Inhibition of S-phase progression by adenoassociated virus Rep78 protein is mediated by hypophosphorylated pRb

EMBO Journal

Volumn 19, Issue 16, 2000, Pages 4351-4361

  Saudan, Philippe ^a,b   Vlach, Jaromir ^a,b   Beard, Peter ^b  

^a CYTOS BIOTECHNOLOGY AG   (Switzerland)

^b SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

Author keywords

AAV; Cell cycle; pRb; Rep; S phase arrest

Indexed keywords

CYCLIN A; CYCLIN B1; CYCLIN E; HELICASE; PROTEIN P21; RETINOBLASTOMA PROTEIN; VIRUS ENZYME;

ADENO ASSOCIATED VIRUS; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL IMMORTALIZATION; CELL TRANSFORMATION; GROWTH INHIBITION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ADENO-ASSOCIATED VIRUS;

EID: 0034663781     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.16.4351     Document Type: Article

References (68)

1. Kip1. EMRO J., 17, 5987-5997.
2. Bantel-Schaal, U. (1990) Adeno-associated parvoviruses inhibit growth of cells derived from malignant human tumors. Int. J. Cancer, 45, 190-194.
3. Barbeau, D., Charbonneau, R., Whalen, S.G., Bayley, S.T. and Branton, P.E. (1994) Functional interactions within adenovirus E1A protein complexes. Oncogene, 9, 359-373.
4. Bayley, S.T. and Mymryk, J.S. (1994) Adenovirus E1A proteins and transformation. Int. J. Oncol., 5, 425-144.
5. Beaton, A., Palumbo, P. and Berns, K.I. (1989) Expression from the adeno-associated virus p5 and p19 promoters is negatively regulated in trans by the rep protein. J. Virol., 63, 4450-4454.
6. Berns, K.I. and Linden, R.M. (1995) The cryptic life style of adeno-associated virus. BioEssays, 17, 237-245.
7. Chejanovsky, N. and Carter, B.J. (1989) Replication of a human parvovirus nonsense mutant in mammalian cells containing an inducible amber suppressor. Virology, 171, 239-247.
8. Chew, Y.P., Ellis, M., Wilkie, S. and Mittnacht, S. (1998) pRB phosphorylation mutants reveal role of pRB in regulating S-phase completion by a mechanism independent of E2F. Oncogene, 17, 2177-2186.
9. Chiorini, J.A., Zimmermann, B., Yang, L., Smith, R.H., Ahearn, A., Herberg, F. and Kotin, R.M. (1998) Inhibition of PrKX, a novel protein kinase and the cyclic AMP-dependent protein kinase PKA by the regulatory proteins of adeno-associated virus type 2. Mol. Cell. Biol., 18, 5921-5929.
10. Di Pasquale, G. and Stacey, S.N. (1998) Adeno-associated virus Rep78 protein interacts with protein kinase A and its homolog PRKX and inhibits CREB-dependent transcriptional activation. J. Virol., 72, 7916-7925.
11. Draetta, G., Luca, F., Westendorf, J., Brizuela, L., Ruderman, J. and Beach, D. (1989) Cdc2 protein kinase is complexed with both cyclin A and B: evidence for proteolytic inactivation of MPF. Cell. 56, 829-838.
12. 1 arrest. Cell, 76, 1013-1023.
13. Ferrari, F.K., Samulski, T., Shenk, T. and Samulski, R.J. (1996) Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J. Virol., 70, 3227-3234.
14. Grana, X., Garriga, J. and Mayol, X. (1998) Role of the retinoblastoma protein family, pRB, p107 and p130 in the negative control of cell growth. Oncogene, 17, 3365-3383.
15. Grifman, M., Chen, N.N., Gao, G.P., Cathomen, T., Wilson, J.M. and Weitzman, M.D. (1999) Overexpression of cyclin A inhibits augmentation of recombinant adeno-associated virus transduction by the adenovirus E4orf6 protein. J. Virol., 73, 10010-10019.
16. Harper, J. and Elledge, S. (1996) Cdk inhibitors in development and cancer. Curr. Opin. Genet. Dev., 6, 56-64.
17. Harper, J.W. et al. (1995) Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell, 6, 387-400.
18. Helin, K. (1998) Regulation of cell proliferation by the E2F transcription factors. Curr. Opin. Genet. Dev., 8, 28-35.
19. Hermanns, J., Schulze, A., Jansen-D̈rr, P., Kleinschmidt, J.A., Schmidt, R. and zur Hausen, H. (1997) Infection of primary cells by adeno-associated virus type 2 results in a modulation of cell cycle-regulating proteins. J. Virol., 71, 6020-6027.
20. Hermonat, P.L. (1989) The adeno-associated virus Rep78 gene inhibits cellular transformation induced by bovine papillomavirus. Virology, 172, 253-261.
21. Hermonat, P.L. (1991) Inhibition of H-ras expression by the adeno-associated virus Rep78 transformation suppressor gene product. Cancer Res., 51, 3373-3377.
22. Hermonat, P.L. (1992) Inhibition of bovine papillomavirus plasmid DNA replication by adeno-associated virus. Virology, 189, 329-333.
23. Hermonat, P.L. (1994) Down-regulation of the human c-fos and c-myc proto-oncogene promoters by adeno-associated virus Rep78. Cancer Lett., 81, 129-136.
24. Hörer, M., Weger, S., Butz, K., Hoppe-Seyler, F., Geisen, C. and Kleinschmidt, J.A. (1995) Mutational analysis of adeno-associated virus Rep protein-mediated inhibition of heterologous and homologous promoters. J. Virol., 69, 5485-5496.
25. Im, D.S. and Muzyczka, N. (1990) The AAV origin binding protein Rep68 is an ATP-dependent site-specific endonuclease with DNA helicase activity. Cell, 61, 447-457.
26. Kastan, M.B., Onyekwere, O., Sidransky, D., Vogelstein, B. and Craig, R.W. (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res., 51, 6304-6311.
27. Khleif, S.N., Myers, T., Carter, B.J. and Trempe, J.P. (1991) Inhibition of cellular transformation by the adeno-associated virus rep gene. Virology, 181, 738-741.
28. Klein-Bauemschmitt, P., zur Hausen, H. and Schlehofer, J.R. (1992) Induction of differentiation-associated changes in established human cells by infection with adeno-associated virus type 2. J. Virol., 66, 4191-4200.
29. 1/S transition and S-phase progression. Genes Dev., 12, 2278-2292.
30. Kotin, R.M. et al. (1990) Site-specific integration by adeno-associated virus. Proc. Natl Acad. Sci. USA, 87, 2211-2215.
31. Krtolica, A., Krucher, N.A. and Ludlow, J.W. (1998) Hypoxia-induced pRB hypophosphorylation results from downregulation of CDK and upregulation of PP1 activities. Oncogene, 17, 2295-2304.
32. Kube, D.M., Ponnazhagan, S. and Srivastava, A. (1997) Encapsidation of adeno-associated virus type 2 Rep proteins in wild-type and recombinant progeny virions: Rep-mediated growth inhibition of primary human cells. J. Virol., 71, 7361-7371.
33. Labow, M.A., Graf, L.H., Jr and Berns, K.I. (1987) Adeno-associated virus gene expression inhibits cellular transformation by heterologous genes. Mol. Cell Biol., 7, 1320-1325.
34. Laughlin, C.A., Tratschin, J.D., Coon, H. and Carter, B.J. (1983) Cloning of infectious adeno-associated virus genomes in bacterial plasmids. J. Virol., 48, 79-87.
35. Lukas, C., Sorensen, C.S., Kramer, E., Santoni-Rugiu, E., Lindeneg, C., Peters, J.M., Bartek, J. and Lukas, J. (1999) Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex. Nature, 401, 815-818.
36. 1 arrest: molecular mechanisms and implications for oncogenesis. Oncogene, 18, 3930-3935.
37. Mittnacht, S. (1998) Control of pRB phosphorylation. Curr. Opin. Genet. Dev., 8, 21-27.
38. Moran, E. (1993) DNA tumor virus transforming proteins and the cell cycle. Curr. Opin. Genet. Dev., 3, 63-70.
39. Morgan, D.O. (1997) Cyclin-dependent kinases: engines, clocks and microprocessors. Annu. Rev. Cell. Dev. Biol., 13, 261-291.
40. Morgenstern, J.P. and Land, H. (1990) Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res., 18, 3587-3596.
41. 2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol. Cell. Biol., 18, 629-643.
42. Ohtani, K., DeGregori, J. and Nevins, J.R. (1995) Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl Acad. Sci. USA, 92, 12146-12150.
43. Op De Beeck, A. and Caillet-Fauquet, P. (1997) The NSI protein of the autonomous parvovirus minute virus of mice blocks cellular DNA replication: a consequence of lesions to the chromatin? J. Virol., 71, 5323-5329.
44. Ostrove, J.M., Duckworth, D.H. and Berns, K.I. (1981) Inhibition of adenovirus-transformed cell oncogenicity by adeno-associated virus. Virology, 113, 521-533.
45. 1 events and regulation of cell proliferation. Science, 246, 603-608.
46. Pear, W.S., Scott, M.L. and Nolan, G.P. (1996) Generation of high titre, helper-free retroviruses by transient transfection. In Robbins, P. (ed.), Methods in Molecular Medicine: Gene Therapy Protocols. Humana Press, Totowa, NJ, pp. 41-57.
47. Pereira, D.J., McCarty, D.M. and Muzyczka, N. (1997) The adeno-associated virus (AAV) Rep protein acts as both a repressor and an activator to regulate AAV transcription during a productive infection. J. Virol., 71, 1079-1088.
48. Rommelaere, J. and Cornelis, J.J. (1991) Antineoplastic activity of parvoviruses. J. Virol. Methods, 33, 233-251.
49. Ruas, M. and Peters, G. (1998) The p16INK4a/CDKN2A tumor suppressor and its relatives. Biochim. Biophys. Acta, 1378, F115-F177.
50. Rubin, E., Tamrakar, S. and Ludlow, J.W. (1998) Protein phosphatase type 1, the product of the retinoblastoma susceptibility gene and cell cycle control. Front. Biosci., 3, D1209-1219.
51. Sanchez, Y., Wong, C., Thoma, R.S., Richman, R., Wu, Z., Piwnica-Worms, H. and Elledge, S.J. (1997) Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science, 277, 1497-1501.
52. Schlehofer, J.R. (1994) The tumor suppressive properties of adeno-associated viruses. Mutat. Res., 305, 303-313.
53. 1 cyclin-dependent kinases. Genes Dev., 9, 1149-1163.
54. Smith, R.H. and Kotin, R.M. (1998) The Rep52 gene product of adeno-associated virus is a DNA helicase with 3′-to-5′ polarity. J. Virol., 72, 4874-4881.
55. Smith, R.H., Spano, A.J. and Kotin, R.M. (1997) The Rep78 gene product of adeno-associated virus (AAV) self-associates to form a hexameric complex in the presence of AAV ori sequences. J. Virol., 71, 4461-4471.
56. Srivastava, A., Lusby, E.W. and Berns, K.I. (1983) Nucleotide sequence and organization of the adeno-associated virus 2 genome. J. Virol., 45, 555-564.
57. Tlysty, T.D., Briot, A. and Poulose, B. (1995) Analysis of cell cycle checkpoint status in mammalian cells. Methods Enzymol., 254, 125-133.
58. Kip1 is abrogated by c-Myc. EMBO J., 15, 6595-6604.
59. Voorhoeve, P.M., Watson, R.J., Farlie, P.G., Bernards, R. and Lam, E.W. (1999) Rapid dephosphorylation of p107 following UV irradiation. Oncogene, 18, 679-688.
60. Weinberg, R.A. (1995) The retinoblastoma protein and cell cycle control. Cell, 81, 323-330.
61. Weitzman, M.D., Kyöstiö, S.R., Kotin, R.M. and Owens, R.A. (1994) Adeno-associated virus (AAV) Rep proteins mediate complex formation between AAV DNA and its integration site in human DNA. Proc. Natl Acad. Sci. USA, 91, 5808-5812.
62. Winocour, E., Callaham, M.F. and Huberman, E. (1988) Perturbation of the cell cycle by adeno-associated virus. Virology, 167, 393-399.
63. Wonderling, R.S., Kyöstiö, S.R. and Owens, R.A. (1995) A maltose-binding protein/adeno-associated virus Rep68 fusion protein has DNA-RNA helicase and ATPase activities. J. Virol, 69, 3542-3548.
64. Xiong, Y., Hannon, G.J., Zhang, H., Casso, D., Kobayashi, R. and Beach, D. (1993) p21 is a universal inhibitor of cyclin kinases. Nature, 366, 701-704.
65. Yakinoglu, A.O., Heilbronn, R., Burkle, A., Schlehofer, J.R. and zur Hausen, H. (1988) DNA amplification of adeno-associated virus as a response to cellular genotoxic stress. Cancer Res., 48, 3123-3129.
66. Yang, Q., Chen, F. and Trempe, J.P. (1994) Characterization of cell lines that inducibly express the adeno-associated virus Rep proteins. J. Virol., 68, 4847-4856.
67. Yang, Q., Chen, F., Ross, J. and Trempe, J.P. (1995) Inhibition of cellular and SV40 DNA replication by the adeno-associated virus Rep proteins. Virology, 207, 246-250.
68. Zetterberg, A., Larsson, O. and Wiman, K.G. (1995) What is the restriction point? Curr. Opin. Cell Biol, 7, 835-842.