p53 is phosphorylated by CDK7-cyclin H in a p36(MAT1)-dependent manner

Molecular and Cellular Biology

Volumn 17, Issue 12, 1997, Pages 7220-7229

  Ko, Linda J ^a   Shieh, Sheau Yann ^a   Chen, Xinbin ^b   Jayaraman, Lata ^a   Tamai, Katsuyuki ^c   Taya, Yoichi ^d   Prives, Carol ^a   Pan, Zhen Qiang ^e  

^a Columbia University ^*  (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c Medical & Biological Laboratories Co Ltd   (Japan)

^d NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^e MOUNT SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLIN H; CYCLINE; PROTEIN; PROTEIN KINASE; PROTEIN KINASE CAK; PROTEIN P 36; PROTEIN P53; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; DNA REPAIR; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; ENZYME SUBUNIT; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

EID: 0030724673     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.12.7220     Document Type: Article

References (72)

1. Adamczewski, J. P., M. Rossignol, J.-P. Tassan, E. A. Nigg, V. Moncollin, and J. M. Egly. 1996. MAT1, cdk7 and cyclin H form a kinase complex which is UV light-sensitive upon association with TFIIH. EMBO J. 15:1877-1884.
2. Bargonetti, J., I. Reynisdottir, P. N. Friedman, and C. Prives. 1992. Site-specific binding of wild-type p53 to cellular DNA is inhibited by SV40 T antigen and mutant p53. Genes Dev. 6:1886-1898.
3. Bischoff, J. R., P. N. Friedman, D. R. Marshak, C. Prives, and D. Beach. 1990. Human p53 is phosphorylated by p60-cdc2 and cyclin B-cdc2. Proc. Natl. Acad. Sci. USA 87:4766-4770.
4. Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201:110-149.
5. Brown, A. J., T. Jones, and J. Shuttleworth. 1994. Expression and activity of p40MO15, the catalytic subunit of cdk-activating kinase, during Xenopus oogenesis and embryogenesis. Mol. Biol. Cell 5:921-932.
6. Casnellie, J. E. 1991. Assay of protein kinases using peptides with basic residues for phosphocellulose binding. Methods Enzymol. 200:115-127.
7. Cho, Y., S. Gorina, P. D. Jeffrey, and N. P. Pavletich. 1994. Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science 265:346-355.
8. Connell-Crowley, L., M. J. Solomon, N. Wei, and J. W. Harper. 1993. Phosphorylation independent activation of human cyclin-dependent kinase 2 by cyclin A in vitro. Mol. Biol. Cell 4:79-92.
9. Devault, A., A.-M. Martinez, D. Fesquet, J.-C. Labbe, N. Morin, J.-P. Tassan, E. A. Nigg, J.-C. Cavadore, and M. Doree. 1995. MAT1 ('menage a trois') a new RING finger protein subunit stabilizing cyclin H-cdk7 complexes in starfish and Xenopus CAK. EMBO J. 14:5027-5036.
10. Drapkin, R., J. T. Reardon, A. Ansari, J. C. Huang, L. Zawel, K. Ahn, A. Sancar, and D. Reinberg. 1994. Dual role of TFIIH in DNA repair and in transcription by RNA polymerasc II. Nature 368:769-772.
11. Dutta, A., J. M. Ruppert, J. C. Aster, and E. Winchester. 1993. Inhibition of DNA replication factor RPA by p53. Nature 365:79-82.
12. 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.
13. Farmer, G., J. Colgan, Y. Nakatani, J. L. Manley, and C. Prives. 1996. Functional interaction between p53, the TATA-binding protein (TBP), and TBP-associated factors in vivo. Mol. Biol. Cell 16:4295-4304.
14. Feaver, W. J., J. Q. Svejstrup, N. L. Henry, and R. D. Kornberg. 1994. Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/TFIIK. Cell 79:1103-1109.
15. Fesquet, D. 1993. The MO15 gene encodes the catalytic subunit of a protein kinase that activates cdc2 and other cyclin-dependent kinases (CDKs) through phosphorylation of Thr161 and its homologues. EMBO J. 12:3111-3121.
16. Fiscella, M., S. J. Ullrich, N. Zambriano, W. T. Shields, D. Liu, S. P. Lees-Miller, C. W. Anderson, W. E. Mercer, and E. Appella. 1993. Mutation of the serine 15 phosphorylation site of human p53 reduces the ability of p53 to inhibit cell cycle progression. Oncogene 8:1519-1528.
17. Fisher, R. P., P. Jin, H. M. Chamberlin, and D. O. Morgan. 1995. Alternative mechanisms of CAK assembly require an assembly factor or an activating kinase. Cell 83:47-57.
18. Ford, J. M., and P. C. Hanawalt. 1995. Li-Fraumeni syndrome fibroblasts homozygous for p53 mutations are deficient in global DNA repair but exhibit normal transcription-coupled repair and enhanced UV resistance. Proc. Natl. Acad. Sci. USA 92:8876-8880.
19. Friedlander, P., Y. Legros, T. Soussi, and C. Prives. 1996. Regulation of mutant p53 temperature-sensitive DNA binding. J. Biol. Chem. 271:25468-25478.
20. Gottlieb, T., and M. Oren. 1996. p53 in growth control and neoplasia. Biochim. Biophys. Acta 1287:77-102.
21. Havre, P. A., J. Yuan, L. Hedrick, K. R. Cho, and P. M. Glazer. 1995. p53 inactivation by HPV16 results in increased mutagenesis in human cells. Cancer Res. 55:4420-4424.
22. He, Z., B. T. Brinton, J. Greenblatt, J. A. Hassell, and C. J. Ingels. 1993. The transactivator proteins VP16 and GAL4 bind replication factor A. Cell 73:1223-1232.
23. Hupp, T. R., and D. P. Lane. 1994. Allosteric activation of latent p53 tetramers. Curr. Biol. 4:865-875.
24. Hupp, T. R., D. W. Meek, C. A. Midgley, and D. P. Lane. 1992. Regulation of the specific DNA binding function of p53. Cell 71:875-886.
25. Ishizaki, K., Y. Ejima, T. Matsunaga, R. Hara, A. Sakamoto, M. Ikenaga, Y. Ikawa, and S. I. Aizawa. 1994. Increased UV-induced SCEs but normal repair of DNA damage in p53-deficient mouse cells. Int. J. Cancer 57:254-257.
26. Jayaraman, L., E. Freulich, and C. Prives. Functional dissection of the p53 tumor suppressor protein. Methods Enzymol., in press.
27. Jayaraman, L., K. G. K. Murthy, C. Zhu, T. Curran, S. Xanthoudakis, and C. Prives. 1997. Identification of redox/repair protein Ref-1 as a potent activator of p53. Genes Dev. 11:558-570.
28. Jayaraman, L., and C. Prives. 1995. Activation of p53 sequence-specific DNA binding by short single strands of DNA requires the p53 C-terminus. Cell 81:1021-1029.
29. Kitagawa, M., H. Higashi, H.-K. Jung, I. Suzuki-Takahashi, M. Ikeda, K. Tamai, J.-Y. Kato, K. Segawa, E. Yoshida, S. Nishimura, and Y. Taya. 1996. The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J. 15:7060-7069.
30. Ko, L. J., and C. Prives. 1996. p53: puzzle and paradigm. Genes Dev. 10:1054-1072.
31. Kussie, P. H., S. Gorina, V. Marechal, B. Elenbaas, J. Moreau, A. J. Levine, and N. P. Pavletich. 1996. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 274:948-953.
32. Lee, S., B. Elenbaas, A. Levine, and J. Griffith. 1995. p53 and its 14 kDa C-terminal domain recognize primary DNA damage in the form of insertion/deletion mismatches. Cell 81:1013-1020.
33. Lees-Miller, S., K. Sakaguchi, S. Ullrich, E. Appella, and C. W. Anderson. 1992. Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell. Biol. 12:5041-5049.
34. Leveillard, T., L. Andera, N. Bissonnette, L. Schaeffer, L. Bracco, J.-M. Egly, and B. Wasylyk. 1996. Functional interactions between p53 and the TFIIH complex are affected by tumour-associated mutations. EMBO J. 15:1615-1624.
35. Levine, A. J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323-331.
36. Li, R., and M. R. Botchan. 1993. The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein A and stimulate in vitro BPV-1 DNA replication. Cell 73:1207-1221.
37. Lin, J., J. Chen, B. Elenbaas, and A. J. Levine. 1994. Several hydrophobic amino acids in the p53 amino-terminal domain are required for transcriptional activation, binding to mdm-2 and the adenovirus 5 E1B 55-kD protein. Genes Dev. 8:1235-1246.
38. II31 protein is a transcriptional coactivator of the p53 protein. Proc. Natl. Acad. Sci. USA 92:5154-5158.
39. 2 terminus of p53 facilitates transactivation. Cancer Res. 55:2410-2417.
40. Meek, D. 1994. Post-translational modification of p53. Semin. Cancer Biol. 5:203-210.
41. Meek, D. W., and W. Eckhart. 1988. Phosphorylation of p53 in normal and simian virus 40-transformed NIH 3T3 cells. Mol. Cell. Biol. 8:461-465.
42. Milne, D. M., L. E. Campbell, D. G. Campbell, and D. W. Meek. 1995. p53 is phosphorylated in vitro and in vivo by an ultraviolet radiation-induced protein kinase characteristic of the c-jun kinase, JNK1. J. Biol. Chem. 270: 5511-5518.
43. Milne, D. M., R. H. Palmer, D. G. Campbell, and D. W. Meek. 1992. Phosphorylation of the p53 tumor-suppressor protein at three N-terminal sites by a novel casein kinase I-like enzyme. Oncogenc 7:1361-1369.
44. Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131-134.
45. Pavletich, N. P., K. A. Chambers, and C. O. Pabo. 1993. The DNA-binding domain of p53 contains the four conserved regions and the major mutation hot spots. Genes Dev. 7:2556-2564.
46. Poon, R. Y. C., K. Yamashita, J. P. Adamczewski, T. Hunt, and J. Shuttleworth. 1993. The cdc2-related protein p40MO15 is the catalytic subunit of a protein kinase that can activate p33cdk2 and p34cdc2. EMBO J. 12:3123-3132.
47. Poon, R. Y. C., K. Yamashita, M. Howell, M. A. Ershler, A. Belyavsky, and T. Hunt. 1994. Cell cycle regulation of the p34cdc2/p33cdk2 activating kinase p40MO15. J. Cell Sci. 107:2789-2799.
48. Reardon, J. T., H. Ge, E. Gibbs, A. Sancar, J. Hurwitz, and Z.-Q. Pan. 1996. Isolation and characterization of two human transcription factor IIH (TFIIH)-related complexes: ERCC2/CAK and TFIIH*. Proc. Natl. Acad. Sci. USA 93:6482-6487.
49. Reed, M., B. Woelker, P. Wang, Y. Wang, M. E. Anderson, and P. Tegtmeyer. 1995. The C-terminal domain of p53 recognizes DNA damaged by ionizing radiation. Proc. Natl. Acad. Sci. USA 92:9455-9459.
50. Rossignol, M., I. Kolb-Cheynel, and J.-M. Egly. 1997. Substrate specificity of the cdk-activating kinase (CAK) is altered upon association with TFIIH. EMBO J. 16:1628-1637.
51. Roy, R., J. P. Adamczewski, T. Seroz, W. Vermeulen, J.-P. Tassan, L. Schaeffer, E. A. Nigg, J. H. J. Hoeijmakers, and J.-M. Egly. 1994. The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor. Cell 79:1093-1101.
52. Sands, A. T., M. B. Suraokar, A. Sanchez, J. E. Marth, L. A. Donehower, and A. Bradley. 1995. p53 deficiency does not affect the accumulation of point mutations in a transgene target. Proc. Natl. Acad. Sci. USA 92:8517-8521.
53. Scherr, C. J. 1994. G1 phase progression: cycling on cue. Cell 79:551-555.
54. Serizawa, H., T. P. Makela, J. W. Conaway, R. C. Conaway, R. A. Weinberg, and R. A. Young. 1995. Association of Cdk-activating kinase subunits with transcription factor TFIIH. Nature 374:280-282.
55. Seroz, T., J. R. Hwang, V. Moncollin, and J. M. Egly. 1995. TFIIH: a link between transcription, DNA repair and cell cycle regulation. Curr. Opin. Genet. Dev. 5:217-221.
56. Shiekhattar, R., F. Mermelstein, R. P. Fisher, R. Drapkin, B. Dynlacht, H. C. Wessling, D. O. Morgan, and D. Reinberg. 1995. Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature 374: 283-287.
57. Shuttleworth, J., R. Godfrey, and A. Colman. 1990. p40MO15, a cdc2-related protein kinase involved in negative regulation of meiotic maturation of Xenopus laevis oocytes. EMBO J. 9:3233-3240.
58. Smith, M. L., I.-T. Chen, Q. Zhan, P. M. O'Connor, and A. J. Fornace, Jr. 1995. Involvement of the p53 tumor suppressor in repair of u.v.-type DNA damage. Oncogene 10:1053-1059.
59. Solomon, M. J., W. J. Harper, and J. Shuttleworth. 1993. CAK, the p34cdc2 activating kinase, contains a protein identical to or closely related to p40MO15. EMBO J. 12:3133-3142.
60. Takenaka, I., F. Morin, B. R. Seizinger, and N. Kley. 1995. Regulation of the sequence-specific DNA binding function of p53 by protein kinase C and protein phosphatases. J. Biol. Chem. 270:5405-5411.
61. Tassan, J.-P., M. Jaquenoud, A. M. Fry, S. Frutiger, G. J. Hughes, and E. A. Nigg. 1995. In vitro assembly of a functional human CDK7-cyclin H complex requires MAT1, a novel 36 kDa RING finger protein. EMBO J. 14:5608-5617.
62. Tassan, J. P., S. J. Schultz, J. Bartek, and E. A. Nigg. 1994. Cell cycle analysis of the activity, subcellular localization, and subunit composition of human CAK (CDK-activating kinase). J. Cell Biol. 127:467-478.
63. Thut, C., J. L. Chen, R. Klemm, and R. Tjian. 1995. p53 transcriptional activation mediated by coactivators TAFII40 and TAFII60. Science 267:100-104.
64. Unger, T. Personal communication.
65. Wang, X. W., K. Forrester, H. Yeh, M. A. Feitelson, J.-R. Gu, and C. C. Harris. 1994. Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding, transcriptional activity, and association with transcription factor ERCC3. Proc. Natl. Acad. Sci. USA 91:2230-2234.
66. Wang, X. W., H. Yeh, L. Schaeffer, R. Roy, V. Moncollin, J.-M. Egly, Z. Wang, E. C. Friedberg, M. K. Evans, B. G. Taffe, V. A. Bohr, G. Weeda, J. H. J. Hoeijmakers, K. Forrester, and C. C. Harris. 1995. p53 modulation of TFIIH-associated nucleotide excision repair activity. Nature Genet. 10: 188-193.
67. Wang, Y., and C. Prives. 1995. Increased and altered DNA binding of human p53 by S and G2/M but not G1 cyclin-dependent kinases. Nature 376:88-91.
68. Wang, Z., J. Q. Svejstrup, W. J. Feaver, X. Wu, R. D. Kornberg, and E. C. Friedberg. 1994. Transcription factor b (TFIIH) is required during nucleotide excision repair in yeast. Nature 368:74-76.
69. Xiao, H., A. Pearson, B. Coulombe, R. Truant, S. Zhang, J. L. Regier, S. J. Triezenberg, D. Reinberg, O. Flores, C. J. Ingles, and J. Greenblatt. 1994. Binding of basal transcription factor TFIIH to the acidic activation domains of VP16 and p53. Mol. Cell. Biol. 14:7013-7024.
70. Yankulov, K. Y., and D. L. Bentley. 1997. Regulation of CDK7 substrate specificity by MAT1 and TFIIH. EMBO J. 16:1638-1646.
71. Yee, A., M. A. Nichols, L. Wu, F. L. Hall, R. Kobayashi, and Y. Xiong. 1995. Molecular cloning of CDK7-associated human MAT1, a cyclin-dependent kinase-activating kinase (CAK) assembly factor. Cancer Res. 55:6058-6062.
72. Zhang, W., C. McClain, J.-P. Gau, X.-Y. Guo, and A. B. Deisseroth. 1994. Hyperphosphorylation of p53 induced by okadaic acid attenuates its transcriptional activation function. Cancer Res. 54:4448-1453.