Skip to main content

Epigenetic Dysregulation in Virus-Associated Neoplasms

  • Chapter
  • First Online:
Patho-Epigenetics of Infectious Disease

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 879))

Abstract

The oncoproteins of human tumor viruses regularly interact with the cellular epigenetic machinery. Such interactions alter the epigenome of the host cell and reprogram its gene expression pattern. Altered levels or redistribution of (cytosine-5)-DNA methyltransferases and changes in the cellular methylome were observed in Kaposi sarcoma-associated herpesvirus (KSHV), hepatitis B virus (HBV), hepatitis D virus (HDV), hepatitis C virus (HCV), and human papillomavirus (HPV) associated neoplasms and cell lines. Methylation-mediated silencing of cellular promoters was also noted in Merkel cell polyomavirus (MCPyV) positive Merkel cell carcinomas, and, as discussed elsewhere, in EBV-associated malignancies and adenovirus-induced rodent tumors as well. Promoter activation also occurred, either associated with DNA hypomethylation or with the induction of euchromatic histone modifications by viral oncoproteins. It is worthy to notice that HCV infection induced large, hypomethylated blocks of cellular chromatin, although the exact molecular mechanism remains to be elucidated. In hepatoma cells expressing HBx, the oncoprotein encoded by the HBV genome, demethylation of the repetitive satellite 2 sequences was observed, due to downregulation of the de novo DNA methyltransferase DNMT3B. Tax and HBZ, the oncoproteins of human T-cell lymphotropic virus type I (HTLV-I), can both activate and silence distinct cellular promoters by interacting with cellular enzymes involved in histone modification.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ali N, Allam H, May R, Sureban SM, Bronze MS, Bader T, Umar S, Anant S, Houchen CW (2011) Hepatitis C virus-induced cancer stem cell-like signatures in cell culture and murine tumor xenografts. J Virol 85:12292–12303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arora P, Kim EO, Jung JK, Jang KL (2008) Hepatitis C virus core protein downregulates E-cadherin expression via activation of DNA methyltransferase 1 and 3b. Cancer Lett 261:244–252

    Article  CAS  PubMed  Google Scholar 

  • Ay E, Buzas K, Banati F, Minarovits J (2012) Recent results in the development of fetal immune system: self, epigenetic regulation, fetal immune responses. In: Berencsi G (ed) Maternal fetal transmission of human viruses and their influence on tumorigenesis. Springer, New York, pp 51–82

    Chapter  Google Scholar 

  • Ay E, Banati F, Mezei M, Bakos A, Niller HH, Buzas K, Minarovits J (2013) Epigenetics of HIV infection: promising research areas and implications for therapy. AIDS Rev 15(3):181–188

    PubMed  Google Scholar 

  • Benegiamo G, Vinciguerra M, Mazzoccoli G, Piepoli A, Andriulli A, Pazienza V (2012) DNA methyltransferases 1 and 3b expression in Huh-7 cells expressing HCV core protein of different genotypes. Dig Dis Sci 57:1598–1603

    Article  CAS  PubMed  Google Scholar 

  • Benegiamo G, Vinciguerra M, Guarnieri V, Niro GA, Andriulli A, Pazienza V (2013) Hepatitis delta virus induces specific DNA methylation processes in Huh-7 liver cancer cells. FEBS Lett 587:1424–1428

    Article  CAS  PubMed  Google Scholar 

  • Boyer SN, Wazer DE, Band V (1996) E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res 56:4620–4624

    CAS  PubMed  Google Scholar 

  • Chen HS, Lu F, Lieberman PM (2013a) Epigenetic regulation of EBV and KSHV latency. Curr Opin Virol 3:251–259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Denard B, Huang H, Ye J (2013b) Epigenetic silencing of antiviral genes renders clones of Huh-7 cells permissive for hepatitis C virus replication. J Virol 87:659–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng J, Kydd AR, Nakase K, Noonan KM, Murakami A, Tao H, Dwyer M, Xu C, Zhu Q, Marasco WA (2007) Negative regulation of the SH2-homology containing protein-tyrosine phosphatase-1 (SHP-1) P2 promoter by the HTLV-1 Tax oncoprotein. Blood 110:2110–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng H, Ren T, Sun SC (2012) New insight into the oncogenic mechanism of the retroviral oncoprotein Tax. Protein Cell 3:581–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng J, Rozenblatt-Rosen O, Paulson KG, Nghiem P, Decaprio JA (2013) Merkel cell polyomavirus large T antigen has growth-promoting and inhibitory activities. J Virol 87:6118–6126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darst RP, Haecker I, Pardo CE, Renne R, Kladde MP (2013) Epigenetic diversity of Kaposi’s sarcoma-associated herpesvirus. Nucleic Acids Res 41:2993–3009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Costa ZJ, Jolly C, Androphy EJ, Mercer A, Matthews CM, Hibma MH (2012) Transcriptional repression of E-cadherin by human papillomavirus type 16 E6. PLoS One 7:e48954

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Doerfler W (2012) The impact of foreign DNA integration on tumor biology and evolution via epigenetic alterations. In: Minarovits J, Niller HH (eds) Patho-epigenetics of disease. Springer, New York, pp 14–378

    Google Scholar 

  • Ewald D, Li M, Efrat S, Auer G, Wall RJ, Furth PA, Hennighausen L (1996) Time-sensitive reversal of hyperplasia in transgenic mice expressing SV40 T antigen. Science 273:1384–1386

    Article  CAS  PubMed  Google Scholar 

  • Farkas SA, Milutin-Gasperov N, Grce M, Nilsson TK (2013) Genome-wide DNA methylation assay reveals novel candidate biomarker genes in cervical cancer. Epigenetics 8:1213–1225

    Article  CAS  PubMed  Google Scholar 

  • Fernandez AF, Esteller M (2010) Viral epigenomes in human tumorigenesis. Oncogene 29:1405–1420

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ganem D (2010) KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. J Clin Invest 120:939–949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gunther T, Schreiner S, Dobner T, Tessmer U, Grundhoff A (2014) Influence of ND10 components on epigenetic determinants of early KSHV latency establishment. PLoS Pathog 10:e1004274

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hansen KD, Sabunciyan S, Langmead B, Nagy N, Curley R, Klein G, Klein E, Salamon D, Feinberg AP (2014) Large-scale hypomethylated blocks associated with Epstein-Barr virus-induced B-cell immortalization. Genome Res 24:177–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan UA, Zannetti C, Parroche P, Goutagny N, Malfroy M, Roblot G, Carreira C, Hussain I, Muller M, Taylor-Papadimitriou J, Picard D, Sylla BS, Trinchieri G, Medzhitov R, Tommasino M (2013) The human papillomavirus type 16 E7 oncoprotein induces a transcriptional repressor complex on the Toll-like receptor 9 promoter. J Exp Med 210:1369–1387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He M, Zhang W, Bakken T, Schutten M, Toth Z, Jung JU, Gill P, Cannon M, Gao SJ (2012) Cancer angiogenesis induced by Kaposi sarcoma-associated herpesvirus is mediated by EZH2. Cancer Res 72:3582–3592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helmbold P, Lahtz C, Enk A, Herrmann-Trost P, Marsch W, Kutzner H, Dammann RH (2009) Frequent occurrence of RASSF1A promoter hypermethylation and Merkel cell polyomavirus in Merkel cell carcinoma. Mol Carcinog 48:903–909

    Article  CAS  PubMed  Google Scholar 

  • Herceg Z, Paliwal A (2011) Epigenetic mechanisms in hepatocellular carcinoma: how environmental factors influence the epigenome. Mutat Res 727:55–61

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Vargas H, Lambert MP, Le Calvez-Kelm F, Gouysse G, McKay-Chopin S, Tavtigian SV, Scoazec JY, Herceg Z (2010) Hepatocellular carcinoma displays distinct DNA methylation signatures with potential as clinical predictors. PLoS One 5:e9749

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hinrichsen I, Kemp M, Peveling-Oberhag J, Passmann S, Plotz G, Zeuzem S, Brieger A (2014) Promoter methylation of MLH1, PMS2, MSH2 and p16 is a phenomenon of advanced-stage HCCs. PLoS One 9:e84453

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hlady RA, Tiedemann RL, Puszyk W, Zendejas I, Roberts LR, Choi JH, Liu C, Robertson KD (2014) Epigenetic signatures of alcohol abuse and hepatitis infection during human hepatocarcinogenesis. Oncotarget 5:9425–9443

    Article  PubMed  PubMed Central  Google Scholar 

  • Holland D, Hoppe-Seyler K, Schuller B, Lohrey C, Maroldt J, Durst M, Hoppe-Seyler F (2008) Activation of the enhancer of zeste homologue 2 gene by the human papillomavirus E7 oncoprotein. Cancer Res 68:9964–9972

    Article  CAS  PubMed  Google Scholar 

  • Hoppe-Seyler F, Hoppe-Seyler K (2011) Emerging topics in human tumor virology. Int J Cancer 129:1289–1299

    Article  CAS  PubMed  Google Scholar 

  • Houben R, Schrama D, Becker JC (2009) Molecular pathogenesis of Merkel cell carcinoma. Exp Dermatol 18:193–198

    Article  CAS  PubMed  Google Scholar 

  • Hsieh YH, Hsu JL, Su IJ, Huang W (2011) Genomic instability caused by hepatitis B virus: into the hepatoma inferno. Front Biosci (Landmark Ed) 16:2586–2597

    Article  CAS  Google Scholar 

  • Hu J, Yang Y, Turner PC, Jain V, McIntyre LM, Renne R (2014) LANA binds to multiple active viral and cellular promoters and associates with the H3K4methyltransferase hSET1 complex. PLoS Pathog 10:e1004240

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang CR, Lo SJ (2014) Hepatitis D virus infection, replication and cross-talk with the hepatitis B virus. World J Gastroenterol 20:14589–14597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyland PL, McDade SS, McCloskey R, Dickson GJ, Arthur K, McCance DJ, Patel D (2011) Evidence for alteration of EZH2, BMI1, and KDM6A and epigenetic reprogramming in human papillomavirus type 16 E6/E7-expressing keratinocytes. J Virol 85:10999–11006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iacovides D, Michael S, Achilleos C, Strati K (2013) Shared mechanisms in stemness and carcinogenesis: lessons from oncogenic viruses. Front Cell Infect Microbiol 3:66

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ishikawa C, Kawakami H, Uchihara JN, Senba M, Mori N (2013) CD69 overexpression by human T-cell leukemia virus type 1 Tax transactivation. Biochim Biophys Acta 1833:1542–1552

    Article  CAS  PubMed  Google Scholar 

  • James MA, Lee JH, Klingelhutz AJ (2006) HPV16-E6 associated hTERT promoter acetylation is E6AP dependent, increased in later passage cells and enhanced by loss of p300. Int J Cancer 119:1878–1885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong S, Liang G, Sharma S, Lin JC, Choi SH, Han H, Yoo CB, Egger G, Yang AS, Jones PA (2009) Selective anchoring of DNA methyltransferases 3A and 3B to nucleosomes containing methylated DNA. Mol Cell Biol 29:5366–5376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong SW, Jang JY, Chung RT (2012) Hepatitis C virus and hepatocarcinogenesis. Clin Mol Hepatol 18:347–356

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones PA, Baylin SB (2007) The epigenomics of cancer. Cell 128:683–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones T, Ye F, Bedolla R, Huang Y, Meng J, Qian L, Pan H, Zhou F, Moody R, Wagner B, Arar M, Gao SJ (2012) Direct and efficient cellular transformation of primary rat mesenchymal precursor cells by KSHV. J Clin Invest 122:1076–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung JK, Park SH, Jang KL (2010) Hepatitis B virus X protein overcomes the growth-inhibitory potential of retinoic acid by downregulating retinoic acid receptor-beta2 expression via DNA methylation. J Gen Virol 91:493–500

    Article  CAS  PubMed  Google Scholar 

  • Kehn K, Fuente CL, Strouss K, Berro R, Jiang H, Brady J, Mahieux R, Pumfery A, Bottazzi ME, Kashanchi F (2005) The HTLV-I Tax oncoprotein targets the retinoblastoma protein for proteasomal degradation. Oncogene 24:525–540

    Article  CAS  PubMed  Google Scholar 

  • Kim CM, Koike K, Saito I, Miyamura T, Jay G (1991) HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 351:317–320

    Article  CAS  PubMed  Google Scholar 

  • Kim KY, Huerta SB, Izumiya C, Wang DH, Martinez A, Shevchenko B, Kung HJ, Campbell M, Izumiya Y (2013) Kaposi’s Sarcoma-Associated Herpesvirus (KSHV) Latency-Associated Nuclear Antigen Regulates the KSHV Epigenome by Association with the Histone Demethylase KDM3A. J Virol 87:6782–6793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laurson J, Khan S, Chung R, Cross K, Raj K (2010) Epigenetic repression of E-cadherin by human papillomavirus 16 E7 protein. Carcinogenesis 31:918–926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lechner M, Fenton T, West J, Wilson G, Feber A, Henderson S, Thirlwell C, Dibra HK, Jay A, Butcher L, Chakravarthy AR, Gratrix F, Patel N, Vaz F, O’Flynn P, Kalavrezos N, Teschendorff AE, Boshoff C, Beck S (2013a) Identification and functional validation of HPV-mediated hypermethylation in head and neck squamous cell carcinoma. Genome Med 5:15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lechner M, Frampton GM, Fenton T, Feber A, Palmer G, Jay A, Pillay N, Forster M, Cronin MT, Lipson D, Miller VA, Brennan TA, Henderson S, Vaz F, O’Flynn P, Kalavrezos N, Yelensky R, Beck S, Stephens PJ, Boshoff C (2013b) Targeted next-generation sequencing of head and neck squamous cell carcinoma identifies novel genetic alterations in HPV+ and HPV- tumors. Genome Med 5:49

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee KM, Choi KH, Ouellette MM (2004) Use of exogenous hTERT to immortalize primary human cells. Cytotechnology 45:33–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee H, Woo YJ, Kim SS, Kim SH, Park BJ, Choi D, Jang KL (2013) Hepatitis C virus core protein overcomes all-trans retinoic acid-induced cell growth arrest by inhibiting retinoic acid receptor-beta2 expression via DNA methylation. Cancer Lett 335:372–379

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Liao FT, Lee YJ, Ko JL, Tsai CC, Tseng CJ, Sheu GT (2009) Hepatitis delta virus epigenetically enhances clusterin expression via histone acetylation in human hepatocellular carcinoma cells. J Gen Virol 90:1124–1134

    Article  CAS  PubMed  Google Scholar 

  • Lindsey S, Langhans SA (2014) Crosstalk of oncogenic signaling pathways during epithelial-mesenchymal transition. Front Oncol 4:358

    Article  PubMed  PubMed Central  Google Scholar 

  • Machida K, Chen CL, Liu JC, Kashiwabara C, Feldman D, French SW, Sher L, Hyeongnam JJ, Tsukamoto H (2012) Cancer stem cells generated by alcohol, diabetes, and hepatitis C virus. J Gastroenterol Hepatol 27(Suppl 2):19–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marjanovic ND, Weinberg RA, Chaffer CL (2013) Cell plasticity and heterogeneity in cancer. Clin Chem 59:168–179

    Article  CAS  PubMed  Google Scholar 

  • Matsusaka K, Kaneda A, Nagae G, Ushiku T, Kikuchi Y, Hino R, Uozaki H, Seto Y, Takada K, Aburatani H, Fukayama M (2011) Classification of Epstein-Barr virus-positive gastric cancers by definition of DNA methylation epigenotypes. Cancer Res 71:7187–7197

    Article  CAS  PubMed  Google Scholar 

  • Mattsson K, Kiss C, Platt GM, Simpson GR, Kashuba E, Klein G, Schulz TF, Szekely L (2002) Latent nuclear antigen of Kaposi’s sarcoma herpesvirus/human herpesvirus-8 induces and relocates RING3 to nuclear heterochromatin regions. J Gen Virol 83:179–188

    Article  CAS  PubMed  Google Scholar 

  • McCabe MT, Low JA, Daignault S, Imperiale MJ, Wojno KJ, Day ML (2006) Inhibition of DNA methyltransferase activity prevents tumorigenesis in a mouse model of prostate cancer. Cancer Res 66:385–392

    Article  CAS  PubMed  Google Scholar 

  • McLaughlin-Drubin ME, Crum CP, Munger K (2011) Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc Natl Acad Sci U S A 108:2130–2135

    Article  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 

  • Minarovits J (2009) Microbe-induced epigenetic alterations in host cells: the coming era of patho-epigenetics of microbial infections. A review. Acta Microbiol Immunol Hung 56:1–19

    Article  CAS  PubMed  Google Scholar 

  • Minarovits J, Niller HH (2013) Patho-epigenetics. Med Epigenetics 1:37–45

    Article  CAS  Google Scholar 

  • Munoz P, Iliou MS, Esteller M (2012) Epigenetic alterations involved in cancer stem cell reprogramming. Mol Oncol 6:620–636

    Article  CAS  PubMed  Google Scholar 

  • Nakachi S, Nakazato T, Ishikawa C, Kimura R, Mann DA, Senba M, Masuzaki H, Mori N (2011) Human T-cell leukemia virus type 1 tax transactivates the matrix metalloproteinase 7 gene via JunD/AP-1 signaling. Biochim Biophys Acta 1813:731–741

    Article  CAS  PubMed  Google Scholar 

  • Nead MA, McCance DJ (1998) Activities of the transforming proteins of human papillomaviruses. In: McCance DJ (ed) Human tumor viruses. ASM Press, Washington, DC, pp 225–251

    Chapter  Google Scholar 

  • Newman CL, Rosenblatt JD (1998) Human T-cell lymphotropic viruses. In: McCance D (ed) Human tumor viruses. ASM Press, Washington, DC, pp 331–357

    Chapter  Google Scholar 

  • Niller HH, Minarovits J (2012) Epigenetics and human infectious diseases. In: Tollefsbol TO (ed) Epigenetics in human disease. Academic, Waltham, pp 415–442

    Chapter  Google Scholar 

  • Niller HH, Banati F, Ay E, Minarovits J (2012a) Epigenetic changes in virus-associated neoplasms. In: Minarovits J, Niller HH (eds) Patho-epigenetics of disease. Springer, New York, pp 179–225

    Chapter  Google Scholar 

  • Niller HH, Banati F, Ay E, Minarovits J (2012b) Microbe-induced epigenetic alterations. In: Minarovits J, Niller HH (eds) Patho-epigenetics of disease. Springer, New York, pp 419–455

    Chapter  Google Scholar 

  • Niller HH, Tarnai Z, Decsi G, Zsedenyi A, Banati F, Minarovits J (2014) Role of epigenetics in EBV regulation and pathogenesis. Future Microbiol 9:747–756

    Article  CAS  PubMed  Google Scholar 

  • Nyborg JK, Egan D, Sharma N (2010) The HTLV-1 Tax protein: revealing mechanisms of transcriptional activation through histone acetylation and nucleosome disassembly. Biochim Biophys Acta 1799:266–274

    Article  CAS  PubMed  Google Scholar 

  • Okamoto Y, Shinjo K, Shimizu Y, Sano T, Yamao K, Gao W, Fujii M, Osada H, Sekido Y, Murakami S, Tanaka Y, Joh T, Sato S, Takahashi S, Wakita T, Zhu J, Issa JP, Kondo Y (2014) Hepatitis virus infection affects DNA methylation in mice with humanized livers. Gastroenterology 146:562–572

    Article  CAS  PubMed  Google Scholar 

  • Or YY, Hui AB, Tam KY, Huang DP, Lo KW (2005) Characterization of chromosome 3q and 12q amplicons in nasopharyngeal carcinoma cell lines. Int J Oncol 26:49–56

    CAS  PubMed  Google Scholar 

  • Pagano JS, Blaser M, Buendia MA, Damania B, Khalili K, Raab-Traub N, Roizman B (2004) Infectious agents and cancer: criteria for a causal relation. Semin Cancer Biol 14:453–471

    Article  CAS  PubMed  Google Scholar 

  • Park IY, Sohn BH, Yu E, Suh DJ, Chung YH, Lee JH, Surzycki SJ, Lee YI (2007) Aberrant epigenetic modifications in hepatocarcinogenesis induced by hepatitis B virus X protein. Gastroenterology 132:1476–1494

    Article  CAS  PubMed  Google Scholar 

  • Paschos K, Allday MJ (2010) Epigenetic reprogramming of host genes in viral and microbial pathogenesis. Trends Microbiol 18:439–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polakowski N, Gregory H, Mesnard JM, Lemasson I (2010) Expression of a protein involved in bone resorption, Dkk1, is activated by HTLV-1 bZIP factor through its activation domain. Retrovirology 7:61

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Quan H, Zhou F, Nie D, Chen Q, Cai X, Shan X, Zhou Z, Chen K, Huang A, Li S, Tang N (2014) Hepatitis C virus core protein epigenetically silences SFRP1 and enhances HCC aggressiveness by inducing epithelial-mesenchymal transition. Oncogene 33:2826–2835

    Article  CAS  PubMed  Google Scholar 

  • Ripoli M, Barbano R, Balsamo T, Piccoli C, Brunetti V, Coco M, Mazzoccoli G, Vinciguerra M, Pazienza V (2011) Hypermethylated levels of E-cadherin promoter in Huh-7 cells expressing the HCV core protein. Virus Res 160:74–81

    Article  CAS  PubMed  Google Scholar 

  • Rongrui L, Na H, Zongfang L, Fanpu J, Shiwen J (2014) Epigenetic mechanism involved in the HBV/HCV-related hepatocellular carcinoma tumorigenesis. Curr Pharm Des 20:1715–1725

    Article  PubMed  CAS  Google Scholar 

  • Schutze DM, Kooter JM, Wilting SM, Meijer CJ, Quint W, Snijders PJ, Steenbergen RD (2015) Longitudinal assessment of DNA methylation changes during HPVE6E7-induced immortalization of primary keratinocytes. Epigenetics 10:73–81

    Article  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 U S A 103:14554–14559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shon JK, Shon BH, Park IY, Lee SU, Fa L, Chang KY, Shin JH, Lee YI (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

    Article  CAS  PubMed  Google Scholar 

  • Soto AM, Sonnenschein C (2014) One hundred years of somatic mutation theory of carcinogenesis: is it time to switch? Bioessays 36:118–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steenbergen RD, Ongenaert M, Snellenberg S, Trooskens G, Van Der Meide WF, Pandey D, Bloushtain-Qimron N, Polyak K, Meijer CJ, Snijders PJ, Van Criekinge W (2013) Methylation-specific digital karyotyping of HPV16E6E7-expressing human keratinocytes identifies novel methylation events in cervical carcinogenesis. J Pathol 231:53–62

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stunkel W, Campbell RM (2011) Sirtuin 1 (SIRT1): the misunderstood HDAC. J Biomol Screen 16:1153–1169

    Article  CAS  PubMed  Google Scholar 

  • Szalmas A, Konya J (2009) Epigenetic alterations in cervical carcinogenesis. Semin Cancer Biol 19:144–152

    Article  CAS  PubMed  Google Scholar 

  • Takagi K, Fujiwara K, Takayama T, Mamiya T, Soma M, Nagase H (2013) DNA hypermethylation of zygote arrest 1 (ZAR1) in hepatitis C virus positive related hepatocellular carcinoma. Springerplus 2:150

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tang S, Hu W, Hu J, Wu S, Li J, Luo Y, Cao M, Zhou H, Jiang X (2015) Hepatitis B virus X protein promotes P3 transcript expression of the insulin-like growth factor 2 gene via inducing hypomethylation of P3 promoter in hepatocellular carcinoma. Liver Int 35:608–619

    Article  CAS  PubMed  Google Scholar 

  • Tarocchi M, Polvani S, Marroncini G, Galli A (2014) Molecular mechanism of hepatitis B virus-induced hepatocarcinogenesis. World J Gastroenterol 20:11630–11640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong A, Gou L, Lau QC, Chen B, Zhao X, Li J, Tang H, Chen L, Tang M, Huang C, Wei YQ (2009) Proteomic profiling identifies aberrant epigenetic modifications induced by hepatitis B virus X protein. J Proteome Res 8:1037–1046

    Article  CAS  PubMed  Google Scholar 

  • Van Doorslaer K (2013) Evolution of the papillomaviridae. Virology 445:11–20

    Article  PubMed  CAS  Google Scholar 

  • Van Regenmortel MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, McGeogh DJ, Maniloff J, Mayo MA, Pringle CR, Wickner RB (2000) Virus taxonomy. The classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses (ICTV). Academic, San Diego

    Google Scholar 

  • Verhaegen ME, Mangelberger D, Harms PW, Vozheiko TD, Weick JW, Wilbert DM, Saunders TL, Ermilov AN, Bichakjian CK, Johnson TM, Imperiale MJ, Dlugosz AA (2015) Merkel cell polyomavirus small T antigen is oncogenic in transgenic mice. J Invest Dermatol 135:1415–1424 (Epub was October 2014)

    Google Scholar 

  • Viejo-Borbolla A, Ottinger M, Bruning E, Burger A, Konig R, Kati E, Sheldon JA, Schulz TF (2005) Brd2/RING3 interacts with a chromatin-binding domain in the Kaposi’s sarcoma-associated herpesvirus latency-associated nuclear antigen 1 (LANA-1) that is required for multiple functions of LANA-1. J Virol 79:13618–13629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White MK, Gordon J, Khalili K (2013) The rapidly expanding family of human polyomaviruses: recent developments in understanding their life cycle and role in human pathology. PLoS Pathog 9:e1003206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson GA, Lechner M, Koferle A, Caren H, Butcher LM, Feber A, Fenton T, Jay A, Boshoff C, Beck S (2013) Integrated virus-host methylome analysis in head and neck squamous cell carcinoma. Epigenetics 8:953–961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong DK, Walker BD (1998) Hepatitis C virus. In: McCance DJ (ed) Human tumor viruses. ASM Press, Washington, DC, pp 301–329

    Chapter  Google Scholar 

  • Wurm T, Wright DG, Polakowski N, Mesnard JM, Lemasson I (2012) The HTLV-1-encoded protein HBZ directly inhibits the acetyl transferase activity of p300/CBP. Nucleic Acids Res 40:5910–5925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Q, Chen L, Shan X, Shan X, Tang J, Zhou F, Chen Q, Quan H, Nie D, Zhang W, Huang AL, Tang N (2014) Epigenetic silencing of SFRP1 and SFRP5 by hepatitis B virus X protein enhances hepatoma cell tumorigenicity through Wnt signaling pathway. Int J Cancer 135:635–646

    Article  CAS  PubMed  Google Scholar 

  • Ye F, Lei X, Gao SJ (2011) Mechanisms of Kaposi’s sarcoma-associated herpesvirus latency and reactivation. Adv Virol 2011:193860

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng B, Li Z, Chen R, Guo N, Zhou J, Zhou Q, Lin Q, Cheng D, Liao Q, Zheng L, Gong Y (2012) Epigenetic regulation of miR-124 by hepatitis C virus core protein promotes migration and invasion of intrahepatic cholangiocarcinoma cells by targeting SMYD3. FEBS Lett 586:3271–3278

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Laribee RN, Klemsz MJ, Roman A (2004) Human papillomavirus type 16 E7 protein increases acetylation of histone H3 in human foreskin keratinocytes. Virology 329:189–198

    Article  CAS  PubMed  Google Scholar 

  • Zhao T, Matsuoka M (2012) HBZ and its roles in HTLV-1 oncogenesis. Front Microbiol 3:247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Wu G, Bu F, Lu B, Liang A, Cao L, Tong X, Lu X, Wu M, Guo Y (2010) Epigenetic silence of ankyrin-repeat-containing, SH3-domain-containing, and proline-rich-region- containing protein 1 (ASPP1) and ASPP2 genes promotes tumor growth in hepatitis B virus-positive hepatocellular carcinoma. Hepatology 51:142–153

    Article  CAS  PubMed  Google Scholar 

  • Zhao T, Satou Y, Sugata K, Miyazato P, Green PL, Imamura T, Matsuoka M (2011) HTLV-1 bZIP factor enhances TGF-beta signaling through p300 coactivator. Blood 118:1865–1876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng DL, Zhang L, Cheng N, Xu X, Deng Q, Teng XM, Wang KS, Zhang X, Huang J, Han ZG (2009) Epigenetic modification induced by hepatitis B virus X protein via interaction with de novo DNA methyltransferase DNMT3A. J Hepatol 50:377–387

    Article  CAS  PubMed  Google Scholar 

  • Zielke K, Full F, Teufert N, Schmidt M, Muller-Fleckenstein I, Alberter B, Ensser A (2012) The insulator protein CTCF binding sites in the orf73/LANA promoter region of herpesvirus saimiri are involved in conferring episomal stability in latently infected human T cells. J Virol 86:1862–1873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zur Hausen H (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342–350

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hans Helmut Niller .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Minarovits, J., Demcsák, A., Banati, F., Niller, H.H. (2016). Epigenetic Dysregulation in Virus-Associated Neoplasms. In: Minarovits, J., Niller, H. (eds) Patho-Epigenetics of Infectious Disease. Advances in Experimental Medicine and Biology, vol 879. Springer, Cham. https://doi.org/10.1007/978-3-319-24738-0_4

Download citation

Publish with us

Policies and ethics