Cancer Letters
Volume 305, Issue 2 , Pages 200-217 , 28 June 2011

Viral hit and run-oncogenesis: Genetic and epigenetic scenarios

  • Hans Helmut Niller

      Affiliations

    • Institute for Medical Microbiology and Hygiene of the University of Regensburg, Franz-Josef-Strauß-Allee 11, D-93053 Regensburg, Germany
    • Corresponding Author InformationCorresponding author.
  • ,
  • Hans Wolf

      Affiliations

    • Institute for Medical Microbiology and Hygiene of the University of Regensburg, Franz-Josef-Strauß-Allee 11, D-93053 Regensburg, Germany
  • ,
  • Janos Minarovits

      Affiliations

    • Microbiological Research Group of the National Center for Epidemiology, Pihenö ut 1, H-1529 Budapest, Hungary

Received 19 February 2010 ,Revised 29 July 2010 ,Accepted 9 August 2010.

References 

  1. Skinner GR. Transformation of primary hamster embryo fibroblasts by type 2 simplex virus: evidence for a “hit and run” mechanism. Br. J. Exp. Pathol. 1976;57:361–376
  2. Galloway DA, McDougall JK. The oncogenic potential of herpes simplex viruses: evidence for a ‘hit-and-run’ mechanism. Nature. 1983;302:21–24
  3. Galloway DA, McDougall JK. Alterations in the cellular phenotype induced by herpes simplex viruses. J. Med. Virol. 1990;31:36–42
  4. Bauer G, Kahl S, Sawhney IS, Hofler P, Gerspach R, Matz B. Transformation of rodent fibroblasts by herpes simplex virus: presence of morphological transforming region 1 (MTR 1) is not required for the maintenance of the transformed state. Int. J. Cancer. 1992;51:754–760
  5. Nelson JA, Fleckenstein B, Galloway DA, McDougall JK. Transformation of NIH 3T3 cells with cloned fragments of human cytomegalovirus strain AD169. J. Virol. 1982;43:83–91
  6. Clanton DJ, Jariwalla RJ, Kress C, Rosenthal LJ. Neoplastic transformation by a cloned human cytomegalovirus DNA fragment uniquely homologous to one of the transforming regions of herpes simplex virus type 2. Proc. Natl. Acad. Sci. USA. 1983;80:3826–3830
  7. Iwasaka T, Hayashi Y, Yokoyama M, Hara K, Matsuo N, Sugimori H. ‘Hit and run’ oncogenesis by human papillomavirus type 18 DNA. Acta Obstet. Gynecol. Scand. 1992;71:219–223
  8. Shen Y, Zhu H, Shenk T. Human cytomagalovirus IE1 and IE2 proteins are mutagenic and mediate “hit-and-run” oncogenic transformation in cooperation with the adenovirus E1A proteins. Proc. Natl. Acad. Sci. USA. 1997;94:3341–3345
  9. Iwasaka T, Yokoyama M, Hayashi Y, Sugimori H. Combined herpes simplex virus type 2 and human papillomavirus type 16 or 18 deoxyribonucleic acid leads to oncogenic transformation. Am. J. Obstet. Gynecol. 1988;159:1251–1255
  10. DiPaolo JA, Woodworth CD, Popescu NC, Koval DL, Lopez JV, Doniger J. HSV-2-induced tumorigenicity in HPV16-immortalized human genital keratinocytes. Virology. 1990;177:777–779
  11. Lau CC, Gadi IK, Kalvonjian S, Anisowicz A, Sager R. Plasmid-induced “hit-and-run” tumorigenesis in Chinese hamster embryo fibroblast (CHEF) cells. Proc. Natl. Acad. Sci. USA. 1985;82:2839–2843
  12. zur Hausen H. Viruses in human cancers. Eur. J. Cancer. 1999;35:1174–1181
  13. Pagano JS, Blaser M, Buendia MA, Damania B, Khalili K, Raab-Traub N, et al. Infectious agents and cancer: criteria for a causal relation. Semin. Cancer Biol. 2004;14:453–471
  14. Cougot D, Neuveut C, Buendia MA. HBV induced carcinogenesis. J. Clin. Virol. 2005;34(Suppl. 1):S75–S78
  15. Chemin I, Zoulim F. Hepatitis B virus induced hepatocellular carcinoma. Cancer Lett. 2009;286:52–59
  16. Hessein M, el Gendy S, Attallah AM, el Awady MK, Abdel Hady AM, Medhat A, et al. Hit-and-run mechanism of HBV-mediated progression to hepatocellular carcinoma. Tumori. 2005;91:241–247
  17. Guidotti LG, Chisari FV. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu. Rev. Immunol. 2001;19:65–91
  18. Neumann-Haefelin C, Blum HE, Chisari FV, Thimme R. T cell response in hepatitis C virus infection. J. Clin. Virol. 2005;32:75–85
  19. Kasprzak A, Adamek A. Role of hepatitis C virus proteins (C, NS3, NS5A) in hepatic oncogenesis. Hepatol. Res. 2008;38:1–26
  20. Machida K, Liu JC, McNamara G, Levine A, Duan L, Lai MM. Hepatitis C virus causes uncoupling of mitotic checkpoint and chromosomal polyploidy through the Rb pathway. J. Virol. 2009;83:12590–12600
  21. Lai CK, Jeng KS, Machida K, Cheng YS, Lai MM. Hepatitis C virus NS3/4A protein interacts with ATM, impairs DNA repair and enhances sensitivity to ionizing radiation. Virology. 2008;370:295–309
  22. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science. 1989;244:359–362
  23. Takeda S, Shibata M, Morishima T, Harada A, Nakao A, Takagi H, et al. Hepatitis C virus infection in hepatocellular carcinoma. Detection of plus-strand and minus-strand viral RNA. Cancer. 1992;70:2255–2259
  24. Negri E, Little D, Boiocchi M, La Vecchia C, Franceschi S. B-cell non-Hodgkin’s lymphoma and hepatitis C virus infection: a systematic review. Int. J. Cancer. 2004;111:1–8
  25. Ivanovski M, Silvestri F, Pozzato G, Anand S, Mazzaro C, Burrone OR, et al. Somatic hypermutation, clonal diversity, and preferential expression of the VH 51p1/VL kv325 immunoglobulin gene combination in hepatitis C virus-associated immunocytomas. Blood. 1998;91:2433–2442
  26. Machida K, Cheng KT, Pavio N, Sung VM, Lai MM. Hepatitis C virus E2-CD81 interaction induces hypermutation of the immunoglobulin gene in B cells. J. Virol. 2005;79:8079–8089
  27. Sung VM, Shimodaira S, Doughty AL, Picchio GR, Can H, Yen TS, et al. Establishment of B-cell lymphoma cell lines persistently infected with hepatitis C virus in vivo and in vitro: the apoptotic effects of virus infection. J. Virol. 2003;77:2134–2146
  28. Endo Y, Marusawa H, Kinoshita K, Morisawa T, Sakurai T, Okazaki IM, et al. Expression of activation-induced cytidine deaminase in human hepatocytes via NF-kappaB signaling. Oncogene. 2007;26:5587–5595
  29. Takai A, Toyoshima T, Uemura M, Kitawaki Y, Marusawa H, Hiai H, et al. A novel mouse model of hepatocarcinogenesis triggered by AID causing deleterious p53 mutations. Oncogene. 2009;28:469–478
  30. Machida K, Cheng KT, Sung VM, Shimodaira S, Lindsay KL, Levine AM, et al. Hepatitis C virus induces a mutator phenotype: enhanced mutations of immunoglobulin and protooncogenes. Proc. Natl. Acad. Sci. USA. 2004;101:4262–4267
  31. Mazzaro C, Franzin F, Tulissi P, Pussini E, Crovatto M, Carniello GS, et al. Regression of monoclonal B-cell expansion in patients affected by mixed cryoglobulinemia responsive to alpha-interferon therapy. Cancer. 1996;77:2604–2613
  32. Casato M, Mecucci C, Agnello V, Fiorilli M, Knight GB, Matteucci C, et al. Regression of lymphoproliferative disorder after treatment for hepatitis C virus infection in a patient with partial trisomy 3, Bcl-2 overexpression, and type II cryoglobulinemia. Blood. 2002;99:2259–2261
  33. Hermine O, Lefrere F, Bronowicki JP, Mariette X, Jondeau K, Eclache-Saudreau V, et al. Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. New Engl. J. Med. 2002;347:89–94
  34. Levine AM, Shimodaira S, Lai MM. Treatment of HCV-related mantle-cell lymphoma with ribavirin and pegylated interferon Alfa. New Engl. J. Med. 2003;349:2078–2079
  35. Pagano JS. Viruses and lymphomas. New Engl. J. Med. 2002;347:78–79
  36. Op den Brouw ML, Binda RS, van Roosmalen MH, Protzer U, Janssen HL, van der Molen RG, et al. Hepatitis B virus surface antigen impairs myeloid dendritic cell function: a possible immune escape mechanism of hepatitis B virus. Immunology. 2009;126:280–289
  37. Moens U, Johannessen M. Human polyomaviruses and cancer: expanding repertoire. J. Dtsch. Dermatol. Ges. 2008;6:704–708
  38. Jiang M, Abend JR, Johnson SF, Imperiale MJ. The role of polyomaviruses in human disease. Virology. 2009;384:266–273
  39. Allander T, Andreasson K, Gupta S, Bjerkner A, Bogdanovic G, Persson MA, et al. Identification of a third human polyomavirus. J. Virol. 2007;81:4130–4136
  40. Gaynor AM, Nissen MD, Whiley DM, Mackay IM, Lambert SB, Wu G, et al. Identification of a novel polyomavirus from patients with acute respiratory tract infections. PLoS Pathog. 2007;3:e64
  41. Carter JJ, Paulson KG, Wipf GC, Miranda D, Madeleine MM, Johnson LG, et al. Association of Merkel cell polyomavirus-specific antibodies with Merkel cell carcinoma. J. Natl. Cancer Inst. 2009;101:1510–1522
  42. Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science. 2008;319:1096–1100
  43. Shuda M, Feng H, Kwun HJ, Rosen ST, Gjoerup O, Moore PS, et al. T antigen mutations are a human tumor-specific signature for Merkel cell polyomavirus. Proc. Natl. Acad. Sci. USA. 2008;105:16272–16277
  44. Sharp CP, Norja P, Anthony I, Bell JE, Simmonds P. Reactivation and mutation of newly discovered WU, KI, and Merkel cell carcinoma polyomaviruses in immunosuppressed individuals. J. Infect. Dis. 2009;199:398–404
  45. Kassem A, Technau K, Kurz AK, Pantulu D, Loning M, Kayser G, et al. Merkel cell polyomavirus sequences are frequently detected in nonmelanoma skin cancer of immunosuppressed patients. Int. J. Cancer. 2009;125:356–361
  46. zur Hausen H. Novel human polyomaviruses – re-emergence of a well known virus family as possible human carcinogens. Int. J. Cancer. 2008;123:247–250
  47. Sihto H, Kukko H, Koljonen V, Sankila R, Bohling T, Joensuu H. Clinical factors associated with Merkel cell polyomavirus infection in Merkel cell carcinoma. J. Natl. Cancer Inst. 2009;101:938–945
  48. Pett M, Coleman N. Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis?. J. Pathol. 2007;212:356–367
  49. Del Valle L, White MK, Khalili K. Potential mechanisms of the human polyomavirus JC in neural oncogenesis. J. Neuropathol. Exp. Neurol. 2008;67:729–740
  50. Khalili K, Del Valle L, Otte J, Weaver M, Gordon J. Human neurotropic polyomavirus, JCV, and its role in carcinogenesis. Oncogene. 2003;22:5181–5191
  51. Del Valle L, White MK, Enam S, Oviedo SP, Bromer MQ, Thomas RM, et al. Detection of JC virus DNA sequences and expression of viral T antigen and agnoprotein in esophageal carcinoma. Cancer. 2005;103:516–527
  52. Pina-Oviedo S, Leon-Bojorge B, Cuesta-Mejias T, White MK, Ortiz-Hidalgo C, Khalili K, et al. Glioblastoma multiforme with small cell neuronal-like component: association with human neurotropic JC virus. Acta Neuropathol. 2006;111:388–396
  53. Newcomb PA, Bush AC, Stoner GL, Lampe JW, Potter JD, Bigler J. No evidence of an association of JC virus and colon neoplasia. Cancer Epidemiol. Biomark. Prev. 2004;13:662–666
  54. Boland CR, Bigler J, Newcomb PA, Lampe JW, Potter JD. Evidence for an association between JC virus and colorectal neoplasia. Cancer Epidemiol. Biomark. Prev. 2004;13:2285–2286
  55. Ricciardiello L, Baglioni M, Giovannini C, Pariali M, Cenacchi G, Ripalti A, et al. Induction of chromosomal instability in colonic cells by the human polyomavirus JC virus. Cancer Res. 2003;63:7256–7262
  56. Niv Y, Goel A, Boland CR. JC virus and colorectal cancer: a possible trigger in the chromosomal instability pathways. Curr. Opin. Gastroenterol. 2005;21:85–89
  57. Tognon M, Corallini A, Martini F, Negrini M, Barbanti-Brodano G. Oncogenic transformation by BK virus and association with human tumors. Oncogene. 2003;22:5192–5200
  58. Abend JR, Jiang M, Imperiale MJ. BK virus and human cancer: innocent until proven guilty. Semin. Cancer Biol. 2009;19:252–260
  59. Tauber B, Dobner T. Adenovirus early E4 genes in viral oncogenesis. Oncogene. 2001;20:7847–7854
  60. Pfeffer A, Schubbert R, Orend G, Hilger-Eversheim K, Doerfler W. Integrated viral genomes can be lost from adenovirus type 12-induced hamster tumor cells in a clone-specific, multistep process with retention of the oncogenic phenotype. Virus Res. 1999;59:113–127
  61. Nevels M, Tauber B, Spruss T, Wolf H, Dobner T. “Hit-and-run” transformation by adenovirus oncogenes. J. Virol. 2001;75:3089–3094
  62. Baker A, Rohleder KJ, Hanakahi LA, Ketner G. Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation. J. Virol. 2007;81:7034–7040
  63. Stracker TH, Carson CT, Weitzman MD. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature. 2002;418:348–352
  64. Dallaire F, Blanchette P, Groitl P, Dobner T, Branton PE. Identification of integrin alpha3 as a new substrate of the adenovirus E4orf6/E1B 55-kilodalton E3 ubiquitin ligase complex. J. Virol. 2009;83:5329–5338
  65. Hart LS, Yannone SM, Naczki C, Orlando JS, Waters SB, Akman SA, et al. The adenovirus E4orf6 protein inhibits DNA double strand break repair and radiosensitizes human tumor cells in an E1B-55K-independent manner. J. Biol. Chem. 2005;280:1474–1481
  66. Thompson MP, Kurzrock R. Epstein–Barr virus and cancer. Clin. Cancer Res. 2004;10:803–821
  67. Niller HH, Wolf H, Minarovits J. Epstein–Barr virus. In:  Minarovits J,  Gonczol E,  Valyi-Nagy T editor. Latency Strategies of Herpesviruses. New York: Springer; 2007;p. 154–191
  68. Deyrup AT. Epstein–Barr virus-associated epithelial and mesenchymal neoplasms. Hum. Pathol. 2008;39:473–483
  69. Niller HH, Wolf H, Minarovits J. Regulation and dysregulation of Epstein–Barr virus latency: implications for the development of autoimmune diseases. Autoimmunity. 2008;41:298–328
  70. Maeda E, Akahane M, Kiryu S, Kato N, Yoshikawa T, Hayashi N, et al. Spectrum of Epstein–Barr virus-related diseases: a pictorial review. Jpn. J. Radiol. 2009;27:4–19
  71. Niller HH, Wolf H, Minarovits J. Epigenetic dysregulation of the host cell genome in Epstein–Barr virus-associated neoplasia. Semin. Cancer Biol. 2009;19:158–164
  72. Niller HH, Wolf H, Ay E, Minarovits J. Epigenetic dysregulation of Epstein–Barr virus latency and development of autoimmune disease. In:  Ballestar E editors. Epigenetic Contributions in Autoimmune Disease. Austin: Landes Bioscience; 2010;p. 1–21
  73. Griffin BE, Karran L. Immortalization of monkey epithelial cells by specific fragments of Epstein–Barr virus DNA. Nature. 1984;309:78–82
  74. Nanbo A, Inoue K, Adachi-Takasawa K, Takada K. Epstein–Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt’s lymphoma. EMBO J. 2002;21:954–965
  75. Iwakiri D, Zhou L, Samanta M, Matsumoto M, Ebihara T, Seya T, et al. Epstein–Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3. J. Exp. Med. 2009;206:2091–2099
  76. Geser A, De The G, Lenoir G, Day NE, Williams EH. Final case reporting from the Ugandan prospective study of the relationship between EBV and Burkitt’s lymphoma. Int. J. Cancer. 1982;29:397–400
  77. Mueller N, Evans A, Harris NL, Comstock GW, Jellum E, Magnus K, et al. Hodgkin’s disease and Epstein–Barr virus. Altered antibody pattern before diagnosis. New Engl. J. Med. 1989;320:689–695
  78. Levine PH, Stemmermann G, Lennette ET, Hildesheim A, Shibata D, Nomura A. Elevated antibody titers to Epstein–Barr virus prior to the diagnosis of Epstein–Barr-virus-associated gastric adenocarcinoma. Int. J. Cancer. 1995;60:642–644
  79. Zeng Y, Zhang LG, Li HY, Jan MG, Zhang Q, Wu YC, et al. Serological mass survey for early detection of nasopharyngeal carcinoma in Wuzhou City, China. Int. J. Cancer. 1982;29:139–141
  80. Miller G, Rabson M, Heston L. Epstein–Barr virus with heterogeneous DNA disrupts latency. J. Virol. 1984;50:174–182
  81. Miller G, Heston L, Countryman J. P3HR-1 Epstein–Barr virus with heterogeneous DNA is an independent replicon maintained by cell-to-cell spread. J. Virol. 1985;54:45–52
  82. Ikuta K, Srinivas SK, Schacker T, Miyagi J, Scott RS, Sixbey JW. Points of recombination in Epstein–Barr virus (EBV) strain P3HR-1-derived heterogeneous DNA as indexes to EBV DNA recombinogenic events in vivo. J. Virol. 2008;82:11516–11525
  83. Patton DF, Shirley P, Raab-Traub N, Resnick L, Sixbey JW. Defective viral DNA in Epstein–Barr virus-associated oral hairy leukoplakia. J. Virol. 1990;64:397–400
  84. Ryan JL, Morgan DR, Dominguez RL, Thorne LB, Elmore SH, Mino-Kenudson M, et al. High levels of Epstein–Barr virus DNA in latently infected gastric adenocarcinoma. Lab. Invest. 2009;89:80–90
  85. Jankelevich S, Kolman JL, Bodnar JW, Miller G. A nuclear matrix attachment region organizes the Epstein–Barr viral plasmid in Raji cells into a single DNA domain. EMBO J. 1992;11:1165–1176
  86. Wensing B, Stuhler A, Jenkins P, Hollyoake M, Karstegl CE, Farrell PJ. Variant chromatin structure of the oriP region of Epstein–Barr virus and regulation of EBER1 expression by upstream sequences and oriP. J. Virol. 2001;75:6235–6241
  87. White RE, Wade-Martins R, James MR. Sequences adjacent to oriP improve the persistence of Epstein–Barr virus-based episomes in B cells. J. Virol. 2001;75:11249–11252
  88. Bankier AT, Deininger PL, Farrell PJ, Barrell BG. Sequence analysis of the 17, 166 base-pair EcoRI fragment C of B95-8 Epstein–Barr virus. Mol. Biol. Med. 1983;1:21–45
  89. Jones MD, Foster L, Sheedy T, Griffin BE. The EB virus genome in Daudi Burkitt’s lymphoma cells has a deletion similar to that observed in a non-transforming strain (P3HR-1) of the virus. EMBO J. 1984;3:813–821
  90. Kolman JL, Kolman CJ, Miller G. Marked variation in the size of genomic plasmids among members of a family of related Epstein–Barr viruses. Proc. Natl. Acad. Sci. USA. 1992;89:7772–7776
  91. Adams A, Lindahl T, Klein G. Linear association between cellular DNA and Epstein–Barr virus DNA in a human lymphoblastoid cell line. Proc. Natl. Acad. Sci. USA. 1973;70:2888–2892
  92. Kaschka-Dierich C, Adams A, Lindahl T, Bornkamm GW, Bjursell G, Klein G, et al. Intracellular forms of Epstein–Barr virus DNA in human tumour cells in vivo. Nature. 1976;260:302–306
  93. Gulley ML, Raphael M, Lutz CT, Ross DW, Raab-Traub N. Epstein–Barr virus integration in human lymphomas and lymphoid cell lines. Cancer. 1992;70:185–191
  94. Delecluse HJ, Bartnizke S, Hammerschmidt W, Bullerdiek J, Bornkamm GW. Episomal and integrated copies of Epstein–Barr virus coexist in Burkitt lymphoma cell lines. J. Virol. 1993;67:1292–1299
  95. Wolf J, Pawlita M, Jox A, Kohls S, Bartnitzke S, Diehl V, et al. Integration of Epstein Barr virus near the breakpoint of a translocation 11; 19 in a Burkitt’s lymphoma cell line. Cancer Genet. Cytogenet. 1993;67:90–94
  96. Wolf J, Jox A, Skarbek H, Pukrop T, Bartnitzke S, Pawlita M, et al. Selective loss of integrated Epstein–Barr virus genomes after long-term cultivation of Burkitt’s lymphoma×B-lymphoblastoid cell hybrids due to chromatin instability at the integration site. Virology. 1995;212:179–185
  97. Jox A, Rohen C, Belge G, Bartnitzke S, Pawlita M, Diehl V, et al. Integration of Epstein–Barr virus in Burkitt’s lymphoma cells leads to a region of enhanced chromosome instability. Ann. Oncol. 1997;8(Suppl. 2):131–135
  98. Shimizu N, Tanabe-Tochikura A, Kuroiwa Y, Takada K. Isolation of Epstein–Barr virus (EBV)-negative cell clones from the EBV-positive Burkitt’s lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J. Virol. 1994;68:6069–6073
  99. Srinivas SK, Sample JT, Sixbey JW. Spontaneous loss of viral episomes accompanying Epstein–Barr virus reactivation in a Burkitt’s lymphoma cell line. J. Infect. Dis. 1998;177:1705–1709
  100. Razzouk BI, Srinivas S, Sample CE, Singh V, Sixbey JW. Epstein–Barr virus DNA recombination and loss in sporadic Burkitt’s lymphoma. J. Infect. Dis. 1996;173:529–535
  101. Trivedi P, Zhang QJ, Chen F, Minarovits J, Ekman M, Biberfeld P, et al. Parallel existence of Epstein–Barr virus (EBV) positive and negative cells in a sporadic case of Burkitt lymphoma. Oncogene. 1995;11:505–510
  102. Niller HH, Salamon D, Ilg K, Koroknai A, Banati F, Bauml G, et al. The in vivo binding site for oncoprotein c-Myc in the promoter for Epstein–Barr virus (EBV) encoding RNA (EBER) 1 suggests a specific role for EBV in lymphoma genesis. Med. Sci. Monit. 2003;9:HY1–HY9
  103. Niller HH, Salamon D, Ilg K, Koroknai A, Banati F, Schwarzmann F, et al. EBV-associated neoplasms: alternative pathogenetic pathways. Med. Hypotheses. 2004;62:387–391
  104. Niller HH, Salamon D, Banati F, Schwarzmann F, Wolf H, Minarovits J. The LCR of EBV makes Burkitt’s lymphoma endemic. Trends Microbiol. 2004;12:495–499
  105. Chau CM, Lieberman PM. Dynamic chromatin boundaries delineate a latency control region of Epstein–Barr virus. J. Virol. 2004;78:12308–12319
  106. Day L, Chau CM, Nebozhyn M, Rennekamp AJ, Showe M, Lieberman PM. Chromatin profiling of Epstein–Barr virus latency control region. J. Virol. 2007;81:6389–6401
  107. Salamon D, Banati F, Koroknai A, Ravasz M, Szenthe K, Bathori Z, et al. Binding of CCCTC-binding factor in vivo to the region located between Rep∗ and C-promoter of Epstein–Barr virus is unaffected by CpG methylation and does not correlate with Cp activity. J. Gen. Virol. 2009;
  108. Keegan TH, Glaser SL, Clarke CA, Gulley ML, Craig FE, Digiuseppe JA, et al. Epstein–Barr virus as a marker of survival after Hodgkin’s lymphoma: a population-based study. J. Clin. Oncol. 2005;23:7604–7613
  109. Kvale G, Hoiby EA, Pedersen E. Hodgkin’s disease in patients with previous infectious mononucleosis. Int. J. Cancer. 1979;23:593–597
  110. Hjalgrim H, Askling J, Rostgaard K, Hamilton-Dutoit S, Frisch M, Zhang JS, et al. Characteristics of Hodgkin’s lymphoma after infectious mononucleosis. New Engl. J. Med. 2003;349:1324–1332
  111. O’Grady J, Stewart S, Elton RA, Krajewski AS. Epstein–Barr virus in Hodgkin’s disease and site of origin of tumour. Lancet. 1994;343:265–266
  112. Veltri RW, Shah SH, McClung JE, Klingberg WG, Sprinkle PM. Epstein–Barr virus fatal infectious mononucleosis, and Hodgkin’s disease in siblings. Cancer. 1983;51:509–520
  113. Hjalgrim H, Smedby KE, Rostgaard K, Molin D, Hamilton-Dutoit S, Chang ET, et al. Infectious mononucleosis, childhood social environment, and risk of Hodgkin lymphoma. Cancer Res. 2007;67:2382–2388
  114. He Y, Xiao R, Ji X, Li L, Chen L, Xiong J, et al. EBV promotes human CD8 NKT cell development. PLoS Pathog. 2010;20(6):e1000915
  115. Biggar RJ, Jaffe ES, Goedert JJ, Chaturvedi A, Pfeiffer R, Engels EA. Hodgkin lymphoma and immunodeficiency in persons with HIV/AIDS. Blood. 2006;108:3786–3791
  116. Diepstra A, Niens M, Vellenga E, van Imhoff GW, Nolte IM, Schaapveld M, et al. Association with HLA class I in Epstein–Barr-virus-positive and with HLA class III in Epstein–Barr-virus-negative Hodgkin’s lymphoma. Lancet. 2005;365:2216–2224
  117. Niens M, Jarrett RF, Hepkema B, Nolte IM, Diepstra A, Platteel M, et al. HLA-A∗02 is associated with a reduced risk and HLA-A∗01 with an increased risk of developing EBV + Hodgkin lymphoma. Blood. 2007;110:3310–3315
  118. McAulay KA, Higgins CD, Macsween KF, Lake A, Jarrett RF, Robertson FL, et al. HLA class I polymorphisms are associated with development of infectious mononucleosis upon primary EBV infection. J. Clin. Invest. 2007;117:3042–3048
  119. Glaser SL, Lin RJ, Stewart SL, Ambinder RF, Jarrett RF, Brousset P, et al. Epstein–Barr virus-associated Hodgkin’s disease: epidemiologic characteristics in international data. Int. J. Cancer. 1997;70:375–382
  120. Alexander FE, Lawrence DJ, Freeland J, Krajewski AS, Angus B, Taylor GM, et al. An epidemiologic study of index and family infectious mononucleosis and adult Hodgkin’s disease (HD): evidence for a specific association with EBV+ve HD in young adults. Int. J. Cancer. 2003;107:298–302
  121. Delecluse HJ, Marafioti T, Hummel M, Dallenbach F, Anagnostopoulos I, Stein H. Disappearance of the Epstein–Barr virus in a relapse of Hodgkin’s disease. J. Pathol. 1997;182:475–479
  122. Brousset P, Schlaifer D, Meggetto F, Bachmann E, Rothenberger S, Pris J, et al. Persistence of the same viral strain in early and late relapses of Epstein–Barr virus-associated Hodgkin’s disease. Blood. 1994;84:2447–2451
  123. Nerurkar AY, Vijayan P, Srinivas V, Soman CS, Dinshaw KA, Advani SH, et al. Discrepancies in Epstein–Barr virus association at presentation and relapse of classical Hodgkin’s disease: impact on pathogenesis. Ann. Oncol. 2000;11:475–478
  124. Staratschek-Jox A, Kotkowski S, Belge G, Rudiger T, Bullerdiek J, Diehl V, et al. Detection of Epstein–Barr virus in Hodgkin–Reed–Sternberg cells: no evidence for the persistence of integrated viral fragments inLatent membrane protein-1 (LMP-1)-negative classical Hodgkin’s disease. Am. J. Pathol. 2000;156:209–216
  125. Gallagher A, Perry J, Freeland J, Alexander FE, Carman WF, Shield L, et al. Hodgkin lymphoma and Epstein–Barr virus (EBV): No evidence to support hit-and-run mechanism in cases classified as non-EBV-associated. Int. J. Cancer. 2003;104:624–630
  126. Rowlings PA, Curtis RE, Passweg JR, Deeg HJ, Socie G, Travis LB, et al. Increased incidence of Hodgkin’s disease after allogeneic bone marrow transplantation. J. Clin. Oncol. 1999;17:3122–3127
  127. Gan YJ, Razzouk BI, Su T, Sixbey JW. A defective rearranged Epstein–Barr virus genome in EBER-negative and EBER-positive Hodgkin’s disease. Am. J. Pathol. 2002;160:781–786
  128. Savu A, Potter J, Li S, Yasui Y. Breast cancer and microbial cancer incidence in female populations around the world: a surprising hyperbolic association. Int. J. Cancer. 2008;123:1094–1099
  129. Gutensohn N, Cole P. Epidemiology of hodgkin’s disease in the young. Int. J. Cancer. 1977;19:595–604
  130. Richardson A. Is breast cancer caused by late exposure to a common virus?. Med. Hypotheses. 1997;48:491–497
  131. Strum SB, Park JK, Rappaport H. Observation of cells resembling Sternberg–Reed cells in conditions other than Hodgkin’s disease. Cancer. 1970;26:176–190
  132. Yasui Y, Potter JD, Stanford JL, Rossing MA, Winget MD, Bronner M, et al. Breast cancer risk and “delayed” primary Epstein–Barr virus infection. Cancer Epidemiol. Biomarkers Prev. 2001;10:9–16
  133. Glaser SL, Hsu JL, Gulley ML. Epstein–Barr virus and breast cancer: state of the evidence for viral carcinogenesis. Cancer Epidemiol. Biomarkers Prev. 2004;13:688–697
  134. Labrecque LG, Barnes DM, Fentiman IS, Griffin BE. Epstein–Barr virus in epithelial cell tumors: a breast cancer study. Cancer Res. 1995;55:39–45
  135. Arbach H, Viglasky V, Lefeu F, Guinebretiere JM, Ramirez V, Bride N, et al. Epstein–Barr virus (EBV) genome and expression in breast cancer tissue: effect of EBV infection of breast cancer cells on resistance to paclitaxel (Taxol). J. Virol. 2006;80:845–853
  136. Huang J, Chen H, Hutt-Fletcher L, Ambinder RF, Hayward SD. Lytic viral replication as a contributor to the detection of Epstein–Barr virus in breast cancer. J. Virol. 2003;77:13267–13274
  137. Bonnet M, Guinebretiere JM, Kremmer E, Grunewald V, Benhamou E, Contesso G, et al. Detection of Epstein–Barr virus in invasive breast cancers. J. Natl. Cancer Inst. 1999;91:1376–1381
  138. Stewart T, Tsai SC, Grayson H, Henderson R, Opelz G. Incidence of de-novo breast cancer in women chronically immunosuppressed after organ transplantation. Lancet. 1995;346:796–798
  139. Wolf H, zur Hausen H, Becker V. EB viral genomes in epithelial nasopharyngeal carcinoma cells. Nat. New Biol. 1973;244:245–247
  140. Desgranges C, Wolf H, de The G, Shanmugaratnam K, Cammoun N, Ellouz R, et al. Nasopharyngeal carcinoma. X. Presence of Epstein–Barr genomes in separated epithelial cells of tumours in patients from Singapore, Tunisia and Kenya. Int. J. Cancer. 1975;16:7–15
  141. Zeng Y. Seroepidemiological studies on nasopharyngeal carcinoma in China. Adv. Cancer Res. 1985;44:121–138
  142. Zeng Y. EB virus, nasopharyngeal carcinoma,. In:  Zeng Y,  Ou B editor. Etiology and Pathogenesis of Nasopharyngeal Carcinoma. Beijing: The People’s Medical Publishing House; 1987;p. 18
  143. Lo KW, To KF, Huang DP. Focus on nasopharyngeal carcinoma. Cancer Cell. 2004;5:423–428
  144. Yeung WM, Zong YS, Chiu CT, Chan KH, Sham JS, Choy DT, et al. Epstein–Barr virus carriage by nasopharyngeal carcinoma in situ. Int. J. Cancer. 1993;53:746–750
  145. Sam CK, Brooks LA, Niedobitek G, Young LS, Prasad U, Rickinson AB. Analysis of Epstein–Barr virus infection in nasopharyngeal biopsies from a group at high risk of nasopharyngeal carcinoma. Int. J. Cancer. 1993;53:957–962
  146. Pathmanathan R, Prasad U, Sadler R, Flynn K, Raab-Traub N. Clonal proliferations of cells infected with Epstein–Barr virus in preinvasive lesions related to nasopharyngeal carcinoma. New Engl. J. Med. 1995;333:693–698
  147. Pak MW, To KF, Lo YM, Chan LY, Tong JH, Lo KW, et al. Nasopharyngeal carcinoma in situ (NPCIS) – pathologic and clinical perspectives. Head Neck. 2002;24:989–995
  148. Cheung FM, Pang SW, Yau TK, Chow SK, Lo KW. Nasopharyngeal intraepithelial lesion: latent Epstein–Barr virus infection with malignant potential. Histopathology. 2004;45:171–179
  149. Raab-Traub N. Epstein–Barr virus in the pathogenesis of NPC. Semin. Cancer Biol. 2002;12:431–441
  150. zur Hausen H, de Villiers EM. Virus target cell conditioning model to explain some epidemiologic characteristics of childhood leukemias and lymphomas. Int. J. Cancer. 2005;115:1–5
  151. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, et al. Functional delivery of viral miRNAs via exosomes. Proc. Natl. Acad. Sci. USA. 2010;107:6328–6333
  152. Cheung ST, Huang DP, Hui AB, Lo KW, Ko CW, Tsang YS, et al. Nasopharyngeal carcinoma cell line (C666-1) consistently harbouring Epstein–Barr virus. Int. J. Cancer. 1999;83:121–126
  153. Dittmer DP, Hilscher CJ, Gulley ML, Yang EV, Chen M, Glaser R. Multiple pathways for Epstein–Barr virus episome loss from nasopharyngeal carcinoma. Int. J. Cancer. 2008;123:2105–2112
  154. Teramoto N, Maeda A, Kobayashi K, Hayashi K, Oka T, Takahashi K, et al. Epstein–Barr virus infection to Epstein–Barr virus-negative nasopharyngeal carcinoma cell line TW03 enhances its tumorigenicity. Lab. Invest. 2000;80:303–312
  155. Kripalani-Joshi S, Law HY. Identification of integrated Epstein–Barr virus in nasopharyngeal carcinoma using pulse field gel electrophoresis. Int. J. Cancer. 1994;56:187–192
  156. Hitt MM, Allday MJ, Hara T, Karran L, Jones MD, Busson P, et al. EBV gene expression in an NPC-related tumour. EMBO J. 1989;8:2639–2651
  157. Smith P. Epstein–Barr virus complementary strand transcripts (CSTs/BARTs) and cancer. Semin. Cancer Biol. 2001;11:469–476
  158. Karran L, Teo CG, King D, Hitt MM, Gao YN, Wedderburn N, et al. Establishment of immortalized primate epithelial cells with sub-genomic EBV DNA. Int. J. Cancer. 1990;45:763–772
  159. Xue SA, Lampert IA, Haldane JS, Bridger JE, Griffin BE. Epstein–Barr virus gene expression in human breast cancer: protagonist or passenger?. Br. J. Cancer. 2003;89:113–119
  160. Gao Y, Lu YJ, Xue SA, Chen H, Wedderburn N, Griffin BE. Hypothesis: a novel route for immortalization of epithelial cells by Epstein–Barr virus. Oncogene. 2002;21:825–835
  161. Counter CM, Botelho FM, Wang P, Harley CB, Bacchetti S. Stabilization of short telomeres and telomerase activity accompany immortalization of Epstein–Barr virus-transformed human B lymphocytes. J. Virol. 1994;68:3410–3414
  162. Hochberg D, Middeldorp JM, Catalina M, Sullivan JL, Luzuriaga K, Thorley-Lawson DA. Demonstration of the Burkitt’s lymphoma Epstein–Barr virus phenotype in dividing latently infected memory cells in vivo. Proc. Natl. Acad. Sci. USA. 2004;101:239–244
  163. Souza TA, Stollar BD, Sullivan JL, Luzuriaga K, Thorley-Lawson DA. Peripheral B cells latently infected with Epstein–Barr virus display molecular hallmarks of classical antigen-selected memory B cells. Proc. Natl. Acad. Sci. USA. 2005;102:18093–18098
  164. Niller HH, Salamon D, Rahmann S, Ilg K, Koroknai A, Banati F, et al. A 30 kb region of the Epstein–Barr virus genome is colinear with the rearranged human immunoglobulin gene loci: implications for a “ping-pong evolution” model for persisting viruses and their hosts. A review. Acta Microbiol. Immunol. Hung. 2004;51:469–484
  165. Hsu DH, de Waal MR, Fiorentino DF, Dang MN, Vieira P, de Vries J, et al. Expression of interleukin-10 activity by Epstein–Barr virus protein BCRF1. Science. 1990;250:830–832
  166. Kilger E, Kieser A, Baumann M, Hammerschmidt W. Epstein–Barr virus-mediated B-cell proliferation is dependent upon latent membrane protein 1, which simulates an activated CD40 receptor. EMBO J. 1998;17:1700–1709
  167. Caldwell RG, Wilson JB, Anderson SJ, Longnecker R. Epstein–Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals. Immunity. 1998;9:405–411
  168. Goossens T, Klein U, Kuppers R. Frequent occurrence of deletions and duplications during somatic hypermutation: implications for oncogene translocations and heavy chain disease. Proc. Natl. Acad. Sci. USA. 1998;95:2463–2468
  169. Brys A, Maizels N. LR1 regulates c-myc transcription in B-cell lymphomas. Proc. Natl. Acad. Sci. USA. 1994;91:4915–4919
  170. Sun R, Spain TA, Lin SF, Miller G. Autoantigenic proteins that bind recombinogenic sequences in Epstein–Barr virus and cellular DNA. Proc. Natl. Acad. Sci. USA. 1994;91:8646–8650
  171. Li MJ, Maizels N. Activation and targeting of immunoglobulin switch recombination by activities induced by EBV infection. J. Immunol. 1999;163:6659–6664
  172. Bornkamm GW, Hudewentz J, Freese UK, Zimber U. Deletion of the nontransforming Epstein–Barr virus strain P3HR-1 causes fusion of the large internal repeat to the DSL region. J. Virol. 1982;43:952–968
  173. Rabson M, Gradoville L, Heston L, Miller G. Non-immortalizing P3J-HR-1 Epstein–Barr virus: a deletion mutant of its transforming parent, Jijoye. J. Virol. 1982;44:834–844
  174. Patton DF, Ribeiro RC, Jenkins JJ, Sixbey JW. Thymic carcinoma with a defective Epstein–Barr virus encoding the BZLF1 trans-activator. J. Infect. Dis. 1994;170:7–12
  175. Epeldegui M, Hung YP, McQuay A, Ambinder RF, Martinez-Maza O. Infection of human B cells with Epstein–Barr virus results in the expression of somatic hypermutation-inducing molecules and in the accrual of oncogene mutations. Mol. Immunol. 2007;44:934–942
  176. Chapman CJ, Mockridge CI, Rowe M, Rickinson AB, Stevenson FK. Analysis of VH genes used by neoplastic B cells in endemic Burkitt’s lymphoma shows somatic hypermutation and intraclonal heterogeneity. Blood. 1995;85:2176–2181
  177. Tamaru J, Hummel M, Marafioti T, Kalvelage B, Leoncini L, Minacci C, et al. Burkitt’s lymphomas express VH genes with a moderate number of antigen-selected somatic mutations. Am. J. Pathol. 1995;147:1398–1407
  178. Harris RS, Croom-Carter DS, Rickinson AB, Neuberger MS. Epstein–Barr virus and the somatic hypermutation of immunoglobulin genes in Burkitt’s lymphoma cells. J. Virol. 2001;75:10488–10492
  179. Gualandi G, Giselico L, Carloni M, Palitti F, Mosesso P, Alfonsi AM. Enhancement of genetic instability in human B cells by Epstein–Barr virus latent infection. Mutagenesis. 2001;16:203–208
  180. Liu MT, Chen YR, Chen SC, Hu CY, Lin CS, Chang YT, et al. Epstein–Barr virus latent membrane protein 1 induces micronucleus formation, represses DNA repair and enhances sensitivity to DNA-damaging agents in human epithelial cells. Oncogene. 2004;23:2531–2539
  181. Ramiro AR, Jankovic M, Callen E, Difilippantonio S, Chen HT, McBride KM, et al. Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature. 2006;440:105–109
  182. He B, Raab-Traub N, Casali P, Cerutti A. EBV-encoded latent membrane protein 1 cooperates with BAFF/BLyS and APRIL to induce T cell-independent Ig heavy chain class switching. J. Immunol. 2003;171:5215–5224
  183. Tobollik S, Meyer L, Buettner M, Klemmer S, Kempkes B, Kremmer E, et al. Epstein–Barr virus nuclear antigen 2 inhibits AID expression during EBV-driven B-cell growth. Blood. 2006;108:3859–3864
  184. Araujo I, Foss HD, Hummel M, Anagnostopoulos I, Barbosa HS, Bittencourt A, et al. Frequent expansion of Epstein–Barr virus (EBV) infected cells in germinal centres of tonsils from an area with a high incidence of EBV-associated lymphoma. J. Pathol. 1999;187:326–330
  185. Kurth J, Hansmann ML, Rajewsky K, Kuppers R. Epstein–Barr virus-infected B cells expanding in germinal centers of infectious mononucleosis patients do not participate in the germinal center reaction. Proc. Natl. Acad. Sci. USA. 2003;100:4730–4735
  186. Roughan JE, Thorley-Lawson DA. The intersection of Epstein–Barr virus with the germinal center. J. Virol. 2009;83:3968–3976
  187. Roughan JE, Torgbor C, Thorley-Lawson DA. Germinal center B cells latently infected with Epstein–Barr virus proliferate extensively but do not increase in number. J. Virol. 2010;84:1158–1168
  188. Uchida J, Yasui T, Takaoka-Shichijo Y, Muraoka M, Kulwichit W, Raab-Traub N, et al. Mimicry of CD40 signals by Epstein–Barr virus LMP1 in B lymphocyte responses. Science. 1999;286:300–303
  189. Srinivas SK, Sixbey JW. Epstein–Barr virus induction of recombinase-activating genes RAG1 and RAG2. J. Virol. 1995;69:8155–8158
  190. Tsimbouri P, Drotar ME, Coy JL, Wilson JB. Bcl-xL and RAG genes are induced and the response to IL-2 enhanced in EmuEBNA-1 transgenic mouse lymphocytes. Oncogene. 2002;21:5182–5187
  191. Kuhn-Hallek I, Sage DR, Stein L, Groelle H, Fingeroth JD. Expression of recombination activating genes (RAG-1 and RAG-2) in Epstein–Barr virus-bearing B cells. Blood. 1995;85:1289–1299
  192. Wagner HJ, Scott RS, Buchwald D, Sixbey JW. Peripheral blood lymphocytes express recombination-activating genes 1 and 2 during Epstein–Barr virus-induced infectious mononucleosis. J. Infect. Dis. 2004;190:979–984
  193. Dreyfus DH. The DDE recombinases: diverse roles in acquired and innate immunity. Ann. Allergy Asthma Immunol. 2006;97:567–576
  194. Dreyfus DH. Paleo-immunology: evidence consistent with insertion of a primordial herpes virus-like element in the origins of acquired immunity. PLoS ONE. 2009;4:e5778
  195. Meru N, Jung A, Lisner R, Niedobitek G. Expression of the recombination activating genes (RAG1 and RAG2) is not detectable in Epstein–Barr virus-associated human lymphomas. Int. J. Cancer. 2001;92:75–78
  196. Meru N, Jung A, Baumann I, Niedobitek G. Expression of the recombination-activating genes in extrafollicular lymphocytes but no apparent reinduction in germinal center reactions in human tonsils. Blood. 2002;99:531–537
  197. Sato H, Takimoto T, Tanaka S, Tanaka J, Raab-Traub N. Concatameric replication of Epstein–Barr virus: structure of the termini in virus-producer and newly transformed cell lines. J. Virol. 1990;64:5295–5300
  198. Sun R, Spain TA, Lin SF, Miller G. Sp1 binds to the precise locus of end processing within the terminal repeats of Epstein–Barr virus DNA. J. Virol. 1997;71:6136–6143
  199. Kudoh A, Iwahori S, Sato Y, Nakayama S, Isomura H, Murata T, et al. Homologous recombinational repair factors are recruited and loaded onto the viral DNA genome in Epstein–Barr virus replication compartments. J. Virol. 2009;83:6641–6651
  200. Dreyfus DH. Oncogenesis in Ataxia Telangectasia: roles of ATM, p53, NF-kB and DDE recombination pathogenesis. In:  Ahmad SI editors. Molecular Mechanisms of Ataxia Teleangiectasia. Austin: Landes Bioscience; 2009;p. 78–90
  201. Kimoto Y. Expression of heavy-chain constant region of immunoglobulin and T-cell receptor gene transcripts in human non-hematopoietic tumor cell lines. Genes Chromosomes Cancer. 1998;22:83–86
  202. Chelly J, Concordet JP, Kaplan JC, Kahn A. Illegitimate transcription: transcription of any gene in any cell type. Proc. Natl. Acad. Sci. USA. 1989;86:2617–2621
  203. Qiu X, Zhu X, Zhang L, Mao Y, Zhang J, Hao P, et al. Human epithelial cancers secrete immunoglobulin g with unidentified specificity to promote growth and survival of tumor cells. Cancer Res. 2003;63:6488–6495
  204. Raschke S, Balz V, Efferth T, Schulz WA, Florl AR. Homozygous deletions of CDKN2A caused by alternative mechanisms in various human cancer cell lines. Genes Chromosomes Cancer. 2005;42:58–67
  205. Chen Z, Gu J. Immunoglobulin G expression in carcinomas and cancer cell lines. FASEB J. 2007;21:2931–2938
  206. Babbage G, Ottensmeier CH, Blaydes J, Stevenson FK, Sahota SS. Immunoglobulin heavy chain locus events and expression of activation-induced cytidine deaminase in epithelial breast cancer cell lines. Cancer Res. 2006;66:3996–4000
  207. Liu HD, Zheng H, Li M, Hu DS, Tang M, Cao Y. Upregulated expression of kappa light chain by Epstein–Barr virus encoded latent membrane protein 1 in nasopharyngeal carcinoma cells via NF-kappaB and AP-1 pathways. Cell Signal. 2007;19:419–427
  208. Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293:1074–1080
  209. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16:6–21
  210. Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 2003;278:4035–4040
  211. Cernilogar FM, Orlando V. Epigenome programming by Polycomb and Trithorax proteins. Biochem. Cell Biol. 2005;83:322–331
  212. Laue K, Daujat S, Crump JG, Plaster N, Roehl HH, Kimmel CB, et al. The multidomain protein Brpf1 binds histones and is required for Hox gene expression and segmental identity. Development. 2008;135:1935–1946
  213. Ushijima T. Epigenetic field for cancerization. J. Biochem. Mol. Biol. 2007;40:142–150
  214. Ehrlich M. DNA hypomethylation and cancer. In:  Ehrlich M editors. DNA Alterations in Cancer. Westborough: Eaton Publishing; 2000;p. 273–291
  215. Hsiao SH, Huang TH, Leu YW. Excavating relics of DNA methylation changes during the development of neoplasia. Semin. Cancer Biol. 2009;19:198–208
  216. Leu YW, Yan PS, Fan M, Jin VX, Liu JC, Curran EM, et al. Loss of estrogen receptor signaling triggers epigenetic silencing of downstream targets in breast cancer. Cancer Res. 2004;64:8184–8192
  217. Sakuma K, Chong JM, Sudo M, Ushiku T, Inoue Y, Shibahara J, et al. High-density methylation of p14ARF and p16INK4A in Epstein–Barr virus-associated gastric carcinoma. Int. J. Cancer. 2004;112:273–278
  218. Ushiku T, Chong JM, Uozaki H, Hino R, Chang MS, Sudo M, et al. P73 gene promoter methylation in Epstein–Barr virus-associated gastric carcinoma. Int. J. Cancer. 2007;120:60–66
  219. Kang GH, Lee S, Cho NY, Gandamihardja T, Long TI, Weisenberger DJ, et al. DNA methylation profiles of gastric carcinoma characterized by quantitative DNA methylation analysis. Lab. Invest. 2008;88:161–170
  220. Fletcher TM, Xiao N, Mautino G, Baumann CT, Wolford R, Warren BS, et al. ATP-dependent mobilization of the glucocorticoid receptor during chromatin remodeling. Mol. Cell Biol. 2002;22:3255–3263
  221. Nagaich AK, Rayasam GV, Martinez ED, Becker M, Qiu Y, Johnson TA, et al. Subnuclear trafficking and gene targeting by steroid receptors. Ann. NY Acad. Sci. 2004;1024:213–220
  222. Yao T, Song L, Jin J, Cai Y, Takahashi H, Swanson SK, et al. Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the Ino80 chromatin-remodeling complex. Mol. Cell. 2008;31:909–917
  223. Jung JK, Arora P, Pagano JS, Jang KL. 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. 2007;67:5771–5778
  224. Park IY, Sohn BH, Yu E, Suh DJ, Chung YH, Lee JH, et al. Aberrant epigenetic modifications in hepatocarcinogenesis induced by hepatitis B virus X protein. Gastroenterology. 2007;132:1476–1494
  225. Nagai H, Baba M, Konishi N, Kim YS, Nogami M, Okumura K, et al. Isolation of NotI clusters hypomethylated in HBV-integrated hepatocellular carcinomas by two-dimensional electrophoresis. DNA Res. 1999;6:219–225
  226. Arora P, Kim EO, Jung JK, Jang KL. Hepatitis C virus core protein downregulates E-cadherin expression via activation of DNA methyltransferase 1 and 3b. Cancer Lett. 2008;261:244–252
  227. Naka K, Abe K, Takemoto K, Dansako H, Ikeda M, Shimotohno K, et al. Epigenetic silencing of interferon-inducible genes is implicated in interferon resistance of hepatitis C virus replicon-harboring cells. J. Hepatol. 2006;44:869–878
  228. Yang B, Guo M, Herman JG, Clark DP. Aberrant promoter methylation profiles of tumor suppressor genes in hepatocellular carcinoma. Am. J. Pathol. 2003;163:1101–1107
  229. Li X, Hui AM, Sun L, Hasegawa K, Torzilli G, Minagawa M, et al. P16INK4A hypermethylation is associated with hepatitis virus infection, age, and gender in hepatocellular carcinoma. Clin. Cancer Res. 2004;10:7484–7489
  230. Narimatsu T, Tamori A, Koh N, Kubo S, Hirohashi K, Yano Y, et al. P16 promoter hypermethylation in human hepatocellular carcinoma with or without hepatitis virus infection. Intervirology. 2004;47:26–31
  231. Helt AM, Galloway DA. Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis. 2003;24:159–169
  232. Iaquinta PJ, Lees JA. Life and death decisions by the E2F transcription factors. Curr. Opin. Cell Biol. 2007;19:649–657
  233. McCabe MT, Davis JN, Day ML. Regulation of DNA methyltransferase 1 by the pRb/E2F1 pathway. Cancer Res. 2005;65:3624–3632
  234. McCabe MT, Low JA, Imperiale MJ, Day ML. Human polyomavirus BKV transcriptionally activates DNA methyltransferase 1 through the pRb/E2F pathway. Oncogene. 2006;25:2727–2735
  235. Burgers WA, Blanchon L, Pradhan S, de Launoit Y, Kouzarides T, Fuks F. Viral oncoproteins target the DNA methyltransferases. Oncogene. 2007;26:1650–1655
  236. Lilley CE, Chaurushiya MS, Weitzman MD. Chromatin at the intersection of viral infection and DNA damage. Biochim. Biophys. Acta. 2009;1:1–10(epub ahead of print)
  237. Heller H, Kammer C, Wilgenbus P, Doerfler W. Chromosomal insertion of foreign (adenovirus type 12, plasmid, or bacteriophage lambda) DNA is associated with enhanced methylation of cellular DNA segments. Proc. Natl. Acad. Sci. USA. 1995;92:5515–5519
  238. Doerfler W. Epigenetic mechanisms in human adenovirus type 12 oncogenesis. Semin. Cancer Biol. 2009;19:136–143
  239. Ewald D, Li M, Efrat S, Auer G, Wall RJ, Furth PA, et al. Time-sensitive reversal of hyperplasia in transgenic mice expressing SV40 T antigen. Science. 1996;273:1384–1386
  240. Furth PA, Li M, Hennighausen L. Studying development of disease through temporally controlled gene expression in the salivary gland. Ann. NY Acad. Sci. 1998;842:181–187
  241. Vertino PM, Issa JP, Pereira-Smith OM, Baylin SB. Stabilization of DNA methyltransferase levels and CpG island hypermethylation precede SV40-induced immortalization of human fibroblasts. Cell Growth Differ. 1994;5:1395–1402
  242. Soejima K, Fang W, Rollins BJ. DNA methyltransferase 3b contributes to oncogenic transformation induced by SV40T antigen and activated Ras. Oncogene. 2003;22:4723–4733
  243. Pantry SN, Medveczky PG. Epigenetic regulation of Kaposi’s sarcoma-associated herpesvirus replication. Semin. Cancer Biol. 2009;19:153–157
  244. Tsai CN, Tsai CL, Tse KP, Chang HY, Chang YS. The Epstein–Barr virus oncogene product, latent membrane protein 1, induces the downregulation of E-cadherin gene expression via activation of DNA methyltransferases. Proc. Natl. Acad. Sci. USA. 2002;99:10084–10089
  245. Tsai CL, Li HP, Lu YJ, Hsueh C, Liang Y, Chen CL, et al. Activation of DNA methyltransferase 1 by EBV LMP1 Involves c-Jun NH(2)-terminal kinase signaling. Cancer Res. 2006;66:11668–11676
  246. Shamay M, Krithivas A, Zhang J, Hayward SD. Recruitment of the de novo DNA methyltransferase Dnmt3a by Kaposi’s sarcoma-associated herpesvirus LANA. Proc. Natl. Acad. Sci. USA. 2006;103:14554–14559
  247. Di Bartolo DL, Cannon M, Liu YF, Renne R, Chadburn A, Boshoff C, et al. KSHV LANA inhibits TGF-beta signaling through epigenetic silencing of the TGF-beta type II receptor. Blood. 2008;111:4731–4740
  248. Boxus M, Twizere JC, Legros S, Dewulf JF, Kettmann R, Willems L. The HTLV-1 tax interactome. Retrovirology. 2008;5(76):76
  249. Ching YP, Chan SF, Jeang KT, Jin DY. The retroviral oncoprotein Tax targets the coiled-coil centrosomal protein TAX1BP2 to induce centrosome overduplication. Nat. Cell Biol. 2006;8:717–724
  250. Kamihira S, Atogami S, Sohda H, Momita S, Toryia K, Ikeda S, et al. DNA aneuploidy of adult T-cell leukemia cells. Leuk. Res. 1994;18:79–84
  251. Matsuoka M. Human T-cell leukemia virus type I (HTLV-I) infection and the onset of adult T-cell leukemia (ATL). Retrovirology. 2005;2(27):1–13
  252. Nakase K, Cheng J, Zhu Q, Marasco WA. Mechanisms of SHP-1 P2 promoter regulation in hematopoietic cells and its silencing in HTLV-1-transformed T cells. J. Leukocyte Biol. 2009;85:165–174

PII: S0304-3835(10)00388-5

doi: 10.1016/j.canlet.2010.08.007

Cancer Letters
Volume 305, Issue 2 , Pages 200-217 , 28 June 2011