Human endogenous retroviruses and cancer: Causality and therapeutic possibilities

World Journal of Gastroenterology

Volumn 18, Issue 42, 2012, Pages 6027-6035

  Mullins, Christina S ^a   Linnebacher, Michael ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Gastrointestinal cancer; Human endogenous retroviruses; Therapeutic targets; Tumor specific antigens; Tumorigenesis

Indexed keywords

ANTIRETROVIRUS AGENT; TUMOR ANTIGEN;

ACTIVE IMMUNIZATION; APOPTOSIS; ARTICLE; BREAST CANCER; CYTOTOXIC T LYMPHOCYTE; ENDOGENOUS RETROVIRUS; GERM CELL TUMOR; HODGKIN DISEASE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOGENICITY; KIDNEY CANCER; LONG TERMINAL REPEAT; MELANOMA; METHYLATION; NEOPLASM; NONHUMAN; OPEN READING FRAME; OVARY CANCER; PASSIVE IMMUNIZATION; PROSTATE CANCER; PROTEIN EXPRESSION; RETROVIRUS INFECTION; VIRUS CARCINOGENESIS; VIRUS INHIBITION; VIRUS VIRULENCE;

EID: 84869782319     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v18.i42.6027     Document Type: Article

References (79)

1. Blikstad V, Benachenhou F, Sperber GO, Blomberg J. Evolution of human endogenous retroviral sequences: a conceptual account. Cell Mol Life Sci 2008; 65: 3348-3365
2. Bannert N, Kurth R. Retroelements and the human genome: new perspectives on an old relation. Proc Natl Acad Sci USA 2004; 101 Suppl 2: 14572-14579
3. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, Stange-Thomann N, Stojanovic N, Subramanian A, Wyman D, Rogers J, Sulston J, Ainscough R, Beck S, Bentley D, Burton J, Clee C, Carter N, Coulson A, Deadman R, Deloukas P, Dunham A, Dunham I, Durbin R, French L, Grafham D, Gregory S, Hubbard T, Humphray S, Hunt A, Jones M, Lloyd C, McMurray A, Matthews L, Mercer S, Milne S, Mullikin JC, Mungall A, Plumb R, Ross M, Shownkeen R, Sims S, Waterston RH, Wilson RK, Hillier LW, McPherson JD, Marra MA, Mardis ER, Fulton LA, Chinwalla AT, Pepin KH, Gish WR, Chissoe SL, Wendl MC, Delehaunty KD, Miner TL, Delehaunty A, Kramer JB, Cook LL, Fulton RS, Johnson DL, Minx PJ, Clifton SW, Hawkins T, Branscomb E, Predki P, Richardson P, Wenning S, Slezak T, Doggett N, Cheng JF, Olsen A, Lucas S, Elkin C, Uberbacher E, Frazier M, Gibbs RA, Muzny DM, Scherer SE, Bouck JB, Sodergren EJ, Worley KC, Rives CM, Gorrell JH, Metzker ML, Naylor SL, Kucherlapati RS, Nelson DL, Weinstock GM, Sakaki Y, Fujiyama A, Hattori M, Yada T, Toyoda A, Itoh T, Kawagoe C, Watanabe H, Totoki Y, Taylor T, Weissenbach J, Heilig R, Saurin W, Artiguenave F, Brottier P, Bruls T, Pelletier E, Robert C, Wincker P, Smith DR, Doucette-Stamm L, Rubenfield M, Weinstock K, Lee HM, Dubois J, Rosenthal A, Platzer M, Nyakatura G, Taudien S, Rump A, Yang H, Yu J, Wang J, Huang G, Gu J, Hood L, Rowen L, Madan A, Qin S, Davis RW, Federspiel NA, Abola AP, Proctor MJ, Myers RM, Schmutz J, Dickson M, Grimwood J, Cox DR, Olson MV, Kaul R, Raymond C, Shimizu N, Kawasaki K, Minoshima S, Evans GA, Athanasiou M, Schultz R, Roe BA, Chen F, Pan H, Ramser J, Lehrach H, Reinhardt R, McCombie WR, de la Bastide M, Dedhia N, Blöcker H, Hornischer K, Nordsiek G, Agarwala R, Aravind L, Bailey JA, Bateman A, Batzoglou S, Birney E, Bork P, Brown DG, Burge CB, Cerutti L, Chen HC, Church D, Clamp M, Copley RR, Doerks T, Eddy SR, Eichler EE, Furey TS, Galagan J, Gilbert JG, Harmon C, Hayashizaki Y, Haussler D, Hermjakob H, Hokamp K, Jang W, Johnson LS, Jones TA, Kasif S, Kaspryzk A, Kennedy S, Kent WJ, Kitts P, Koonin EV, Korf I, Kulp D, Lancet D, Lowe TM, McLysaght A, Mikkelsen T, Moran JV, Mulder N, Pollara VJ, Ponting CP, Schuler G, Schultz J, Slater G, Smit AF, Stupka E, Szustakowski J, Thierry-Mieg D, Thierry-Mieg J, Wagner L, Wallis J, Wheeler R, Williams A, Wolf YI, Wolfe KH, Yang SP, Yeh RF, Collins F, Guyer MS, Peterson J, Felsenfeld A, Wetterstrand KA, Patrinos A, Morgan MJ, de Jong P, Catanese JJ, Osoegawa K, Shizuya H, Choi S, Chen YJ. Initial sequencing and analysis of the human genome. Nature 2001; 409: 860-921
4. Cohen M, Larsson E. Human endogenous retroviruses. Bioessays 1988; 9: 191-196
5. Nelson PN, Carnegie PR, Martin J, Davari Ejtehadi H, Hooley P, Roden D, Rowland-Jones S, Warren P, Astley J, Murray PG. Demystified. Human endogenous retroviruses. Mol Pathol 2003; 56: 11-18
6. Volff JN. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 2006; 28: 913-922
7. Goff SP. Retrovirus restriction factors. Mol Cell 2004; 16: 849-859
8. Mbisa JL, Bu W, Pathak VK. APOBEC3F and APOBEC3G inhibit HIV-1 DNA integration by different mechanisms. J Virol 2010; 84: 5250-5259
9. Maksakova IA, Mager DL, Reiss D. Keeping active endogenous retroviral-like elements in check: the epigenetic perspective. Cell Mol Life Sci 2008; 65: 3329-3347
10. Kim DS, Hahn Y. Human-specific antisense transcripts induced by the insertion of transposable element. Int J Mol Med 2010; 26: 151-157
11. Bannert N, Kurth R. The evolutionary dynamics of human endogenous retroviral families. Annu Rev Genomics Hum Genet 2006; 7: 149-173
12. Hedges DJ, Batzer MA. From the margins of the genome: mobile elements shape primate evolution. Bioessays 2005; 27: 785-794
13. Kazazian HH. Mobile elements: drivers of genome evolution. Science 2004; 303: 1626-1632
14. Kozeretska IA, Demydov SV, Ostapchenko LI. Mobile genetic elements and cancer. From mutations to gene therapy. Exp Oncol 2011; 33: 198-205
15. Rowe HM, Trono D. Dynamic control of endogenous retroviruses during development. Virology 2011; 411: 273-287
16. Deininger PL, Batzer MA. Mammalian retroelements. Genome Res 2002; 12: 1455-1465
17. Ling J, Pi W, Bollag R, Zeng S, Keskintepe M, Saliman H, Krantz S, Whitney B, Tuan D. The solitary long terminal repeats of ERV-9 endogenous retrovirus are conserved during primate evolution and possess enhancer activities in embryonic and hematopoietic cells. J Virol 2002; 76: 2410-2423
18. Medstrand P, Landry JR, Mager DL. Long terminal repeats are used as alternative promoters for the endothelin B receptor and apolipoprotein C-I genes in humans. J Biol Chem 2001; 276: 1896-1903
19. Kim DS, Hahn Y. Identification of human-specific transcript variants induced by DNA insertions in the human genome. Bioinformatics 2011; 27: 14-21
20. Pötgens AJ, Drewlo S, Kokozidou M, Kaufmann P. Syncytin: the major regulator of trophoblast fusion? Recent developments and hypotheses on its action. Hum Reprod Update 2004; 10: 487-496
21. Braoudaki M, Tzortzatou-Stathopoulou F. Tumorigenesis related to retroviral infections. J Infect Dev Ctries 2011; 5: 751-758
22. Maeda N, Fan H, Yoshikai Y. Oncogenesis by retroviruses: old and new paradigms. Rev Med Virol 2008; 18: 387-405
23. Schulz WA, Steinhoff C, Florl AR. Methylation of endogenous human retroelements in health and disease. Curr Top Microbiol Immunol 2006; 310: 211-250
24. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002; 3: 415-428
25. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002; 21: 5400-5413
26. Ruprecht K, Mayer J, Sauter M, Roemer K, Mueller-Lantzsch N. Endogenous retroviruses and cancer. Cell Mol Life Sci 2008; 65: 3366-3382
27. Dunn CA, Medstrand P, Mager DL. An endogenous retroviral long terminal repeat is the dominant promoter for human beta1,3-galactosyltransferase 5 in the colon. Proc Natl Acad Sci USA 2003; 100: 12841-12846
28. Lamprecht B, Walter K, Kreher S, Kumar R, Hummel M, Lenze D, Köchert K, Bouhlel MA, Richter J, Soler E, Stadhouders R, Jöhrens K, Wurster KD, Callen DF, Harte MF, Giefing M, Barlow R, Stein H, Anagnostopoulos I, Janz M, Cockerill PN, Siebert R, Dörken B, Bonifer C, Mathas S. Derepression of an endogenous long terminal repeat activates the CSF1R proto-oncogene in human lymphoma. Nat Med 2010; 16: 571-579, 1p following 579
29. Oricchio E, Sciamanna I, Beraldi R, Tolstonog GV, Schumann GG, Spadafora C. Distinct roles for LINE-1 and HERV-K retroelements in cell proliferation, differentiation and tumor progression. Oncogene 2007; 26: 4226-4233
30. Mangeney M, Heidmann T. Tumor cells expressing a retroviral envelope escape immune rejection in vivo. Proc Natl Acad Sci USA 1998; 95: 14920-14925
31. Blaise S, Mangeney M, Heidmann T. The envelope of Mason-Pfizer monkey virus has immunosuppressive properties. J Gen Virol 2001; 82: 1597-1600
32. Kim C, Rubin CM, Schmid CW. Genome-wide chromatin remodeling modulates the Alu heat shock response. Gene 2001; 276: 127-133
33. Jackson-Grusby L, Beard C, Possemato R, Tudor M, Fambrough D, Csankovszki G, Dausman J, Lee P, Wilson C, Lander E, Jaenisch R. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet 2001; 27: 31-39
34. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674
35. Götzinger N, Sauter M, Roemer K, Mueller-Lantzsch N. Regulation of human endogenous retrovirus-K Gag expression in teratocarcinoma cell lines and human tumours. J Gen Virol 1996; 77 (Pt 12): 2983-2990
36. Boller K, König H, Sauter M, Mueller-Lantzsch N, Löwer R, Löwer J, Kurth R. Evidence that HERV-K is the endogenous retrovirus sequence that codes for the human teratocarcinoma-derived retrovirus HTDV. Virology 1993; 196: 349-353
37. Menendez L, Benigno BB, McDonald JF. L1 and HERV-W retrotransposons are hypomethylated in human ovarian carcinomas. Mol Cancer 2004; 3: 12
38. Wang-Johanning F, Liu J, Rycaj K, Huang M, Tsai K, Rosen DG, Chen DT, Lu DW, Barnhart KF, Johanning GL. Expression of multiple human endogenous retrovirus surface envelope proteins in ovarian cancer. Int J Cancer 2007; 120: 81-90
39. Wentzensen N, Coy JF, Knaebel HP, Linnebacher M, Wilz B, Gebert J, von Knebel Doeberitz M. Expression of an endogenous retroviral sequence from the HERV-H group in gastrointestinal cancers. Int J Cancer 2007; 121: 1417-1423
40. Krueger F, Kreck B, Franke A, Andrews SR. DNA methylome analysis using short bisulfite sequencing data. Nat Methods 2012; 9: 145-151
41. Mallet F, Bouton O, Prudhomme S, Cheynet V, Oriol G, Bonnaud B, Lucotte G, Duret L, Mandrand B. The endogenous retroviral locus ERVWE1 is a bona fide gene involved in hominoid placental physiology. Proc Natl Acad Sci USA 2004; 101: 1731-1736
42. Blond JL, Lavillette D, Cheynet V, Bouton O, Oriol G, Chapel-Fernandes S, Mandrand B, Mallet F, Cosset FL. An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J Virol 2000; 74: 3321-3329
43. Dittmar T, Schwitalla S, Seidel J, Haverkampf S, Reith G, Meyer-Staeckling S, Brandt BH, Niggemann B, Zänker KS. Characterization of hybrid cells derived from spontaneous fusion events between breast epithelial cells exhibiting stem-like characteristics and breast cancer cells. Clin Exp Metastasis 2011; 28: 75-90
44. Rappa G, Mercapide J, Lorico A. Spontaneous formation of tumorigenic hybrids between breast cancer and multipotent stromal cells is a source of tumor heterogeneity. Am J Pathol 2012; 180: 2504-2515
45. Lazova R, Chakraborty A, Pawelek JM. Leukocyte-cancer cell fusion: initiator of the warburg effect in malignancy? Adv Exp Med Biol 2011; 714: 151-172
46. Sauter M, Schommer S, Kremmer E, Remberger K, Dölken G, Lemm I, Buck M, Best B, Neumann-Haefelin D, Mueller-Lantzsch N. Human endogenous retrovirus K10: expression of Gag protein and detection of antibodies in patients with seminomas. J Virol 1995; 69: 414-421
47. Ishida T, Obata Y, Ohara N, Matsushita H, Sato S, Uenaka A, Saika T, Miyamura T, Chayama K, Nakamura Y, Wada H, Yamashita T, Morishima T, Old LJ, Nakayama E. Identification of the HERV-K gag antigen in prostate cancer by SEREX using autologous patient serum and its immunogenicity. Cancer Immun 2008; 8: 15
48. Contreras-Galindo R, Kaplan MH, Leissner P, Verjat T, Ferlenghi I, Bagnoli F, Giusti F, Dosik MH, Hayes DF, Gitlin SD, Markovitz DM. Human endogenous retrovirus K (HML-2) elements in the plasma of people with lymphoma and breast cancer. J Virol 2008; 82: 9329-9336
49. Büscher K, Hahn S, Hofmann M, Trefzer U, Ozel M, Sterry W, Löwer J, Löwer R, Kurth R, Denner J. Expression of the human endogenous retrovirus-K transmembrane envelope, Rec and Np9 proteins in melanomas and melanoma cell lines. Melanoma Res 2006; 16: 223-234
50. Löwer R, Boller K, Hasenmaier B, Korbmacher C, Müller-Lantzsch N, Löwer J, Kurth R. Identification of human endogenous retroviruses with complex mRNA expression and particle formation. Proc Natl Acad Sci USA 1993; 90: 4480-4484
51. Muster T, Waltenberger A, Grassauer A, Hirschl S, Caucig P, Romirer I, Födinger D, Seppele H, Schanab O, Magin-Lachmann C, Löwer R, Jansen B, Pehamberger H, Wolff K. An endogenous retrovirus derived from human melanoma cells. Cancer Res 2003; 63: 8735-8741
52. Morgan D, Brodsky I. Human endogenous retrovirus (HERV-K) particles in megakaryocytes cultured from essential thrombocythemia peripheral blood stem cells. Exp Hematol 2004; 32: 520-525
53. Seifarth W, Skladny H, Krieg-Schneider F, Reichert A, Hehlmann R, Leib-Mösch C. Retrovirus-like particles released from the human breast cancer cell line T47-D display type B-and C-related endogenous retroviral sequences. J Virol 1995; 69: 6408-6416
54. Stocking C, Kozak CA. Murine endogenous retroviruses. Cell Mol Life Sci 2008; 65: 3383-3398
55. Howard G, Eiges R, Gaudet F, Jaenisch R, Eden A. Activation and transposition of endogenous retroviral elements in hypomethylation induced tumors in mice. Oncogene 2008; 27: 404-408
56. Romanish MT, Cohen CJ, Mager DL. Potential mechanisms of endogenous retroviral-mediated genomic instability in human cancer. Semin Cancer Biol 2010; 20: 246-253
57. Sun C, Skaletsky H, Rozen S, Gromoll J, Nieschlag E, Oates R, Page DC. Deletion of azoospermia factor a (AZFa) region of human Y chromosome caused by recombination between HERV15 proviruses. Hum Mol Genet 2000; 9: 2291-2296
58. Lamprecht B, Bonifer C, Mathas S. Repeat-element driven activation of proto-oncogenes in human malignancies. Cell Cycle 2010; 9: 4276-4281
59. Takahashi Y, Harashima N, Kajigaya S, Yokoyama H, Cherkasova E, McCoy JP, Hanada K, Mena O, Kurlander R, Tawab A, Srinivasan R, Lundqvist A, Malinzak E, Geller N, Lerman MI, Childs RW. Regression of human kidney cancer following allogeneic stem cell transplantation is associated with recognition of an HERV-E antigen by T cells. J Clin Invest 2008; 118: 1099-1109
60. Schiavetti F, Thonnard J, Colau D, Boon T, Coulie PG. A human endogenous retroviral sequence encoding an antigen recognized on melanoma by cytolytic T lymphocytes. Cancer Res 2002; 62: 5510-5516
61. Hahn S, Ugurel S, Hanschmann KM, Strobel H, Tondera C, Schadendorf D, Löwer J, Löwer R. Serological response to human endogenous retrovirus K in melanoma patients correlates with survival probability. AIDS Res Hum Retroviruses 2008; 24: 717-723
62. Boller K, Janssen O, Schuldes H, Tönjes RR, Kurth R. Characterization of the antibody response specific for the human endogenous retrovirus HTDV/HERV-K. J Virol 1997; 71: 4581-4588
63. Wang-Johanning F, Radvanyi L, Rycaj K, Plummer JB, Yan P, Sastry KJ, Piyathilake CJ, Hunt KK, Johanning GL. Human endogenous retrovirus K triggers an antigen-specific immune response in breast cancer patients. Cancer Res 2008; 68: 5869-5877
64. Ripberger E, Linnebacher M, Schwitalle Y, Gebert J, von Knebel Doeberitz M. Identification of an HLA-A0201-restricted CTL epitope generated by a tumor-specific frameshift mutation in a coding microsatellite of the OGT gene. J Clin Immunol 2003; 23: 415-423
65. SenGupta D, Tandon R, Vieira RG, Ndhlovu LC, Lown-Hecht R, Ormsby CE, Loh L, Jones RB, Garrison KE, Martin JN, York VA, Spotts G, Reyes-Terán G, Ostrowski MA, Hecht FM, Deeks SG, Nixon DF. Strong human endogenous retrovirus-specific T cell responses are associated with control of HIV-1 in chronic infection. J Virol 2011; 85: 6977-6985
66. Carlini F, Ridolfi B, Molinari A, Parisi C, Bozzuto G, Toccacieli L, Formisano G, De Orsi D, Paradisi S, Grober OM, Ravo M, Weisz A, Arcieri R, Vella S, Gaudi S. The reverse transcription inhibitor abacavir shows anticancer activity in prostate cancer cell lines. PLoS One 2010; 5: e14221
67. Harris RS. Enhancing immunity to HIV through APOBEC. Nat Biotechnol 2008; 26: 1089-1090
68. Argyris EG, Acheampong E, Wang F, Huang J, Chen K, Mukhtar M, Zhang H. The interferon-induced expression of APOBEC3G in human blood-brain barrier exerts a potent intrinsic immunity to block HIV-1 entry to central nervous system. Virology 2007; 367: 440-451
69. Sawyer SL, Wu LI, Emerman M, Malik HS. Positive selection of primate TRIM5alpha identifies a critical speciesspecific retroviral restriction domain. Proc Natl Acad Sci USA 2005; 102: 2832-2837
70. Wang-Johanning F, Rycaj K, Plummer JB, Li M, Yin B, Frerich K, Garza JG, Shen J, Lin K, Yan P, Glynn SA, Dorsey TH, Hunt KK, Ambs S, Johanning GL. Immunotherapeutic potential of anti-human endogenous retrovirus-K envelope protein antibodies in targeting breast tumors. J Natl Cancer Inst 2012; 104: 189-210
71. Sensi M, Anichini A. Unique tumor antigens: evidence for immune control of genome integrity and immunogenic targets for T cell-mediated patient-specific immunotherapy. Clin Cancer Res 2006; 12: 5023-5032
72. Linnebacher M, Gebert J, Rudy W, Woerner S, Yuan YP, Bork P, von Knebel Doeberitz M. Frameshift peptide-derived T-cell epitopes: a source of novel tumor-specific antigens. Int J Cancer 2001; 93: 6-11
73. Mizuuchi M, Hirohashi Y, Torigoe T, Kuroda T, Yasuda K, Shimizu Y, Saito T, Sato N. Novel oligomannose liposome-DNA complex DNA vaccination efficiently evokes anti-HPV E6 and E7 CTL responses. Exp Mol Pathol 2012; 92: 185-190
74. Serafino A, Balestrieri E, Pierimarchi P, Matteucci C, Moroni G, Oricchio E, Rasi G, Mastino A, Spadafora C, Garaci E, Vallebona PS. The activation of human endogenous retrovirus K (HERV-K) is implicated in melanoma cell malignant transformation. Exp Cell Res 2009; 315: 849-862
75. Herbst H, Sauter M, Fuchs H, Kühler-Obbarius C, Löning T, Mueller-Lantzsch N. Gene products of human endogenous retrovirus (HERV)-K in germ cell and trophoblastic tumors. Verh Dtsch Ges Pathol 1997; 81: 464-470
76. de Parseval N, Diop G, Blaise S, Helle F, Vasilescu A, Matsuda F, Heidmann T. Comprehensive search for intra-and inter-specific sequence polymorphisms among coding envelope genes of retroviral origin found in the human genome: genes and pseudogenes. BMC Genomics 2005; 6: 117
77. Mullins CS, Linnebacher M. Endogenous retrovirus sequences as a novel class of tumor-specific antigens: an example of HERV-H env encoding strong CTL epitopes. Cancer Immunol Immunother 2012; 61: 1093-1100
78. Garbe Y, Maletzki C, Linnebacher M. An MSI tumor specific frameshift mutation in a coding microsatellite of MSH3 encodes for HLA-A0201-restricted CD8+ cytotoxic T cell epitopes. PLoS One 2011; 6: e26517
79. Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, Skog J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2011; 2: 180