Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome

Nature Cell Biology - Tập 2 Số 8 - Trang 469-475 - 2000
Helen M. Beere1, Beni B. Wolf1, Kelvin Cain2, Dick D. Mosser3, Artin Mahboubi1, Tomomi Kuwana1, Pankaj Tailor4, Richard I. Morimoto5, Gerald M. Cohen2, Douglas R. Green1
1La Jolla Institute for Allergy and Immunology, 10355 Science Center Drive, San Diego, 92121, USA, California
2MRC Toxicology Unit, Hodgkin Building, University of Leicester, Lancaster Road, Leicester LE1 9HN, UK
3Biotechnology Research Institute, National Research Council of Canada, Montreal,, H4P 2R2, Quebec, Canada
4Department of Biochemistry, McGill University, McIntyre Medical Building, 3655 Drummond Street, Montreal, H3G 1YG, Quebec, Canada
5Department of Biochemistry, Molecular Biology and Cell Biology, Northwestern University, 2153 North Campus Drive, Evanston, 60208, Illinois , USA

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Tài liệu tham khảo

Wolf, B. & Green, D. R. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J. Biol. Chem. 274, 20049–20052 (1999).

Liu, X., Kim, C. N., Yang, J., Jemmerson, R. & Wang, X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86, 147–157 (1996).

Zou, H., Henzel, W. J., Liu, X., Lutschg, A. & Wang, X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90, 405–413 (1997).

Srinivasula, S. M., Ahmad, M., Fernandes-Alnemri, T. & Alnemri, E. S. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell 1, 949–957 (1998).

Zou, H., Li, Y., Liu, X. & Wang, X. An APAF-1 cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274, 11549–11556 (1999).

Cain, K. et al. Apaf-1 oligomerizes into biologically active ~700-kDa and inactive ~1.4-MDa apoptosome complexes. J. Biol. Chem. 275, 6067–6070 (2000).

Cain, K., Brown, D. G., Langlais, C. & Cohen, G. M. Caspase activation involves the formation of the aposome, a large (~700 kDa) caspase-activating complex. J. Biol. Chem. 274, 22686–22692 (1999).

Hu, Y., Benedict, M. A., Ding, L. & Nunez, G. Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1-mediated caspase- 9 activation and apoptosis. EMBO J. 18, 3586–3595 (1999).

Lindquist, S. & Craig, E. A. The heat-shock proteins. Annu. Rev. Genet. 22, 631–677 (1988).

Gething, M. J. & Sambrook, J. Protein folding in the cell. Nature 355, 33–45 (1992).

Parsell, D. A., Taulien, J. & Lindquist, S. The role of heat-shock proteins in thermotolerance. Phil. Trans. R. Soc. Lond. B 339, 279–285 (1993).

Parsell, D. A. & Lindquist, S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27, 437–496 (1993).

Milarski, K. L. & Morimoto, R. I. Expression of human HSP70 during the synthetic phase of the cell cycle. Proc. Natl Acad. Sci. USA 83, 9517–9521 (1986).

Samali, A. & Orrenius, S. Heat shock proteins: regulators of stress response and apoptosis. Cell Stress Chaperones 3, 228–236 (1998).

Jaattela, M. Escaping cell death: survival proteins in cancer. Exp. Cell Res. 248, 30–43 (1999).

Freeman, B. C., Myers, M. P., Schumacher, R. & Morimoto, R. I. Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1. EMBO J. 14, 2281–2292 (1995).

Kluck, R. M., Bossy-Wetzel, E., Green, D. R. & Newmeyer, D. D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132–1136 (1997).

Li, P. et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479–489 (1997).

Stennicke, H. R. et al. Caspase-9 can be activated without proteolytic processing. J. Biol. Chem. 274, 8359–8362 (1999).

Benedict, M. A., Hu, Y., Inohara, N. & Nunez, G. Expression and functional analysis of Apaf-1 isoforms. Extra WD-40 repeat is required for cytochrome c binding and regulated activation of procaspase-9. J. Biol. Chem. 275, 8461–8468 (2000).

Hahn, G. M. & Li, G. C. Thermotolerance and heat shock proteins in mammalian cells. Radiat. Res. 92, 452–457 (1982).

Mosser, D. D. & Martin, L. H. Induced thermotolerance to apoptosis in a human T lymphocyte cell line. J. Cell Physiol. 151, 561–570 (1992).

Mosser, D. D., Caron, A. W., Bourget, L., Denis-Larose, C. & Massie, B. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell Biol. 17, 5317–5327 (1997).

Samali, A. & Cotter, T. G. Heat shock proteins increase resistance to apoptosis. Exp. Cell Res. 223, 163–170 (1996).

Simon, M. M. et al. 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 (1995).

Jaattela, M., Wissing, D., Bauer, P. A. & Li, G. C. Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J. 11, 3507–3512 (1992).

Liossis, S. N., Ding, X. Z., Kiang, J. G. & Tsokos, G. C. Overexpression of the heat shock protein 70 enhances the TCR/CD 3- and Fas/Apo-1/CD 95-mediated apoptotic cell death in Jurkat T cells. J. Immunol. 158, 5668–5675 (1997).

Creagh, E. M. & Cotter, T. G. Selective protection by hsp70 against cytotoxic drug-, but not Fas- induced T-cell apoptosis. Immunology 97, 36–44 (1999).

Mehlen, P., Schulze-Osthoff, K. & Arrigo, A. P. Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J. Biol. Chem. 271, 16510–16514 (1996).

Li, C-Y., Lee, J-S., Ko, Y-G., Kim, J-I., & Seo, J-S. Hsp70 inhibits apoptosis downstream of cytochrome c release and upstream of caspase-3 activation. J. Biol. Chem. (in the press).

Jaattela, M., Wissing, D., Kokholm, K., Kallunki, T. & Egeblad, M. Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J. 17, 6124–6134 (1998).

Gabai, V. L. et al. Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J. Biol. Chem. 272, 18033–18037 (1997).

Patriarca, E. J. & Maresca, B. Acquired thermotolerance following heat shock protein synthesis prevents impairment of mitochondrial ATPase activity at elevated temperatures in Saccharomyces cerevisiae. Exp. Cell. Res. 190, 57–64 (1990).

Polla, B. S. et al. Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc. Natl Acad. Sci. USA 93, 6458–6463 (1996).

Evan, G.I. et al. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69, 119–128 (1992).

Juin, P., Hueber, A. O., Littlewood, T. & Evan, G. c-Myc-induced sensitization to apoptosis is mediated through cytochrome c release. Genes Dev. 13, 1367–1381 (1999).

Cecconi, F., Alvarez-Bolado, G., Meyer, B. I., Roth, K. A. & Gruss, P. Apaf-1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94, 727–737 (1998).

Yoshida, H. et al. Apaf-1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94, 739–750 (1998).

Soengas, M. S. et al. Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition. Science 284, 156–159 (1999).

Xanthoudakis, S. et al. Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J. 18, 2049–2056 (1999).

Wolf, B., Schuler, M., Echeverri, F. & Green, D. R. Caspase-3 is the primary activator of apoptotic DNA fragmentation via DFF 45/ICAD inactivation. J. Biol. Chem. 274, 30651–30656 (1999).

Rodriguez, J. & Lazebnik, Y. Caspase-9 and APAF-1 form an active holoenzyme. Genes Dev. 13, 3179–3184 (1999).

Wolf, B.B. et al. Calpain functions in a caspase-independent manner to promote apoptosis-like events during platelet activation. Blood 94, 1683–1692 (1999).