Saccharomyces cerevisiae Hsp104 enhances the chaperone capacity of human cells and inhibits heat stress-induced proapoptotic signaling

Biochemistry

Volumn 43, Issue 25, 2004, Pages 8107-8115

  Mosser, Dick D ^a   Ho, Sylvia ^b   Glover, John R ^b  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; GENES; MOLECULAR STRUCTURE; OLIGOMERS; PROTEINS; STRESSES; THERMAL EFFECTS;

CYTOPLASM; NUCLEAR ENVELOPES; NUCLEOPLASM; THERMOTOLERANCE FACTORS;

MICROBIOLOGY;

CHAPERONE; DNA; HEAT SHOCK PROTEIN 100; HEAT SHOCK PROTEIN 104; HEAT SHOCK PROTEIN 70; LUCIFERASE; PROCASPASE 3; PROTEIN HDJ1; PROTEIN HDJ2; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL NUCLEUS MEMBRANE; CELL VIABILITY; CYTOPLASM; ENZYME PHOSPHORYLATION; HEAT STRESS; HEAT TOLERANCE; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; T LYMPHOCYTE; TRANSGENE;

AMINO ACID SUBSTITUTION; APOPTOSIS; CASPASE 3; CASPASES; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; CELL SURVIVAL; CYTOPLASM; ESCHERICHIA COLI; GENE EXPRESSION; HEAT STRESS DISORDERS; HEAT-SHOCK PROTEINS; HUMANS; LUCIFERASES; MOLECULAR CHAPERONES; NUCLEAR ENVELOPE; PROTEIN FOLDING; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

ANIMALIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 3042561822     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0493766     Document Type: Article

References (54)

1. Gerner, E. W., and Schneider, M. J. (1975) Induced thermal resistance in HeLa cells, Nature 256, 500-502.
2. Parsell, D. A., and Lindquist, S. (1994) in The Biology of Heat Shock Proteins and Molecular Chaperones (Morimoto, R. I., Tissieres, A., and Georgopoulos, C., Eds.) pp 457-493, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. Mosser, D. D., and Martin, L. H. (1992) Induced thermotolerance to apoptosis in a human T lymphocyte cell line, J. Cell. Physiol. 151, 457-494.
4. McMillan, D. R., Xiao, X., Shao, L., Graves, K., and Benjamin, I. J. (1998) Targeted disruption of heat shock transcription factor 1 abolishes thermotolernce and protection against heat inducible apoptosis, J. Biol. Chem. 273, 7523-7528.
5. Beere, H. M., and Green, D. R. (2001) Stress management-heat shock protein-70 and the regulation of apoptosis, Trends Cell Biol. 11, 6-10.
6. Samali, A., Robertson, J. D., Peterson, E., Manero, F., van Zeijl, L., Paul, C., Cotgreave, I. A., Arrigo, A. P., and Orrenius, S. (2001) Hsp27 protects mitochondria of thermotolerant cells against apoptotic stimuli, Cell Stress Chaperones 6, 49-58.
7. Sanchez, Y., Parsell, D. A., Taulien, J., Vogel, J. L., Craig, E. A., and Lindquist, S. (1993) Genetic evidence for a functional relationship between Hsp104 and Hsp70, J. Bacteriol. 175, 6484-6491.
8. Petko, L., and Lindquist, S. (1986) Hsp26 is not required for growth at high temperatures, nor for thermotolerance, spore development, or germination, Cell 45, 885-894.
9. Sanchez, Y., and Lindquist, S. L. (1990) HSP104 required for induced thermotolerance, Science 248, 1112-1115.
10. Parsell, D. A., Kowal, A. S., Singer, M. A., and Lindquist, S. (1994) Protein disaggregation mediated by heat-shock protein Hsp104, Nature 372, 475-478.
11. Glover, J. R., and Lindquist, S. (1998) Hsp104, Hsp70, and Hsp40: A novel chaperone system that rescues previously aggregated proteins, Cell 94, 73-82.
12. Krzewska, J., Langer, T., and Liberek, K. (2001) Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding, FEBS Lett. 489, 92-96.
13. Goloubinoff, P., Mogk, A., Zvi, A. P., Tomoyasu, T., and Bukau, B. (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network, Proc. Natl. Acad. Sci. U.S.A. 96, 13732-13737.
14. Queitsch, C., Hong, S. W., Vierling, E., and Lindquist, S. (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis, Plant Cell 12, 479-492.
15. Hong, S. W., and Vierling, E. (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high-temperature stress, Proc. Natl. Acad. Sci. U.S.A. 97, 4392-4397.
16. Nieto-Sotelo, J., Martinez, L. M., Ponce, G., Cassab, G. I., Alagon, A., Meeley, R. B., Ribaut, J. M., and Yang, R. (2002) Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth, Plant Cell 14, 1621-1633.
17. Squires, C. L., Pedersen, S., Ross, B. M., and Squires, C. (1991) ClpB is the Escherichia coli heat shock protein F84.1, J. Bacteriol. 173, 4254-4262.
18. Thomas, J. G., and Baneyx, F. (1998) Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: Comparison with ClpA, ClpB, and HtpG in vivo, J. Bacteriol. 180, 5165-5172.
19. 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.
20. 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.
21. Mosser, D. D., Caron, A. W., Bourget, L., Meriin, A. B., Sherman, M. Y., Morimoto, R. I., and Massie, B. (2000) The chaperone function of hsp70 is required for protection against stress-induced apoptosis, Mol. Cell. Biol. 20, 7146-7159.
22. Caron, A. W., Massie, B., and Mosser, D. D. (2000) Use of a micromanipulator for high-efficiency cloning of cells co-expressing fluorescent proteins, Methods Cell Sci. 22, 137-145.
23. Parsell, D. A., Sanchez, Y., Stitzel, J. D., and Lindquist, S. (1991) Hsp104 is a highly conserved protein with two essential nucleotide-binding sites, Nature 353, 270-273.
24. Michels, A. A., Nguyen, V. T., Konings, A. W., Kampinga, H. H., and Bensaude, O. (1995) Thermostability of a nuclear-targeted luciferase expressed in mammalian cells. Destabilizing influence of the intranuclear microenvironment, Eur. J. Biochem. 234, 382-389.
25. Nollen, E. A., Brunsting, J. F., Roelofsen, H., Weber, L. A., and Kampinga, H. H. (1999) In vivo chaperone activity of heat shock protein 70 and thermotolerance, Mol. Cell. Biol. 19, 2069-7209.
26. Kawai, R., Fujita, K., Iwahashi, H., and Komatsu, Y. (1999) Direct evidence for the intracellular localization of Hsp104 in Saccharomyces cerevisiae by immunoelectron microscopy, Cell Stress Chaperones 4, 46-53.
27. Kudo, N., Wolff, B., Sekimoto, T., Schreiner, E. P., Yoneda, Y., Yanagida, M., Horinouchi, S., and Yoshida, M. (1998) Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRMI, Exp. Cell Res. 242, 540-547.
28. Welch, W. J., and Feramisco, J. R. (1984) Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells, J. Biol. Chem. 259, 4501-4513.
29. Diamant, S., Ben-Zvi, A. P., Bukau, B., and Goloubinoff, P. (2000) Size-dependent disaggregation of stable protein aggregates by the DnaK chaperone machinery, J. Biol. Chem. 275, 21107-21113.
30. Corydon, T. J., Wilsbech, M., Jespersgaard, C., Andresen, B. S., Borglum, A. D., Pedersen, S., Bolund, L., Gregersen, N., and Bross, P. (2000) Human and mouse mitochondrial orthologs of bacterial ClpX, Mamm. Genome 11, 899-905.
31. Kang, S., Ortega, J., Singh, S., Wang, N., Huang, N., Steven, A., and Maurizi, M. (2002) Functional proteolytic complexes of the human mitochondrial ATP-dependent protease, hClpXP, J. Biol. Chem. 277, 21095-21102.
32. Perier, F., Radeke, C. M., Raab-Graham, K. F., and Vandenberg, C. A. (1995) Expression of a putative ATPase suppresses the growth defect of a yeast potassium transport mutant: Identification of a mammalian member of the Clp/HSP104 family, Gene 152, 157-163.
33. Murdock, D. G., Boone, B. E., Esposito, L. A., and Wallace, D. C. (1999) Up-regulation of nuclear and mitochondrial genes in the skeletal muscle of mice lacking the heart/muscle isoform of the adenine nucleotide translocator, J. Biol. Chem. 274, 14429-14433.
34. Chernoff, Y. O., Lindquist, S. L., Ono, B., Inge-Vechtomov, S. G., and Liebman, S. W. (1995) Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+], Science 268, 880-884.
35. Moriyama, H., Edskes, H. K., and Wickner, R. B. (2000) [URE3] Prion propagation in Saccharomyces cerevisiae: Requirement for chaperone Hsp104 and curing by overexpressed chaperone Ydj1p, Mol. Cell. Biol. 20, 8916-8922.
36. Derkatch, I. L., Bradley, M. E., Masse, S. V., Zadorsky, S. P., Polozkov, G. V., Inge-Vechtomov, S. G., and Liebman, S. W. (2000) Dependence and independence of [PSI(+)] and [PIN(+)]: A two-prion system in yeast? EMBO J. 19, 1942-1952.
37. Bao, Y. P., Cook, L. J., O'Donovan, D., Uyama, E., and Rubinsztein, D. C. (2002) Mammalian, yeast, bacterial, and chemical chaperones reduce aggregate formation and death in a cell model of oculopharyngeal muscular dystrophy, J. Biol. Chem. 277, 12263-12269.
38. Carmichael, J., Chatellier, J., Woolfson, A., Milstein, C., Fersht, A. R., and Rubinsztein, D. C. (2000) Bacterial and yeast chaperones reduce both aggregate formation and cell death in mammalian cell models of Huntington's disease, Proc. Natl. Acad. Sci. U.S.A. 97, 9701-9705.
39. Satyal, S. H., Schmidt, E., Kitagawa, K., Sondheimer, N., Lindquist, S., Kramer, J. M., and Morimoto, R. I. (2000) Polyglutamine aggregates alter protein folding homeostasis in Caenorhabditis elegans, Proc. Natl. Acad. Sci. U.S.A. 97, 5750-5755.
40. Cummings, C. J., Mancini, M. A., Antalffy, B., DeFranco, D. B., Orr, H. T., and Zoghbi, H. Y. (1998) Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1, Nat. Genet. 19, 148-154.
41. Zander, C., Takahashi, J., El Hachimi, K. H., Fujigasaki, H., Albanese, V., Lebre, A. S., Stevanin, G., Duyckaerts, C., and Brice, A. (2001) Similarities between spinocerebellar ataxia type 7 (SCA7) cell models and human brain: Proteins recruited in inclusions and activation of caspase-3, Hum. Mol. Genet. 10, 2569-2579.
42. Watanabe, M., Dykes-Hoberg, M., Culotta, V. C., Price, D. L., Wong, P. C., and Rothstein, J. D. (2001) Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues, Neurobiol. Dis. 8, 933-941.
43. Abel, A., Walcott, J., Woods, J., Duda, J., and Merry, D. E. (2001) Expression of expanded repeat androgen receptor produces neurologic disease in transgenic mice, Hum. Mol. Genet. 10, 107-116.
44. Vogel, J. L., Parsell, D. A., and Lindquist, S. (1995) Heat-shock proteins Hsp104 and Hsp70 reactivate mRNA splicing after heat inactivation, Curr. Biol. 5, 306-317.
45. Bracken, A. P., and Bond, U. (1999) Reassembly and protection of small nuclear ribonucleoprotein particles by heat shock proteins in yeast cells, RNA 5, 1586-1596.
46. Roti Roti, J. L., Kampinga, H. H., Malyapa, R. S., Wright, W. D., vanderWaal, R. P., and Xu, M. (1998) Nuclear matrix as a target for hyperthermic killing of cancer cells, Cell Stress Chaperones 3, 245-255.
47. Ravagnan, L., Gurbuxani, S., Susin, S. A., Maisse, C., Daugas, E., Zamzami, N., Mak, T., Jaattela, M., Penninger, J. M., Garrido, C., and Kroemer, G. (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor, Nat. Cell Biol. 3, 839-843.
48. Beere, H. M., Wolf, B. B., Cain, K., Mosser, D. D., Mahboubi, A., Kuwana, T., Tailor, P., Morimoto, R. I., Cohen, G. M., and Green, D. R. (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome, Nat. Cell Biol. 2, 469-475.
49. Saleh, A., Srinivasula, S. M., Balkir, L., Robbins, P. D., and Alnemri, E. S. (2000) Negative regulation of the Apaf-1 apoptosome by Hsp70, Nat. Cell Biol. 2, 476-483.
50. Meriin, A. B., Yaglom, J. A., Gabai, V. L., Zon, L., Ganiatsas, S., Mosser, D. D., 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.
51. Park, H. S., Lee, J. S., Huh, S. H., Seo, J. S., and Choi, E. J. (2001) Hsp72 functions as a natural inhibitory protein of c-Jun N-terminal kinase, EMBO J. 20, 446-456.
52. Merienne, K., Helmlinger, D., Perkin, G. R., Devys, D., and Trottier, Y. (2003) Polyglutamine expansion induces a protein-damaging stress connecting heat shock protein 70 to the JNK pathway, J. Biol. Chem. 278, 16957-16967.
53. Cowan, K. J., Diamond, M. I., and Welch, W. J. (2003) Polyglutamine protein aggregation and toxicity are linked to the cellular stress response, Hum. Mol. Genet. 12, 1377-1391.
54. Zhou, H., Li, S. H., and Li, X. J. (2001) Chaperone suppression of cellular toxicity of huntingtin is independent of polyglutamine aggregation, J. Biol. Chem. 276, 48417-48424.