Rearranged JC virus noncoding control regions found in progressive multifocal leukoencephalopathy patient samples increase virus early gene expression and replication rate

Journal of Virology

Volumn 84, Issue 20, 2010, Pages 10448-10456

  Gosert, Rainer ^a   Kardas, Piotr ^a   Major, Eugene O ^b   Hirsch, Hans H ^a,c  

^a UNIVERSITY OF BASEL   (Switzerland)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSACTIVATOR PROTEIN; VIRUS LARGE T ANTIGEN;

ADULT; ANTIGEN EXPRESSION; ARTICLE; ASTROCYTE; CEREBROSPINAL FLUID; CLINICAL ARTICLE; FEMALE; GENE EXPRESSION; GENE INSERTION; GLIA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; JC VIRUS; LEUKOENCEPHALOPATHY; MALE; PRIORITY JOURNAL; VIRUS REPLICATION;

ADULT; ANIMALS; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; COS CELLS; DNA PRIMERS; DNA, VIRAL; FEMALE; GENE EXPRESSION; GENE REARRANGEMENT; GENES, REPORTER; GENES, VIRAL; HUMANS; JC VIRUS; LEUKOENCEPHALOPATHY, PROGRESSIVE MULTIFOCAL; MALE; MIDDLE AGED; TRANSFECTION; VIRUS REPLICATION;

JC POLYOMAVIRUS; POLYOMAVIRUS; SIMIAN VIRUS 40;

EID: 77957195722     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00614-10     Document Type: Article

References (60)

1. Agostini, H. T., C. F. Ryschkewitsch, E. J. Singer, and G. L. Stoner. 1997. JC virus regulatory region rearrangements and genotypes in progressive multifocal leukoencephalopathy: two independent aspects of virus variation. J. Gen. Virol. 78:659-664.
2. Albrecht, H., C. Hoffmann, O. Degen, A. Stoehr, A. Plettenberg, T. Mertenskotter, C. Eggers, and H. J. Stellbrink. 1998. Highly active antiretroviral therapy significantly improves the prognosis of patients with HIV-associated progressive multifocal leukoencephalopathy. AIDS 12:1149-1154.
3. Astrom, K. E., E. L. Mancall, and E. P. Richardson, Jr. 1958. Progressive multifocal leuko-encephalopathy; a hitherto unrecognized complication of chronic lymphatic leukaemia and Hodgkin's disease. Brain 81:93-111.
4. Ault, G. S., and G. L. Stoner. 1993. Human polyomavirus JC promoter/enhancer rearrangement patterns from progressive multifocal leukoencephalopathy brain are unique derivatives of a single archetypal structure. J. Gen. Virol. 74:1499-1507.
5. Berger, J. R., B. Kaszovitz, M. J. Post, and G. Dickinson. 1987. Progressive multifocal leukoencephalopathy associated with human immunodeficiency virus infection. A review of the literature with a report of sixteen cases. Ann. Intern. Med. 107:78-87.
6. Boldorini, R., E. Omodeo-Zorini, M. Nebuloni, E. Benigni, L. Vago, A. Ferri, and G. Monga. 2003. Lytic JC virus infection in the kidneys of AIDS subjects. Mod. Pathol. 16:35-42.
7. Bossolasco, S., G. Calori, F. Moretti, A. Boschini, D. Bertelli, M. Mena, S. Gerevini, A. Bestetti, R. Pedale, S. Sala, S. Sala, A. Lazzarin, and P. Cinque. 2005. Prognostic significance of JC virus DNA levels in cerebrospinal fluid of patients with HIV-associated progressive multifocal leukoencephalopathy. Clin. Infect. Dis. 40:738-744.
8. Cinque, P., I. J. Koralnik, and D. B. Clifford. 2003. The evolving face of human immunodeficiency virus-related progressive multifocal leukoencephalopathy: defining a consensus terminology. J. Neurovirol 9(Suppl. 1):88-92.
9. Cinque, P., C. Pierotti, M. G. Vigano, A. Bestetti, C. Fausti, D. Bertelli, and A. Lazzarin. 2001. The good and evil of HAART in HIV-related progressive multifocal leukoencephalopathy. J. Neurovirol. 7:358-363. (Pubitemid 32894242)
10. Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16:10881-10890.
11. Daniel, A. M., J. J. Swenson, R. P. Mayreddy, K. Khalili, and R. J. Frisque. 1996. Sequences within the early and late promoters of archetype JC virus restrict viral DNA replication and infectivity. Virology 216:90-101.
12. Delbue, S., G. Sotgiu, D. Fumagalli, M. Valli, E. Borghi, R. Mancuso, E. Marchioni, R. Maserati, and P. Ferrante. 2005. A case of a progressive multifocal leukoencephalopathy patient with four different JC virus transcriptional control region rearrangements in cerebrospinal fluid, blood, serum, and urine. J. Neurovirol. 11:51-57.
13. De Luca, A., A. Ammassari, P. Pezzotti, P. Cinque, J. Gasnault, J. Berenguer, S. Di Giambenedetto, A. Cingolani, Y. Taoufik, P. Miralles, C. M. Marra, and A. Antinori. 2008. Cidofovir in addition to antiretroviral treatment is not effective for AIDS-associated progressive multifocal leukoencephalopathy: a multicohort analysis. AIDS 22:1759-1767.
14. Drachenberg, C. B., H. H. Hirsch, J. C. Papadimitriou, R. Gosert, R. K. Wali, R. Munivenkatappa, J. Nogueira, C. B. Cangro, A. Haririan, S. Mendley, and E. Ramos. 2007. Polyomavirus BK versus JC replication and nephropathy in renal transplant recipients: a prospective evaluation. Transplantation 84:323-330.
15. Du Pasquier, R. A., P. Autissier, Y. Zheng, J. Jean-Jacques, and I. J. Koralnik. 2005. Presence of JC virus-specific CTL in the cerebrospinal fluid of PML patients: rationale for immune-based therapeutic strategies. AIDS 19:2069-2076.
16. Du Pasquier, R. A., and I. J. Koralnik. 2003. Inflammatory reaction in progressive multifocal leukoencephalopathy: harmful or beneficial? J. Neurovirol. 9(Suppl. 1):25-31.
17. Du Pasquier, R. A., M. J. Kuroda, Y. Zheng, J. Jean-Jacques, N. L. Letvin, and I. J. Koralnik. 2004. A prospective study demonstrates an association between JC virus-specific cytotoxic T lymphocytes and the early control of progressive multifocal leukoencephalopathy. Brain 127:1970-1978.
18. Du Pasquier, R. A., J. E. Schmitz, J. Jean-Jacques, Y. Zheng, J. Gordon, K. Khalili, N. L. Letvin, and I. J. Koralnik. 2004. Detection of JC virus-specific cytotoxic T lymphocytes in healthy individuals. J. Virol. 78:10206-10210.
19. Du Pasquier, R. A., M. C. Stein, M. A. Lima, X. Dang, J. Jean-Jacques, Y. Zheng, N. L. Letvin, and I. J. Koralnik. 2006. JC virus induces a vigorous CD8+ cytotoxic T cell response in multiple sclerosis patients. J. Neuroimmunol. 176:181-186.
20. Egli, A., L. Infanti, A. Dumoulin, A. Buser, J. Samaridis, C. Stebler, R. Gosert, and H. H. Hirsch. 2009. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J. Infect. Dis. 199:837-846.
21. Frisque, R. J., G. L. Bream, and M. T. Cannella. 1984. Human polyomavirus JC virus genome. J. Virol. 51:458-469.
22. Funk, G. A., R. Gosert, P. Comoli, F. Ginevri, and H. H. Hirsch. 2008. Polyomavirus BK replication dynamics in vivo and in silico to predict cytopathology and viral clearance in kidney transplants. Am. J. Transplant. 8:2368-2377.
23. Giudici, B., B. Vaz, S. Bossolasco, S. Casari, A. M. Brambilla, W. Luke, A. Lazzarin, T. Weber, and P. Cinque. 2000. Highly active antiretroviral therapy and progressive multifocal leukoencephalopathy: effects on cerebrospinal fluid markers of JC virus replication and immune response. Clin. Infect. Dis. 30:95-99.
24. Gosert, R., C. H. Rinaldo, G. A. Funk, A. Egli, E. Ramos, C. B. Drachenberg, and H. H. Hirsch. 2008. Polyomavirus BK with rearranged noncoding control region emerge in vivo in renal transplant patients and increase viral replication and cytopathology. J. Exp. Med. 205:841-852.
25. Hirsch, H. H., G. Kaufmann, P. Sendi, and M. Battegay. 2004. Immune reconstitution in HIV-infected patients. Clin. Infect. Dis. 38:1159-1166.
26. Hirsch, H. H., P. R. Meylan, W. Zimmerli, A. Iten, M. Battegay, and P. Erb. 1998. HIV-1-infected patients with focal neurologic signs: diagnostic role of PCR for Toxoplasma gondii, Epstein-Barr virus, and JC virus. Clin. Microbiol. Infect. 4:577-584.
27. Hirsch, H. H., and J. Steiger. 2003. Polyomavirus BK. Lancet Infect. Dis. 3:611-623.
28. Horton, R. M., H. D. Hunt, S. N. Ho, J. K. Pullen, and L. R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
29. Hou, J., and E. Major. 2005. Management of infections by the human polyomavirus JC: past, present and future. Expert Rev. Anti-Infect. Ther. 3:629-640.
30. Houff, S. A., E. O. Major, D. A. Katz, C. V. Kufta, J. L. Sever, S. Pittaluga, J. R. Roberts, J. Gitt, N. Saini, and W. Lux. 1988. Involvement of JC virus-infected mononuclear cells from the bone marrow and spleen in the pathogenesis of progressive multifocal leukoencephalopathy. N. Engl. J. Med. 318:301-305.
31. Imperiale, M. J., and E. O. Major. 2007. Polyomaviruses, p. 2263-2298. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
32. Jilek, S., E. Jaquiery, H. H. Hirsch, A. Lysandropoulos, M. Canales, L. Guignard, M. Schluep, G. Pantaleo, and R. A. Du Pasquier. 2010. Immune responses to JC virus in patients with multiple sclerosis treated with natalizumab: a cross-sectional and longitudinal study. Lancet Neurol. 9:264-272.
33. Kazory, A., D. Ducloux, J. M. Chalopin, R. Angonin, B. Fontaniere, and H. Moret. 2003. The first case of JC virus allograft nephropathy. Transplantation 76:1653-1655.
34. Khanna, N., L. Elzi, N. J. Mueller, C. Garzoni, M. Cavassini, C. A. Fux, P. Vernazza, E. Bernasconi, M. Battegay, H. H. Hirsch, et al. 2009. Incidence and outcome of progressive multifocal leukoencephalopathy in 20 years of the Swiss HIV cohort study. Clin. Infect. Dis. 48:1459-1466.
35. Khanna, N., M. Wolbers, N. J. Mueller, C. Garzoni, R. A. Du Pasquier, C. A. Fux, P. Vernazza, E. Bernasconi, R. Viscidi, M. Battegay, and H. H. Hirsch. 2009. JC virus-specific immune responses in human immunodeficiency virus type 1 patients with progressive multifocal leukoencephalopathy. J. Virol. 83:4404-4411.
36. Klimkait, T., F. Stauffer, E. Lupo, and C. Sonderegger-Rubli. 1998. Dissecting the mode of action of various HIV-inhibitor classes in a stable cellular system. Arch. Virol. 143:2109-2131.
37. Koralnik, I. J., R. A. Du Pasquier, and N. L. Letvin. 2001. JC virus-specific cytotoxic T lymphocytes in individuals with progressive multifocal leukoencephalopathy. J. Virol. 75:3483-3487.
38. Lindå, H., A. von Heijne, E. O. Major, C. Ryschkewitsch, J. Berg, T. Olsson, and C. Martin. 2009. Progressive multifocal leukoencephalopathy after natalizumab monotherapy. N. Engl. J. Med. 361:1081-1087.
39. Loeber, G., and K. Dorries. 1988. DNA rearrangements in organ-specific variants of polyomavirus JC strain GS. J. Virol. 62:1730-1735.
40. Major, E. O. 2009. Reemergence of PML in natalizumab-treated patients-new cases, same concerns. N. Engl. J. Med. 361:1041-1043.
41. Martin, J. D., D. M. King, J. M. Slauch, and R. J. Frisque. 1985. Differences in regulatory sequences of naturally occurring JC virus variants. J. Virol. 53:306-311.
42. Messam, C. A., J. Hou, R. M. Gronostajski, and E. O. Major. 2003. Lineage pathway of human brain progenitor cells identified by JC virus susceptibility. Ann. Neurol. 53:636-646.
43. Newman, J. T., and R. J. Frisque. 1997. Detection of archetype and rearranged variants of JC virus in multiple tissues from a pediatric PML patient. J. Med. Virol. 52:243-252.
44. Padgett, B. L., D. L. Walker, G. M. ZuRhein, R. J. Eckroade, and B. H. Dessel. 1971. Cultivation of papova-like virus from human brain with progressive multifocal leukoencephalopathy. Lancet i:1257-1260.
45. Rinaldo, C. H., T. Traavik, and A. Hey. 1998. The agnogene of the human polyomavirus BK is expressed. J. Virol. 72:6233-6236.
46. Safdar, A., R. J. Rubocki, J. A. Horvath, K. K. Narayan, and R. L. Waldron. 2002. Fatal immune restoration disease in human immunodeficiency virus type 1-infected patients with progressive multifocal leukoencephalopathy: impact of antiretroviral therapy-associated immune reconstitution. Clin. Infect. Dis. 35:1250-1257.
47. Stettner, M. R., J. A. Nance, C. A. Wright, Y. Kinoshita, W. K. Kim, S. Morgello, J. Rappaport, K. Khalili, J. Gordon, and E. M. Johnson. 2009. SMAD proteins of oligodendroglial cells regulate transcription of JC virus early and late genes coordinately with the Tat protein of human immunodeficiency virus type 1. J. Gen. Virol. 90:2005-2014.
48. Sugimoto, C., M. Hasegawa, A. Kato, H. Y. Zheng, H. Ebihara, F. Taguchi, T. Kitamura, and Y. Yogo. 2002. Evolution of human polyomavirus JC: implications for the population history of humans. J. Mol. Evol. 54:285-297.
49. Sugimoto, C., D. Ito, K. Tanaka, H. Matsuda, H. Saito, H. Sakai, K. Fujihara, Y. Itoyama, T. Yamada, J. Kira, R. Matsumoto, M. Mori, K. Nagashima, and Y. Yogo. 1998. Amplification of JC virus regulatory DNA sequences from cerebrospinal fluid: diagnostic value for progressive multifocal leukoencephalopathy. Arch. Virol. 143:249-262.
50. Tada, H., J. Rappaport, M. Lashgari, S. Amini, F. Wong-Staal, and K. Khalili. 1990. Trans-activation of the JC virus late promoter by the tat protein of type 1 human immunodeficiency virus in glial cells. Proc. Natl. Acad. Sci. U. S. A. 87:3479-3483.
51. Vacante, D. A., R. Traub, and E. O. Major. 1989. Extension of JC virus host range to monkey cells by insertion of a simian virus 40 enhancer into the JC virus regulatory region. Virology 170:353-361.
52. Van Assche, G., M. Van Ranst, R. Sciot, B. Dubois, S. Vermeire, M. Noman, J. Verbeeck, K. Geboes, W. Robberecht, and P. Rutgeerts. 2005. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease. N. Engl. J. Med. 353:362-368.
53. Yasuda, Y., H. Yabe, H. Inoue, T. Shimizu, M. Yabe, Y. Yogo, and S. Kato. 2003. Comparison of PCR-amplified JC virus control region sequences from multiple brain regions in PML. Neurology 61:1617-1619.
54. Yogo, Y., J. Guo, T. Iida, K. Satoh, F. Taguchi, H. Takahashi, W. W. Hall, and K. Nagashima. 1994. Occurrence of multiple JC virus variants with distinctive regulatory sequences in the brain of a single patient with progressive multifocal leukoencephalopathy. Virus Genes 8:99-105.
55. Yogo, Y., T. Kitamura, C. Sugimoto, T. Ueki, Y. Aso, K. Hara, and F. Taguchi. 1990. Isolation of a possible archetypal JC virus DNA sequence from nonimmunocompromised individuals. J. Virol. 64:3139-3143. (Pubitemid 20171319)
56. Yogo, Y., T. Matsushima-Ohno, T. Hayashi, C. Sugimoto, M. Sakurai, and I. Kanazawa. 2001. JC virus regulatory region rearrangements in the brain of a long surviving patient with progressive multifocal leukoencephalopathy. J. Neurol. Neurosurg. Psychiatry 71:397-400.
57. Yogo, Y., S. Zhong, A. Shibuya, T. Kitamura, and Y. Homma. 2008. Transcriptional control region rearrangements associated with the evolution of JC polyomavirus. Virology 380:118-123.
58. Yoshiike, K., and K. K. Takemoto. 1986. Studies with BK virus and monkey lymphotropic papovavirus, p. 295-326. In N. P. Salzman (ed.), The Polyomaviridae, vol. 1. Plenum Press, New York, NY.
59. Zheng, H. Y., Y. Yasuda, S. Kato, T. Kitamura, and Y. Yogo. 2004. Stability of JC virus coding sequences in a case of progressive multifocal leukoencephalopathy in which the viral control region was rearranged markedly. Arch. Pathol. Lab. Med. 128:275-278.
60. Zurhein, G., and S. M. Chou. 1965. Particles resembling papova viruses in human cerebral demyelinating disease. Science 148:1477-1479.