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Molecular and Cellular Biology, October 2000, p. 7146-7159, Vol. 20, No. 19
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

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

Dick D. Mosser,1,* Antoine W. Caron,1 Lucie Bourget,1 Anatoli B. Meriin,2 Michael Y. Sherman,2 Richard I. Morimoto,3 and Bernard Massie1,4,5

Biotechnology Research Institute, Montreal, Quebec H4P 2R2,1 INRS-IAF, University of Quebec, Laval, Quebec H7N 4Z3,4 and Department of Microbiology and Immunology, Faculty of Medicine, University of Montreal, Montreal, Quebec H3C 3J7,5 Canada; Boston Biomedical Research Institute, Boston, Massachusetts 021142; and Department of Biochemistry, Molecular Biology and Cell Biology, Rice Institute for Biomedical Research, Northwestern University, Evanston, Illinois 602083

Received 3 February 2000/Returned for modification 3 April 2000/Accepted 14 July 2000

Cellular stress can trigger a process of self-destruction known as apoptosis. Cells can also respond to stress by adaptive changes that increase their ability to tolerate normally lethal conditions. Expression of the major heat-inducible protein hsp70 protects cells from heat-induced apoptosis. hsp70 has been reported to act in some situations upstream or downstream of caspase activation, and its protective effects have been said to be either dependent on or independent of its ability to inhibit JNK activation. Purified hsp70 has been shown to block procaspase processing in vitro but is unable to inhibit the activity of active caspase 3. Since some aspects of hsp70 function can occur in the absence of its chaperone activity, we examined whether hsp70 lacking its ATPase domain or the C-terminal EEVD sequence that is essential for peptide binding was required for the prevention of apoptosis. We generated stable cell lines with tetracycline-regulated expression of hsp70, hsc70, and chaperone-defective hsp70 mutants lacking the ATPase domain or the C-terminal EEVD sequence or containing AAAA in place of EEVD. Overexpression of hsp70 or hsc70 protected cells from heat shock-induced cell death by preventing the processing of procaspases 9 and 3. This required the chaperone function of hsp70 since hsp70 mutant proteins did not prevent procaspase processing or provide protection from apoptosis. JNK activation was inhibited by both hsp70 and hsc70 and by each of the hsp70 domain mutant proteins. The chaperoning activity of hsp70 is therefore not required for inhibition of JNK activation, and JNK inhibition was not sufficient for the prevention of apoptosis. Release of cytochrome c from mitochondria was inhibited in cells expressing full-length hsp70 but not in cells expressing the protein with ATPase deleted. Together with the recently identified ability of hsp70 to inhibit cytochrome c-mediated procaspase 9 processing in vitro, these data demonstrate that hsp70 can affect the apoptotic pathway at the levels of both cytochrome c release and initiator caspase activation and that the chaperone function of hsp70 is required for these effects.

* Corresponding author. Mailing address: National Research Council, Biotechnology Research Institute, 6100 Royalmount Ave., Montreal, Quebec, Canada H4P 2R2. Phone: (514) 496-6843. Fax: (514) 496-5143. E-mail: dick.mosser{at}nrc.ca.

Molecular and Cellular Biology, October 2000, p. 7146-7159, Vol. 20, No. 19
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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