Repression of CDK1 and other genes with CDE and CHR promoter elements during DNA damage-induced G2/M arrest in human cells

Molecular and Cellular Biology

Volumn 20, Issue 7, 2000, Pages 2358-2366

  Badie, Christophe ^a   Itzhaki, Jane E ^a,b   Sullivan, Matthew J ^a   Carpenter, Adam J ^a   Porter, Andrew C G ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; CYCLIN DEPENDENT KINASE; CYCLINE; DNA TOPOISOMERASE (ATP HYDROLYSING);

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; DNA DAMAGE; DOWN REGULATION; FIBROBLAST; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MITOSIS; MITOSIS INHIBITION; PHOSPHORYLATION; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION;

CDC2 PROTEIN KINASE; CELL CYCLE; CELL LINE; DNA DAMAGE; DNA REPLICATION; DOWN-REGULATION; FLOW CYTOMETRY; G2 PHASE; GAMMA RAYS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, REPORTER; HUMANS; MITOSIS; MUTATION; NUCLEAR PROTEINS; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); REGULATORY SEQUENCES, NUCLEIC ACID; RNA, MESSENGER; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0034019111     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.7.2358-2366.2000     Document Type: Article

References (65)

1. Agarwal, M. L., A. Agarwal, W. R. Taylor, and G. R. Stark. 1995. p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc. Natl. Acad. Sci. USA 92:8493-8497.
2. Amon, A., U. Surana, I. Muroff, and K. Nasmyth. 1992. Regulation of p34CDC28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae. Nature 355:368-371.
3. Azzam, E. I., S. M. de Toledo, M. J. Pykett, H. Nagasawa, and J. B. Little. 1997. CDC2 is down-regulated by ionizing radiation in a p53-dependent manner. Cell Growth Differ. 8:1161-1169.
4. Badie, C., J. Bourhis, J. Sobczak-Thepot, H. Haddada, M. Chiron, M. Janicot, F. Janot, and G. Vassal. p53-dependent G2 arrest associated with a decrease in cyclins A2 and B1 levels in a human carcinoma cell line. Br. J. Cancer, in press.
5. Banin, S., L. Moyal, S. Shieh, Y. Taya, C. W. Anderson, L. Chessa, N. I. Smorodinsky, C. Prives, Y. Reiss, Y. Shiloh, and Y. Ziv. 1998. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281: 1674-1677.
6. Canman, C. E., D. S. Lim, K. A. Cimprich, Y. Taya, K. Tamai, K. Sakaguchi, E. Appella, M. B. Kastan, and J. D. Siliciano. 1998. Activation of the ATM kinase hy ionizing radiation and phosphorylation of p53. Science 281:1677-1679.
7. Cox, L. S., and D. P. Lane. 1995, Tumour suppressors, kinases and clamps: how p53 regulates the cell cycle in response to DNA damage. Bioessays 17: 501-508.
8. Dalton, S. 1992. Cell cycle regulation of the human cdc2 gene. EMBO J. 11: 1797-1804.
9. Desdouets, C., C. Ory, G. Matesic, T. Soussi, C. Brechot, and J. Sobczak Thepot. 1996. ATF/CREB site mediated transcriptional activation and p53 dependent repression of the cyclin A promoter. FEBS Lett. 385:34-38.
10. de Toledo, S. M., E. I. Azzam, P. Keng, S. Laffrenier, and J. B. Little. 1998. Regulation by ionizing radiation of CDC2, cyclin A, cyclin B, thymidine kinase, topoisomerase IIalpha, and RAD51 expression in normal human diploid fibroblasts is dependent on p53/p21Waf1. Cell Growth Differ. 9: 887-896.
11. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
12. 2/M-phase transition. Mol. Cell. Biol. 18:546-557.
13. Elledge, S. J. 1996. Cell cycle checkpoints: preventing an identity crisis. Science 274:1664-1672.
14. Enoch, T., and C. Norbury. 1995. Cellular responses to DNA damage: cell-cycle checkpoints, apoptosis and the roles of p53 and ATM. Trends Biochem. Sci. 20:426-430.
15. Good, L., J. Chen, and K. Y. Chen. 1995. Analysis of sequence-specific binding activity of cis-elements in human thymidine kinase gene promoter during G1/S phase transition. J. Cell. Physiol. 163:636-644.
16. Hartwell, L., T. Weinert, L. Kadyk, and B. Garvik. 1994. Cell cycle checkpoints, genomic integrity, and cancer. Cold Spring Harbor Symp. Quant. Biol. 59:259-263.
17. Hartwell, L. H., and T. A. Weinert. 1989. Checkpoints: controls that ensure the order of cell cycle events. Science 246:629-634.
18. Hayles, J., D. Fisher, A. Woollard, and P. Nurse. 1994. Temporal order of S phase and mitosis in fission yeast is determined by the state of the p34cdc2-mitotic B cyclin complex. Cell 78:813-822.
19. Hermeking, H., C. Lengauer, K. Pulyak, T. C. He, L. Zhang, S. Thiagalingam, K. W. Kinzler, and B. Vogelstein. 1997. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1:3-11.
20. Herzinger, T., J. O. Funk, K. Hillmer, D. Eick, D. A. Wolf, and P. Kind. 1995. Ultraviolet B irradiation-induced G2 cell cycle arrest in human keratinocytes by inhibitory phosphorylation of the cdc2 cell cycle kinase. Oncogene 11: 2151-2156.
21. Hofmann, J., P. M. O'Connor, J. Jackman, C. Schubert, F. Ueberall, K. W. Kohn, and H. Grunicke. 1994. The protein kinase C inhibitor ilmofosine (BM 41 440) arrests cells in G2 phase and suppresses CDC2 kinase activation through a mechanism different from that of DNA damaging agents. Biochem. Biophys. Res. Commun. 199:937-943.
22. Hwang, A., W. G. McKenna, and R. J. Muschel. 1998. Cell cycle-dependent usage of transcriptional start sites. A novel mechanism for regulation of cyclin B1. J. Biol. Chem. 273:31505-31509.
23. Innocente, S. A., J. L. Abrahamson, J. P. Cogswell, and J. M. Lee. 1999. p53 regulates a G2 checkpoint through cyclin B1. Proc. Natl. Acad. Sci. USA 96: 2147-2152.
24. Isaacs, R. J., S. L. Davies, M. I. Sandri, C. Redwood, N. J. Wells, and I. D. Hickson. 1998. Physiological regulation of eukaryotic topoisomerase II. Biochim. Biophys. Acta 1400:121-137.
25. Itzhaki, J. E., C. S. Gilbert, and A. C. G. Porter. 1997. Construction by gene targeting in human cells of a "conditional" CDC2 mutant that rereplicates its DNA. Nat. Genet. 15:258-265.
26. Jimenez, G. S., F. Bryntesson, M. I. Torres Arzayus, A. Priestley, M. Beeche, S. Saito, K. Sakaguchi, E. Appella, P. A. Jeggo, G. E. Taccioli, G. M. Wahl, and M. Hubank. 1999. DNA-dependent protein kinase is not required for the p53-dependent response to DNA damage. Nature 400:81-83.
27. Jin, P., Y. Gu, and D. O. Morgan. 1996. Role of inhibitory CDC2 phosphorylation in radiation-induced G2 arrest in human cells. J. Cell Biol. 134: 963-970.
28. Jin, P., S. Hardy, and D. O. Morgan. 1998. Nuclear localization of cyclin B1 controls mitotic entry after DNA damage. J. Cell Biol. 141:875-885.
29. Kao, G. D., W. G. McKenna, A. Maity, K. Blank, and R. J. Muschel. 1997. Cyclin B1 availability is a rate-limiting component of the radiation-induced G2 delay in HeLa cells. Cancer Res. 57:753-758.
30. Katula, K. S., K. L. Wright, H. Paul, D. R. Surman, F. J. Nuckolls, J. W. Smith, J. P. Ting, J. Yates, and J. P. Cogswell. 1997. Cyclin-dependent kinase activation and S-phase induction of the cyclin B1 gene are linked through the CCAAT elements. Cell Growth Differ. 8:811-820.
31. Kharbanda, S., A. Saleem, R. Datta, Z. M. Yuan, R. Weichselbaum, and D. Kufe. 1994. Ionizing radiation induces rapid tyrosine phosphorylation of p34cdc2. Cancer Res. 54:1412-1414.
32. Lanni, J. S., and T. Jacks. 1998. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol. Cell. Biol. 18: 1055-1064.
33. Liu, N., F. C. Lucibello, K. Engeland, and R. Muller. 1998. A new model of cell cycle-regulated transcription: repression of the cyclin A promoter by CDF-1 and anti-repression by E2F. Oncogene 16:2957-2963.
34. Liu, N., F. C. Lucibello, K. Korner, L. A. Wolfraim, J. Zwicker, and R. Muller. 1997. CDF-1, a novel E2F-unrelated factor, interacts with cell cycle-regulated repressor elements in multiple promoters. Nucleic Acids Res. 25: 4915-4920.
35. Lucibello, F. C., M. Truss, J. Zwicker, F. Ehlert, M. Beato, and R. Muller. 1995. Periodic cdc25C transcription is mediated by a novel cell cycle-regulated repressor element (CDE). EMBO J. 14:132-142.
36. Matsuoka, S., M. Huang, and S. J. Elledge. 1998. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282:1893-1897.
37. McGowan, C. H., P. Russell, and S. I. Reed. 1990. Periodic biosynthesis of the human M-phase-promoting factor catalytic subunit p34 during the cell cycle. Mol. Cell. Biol. 10:3847-3851.
38. Mitchel, R. E., A. Chan, B. P. Smith, S. D. Child, and M. C. Paterson. 1984. The effects of hyperthermia and ionizing radiation in normal and ataxia telangiectasia human fibroblast lines. Radiat. Res. 99:627-635.
39. Nurse, P. 1997. Checkpoint pathways come of age. Cell 91:865-867.
40. Nusse, M., W. Beisker, C. Hoffmann, and A. Tarnok. 1990. Flow cytometric analysis of G1-and G2/M-phase subpopulations in mammalian cell nuclei using side scatter and DNA content measurements. Cytometry 11:813-821.
41. O'Connell, M. J., J. M. Raleigh, H. M. Verkade, and P. Nurse. 1997. Chk1 is a wee 1 kinase in the G2 DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J. 16:545-554.
42. O'Connor, P. M., D. K. Ferris, I. Hoffmann, J. Jackman, G. Draetta, and K. W. Kohn. 1994. Role of the cdc25C phosphatase in G2 arrest induced by nitrogen mustard. Proc. Natl. Acad. Sci. USA 91:9480-9484.
43. Pellegata, N. S., R. J. Antoniono, J. L. Redpath, and E. J. Stanbridge. 1996. DNA damage and p53-mediated cell cycle arrest: a reevaluation. Proc. Natl. Acad. Sci. USA 93:15209-15214.
44. Poon, R. Y. C., W. Jiang, H. Toyoshima, and T. Hunter. 1996. Cyclin-dependent kinases are inactivated by a combination of p21 and Thr-14/ Tyr-15 phosphorylation after UV-induced DNA damage. J. Biol. Chem. 271: 13283-13291.
45. Porter, A. C. G., and J. E. Itzhaki. 1993. Gene targeting in human somatic cells. Complete inactivation of an interferon-inducible gene. Eur. J. Biochem. 218:273-281.
46. Rhind, N., and P. Russell. 1998. Mitotic DNA damage and replication checkpoints in yeast. Curr. Opin. Cell Biol. 10:749-758.
47. 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.
48. Sandri, M. I., R. J. Isaacs, W. M. Ongkeko, A. L. Harris, I. D. Hickson, M. Broggini, and F. Vikhanskaya. 1996. p53 regulates the minimal promoter of the human topoisomerase IIalpha gene. Nucleic Acids Res. 24:4464-4470.
49. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
50. Shelby, R. D., O. Vafa, and K. F. Sullivan. 1997. Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites. J. Cell Biol. 136:501-513.
51. Sorger, P. K., and A. W. Murray. 1992. S-phase feedback control in budding yeast independent of tyrosine phosphorylation of p34cdc28. Nature 355: 365-368.
52. Sugarman, J. L., A. H. Schonthal, and C. K. Glass. 1995. Identification of a cell-type-specific and E2F-independent mechanism for repression of cdc2 transcription. Mol. Cell. Biol. 15:3282-3290.
53. Talis, A. L., J. M. Huibregtse, and P. M. Howley. 1998. The role of E6AP in the regulation of p53 protein levels in human papillomavirus (HPV)-positive and HPV-negative cells. J. Biol. Chem. 273:6439-6445.
54. Waldman, T., Y. Zhang, L. Dillehay, J. Yu, K. Kanzler, B. Vogelstein, and J. Williams. 1997. Cell-cycle arrest versus cell death in cancer therapy. Nat. Med. 3:1034-1036.
55. Wang, J. Y. 1998. Cellular responses to DNA damage. Curr. Opin. Cell Biol. 10:240-247. (Erratum, 10:416.)
56. Wang, Q., G. P. Zambetti, and D. P. Suttle. 1997. Inhibition of DNA topoisomerase II alpha gene expression by the p53 tumor suppressor. Mol. Cell. Biol. 17:389-397.
57. Weinert, T. 1997. A DNA damage checkpoint meets the cell cycle engine. Science 277:1450-1451.
58. Welch, P. J., and J. Y. Wang. 1992. Coordinated synthesis and degradation of cdc2 in the mammalian cell cycle. Proc. Natl. Acad. Sci. USA 89:3093-3097.
59. Winters, Z. E., W. M. Ongkeko, A. L. Harris, and C. J. Norbury. 1998. p53 regulates Cdc2 independently of inhibitory phosphorylation to reinforce radiation-induced G2 arrest in human cells. Oncogene 17:673-684.
60. Woo, R. A., K. G. McLure, S. P. Lees Miller, D. E. Rancourt, and P. W. Lee. 1998. DNA-dependent protein kinase acts upstream of p53 in response to DNA damage. Nature 394:700-704.
61. Yamamoto, A., V. Guacci, and D. Koshland. 1996. Pds1p, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s). J. Cell Biol. 133:99-110.
62. Yáñez, R. J., and A. C. G. Porter. 1999. Gene targeting is enhanced in human cells overexpressing hRAD51. Gene Ther. 6:1282-1290.
63. Zwicker, J., K. Korner, and R. Muller. 1999. The SV40 large T oncoprotein disrupts DNA-binding of the cell cycle-regulated transcriptional repressor CDF. Oncogene 18:2023-2025.
64. Zwicker, J., and R. Muller. 1995. Cell cycle-regulated transcription in mammalian cells. Prog. Cell Cycle Res. 1:91-99.
65. Zwicker, J., and R. Muller. 1997. Cell-cycle regulation of gene expression by transcriptional repression. Trends Genet. 13:3-6.