Proteolytic cleavage of human p53 by calpain: A potential regulator of protein stability

Molecular and Cellular Biology

Volumn 17, Issue 1, 1997, Pages 460-468

  Kubbutat, Michael H G ^a   Vousden, Karen H ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; DNA CLEAVAGE; DNA DAMAGE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; PROTEIN SYNTHESIS REGULATION; PROTEIN TARGETING; SPINDLE CELL; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

HUMAN PAPILLOMAVIRUS;

EID: 0031014946     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.1.460     Document Type: Article

References (70)

1. Aloni-Grinstein, R., D. Schwartz, and V. Rotter. 1995. Accumulation of wild-type p53 protein upon γ-irradiation induces a G2 arrest-dependent immunoglobulin κ light chain gene expression. EMBO J. 14:1392-1401.
2. Atadja, P., H. Wong, I. Garkavtsev, C. Veillette, and K. Riabowol. 1995. Increased activity of p53 in senescing fibroblasts. Proc. Natl. Acad. Sci. USA 92:8348-8352.
3. Bachmair, A., D. Finley, and A. Varshavsky. 1986. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234:179-186.
4. Bartek, J., J. Bartkova, J. Lukas, Z. Staskova, B. Vojtesek, and D. P. Lane. 1993. Immunohistochemical analysis of the p53 oncoprotein on paraffin sections using a series of novel monoclonal antibodies. J. Pathol. 169:27-34.
5. Bates, S., and K. H. Vousden. 1996. p53 in signalling checkpoint arrest or apoptosis. Curr. Opin. Genet. Dev. 6:1-7.
6. Caelles, C., A. Helmberg, and M. Karin. 1994. p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 370: 220-223.
7. Carillo, S., M. Pariat, A.-M. Steff, I. Jariel-Encontre, F. Poulat, P. Berta, and M. Piechaczyk. 1996. PEST motifs arc not required for rapid calpain-mediated proteolysis of c-fos protein. Biochem. J. 313:245-251.
8. 1 arrest and apoptosis functions of the p53 tumor suppressor protein. Mol. Cell. Biol. 16:2445-2452.
9. Chowdary, D. R., J. J. Dermody, K. K. Jha, and H. L. Ozer. 1994. Accumulation of p53 in a mutant cell line defective in the ubiquitin pathway. Mol. Cell. Biol. 14:1997-2003.
10. Croall, D. E., and G. N. DeMartino. 1991. Calcium-activated neutral protease (calpain) system: structure, function, and regulation. Physiol. Rev. 71:813-847.
11. Crook, T., N. J. Marston, E. A. Sara, and K. H. Vousden. 1994. Transcriptional activation by p53 correlates with suppression of growth but not transformation. Cell 79:817-827.
12. Crook, T., J. A. Tidy, and K. H. Vousden. 1991. Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and transactivation. Cell 67:547-556.
13. Crook, T., and K. H. Vousden. 1992. Properties of p53 mutations detected in primary and secondary cervical cancers suggest mechanisms of metastasis and involvement of environmental carcinogens. EMBO J. 11:3935-3940.
14. Cross, S. M., C. A. Sanchez, C. A. Morgan, M. K. Schimke, S. Ramel, R. L. Idzerda, W. H. Raskind, and B. J. Reid. 1995. A p53-dependent mouse spindle checkpoint. Science 267:1353-1356.
15. Dameron, K. M., O. V. Volpert, M. A. Tainsky, and N. Bouck. 1994. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science 265:1582-1584.
16. 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.
17. Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. Montgomery, Jr., J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature 356: 215-221.
18. Feinstein, E., R. P. Gale, J. Reed, and E. Canaani. 1992. Expression of the normal p53 gene induces differentiation of K562 cells. Oncogene 7:1853-1857.
19. Figueiredo-Pereira, M. E., N. Banik, and S. Wilk. 1994. Comparison of the effect of calpain inhibitors on two extralysosomal proteinases: the multicatalytic proteinase complex and m-calpain. J. Neurochem. 62:1989-1994.
20. Fritsche, M., C. Haessler, and G. Brandner. 1993. Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene 8:307-318.
21. Fukasawa, K., T. Choi, R. Kuriyama, S. Rulong, and G. F. Vande Woude. 1996. Abnormal centrosome amplification in the absence of p53. Science 271:1744-1747.
22. Funk, W. D., D. T. Pak, R. H. Karas, W. E. Wright, and J. W. Shay. 1992. A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol. 12:2866-2871.
23. Goll, D. E., V. F. Thompson, R. G. Taylor, and T. Zalewska. 1992. Is calpain activity regulated by membranes and autolysis or by calcium and calpastatin? Bioessays 14:549-556.
24. Gopalakrishna, R., and S. H. Barsky. 1986. Hydrophobic association of calpains with subcellular organelles. Compartmentalization of calpains and the endogenous inhibitor calpastatin in tissues. J. Biol. Chem. 261:13936-13942.
25. 1-phase checkpoint by low-oxygen conditions is independent of p53 status. Mol. Cell. Biol. 14:6264-6277.
26. Haupt, Y., Y. Barak, and M. Oren. 1996. Cell type-specific inhibition of p53-mediated apoptosis by mdm2. EMBO J. 15:1596-1606.
27. Haupt, Y., A. Kazaz, R. Maya, and M. Oren. MDM2 promotes the rapid degradation of p53. Submitted for publication.
28. Haupt, Y., S. Rowan, E. Shaulian, K. H. Vousden, and M. Oren. 1995. Induction of apoptosis in HeLa cells by trans-activation deficient p53. Genes Dev. 9:2170-2183.
29. Hickman, E. S., S. M. Picksley, and K. H. Vousden. 1994. Cells expressing HPV16 E7 continue cell cycle progression following DNA damage induced p53 activation. Oncogene 9:2177-2181.
30. Hirai, S., H. Kawasaki, M. Yaniv, and K. Suzuki. 1991 Degradation of transcription factors, c-Jun and c-Fos, by calpain. FEBS Lett. 287:57-61.
31. Hollstein, M., K. Rice, M. S. Greenblatt, T. Soussi, R. Fuchs, T. Sørlie, E. Hovig, B. Smith-Sørensen, R. Montesano, and C. C. Harris. 1994. Database of p53 gene somatic mutations in human tumors and cell lines. Nucleic Acids Res. 22:3551-3555.
32. Hupp, T. R., A. Sparks, and D. P. Lane. 1995. Small peptides activate the latent sequence-specific DNA binding function of p53. Cell 83:237-245.
33. Jacks, T., L. Remington, B. O. Williams, E. M. Schmitt, S. Halachmi, R. T. Bronson, and R. A. Weinberg. 1994. Tumour spectrum analysis in p53-mutant mice. Curr. Biol. 4:1-7.
34. Kastan, M. B., O. Onyekwere, D. Sidransky, B. Vogelstein, and R. W. Craig. 1991. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304-6311.
35. Kern, S., K. Kinzler, A. Bruskin, D. Jarosz, P. Friedman, C. Prives, and B. Vogelstein. 1991. Identification of p53 as a sequence specific DNA binding protein. Science 252:1708-1711.
36. Kessis, T. D., R. J. Slebos, W. G. Nelson, M. B. Kastan, B. S. Plunkett, S. M. Han, A. T. Lorincz, L. Hedrick, and K. R. Cho. 1993. Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage. Proc. Natl. Acad. Sci. USA 90:3988-3992.
37. Kubbutat, M. H. G., and K. H. Vousden. Regulation of p53 stability by mdm2. Submitted for publication.
38. Legros, Y., A. Meyer, K. Ory, and T. Soussi. 1994. Mutations in p53 produce a common conformational effect that can be detected with a panel of monoclonal antibodies directed toward the central part of the p53 protein. Oncogene 9:3689-3694.
39. 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.
40. Linke, S. P., K. C. Clarkin, A. Di Leonardo, A. Tsou, and G. M. Wahl. 1996. A reversible, p53-dependent G0/G1 cell cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage. Genes Dev. 10:934-947.
41. Lu, X., and D. P. Lane. 1993. Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell 75:765-778.
42. Maki, C. G., J. Huibregtse, and P. M. Howley. 1996. In vivo ubiquitination and proteosome-mediated degradation of p53. Cancer Res. 56:2649-2654.
43. Maltzman, W., and L. Czyzyk. 1984. UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol. Cell. Biol. 4:1689-1694.
44. Marston, N. J. 1996. Ph.D. thesis. University of London, London, England.
45. Marston, N. J., T. Crook, and K. H. Vousden. 1994. Interaction of p53 with MDM2 is independent of E6 and does not mediate wild type transformation suppressor function. Oncogene 9:2707-2716.
46. Marston, N. J., J. R. Jenkins, and K. H. Vousden. 1995. Oligomerisation of full length p53 contributes to the interaction with mdm2 but not HPV E6. Oncogene 10:1709-1715.
47. Matlashewski, G. J., S. Tuck, D. Pim, P. Lamb, J. Schneider, and L. V. Crawford. 1987. Primary structure polymorphism at amino acid residue 72 of human p53. Mol. Cell. Biol. 7:961-963.
48. Meek, D. W. 1994. Post-translational modification of p53. Semin. Cancer Biol. 5:203-210.
49. Nakamura, M., M. Mori, Y. Morishita, S. Mori, and S. Kawashima. 1992. Specific increase in calcium-activated neutral protease with low calcium sensitivity (m-calpain) in proerythroblastic K562 cell line cells induced to differentiation by phorbol 12-myristate 13-acetate. Exp. Cell Res. 200:513-522.
50. Pietenpol, J. A., T. Tokino, S. Thiagaligam, W. EI-Deiry, K. W. Kinzler, and B. Vogelstein. 1994. Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc. Natl. Acad. Sci. USA 91:1998-2002.
51. Rock, K. L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A. L. Goldberg. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78:761-771.
52. Sabbatini, P., J. Lin, A. J. Levine, and E. White. 1995. Essential role for p53-mediated transcription in E1A-induced apoptosis. Genes Dev. 9:2184-2192.
53. Sarin, A., D. H. Adams, and P. A. Henkart. 1993. Protease inhibitors selectively block T-cell receptor-triggered programmed cell-death in a murine T-cell hybridoma and activated peripheral T-cells. J. Exp. Med. 178:1693-1700.
54. Scheffner, M., J. M. Huibregtse, R. D. Vierstra, and P. M. Howley. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505.
55. Scheffner, M., T. Takahashi, J. M. Huibregtse, J. D. Minna, and P. M. Howley. 1992. Interaction of the human papillomavirus type 16 oncoprotein with wild-type and mutant p53 proteins. J. Virol. 66:5100-5105.
56. 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.
57. Sibbet, G. J., and M. S. Campo. 1990. Multiple interactions between cellular factors and the non-coding region of human papillomavirus type 16. J. Gen. Virol. 71:2699-2707.
58. Squier, M. K., A. C. Miller, A. M. Malkinson, and J. J. Cohen. 1994. Calpain activation in apoptosis. J. Cell. Physiol. 159:229-237.
59. Stephen, C. W., P. Helminen, and D. P. Lane. 1995. Characterisation of epitopes of human p53 using phage-displayed peptide libraries: insights into antibody-peptide interactions. J. Mol. Biol. 248:58-78.
60. Unger, T., M. M. Nau, S. Segal, and J. D. Minna. 1992. p53: a transdominant regulator of transcription whose function is ablated by mutations occurring in human cancer. EMBO J. 11:1383-1390.
61. Varshavsky, A. 1992. The N-end rule. Cell 69:725-735.
62. Vojtesek, B., and D. P. Lane. 1993. Regulation of p53 protein expression in human breast cancer cell lines. J. Cell Sci. 105:607-612.
63. waf1/cip1. Genes Dev. 8:2817-2830.
64. Watanabe, N., G. F. Vande Woude, Y. Ikawa, and N. Sagata. 1989. Specific proteolysis of the c-mos proto-oncogene product by calpain on fertilization of Xenopus eggs. Nature 342:505-511.
65. Watt, F., and P. L. Molloy. 1993. Specific cleavage of transcription factors by the thiol protease, m-calpain. Nucleic Acids Res. 21:5092-5100.
66. Wrede, D., J. A. Tidy, T. Crook, D. Lane, and K. H. Vousden. 1991. Expression of RB and p53 proteins in HPV-positive and HPV-negative cervical carcinoma cell lines. Mol. Carcinog. 4:171-175.
67. Yonish-Rouach, E., V. Deguin, T. Zaitchouk, C. Breugnot, Z. Mishal, J. R. Jenkins, and E. May. 1996. Transcriptional activation plays a role in the induction of apoptosis by transiently transfected wild-type p53. Oncogene 12:2197-2205.
68. Zambetti, G. P., and A. J. Levine. 1993. A comparison of the biological activities of wild-type and mutant p53. FASEB J. 7:855-865.
69. Zhan, Q. M., F. Carrier, and A. J. Fornace. 1993. Induction of cellular p53 activity by DNA-damaging agents and growth arrest. Mol. Cell. Biol. 13: 4242-4250.
70. Zhu, W., P. E. Murtha, and C. Y. F. Young. 1995. Calpain inhibitor-induced apoptosis in human prostate adenocarcinoma cells. Biochem. Biophys. Res. Commun. 214:1130-1137.