Genetic Variation of Human Papillomavirus Type 16 in Individual Clinical Specimens Revealed by Deep Sequencing
Identifieur interne : 000189 ( Ncbi/Curation ); précédent : 000188; suivant : 000190Genetic Variation of Human Papillomavirus Type 16 in Individual Clinical Specimens Revealed by Deep Sequencing
Auteurs : Iwao Kukimoto [Japon] ; Tomohiko Maehama [Japon] ; Tsuyoshi Sekizuka [Japon] ; Yumiko Ogasawara [Japon] ; Kazunari Kondo [Japon] ; Rika Kusumoto-Matsuo [Japon] ; Seiichiro Mori [Japon] ; Yoshiyuki Ishii [Japon] ; Takamasa Takeuchi [Japon] ; Toshiyuki Yamaji [Japon] ; Fumihiko Takeuchi [Japon] ; Kentaro Hanada [Japon] ; Makoto Kuroda [Japon]Source :
- PLoS ONE [ 1932-6203 ] ; 2013.
Abstract
Viral genetic diversity within infected cells or tissues, called viral quasispecies, has been mostly studied for RNA viruses, but has also been described among DNA viruses, including human papillomavirus type 16 (HPV16) present in cervical precancerous lesions. However, the extent of HPV genetic variation in cervical specimens, and its involvement in HPV-induced carcinogenesis, remains unclear. Here, we employ deep sequencing to comprehensively analyze genetic variation in the HPV16 genome isolated from individual clinical specimens. Through overlapping full-circle PCR, approximately 8-kb DNA fragments covering the whole HPV16 genome were amplified from HPV16-positive cervical exfoliated cells collected from patients with either low-grade squamous intraepithelial lesion (LSIL) or invasive cervical cancer (ICC). Deep sequencing of the amplified HPV16 DNA enabled
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DOI: 10.1371/journal.pone.0080583
PubMed: 24236186
PubMed Central: 3827439
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Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry and Cell Biology, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Kuroda, Makoto" sort="Kuroda, Makoto" uniqKey="Kuroda M" first="Makoto" last="Kuroda">Makoto Kuroda</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno 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sortKey="Kukimoto, Iwao" sort="Kukimoto, Iwao" uniqKey="Kukimoto I" first="Iwao" last="Kukimoto">Iwao Kukimoto</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Maehama, Tomohiko" sort="Maehama, Tomohiko" uniqKey="Maehama T" first="Tomohiko" last="Maehama">Tomohiko Maehama</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Department of Biochemistry and Cell Biology, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry and Cell Biology, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Sekizuka, Tsuyoshi" sort="Sekizuka, Tsuyoshi" uniqKey="Sekizuka T" first="Tsuyoshi" last="Sekizuka">Tsuyoshi Sekizuka</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Ogasawara, Yumiko" sort="Ogasawara, Yumiko" uniqKey="Ogasawara Y" first="Yumiko" last="Ogasawara">Yumiko Ogasawara</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Kondo, Kazunari" sort="Kondo, Kazunari" uniqKey="Kondo K" first="Kazunari" last="Kondo">Kazunari Kondo</name><affiliation wicri:level="3"><nlm:aff id="aff3"><addr-line>NTT Medical Center Tokyo, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>NTT Medical Center Tokyo, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Kusumoto Matsuo, Rika" sort="Kusumoto Matsuo, Rika" uniqKey="Kusumoto Matsuo R" first="Rika" last="Kusumoto-Matsuo">Rika Kusumoto-Matsuo</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Mori, Seiichiro" sort="Mori, Seiichiro" uniqKey="Mori S" first="Seiichiro" last="Mori">Seiichiro Mori</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Ishii, Yoshiyuki" sort="Ishii, Yoshiyuki" uniqKey="Ishii Y" first="Yoshiyuki" last="Ishii">Yoshiyuki Ishii</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Takeuchi, Takamasa" sort="Takeuchi, Takamasa" uniqKey="Takeuchi T" first="Takamasa" last="Takeuchi">Takamasa Takeuchi</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Yamaji, Toshiyuki" sort="Yamaji, Toshiyuki" uniqKey="Yamaji T" first="Toshiyuki" last="Yamaji">Toshiyuki Yamaji</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Department of Biochemistry and Cell Biology, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry and Cell Biology, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Takeuchi, Fumihiko" sort="Takeuchi, Fumihiko" uniqKey="Takeuchi F" first="Fumihiko" last="Takeuchi">Fumihiko Takeuchi</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Hanada, Kentaro" sort="Hanada, Kentaro" uniqKey="Hanada K" first="Kentaro" last="Hanada">Kentaro Hanada</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Department of Biochemistry and Cell Biology, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Department of Biochemistry and Cell Biology, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author><author><name sortKey="Kuroda, Makoto" sort="Kuroda, Makoto" uniqKey="Kuroda M" first="Makoto" last="Kuroda">Makoto Kuroda</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo, Japan</addr-line></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Pathogen Genomics Center, National Institute of Infectious Diseases, Tokyo</wicri:regionArea><placeName><settlement type="city">Tokyo</settlement><region type="région">Région de Kantō</region></placeName></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2013">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Viral genetic diversity within infected cells or tissues, called viral quasispecies, has been mostly studied for RNA viruses, but has also been described among DNA viruses, including human papillomavirus type 16 (HPV16) present in cervical precancerous lesions. However, the extent of HPV genetic variation in cervical specimens, and its involvement in HPV-induced carcinogenesis, remains unclear. Here, we employ deep sequencing to comprehensively analyze genetic variation in the HPV16 genome isolated from individual clinical specimens. Through overlapping full-circle PCR, approximately 8-kb DNA fragments covering the whole HPV16 genome were amplified from HPV16-positive cervical exfoliated cells collected from patients with either low-grade squamous intraepithelial lesion (LSIL) or invasive cervical cancer (ICC). Deep sequencing of the amplified HPV16 DNA enabled <italic>de novo</italic> assembly of the full-length HPV16 genome sequence for each of 7 specimens (5 LSIL and 2 ICC samples). Subsequent alignment of read sequences to the assembled HPV16 sequence revealed that 2 LSILs and 1 ICC contained nucleotide variations within E6, E1 and the non-coding region between E5 and L2 with mutation frequencies of 0.60% to 5.42%. In transient replication assays, a novel E1 mutant found in ICC, E1 Q381E, showed reduced ability to support HPV16 origin-dependent replication. In addition, partially deleted E2 genes were detected in 1 LSIL sample in a mixed state with the intact E2 gene. Thus, the methods used in this study provide a fundamental framework for investigating the influence of HPV somatic genetic variation on cervical carcinogenesis. </p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Zur Hausen, H" uniqKey="Zur Hausen H">H zur Hausen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="De Sanjose, S" uniqKey="De Sanjose S">S de Sanjose</name></author><author><name sortKey="Quint, Wg" uniqKey="Quint W">WG Quint</name></author><author><name sortKey="Alemany, L" uniqKey="Alemany L">L Alemany</name></author><author><name sortKey="Geraets, Dt" uniqKey="Geraets D">DT Geraets</name></author><author><name sortKey="Klaustermeier, Je" uniqKey="Klaustermeier J">JE Klaustermeier</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kajitani, N" uniqKey="Kajitani N">N Kajitani</name></author><author><name sortKey="Satsuka, A" uniqKey="Satsuka A">A 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