Endoplasmic reticulum stress induces p53 cytoplasmic localization and prevents p53-dependent apoptosis by a pathway involving glycogen synthase kinase-3β

Genes and Development

Volumn 18, Issue 3, 2004, Pages 261-277

  Qu, LiKe ^a   Huang, Shirley ^a   Baltzis, Dionissios ^a   Rivas Estilla, Ana Maria ^a   Pluquet, Olivier ^a   Hatzoglou, Maria ^b   Koumenis, Costas ^c   Taya, Yoichi ^d   Yoshimura, Akihiko ^e   Koromilas, Antonis E ^a  

^a MCGILL UNIVERSITY   (Canada)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

^d NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^e KYUSHU UNIVERSITY   (Japan)

Author keywords

Apoptosis; Endoplasmic reticulum stress; Glycogen synthase kinase 3 ; p53; Protein localization; Protein phosphorylation

Indexed keywords

ALANINE; GLYCOGEN SYNTHASE KINASE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN P53; SERINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL CYCLE; CONTROLLED STUDY; CYTOPLASM; DNA DAMAGE; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME BINDING; GENE INACTIVATION; GENETICS; HUMAN; HUMAN CELL; METABOLISM; MOUSE; MUTATION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; SIGNAL TRANSDUCTION; STRESS; TUMOR SUPPRESSOR GENE;

APOPTOSIS; CELL CYCLE; CELLS, CULTURED; CYTOPLASM; DNA DAMAGE; ENDOPLASMIC RETICULUM; GENES, P53; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASES; MUTATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 10744232627     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1165804     Document Type: Article

References (61)

1. Aloni-Grinstein, R., Zan-Bar, I., Alboum, I., Goldfinger, N., and Rotter, V. 1993. Wild type p53 functions as a control protein in the differentiation pathway of the B-cell lineage. Oncogene 8: 3297-3305.
2. Alt, J.R., Cleveland, J.L., Hannink, M., and Diehl, J.A. 2000. Phosphorylation-dependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes & Dev. 14: 3102-3114.
3. Appella, E. and Anderson, C.W. 2001. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. Biochem. 268: 2764-2772.
4. Aridor, M. and Balch, W.E. 1999. Integration of endoplasmic reticulum signaling in health and disease. Nat. Med. 5: 745-751.
5. Ashcroft, M., Taya, Y., and Vousden, K.H. 2000. Stress signals utilize multiple pathways to stabilize p53. Mol. Cell. Biol. 20: 3224-3233.
6. Bijur, G.N., De Sarno, P., and Jope, R.S. 2000. Glycogen synthase kinase-3β facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium. J. Biol. Chem. 275: 7583-7590.
7. Bischoff, J.R., Friedman, P.N., Marshak, D.R., Prives, C., and Beach, D. 1990. Human p53 is phosphorylated by p60-cdc2 and cyclin B-cdc2. Proc. Natl. Acad. Sci. 87: 4766-4770.
8. Blaydes, J.P., Luciani, M.G., Pospisilova, S., Ball, H.M., Vojtesek, B., and Hupp, T.R. 2001. Stoichiometric phosphorylation of human p53 at Ser315 stimulates p53-dependent transcription. J. Biol. Chem. 276: 4699-4708.
9. Bosari, S., Viale, G., Bossi, P., Maggioni, M., Coggi, G., Murray, J.J., and Lee, A.K. 1994. Cytoplasmic accumulation of p53 protein: An independent prognostic indicator in colorectal adenocarcinomas. J. Natl. Cancer Inst. 86: 681-687.
10. Boyd, S.D., Tsai, K.Y., and Jacks, T. 2000. An intact HDM2 RING-finger domain is required for nuclear exclusion of p53. Nat. Cell. Biol. 2: 563-568.
11. Brewer, J.W., Hendershot, L.M., Sherr, C.J., and Diehl, J.A. 1999. Mammalian unfolded protein response inhibits cyclin D1 translation and cell-cycle progression. Proc. Natl. Acad. Sci. 96: 8505-8510.
12. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., Brown, J.P., Sedivy, J.M., Kinzler, K.W., and Vogelstein, B. 1998. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501.
13. Bunz, F., Hwang, P.M., Torrance, C., Waldman, T., Zhang, Y., Dillehay, L., Williams, J., Lengauer, C., Kinzler, K.W., and Vogelstein, B. 1999. Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J. Clin. Invest. 104: 263-269.
14. Chernov, M.V., Bean, L.J., Lerner, N., and Stark, G.R. 2001. Regulation of ubiquitination and degradation of p53 in unstressed cells through C-terminal phosphorylation. J. Biol. Chem. 276: 31819-31824.
15. Cohen, P. and Frame, S. 2001. The renaissance of GSK3. Nat. Rev. Mol. Cell. Biol. 2: 769-776.
16. Cross, D.A., Culbert, A.A., Chalmers, K.A., Facci, L., Skaper, S.D., and Reith, A.D. 2001. Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death. J. Neurochem. 77: 94-102.
17. Cuddihy, A.R., Wong, A.H., Tam, N.W., Li, S., and Koromilas, A.E. 1999. The double-stranded RNA activated protein kinase PKR physically associates with the tumor suppressor p53 protein and phosphorylates human p53 on serine 392 in vitro. Oncogene 18: 2690-2702.
18. Diehl, J.A., Cheng, M., Roussel, M.F., and Sherr, C.J. 1998. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes & Dev. 12: 3499-3511.
19. Doble, B.W. and Woodgett, J.R. 2003. GSK-3: Tricks of the trade for a multi-tasking kinase. J. Cell. Sci. 116: 1175-1186.
20. Ferri, K. F. and Kroemer, G. 2001. Organelle-specific initiation of cell death pathways. Nat. Cell. Biol. 3: E255-E263.
21. Frame, S. and Cohen, P. 2001. GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359: 1-16.
22. Harding, H.P., Calfon, M., Urano, F., Novoa, I., and Ron, D. 2002. Transcriptional and translational control in the Mammalian unfolded protein response. Annu. Rev. Cell. Dev. Biol. 18: 575-599.
23. Hengstermann, A., Whitaker, N.J., Zimmer, D., Zentgraf, H., and Scheffner, M. 1998. Characterization of sequence elements involved in p53 stability regulation reveals cell type dependence for p53 degradation. Oncogene 17: 2933-2941.
24. Hetman, M., Cavanaugh, J.E., Kimelman, D., and Xia, Z. 2000. Role of glycogen synthase kinase-3β in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20: 2567-2574.
25. Hirao, A., Kong, Y.Y., Matsuoka, S., Wakeham, A., Ruland, J., Yoshida, H., Liu, D., Elledge, S.J., and Mak, T.W. 2000. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287: 1824-1827.
26. Hoeflich, K.P., Luo, J., Rubie, E.A., Tsao, M.S., Jin, O., and Woodgett, J.R. 2000. Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 406: 86-90.
27. Huang, S., Qu, L.K., Cuddihy, A.R., Ragheb, R., Taya, Y., and Koromilas, A.E. 2003. Protein kinase inhibitor 2-aminopurine overrides multiple genotoxic stress-induced cellular pathways to promote cell survival. Oncogene 22: 3721-3733.
28. Kaneko, Y. and Tsukamoto, A. 1995. Apoptosis and nuclear levels of p53 protein and proliferating cell nuclear antigen in human hepatoma cells cultured with tumor promoters. Cancer Lett. 91: 11-17.
29. Kaufman, R.J., Scheuner, D., Schroder, M., Shen, X., Lee, K., Liu, C.Y., and Arnold, S.M. 2002. The unfolded protein response in nutrient sensing and differentiation. Nat. Rev. Mol. Cell. Biol. 3: 411-421.
30. Klein, P.S. and Melton, D.A. 1996. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. 93: 8455-8459.
31. Lee, A.S. 2001. The glucose-regulated proteins: Stress induction and clinical applications. Trends Biochem. Sci. 26: 504-510.
32. Liang, S.H. and Clarke, M.F. 2001. Regulation of p53 localization. Eur. J. Biochem. 268: 2779-2783.
33. Lu, H., Fisher, R.P., Bailey, P., and Levine, A.J. 1997. The CDK7-cycH-p36 complex of transcription factor IIH phosphorylates p53, enhancing its sequence-specific DNA binding activity in vitro. Mol. Cell. Biol. 17: 5923-5934.
34. Matsuoka, S., Huang, M., and Elledge, S.J. 1998. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282: 1893-1897.
35. Michael, D. and Oren, M. 2002. The p53 and Mdm2 families in cancer. Curr. Opin. Genet. Dev. 12: 53-59.
36. Moll, U.M., Riou, G., and Levine, A.J. 1992. Two distinct mechanisms alter p53 in breast cancer: Mutation and nuclear exclusion. Proc. Natl. Acad. Sci. 89: 7262-7266.
37. Moll, U.M., LaQuaglia, M., Benard, J., and Riou, G. 1995. Wild-type p53 protein undergoes cytoplasmic sequestration in undifferentiated neuroblastomas but not in differentiated tumors. Proc. Natl. Acad. Sci. 92: 4407-4411.
38. Moll, U.M., Ostermeyer, A.G., Haladay, R., Winkfield, B., Frazier, M., and Zambetti, G. 1996. Cytoplasmic sequestration of wild-type p53 protein impairs the G1 checkpoint after DNA damage. Mol. Cell. Biol. 16: 1126-1137.
39. Nakamura, S., Roth, J.A., and Mukhopadhyay, T. 2000. Multiple lysine mutations in the C-terminal domain of p53 interfere with MDM2-dependent protein degradation and ubiquitination. Mol. Cell. Biol. 20: 9391-9398.
40. Rowan, S., Ludwig, R.L., Haupt, Y., Bates, S., Lu, X., Oren, M., and Vousden, K.H. 1996. Specific loss of apoptotic but not cell-cycle arrest function in a human tumor derived p53 mutant. EMBO J. 15: 827-838.
41. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
42. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., Gillespie, P., Saunders, T., Bonner-Weir, S., and Kaufman, R.J. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7: 1165-1176.
43. Schlamp, C.L., Poulsen, G.L., Nork, T.M., and Nickells, R.W. 1997. Nuclear exclusion of wild-type p53 in immortalized human retinoblastoma cells. J. Natl. Cancer Inst, 89: 1530-1536.
44. Sharpless, N.E. and DePinho, R.A. 2002. p53: Good cop/bad cop. Cell 110: 9-12.
45. Song, L., De Sarno, P., and Jope, R.S. 2002. Central role of glycogen synthase kinase-3β in endoplasmic reticulum stress-induced caspase-3 activation. J. Biol. Chem. 277: 44701-44708.
46. Spotts, G.D., Patel, S.V., Xiao, Q., and Hann, S.R. 1997. Identification of downstream-initiated c-Myc proteins which are dominant-negative inhibitors of transactivation by full-length c-Myc proteins. Mol. Cell. Biol. 17: 1459-1468.
47. Stambolic, V. and Woodgett, J.R. 1994. Mitogen inactivation of glycogen synthase kinase-3 β in intact cells via serine 9 phosphorylation. Biochem. J. 303: 701-704.
48. Stenmark-Askmalm, M., Stal, O., Sullivan, S., Ferraud, L., Sun, X.F., Carstensen, J., and Nordenskjold, B. 1994. Cellular accumulation of p53 protein: An independent prognostic factor in stage II breast cancer. Eur. J. Cancer 30A: 175-180.
49. Stommel, J.M., Marchenko, N.D., Jimenez, G.S., Moll, U.M., Hope, T.J., and Wahl, G.M. 1999. A leucine-rich nuclear export signal in the p53 tetramerization domain: Regulation of subcellular localization and p53 activity by NES masking. EMBO J. 18: 1660-1672.
50. Sun, X.F., Carstensen, J.M., Zhang, H., Stal, O., Wingren, S., Hatschek, T., and Nordenskjold, B. 1992. Prognostic significance of cytoplasmic p53 oncoprotein in colorectal adenocarcinoma. Lancet 340: 1369-1373.
51. Travers, K.J., Patil, C.K., Wodicka, L., Lockhart, D.J., Weissman, J.S., and Walter, P. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258.
52. Turenne, G.A. and Price, B.D. 2001. Glycogen synthase kinase3 β phosphorylates serine 33 of p53 and activates p53's transcriptional activity. BMC Cell Biol. 2: 12.
53. Uberti, D., Carsana, T., Bernardi, E., Rodella, L., Grigolato, P., Lanni, C., Racchi, M., Govoni, S., and Memo, M. 2002. Selective impairment of p53-mediated cell death in fibroblasts from sporadic Alzheimer's disease patients. J. Cell. Sci. 115: 3131-3138.
54. Ueda, H., Ullrich, S.J., Gangemi, J.D., Kappel, C.A., Ngo, L., Feitelson, M.A., and Jay, G. 1995. Functional inactivation but not structural mutation of p53 causes liver cancer. Nat. Genet. 9: 41-47.
55. Vousden, K.H. and Lu, X. 2002. Live or let die: The cell's response to p53. Nat. Rev. Cancer 2: 594-604.
56. Wahl, G.M. and Carr, A.M. 2001. The evolution of diverse biological responses to DNA damage: Insights from yeast and p53. Nat. Cell. Biol. 3: E277-E286.
57. Wang, Y. and Prives, C. 1995. Increased and altered DNA binding of human p53 by S and G2/M but not G1 cyclin-dependent kinases. Nature 376: 88-91.
58. Watcharasit, P., Bijur, G.N., Zmijewski, J.W., Song, L., Zmijewska, A., Chen, X., Johnson, G.V., and Jope, R.S. 2002. Direct, activating interaction between glycogen synthase kinase-3β and p53 after DNA damage. Proc. Natl. Acad. Sci. 99: 7951-7955.
59. Waterman, M.J., Stavridi, E.S., Waterman, J.L., and Halazonetis, T.D. 1998. ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat. Genet. 19: 175-178.
60. Wong, A.H., Tam, N.W., Yang, Y.L., Cuddihy, A.R., Li, S., Kirchhoff, S., Hauser, H., Decker, T., and Koromilas, A.E. 1997. Physical association between STAT1 and the interferon-inducible protein kinase PKR and implications for interferon and double-stranded RNA signaling pathways. EMBO J. 16: 1291-1304.
61. Zhang, Y. and Xiong, Y. 2001. A p53 amino-terminal nuclear export signal inhibited by DNA damage-induced phosphorylation. Science 292: 1910-1915.