Protein chaperones and the heat shock response in Saccharomyces cerevisiae

Current Opinion in Microbiology

Volumn 1, Issue 2, 1998, Pages 197-203

  Morano, Kevin A ^a   Liu, Phillip C C ^a   Thiele, Dennis J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SACCHAROMYCES CEREVISIAE;

CHAPERONE; HEAT SHOCK PROTEIN;

GENE EXPRESSION REGULATION; GENETICS; HEAT SHOCK RESPONSE; METABOLISM; PHYSIOLOGY; REVIEW; SACCHAROMYCES CEREVISIAE;

GENE EXPRESSION REGULATION, FUNGAL; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; MOLECULAR CHAPERONES; SACCHAROMYCES CEREVISIAE;

EID: 0032034779     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(98)80011-8     Document Type: Article

References (44)

1. Liu X-D, Liu PCC, Santoro N, Thiele DJ: Conservation of a stress response: human heat shock transcription factors functionally substitute for yeast HSF. EMBO J 1997, 16:6466-6477.
2. Picard D, Khursheed B, Garabedian MJ, Fortin MG, Lindquist S, Yamamoto KR: Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 1990, 348:166-168.
3. Craig EA, Baxter BK, Becker J, Halladay J, Ziegelhoffer T: Cytosolic hsp70s of Saccharomyces cerevisiae: roles in protein synthesis, protein translocation, proteolysis, and regulation. In The Biology of Heat Shock Proteins, Molecular Chaperones. Edited by Morimoto RI, Tissieres A, Georgopolous C, New York: Cold Spring Harbor Laboratory Press; 1994:31-52.
4. James P, Pfund C, Craig EA: Functional specificity among Hsp70 molecular chaperones. Science 1997, 275:387-389. Argues against the long-standing hypothesis that specificity among Hsp70s is caused by differences in peptide binding. Domain-swapping experiments between two families of Hsp70s with different roles in vivo show that the peptide-binding domains of Hsp70 do not mediate functional distinction but suggest more elaborate, intramolecular controls.
5. Craven RA, Egerton M, Stirling CJ: A novel Hsp70 of the yeast ER lumen is required for the efficient translocation of a number of protein precursors. EMBO J 1996, 15:2640-2650.
6. Hamilton TG, Flynn GC: Cer1p, a novel Hsp70-related protein required for posttranslational endoplasmic reticulum translocation in yeast. J Biol Chem 1996, 271:30610-30613.
7. Baxter BK, James P, Evans T, Craig EA: SS/1 encodes a novel Hsp70 of the Saccharomyces cerevisiae endoplasmic reticulum. Mol Cell Biol 1996, 16:6444-6456.
8. Craven RA, Tyson JR, Stirling CJ: A novel subfamily of Hsp70s in the endoplasmic reticulum. Trends Cell Biol 1997, 7:277-282.
9. Shamu CE: Splicing together the unfolded-protein response. Curr Biol 1997, 7:67-70.
10. Saris N, Holkeri H, Craven RA, Stirling CJ, Makarow M: The Hsp70 homologue Lhs1p is involved in a novel function of the yeast endoplasmic reticulum, refolding and stabilization of heat-denatured protein aggregates. J Cell Biol 1997, 137:813-824. This report elegantly follows the unfolding and refolding of a model substrate protein of the endoplasmic reticulum (ER) in vivo, and directly implicates Lhs1p/Ssip/Cer1p as a major chaperone component of the ER required for recovery from severe thermal stress.
11. Bohen SP, Yamamoto KR: Modulation of steroid receptor signal transduction by heat shock proteins. In The Biology of Heat Shock Proteins, Molecular Chaperones. Edited by Morimoto RI, Tissieres A, Georgopolous C. New York: Cold Spring Harbor Laboratory Press; 1994:313-334.
12. Pratt WB, Toft DO: Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 1997, 18:306-360.
13. Chang HC, Lindquist S: Conservation of Hsp90 macromolecular complexes in Saccharomyces cerevisiae. J Biol Chem 1994, 269:24983-24988.
14. Kimura Y, Yahara I, Lindquist S: Role of the protein chaperone YDJ1 in establishing Hsp90-mediated signal transduction pathways. Science 1995, 268:1362-1365.
15. Chang HC, Nathan DF, Lindquist S: In vivo analysis of the Hsp90 cochaperone Stil (p60). Mol Cell Biol 1997, 17:318-325. This paper provides the first in vivo evidence for interaction between Sti1p (p60), and Hsp90, implicating Sti1p as a critical component of the chaperone complex. Importantly, levels of Sti1p are shown to influence the amount of Ydj1p associated with Hsp90/glucocorticoid receptor complexes, a first step toward defining discrete stages in a folding pathway for substrate proteins.
16. Kimura Y, Rutherford SL, Miyata Y, Yahara I, Freeman BC, Yue L, Morimoto RI, Lindquist S: Cdc37 is a molecular chaperone with specific functions in signal transduction. Genes Dev 1997, 11:1775-1785. Demonstration of a chaperone function for the Hsp90 chaperone complex subunit Cdc37p. Cdc37p, like Hsp90, maintains substrates in an activation-competent state, but requires Hsp70, and Dnaj function for complete refolding. Despite similar chaperone activities, Cdc37p and Hsp90 are not interchangeable.
17. Duina AA, Chang HC, Marsh JA, Lindquist S, Gaber RF: A cyclophilin function in Hsp90-dependent signal transduction. Science 1996, 274:1713-1715. Together with Chang and Lindquist, 1994 [13], identifies the presumptive cyclophilin subunits in the Hsp90 chaperone complex as Cpr6p, and Cpr7p. Loss of function of these genes also results in reduced activity of both the glucocorticoid receptor and v-Src, two Hsp90-dependent signal transducers, consistent with an active role in the Hsp90 complex.
18. Johnson JL, Craig EA: Protein folding in vivo: unraveling complex pathways. Cell 1997, 90:201-204. A very nice review which summarizes mechanistic aspects of protein folding in the eukaryolic cytosol, bringing together data from both yeast and mammalian systems.
19. Gerber MR, Farrell A, Deshaies RJ, Herskowitz I, Morgan DO: Cdc37 is required for association of the protein kinase Cdc28 with G1 and mitotic cyclins. Proc Natl Acad Sci USA 1995, 92:4651-4655.
20. Cdc37 is a protein kinase-targeting subunit of Hsp90 that binds and stabilizes Cdk4. Genes Dev 1996, 10:1491-1502.
21. Schutz AR, Giddings T Jr, Steiner E, Winey M: The yeast CDC37 gene interacts with MPS1 and is required for proper execution of spindle pole body duplication. J Cell Biol 1997, 136:969-982.
22. Aligue R, Akhavan-Niak H, Russell P: A role for Hsp90 in cell cycle control: Wee1 tyrosine kinase activity requires interaction with Hsp90. EMBO J 1994, 13:6099-6106.
23. Borkovich KA, Farrelly FW, Finkelstein DB, Taulien J, Lindquist S: Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 1989, 9:3919-3930.
24. Breter HJ, Ferguson J, Peterson TA, Reed SI: Isolation and transcriptional characterization of three genes which function at start, the controlling event of the Saccharomyces cerevisiae cell division cycle: CDC36, CDC37, and CDC39. Mol Cell Biol 1983, 3:881-891.
25. Koch KA, Pena MMO, Thiele DJ: Copper-binding motifs in catalysis, transport, detoxification and signaling. Chem Biol 1997, 4:549-560.
26. Silar P, Butler G, Thiele DJ: Heat shock transcription factor activates transcription of the yeast metallothionein gene. Mol Cell Biol 1991, 11:1232-1238.
27. Liu X-D, Thiele DJ: Oxidative stress induces heat shock factor phosphorylation and HSF-dependent activation of yeast metallothionein gene transcription. Genes Dev 1996, 10:592-603.
28. Ruis H, Schuller C: Stress signaling in yeast. Bioessays 1995, 17:959-965.
29. Wieser R, Adam G, Wagner A, Schuller C, Marchler G, Ruis H, Krawiec Z, Bilinski T: Heat shock factor-independent heat control of transcription of the CTT1 gene encoding the cytosolic catalase T of Saccharomyces cerevisiae. J Biol Chem 1991, 266:12406-12411.
30. Bell W, Klaassen P, Ohnacker M, Boller T, Herweijer M, Schoppink P, Van der Zee P, Wiemken A: Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation. Eur J Biochem 1992, 209:951-959.
31. De Virgilio C, Burckert N, Bell W, Jeno P, Boller T, Wiemken A: Disruption of TPS2, the gene encoding the 100-kDa subunit of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae, causes accumulation of trehalose-6-phosphate and loss of trehalose-6-phosphate phosphatase activity. Eur J Biochem 1993, 212:315-323.
32. Albertyn J, Hohmann S, Thevelein JM, Prior BA: GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 1994, 14:4135-4144.
33. Varela JC, Praekelt UM, Meacock PA, Planta RJ, Mager WH: The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol Cell Biol 1995, 15:6232-6245.
34. Lindquist S, Kim G: Heat-shock protein 104 expression is sufficient for thermotolerance in yeast. Proc Natl Acad Sci USA 1996, 93:5301-5306.
35. Schmitt AP, McEntee K: Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1996, 93:5777-5782. This paper, along with Martinez-Pastor et al., 1996 [36••], identifies Msn2p and Msn4p as the transcription factors which bind to stress response elements (STREs) and mediate gene induction in the general stress response. The authors use a molecular biological approach to isolate Msn2p by screening a phage expression library with a radiolabeled STRE probe, then demonstrate through gene inactivation studies the requirement for MSN2 for STRE-mediated transcription.
36. Martinez-Pastor MT, Marchler G, Schuller C, Marchler-Bauer A, Ruis H, Estruch F: The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 1996, 15:2227-2235. This study originates from a prior observation that msn2msn4 cells respond poorly to carbon source adaptation and conclusively demonstrates that Msn2p and Msn4p are required for activation of several stress response element containing genes in response to stress. Together with Schmitt and McEntee. 1996 [35••], this report significantly advances understanding of the general stress response pathway.
37. Saavedra C, Tung KS, Amberg DC, Hopper AK, Cole CN: Regulation of mRNA export in response to stress in Saccharomyces cerevisiae. Genes Dev 1996, 10:1608-1620. This paper demonstrates selective export of SSA1 and SSA4 mRNAs during heat shock while bulk mRNAs are retained in the nucleus. Results of genetic experiments showing that several genes required for bulk mRNA export are dispensible for SSA4 export during heat shock suggests an alternative stress-resistant export mechanism.
38. Tani T, Derby RJ, Hiraoka Y, Spector DL: Nucleolar accumulation of poly (A)+ RNA in heat-shocked yeast cells: implication of nucleolar involvement in mRNA transport. Mol Biol Cell 1995, 6:1515-1534.
39. Liu Y, Liang S, Tartakoff AM: Heat shock disassembles the nucleolus and inhibits nuclear protein import and poly(A)+ RNA export. EMBO J 1996, 15:6750-6757. Together with Saavedra et al., 1996 [37•], this paper provides evidence for altered trafficking of macromolecules into and out of the nucleus during heat shock. Relocation of nucleolar proteins to the cytosol coupled with a block in protein import into the nucleus is proposed to underlie gross changes in nucleolar structure during severe thermal stress.
40. Saavedra CA, Hammell CM, Heath CV, Cole CN: Yeast heat-shock mRNAs are exported through a distinct pathway defined by Rip1p. Genes Dev 1997, 11:2845-2856. The requirement for Rip1p in the export of SSA4 mRNA in response to thermal stress but not under normal growth conditions is demonstrated genetically. Rip1 is the first component to be identified that defines a distinct pathway used for export of heat shock mRNAs under stress conditions (see also Saavedra et al., 1996 [37•]).
41. Barnes CA, MacKenzie MM, Johnston GC, Singer RA: Efficient translation of an SSA1-derived heat-shock mRNA in yeast cells limited for cap-binding protein and elF-4F. Mol Gen Genet 1995, 246:619-627.
42. Vogel JL, Parsell DA, Lindquist S: Heat-shock proteins Hsp104 and Hsp70 reactivate mRNA splicing after heat inactivation. Curr Biol 1995, 5:306-317.
43. Duncan RF: Translational control during heat shock. In Translational Control. Edited by Hershey JWB, Mathews MB, Sonenberg N. Plainview, NY: Cold Spring Harbor Press; 1996:271-293.
44. Stutz F, Kantor J, Zhang D, McCarthy T, Neville M, Rosbach M: The yeast nucleoporin Rip1p contributes to multiple export pathways with no essential role for its FG-repeat region. Genes Dev 1997, 11:2857-2868.