Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review
  • Published:

Viral epigenomes in human tumorigenesis

Abstract

Viruses are associated with 15–20% of human cancers worldwide. In the last century, many studies were directed towards elucidating the molecular mechanisms and genetic alterations by which viruses cause cancer. The importance of epigenetics in the regulation of gene expression has prompted the investigation of virus and host interactions not only at the genetic level but also at the epigenetic level. In this study, we summarize the published epigenetic information relating to the genomes of viruses directly or indirectly associated with the establishment of tumorigenic processes. We also review aspects such as viral replication and latency associated with epigenetic changes and summarize what is known about epigenetic alterations in host genomes and the implications of these for the tumoral process. The advances made in characterizing epigenetic features in cancer-causing viruses have improved our understanding of their functional mechanisms. Knowledge of the epigenetic changes that occur in the genome of these viruses should provide us with markers for following cancer progression, as well as new tools for cancer therapy.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Ambinder RF, Robertson KD, Tao Q . (1999). DNA methylation and the Epstein-Barr virus. Semin Cancer Biol 9: 369–375.

    CAS  PubMed  Google Scholar 

  • Aresté C, Blackbourn DJ . (2009). Modulation of the immune system by Kaposi's sarcoma-associated herpesvirus. Trends Microbiol 17: 119–129.

    PubMed  Google Scholar 

  • Avvakumov N, Torchia J, Mymryk JS . (2003). Interaction of the HPV E7 proteins with the pCAF acetyltransferase. Oncogene 22: 3833–3841.

    CAS  PubMed  Google Scholar 

  • Badal S, Badal V, Calleja-Macias IE, Kalantari M, Chuang LSH, Li BFL et al. (2004). The human papillomavirus-18 genome is efficiently targeted by cellular DNA methylation. Virology 324: 483–492.

    CAS  PubMed  Google Scholar 

  • Badal V, Chuang LS, Tan EH, Badal S, Villa LL, Wheeler CM et al. (2003). CpG methylation of human papillomavirus type 16 DNA in cervical cancer cell lines and in clinical specimens: genomic hypomethylation correlates with carcinogenic progression. J Virol 77: 6227–6234.

    PubMed  PubMed Central  Google Scholar 

  • Ballestas ME, Chatis PA, Kaye KM . (1999). Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284: 641–644.

    CAS  PubMed  Google Scholar 

  • Barozzi P, Potenza L, Riva G, Vallerini D, Quadrelli C, Bosco R et al. (2007). B cells and herpesviruses: a model of lymphoproliferation. Autoimmun Rev 7: 132–136.

    PubMed  Google Scholar 

  • Beck J, Nassal M . (2007). Hepatitis B virus replication. World J Gastroenterol 13: 48–64.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bednarik DP, Cook JA, Pitha PM . (1990). Inactivation of the HIV LTR by DNA CpG methylation: evidence for a role in latency. EMBO J 9: 1157–1164.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bernat A, Avvakumov N, Mymryk JS, Banks L . (2003). Interaction between the HPV E7 oncoprotein and the transcriptional coactivator p300. Oncogene 22: 7871–7881.

    PubMed  Google Scholar 

  • Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ et al. (2005). Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169–181.

    CAS  PubMed  Google Scholar 

  • Bernstein BE, Meissner A, Lander ES . (2007). The mammalian epigenome. Cell 128: 669–681.

    CAS  PubMed  Google Scholar 

  • Bhattacharjee B, Sengupta S . (2006). CpG methylation of HPV 16 LCR at E2 binding site proximal to P97 is associated with cervical cancer in presence of intact E2. Virology 354: 280–285.

    CAS  PubMed  Google Scholar 

  • Bhende PM, Seaman WT, Delecluse HJ, Kenney SC . (2005). BZLF1 activation of the methylated form of the BRLF1 immediate-early promoter is regulated by BZLF1 residue 186. J Virol 79: 7338–7348.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F et al. (2009). A review of human carcinogens–Part B: biological agents. Lancet Oncol 10: 321–322.

    PubMed  Google Scholar 

  • Brandsma JL, Sun Y, Lizardi PM, Tuck DP, Zelterman D, Haines III GK et al. (2009). Distinct human papillomavirus type 16 methylomes in cervical cells at different stages of premalignancy. Virology 389: 100–107.

    CAS  PubMed  Google Scholar 

  • Brehm A, Nielsen SJ, Miska EA, McCance DJ, Reid JL, Bannister AJ et al. (1999). The E7 oncoprotein associates with Mi2 and histone deacetylase activity to promote cell growth. EMBO J 18: 2449–2458.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Breitbart M, Rohwer F . (2005). Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13: 278–284.

    CAS  PubMed  Google Scholar 

  • Brooks AR, Harkins RN, Wang P, Qian HS, Liu P, Rubanyi GM . (2004). Transcriptional silencing is associated with extensive methylation of the CMV promoter following adenoviral gene delivery to muscle. J Gene Med 6: 395–404.

    CAS  PubMed  Google Scholar 

  • Bubman D, Guasparri I, Cesarman E . (2007). Deregulation of c-Myc in primary effusion lymphoma by Kaposi's sarcoma herpesvirus latency-associated nuclear antigen. Oncogene 26: 4979–4986.

    CAS  PubMed  Google Scholar 

  • Burgers WA, Blanchon L, Pradhan S, Launoit Yd, Kouzarides T, Fuks F . (2006). Viral oncoproteins target the DNA methyltransferases. Oncogene 26: 1650–1655.

    PubMed  PubMed Central  Google Scholar 

  • Butel JS . (2000). Viral carcinogenesis: revelation of molecular mechanisms and etiology of human disease. Carcinogenesis 21: 405–426.

    CAS  PubMed  Google Scholar 

  • Cai X, Schafer A, Lu S, Bilello JP, Desrosiers RC, Edwards R et al. (2006). Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog 2: e23.

    PubMed  PubMed Central  Google Scholar 

  • Carbone A, Cabras A, Gloghini A . (2007). HIV-associated Hodgkin's lymphoma. Antiapoptotic pathways and mechanisms for immune escape by tumor cells in the setting of improved immunity. Int J Biol Markers 22: 161–163.

    CAS  PubMed  Google Scholar 

  • Carbone A, Gloghini A . (2005). AIDS-related lymphomas: from pathogenesis to pathology. Br J Haematol 130: 662–670.

    CAS  PubMed  Google Scholar 

  • Carbone A, Gloghini A, Serraino D, Spina M . (2009). HIV-associated Hodgkin lymphoma. Curr Opin HIV AIDS 4: 3–10.

    PubMed  Google Scholar 

  • Cinatl Jr J, Cinatl J, Vogel JU, Rabenau H, Kornhuber B, Doerr HW . (1996). Modulatory effects of human cytomegalovirus infection on malignant properties of cancer cells. Intervirology 39: 259–269.

    PubMed  Google Scholar 

  • Cinatl J, Scholz M, Kotchetkov R, Vogel J-U, Wilhelm Doerr H . (2004). Molecular mechanisms of the modulatory effects of HCMV infection in tumor cell biology. Trends Mol Med 10: 19–23.

    CAS  PubMed  Google Scholar 

  • Colot V, Rossignol J-L . (1999). Eukaryotic DNA methylation as an evolutionary device. BioEssays 21: 402–411.

    CAS  PubMed  Google Scholar 

  • Cotter MA, Robertson ES . (1999). The latency-associated nuclear antigen tethers the Kaposi's sarcoma-associated herpesvirus genome to host chromosomes in body cavity-based lymphoma cells. Virology 264: 254–264.

    CAS  PubMed  Google Scholar 

  • Cougot D, Neuveut C, Buendia MA . (2005). HBV induced carcinogenesis. J Clin Virol 34: S75–S78.

    CAS  PubMed  Google Scholar 

  • Cougot D, Wu Y, Cairo S, Caramel J, Renard C-A, Levy L et al. (2007). The Hepatitis B Virus X protein functionally interacts with CREB-binding protein/p300 in the regulation of CREB-mediated transcription. J Biol Chem 282: 4277–4287.

    CAS  PubMed  Google Scholar 

  • Countryman JK, Gradoville L, Miller G . (2008). Histone hyperacetylation occurs on promoters of lytic cycle regulatory genes in Epstein-Barr virus-infected cell lines which are refractory to disruption of latency by histone deacetylase inhibitors. J Virol 82: 4706–4719.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cuevas-Bennett C, Shenk T . (2008). Dynamic histone H3 acetylation and methylation at human cytomegalovirus promoters during replication in fibroblasts. J Virol 82: 9525–9536.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cullen BR . (2009). Viral and cellular messenger RNA targets of viral microRNAs. Nature 457: 421–425.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chang Y, Lee HH, Chen YT, Lu J, Wu SY, Chen CW et al. (2006). Induction of the early growth response 1 gene by Epstein-Barr virus lytic transactivator Zta. J Virol 80: 7748–7755.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Ueda K, Sakakibara S, Okuno T, Parravicini C, Corbellino M et al. (2001). Activation of latent Kaposi's sarcoma-associated herpesvirus by demethylation of the promoter of the lytic transactivator. Proc Natl Acad Sci 98: 4119–4124.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chuang JC, Jones PA . (2007). Epigenetics and microRNAs. Pediatr Res 61: 24R–29R.

    CAS  PubMed  Google Scholar 

  • Damania B . (2007). DNA tumor viruses and human cancer. Trends Microbiol 15: 38–44.

    CAS  PubMed  Google Scholar 

  • Danos O, Katinka M, Yaniv M . (1980). Molecular cloning, refined physical map and heterogeneity of methylation sites of papilloma virus type 1a DNA. Eur J Biochem 109: 457–461.

    CAS  PubMed  Google Scholar 

  • de Villiers E-M, Fauquet C, Broker TR, Bernard H-U, zur Hausen H . (2004). Classification of papillomaviruses. Virology 324: 17–27.

    CAS  PubMed  Google Scholar 

  • DeCaprio JA . (2009). How the Rb tumor suppressor structure and function was revealed by the study of Adenovirus and SV40. Virology 384: 274–284.

    CAS  PubMed  Google Scholar 

  • Derse D, Crise B, Li Y, Princler G, Lum N, Stewart C et al. (2007). Human T-cell leukemia virus type 1 integration target sites in the human genome: comparison with those of other retroviruses. J Virol 81: 6731–6741.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Di Bartolo DL, Cannon M, Liu YF, Renne R, Chadburn A, Boshoff C et al. (2008). KSHV LANA inhibits TGF-beta signaling through epigenetic silencing of the TGF-beta type II receptor. Blood 111: 4731–4740.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dickerson SJ, Xing Y, Robinson AR, Seaman WT, Gruffat H, Kenney SC . (2009). Methylation-dependent binding of the epstein-barr virus BZLF1 protein to viral promoters. PLoS Pathog 5: e1000356.

    PubMed  PubMed Central  Google Scholar 

  • Doerfler W . (1991). Patterns of DNA methylation–evolutionary vestiges of foreign DNA inactivation as a host defense mechanism. A proposal. Biol Chem Hoppe-Seyler 372: 557–564.

    CAS  PubMed  Google Scholar 

  • Doerfler W . (1996). A new concept in (adenoviral) oncogenesis: integration of foreign DNA and its consequences. Biochim Biophys Acta (BBA) Rev Cancer 1288: F79–F99.

    Google Scholar 

  • Doi K, Wu X, Taniguchi Y, Yasunaga J, Satou Y, Okayama A et al. (2005). Preferential selection of human T-cell leukemia virus type I provirus integration sites in leukemic versus carrier states. Blood 106: 1048–1053.

    CAS  PubMed  Google Scholar 

  • Dolken L, Pfeffer S, Koszinowski UH . (2009). Cytomegalovirus microRNAs. Virus Genes 38: 355–364.

    PubMed  Google Scholar 

  • Dourmishev LA, Dourmishev AL, Palmeri D, Schwartz RA, Lukac DM . (2003). Molecular genetics of Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8) epidemiology and pathogenesis. Microbiol Mol Biol Rev 67: 175–212.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duverger A, Jones J, May J, Bibollet-Ruche F, Wagner FA, Cron RQ et al. (2009). Determinants of the establishment of human immunodeficiency virus type 1 latency. J Virol 83: 3078–3093.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dyson PJ, Farrell PJ . (1985). Chromatin structure of Epstein-Barr virus. J Gen Virol 66: 1931–1940.

    CAS  PubMed  Google Scholar 

  • Elgui de Oliveira D . (2007). DNA viruses in human cancer: an integrated overview on fundamental mechanisms of viral carcinogenesis. Cancer Lett 247: 182–196.

    CAS  PubMed  Google Scholar 

  • Esteller M . (2008). Epigenetics in cancer. N Engl J Med 358: 1148–1159.

    CAS  PubMed  Google Scholar 

  • Feinberg AP, Cui H, Ohlsson R . (2002). DNA methylation and genomic imprinting: insights from cancer into epigenetic mechanisms. Semin Cancer Biol 12: 389–398.

    CAS  PubMed  Google Scholar 

  • Fejer G, Koroknai A, Banati F, Gyory I, Salamon D, Wolf H et al. (2008). Latency type-specific distribution of epigenetic marks at the alternative promoters Cp and Qp of Epstein-Barr virus. J Gen Virol 89: 1364–1370.

    CAS  PubMed  Google Scholar 

  • Feng H, Shuda M, Chang Y, Moore PS . (2008). Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319: 1096–1100.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez AF, Rosales C, Lopez-Nieva P, Grana O, Ballestar E, Ropero S et al. (2009). The dynamic DNA methylomes of double-stranded DNA viruses associated with human cancer. Genome Res 19: 438–451.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrari R, Berk AJ, Kurdistani SK . (2009). Viral manipulation of the host epigenome for oncogenic transformation. Nat Rev Genet 10: 290–294.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flanagan JM . (2007). Host epigenetic modifications by oncogenic viruses. Br J Cancer 96: 183–188.

    CAS  PubMed  Google Scholar 

  • Fraga MF, Esteller M . (2005). Towards the human cancer epigenome: a first draft of histone modifications. Cell Cycle 4: 1377–1381.

    CAS  PubMed  Google Scholar 

  • Friborg J, Kong W-p, Hottiger MO, Nabel GJ . (1999). p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 402: 889–894.

    CAS  PubMed  Google Scholar 

  • Fujimuro M, Wu FY, ApRhys C, Kajumbula H, Young DB, Hayward GS et al. (2003). A novel viral mechanism for dysregulation of beta-catenin in Kaposi's sarcoma-associated herpesvirus latency. Nat Med 9: 300–306.

    CAS  PubMed  Google Scholar 

  • Fukayama M, Hino R, Uozaki H . (2008). Epstein-Barr virus and gastric carcinoma: virus-host interactions leading to carcinoma. Cancer Sci 99: 1726–1733.

    CAS  PubMed  Google Scholar 

  • Georg WB . (2009). Epstein-Barr virus and the pathogenesis of Burkitt's lymphoma: more questions than answers. Int J Cancer 124: 1745–1755.

    Google Scholar 

  • Gerle B, Koroknai A, Fejer G, Bakos A, Banati F, Szenthe K et al. (2007). Acetylated histone H3 and H4 mark the upregulated LMP2A promoter of Epstein-Barr virus in lymphoid cells. J Virol 81: 13242–13247.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Godden-Kent D, Talbot SJ, Boshoff C, Chang Y, Moore P, Weiss RA et al. (1997). The cyclin encoded by Kaposi's sarcoma-associated herpesvirus stimulates cdk6 to phosphorylate the retinoblastoma protein and histone H1. J Virol 71: 4193–4198.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goel A, Li M-S, Nagasaka T, Shin SK, Fuerst F, Ricciardiello L et al. (2006). Association of JC Virus T-antigen expression with the methylator phenotype in sporadic colorectal cancers. Gastroenterology 130: 1950–1961.

    CAS  PubMed  Google Scholar 

  • Gottwein E, Cullen BR . (2008). Viral and cellular MicroRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 3: 375–387.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gray KS, Allen III RD, Farrell ML, Forrest JC, Speck SH . (2009). Alternatively Initiated Gene 50/RTA transcripts expressed during murine and human gammaherpesvirus reactivation from latency. J Virol 83: 314–328.

    CAS  PubMed  Google Scholar 

  • Grey F, Hook L, Nelson J . (2008). The functions of herpesvirus-encoded microRNAs. Med Microbiol Immunol 197: 261–267.

    CAS  PubMed  Google Scholar 

  • Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM . (2007). Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet 370: 59–67.

    PubMed  Google Scholar 

  • Grundhoff A, Sullivan CS, Ganem D . (2006). A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. RNA 12: 733–750.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guasparri I, Keller SA, Cesarman E . (2004). KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med 199: 993–1003.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Y, Li Y, Mu S, Zhang J, Yan Z . (2009). Evidence that methylation of hepatitis B virus covalently closed circular DNA in liver tissues of patients with chronic hepatitis B modulates HBV replication. J Med Virol 81: 1177–1183.

    CAS  PubMed  Google Scholar 

  • Gurtsevitch VE . (2008). Human oncogenic viruses: hepatitis B and hepatitis C viruses and their role in hepatocarcinogenesis. Biochemistry (Mosc) 73: 504–513.

    CAS  Google Scholar 

  • Han Y, Lin YB, An W, Xu J, Yang HC, O'Connell K et al. (2008). Orientation-dependent regulation of integrated HIV-1 expression by host gene transcriptional readthrough. Cell Host Microbe 4: 134–146.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heather J, Flower K, Isaac S, Sinclair AJ . (2009). The Epstein-Barr virus lytic cycle activator Zta interacts with methylated ZRE in the promoter of host target gene egr1. J Gen Virol 90: 1450–1454.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Herceg Z, Paliwal A . (2009). HBV protein as a double-barrel shot-gun targets epigenetic landscape in liver cancer. J Hepatol 50: 252–255.

    CAS  PubMed  Google Scholar 

  • Herman JG, Baylin SB . (2003). Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349: 2042–2054.

    CAS  PubMed  Google Scholar 

  • Hino R, Uozaki H, Murakami N, Ushiku T, Shinozaki A, Ishikawa S et al. (2009). Activation of DNA methyltransferase 1 by EBV latent membrane protein 2A leads to promoter hypermethylation of PTEN gene in gastric carcinoma. Cancer Res 69: 2766–2774.

    CAS  PubMed  Google Scholar 

  • Hinuma Y, Nagata K, Hanaoka M, Nakai M, Matsumoto T, Kinoshita KI et al. (1981). Adult T-cell leukemia: antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proc Natl Acad Sci 78: 6476–6480.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holliday R . (1987). The inheritance of epigenetic defects. Science 238: 163–170.

    CAS  PubMed  Google Scholar 

  • Horenstein MG, Moontasri NJ, Cesarman E . (2008). The pathobiology of Kaposi's sarcoma: advances since the onset of the AIDS epidemic. J Cutan Pathol 35 (Suppl 2): 40–44.

    PubMed  Google Scholar 

  • Horikawa I, Barrett JC . (2003). Transcriptional regulation of the telomerase hTERT gene as a target for cellular and viral oncogenic mechanisms. Carcinogenesis 24: 1167–1176.

    CAS  PubMed  Google Scholar 

  • Howie HL, Katzenellenbogen RA, Galloway DA . (2009). Papillomavirus E6 proteins. Virology 384: 324–334.

    CAS  PubMed  Google Scholar 

  • Hublarova P, Hrstka R, Rotterova P, Rotter L, Coupkova M, Badal V et al. (2009). Prediction of human papillomavirus 16 e6 gene expression and cervical intraepithelial neoplasia progression by methylation status. Int J Gynecol Cancer 19: 321–325.

    PubMed  Google Scholar 

  • International Collaboration on HIV and Cancer (2000). Highly active antiretroviral therapy and incidence of cancer in human immunodeficiency virus-infected adults. J Natl Cancer Inst 92: 1823–1830.

    Google Scholar 

  • Ioudinkova E, Arcangeletti MC, Rynditch A, De Conto F, Motta F, Covan S et al. (2006). Control of human cytomegalovirus gene expression by differential histone modifications during lytic and latent infection of a monocytic cell line. Gene 384: 120–128.

    CAS  PubMed  Google Scholar 

  • Ishida T, Hamano A, Koiwa T, Watanabe T . (2006). 5′ long terminal repeat (LTR)-selective methylation of latently infected HIV-1 provirus that is demethylated by reactivation signals. Retrovirology 3: 69.

    PubMed  PubMed Central  Google Scholar 

  • Javier RT, Butel JS . (2008). The history of tumor virology. Cancer Res 68: 7693–7706.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jenner RG, Alba MM, Boshoff C, Kellam P . (2001). Kaposi's sarcoma-associated herpesvirus latent and lytic gene expression as revealed by DNA arrays. J Virol 75: 891–902.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang G, Espeseth A, Hazuda DJ, Margolis DM . (2007). c-Myc and Sp1 contribute to proviral latency by recruiting histone deacetylase 1 to the human immunodeficiency virus type 1 promoter. J Virol 81: 10914–10923.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang M, Abend JR, Johnson SF, Imperiale MJ . (2009). The role of polyomaviruses in human disease. Virology 384: 266–273.

    CAS  PubMed  Google Scholar 

  • Jin W-B, Wu F-L, Kong D, Guo A-G . (2007). HBV-encoded microRNA candidate and its target. Comput Biol Chem 31: 124–126.

    CAS  PubMed  Google Scholar 

  • Jones PA, Takai D . (2001). The role of DNA methylation in mammalian epigenetics. Science 293: 1068–1070.

    CAS  PubMed  Google Scholar 

  • Jones PA, Baylin SB . (2002). The fundamental role of epigenetic events in cancer. Nat Rev Genet 3: 415–428.

    CAS  PubMed  Google Scholar 

  • Jung JK, Arora P, Pagano JS, Jang KL . (2007). Expression of DNA Methyltransferase 1 is activated by hepatitis B Virus X protein via a regulatory circuit involving the p16INK4a-cyclin D1-CDK 4/6-pRb-E2F1 pathway. Cancer Res 67: 5771–5778.

    CAS  PubMed  Google Scholar 

  • Kalantari M, Calleja-Macias IE, Tewari D, Hagmar B, Lie K, Barrera-Saldana HA et al. (2004). Conserved methylation patterns of human papillomavirus type 16 DNA in asymptomatic infection and cervical neoplasia. J Virol 78: 12762–12772.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kamoi K, Yamamoto K, Misawa A, Miyake A, Ishida T, Tanaka Y et al. (2006). SUV39H1 interacts with HTLV-1 tax and abrogates tax transactivation of HTLV-1 LTR. Retrovirology 3: 5.

    PubMed  PubMed Central  Google Scholar 

  • Kedes DH, Lagunoff M, Renne R, Ganem D . (1997). Identification of the gene encoding the major latency-associated nuclear antigen of the Kaposi's sarcoma-associated herpesvirus. J Clin Invest 100: 2606–2610.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim K, Garner-Hamrick PA, Fisher C, Lee D, Lambert PF . (2003). Methylation patterns of papillomavirus DNA, its influence on E2 function, and implications in viral infection. J Virol 77: 12450–12459.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kinlen L . (2004). Infections and immune factors in cancer: the role of epidemiology. Oncogene 23: 6341–6348.

    CAS  PubMed  Google Scholar 

  • Klein E, Kis LL, Klein G . (2007). Epstein-Barr virus infection in humans: from harmless to life endangering virus-lymphocyte interactions. Oncogene 26: 1297–1305.

    CAS  PubMed  Google Scholar 

  • Koiwa T, Hamano-Usami A, Ishida T, Okayama A, Yamaguchi K, Kamihira S et al. (2002). 5′-Long terminal repeat-selective CpG methylation of latent human T-cell leukemia virus type 1 provirus in vitro and in vivo. J Virol 76: 9389–9397.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lai H-C, Lin Y-W, Huang THM, Yan P, Huang R-L, Wang H-C et al. (2008). Identification of novel DNA methylation markers in cervical cancer. Int J Cancer 123: 161–167.

    CAS  PubMed  Google Scholar 

  • Lee D, Lee B, Kim J, Kim DW, Choe J . (2000). cAMP response element-binding protein-binding protein binds to human papillomavirus E2 protein and activates E2-dependent transcription. J Biol Chem 275: 7045–7051.

    CAS  PubMed  Google Scholar 

  • Lenasi T, Contreras X, Peterlin BM . (2008). Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe 4: 123–133.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Levine AJ . (2009). The common mechanisms of transformation by the small DNA tumor viruses: the inactivation of tumor suppressor gene products: p53. Virology 384: 285–293.

    CAS  PubMed  Google Scholar 

  • Li H, Minarovits J . (2003). Host cell-dependent expression of latent Epstein-Barr virus genomes: regulation by DNA methylation. Adv Cancer Res 89: 133–156.

    CAS  PubMed  Google Scholar 

  • Li HP, Leu YW, Chang YS . (2005). Epigenetic changes in virus-associated human cancers. Cell Res 15: 262–271.

    CAS  PubMed  Google Scholar 

  • Li Q, Zhou F, Ye F, Gao S-J . (2008). Genetic disruption of KSHV major latent nuclear antigen LANA enhances viral lytic transcriptional program. Virology 379: 234–244.

    CAS  PubMed  Google Scholar 

  • Lin Z, Bazzaro M, Wang M-C, Chan KC, Peng S, Roden RBS . (2009). Combination of proteasome and HDAC inhibitors for uterine cervical cancer treatment. Clin Cancer Res 15: 570–577.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Zhao JJ, Wang CM, Li MY, Han P, Wang L et al. (2009). Altered expression profiles of microRNAs in a stable hepatitis B virus-expressing cell line. Chin Med J (Engl) 122: 10–14.

    CAS  Google Scholar 

  • Lu F, Day L, Gao SJ, Lieberman PM . (2006). Acetylation of the latency-associated nuclear antigen regulates repression of Kaposi's sarcoma-associated herpesvirus lytic transcription. J Virol 80: 5273–5282.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lujambio A, Ropero S, Ballestar E, Fraga MF, Cerrato C, Setien F et al. (2007). Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res 67: 1424–1429.

    CAS  PubMed  Google Scholar 

  • Lupberger J, Hildt E . (2007). Hepatitis B virus-induced oncogenesis. World J Gastroenterol 13: 74–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez I, Gardiner AS, Board KF, Monzon FA, Edwards RP, Khan SA . (2008). Human papillomavirus type 16 reduces the expression of microRNA-218 in cervical carcinoma cells. Oncogene 27: 2575–2582.

    CAS  PubMed  Google Scholar 

  • Matsuoka M, Jeang K-T . (2007). Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat Rev Cancer 7: 270–280.

    CAS  PubMed  Google Scholar 

  • McCabe MT, Low JA, Imperiale MJ, Day ML . (2006). Human polyomavirus BKV transcriptionally activates DNA methyltransferase 1 through the pRb//E2F pathway. Oncogene 25: 2727–2735.

    CAS  PubMed  Google Scholar 

  • McCormick C, Ganem D . (2005). The Kaposin B protein of KSHV activates the p38/MK2 pathway and stabilizes cytokine mRNAs. Science 307: 739–741.

    CAS  PubMed  Google Scholar 

  • McLaughlin-Drubin ME, Munger K . (2008). Viruses associated with human cancer. Biochim Biophys Acta 1782: 127–150.

    CAS  PubMed  Google Scholar 

  • McLaughlin-Drubin ME, Münger K . (2009). The human papillomavirus E7 oncoprotein. Virology 384: 335–344.

    CAS  PubMed  Google Scholar 

  • Mehta AK, Majumdar SS, Alam P, Gulati N, Brahmachari V . (2009). Epigenetic regulation of cytomegalovirus major immediate-early promoter activity in transgenic mice. Gene 428: 20–24.

    CAS  PubMed  Google Scholar 

  • Michaelis M, Doerr HW, Cinatl J . (2009). The story of human cytomegalovirus and cancer: increasing evidence and open questions. Neoplasia 11: 1–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller RH, Robinson WS . (1983). Integrated hepatitis B virus DNA sequences specifying the major viral core polypeptide are methylated in PLC/PRF/5 cells. Proc Natl Acad Sci 80: 2534–2538.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minarovits J . (2006). Epigenotypes of latent herpesvirus genomes. Curr Top Microbiol Immunol 310: 61–80.

    CAS  PubMed  Google Scholar 

  • Mok HP, Lever AM . (2007). Chromatin, gene silencing and HIV latency. Genome Biol 8: 228.

    PubMed  PubMed Central  Google Scholar 

  • Nair V, Zavolan M . (2006). Virus-encoded microRNAs: novel regulators of gene expression. Trends Microbiol 14: 169–175.

    CAS  PubMed  Google Scholar 

  • Niemhom S, Kitazawa S, Kitazawa R, Maeda S, Leopairat J . (2008). Hypermethylation of epithelial-cadherin gene promoter is associated with Epstein-Barr virus in nasopharyngeal carcinoma. Cancer Detect Prev 32: 127–134.

    CAS  PubMed  Google Scholar 

  • Niller HH, Wolf H, Minarovits J . (2008). Regulation and dysregulation of Epstein-Barr virus latency: implications for the development of autoimmune diseases. Autoimmunity 41: 298–328.

    CAS  PubMed  Google Scholar 

  • Pantry SN, Medveczky PG . (2009). Epigenetic regulation of Kaposi's sarcoma-associated herpesvirus replication. Semin Cancer Biol 19: 153–157.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park IY, Sohn BH, Yu E, Suh DJ, Chung Y-H, Lee J-H et al. (2007a). Aberrant epigenetic modifications in hepatocarcinogenesis induced by hepatitis B virus X protein. Gastroenterology 132: 1476–1494.

    CAS  PubMed  Google Scholar 

  • Park J-H, Jeon J-P, Shim S-M, Nam H-Y, Kim J-W, Han B-G et al. (2007b). Wp specific methylation of highly proliferated LCLs. Biochem Biophys Res Commun 358: 513–520.

    CAS  PubMed  Google Scholar 

  • Park J-J, Kim Y-E, Pham HT, Kim ET, Chung Y-H, Ahn J-H . (2007c). Functional interaction of the human cytomegalovirus IE2 protein with histone deacetylase 2 in infected human fibroblasts. J Gen Virol 88: 3214–3223.

    CAS  PubMed  Google Scholar 

  • Patel D, Huang SM, Baglia LA, McCance DJ . (1999). The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300. EMBO J 18: 5061–5072.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paulson EJ, Speck SH . (1999). Differential methylation of Epstein-Barr virus latency promoters facilitates viral persistence in healthy seropositive individuals. J Virol 73: 9959–9968.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Payer B, Lee JT . (2008). X chromosome dosage compensation: how mammals keep the balance. Ann Rev Genet 42: 733–772.

    CAS  PubMed  Google Scholar 

  • Peng YC, Breiding DE, Sverdrup F, Richard J, Androphy EJ . (2000). AMF-1/Gps2 binds p300 and enhances its interaction with papillomavirus E2 proteins. J Virol 74: 5872–5879.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J et al. (2004). Identification of virus-encoded MicroRNAs. Science 304: 734–736.

    CAS  PubMed  Google Scholar 

  • Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gallo RC . (1980). Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci 77: 7415–7419.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pollicino T, Belloni L, Raffa G, Pediconi N, Squadrito G, Raimondo G et al. (2006). Hepatitis B virus replication is regulated by the acetylation status of hepatitis B virus cccDNA-bound H3 and H4 histones. Gastroenterology 130: 823–837.

    CAS  PubMed  Google Scholar 

  • Proietti FA, Carneiro-Proietti ABF, Catalan-Soares BC, Murphy EL . (2005). Global epidemiology of HTLV-I infection and associated diseases. Oncogene 24: 6058–6068.

    CAS  PubMed  Google Scholar 

  • Prosch S, Stein J, Staak K, Liebenthal C, Volk HD, Kruger DH . (1996). Inactivation of the very strong HCMV immediate early promoter by DNA CpG methylation in vitro. Biol Chem Hoppe-Seyler 377: 195–201.

    CAS  PubMed  Google Scholar 

  • Radkov SA, Kellam P, Boshoff C . (2000). The latent nuclear antigen of Kaposi sarcoma-associated herpesvirus targets the retinoblastoma-E2F pathway and with the oncogene Hras transforms primary rat cells. Nat Med 6: 1121–1127.

    CAS  PubMed  Google Scholar 

  • Reeves M, Murphy J, Greaves R, Fairley J, Brehm A, Sinclair J . (2006). Autorepression of the human cytomegalovirus major immediate-early promoter/enhancer at late times of infection is mediated by the recruitment of chromatin remodeling enzymes by IE86. J Virol 80: 9998–10009.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reshmi G, Pillai MR . (2008). Beyond HPV: oncomirs as new players in cervical cancer. FEBS Lett 582: 4113–4116.

    CAS  PubMed  Google Scholar 

  • Richman DD, Margolis DM, Delaney M, Greene WC, Hazuda D, Pomerantz RJ . (2009). The challenge of finding a cure for HIV infection. Science 323: 1304–1307.

    CAS  PubMed  Google Scholar 

  • Robertson KD, Ambinder RF . (1997). Methylation of the Epstein-Barr virus genome in normal lymphocytes. Blood 90: 4480–4484.

    CAS  PubMed  Google Scholar 

  • Rollins RA, Haghighi F, Edwards JR, Das R, Zhang MQ, Ju J et al. (2006). Large-scale structure of genomic methylation patterns. Genome Res 16: 157–163.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roulston A, Marcellus RC, Branton PE . (1999). Viruses and apoptosis. Ann Rev Microbiol 53: 577–628.

    CAS  Google Scholar 

  • Sakakibara S, Ueda K, Nishimura K, Do E, Ohsaki E, Okuno T et al. (2004). Accumulation of heterochromatin components on the terminal repeat sequence of Kaposi's sarcoma-associated herpesvirus mediated by the latency-associated nuclear antigen. J Virol 78: 7299–7310.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Salamon D, Takacs M, Ujvari D, Uhlig J, Wolf H, Minarovits J et al. (2001). Protein-DNA binding and CpG methylation at nucleotide resolution of latency-associated promoters Qp, Cp, and LMP1p of Epstein-Barr virus. J Virol 75: 2584–2596.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Samols MA, Skalsky RL, Maldonado AM, Riva A, Lopez MC, Baker HV et al. (2007). Identification of cellular genes targeted by KSHV-encoded microRNAs. PLoS Pathog 3: e65.

    PubMed  PubMed Central  Google Scholar 

  • Scaria V, Hariharan M, Maiti S, Pillai B, Brahmachari SK . (2006). Host-virus interaction: a new role for microRNAs. Retrovirology 3: 68.

    PubMed  PubMed Central  Google Scholar 

  • Seeger C, Mason WS . (2000). Hepatitis B virus biology. Microbiol Mol Biol Rev 64: 51–68.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seo GJ, Fink LH, O'Hara B, Atwood WJ, Sullivan CS . (2008). Evolutionarily conserved function of a viral microRNA. J Virol 82: 9823–9828.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shamay M, Krithivas A, Zhang J, Hayward SD . (2006). Recruitment of the de novo DNA methyltransferase Dnmt3a by Kaposi's sarcoma-associated herpesvirus LANA. Proc Natl Acad Sci 103: 14554–14559.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharara AI, Hunt CM, Hamilton JD . (1996). Hepatitis C. Ann Intern Med 125: 658–668.

    CAS  PubMed  Google Scholar 

  • Shaw JE, Levinger LF, Carter Jr CW . (1979). Nucleosomal structure of Epstein-Barr virus DNA in transformed cell lines. J Virol 29: 657–665.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shon JK, Shon BH, Park IY, Lee SU, Fa L, Chang KY et al. (2009). Hepatitis B virus-X protein recruits histone deacetylase 1 to repress insulin-like growth factor binding protein 3 transcription. Virus Res 139: 14–21.

    CAS  PubMed  Google Scholar 

  • Soderberg-Naucier C . (2006). Does cytomegalovirus play a causative role in the development of various inflammatory diseases and cancer? J Intern Med 259: 219–246.

    Google Scholar 

  • Steenbergen RD, Walboomers JM, Meijer CJ, van der Raaij-Helmer EM, Parker JN, Chow LT et al. (1996). Transition of human papillomavirus type 16 and 18 transfected human foreskin keratinocytes towards immortality: activation of telomerase and allele losses at 3p, 10p, 11q and/or 18q. Oncogene 13: 1249–1257.

    CAS  PubMed  Google Scholar 

  • Stuber G, Mattsson K, Flaberg E, Kati E, Markasz L, Sheldon JA et al. (2007). HHV-8 encoded LANA-1 alters the higher organization of the cell nucleus. Mol Cancer 6: 28.

    PubMed  PubMed Central  Google Scholar 

  • Sun R, Lin SF, Gradoville L, Yuan Y, Zhu F, Miller G . (1998). A viral gene that activates lytic cycle expression of Kaposi's sarcoma-associated herpesvirus. Proc Natl Acad Sci 95: 10866–10871.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takeda S, Maeda M, Morikawa S, Taniguchi Y, Yasunaga J-i, Nosaka K et al. (2004). Genetic and epigenetic inactivation of tax gene in adult T-cell leukemia cells. Int J Cancer 109: 559–567.

    CAS  PubMed  Google Scholar 

  • Taniguchi Y, Nosaka K, Yasunaga J, Maeda M, Mueller N, Okayama A et al. (2005). Silencing of human T-cell leukemia virus type I gene transcription by epigenetic mechanisms. Retrovirology 2: 64.

    PubMed  PubMed Central  Google Scholar 

  • Tao Q, Robertson KD . (2003). Stealth technology: how Epstein-Barr virus utilizes DNA methylation to cloak itself from immune detection. Clin Immunol 109: 53–63.

    CAS  PubMed  Google Scholar 

  • Tao Q, Robertson KD, Manns A, Hildesheim A, Ambinder RF . (1998). The Epstein-Barr virus major latent promoter Qp is constitutively active, hypomethylated, and methylation sensitive. J Virol 72: 7075–7083.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thain A, Jenkins O, Clarke AR, Gaston K . (1996). CpG methylation directly inhibits binding of the human papillomavirus type 16 E2 protein to specific DNA sequences. J Virol 70: 7233–7235.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tischoff I, Tannapfe A . (2008). DNA methylation in hepatocellular carcinoma. World J Gastroenterol 14: 1741–1748.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai CL, Li HP, Lu YJ, Hsueh C, Liang Y, Chen CL et al. (2006). Activation of DNA methyltransferase 1 by EBV LMP1 Involves c-Jun NH(2)-terminal kinase signaling. Cancer Res 66: 11668–11676.

    CAS  PubMed  Google Scholar 

  • Turan T, Kalantari M, Calleja-Macias IE, Cubie HA, Cuschieri K, Villa LL et al. (2006). Methylation of the human papillomavirus-18 L1 gene: a biomarker of neoplastic progression? Virology 349: 175–183.

    CAS  PubMed  Google Scholar 

  • Turan T, Kalantari M, Cuschieri K, Cubie HA, Skomedal H, Bernard HU . (2007). High-throughput detection of human papillomavirus-18 L1 gene methylation, a candidate biomarker for the progression of cervical neoplasia. Virology 361: 185–193.

    CAS  PubMed  Google Scholar 

  • Verma SC, Choudhuri T, Robertson ES . (2007). The minimal replicator element of the Kaposi's sarcoma-associated herpesvirus terminal repeat supports replication in a semiconservative and cell-cycle-dependent manner. J Virol 81: 3402–3413.

    CAS  PubMed  Google Scholar 

  • Vivekanandan P, Thomas D, Torbenson M . (2008). Hepatitis B viral DNA is methylated in liver tissues. J Viral Hepat 15: 103–107.

    CAS  PubMed  Google Scholar 

  • Vivekanandan P, Thomas D, Torbenson M . (2009). Methylation regulates Hepatitis B viral protein expression. J Infect Dis 199: 1286–1291.

    CAS  PubMed  Google Scholar 

  • Wang X, Tang S, Le SY, Lu R, Rader JS, Meyers C et al. (2008). Aberrant expression of oncogenic and tumor-suppressive microRNAs in cervical cancer is required for cancer cell growth. PLoS One 3: e2557.

    PubMed  PubMed Central  Google Scholar 

  • Wang X, Wang HK, McCoy JP, Banerjee NS, Rader JS, Broker TR et al. (2009). Oncogenic HPV infection interrupts the expression of tumor-suppressive miR-34a through viral oncoprotein E6. RNA 15: 637–647.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wentzensen N, Sherman ME, Schiffman M, Wang SS . (2009). Utility of methylation markers in cervical cancer early detection: appraisal of the state-of-the-science. Gynecol Oncol 112: 293–299.

    CAS  PubMed  Google Scholar 

  • Whitby D . (2009). Searching for targets of viral microRNAs. Nat Genet 41: 7–8.

    CAS  PubMed  Google Scholar 

  • Whiteside MA, Siegel EM, Unger ER . (2008). Human papillomavirus and molecular considerations for cancer risk. Cancer 113: 2981–2994.

    CAS  PubMed  Google Scholar 

  • Wiencke JK, Zheng S, Morrison Z, Yeh RF . (2007). Differentially expressed genes are marked by histone 3 lysine 9 trimethylation in human cancer cells. Oncogene 27: 2412–2421.

    PubMed  Google Scholar 

  • Williams H, Crawford DH . (2006). Epstein-Barr virus: the impact of scientific advances on clinical practice. Blood 107: 862–869.

    CAS  PubMed  Google Scholar 

  • Woodman CBJ, Collins SI, Young LS . (2007). The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer 7: 11–22.

    CAS  PubMed  Google Scholar 

  • Yasunaga J-i, Matsuoka M . (2007). Leukaemogenic mechanism of human T-cell leukaemia virus type I. Rev Med Virol 17: 301–311.

    CAS  PubMed  Google Scholar 

  • Yoder JA, Walsh CP, Bestor TH . (1997). Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13: 335–340.

    CAS  PubMed  Google Scholar 

  • Yokosuka O, Arai M . (2006). Molecular biology of hepatitis B virus: effect of nucleotide substitutions on the clinical features of chronic hepatitis B. Med Mol Morphol 39: 113–120.

    PubMed  Google Scholar 

  • Yoshioka M, Kikuta H, Ishiguro N, Endo R, Kobayashi K . (2003). Latency pattern of Epstein-Barr virus and methylation status in Epstein-Barr virus-associated hemophagocytic syndrome. J Med Virol 70: 410–419.

    CAS  PubMed  Google Scholar 

  • Young LS, Rickinson AB . (2004). Epstein-Barr virus: 40 years on. Nat Rev Cancer 4: 757–768.

    CAS  PubMed  Google Scholar 

  • Zheng D-L, Zhang L, Cheng N, Xu X, Deng Q, Teng X-M et al. (2009). Epigenetic modification induced by hepatitis B virus X protein via interaction with de novo DNA methyltransferase DNMT3A. J Hepatol 50: 377–387.

    CAS  PubMed  Google Scholar 

  • Zheng ZM, Baker CC . (2006). Papillomavirus genome structure, expression, and post-transcriptional regulation. Front Biosci 11: 2286–2302.

    CAS  PubMed  PubMed Central  Google Scholar 

  • zur Hausen H . (1977). Human papillomaviruses and their possible role in squamous cell carcinomas. Curr Top Microbiol Immunol 78: 1–30.

    CAS  PubMed  Google Scholar 

  • zur Hausen H . (2006). Infections Causing Human Cancer. Wiley-VCH; Chichester: John Wiley: Weinheim.

    Google Scholar 

  • zur Hausen H . (2009). Papillomaviruses in the causation of human cancers—a brief historical account. Virology 384: 260–265.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by grants I+D+I MCYT08-03, Spanish Association Against Cancer (AECC), Fundacion Mutua Madrileña and the Swiss Bridge Award. ME is an ICREA (Institucio Catalana de Recerca i Estudis Avançats) Research Professor.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M Esteller.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fernandez, A., Esteller, M. Viral epigenomes in human tumorigenesis. Oncogene 29, 1405–1420 (2010). https://doi.org/10.1038/onc.2009.517

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/onc.2009.517

Keywords

This article is cited by

Search

Quick links