Hsp7O exerts its anti-apoptotic function downstream of caspase-3-like proteases

EMBO Journal

Volumn 17, Issue 21, 1998, Pages 6124-6134

  Jäättelä, Marja ^a   Wissing, Dorte ^a   Kokholm, Klaus ^a   Kallunki, Tuula ^a   Egeblad, Mikala ^a  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

Author keywords

Apoptosis; cPLA2; JNK; Mitochondrial; TNF

Indexed keywords

CYSTEINE PROTEINASE; CYTOCHROME C; DOXORUBICIN; FREE RADICAL; HEAT SHOCK PROTEIN 70; PHOSPHOLIPASE A2; PROTEIN KINASE; STAUROSPORINE; TUMOR NECROSIS FACTOR; ACETYL ASPARTYL GLUTAMYL VALYL ASPARTAL; ACETYL-ASPARTYL-GLUTAMYL-VALYL-ASPARTAL; ANTISENSE OLIGONUCLEOTIDE; CASP3 PROTEIN, HUMAN; CASPASE; CASPASE 3; MITOGEN ACTIVATED PROTEIN KINASE; OLIGOPEPTIDE; PHOSPHOLIPASE A; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEINASE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL LINE; CELL CULTURE; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; MITOCHONDRION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

APOPTOSIS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CASPASE 3; CASPASES; CELL SURVIVAL; CYTOCHROME C GROUP; DOXORUBICIN; ENDOPEPTIDASES; FREE RADICALS; GENE EXPRESSION REGULATION; HSP70 HEAT-SHOCK PROTEINS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; OLIGONUCLEOTIDES, ANTISENSE; OLIGOPEPTIDES; PHOSPHOLIPASES A; SIGNAL TRANSDUCTION; STAUROSPORINE; TRANSFECTION; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0032476668     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.21.6124     Document Type: Article

References (54)

1. Beyaer, R., Kidd, V.J., Cornelius, S., Van de Craen, M., Denecker, G., Lahti, M., Gururajan, R., Vandenabeele, P. and Fiers, W. (1997) Cleavage of PITSLRE kinases by ICE/CASP-1 and CPP32/CASP-3 during apoptosis induced by tumor necrosis factor. J. Biol. Chem., 272, 11694-11697.
2. Boise, L.H., González-García, M., Postema, C.E., Ding, L., Lindsten, T., Turka, L.A., Mao, X., Nuñez, G. and Thomson, G.B. (1993) Bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell, 744, 597-608.
3. Bossy-Wetzel, E., Newmeyer, D.D. and Green, D.R. (1998) Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J., 17, 37-49.
4. Cardone, M.H., Salvesen, G.S., Widmann, C., Johnson, G. and Frisch, S.M. (1997) The regulation of anoikis: MEKK-1 activation requires cleavage by caspases. Cell 90, 315-323.
5. Ciocca, D.R., Clark, G.M., Tandon, A.K., Fuqua, S.A., Welch, W.J. and McGuire, W.L. (1993) Heat shock protein hsp70 in patients with axillary lymph node-negative breast cancer: prognostic implications. J. Natl Cancer Inst., 85, 570-574.
6. Deveraux, Q.L., Takahashi, R., Salvesen, G.S. and Reed, J.C. (1997) X-linked IAP is a direct inhibitor of cell-death proteases. Nature, 388, 300-304.
7. Ferrarini, M., Heltai, S., Zucchi, M.R. and Rugarli, C. (1993) Unusual expression and localization of heat-shock proteins in human tumor cells. Int. J. Cancer, 51, 613-619.
8. Ghayur, T. et al. (1996) Proteolytic activation of protein kinase C δ by ICE/CED 3-like protease induces characteristics of apoptosis. J. Exp. Med., 184, 2399-2404.
9. Graves, J.D., Gotoh, Y., Draves, K.E., Ambrose, D., Han, D.K.M., Wright, M., Chernoff, J., Clark, E.A. and Krebs, E.G. (1998) Caspase-mediated activation and induction of apoptosis by the mammalian Ste20-like kinase Mst1. EMBO J., 17, 2224-2234.
10. Hibi, M., Lin, A., Smeal, T., Minden, A. and Karin, M. (1993) Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev., 7, 2135-2148.
11. 2. J. Immunol., 151, 4286-4294.
12. Jäättelä, M. (1995) Overexpression of hsp70 confers tumorigenicity to mouse fibrosarcoma cells. Int. J. Cancer, 60, 689-693.
13. Jäättelä, M. and Wissing, D. (1993) Heat shock proteins protect cells from monocyte cytotoxicity: possible mechanism of self-protection. J. Exp. Med., 177, 231-236.
14. Jäättelä, M., Saksela, K. and Saksela, E. (1989) Heat shock protects WEHI-164 target cells from the cytolysis by tumor necrosis factors α and α. Eur. J. Immunol., 19, 1413-1417.
15. Jäättelä, M., Wissing, D., Bauer, P.A. and Li, G.C. (1992) Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J., 11, 3507-3512.
16. 2 in breast carcinoma cells. Oncogene, 10, 2297-2305.
17. Jonston, R.N. and Kucey, B.L. (1988) Competitive inhibition of hsp70 gene expression causes thermosensitivity. Science. 242, 1551-1554.
18. Kallunki, T., Su, B., Tsigelny, I., Sluss, H.K., Derijard, B., Moore, G., Davis, R. and Karin, M. (1994) JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation. Genes Dev., 8, 2996-3007.
19. Karlseder, J., Wissing, D., Holzer, G., Orel, L., Sliutz, G., Auer, H., Jäättelä, M. and Simon, M.M. (1996) Hsp70 Overexpression mediates the escape of a doxorubicin induced G2 cell cycle arrest. Biochem. Biophys. Res. Commun., 220, 153-159.
20. Kaur, J. and Ralhan, R. (1995) Differential expression of 70-kDa heat shock protein in human oral tumorigenesis. Int. J. Cancer, 63, 774-779.
21. Kerr, J.F.R., Wyllie, A.H. and Currie, A.R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer, 26, 239-257.
22. Kerr, J.F.R., Winterford, C.M. and Harmon, B.V. (1994) Apoptosis. Its significance in cancer and cancer therapy. Cancer, 73, 2013-2026.
23. Kluck, R.M., Bossy-Wetzel, E., Green, D.R. and Newmeyer, D.D. (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science, 275, 1132-1136.
24. Lazebnik, Y.A., Kaufmann, S.H., Desnoyers, S., Poirier, G.G. and Earnshaw, W.C. (1994) Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature, 371, 346-347.
25. Lee, N., MacDonald, H., Reinhard, C., Halenbeck, R., Roulston, A., Shi, T. and Williams, L.T. (1997) Activation of hPAK65 by caspase cleavage induces some of the morphological and biochemical changes of apoptosis. Proc. Natl Acad. Sci. USA, 94, 13642-13647.
26. Li, G.C. and Werb, Z. (1982) Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. Proc. Natl Acad. Sci. USA, 79, 3218-3222.
27. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemeri, E.S. and Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates apoptotic protease cascade. Cell, 91, 479-489.
28. Liu, X., Kim, C.N., Yang, J., Jemmerson, R. and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell, 86, 147-157.
29. Liu, X., Zou, C., Slaughter, C. and Wang, X. (1997) DFF, a heteromeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell, 89, 175-184.
30. Liu, Z.-G., Hsu, H., Goeddel, D.V. and Karin, M. (1996) Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kB activation prevents cell death. Cell, 87, 565-576.
31. Milarski, K.L. and Morimoto, R.I. (1986) Expression of human HSP70 during synthetic phase of the cell cycle. Proc. Natl Acad. Sci. USA, 83, 9517-9521.
32. r 70, 000 heat shock genes in control or heat shock leukemic cells as correlated to their heat response. Cancer Res., 50, 2877-2884.
33. Mosser, D.D., Caron, A.W., Bourget, L., Denis-Larose, C. and Massie, B. (1997) Role of human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol., 17, 5317-5327.
34. Nagata, S. (1997) Apoptosis by death factor. Cell, 88, 355-365.
35. Natoli, G., Costanzo, A., Ianni, A., Templeton, D.J., Woodgett, J.R., Balsano, C. and Levrero, M. (1997) Activation of SAPK/JNK by TNF receptor through a noncytotoxic TRAF2-dependent pathway. Science, 275, 200-203.
36. Polla, B.S., Kantengwa, S., François, D., Salvioli, S., Franceschi, C., Marsac, C. and Cossarizza, A. (1996) Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc. Natl Acad. Sci. USA, 93, 6458-6463.
37. Riabolow, K.T., Mizzen, L.A. and Welch, W.J. (1988) Heat shock is lethal to fibroblasts microinjected with antibodies against hsp70. Science, 242, 433-436.
38. Rothe, M., Pan, M.-G., Henzel, W.J., Ayers, T.M. and Goeddel, D.V. (1995) The TNFR2-TRAF signaling complex contains two novel proteins related to baculovirus inhibitor of apoptosis proteins. Cell, 83, 1243-1252.
39. Saksela, K. and Baltimore, D. (1993) Negative regulation of immunoglobulin kappa light-chain gene transcription by a short sequence homologous to the murine B1 repetitive element, Mol. Cell. Biol., 13, 3698-3705.
40. Seo, J.S., Park, Y.M., Kim, J.I., Shim, E.H., Kim, C.W., Jang, J.J., Kim, S.H. and Lee, W.H. (1996) T cell lymphoma in transgenic mice expressing the human hsp70 gene. Biochem. Biophys. Res. Commun., 218, 582-587.
41. Shimizu, S., Eguchi, Y. Kamiike, W., Waguri, S., Uchiyama, Y., Matsuda, H. and Tsujimoto, Y. (1996) Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene, 13, 21-29.
42. Simon, M.M., Krone, C., Schwarz, A., Luger, T.A., Jäättelä, M. and Schwarz, T. (1995) Heat shock protein 70 overexpression affects the response to ultraviolet light in murine fibroblasts. Evidence for increased cell viability and suppression of cytokine release. J. Clin. Invest., 95, 926-933.
43. Susin, S.A., Zamzami, N., Castedo, M., Daugas, E., Wang, H.-G., Geley, S., Fassy, F., Reed, J.C. and Kroemer, J.C. (1997) The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis. J. Exp. Med., 186, 25-37.
44. Tewari, M. and Dixit, V.M. (1995) Fas- and tumor necrosis factor-induced apoptosis is inhibited by pox virus crmA gene product. J. Biol. Chem., 270, 3255-3260.
45. Tewari, M., Quan, L.T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D.R., Poirien, G.G., Salvesen, G.S. and Dixit, V.M. (1995) Yama/CPP32β, a mammalian homolog of CED-3, is a crmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell, 81, 801-809.
46. Vaux, D.L., Cory, S. and Adams, J.M. (1988) Bcl-2 gene promotes haemopoetic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature, 335, 440-442.
47. Verheij, M. et al. (1996) Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature, 380, 75-79.
48. White, E. (1996) Life, death and the pursuit of apoptosis. Genes Dev., 10, 1-15.
49. Wissing, D., Mouritzen, H., Egeblad, M., Poirier, G.G. and Jäättelä, M. (1997) Involvement of caspase-dependent activation of cytosolic phospholipase A2 in tumor necrosis factor-induced apoptosis. Proc. Natl Acad. Sci. USA, 94, 5073-5077.
50. Wissing, D., Mouritzen, H. and Jäättelä, M. (1998) TNF-induced mitochondrial changes and activation of apoptotic proteases are inhibited by A20. Free Radical Biol. Med, . 25, 57-65.
51. Woo, M. et al. (1998) Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes. Genes Dev., 12, 806-819.
52. Xia, Z., Dickens, M., Reingeaud, J., Davis, R.J. and Greenberg, M.E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science, 270, 1326-1331.
53. Yang, J., Liu, X., Bhalla, K., Kim, C.N., Ibrado, A.M., Cai, J., Peng.T.-I., Jones, D.P. and Wang, X. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria is blocked. Science, 275, 1129-1132.
54. Zamzami, N. et al. (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med., 182, 367-377.