected with ELISA using lysate of KSHV viral particles or recombinant viral proteins as antigens, or immunofluorescence assay using KSHV-infected cells. The seroprevalence of KSHV infection differs among regions/countries. Among the general population, KSHV seropositivity is less than 10% in northern Europe, America, and Asia, 10–30% in the Mediterranean region, and more than 50% in most of sub-Saharan Africa (Davis et al., <xref ref-type="bibr" rid="B21">1997</xref>
; Kedes et al., <xref ref-type="bibr" rid="B44">1997</xref>
; Chatlynne et al., <xref ref-type="bibr" rid="B18">1998</xref>
; Mayama et al., <xref ref-type="bibr" rid="B53">1998</xref>
; Rabkin et al., <xref ref-type="bibr" rid="B64">1998</xref>
; Katano et al., <xref ref-type="bibr" rid="B41">2000a</xref>
). The homosexual population exhibits higher positivity (8–25%) than the general population (Grulich et al., <xref ref-type="bibr" rid="B32">2005</xref>
; Casper et al., <xref ref-type="bibr" rid="B14">2006</xref>
; Engels et al., <xref ref-type="bibr" rid="B24">2007</xref>
). Although the transmission modes of KSHV have not yet been clarified, transmission though saliva is likely (Pauk et al., <xref ref-type="bibr" rid="B63">2000</xref>
), because high KSHV copy numbers are detected in saliva of seropositives. Horizontal transmission through the saliva transmission is suggested among children in endemic countries, while sexual transmission may be predominant among homosexual men in non-endemic countries. Organ transplantation can transmit KSHV (Regamey et al., <xref ref-type="bibr" rid="B65">1998</xref>
). Transmission of KSHV through blood transfusion is controversial. While KSHV seroconversion was found in US transfusion recipients (Hladik et al., <xref ref-type="bibr" rid="B34">2006</xref>
), later studies found no significant association of KSHV infection between transfusion groups and non-transfusion groups (Cannon et al., <xref ref-type="bibr" rid="B12">2009</xref>
).</p>
<p>Genotypes of KSHV are categorized based on sequences of the hypervariable regions in its <italic>K1</italic>
gene (Meng et al., <xref ref-type="bibr" rid="B54">1999</xref>
; Zong et al., <xref ref-type="bibr" rid="B88">1999</xref>
; Biggar et al., <xref ref-type="bibr" rid="B9">2000</xref>
; Kazanji et al., <xref ref-type="bibr" rid="B43">2005</xref>
; Hayward and Zong, <xref ref-type="bibr" rid="B33">2007</xref>
; Kanno et al., <xref ref-type="bibr" rid="B38">2010</xref>
). The KSHV <italic>K1</italic>
genes are classified into at five groups: A, B, C, D, and E (Table <xref ref-type="table" rid="T2">2</xref>
). Geographical differences in KSHV genotypes may reflect the history of migration of human populations (Zong et al., <xref ref-type="bibr" rid="B88">1999</xref>
). Subtypes A and C were detected in Japan and subtype A was seen more frequently in AIDS-associated cases than non-AIDS patients (Kanno et al., <xref ref-type="bibr" rid="B38">2010</xref>
). There is no correlation between genotype and KSHV-related disease, including KS, PEL, and multicentric Castleman’s disease (MCD).</p>
<table-wrap id="T2" position="float"><label>Table 2</label>
<caption><p><bold>Kaposi’s sarcoma-associated herpesvirus genotypes</bold>
.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Genotype</th>
<th align="left" rowspan="1" colspan="1">Patients, infected persons</th>
</tr>
</thead>
<tbody><tr><td align="left" rowspan="1" colspan="1">A</td>
<td align="left" rowspan="1" colspan="1">AIDS–KS patients in the US, Europe, Eurasia</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">B</td>
<td align="left" rowspan="1" colspan="1">KS patients of African heritage</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">C</td>
<td align="left" rowspan="1" colspan="1">Classic KS, iatrogenic, and AIDS–KS in Eurasia, US AIDS–KS, Taiwan, Korea, China, Middle East</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">D</td>
<td align="left" rowspan="1" colspan="1">KS patients of Pacific island</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">E</td>
<td align="left" rowspan="1" colspan="1">South American (partial), Brazil Amerindian, Guinea Amerindian</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
<sec><title>KSHV-Related Diseases</title>
<p>Fragments of the KSHV genome have been detected in DNA samples extracted from various diseases by PCR. However, the only diseases whose associations with KSHV infection are widely accepted among researchers in this field are KS, PEL, and MCD (Table <xref ref-type="table" rid="T3">3</xref>
). KSHV is distributed all over the world, and there are many individuals with KSHV infections. Therefore, a low KSHV titer, as detected by PCR, does not mean that a disease is associated with KSHV infection. Because KSHV LANA-1 is always expressed in KSHV-infected cells, LANA-1 immunohistochemistry is a powerful and confirmative tool to detect KSHV-infected cells in pathological samples, and the association with KSHV infection in diseases should be examined by LANA-1 immunohistochemistry on tissue samples.</p>
<table-wrap id="T3" position="float"><label>Table 3</label>
<caption><p><bold>Kaposi’s sarcoma-associated herpesvirus and diseases</bold>
.</p>
</caption>
<table frame="hsides" rules="groups"><tbody><tr><td align="left" rowspan="1" colspan="1">Usually detected (Confirmed association in all cases)</td>
<td align="left" rowspan="1" colspan="1">Kaposi’s sarcoma (all subtypes), primary effusion lymphoma</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Partially detected (Confirmed association only in KSHV<sup>+</sup>
cases)</td>
<td align="left" rowspan="1" colspan="1">Multicentric Castleman’s disease including POEMS (polyneuropathy, organomegaly, endocrinopathy, M protein, skin changes) syndrome, febrile maculopapular skin rash, hemophagocytic syndrome</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Detected in reports, but no association with KSHV infection</td>
<td align="left" rowspan="1" colspan="1">Multiple myeloma, primary pulmonary hypertension, Bowen disease, squamous cell carcinoma, Paget disease, actinic keratosis etc.</td>
</tr>
</tbody>
</table>
</table-wrap>
<sec><title>Primary KSHV infection</title>
<p>A mass study of immunocompetent children in Egypt, where KSHV infection is common, suggested that a febrile maculopapular skin rash was associated with primary KSHV infection (Andreoni et al., <xref ref-type="bibr" rid="B1">2002</xref>
). Seroconversion for KSHV was confirmed in those patients and transmission through saliva was implied by DNA sequences in saliva. A study of homosexual men without HIV infection suggested that diarrhea, fatigue, localized skin rash, and lymphadenopathy were also symptoms of primary KSHV infection (Wang et al., <xref ref-type="bibr" rid="B84">2001</xref>
). Moreover, active KSHV infection may be associated with non-malignant illnesses such as fever, cutaneous rash, and hepatitis after peripheral blood stem cell/bone marrow transplantation (Luppi et al., <xref ref-type="bibr" rid="B51">2000</xref>
).</p>
</sec>
<sec><title>Kaposi's sarcoma</title>
<p>Kaposi’s sarcoma is most important and common of KSHV-associated diseases. Four clinical subtypes have been recognized: classic, AIDS-associated, post-transplantational (iatrogenic or immunodeficient), and African (endemic) subtypes (Antman and Chang, <xref ref-type="bibr" rid="B2">2000</xref>
). These four subtypes of KS are histologically indistinguishable. In the AIDS–KS subtype, KS occurs only in homosexual men. KS occurs in the skin, oral cavity, gastrointestinal tract, lung, liver, lymph node, etc. Skin lesions of KS are most common; they are clinically classified as patchy, plaque, and nodular stages. In the patchy stage, small red flat lesions are observed on the skin. Histologically, dilated, abnormally shaped blood vessels with extravasated red blood cells and edema are found in KS lesions. In the plaque stage, patchy lesions fuse together to form plaque lesions. Proliferation of the spindle-shaped cells is seen around vessels in the plaque stage. In the final nodular stage, brown nodular, and elevated lesions are observed. Histologically, proliferation of spindle cells with slit-like vascular spaces is found (Figure <xref ref-type="fig" rid="F1">1</xref>
A). Multiple KS lesions in the extremities or face are often complicated with lymphedema. Pulmonary lesions may lead to fatal respiratory compromise.</p>
<p>Kaposi’s sarcoma should be diagnosed with histology and immunohistochemistry. Immunohistochemical staining with anti-LANA-1 antibody shows that the viral protein is expressed in KS cells, irrespective of clinical type or disease stage (Dupin et al., <xref ref-type="bibr" rid="B23">1999</xref>
; Katano et al., <xref ref-type="bibr" rid="B40">1999b</xref>
). Expression of LANA-1 can be seen in nuclei of KS spindle cells with a speckled pattern (Figure <xref ref-type="fig" rid="F1">1</xref>
B). The lymphatic marker, podoplanin (D2-40), is also expressed in KS cells (Weninger et al., <xref ref-type="bibr" rid="B85">1999</xref>
). In addition to histological investigation, PCR analysis is useful for the KS diagnosis. Because each KS cell contains about one copy of the KSHV genome, KSHV DNA fragments are consistently detected by PCR, even in formalin-fixed paraffin-embedded KS tissues (Asahi-Ozaki et al., <xref ref-type="bibr" rid="B5">2006</xref>
). PCR sometimes, but not always, detects KSHV DNA in the sera of KS patients. Serum antibody to KSHV is usually positive in KS patients.</p>
<p>Highly active anti-retroviral therapy (HAART) is effective on KS. Incidence of KS in HIV-infected persons has dramatically decreased in the HAART era. Regression of KS is often observed in patients administrated with HAART. In patients with low CD4 counts, KS progresses earlier than in patients with high CD4 counts. These data suggest that KS progression depends on the host’s immune status (Bower et al., <xref ref-type="bibr" rid="B10">2009</xref>
). Recently, patients with KS were administrated with HAART. Patients with aggressive KS received a combination therapy of HAART and chemotherapy of pegylated liposomal doxorubicin (Martin-Carbonero et al., <xref ref-type="bibr" rid="B52">2008</xref>
). Irradiation or surgical resection is also performed for the case of small skin lesion in addition to HAART. There is no effective anti-KSHV therapy for KS. Although vaccine is the most effective method to prevent viral diseases, no vaccine against KSHV is commercially available at present.</p>
<p>The pathological roles of KSHV in KS have been intensely investigated for a long time. The origin of KS cells is thought to be endothelial cells. However, cellular protein expression in KS cells is very different from those of endothelial cells. Infection by KSHV induces a dynamic alteration of gene expression in endothelial cells (Hong et al., <xref ref-type="bibr" rid="B35">2004</xref>
; Wang et al., <xref ref-type="bibr" rid="B83">2004</xref>
). Analysis via DNA array revealed that endothelial cells reduce expression of blood vascular genes and induce markers of lymphatic endothelial cells after KSHV infection <italic>in vitro</italic>
. Thus, KSHV can affect the expression level of cellular proteins in endothelial cells. LANA-1 is expressed in the nucleus by almost all KS spindle shaped cells (Figure <xref ref-type="fig" rid="F1">1</xref>
B), whereas the expression of lytic proteins is limited in KS lesions. Therefore, it is likely that latent infection by KSHV is important for the pathogenesis of KS. As described above, LANA-1 plays a central role in the establishment and maintenance of latency. In addition to LANA-1, cytokines are important for KS pathogenesis. Some cytokines have been detected in the sera of KS patients at high levels. It has been demonstrated that bFGF, IL-6, oncostatin M (OSM), and tumor necrosis factor (TNF)-alpha are required for growth of KS cells <italic>in vitro</italic>
(Liu et al., <xref ref-type="bibr" rid="B49">1997</xref>
; Faris et al., <xref ref-type="bibr" rid="B25">1998</xref>
; Murakami-Mori et al., <xref ref-type="bibr" rid="B56">1998</xref>
). IL-6 is known to be an important growth factor of KS cells especially <italic>in vitro</italic>
. KSHV-encoded vIL-6 interacts with the receptor of human IL-6, mimics its function partially, and contributes to immune escape mechanism by KS cells as described above. KSHV-infected cells have several immune escape mechanisms besides that of vIL-6. K5, a lytic protein of KSHV, down-regulates MHC class I and co-activation molecules, enabling productively infected cells to escape both cytotoxic T cell and NK cell responses (Ishido et al., <xref ref-type="bibr" rid="B36">2000</xref>
). In addition, latently infected cells are also resistant to cytotoxic T cell responses owing to reduced levels of MHC class I molecules, impaired antigen processing, and expression of the anti-apoptotic KSHV ORF-K13/viral FLICE-inhibitory protein (v-FLIP; Thome et al., <xref ref-type="bibr" rid="B82">1997</xref>
).</p>
</sec>
<sec><title>Primary effusion lymphoma</title>
<p>Primary effusion lymphoma is a rare disease occurring mainly in immunosuppressed patients, in particular HIV-infected homosexual males (Cesarman et al., <xref ref-type="bibr" rid="B15">1995</xref>
; Nador et al., <xref ref-type="bibr" rid="B58">1996</xref>
). PEL appears as lymphomatous effusions occurring in the pleural, abdominal, or pericardial effusion in the absence of a contiguous tumor mass. Some patients with PEL secondarily develop solid tumors in adjacent structures such as the pleura; these solid tumors have been termed extracavity PEL (Chadburn et al., <xref ref-type="bibr" rid="B16">2004</xref>
). About half of PEL patients have KS. These tumors always carry KSHV and are commonly co-infected by EBV. Histologically, the tumor cells exhibit various appearances, from large immunoblastic or plasmablastic cells to cells with more anaplastic morphology (Figure <xref ref-type="fig" rid="F1">1</xref>
C). Nuclei vary from large and round to more irregular in shape, with prominent nucleoli. The cytoplasm can be abundant and is deeply basophilic with vacuoles in occasional cells. Binucleated or multinucleated cells resembling Reed–Sternberg cells can be seen. Mitotic figures are typically numerous. PEL cells are derived from post-germinal center B-cells (Jenner et al., <xref ref-type="bibr" rid="B37">2003</xref>
). Their immunophenotypes are undetermined, i.e., CD45 (+), CD138 (+), B-cell markers (−), T cell markers (−); however, their immunoglobulin genes are clonally rearranged and hypermutated. PEL cells contain high copy numbers (about 50 copies/cells) of KSHV DNA (Cesarman et al., <xref ref-type="bibr" rid="B15">1995</xref>
; Asahi-Ozaki et al., <xref ref-type="bibr" rid="B5">2006</xref>
). PEL cells are sometimes co-infected with EBV, while others are infected only with KSHV. However, expressions of LMPs and EBNAs are suppressed in PEL cells. Several KSHV-infected cell lines have been established from PEL cells (Carbone et al., <xref ref-type="bibr" rid="B13">2010</xref>
). A KSHV<sup>+</sup>
/EBV<sup>−</sup>
cell line, TY-1, was even established from EBV<sup>+</sup>
and KSHV<sup>+</sup>
PEL cases, suggesting that KSHV plays an essential role in the pathogenesis of PEL (Katano et al., <xref ref-type="bibr" rid="B39">1999a</xref>
). Infection by KSHV is predominantly latent in PEL cells, which has made PEL cell lines the most widely studied models for KSHV latency. PEL cells express latent genes coded in the latent cluster in KSHV genome (Figure <xref ref-type="fig" rid="F1">1</xref>
D). However, it is not easy to detect latent viral protein expressions other than LANA-1. The expression pattern of KSHV-encoded proteins is almost the same as KS, except that PEL cell express LANA-2 protein (Rivas et al., <xref ref-type="bibr" rid="B68">2001</xref>
). Most PEL lines display a very small subpopulation of cells that stain for markers of lytic reactivation such as ORF50, ORF59, and K8.1 (Katano et al., <xref ref-type="bibr" rid="B42">2000b</xref>
). Although KSHV-encoded vIL-6 is thought as a lytic protein, vIL-6 is detected more frequently in PEL cells than other lytic proteins. It has been demonstrated that vIL-6 is a multifunctional protein; vIL-6 can bind to IL-6 receptor gp130 in the absence of another subunit of IL-6 receptor, gp80, suggesting vIL-6 can induce cytokine signals in a broader range of cell types (Chatterjee et al., <xref ref-type="bibr" rid="B19">2002</xref>
). The signal from gp130 often secretes human IL-6 itself, raising the possibility of an autocrine loop. vIL-6 also induces VEGF expression, resulting in an indirect proliferation effect on PEL cells (Aoki et al., <xref ref-type="bibr" rid="B4">1999</xref>
).</p>
</sec>
<sec><title>Multicentric Castleman’s disease</title>
<p>Multicentric Castleman’s disease is characterized by plasmacytic lymphoadenopathy with polyclonal hyperimmunoglobulinemia and high levels of IL-6 in the serum. Histologically, follicular hyperplasia with proliferation of plasma cells and hyaline vascular alterations are observed in the lymph nodes (Figure <xref ref-type="fig" rid="F1">1</xref>
F). Two distinct histopathologic subtypes have been reported; the hyaline vascular type (HV type) and the plasma cell type (PC-type). The HV type is characterized by enlarged lymphoid follicles, hyalinized germinal centers within an expanded mantle zone, and a highly vascularized interfollicular area. In contrast, in the PC-type, remarkable infiltration of plasma cells is observed in the interfollicular area. Among these mantle zone cells, there are variable numbers of the larger cells, which are approximately twice the size of mantle zone lymphocytes. These cells are characterized by a moderate amount of amphophilic cytoplasm and a large vesicular nucleus containing one or sometimes two prominent nucleoli. These cells have been called plasmablasts, although they frequently have immunoblastic features (Dupin et al., <xref ref-type="bibr" rid="B22">2000</xref>
). The plasmablasts are also found in the interfollicular area of PC-type MCD frequently. In some, but not all cases of MCD, KSHV is detected (Soulier et al., <xref ref-type="bibr" rid="B78">1995</xref>
). Using PCR, KSHV is frequently detected in tissues obtained from patients with MCD associated with HIV infection, but is very rare in MCD cases without HIV infection (Suda et al., <xref ref-type="bibr" rid="B79">2001</xref>
). KSHV was also detected with high frequency in MCD complicated with polyneuropathy, organomegaly, endocrinopathy, M protein, and skin changes (POEMS) syndrome (Belec et al., <xref ref-type="bibr" rid="B8">1999</xref>
). Immunohistochemistry for LANA-1 revealed that KSHV-infected cells are localized in the mantle zone of lymphoid follicles (Figure <xref ref-type="fig" rid="F1">1</xref>
G). Besides LANA-1, other KSHV-encoded lytic proteins such as vIL-6, K8, and K8.1 are also detected in these cells, suggesting KSHV<sup>+</sup>
MCD is associated with KSHV-lytic infection (Dupin et al., <xref ref-type="bibr" rid="B23">1999</xref>
; Katano et al., <xref ref-type="bibr" rid="B42">2000b</xref>
). The KSHV-encoded vIL-6 plays a role in the proliferation of plasma cells, and is also detected in patients’ sera at high levels, suggesting high levels of vIL-6 are associated with MCD pathogenesis (Parravicini et al., <xref ref-type="bibr" rid="B62">1997</xref>
). High levels of KSHV DNA are also detected in the serum, which can be a marker of progressive MCD.</p>
</sec>
<sec><title>Large B-cell lymphoma arising in KSHV-associated MCD</title>
<p>Large B-cell lymphoma arising in KSHV-associated MCD is characterized by a monoclonal proliferation of KSHV-infected lymphoid cells resembling plasmablasts expressing IgM, arising in the setting of MCD (Dupin et al., <xref ref-type="bibr" rid="B22">2000</xref>
; Oksenhendler et al., <xref ref-type="bibr" rid="B60">2002</xref>
). The small confluent sheets of LANA-1<sup>+</sup>
plasmablasts are seen in the interfollicular zone of KSHV-associated MCD. This type of lymphoma occurs in the lymph node or spleen with generalized lymphadenitis and/or massive splenomegaly. Plasmablasts show stippled nuclear staining for LANA-1 and cytoplasmic staining for vIL-6, and strongly express cIgM with λ light-chain restriction.</p>
</sec>
</sec>
<sec><title>Conclusion</title>
<p>Since the discovery of KSHV, 16 years have passed. During the period, some useful diagnostic tools have been developed for pathological examination. Anti-LANA-1 antibody is the most powerful tool for diagnosis of pathological samples of KSHV infection. LANA-1 expression is specific to KSHV infection, because all KSHV-infected cells express LANA-1. Real-time PCR is also a powerful tool for diagnosis. Thus, it is not difficult to diagnose KSHV infection in pathological samples. On the other hand, the pathogenesis, and especially the oncogenesis, of KSHV remain unknown. Although many KSHV-encoded proteins have been characterized and their <italic>in vitro</italic>
functions revealed, it is still not clear if KSHV can fully transform or immortalize endothelial cells. It has been shown that LANA-1 plays a central role in KSHV pathogenesis. However, LANA-1 is not enough for KSHV oncogenesis. KSHV-encoded non-transforming proteins may collaborate to establish and maintain appropriate environment for KSHV-infected cells. Further studies should reveal the mechanism of the collaboration by KSHV-encoded proteins.</p>
</sec>
<sec><title>Conflict of Interest Statement</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
</body>
<back><ack><p>The authors thank Ms. Yuko Sato for her excellent technical assistance. This study was partly supported by a grant for Research on Publicly Essential Drugs and Medical Devices from the Japan Health Sciences Foundation (to Harutaka Katano and Takayuki Kanno, No. SAA4832); Health and Labor Sciences Research Grants (to Harutaka Katano, No. H21-AIDS-Ippan-006, H22-AIDS-Ippan-002, H23-AIDS-Ippan-002, H21-Shinko-Ippan-009) from the Ministry of Health, Labour and Welfare; and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to Harutaka Katano, No. 21590520 and 22390243).</p>
</ack>
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