Down-regulation of Cyclin A gene expression upon genotoxic stress correlates with reduced binding of free E2F to the promoter

Cell Growth and Differentiation

Volumn 8, Issue 6, 1997, Pages 699-710

  Spitkovsky, Dimitry ^a   Schulze, Almut ^a   Boye, Barbara ^a   Jansen Dürr, Pidder ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; CYCLIN A; CYCLIN D1; CYCLIN E; DNA; PROTEIN KINASE INHIBITOR; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL STRAIN 3T3; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; FIBROBLAST; GENOTOXICITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; STRESS;

3T3 CELLS; ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CARRIER PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CISPLATIN; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA-BINDING PROTEINS; DOWN-REGULATION; E2F TRANSCRIPTION FACTORS; E2F4 TRANSCRIPTION FACTOR; ENZYME INHIBITORS; FIBROBLASTS; G1 PHASE; HUMANS; MICE; ONCOGENE PROTEINS; PHOSPHORYLATION; PLASMIDS; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; TRANSCRIPTION FACTOR DP1; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

ANIMALIA; MAMMALIA;

EID: 0030985177     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (70)

1. Murnane, J. P. Cell cycle regulation in response to DNA damage in mammalian cells: a historical perspective. Cancer Metastasis Rev., 14: 17-29, 1995.
2. Aisner, J., and Abrams, J. Cisplatin for small-cell lung cancer. Semin. Oncol., 16: 2-9, 1989.
3. al Sarraf, M. Cisplatin combinations in the treatment of head and neck cancer. Semin. Oncol., 21: 28-34, 1994.
4. Alberts, D. S., Garcia, D., and Mason, L. N. Cisplatin in advanced cancer of the cervix: an update. Semin. Oncol., 18: 11-24, 1991.
5. Sledge, G. J. Cisplatin and platinum analogues in breast cancer. Semin. Oncol., 19: 78-82, 1992.
6. Roberts, J. J., and Friedlos, F. Quantitative aspects of the formation and loss of DNA interstrand crosslinks in Chinese hamster cells following treatment with cis-diamminedichloroplatinum(II) (cisplatin). I. Proportion of DNA-platinum reactions involved in DNA crosslinking. Biochim. Biophys. Acta, 655: 146-151, 1981.
7. Jackel, M., and Kopf, M. P. Influence of cisplatin on cell-cycle progression in xenografted human head and neck carcinomas. Cancer Chemother. Pharmacol., 27: 464-471, 1991.
8. Butz, K., Shahabeddin, L., Geisen, C., Spitkovsky, D., Ullmann, A., and Hoppeseyler, F. Functional p53 protein in human papillomavirus-positive cancer cells. Oncogene, 10: 927-936, 1995.
9. Donaldson, K. L., Goolsby, G. L., and Wahl, A. F. Cytotoxicity of the anticancer agents cisplatin and taxol during cell proliferation and the cell cycle. Int. J. Cancer, 57: 847-855, 1994.
10. Wennerberg, J., Alm, P., Biorklund, A., Killander, D., Langstrom, E., and Trope, C. Cell cycle perturbations in heterotransplanted squamous-cell carcinoma of the head and neck after mitomycin C and cisplatin treatment. Int. J. Cancer, 33: 213-222, 1984.
11. Dileonardo, A., Linke, S. P., Clarkin, K., and Wahl, G. M. DNA damage triggers a prolonged p53-dependent G(1) arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev., 8: 2540-2551, 1994.
12. Dulic, V., Kaufmann, W. K., Wilson, S. J., Tlsty, T. D., Lees, E., Harper, J. W., Elledge, S. J., and Reed, S. I. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell, 76: 1013-1023, 1994.
13. Sherr, C. J. G1 phase progression: cycling on cue. Cell, 79: 551-555, 1994.
14. El-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., and Vogelstein, B. WAF1, a potential mediator of p53 tumor suppression. Cell, 75: 817-825, 1993.
15. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K., and Elledge, S. J. The p21 CDK-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75: 805-816, 1993.
16. Xiong, Y., Hannon, G. J., Zhang, H., Casso, D., Kobayashi, R., and Beach, D. p21 is a universal inhibitor of cyclin kinases. Nature (Lond.), 366: 701-704, 1993.
17. Polyak, K., Lee, M. H., Erdjumentbromage, H., Koff, A., Roberts, J. M., Tempst, P., and Massagué, J. Cloning of p27(Kip1), a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell, 78: 59-66, 1994.
18. Toyoshima, H., and Hunter, T. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell, 78: 67-74, 1994.
19. Serrano, M., Hannon, G. J., and Beach, D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin-D/CDK4. Nature (Lond.), 366: 704-707, 1993.
20. La Thangue, N. B. Drtf1/E2F: an expanding family of heterodimeric transcription factors implicated in cell-cycle control. Trends Biochem. Sci., 19: 108-114, 1994.
21. Schwarz, J. K., Devoto, S. H., Smith, E. J., Chellapan, S. P., Jakoi, L., and Nevins, J. R. Interactions of the p107 and Rb proteins with E2F during the cell proliferation response. EMBO J., 12: 1013-1020, 1993.
22. Hsiao, K. M., Mcmahon, S. L, and Farnham, P. J. Multiple DNA elements are required for the growth regulation of the mouse E2F1 promoter. Genes Dev., 8: 1526-1537, 1994.
23. Johnson, D. G., Ohtani, K., and Nevins, J. R. Autoregulatory control of E2F1 expression in response to positive and negative regulators of cell cycle progression. Genes Dev., 8: 1514-1525, 1994.
24. Schulze, A., Zerfass, K., Spitkovsky, D., Berges, J., Middendorp, S., Jansen-Dürr, P., and Henglein, B. Cell cycle regulation of cyclin A gene transcription is mediated by a variant E2F binding site. Proc. Natl. Acad. Sci. USA, 92: 11264-11268, 1995.
25. Pagano, M., Pepperkok, R., Verde, F., Ansorge, W., and Draetta, G. Cyclin A is required at two points in the human cell cycle. EMBO J., 11: 961-971, 1992.
26. Zindy, F., Lamas, E., Chenivesse, X., Sobczak, J., Fesquet, D., Wang, J., Henglein, B., and Brechot, C. Cyclin A is required in S phase in normal epithelial cells. Biophys. Biochem. Res. Commun., 182: 1144-1154, 1991.
27. Girard, F., Strausfeld, U., Fernandez, A., and Lamb, N. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell, 67: 1169-1179, 1991.
28. Cardoso, M. C., Leonhardt, H., and Nadalginard, B. Reversal of terminal differentiation and control of DNA replication: cyclin-A and Cdk2 specifically localize at subnuclear sites of DNA replication. Cell, 74: 979-992, 1993.
29. D'Urso, G., Marraccino, R. L., Marshak, D. R., and Roberts, J. M. Cell cycle control of DNA replication by a homologue from human cells of the p34cdc2 protein kinase. Science (Washington DC), 250: 786-791, 1990.
30. Henglein, B., Chenivesse, X., Wang, J., Eick, D., and Brechot, C. Structure and cell cycle regulated transcription of the human cyclin A gene. Proc. Natl. Acad. Sci. USA, 91: 5490-5494, 1994.
31. Runkel, L., Shaw, P. E., Herrera, R. E., Hipskind, R. A., and Nordheim, A. Multiple basal promoter elements determine the level of human c-fos transcription. Mol. Cell. Biol., 11: 1270-1280, 1991.
32. Philipp, A., Schneider, A., Vasrik, I., Finke, K., Xiong, Y., Beach, D., Alitalo, K., and Eilers, M. Repression of cyclin D1: a novel function of MYC. Mol. Cell. Biol., 14: 4032-4043, 1994.
33. Hofmann, F., Martelli, F., Livingston, D. M., and Wang, Z. The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes Dev., 10: 2949-2959, 1996.
34. Hateboer, G., Kerkhoven, R. M., Shvarts, A., Bernards, R., and Beijersbergen, R. L. Degradation of E2F by the ubiquitin-proteasome pathway: regulation by retinoblastoma family proteins and adenovirus transforming proteins. Genes Dev., 10: 2960-2970, 1996.
35. Beijersbergen, R. L., and Bernards, R. Cell cycle regulation by the retinoblastoma family of growth inhibitory proteins. Biochim. Biophys. Acta, 1287: 103-120, 1996.
36. Slebos, R. J. C., Lee, M. H., Plunkett, B. S., Kessis, T. D., Williams, B. O., Jacks, T., Hedrick, L., Kastan, M. B., and Cho, K. R. p53-dependent G(1) arrest involves pRB-related proteins and is disrupted by the human papillomavirus 16 E7 oncoprotein. Proc. Natl. Acad. Sci. USA, 91: 5320-5324, 1994.
37. Hall, M., Bates, S., and Peters, G. Evidence for different modes of action of cyclin-dependent kinase inhibitors: p15 and p16 bind to kinases, p21 and p27 bind to cyclins. Oncogene, 11: 1581-1588, 1995.
38. Sherr, C. J. Cancer cell cycles. Science (Washington DC), 274: 1672-1677, 1996.
39. Lees, E. Cyclin dependent kinase regulation. Curr. Opin. Cell Biol., 7: 773-780, 1995.
40. Pera, M. J., Rawlings, C. J., Shackleton, J., and Roberts, J. J. Quantitative aspects of the formation and loss of DNA interstrand crosslinks in Chinese hamster cells following treatment with cis-diamminedichloroplatinum(II) (cisplatin). II. Comparison of results from alkaline elution, DNA renaturation and DNA sedimentation studies. Biochim. Biophys. Acta, 655: 152-166, 1981.
41. King, R. W., Jackson, P. K., and Kirschner, M. W. Mitosis in transition. Cell, 79: 563-571, 1994.
42. Sherr, C. J., and Roberts, J. M. Inhibitors of mammalian G(1) cyclin-dependent kinases. Genes Dev., 9: 1149-1163, 1995.
43. Demarcq, C., Bunch, R. T., Creswell, D., and Eastman, A. The role of cell cycle progression in cisplatin-induced apoptosis in Chinese hamster ovary cells. Cell Growth & Differ., 5: 983-993, 1994.
44. Yamamoto, M., Yoshida, M., Ono, K., Fujita, T., Ohtanifujita, N., Sakai, T., and Nikaido, T. Effect of tumor suppressors on cell cycle-regulatory genes: Rb suppresses P34(Cdc2) expression and normal p53 suppresses cyclin a expression. Exp. Cell Res., 210: 94-101, 1994.
45. Desdouets, C., Matesic, G., Molina, C. A., Foulkes, N. S., Sassonecorsi, P., Brechot, C., and Sobczakthepot, J. Cell cycle regulation of cyclin A gene expression by the cyclic AMP-responsive transcription factors CREB and CREM. Mol. Cell. Biol., 15: 3301-3309, 1995.
46. Yoshizumi, M., Hsieh, C. M., Zhou, F., Tsai, J. C., Patterson, C., Perrella, M. A., and Lee, M. E. The ATF site mediates downregulation of the cyclin A gene during contact inhibition in vascular endothelial cells. Mol. Cell. Biol., 15: 3266-3272, 1995.
47. Zwicker, J., Lucibello, F. C., Wolfraim, L. A., Gross, C., Truss, M., Engeland, K., and Muller, R. Cell cycle regulation of the cyclin A, cdc25C and cdc2 genes is based on a common mechanism of transcriptional repression. EMBO J., 14: 4514-4522, 1995.
48. Resnitzky, D., Hengst, L., and Reed, S. I. Cyclin A-associated kinase activity is rate limiting for entrance into S phase and is negatively regulated in G(1) by p27(Kip1). Mol. Cell. Biol., 15: 4347-4352, 1995.
49. Girard, F., Fernandez, A., and Lamb, N. Delayed cyclin A and B1 degradation in non-transformed mammalian cells. J. Cell Sci., 108: 2599-2608, 1995.
50. Ikeda, M., Jakoi, L., and Nevins, J. R. A unique role for the Rb protein in controlling E2F accumulation during cell growth and differentiation. Proc. Natl. Acad. Sci. USA, 93: 3215-3220, 1996.
51. Lathangue, N. B. E2F and the molecular mechanisms of early cell-cycle control. Biochem. Soc. Transact., 24: 54-59, 1996.
52. Zerfass, K., Spitkovsky, D., Schulze, A., Joswig, S., Henglein, B., and Jansen-Dürr, P. Adenovirus E1A activates cyclin A gene transcription in the absence of growth factors through interaction with p107. J. Virol., 70: 2637-2642, 1996.
53. Mayol, X., Garriga, J., and Grana, X. G1 cyclin/CDK-independent phosphorylation and accumulation of p130 during the transition from G1 to G0 lead to its association with E2F-4. Oncogene, 13: 237-246, 1996.
54. O'Connor, D. J., Lam, E. W. F., Griffin, S., Zhong, S., Leighton, L. C., Burbidge, S. A., and Lu, X. Physical and functional interactions between p53 and cell cycle co-operating transcription factors, E2F1 and DP1. EMBO J., 14: 6184-6192, 1995.
55. Shiyanov, P., Bagchi, S., Adami, G., Kokontis, J., Hay, N., Arroyo, M., Morozov, A., and Raychaudhuri, P. p21 disrupts the interaction between cdk2 and the E2F-p130 complex. Mol. Cell. Biol., 16: 737-744, 1996.
56. Zhu, L., Harlow, E., and Dynlacht, B. D. p107 uses a p21(CIP1)-related domain to bind cyclin/cdk2 and regulate interactions with E2F. Genes Dev., 9: 1740-1752, 1995.
57. KIP1 blocks cyclin E-dependent trans-activation of cyclin A gene expression. Mol. Cell. Biol., 17: 407-415, 1997.
58. Ohtani, K., Degregori, J., and Nevins, J. R. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. USA, 92: 12146-12150, 1995.
59. Botz, J., Zerfass-Thome, K., Spitkovsky, D., Delius, H., Vogt, B., Eilers, M., Hatzigeorgiou, A., and Jansen-Dürr, P. Cell cycle regulation of the murine cyclin E gene depends on an E2F binding site in the promoter. Mol. Cell. Biol., 16: 3401-3409, 1996.
60. Geng, Y., Eaton, E. N., Picon, M., Roberts, J. M., Lundberg, A. S., Gifford, A., Sardet, C., and Weinberg, R. A. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene, 12: 1173-1180, 1996.
61. Yamaguchi, M., Hayashi, Y., Hirose, F., Matsuoka, S., Shiroki, K., and Matsukage, A. Activation of the mouse proliferating cell nuclear antigen gene promoter by adenovirus type 12 E1A proteins. Jpn. J. Cancer Res., 83: 609-617, 1992.
62. Park, K., Choe, J., Osifchin, N. E., Templeton, D. J., Robbins, P. D., and Kim, S. J. The human retinoblastoma susceptibility gene promoter is positively autoregulated by its own product. J. Biol. Chem., 269: 6083-6088, 1994.
63. Zhu, L., Zhu, L., Xie, E., and Chang, L. S. Differential roles of two tandem E2F sites in repression of the human p107 promoter by retinoblastoma and p107 proteins. Mol. Cell. Biol., 15: 3552-3562, 1995.
64. Spitkovsky, D., Steiner, P., Lukas, J., Lees, E., Pagano, M., Schulze, A., Joswig, S., Picard, D., Tommasino, M., Eilers, M., and Jansen-Dürr, P. Modulation of cyclin gene expression by adenovirus E1A in a cell line with E1A-dependent conditional proliferation. J. Virol., 68: 2206-2214, 1994.
65. Jansen-Dürr, P., Meichle, A., Steiner, P., Pagano, M., Finke, K., Botz, J., Wessbecher, J., Draetta, G., and Eilers, M. Differential modulation of cyclin gene expression by MYC. Proc. Natl. Acad. Sci. USA, 90: 2547-2552, 1993.
66. Kaelin, W. J., Krek, W., Sellers, W. R., DeCaprio, J. A., Ajchenbaum, F., Fuchs, C. S., Chittenden, T., Li, Y., Farnham, P. J., Blanar, M. A., and Livingston, D. M. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell, 70: 351-364, 1992.
67. Wang, J., Zindy, F., Chenivesse, X., Lamas, E., Henglein, B., and Brechot, C. Modification of cyclin A expression by hepatitis B virus DNA integration in a hepatocellular carcinoma. Oncogene, 7: 1653-1656, 1992.
68. Spitkovsky, D., Steiner, P., Gopalkrishnan, R., Eilers, M., and Jansen-Dürr, P. The role of p53 in coordinated regulation of cyclin D1 and p21 gene expression by the adenovirus E1A and E1B oncogenes. Oncogene, 10: 2421-2425, 1995.
69. Tiainen, M., Spitkovsky, D., Jansen-Dürr, P., Sacchi, A., and Crescenzi, M. Expression of E1A in terminally differentiated muscle cells reactivates the cell cycle and suppresses tissue-specific genes by separable mechanisms. Mol. Cell. Biol., 16: 5302-5312, 1996.
70. Weintraub, S. J., Prater, C. A., and Dean, D. C. Retinoblastoma protein switches the E2F site from positive to negative element. Nature (Lond.), 358: 259-261, 1992.