Infection of primary cells by adeno-associated virus type 2 results in a modulation of cell cycle-regulating proteins

Journal of Virology

Volumn 71, Issue 8, 1997, Pages 6020-6027

  Hermanns, J ^a   Schulze, A ^a   Jansen Durr P ^a   Kleinschmidt, J A ^a   Schmidt, R ^a   Zur Hausen, H ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN B; CYCLIN D1; CYCLIN DEPENDENT KINASE; CYCLIN E; PROTEIN P21; TRANSCRIPTION FACTOR E2F;

ADENO ASSOCIATED VIRUS; ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; DOWN REGULATION; FIBROBLAST; GENE EXPRESSION REGULATION; GROWTH DISORDER; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIRUS INFECTION;

EID: 0030797433     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.8.6020-6027.1997     Document Type: Article

References (90)

1. Bantel Schaal, U. 1990. Adeno-associated parvoviruses inhibit growth of cells derived from malignant human tumors. Int. J. Cancer 45:190-194.
2. Bantel Schaal, U. 1991. Infection with adeno-associated parvovirus leads to increased sensitivity of mammalian cells to stress. Virology 182:260-268.
3. Bantel Schaal, U. 1995. Growth properties of a human melanoma cell line are altered by adeno-associated parvovirus type 2. Int. J. Cancer 60:269-274.
4. Bantel Schaal, U., and M. Stöhr. 1992. Influence of adeno-associated virus on adherence and growth properties of normal cells. J. Virol. 66:773-779.
5. Bantel Schaal, U., and H. zur Hausen. 1988. Adeno-associated viruses inhibit SV40 DNA amplification and replication of herpes simplex virus in SV40-transformed hamster cells. Virology 164:64-74.
6. Beaton, A., P. Palumbo, and K. I. Berns. 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.
7. Beijersbergen, R. L., L. Carlee, R. M. Kerkhoven, and R. Bernards. 1995. Regulation of the retinoblastoma protein-related p107 by G1 cyclin complexes. Genes Dev. 9:1340-1353.
8. Berns, K. I. 1990. Parvovirus replication. Microbiol. Rev. 54:316-329.
9. Botz, J., K. Zerfass-Thome, D. Spitkovsky, H. Delius, B. Vogt, M. Eilers, A. Hatzigeorgiou, and P. Jansen-Dürr. 1996. Cell cycle regulation of the murine cyclin E gene depends on an E2F binding site in the promoter. Mol. Cell. Biol. 16:3401-3409.
10. Carter, B. J., J. P. Trempe, and E. Mendelson. 1990. Adeno-associated virus gene expression and regulation, p. 227-254. In P. Tijssen (ed.), Handbook of parvoviruses. CRC Press, Boca Raton, Fla.
11. Chin, Y. E., M. Kitagawa, W. C. Su, Z. H. You, Y. Iwamoto, and X. Y. Fu. 1996. Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science 272:719-722.
12. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
13. Church, G. M., and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81:1991-1995.
14. Cobrinik, D., S. F. Dowdy, P. W. Hinds, S. Mittnacht, and R. A. Weinberg. 1992. The retinoblastoma protein and the regulation of cell cycling. Trends Biochem. Sci. 17:312-315.
15. Cobrinik, D., P. Whyte, D. S. Peeper, T. Jacks, and R. A. Weinberg. 1993. Cell cycle-specific association of E2F with the p130 E1A-binding protein. Genes Dev. 7:2392-2404.
16. Cukor, G., N. R. Blacklow, S. Kibrick, and I. C. Swan. 1975. Effect of adeno-associated virus on cancer expression by herpesvirus-transformed hamster cells. J. Natl. Cancer Inst. 55:957-959.
17. Datto, M. B., Y. Li, J. F. Panus, D. J. Howe, Y. Xiong, and X. F. Wang. 1995. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc. Natl. Acad. Sci. USA 92:5545-5549.
18. de la Maza, L. M., and B. J. Carter. 1981. Inhibition of adenovirus oncogenicity in hamsters by adeno-associated virus DNA. JNCI 67:1323-1326.
19. Draetta, G. F. 1994. Mammalian G1 cyclins. Curr. Opin. Cell Biol. 6:842-846.
20. Dulic, V., L. F. Drullinger, E. Lees, S. I. Reed, and G. H. Stein. 1993. Altered regulation of G1 cyclins in senescent human diploid fibroblasts: accumula tion of inactive cyclin E-Cdk2 and cyclin D1-Cdk2 complexes. Proc. Natl. Acad. Sci. USA 90:11034-11038.
21. Dulic, V., W. K. Kaufmann, S. J. Wilson, T. D. Tisty, E. Lees, J. W. Harper, S. J. Elledge, and S. I. Reed. 1994. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76:1013-1023.
22. El-Deiry, W. S., J. W. Harper, P. M. O'Connor, V. E. Velculescu, C. E. Canman, J. Jackman, J. A. Pietenpol, M. Burrell, D. E. Hill, Y. Yang, et al. 1994. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54:1169-1174.
23. El-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
24. Elledge, S. J., and J. W. Harper. 1994. Cdk inhibitors: on the threshold of checkpoints and development. Curr. Opin. Cell Biol. 6:847-852.
25. Elledge, S. J., J. Winston, and J. W. Harper. 1996. A question of balance: the role of cyclin-kinase inhibitors in development and tumorigenesis. Trends Cell Biol. 6:388-392.
26. Fotedar, R., P. Fitzgerald, T. Rouselle, D. Cannella, M. Dorée, H. Messier, and A. Fotedar. 1996. p21 contains independent binding sites for cyclin and cdk2: both sites are required to inhibit cdk2 kinase activity. Oncogene 12: 2155-2164.
27. Geng, Y., E. N. Eaton, M. Picon, J. M. Roberts, A. S. Lundberg, A. Gifford, C. Sardet, and R. A. Weinberg. 1996. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene 12:1173-1180.
28. Guo, K., J. Wang, V. Andres, R. C. Smith, and K. Walsh. 1995. MyoD induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol. Cell. Biol. 15:3823-3829.
29. Halevy, O., B. G. Novitch, D. B. Spicer, S. X. Skapek, J. Rhee, G. J. Hannon, D. Beach, and A. B. Lassar. 1995. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267:1018-1021.
30. Harper, J. W., G. R. Adami, N. Wei, K. Keyomarsi, and S. J. Elledge. 1993. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816.
31. Harper, J. W., and S. J. Elledge. 1996. CDK inhibitors in development and cancer. Curr. Opin. Genet. Dev. 6:56-64.
32. Heilbronn, R., J. R. Schlehofer, and H. zur Hausen. 1984. Selective killing of carcinogen-treated SV40-transformed Chinese hamster cells by a defective parvovirus. Virology 136:439-441.
33. 32a. Hermanns, J. Unpublished data.
34. Hermonat, P. L. 1989. The adeno-associated virus Rep78 gene inhibits cellular transformation induced by bovine papillomavirus. Virology 172:253-261.
35. Hermonat, P. L. 1991. Inhibition of H-ras expression by the adeno-associated virus Rep78 transformation suppressor gene product. Cancer Res. 51:3373-3377.
36. Hinds, P. W. 1995. The retinoblastoma tumor suppressor protein. Curr. Opin. Genet. Dev. 5:79-83.
37. Hoffmann, I., P. R. Clarke, M. J. Marcote, E. Karsenti, and G. Draetta. 1993. Phosphorylation and activation of human cdc25-C by cdc2-cyclin B and its involvement in the self-amplification of MPF at mitosis. EMBO J. 12:53-63.
38. Hörer, M., S. Weger, K. Butz, F. Hoppe-Seyler, C. Geisen, and J. A. Kleinschmidt. 1995. Mutational analysis of adeno-associated virus Rep protein-mediated inhibition of heterologous and homologous promoters. J. Virol. 69:5485-5496.
39. Hsiao, K. M., S. L. McMahon, and P. J. Farnham. 1994. Multiple DNA elements are required for the growth regulation of the mouse E2F1 promoter. Genes Dev. 8:1526-1537.
40. Hunter, T., and J. Pines. 1994. Cyclins and cancer. II. Cyclin D and CDK inhibitors come of age. Cell 79:573-582.
41. Jiang, H., J. Lin, Z. Z. Su, F. R. Collart, E. Huberman, and P. B. Fisher. 1994. Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene 9:3397-3406.
42. Khleif, S. N., T. Myers, B. J. Carter, and J. P. Trempe. 1991. Inhibition of cellular transformation by the adeno-associated virus rep gene. Virology 181:738-741.
43. Kirschstein, R. L., K. O. Smith, and E. A. Peters. 1968. Inhibition of adenovirus 12 oncogenicity by adeno-associated virus. Proc. Soc. Exp. Biol. Med. 128:670-673.
44. Klein-Bauernschmitt, P., M. von Knebel Doebertitz, M. Ehrbar, K. Geletneky, J. Kleinschmidt, and J. R. Schlehofer. 1996. Improved efficacy of chemotherapy by parvovirus-mediated sensitisation of human tumour cells. Eur. J. Cancer 32A:1774-1780.
45. Klein-Bauernschmitt, P., H. zur Hausen, and J. R. Schlehofer. 1992. Induction of differentiation-associated changes in established human cells by infection with adeno-associated virus type 2. J. Virol. 66:4191-4200.
46. Ko, L. J., and C. Prives. 1996. p53: puzzle and paradigm. Genes Dev. 10:1054-1072.
47. Kyostio, S. R., R. A. Owens, M. D. Weitzman, B. A. Antoni, N. Chejanovsky, and B. J. Carter. 1994. Analysis of adeno-associated virus (AAV) wild-type and mutant Rep proteins for their abilities to negatively regulate AAV p5 and p19 mRNA levels. J. Virol. 68:2947-2957.
48. Kyostio, S. R., R. S. Wonderling, and R. A. Owens. 1995. Negative regulation of the adeno-associated virus (AAV) P5 promoter involves both the P5 rep binding site and the consensus ATP-binding motif of the AAV Rep68 protein. J. Virol. 69:6787-6796.
49. Labow, M. A., L. H. Graf, Jr., and K. I. Berns. 1987. Adeno-associated virus gene expression inhibits cellular transformation by heterologous genes. Mol. Cell. Biol. 7:1320-1325.
50. Labow, M. A., P. L. Hermonat, and K. I. Berns. 1986. Positive and negative autoregulation of the adeno-associated virus type 2 genome. J. Virol. 60: 251-258.
51. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
52. La Thangue, N. B. 1996. E2F and the molecular mechanisms of early cell-cycle control. Biochem. Soc. Trans. 24:54-59.
53. Macleod, K. F., N. Sherry, G. Hannon, D. Beach, T. Tokino, K. Kinzler, B. Vogelstein, and T. Jacks. 1995. p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 9:935-944.
54. Mayor, H. D., G. S. Houlditch, and D. M. Mumford. 1973. Influence of adeno-associated satellite virus on adenovirus-induced tumours in hamsters. Nature New Biol. 241:44-46.
55. Mendelson, E., M. G. Smith, I. L. Miller, and B. J. Carter. 1988. Effect of a viral rep gene on transformation of cells by an adeno-associated virus vector. Virology 166:612-615.
56. Michieli, P., M. Chedid, D. Lin, J. H. Pierce, W. E. Mercer, and D. Givol. 1994. Induction of WAF1/CIP1 by a p53-independent pathway. Cancer Res. 54:3391-3395.
57. Waf1 in NIH3T3 cells. Oncogene 12:775-784.
58. Missero, C., E. Calautti, R. Eckner, J. Chin, L. H. Tsai, D. M. Livingston, and G. P. Dotto. 1995. Involvement of the cell-cycle inhibitor Cip1/WAF1 and the E1A-associated p300 protein in terminal differentiation. Proc. Natl. Acad. Sci. USA 92:5451-5455.
59. Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131-134.
60. Müller, R. 1995. Transcriptional regulation during the mammalian cell cycle. Trends Genet. 11:173-178.
61. Murray, A. 1994. Cell cycle checkpoints. Curr. Opin. Cell Biol. 6:872-876.
62. Noda, A., Y. Ning, S. F. Venable, O. M. Pereira Smith, and J. R. Smith. 1994. Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211:90-98.
63. Ohtani, K., J. DeGregori, and J. R. Nevins. 1995. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. USA 92:12146-12150.
64. Ostrove, J. M., D. H. Duckworth, and K. I. Berns. 1981. Inhibition of adenovirus-transformed cell oncogenicity by adeno-associated virus. Virology 113:521-533.
65. Pagano, M., G. Draetta, and P. Jansen-Dürr. 1992. Association of cdk2 kinase with the transcription factor E2F during S phase. Science 255:1144-1147.
66. Cip1 in muscle and other terminally differentiating cells. Science 267: 1024-1027.
67. Rommelaere, J., and P. Tattersall. 1990. Oncosuppression by parvoviruses, p. 41-57. In P. Tijssen (ed.), Handbook of parvoviruses. CRC Press, Boca Raton, Fla.
68. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
69. Schlehofer, J. R. 1994. The tumor suppressive properties of adeno-associated viruses. Mutat. Res. 305:303-313.
70. INK4, the product of the putative tumor suppressor gene MTS1. Oncogene 9:3475-3482.
71. Schulze, A., K. Zerfass, D. Spitkovsky, S. Middendorp, J. Berges, K. Helin, P. Jansen-Dürr, and B. Henglein. 1995. Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc. Natl. Acad. Sci. USA 92:11264-11268.
72. Sheaff, R. J., and J. M. Roberts. 1995. Lessons in p16 from the phylum Falconium. Curr. Biol. 5:28-31.
73. Sherr, R. J., and J. M. Roberts. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
74. Shiyanov, P., S. Bagchi, G. Adami, J. Kokontis, N. Hay, M. Arroyo, A. Morozov, and P. Raychaudhuri. 1996. p21 disrupts the interaction between cdk2 and the E2F-p130 complex. Mol. Cell. Biol. 16:737-744.
75. Siegl, G., and J.-D. Tratschin. 1987. Parvoviruses: agents of distinct pathogenic and molecular potential. FEMS Micobiol. Rev. 46:433-450.
76. Steinman, R. A., B. Hoffman, A. Iro, C. Guillouf, D. A. Liebermann, and M. E. el Houseini. 1994. Induction of p21 (WAF-1/CIP1) during differentiation. Oncogene 9:3389-3396.
77. Tijssen, P. 1990. Handbook of parvoviruses. CRC Press, Boca Raton, Fla.
78. Timchenko, N. A., M. Wilde, M. Nakanishi, J. R. Smith, and G. J. Darlington. 1996. CCAAT/enhancer-binding protein alpha (C/EBPa) inhibits cell proliferation through the p21 (WAF-1/CIP-1/SDI-1) protein. Genes Dev. 10:804-815.
79. Vairo, G., D. M. Livingston, and D. Ginsberg. 1995. Functional interaction between E2F-4 and p130: evidence for distinct mechanisms underlying growth suppression by different retinoblastoma protein family members. Genes Dev. 9:869-881.
80. Waga, S., G. J. Hannon, D. Beach, and B. Stillman. 1994. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369:574-578.
81. Walz, C., and J. R. Schlehofer. 1992. Modification of some biological properties of HeLa cells containing adeno-associated virus DNA integrated into chromosome 17. J. Virol. 66:2990-3002.
82. Walz, C., J. R. Schlehofer, M. Flentje, V. Rudat, and H. zur Hausen. 1992. Adeno-associated virus sensitizes HeLa cell tumors to gamma rays. J. Virol. 66:5651-5657.
83. Weintraub, S. J., C. A. Prater, and D. C. Dean. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature 358:259-261.
84. Whittaker, N. Unpublished data.
85. Winocour, E., M. F. Callaham, and E. Huberman. 1988. Perturbation of the cell cycle by adeno-associated virus. Virology 167:393-399.
86. Wonderling, R. S., and R. A. Owens. 1996. The Rep68 protein of adeno-associated virus type 2 stimulates expression of the platelet-derived growth factor B c-sis proto-oncogene. J. Virol. 70:4783-4786.
87. Xiong, Y., G. J. Hannon, H. Zhang, D. Casso, R. Kobayashi, and D. Beach. 1993. p21 is a universal inhibitor of cyclin kinases. Nature 366:701-704.
88. Yang, Q., F. Chen, and J. P. Trempe. 1994. Characterization of cell lines that inducibly express the adeno-associated virus Rep proteins. J. Virol. 68:4847-4856.
89. KIP1 blocks cyclin E-dependent transactivation of cyclin A gene expression. Mol. Cell. Biol. 17:407-415.
90. Zhu, L., E. Harlow, and B. D. Dynlacht. 1995. p107 uses a p21CIP1-related domain to bind cyclin/cdk2 and regulate interactions with E2F. Genes Dev. 9:1740-1752.