Archetype JC virus efficiently propagates in kidney-derived cells stably expressing HIV-1 Tat
Souichi Nukuzuma
Department of Microbiology, Kobe Institute of Health, 4-6, Minatojima-Nakamachi, Chuo-ku, Kobe, Hyogo 650-0046
Search for more papers by this authorCorresponding Author
Masanori Kameoka
Department of Biochemistry
†Present address: Thailand-Japan Research Collaboration Center on Emerging and Re-emerging Infections (RCC-ERI), Research Institute for Microbial Diseases, Osaka University, Nonthaburi 11000, Thailand.
Correspondence Souichi Nukuzuma, Department of Microbiology, Kobe Institute of Health, 4-6, Minatojima-Nakamachi, Chuo-ku, Kobe, Hyogo 650-0046, Japan.Tel: +81 78 302 6256; fax: +81 78 302 0894; email: [email protected]
Search for more papers by this authorShigeki Sugiura
Medical Genetics Research Center, Nara Medical University, Kashihara, Nara 634-8521
Search for more papers by this authorKazuo Nakamichi
Department of Virology 1, National Institute of Infectious Diseases, Toyama, Shinjuku, Tokyo 162-8640
Search for more papers by this authorChiyoko Nukuzuma
Department of Microbiology, Kobe Institute of Health, 4-6, Minatojima-Nakamachi, Chuo-ku, Kobe, Hyogo 650-0046
Search for more papers by this authorIsao Miyoshi
Department of Medicine, Kochi Medical School, Kohasu, Oko-cho, Nankoku, Kochi 783-8505
Search for more papers by this authorTsutomu Takegami
Division of Molecular Oncology and Virology, Medical Research Institute, Kanazawa Medical University, Ishikawa 920-0293, Japan
Search for more papers by this authorSouichi Nukuzuma
Department of Microbiology, Kobe Institute of Health, 4-6, Minatojima-Nakamachi, Chuo-ku, Kobe, Hyogo 650-0046
Search for more papers by this authorCorresponding Author
Masanori Kameoka
Department of Biochemistry
†Present address: Thailand-Japan Research Collaboration Center on Emerging and Re-emerging Infections (RCC-ERI), Research Institute for Microbial Diseases, Osaka University, Nonthaburi 11000, Thailand.
Correspondence Souichi Nukuzuma, Department of Microbiology, Kobe Institute of Health, 4-6, Minatojima-Nakamachi, Chuo-ku, Kobe, Hyogo 650-0046, Japan.Tel: +81 78 302 6256; fax: +81 78 302 0894; email: [email protected]
Search for more papers by this authorShigeki Sugiura
Medical Genetics Research Center, Nara Medical University, Kashihara, Nara 634-8521
Search for more papers by this authorKazuo Nakamichi
Department of Virology 1, National Institute of Infectious Diseases, Toyama, Shinjuku, Tokyo 162-8640
Search for more papers by this authorChiyoko Nukuzuma
Department of Microbiology, Kobe Institute of Health, 4-6, Minatojima-Nakamachi, Chuo-ku, Kobe, Hyogo 650-0046
Search for more papers by this authorIsao Miyoshi
Department of Medicine, Kochi Medical School, Kohasu, Oko-cho, Nankoku, Kochi 783-8505
Search for more papers by this authorTsutomu Takegami
Division of Molecular Oncology and Virology, Medical Research Institute, Kanazawa Medical University, Ishikawa 920-0293, Japan
Search for more papers by this authorABSTRACT
Pathogenic JCV with rearranged regulatory regions (PML-type) causes PML, a demyelinating disease, in the brains of immunocompromised patients. On the other hand, archetype JCV persistently infecting the kidney is thought to be converted to PML-type virus during JCV replication in the infected host under immunosuppressed conditions. In addition, Tat protein, encoded by HIV-1, markedly enhances the expression of a reporter gene under control of the JCV late promoter.
In order to examine the influence of Tat on JCV propagation, we used kidney-derived COS-7 cells, which only permit archetype JCV, and established COS-tat cells, which express HIV-1 Tat stably. We found that the extent of archetype JCV propagation in COS-tat cells is significantly greater than in COS-7 cells. On the other hand, COS-7 cells express SV40 T antigen, which is a strong stimulator of archetype JCV replication. The expression of SV40 T antigen was enhanced by HIV-1 Tat slightly according to real-time RT-PCR, this was not closely related to JCV replication in COS-tat cells. The efficiency of JCV propagation depended on the extent of expression of functional Tat. To our knowledge, this is the first report of increased production of archetype JCV in a culture system using cell lines stably expressing HIV-1 Tat. We propose here that COS-tat cells are a useful tool for studying the role of Tat in archetype JCV replication in the development of PML.
REFERENCES
- 1 Major E.O., Amemiya K., Tornatore C.S., Houff S.A., Berger J.R. (1992) Pathogenesis and molecular biology of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clin Microbiol Rev 5: 49–73.
- 2 Martin J.D., King D.M., Slauch J.M., Frisque R.J. (1985) Differences in regulatory sequences of naturally occurring JC virus variants. J Virol 53: 306–11.
- 3 Yogo Y., Kitamura T., Sugimoto C., Ueki T., Aso Y., Hara K., Taguchi F. (1990) Isolation of a possible archetypal JC virus DNA sequence from nonimmunocompromised individuals. J Virol 64: 3139–43.
- 4 Agostini H.T., Ryschkewitsch C.F., Stoner G.L. (1996) Genotype profile of human polyomavirus JC excreted in urine of immunocompetent individuals. J Clin Microbiol 34: 159–64.
- 5 Guo J., Kitamura T., Ebihara H., Sugimoto C., Kunitake T., Takehisa J., Na, Y,Q., Al-Ahdal M.N., Hallin A., Kawabe K., Taguchi F., Yogo Y. (1996) Geographical distribution of the human polyomavirus JC virus types A and B and isolation of a new type from Ghana. J Gen Virol 77: 919–27.
- 6 Markowitz R.B., Eaton B.A., Kubik M.F., Latorra D., McGregor J.A., Dynan W.S. (1991) BK virus and JC virus shed during pregnancy have predominantly archetypal regulatory regions. J Virol 65: 4515–9.
- 7 Berger J.R., Major E.O. (1999) Progressive multifocal leukoencephalopathy. Semin Neurol 19: 193–200.
- 8 Ault G.S., Stoner G.L. (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: 1499–507.
- 9 Yogo Y., Kitamura T., Sugimoto C., Hara K., Iida T., Taguchi F., Tajima A., Kawabe K., Aso Y. (1991) Sequence rearrangement in JC virus DNAs molecularly cloned from immunosuppressed renal transplant patients. J Virol 65: 2422–28.
- 10 Daniel A.M., Swenson J.J., Mayreddy R.P.R., Khalili K., Frisque R.J. (1996) Sequences within the early and late promoters of archetype JC virus restrict viral DNA replication and infectivity. Virology 216: 90–101.
- 11 Hara K., Sugimoto C., Kitamura T., Aoki N., Taguchi F., Yogo Y. (1998) Archetype JC virus efficiently replicates in COS-7 cells, simian cells constitutively expressing simian virus 40 T antigen. J Virol 72: 5335–42.
- 12 Jones K.A., Peterlin B.M. (1994) Control of RNA initiation and elongation at the HIV-1 promoter. Annu Rev Biochem 63: 717–43.
- 13 Tada H., Rappaport J., Lashgari M., Amini S., Wong-Staal F., Khalili K. (1990) Trans-activation of the JC virus late promoter by theTat protein of type 1 human immunodeficiency virus in glial cells. Proc Natl Acad Sci U S A 87: 3479–83.
- 14 Daniel D.C., Wortman M.J., Schiller R.J., Liu H., Gan L., Mellen J.S., Chang, C-F., Gallia G.L., Rappaport J., Khalili K., Johnson E.M. (2001) Coordinate effects of human immunodeficiency virus type 1 protein Tat and cellular protein Purα on DNA replication initiated at the JC virus origin. J Gen Virol 82: 1543–53.
- 15 Kameoka M., Rong L., Götte M., Liang C., Russell R.S., Wainberg M.A. (2001) Role for human immunodeficiency virus type 1 Tat protein in suppression of viral reverse transcriptase activity during late stages of viral replication. J Virol 75: 2675–2683.
- 16 Kameoka M., Nukuzuma S., Itaya A., Tanaka Y., Ota K., Ikuta K., Yoshihara K. (1999) RNA interference directed against Poly (ADP-ribose) polymerase 1 efficiently suppresses human immunodeficiency virus type 1 replication in human cells. J Virol 78: 8931–34.
- 17 McNees A.L., White Z.S., Zanwar P., Vilchez R.A., Butel J.S. (2005) Specific and quantitative detection of human polyomaviruses BKV, JCV, and SV40 by real time PCR. J Clin Virol 34: 52–62.
- 18 Knowles W.A., Sharp I.R., Efstratiou L., Hand J.F., Gardner S.D. (1991) Preparation of monoclonal antibodies to JC virus and their use in the diagnosis of progressive multifocal leukoencephalopathy. J Med Virol 34: 127–31.
- 19 Padgett B.L., Walker D.L. (1973) Prevalence of antibodies in human sera against JC virus, an isolate from a case of progressive multifocal leukoencephalopathy. J Infect Dis 127: 467–70.
- 20 Nukuzuma S., Nakamichi K., Nukuzuma C., Takegami T. (2009) Inhibitory effect of serotonin antagonists on JC virus propagation in a carrier culture of human neuroblastoma cells. Microbiol Immunol 53: 496–501.
- 21 Kitamura T., Sugimoto C., Kato A., Ebihara H., Suzuki M., Taguchi F., Kawabe K., Yogo Y. (1997) Persistent JC virus (JCV) infection is demonstrated by continuous shedding of the same JCV strain. J Clin Microbiol 35: 1255–57.
- 22 Caputo A., Sodroski J.G., Haseltine W.A. (1990) Constitutive expression of HIV-1 tat protein in human Jurkat T cells using a BK virus vector. J AIDS 3: 372–79.
- 23 Quivy V., Van Lint C. (2002) Diversity of acetylation targets and roles in transcriptional regulation: the human immunodeficiency virus type 1 promoter as a model system. Biochem Pharmacol 64: 925–34.
- 24 Gluzman Y. (1981) SV40-transformed simian cells support the replication of early SV40 mutants. Cell 23: 175–82.
- 25 Feigenbaum L., Khalili K., Major E., Khoury G. (1987) Regulation of the host range of human papovavirus JCV. Proc Natl Acad Sci USA 84: 3695–8.
- 26 Nukuzuma S., Takasaka T., Zheng H.-Y., Zhong S., Chen Q., Kitamura T., Yogo Y. (2006) Subtype I BK polyomavirus strains grow more efficiently in human renal epithelial cells than subtype IV strains. J Gen Virol 87: 1893–901.
- 27 Crum-Cianflone N., Quigley M., Utz G., Hale B. (2007) BK virus-associated renal failure among HIV patients. AIDS 21: 1501–2.
- 28 Sukov W.R., Lewin M., Sethi S., Rakowski T.A., Lager D.J. (2008) BK virus-associated nephropathy in a patient with AIDS. Am J Kidney Dis 51: e15–8.
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