BK virus and human cancer: Innocent until proven guilty

Seminars in Cancer Biology

Volumn 19, Issue 4, 2009, Pages 252-260

  Abend, Johanna R ^a   Jiang, Mengxi ^a   Imperiale, Michael J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

BK virus; Polyomavirus; Prostate cancer; T antigen

Indexed keywords

CELL DNA; CIDOFOVIR; IMMUNOSUPPRESSIVE AGENT; QUINOLINE DERIVED ANTIINFECTIVE AGENT; VIRUS DNA; VIRUS LARGE T ANTIGEN;

AMINO ACID SEQUENCE; APOPTOSIS; BK VIRUS; CARCINOGENESIS; CARCINOGENICITY; CELL TRANSFORMATION; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; DNA DETERMINATION; DNA REPLICATION; DNA SEQUENCE; HISTOPATHOLOGY; HUMAN; IMMUNE DEFICIENCY; IMMUNOSUPPRESSIVE TREATMENT; MALIGNANT NEOPLASTIC DISEASE; MALIGNANT TRANSFORMATION; NONHUMAN; PHENOTYPE; PROTEIN LOCALIZATION; REVIEW; VIRUS CELL INTERACTION; VIRUS CELL TRANSFORMATION; VIRUS DETECTION; VIRUS INFECTION; VIRUS REACTIVATION; VIRUS REPLICATION; VIRUS TRANSMISSION; VIRUS VIRULENCE;

ANIMALS; BK VIRUS; HUMANS; NEOPLASMS; POLYOMAVIRUS INFECTIONS; TUMOR VIRUS INFECTIONS;

EID: 67349205142     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcancer.2009.02.004     Document Type: Review

References (155)

1. Gardner S.D., Field A.M., Coleman D.V., and Hulme B. New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet 1 7712 (1971) 1253-1257
2. Imperiale M.J. The human polyomaviruses, BKV and JCV: molecular pathogenesis of acute disease and potential role in cancer. Virology 267 1 (2000) 1-7
3. Imperiale M.J. Oncogenic transformation by the human polyomaviruses. Oncogene 20 54 (2001) 7917-7923
4. Tognon M., Corallini A., Martini F., Negrini M., and Barbanti-Brodano G. Oncogenic transformation by BK virus and association with human tumors. Oncogene 22 33 (2003) 5192-5200
5. Rayment I., Baker T.S., Caspar D.L., and Murakami W.T. Polyoma virus capsid structure at 22.5 Å resolution. Nature 295 5845 (1982) 110-115
6. Liddington R.C., Yan Y., Moulai J., Sahli R., Benjamin T.L., and Harrison S.C. Structure of simian virus 40 at 3.8-Å resolution. Nature 354 6351 (1991) 278-284
7. Li T.C., Takeda N., Kato K., Nilsson J., Xing L., Haag L., et al. Characterization of self-assembled virus-like particles of human polyomavirus BK generated by recombinant baculoviruses. Virology 311 1 (2003) 115-124
8. Nilsson J., Miyazaki N., Xing L., Wu B., Hammar L., Li T.C., et al. Structure and assembly of a T = 1 virus-like particle in BK polyomavirus. J Virol 79 9 (2005) 5337-5345
9. Stehle T., Gamblin S.J., Yan Y., and Harrison S.C. The structure of simian virus 40 refined at 3.1 Å resolution. Structure 4 2 (1996) 165-182
10. Cole C.N., and Conzen S.D. Polyomaviridae: the viruses and their replication. In: Knipe D.M., and Howley P.M. (Eds). Fields virology. Fourth ed. vol. 2 (2001), Lippincott Williams & Wilkins, Philadelphia 2141-2174
11. Abend JR, Joseph AE, Das D, Campbell-Cecen DB, Imperiale MJ. A truncated T antigen expressed from an alternatively spliced BK virus early mRNA. J Gen Virol 2009, in press.
12. Low J.A., Magnuson B., Tsai B., and Imperiale M.J. Identification of gangliosides GD1b and GT1b as receptors for BK virus. J Virol 80 3 (2006) 1361-1366
13. Jiang M., Abend J.R., Tsai B., and Imperiale M.J. Early events during BK virus entry and disassembly. J Virol 83 3 (2009) 1350-1358
14. Moriyama T., Marquez J.P., Wakatsuki T., and Sorokin A. Caveolar endocytosis is critical for BK virus infection of human renal proximal tubular epithelial cells. J Virol 81 16 (2007) 8552-8562
15. Moriyama T., and Sorokin A. Intracellular trafficking pathway of BK Virus in human renal proximal tubular epithelial cells. Virology 371 2 (2008) 336-349
16. Waga S., Bauer G., and Stillman B. Reconstitution of complete SV40 DNA replication with purified replication factors. J Biol Chem 269 14 (1994) 10923-10934
17. Knowles W.A. Discovery and epidemiology of the human polyomavirus BK virus (BKV) and JC virus (JCV). Adv Exp Med Biol 577 (2006) 19-45
18. Goudsmit J., Wertheim-van Dillen P., van Strien A., and van der Noordaa J. The role of BK virus in acute respiratory tract disease and the presence of BKV DNA in tonsils. J Med Virol 10 2 (1982) 91-99
19. Bofill-Mas S., Formiga-Cruz M., Clemente-Casares P., Calafell F., and Girones R. Potential transmission of human polyomaviruses through the gastrointestinal tract after exposure to virions or viral DNA. J Virol 75 21 (2001) 10290-10299
20. Bofill-Mas S., Pina S., and Girones R. Documenting the epidemiologic patterns of polyomaviruses in human populations by studying their presence in urban sewage. Appl Environ Microbiol 66 1 (2000) 238-245
21. Hirsch H.H., Steiger J., and Polyomavirus B.K. Lancet Infect Dis 3 10 (2003) 611-623
22. Chesters P.M., Heritage J., and McCance D.J. Persistence of DNA sequences of BK virus and JC virus in normal human tissues and in diseased tissues. J Infect Dis 147 4 (1983) 676-684
23. Heritage J., Chesters P.M., and McCance D.J. The persistence of papovavirus BK DNA sequences in normal human renal tissue. J Med Virol 8 2 (1981) 143-150
24. Nickeleit V., Singh H.K., and Mihatsch M.J. Polyomavirus nephropathy: morphology, pathophysiology, and clinical management. Curr Opin Nephrol Hypertension 12 (2003) 599-605
25. Shinohara T., Matsuda M., Cheng S.H., Marshall J., Fujita M., and Nagashima K. BK virus infection of the human urinary tract. J Med Virol 41 4 (1993) 301-305
26. Doerries K. Human polyomavirus JC and BK persistent infection. Adv Exp Med Biol 577 (2006) 102-116
27. Elsner C., and Dorries K. Evidence of human polyomavirus BK and JC infection in normal brain tissue. Virology 191 1 (1992) 72-80
28. Monini P., Rotola A., Di Luca D., De Lellis L., Chiari E., Corallini A., et al. DNA rearrangements impairing BK virus productive infection in urinary tract tumors. Virology 214 1 (1995) 273-279
29. Martini F., Iaccheri L., Martinelli M., Martinello R., Grandi E., Mollica G., et al. Papilloma and polyoma DNA tumor virus sequences in female genital tumors. Cancer Invest 22 5 (2004) 697-705
30. Chatterjee M., Weyandt T.B., and Frisque R.J. Identification of archetype and rearranged forms of BK virus in leukocytes from healthy individuals. J Med Virol 60 3 (2000) 353-362
31. Pietropaolo V., Fioriti D., Simeone P., Videtta M., Di Taranto C., Arancio A., et al. Detection and sequence analysis of human polyomaviruses DNA from autoptic samples of HIV-1 positive and negative subjects. Int J Immunopathol Pharmacol 16 3 (2003) 269-276
32. Dorries K., Vogel E., Gunther S., and Czub S. Infection of human polyomaviruses JC and BK in peripheral blood leukocytes from immunocompetent individuals. Virology 198 1 (1994) 59-70
33. Chang D., Wang M., Ou W.C., Lee M.S., Ho H.N., and Tsai R.T. Genotypes of human polyomaviruses in urine samples of pregnant women in Taiwan. J Med Virol 48 1 (1996) 95-101
34. Doerries K. Latent and persistent polyomavirus infection. In: Khalili K., and Stoner G.L. (Eds). Human polyomaviruses: molecular and clinical perspectives (2001), Wiley-Liss, New York 197-235
35. Arthur R.R., and Shah K.V. The occurrence and significance of papovaviruses BK and JC in the urine. Prog Med Virol 36 (1989) 42-61
36. Markowitz R.B., Eaton B.A., Kubik M.F., Latorra D., McGregor J.A., and Dynan W.S. BK virus and JC virus shed during pregnancy have predominantly archetypal regulatory regions. J Virol 65 (1991) 4515-4519
37. Jiang M., Abend J.R., Johnson S.F., and Imperiale M.J. The role of polyomaviruses in human disease. Virology 384 2 (2009) 266-273
38. Bressollette-Bodin C., Coste-Burel M., Hourmant M., Sebille V., Andre-Garnier E., and Imbert-Marcille B.M. A prospective longitudinal study of BK virus infection in 104 renal transplant recipients. Am J Transplant 5 8 (2005) 1926-1933
39. Egli A., Binggeli S., Bodaghi S., Dumoulin A., Funk G.A., Khanna N., et al. Cytomegalovirus and polyomavirus BK posttransplant. Nephrol Dial Transplant 22 Suppl. 8 (2007) viii72-viii82
40. Hirsch H.H., Knowles W., Dickenmann M., Passweg J., Klimkait T., Mihatsch M.J., et al. Prospective study of polyomavirus type BK replication and nephropathy in renal-transplant recipients. N Engl J Med 347 7 (2002) 488-496
41. Fogazzi G.B., Cantu M., and Saglimbeni L. 'Decoy cells' in the urine due to polyomavirus BK infection: easily seen by phase-contrast microscopy. Nephrol Dial Transplant 16 7 (2001) 1496-1498
42. Bogdanovic G., Priftakis P., Giraud G., Kuzniar M., Ferraldeschi R., Kokhaei P., et al. Association between a high BK virus load in urine samples of patients with graft-versus-host disease and development of hemorrhagic cystitis after hematopoietic stem cell transplantation. J Clin Microbiol 42 11 (2004) 5394-5396
43. Binet I., Nickeleit V., Hirsch H.H., Prince O., Dalquen P., Gudat F., et al. Polyomavirus disease under new immunosuppressive drugs: a cause of renal graft dysfunction and graft loss. Transplantation 67 6 (1999) 918-922
44. Mengel M., Marwedel M., Radermacher J., Eden G., Schwarz A., Haller H., et al. Incidence of polyomavirus-nephropathy in renal allografts: influence of modern immunosuppressive drugs. Nephrol Dial Transplant 18 6 (2003) 1190-1196
45. Sundsfjord A., Osei A., Rosenqvist H., Van Ghelue M., Silsand Y., Haga H.J., et al. BK and JC viruses in patients with systemic lupus erythematosus: prevalent and persistent BK viruria, sequence stability of the viral regulatory regions, and nondetectable viremia. J Infect Dis 180 1 (1999) 1-9
46. Munoz P., Fogeda M., Bouza E., Verde E., Palomo J., and Banares R. Prevalence of BK virus replication among recipients of solid organ transplants. Clin Infect Dis 41 12 (2005) 1720-1725
47. Rinaldo C.H., and Hirsch H.H. Antivirals for the treatment of polyomavirus BK replication. Expert Rev Anti Infect Ther 5 1 (2007) 105-115
48. Costa J., Howley P.M., Legallais F., Yee C., Young N., and Rabson A.S. Oncogenicity of a nude mouse cell line transformed by a human papovavirus. J Natl Cancer Inst 58 4 (1977) 1147-1149
49. Grossi M.P., Corallini A., Valieri A., Balboni P.G., Poli F., Caputo A., et al. Transformation of hamster kidney cells by fragments of BK virus DNA. J Virol 41 1 (1982) 319-325
50. Grossi M.P., Caputo A., Meneguzzi G., Corallini A., Carra L., Portolani M., et al. Transformation of human embryonic fibroblasts by BK virus, BK virus DNA and a subgenomic BK virus DNA fragment. J Gen Virol 63 2 (1982) 393-403
51. Major E.O., and Di Mayorca G. Malignant transformation of BHK21 clone 13 cells by BK virus-a human papovavirus. Proc Natl Acad Sci U S A 70 11 (1973) 3210-3212
52. Mason Jr. D.H., and Takemoto K.K. Transformation of rabbit kidney cells by BKV(MM) human papovavirus. Int J Cancer 19 3 (1977) 391-395
53. Pagnani M., Corallini A., Caputo A., Altavilla G., Selvatici R., Catozzi L., et al. Co-operation in cell transformation between BK virus and the human c-Harvey-ras oncogene. Int J Cancer 42 3 (1988) 405-413
54. Portolani M., Barbanti-Brodano G., and Placa M.L. Malignant transformation of hamster kidney cells by BK virus. J Virol 15 2 (1975) 420-422
55. Portolani M., and Borgatti M. Stable transformation of mouse, rabbit and monkey cells and abortive transformation of human cells by BK virus, a human papovavirus. J Gen Virol 38 2 (1978) 369-374
56. Seehafer J., Downer D.N., Salmi A., and Colter J.S. Isolation and characterization of BK virus-transformed rat and mouse cells. J Gen Virol 42 3 (1979) 567-578
57. Seehafer J., Salmi A., and Colter J.S. Isolation and characterization of BK virus-transformed hamster cells. Virology 77 1 (1977) 356-366
58. Takemoto K.K., and Martin M.A. Transformation of hamster kidney cells by BK papovavirus DNA. J Virol 17 1 (1975) 247-253
59. Tanaka R., Koprowski H., and Iwasaki Y. Malignant transformation of hamster brain cells in vitro by human papovavirus Bk. J Natl Cancer Inst 56 3 (1976) 671-673
60. van der Noordaa J. Infectivity, oncogenicity and transforming ability of BK virus and BK virus DNA. J Gen Virol 30 3 (1976) 371-373
61. Vasavada R., Eager K.B., Barbanti-Brodano G., Caputo A., and Ricciardi R.P. Adenovirus type 12 early region 1A proteins repress class I HLA expression in transformed human cells. Proc Natl Acad Sci U S A 83 14 (1986) 5257-5261
62. Watanabe S., Kotake S., Nozawa A., Muto T., and Uchida S. Tumorigenicity of human BK papovavirus plaque isolates, wild-type and plaque morphology mutant, in hamsters. Int J Cancer 29 5 (1982) 583-586
63. Corallini A., Tognon M., Negrini M., and Barbanti-Brodano G. Evidence for BK virus as a human tumor virus. In: Khalili K., and Stoner G.L. (Eds). Human polyomaviruses: molecular and clinical perspectives (2001), Wiley-Liss Inc., New York 431-460
64. Barbanti-Brodano G., Sabbioni S., Martini F., Negrini M., Corallini A., and Tognon M. BK virus, JC virus and Simian Virus 40 infection in humans, and association with human tumors. Adv Exp Med Biol 577 (2006) 319-341
65. Harris K.F., Christensen J.B., and Imperiale M.J. BK virus large T antigen: interactions with the retinoblastoma family of tumor suppressor proteins and effects on cellular growth control. J Virol 70 4 (1996) 2378-2386
66. Harris K.F., Christensen J.B., Radany E.H., and Imperiale M.J. Novel mechanisms of E2F induction by BK virus large-T antigen: requirement of both the pRb-binding and the J domains. Mol Cell Biol 18 3 (1998) 1746-1756
67. Rundell K., Major E.O., and Lampert M. Association of cellular 56,000- and 32,000-molecular-weight protein with BK virus and polyoma virus t-antigens. J Virol 37 3 (1981) 1090-1093
68. Sontag E., Fedorov S., Kamibayashi C., Robbins D., Cobb M., and Mumby M. The interaction of SV40 small tumor antigen with protein phosphatase 2A stimulates the map kinase pathway and induces cell proliferation. Cell 75 5 (1993) 887-897
69. Shah K.V., Daniel R.W., Stone K.R., and Elliott A.Y. Investigation of human urogenital tract tumors of papovavirus etiology: brief communication. J Natl Cancer Inst 60 3 (1978) 579-582
70. Grossi M.P., Meneguzzi G., Chenciner N., Corallini A., Poli F., Altavilla G., et al. Lack of association between BK virus and ependymomas, malignant tumors of pancreatic islets, osteosarcomas and other human tumors. Intervirology 15 1 (1981) 10-17
71. Rubinstein R., Schoonakker B.C., and Harley E.H. Recurring theme of changes in the transcriptional control region of BK virus during adaptation to cell culture. J Virol 65 3 (1991) 1600-1604
72. Watanabe S., and Yoshiike K. Change of DNA near the origin of replication enhances the transforming capacity of human papovavirus BK. J Virol 42 3 (1982) 978-985
73. Watanabe S., and Yoshiike K. Decreasing the number of 68-base-pair tandem repeats in the BK virus transcriptional control region reduces plaque size and enhances transforming capacity. J Virol 55 3 (1985) 823-825
74. Zambrano A., Kalantari M., Simoneau A., Jensen J.L., and Villarreal L.P. Detection of human polyomaviruses and papillomaviruses in prostatic tissue reveals the prostate as a habitat for multiple viral infections. The Prostate 53 4 (2002) 263-276
75. De Marzo A.M., Marchi V.L., Epstein J.I., and Nelson W.G. Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. Am J Pathol 155 6 (1999) 1985-1992
76. Shah R., Mucci N.R., Amin A., Macoska J.A., and Rubin M.A. Postatrophic hyperplasia of the prostate gland: neoplastic precursor or innocent bystander?. Am J Pathol 158 5 (2001) 1767-1773
77. Nelson W.G., De Marzo A.M., and Isaacs W.B. Prostate cancer. N Engl J Med 349 4 (2003) 366-381
78. De Marzo A.M., Meeker A.K., Zha S., Luo J., Nakayama M., Platz E.A., et al. Human prostate cancer precursors and pathobiology. Urology 62 5 (2003) 55-62
79. Das D., Wojno K., and Imperiale M.J. BK virus as a cofactor in the etiology of prostate cancer in its early stages. J Virol 82 6 (2008) 2705-2714
80. Das D., Shah R.B., and Imperiale M.J. Detection and expression of human BK virus sequences in neoplastic prostate tissues. Oncogene 23 42 (2004) 7031-7046
81. Foster B.A., Gingrich J.R., Kwon E.D., Madias C., and Greenberg N.M. Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res 57 16 (1997) 3325-3330
82. Ewald D., Li M., Efrat S., Auer G., Wall R.J., Furth P.A., et al. Time-sensitive reversal of hyperplasia in transgenic mice expressing SV40 T antigen. Science 273 5280 (1996) 1384-1386
83. Campo M.S., Moar M.H., Sartirana M.L., Kennedy I.M., and Jarrett W.F. The presence of bovine papillomavirus type 4 DNA is not required for the progression to, or the maintenance of, the malignant state in cancers of the alimentary canal in cattle. EMBO J 4 (1985) 1819-1825
84. Theile M., and Grabowski G. Mutagenic activity of BKV and JCV in human and other mammalian cells. Arch Virol 113 (1990) 221-233
85. Tognon M., Casalone R., Martini F., Mattei M.D., Granata P., Minelli E., et al. Large T antigen coding sequences of two DNA tumor viruses, BK and SV40, and non random chromosome changes in two glioblastoma cell lines. Cancer Genet Cytogenet 90 (1996) 17-23
86. Trabanelli C., Corallini A., Gruppioni R., Sensi A., Bonfatti A., Campioni D., et al. Chromosomal aberrations induced by BK virus T antigen in human fibroblasts. Virology 243 2 (1998) 492-496
87. Russo G., Anzivino E., Fioriti D., Mischitelli M., Bellizzi A., Giordano A., et al. p53 gene mutational rate, Gleason score, and BK virus infection in prostate adenocarcinoma: is there a correlation?. J Med Virol 80 12 (2008) 2100-2107
88. Lau S.K., Lacey S.F., Chen Y.Y., Chen W.G., and Weiss L.M. Low frequency of BK virus in prostatic adenocarcinomas. Apmis 115 6 (2007) 743-749
89. Sfanos K.S., Sauvageot J., Fedor H.L., Dick J.D., De Marzo A.M., and Isaacs W.B. A molecular analysis of prokaryotic and viral DNA sequences in prostate tissue from patients with prostate cancer indicates the presence of multiple and diverse microorganisms. Prostate 68 3 (2008) 306-320
90. Fioriti D., Pietropaolo V., Dal Forno S., Laurenti C., Chiarini F., and Degener A.M. Urothelial bladder carcinoma and viral infections: different association with human polyomaviruses and papillomaviruses. Int J Immunopathol Pharmacol 16 3 (2003) 283-288
91. Geetha D., Tong B.C., Racusen L., Markowitz J.S., and Westra W.H. Bladder carcinoma in a transplant recipient: evidence to implicate the BK human polyomavirus as a causal transforming agent. Transplantation 73 12 (2002) 1933-1936
92. Roberts I.S., Besarani D., Mason P., Turner G., Friend P.J., and Newton R. Polyoma virus infection and urothelial carcinoma of the bladder following renal transplantation. Br J Cancer 99 9 (2008) 1383-1386
93. Monini P., de Lellis L., Rotola A., Di Luca D., Ravaioli T., Bigoni B., et al. Chimeric BK virus DNA episomes in a papillary urothelial bladder carcinoma. Intervirology 38 5 (1995) 304-308
94. Herawi M., Parwani A.V., Chan T., Ali S.Z., and Epstein J.I. Polyoma virus-associated cellular changes in the urine and bladder biopsy samples: a cytohistologic correlation. Am J Surg Pathol 30 3 (2006) 345-350
95. Weinreb D.B., Desman G.T., Amolat-Apiado M.J., Burstein D.E., Godbold Jr. J.H., and Johnson E.M. Polyoma virus infection is a prominent risk factor for bladder carcinoma in immunocompetent individuals. Diagn Cytopathol 34 3 (2006) 201-203
96. Rollison D.E., Sexton W.J., Rodriguez A.R., Kang L.C., Daniel R., and Shah K.V. Lack of BK virus DNA sequences in most transitional-cell carcinomas of the bladder. Int J Cancer 120 6 (2007) 1248-1251
97. Birkeland S.A., Storm H.H., Lamm L.U., Barlow L., Blohme I., Forsberg B., et al. Cancer risk after renal transplantation in the Nordic countries, 1964-1986. Int J Cancer 60 2 (1995) 183-189
98. Buzzeo B.D., Heisey D.M., and Messing E.M. Bladder cancer in renal transplant recipients. Urology 50 4 (1997) 525-528
99. Narayanan M., Szymanski J., Slavcheva E., Rao A., Kelly A., Jones K., et al. BK virus associated renal cell carcinoma: case presentation with optimized PCR and other diagnostic tests. Am J Transplant 7 6 (2007) 1666-1671
100. Kausman J.Y., Somers G.R., Francis D.M., and Jones C.L. Association of renal adenocarcinoma and BK virus nephropathy post transplantation. Pediatr Nephrol 19 4 (2004) 459-462
101. Emerson L.L., Carney H.M., Layfield L.J., and Sherbotie J.R. Collecting duct carcinoma arising in association with BK nephropathy post-transplantation in a pediatric patient. A case report with immunohistochemical and in situ hybridization study. Pediatr Transplant 12 5 (2008) 600-605
102. Knoll A., Stoehr R., Jilg W., and Hartmann A. Low frequency of human polyomavirus BKV and JCV DNA in urothelial carcinomas of the renal pelvis and renal cell carcinomas. Oncol Rep 10 2 (2003) 487-491
103. Lee W., and Langhoff E. Polyomavirus in human cancer development. Adv Exp Med Biol 577 (2006) 310-318
104. Chenciner N., Meneguzzi G., Corallini A., Grossi M.P., Grassi P., Barbanti-Brodano G., et al. Integrated and free viral DNA in hamster tumors induced by BK virus. Proc Natl Acad Sci U S A 77 2 (1980) 975-979
105. Corallini A., Altavilla G., Carra L., Grossi M.P., Federspil G., Caputo A., et al. Oncogenity of BK virus for immunosuppressed hamsters. Arch Virol 73 3-4 (1982) 243-253
106. Corallini A., Altavilla G., Cecchetti M.G., Fabris G., Grossi M.P., Balboni P.G., et al. Ependymomas, malignant tumors of pancreatic islets, and osteosarcomas induced in hamsters by BK virus, a human papovavirus. J Natl Cancer Inst 61 3 (1978) 875-883
107. Corallini A., Barbanti-Brodano G., Bortoloni W., Nenci I., Cassai E., Tampieri M., et al. High incidence of ependymomas induced by BK virus, a human papovavirus: brief communication. J Natl Cancer Inst 59 5 (1977) 1561-1564
108. Uchida S., Watanabe S., Aizawa T., Furuno A., and Muto T. Polyoncogenicity and insulinoma-inducing ability of BK Virus, a human Papovavirus, in Syrian golden hamsters. J Natl Cancer Inst 63 1 (1979) 119-126
109. Fiori M., and Di Mayorca G. Occurrence of BK virus DNA in DNA obtained from certain human tumors. Proc Natl Acad Sci U S A 73 12 (1976) 4662-4666
110. Pater M.M., Pater A., Fiori M., Slota J., and Di Mayorca G. BK virus DNA sequences in human tumors and normal tissues and cell lines. In: Essex M., Todaro G., and Zur Hausen H. (Eds). Viruses in naturally occurring cancers vol. 7 (1980), Cold Spring Harbor Laboratory Press, Cold Spring Harbor 329-341
111. Israel M.A., Martin M.A., Takemoto K.K., Howley P.M., Aaronson S.A., Solomon D., et al. Evaluation of normal and neoplastic human tissue for BK virus. Virology 90 2 (1978) 187-196
112. Wold W.S., Mackey J.K., Brackmann K.H., Takemori N., Rigden P., and Green M. Analysis of human tumors and human malignant cell lines for BK virus-specific DNA sequences. Proc Natl Acad Sci U S A 75 1 (1978) 454-458
113. Dorries K., Loeber G., and Meixensberger J. Association of polyomaviruses JC, SV40, and BK with human brain tumors. Virology 160 1 (1987) 268-270
114. Flaegstad T., Andresen P.A., Johnsen J.I., Asomani S.K., Jorgensen G.E., Vignarajan S., et al. A possible contributory role of BK virus infection in neuroblastoma development. Cancer Res 59 5 (1999) 1160-1163
115. Jorgensen G.E., Johnsen J.I., Ponthan F., Kogner P., Flaegstad T., and Traavik T. Human polyomavirus BK (BKV) and neuroblastoma: mechanisms of oncogenic action and possible strategy for novel treatment. Med Pediatr Oncol 35 6 (2000) 593-596
116. De Mattei M., Martini F., Corallini A., Gerosa M., Scotlandi K., Carinci P., et al. High incidence of BK virus large-T-antigen-coding sequences in normal human tissues and tumors of different histotypes. Int J Cancer 61 6 (1995) 756-760
117. Martini F., Iaccheri L., Lazzarin L., Carinci P., Corallini A., Gerosa M., et al. SV40 early region and large T antigen in human brain tumors, peripheral blood cells, and sperm fluids from healthy individuals. Cancer Res 56 20 (1996) 4820-4825
118. Delbue S., Pagani E., Guerini F.R., Agliardi C., Mancuso R., and Borghi E. Distribution, characterization and significance of polyomavirus genomic sequences in tumors of the brain and its covering. J Med Virol 77 3 (2005) 447-454
119. Arthur R.R., Grossman S.A., Ronnett B.M., Bigner S.H., Vogelstein B., and Shah K.V. Lack of association of human polyomaviruses with human brain tumors. J Neurooncol 20 1 (1994) 55-58
120. Greenlee J.E., Becker L.E., Narayan O., and Johnson R.T. Failure to demonstrate papovavirus tumor antigen in human cerebral neoplasms. Ann Neurol 3 6 (1978) 479-481
121. Weggen S., Bayer T.A., von Deimling A., Reifenberger G., von Schweinitz D., Wiestler O.D., et al. Low frequency of SV40, JC and BK polyomavirus sequences in human medulloblastomas, meningiomas and ependymomas. Brain Pathol 10 1 (2000) 85-92
122. Stolt A., Kjellin M., Sasnauskas K., Luostarinen T., Koskela P., Lehtinen M., et al. Maternal human polyomavirus infection and risk of neuroblastoma in the child. Int J Cancer 113 3 (2005) 393-396
123. Rollison D.E., Utaipat U., Ryschkewitsch C., Hou J., Goldthwaite P., Daniel R., et al. Investigation of human brain tumors for the presence of polyomavirus genome sequences by two independent laboratories. Int J Cancer 113 5 (2005) 769-774
124. Caputo A., Corallini A., Grossi M.P., Carra L., Balboni P.G., Negrini M., et al. Episomal DNA of a BK virus variant in a human insulinoma. J Med Virol 12 1 (1983) 37-49
125. Corallini A., Pagnani M., Viadana P., Silini E., Mottes M., Milanesi G., et al. Association of BK virus with human brain tumors and tumors of pancreatic islets. Int J Cancer 39 1 (1987) 60-67
126. Pagnani M., Negrini M., Reschiglian P., Corallini A., Balboni P.G., Scherneck S., et al. Molecular and biological properties of BK virus-IR, a BK virus variant isolated from a human tumor. J Virol 59 2 (1986) 500-505
127. Calos M.P., and Miller J.H. Transposable elements. Cell 20 3 (1980) 579-595
128. Casini B., Borgese L., Del Nonno F., Galati G., Izzo L., Caputo M., et al. Presence and incidence of DNA sequences of human polyomaviruses BKV and JCV in colorectal tumor tissues. Anticancer Res 25 2A (2005) 1079-1085
129. Hernandez-Losa J., Fedele C.G., Pozo F., Tenorio A., Fernandez V., Castellvi J., et al. Lack of association of polyomavirus and herpesvirus types 6 and 7 in human lymphomas. Cancer 103 2 (2005) 293-298
130. Barzon L., Trevisan M., Masi G., Pacenti M., Sinigaglia A., Macchi V., et al. Detection of polyomaviruses and herpesviruses in human adrenal tumors. Oncogene 27 6 (2008) 857-864
131. Moens U., Subramaniam N., Johansen B., Johansen T., and Traavik T. A steroid hormone response unit in the late leader of the noncoding control region of the human polyomavirus BK confers enhanced host cell permissivity. J Virol 68 4 (1994) 2398-2408
132. Giraud G., Ramqvist T., Ragnarsson-Olding B., and Dalianis T. DNA from BK virus and JC virus and from KI, WU, and MC polyomaviruses as well as from simian virus 40 is not detected in non-UV-light-associated primary malignant melanomas of mucous membranes. J Clin Microbiol 46 11 (2008) 3595-3598
133. Barbanti-Brodano G., Pagnani M., Viadana P., Beth-Giraldo E., Giraldo G., and Corallini A. BK virus DNA in Kaposi's sarcoma. Antibiot Chemother 38 (1987) 113-120
134. Negrini M., Rimessi P., Mantovani C., Sabbioni S., Corallini A., Gerosa M.A., et al. Characterization of BK virus variants rescued from human tumours and tumour cell lines. J Gen Virol 71 Pt 11 (1990) 2731-2736
135. Monini P., Rotola A., de Lellis L., Corallini A., Secchiero P., Albini A., et al. Latent BK virus infection and Kaposi's sarcoma pathogenesis. Int J Cancer 66 6 (1996) 717-722
136. Engels E.A., Rollison D.E., Hartge P., Baris D., Cerhan J.R., Severson R.K., et al. Antibodies to JC and BK viruses among persons with non-Hodgkin lymphoma. Int J Cancer 117 6 (2005) 1013-1019
137. Newton R., Ribeiro T., Alvarez E., Ziegler J., Casabonne D., Carpenter L., et al. BK virus and cancer in Uganda. Eur J Cancer Prev 15 4 (2006) 285-289
138. Newton R., Ribeiro T., Casabonne D., Alvarez E., Touze A., Key T., et al. Antibody levels against BK virus and prostate, kidney and bladder cancers in the EPIC-Oxford cohort. Br J Cancer 93 11 (2005) 1305-1306
139. Lundstig A., Stattin P., Persson K., Sasnauskas K., Viscidi R.P., Gislefoss R.E., et al. No excess risk for colorectal cancer among subjects seropositive for the JC polyomavirus. Int J Cancer 121 5 (2007) 1098-1102
140. Cacciotti P., Libener R., Betta P., Martini F., Porta C., Procopio A., et al. SV40 replication in human mesothelial cells induces HGF/Met receptor activation: a model for viral-related carcinogenesis of human malignant mesothelioma. Proc Natl Acad Sci U S A 98 21 (2001) 12032-12037
141. Cacciotti P., Strizzi L., Vianale G., Iaccheri L., Libener R., Porta C., et al. The presence of simian-virus 40 sequences in mesothelioma and mesothelial cells is associated with high levels of vascular endothelial growth factor. Am J Respir Cell Mol Biol 26 2 (2002) 189-193
142. Catalano A., Romano M., Martinotti S., and Procopio A. Enhanced expression of vascular endothelial growth factor (VEGF) plays a critical role in the tumor progression potential induced by simian virus 40 large T antigen. Oncogene 21 18 (2002) 2896-2900
143. Waheed I., Guo Z.S., Chen G.A., Weiser T.S., Nguyen D.M., and Schrump D.S. Antisense to SV40 early gene region induces growth arrest and apoptosis in T-antigen-positive human pleural mesothelioma cells. Cancer Res 59 24 (1999) 6068-6073
144. Galloway D.A., and McDougall J.K. The oncogenic potential of herpes simplex viruses: evidence for a 'hit-and-run' mechanism. Nature 302 5903 (1983) 21-24
145. Madeley C.R. "Is it the cause?"-Robert Koch and viruses in the 21st century. J Clin Virol 43 1 (2008) 9-12
146. zur Hausen H. Molecular pathogenesis of cancer of the cervix and its causation by specific human papillomavirus types. Curr Top Microbiol Immunol 186 (1994) 131-156
147. zur Hausen H. Viruses in human tumors-reminiscences and perspectives. Adv Cancer Res 68 (1996) 1-22
148. zur Hausen H. Viruses in human cancers. Eur J Cancer 35 14 (1999) 1878-1885
149. zur Hausen H. Oncogenic DNA viruses. Oncogene 20 54 (2001) 7820-7823
150. Barbanti-Brodano G., Martini F., De Mattei M., Lazzarin L., Corallini A., and Tognon M. BK and JC human polyomaviruses and simian virus 40: natural history of infection in humans, experimental oncogenicity, and association with human tumors. Adv Virus Res 50 (1998) 69-99
151. Lednicky J.A., and Butel J.S. Polyomaviruses and human tumors: a brief review of current concepts and interpretations. Front Biosci 4 (1999) D153-D164
152. Kim J.Y., Koralnik I.J., LeFave M., Segal R.A., Pfister L.A., and Pomeroy S.L. Medulloblastomas and primitive neuroectodermal tumors rarely contain polyomavirus DNA sequences. Neuro Oncol 4 3 (2002) 165-170
153. Volter C., Hausen H., Alber D., and de Villiers E.M. Screening human tumor samples with a broad-spectrum polymerase chain reaction method for the detection of polyomaviruses. Virology 237 2 (1997) 389-396
154. Zambrano A., Kalantari M., Simoneau A., Jensen J.L., and Villarreal L.P. Detection of human polyomaviruses and papillomaviruses in prostatic tissue reveals the prostate as a habitat for multiple viral infections. Prostate 53 4 (2002) 263-276
155. Tognon M., Casalone R., Martini F., De Mattei M., Granata P., Minelli E., et al. Large T antigen coding sequences of two DNA tumor viruses, BK and SV40, and nonrandom chromosome changes in two glioblastoma cell lines. Cancer Genet Cytogenet 90 1 (1996) 17-23