The Chaperone Function of hsp70 Is Required for Protection against Stress-Induced Apoptosis

REFERENCES

• Beere, H. M., Wolf, B. B., Cain, K., Mosser, D. D., Mahboubi, A., Kuwana, T., Taylor, P., Morimoto, R. I., Cohen, G., and Green, D. R.. 2000. Heat shock protein 70 (HSP70) inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat. Cell Biol. 2:469–475
   PubMed Web of Science ®Google Scholar
• Bornman, L., Steinmann, C. M., Gericke, G. S., and Polla, B. S.. 1998. In vivo heat shock protects rat myocardial mitochondria. Biochem. Biophys. Res. Commun. 246:836–840
   PubMedGoogle Scholar
• Brar, B. K., Stephanou, A., Wagstaff, M. J., Coffin, R. S., Marber, M. S., Engelmann, G., and Latchman, D. S.. 1999. Heat shock proteins delivered with a virus vector can protect cardiac cells against apoptosis as well as against thermal or hypoxic stress. J. Mol. Cell. Cardiol. 31:135–146
   PubMed Web of Science ®Google Scholar
• Bukau, B., and Horwich, A. L.. 1998. The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366
   PubMed Web of Science ®Google Scholar
• Buzzard, K. A., Giaccia, A. J., Killender, M., and Anderson, R. L.. 1998. Heat shock protein 72 modulates pathways of stress-induced apoptosis. J. Biol. Chem. 273:17147–17153
   PubMedGoogle Scholar
• Caron, A. W., Massie B., and Mosser D. D.. Use of a micromanipulator for high-efficiency cloning of cells co-expressing fluorescent proteins. Methods Cell Sci., in press.
   Google Scholar
• Chen, Y. R., Wang, X., Templeton, D., Davis, R. J., and Tan, T. H.. 1996. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and gamma radiation. Duration of JNK activation may determine cell death and proliferation. J. Biol. Chem. 271:31929–31936
   PubMed Web of Science ®Google Scholar
• Demand, J., Lüders, J., and Höhfeld, J.. 1998. The carboxy-terminal domain of Hsc70 provides binding sites for a distinct set of chaperone cofactors. Mol. Cell. Biol. 18:2023–2028
   PubMed Web of Science ®Google Scholar
• El-Wadawi, R., and Bowler, K.. 1995. The development of thermotolerance protects blowfly flight muscle mitochondrial function from heat damage. J. Exp. Biol. 198:2413–2421
   PubMedGoogle Scholar
• Feder, J. H., Rossi, J. M., Solomon, J., Solomon, N., and Lindquist, S.. 1992. The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev. 6:1402–1413
   PubMed Web of Science ®Google Scholar
• Freeman, B. C., Myers, M. P., Schumacher, R., and Morimoto, R. I.. 1995. Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1. EMBO J. 14:2281–2292
   PubMed Web of Science ®Google Scholar
• Gabai, V. L., Meriin, A. B., Mosser, D. D., Caron, A. W., Rits, S., Shifrin, V. I., and Sherman, M. Y.. 1997. Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J. Biol. Chem. 272:18033–18037
   PubMed Web of Science ®Google Scholar
• Gabai, V. L., Meriin, A. B., Yaglom, J. A., Volloch, V. Z., and Sherman, M. Y.. 1998. Role of Hsp70 in regulation of stress-kinase JNK: implications in apoptosis and aging. FEBS Lett. 438:1–4
   PubMed Web of Science ®Google Scholar
• Goldstein, J. C., Waterhouse, N. J., Juin, P., Evan, G. I., and Green, D. R.. 2000. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat. Cell Biol. 2:156–162
   PubMed Web of Science ®Google Scholar
• Gossen, M., Freundlieb, S., Bender, G., Müller, G., Hillen, W., and Bujard, H.. 1995. Transcriptional activation by tetracyclines in mammalian cells. Science 268:1766–1769
   PubMed Web of Science ®Google Scholar
• Green, D. R., and Reed, J. C.. 1998. Mitochondria and apoptosis. Science 281:1309–1312
   PubMed Web of Science ®Google Scholar
• Gross, A., McDonnell, J. M., and Korsmeyer, S. J.. 1999. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1899–1911
   PubMed Web of Science ®Google Scholar
• Hartl, F. U.. 1996. Molecular chaperones in cellular protein folding. Nature 381:571–579
   PubMed Web of Science ®Google Scholar
• Ip, Y. T., and Davis, R. J.. 1998. Signal transduction by the c-Jun N-terminal kinase (JNK)—from inflammation to development. Curr. Opin. Cell Biol. 10:205–219
   PubMed Web of Science ®Google Scholar
• Jäättelä, M.. 1995. Over-expression of hsp70 confers tumorigenicity to mouse fibrosarcoma cells. Int. J. Cancer. 60:689–693
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Jäättelä, M., Wissing, D., Kokholm, K., Kallunki, T., and Egeblad, M.. 1998. Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J. 17:6124–6134
   PubMed Web of Science ®Google Scholar
• Kim, D., Ouyang, H., and Li, G. C.. 1995. Heat shock protein hsp70 accelerates the recovery of heat-shocked mammalian cells through its modulation of heat shock transcription factor HSF1. Proc. Natl. Acad. Sci. USA 92:2126–2130
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Kwak, H. J., Jun, C. D., Pae, H. O., Yoo, J. C., Park, Y. C., Choi, B. M., Na, Y. G., Park, R. K., Chung, H. T., Chung, H. Y., Park, W. Y., and Seo, J. S.. 1998. The role of inducible 70-kDa heat shock protein in cell cycle control, differentiation, and apoptotic cell death of the human myeloid leukemic HL-60 cells. Cell. Immunol. 187:1–12
   PubMed Web of Science ®Google Scholar
• Kyriakis, J. M., and Avruch, J.. 1996. Protein kinase cascades activated by stress and inflammatory cytokines. Bioessays 18:567–577
   PubMed Web of Science ®Google Scholar
• Landry, J., Chrétien, P., Lambert, H., Hickey, E., and Weber, L. A.. 1989. Heat shock resistance conferred by expression of the HSP27 gene in rodent cells. J. Cell Biol. 109:7–15
   PubMed Web of Science ®Google Scholar
• Lee, W. H., Park, Y. M., Kim, J. I., Park, W. Y., Kim, S. H., Jang, J. J., and Seo, J. S.. 1998. Expression of heat shock protein 70 blocks thymic differentiation of T cells in transgenic mice. Immunology 95:559–565
   PubMedGoogle Scholar
• Li, C. Y., Lee J. S., Ko Y. G., Kim J. I., and Seo J. S.. Hsp70 inhibits apoptosis downstream of cytochrome c release and upstream of caspase-3 activation. J. Biol. Chem., in press.
   Google Scholar
• Li, G. C., Li, L., Liu, R. Y., Rehman, M., and Lee, W. M.. 1992. Heat shock protein hsp70 protects cells from thermal stress even after deletion of its ATP-binding domain. Proc. Natl. Acad. Sci. USA 89:2036–2040
   PubMed Web of Science ®Google Scholar
• Li, G. C., Li, L. G., Liu, Y. K., Mak, J. Y., Chen, L. L., and Lee, W. M.. 1991. Thermal response of rat fibroblasts stably transfected with the human 70-kDa heat shock protein-encoding gene. Proc. Natl. Acad. Sci. USA 88:1681–1685
   PubMed Web of Science ®Google Scholar
• Li, L., Shen, G., and Li, G. C.. 1995. Effects of expressing human Hsp70 and its deletion derivatives on heat killing and on RNA and protein synthesis. Exp. Cell Res. 217:460–468
   PubMedGoogle Scholar
• Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X.. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479–489
   PubMed Web of Science ®Google Scholar
• Liossis, S. N., Ding, X. Z., Kiang, J. G., and Tsokos, G. C.. 1997. Overexpression of the heat shock protein 70 enhances the TCR/CD3- and Fas/Apo-1/CD95-mediated apoptotic cell death in Jurkat T cells. J. Immunol. 158:5668–5675
   PubMedGoogle Scholar
• Maheswaran, S., Englert, C., Zheng, G., Lee, S. B., Wong, J., Harkin, D. P., Bean, J., Ezzell, R., Garvin, A. J., McCluskey, R. T., DeCaprio, J. A., and Haber, D. A.. 1998. Inhibition of cellular proliferation by the Wilms tumor suppressor WT1 requires association with the inducible chaperone Hsp70. Genes Dev. 12:1108–1120
   PubMed Web of Science ®Google Scholar
• Mailhos, C., Howard, M. K., and Latchman, D. S.. 1993. Heat shock protects neuronal cells from programmed cell death by apoptosis. Neuroscience 55:621–627
   PubMed Web of Science ®Google Scholar
• Martin, S. J., Reutelingsperger, C. P., McGahon, A. J., Rader, J. A., van Schie, R. C., LaFace, D. M., and Green, D. R.. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182:1545–1556
   PubMed Web of Science ®Google Scholar
• Massie, B., Mosser, D. D., Koutroumanis, M., Vitté-Mony, I., Lamoureux, L., Couture, F., Paquet, L., Guilbault, C., Dionne, J., Chahla, D., Jolicoeur, P., and Langelier, Y.. 1998. New adenovirus vectors for protein production and gene transfer. Cytotechnology 28:53–64
   PubMedGoogle Scholar
• Meriin, A. B., Yaglom, J. A., Gabai, V. L., Mosser, D. D., Zon, L., and Sherman, M. Y.. 1999. Protein-damaging stresses activate c-Jun N-terminal kinase via inhibition of its dephosphorylation: a novel pathway controlled by HSP72. Mol. Cell. Biol. 19:2547–2555
   PubMed Web of Science ®Google Scholar
• Milarski, K. L., and Morimoto, R. I.. 1986. Expression of human HSP70 during the synthetic phase of the cell cycle. Proc. Natl. Acad. Sci. USA 83:9517–9521
   PubMed Web of Science ®Google Scholar
• Milarski, K. L., Welch, W. J., and Morimoto, R. I.. 1989. Cell cycle-dependent association of HSP70 with specific cellular proteins. J. Cell Biol. 108:413–423
   PubMed Web of Science ®Google Scholar
• Morimoto, R. I.. 1998. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12:3788–3796
   PubMed Web of Science ®Google Scholar
• Morimoto, R. I., Tissières, A., and Georgopoulos, C.. 1994. The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y
   Google Scholar
• Mosser, D. D., Caron, A. W., Bourget, L., Denis-Larose, C., and Massie, B.. 1997. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol. 17:5317–5327
   PubMed Web of Science ®Google Scholar
• Mosser, D. D., Caron, A. W., Bourget, L., Jolicoeur, P., and Massie, B.. 1997. Use of a dicistronic expression cassette encoding the green fluorescent protein for the screening and selection of cells expressing inducible gene products. BioTechniques 22:150–161
   PubMedGoogle Scholar
• Mosser, D. D., Duchaine, J., and Massie, B.. 1993. The DNA-binding activity of the human heat shock transcription factor is regulated in vivo by hsp70. Mol. Cell. Biol. 13:5427–5438
   PubMed Web of Science ®Google Scholar
• Mosser, D. D., and Martin, L. H.. 1992. Induced thermotolerance to apoptosis in a human T lymphocyte cell line. J. Cell. Physiol. 151:561–570
   PubMed Web of Science ®Google Scholar
• Nishina, H., Fischer, K. D., Radvanyi, L., Shahinian, A., Hakem, R., Rubie, E. A., Bernstein, A., Mak, T. W., Woodgett, J. R., and Penninger, J. M.. 1997. Stress-signalling kinase Sek1 protects thymocytes from apoptosis mediated by CD95 and CD3. Nature 385:350–353
   PubMedGoogle Scholar
• Ozturk, S. S., and Palsson, B. O.. 1991. Growth, metabolic, and antibody production kinetics of hybridoma cell culture: 1. Analysis of data from controlled batch reactors. Biotechnol. Prog. 7:471–480
   PubMed Web of Science ®Google Scholar
• Polla, B. S., Kantengwa, S., Francois, 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
   PubMed Web of Science ®Google Scholar
• Saleh, A., Srinivasula, S. M., Acharya, S., Fishel, R., and Alnemri, E. S.. 1999. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J. Biol. Chem. 274:17941–17945
   PubMed Web of Science ®Google Scholar
• Samali, A., Cai, J., Zhivotovsky, B., Jones, D. P., and Orrenius, S.. 1999. Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of jurkat cells. EMBO J. 18:2040–2048
   PubMed Web of Science ®Google Scholar
• Samali, A., and Cotter, T. G.. 1996. Heat shock proteins increase resistance to apoptosis. Exp. Cell Res. 223:163–170
   PubMed Web of Science ®Google Scholar
• Santoro, M. G., Garaci, E., and Amici, C.. 1989. Prostaglandins with antiproliferative activity induce the synthesis of a heat shock protein in human cells. Proc. Natl. Acad. Sci. USA 86:8407–8411
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Shi, Y., Mosser, D. D., and Morimoto, R. I.. 1998. Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 12:654–666
   PubMed Web of Science ®Google Scholar
• Stege, G. J., Li, L., Kampinga, H. H., Konings, A. W., and Li, G. C.. 1994. Importance of the ATP-binding domain and nucleolar localization domain of HSP72 in the protection of nuclear proteins against heat-induced aggregation. Exp. Cell Res. 214:279–284
   PubMedGoogle Scholar
• Susin, S. A., Zamzami, N., Castedo, M., Hirsch, T., Marchetti, P., Macho, A., Daugas, E., Geuskens, M., and Kroemer, G.. 1996. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184:1331–1341
   PubMed Web of Science ®Google Scholar
• Vander Heiden, M. G., and Thompson, C. B.. 1999. Bcl-2 proteins: regulators of apoptosis or of mitochondrial homeostasis? Nat. Cell Biol. 1:E209–E216
   PubMed Web of Science ®Google Scholar
• Vargas-Roig, L. M., Fanelli, M. A., López, L. A., Gago, F. E., Tello, O., Aznar, J. C., and Ciocca, D. R.. 1997. Heat shock proteins and cell proliferation in human breast cancer biopsy samples. Cancer Detect. Prev. 21:441–451
   PubMedGoogle Scholar
• Verheij, M., Bose, R., Lin, X. H., Yao, B., Jarvis, W. D., Grant, S., Birrer, M. J., Szabo, E., Zon, L. I., Kyriakis, J. M., Haimovitz-Friedman, A., Fuks, Z., and Kolesnick, R. N.. 1996. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380:75–79
   PubMed Web of Science ®Google Scholar
• Volloch, V., Mosser, D. D., Massie, B., and Sherman, M. Y.. 1998. Reduced thermotolerance in aged cells results from a loss of an hsp72-mediated control of JNK signaling pathway. Cell Stress Chaperones 3:265–271
   PubMed Web of Science ®Google Scholar
• Volloch, V. Z., Gabai, V. L., Rits, S. R., and Sherman, M. Y.. 1999. ATPase activity of the heat shock protein Hsp72 is dispensable for its effects on dephosphorylation of stress kinase JNK and on heat-induced apoptosis. FEBS Lett. 461:73–76
   PubMedGoogle Scholar
• Volloch, V. Z., and Sherman, M. Y.. 1999. Oncogenic potential of Hsp72. Oncogene 18:3648–3651
   PubMed Web of Science ®Google Scholar
• Wei, Y. Q., Zhao, X., Kariya, Y., Teshigawara, K., and Uchida, A.. 1995. Inhibition of proliferation and induction of apoptosis by abrogation of heat-shock protein (HSP) 70 expression in tumor cells. Cancer Immunol. Immunother. 40:73–78
   PubMed Web of Science ®Google Scholar
• Wolf, C. M., and Eastman, A.. 1999. The temporal relationship between protein phosphatase, mitochondrial cytochrome c release, and caspase activation in apoptosis. Exp. Cell Res. 247:505–513
   PubMedGoogle Scholar
• Xanthoudakis, S., Roy, S., Rasper, D., Hennessey, T., Aubin, Y., Cassady, R., Tawa, P., Ruel, R., Rosen, A., and Nicholson, D. W.. 1999. Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J. 18:2049–2056
   PubMed Web of Science ®Google Scholar
• Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J., and Greenberg, M. E.. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326–1331
   PubMed Web of Science ®Google Scholar
• Yaglom, J. A., Gabai, V. L., Meriin, A. B., Mosser, D. D., and Sherman, M. Y.. 1999. The function of HSP72 in suppression of c-Jun N-terminal kinase activation can be dissociated from its role in prevention of protein damage. J. Biol. Chem. 274:20223–20228
   PubMed Web of Science ®Google Scholar
• 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 blocked. Science 275:1129–1132
   PubMed Web of Science ®Google Scholar
• Zanke, B. W., Boudreau, K., Rubie, E., Winnett, E., Tibbles, L. A., Zon, L., Kyriakis, J., Liu, F. F., and Woodgett, J. R.. 1996. The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr. Biol. 6:606–613
   PubMed Web of Science ®Google Scholar