The Hsp110 protein chaperone Sse1 is required for yeast cell wall integrity and morphogenesis

Current Genetics

Volumn 54, Issue 1, 2008, Pages 1-11

  Shaner, Lance ^a   Gibney, Patrick A ^a   Morano, Kevin A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Cell integrity; Chaperone; Heat shock; Hsp110; Hsp70; Hsp90; Morphogenesis; Yeast

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE SLT2; PROTEIN MBP1; PROTEIN SSE1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MBF; TRANSCRIPTION FACTOR RLM1; TRANSCRIPTION FACTOR SBF; TRANSCRIPTION FACTOR SWI4; TRANSCRIPTION FACTOR SWI6;

ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DOWNSTREAM PROCESSING; FUNGAL VIABILITY; FUNGUS GROWTH; GENE MUTATION; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TEMPERATURE DEPENDENCE; YEAST;

CELL WALL; FUNGAL PROTEINS; GENES, FUNGAL; HSP110 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; MORPHOGENESIS; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 43349108797     PISSN: 01728083     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00294-008-0193-y     Document Type: Article

References (47)

1. Baetz K, Moffat J, Haynes J, Chang M, Andrews B (2001) Transcriptional coregulation by the cell integrity mitogen-activated protein kinase Slt2 and the cell cycle regulator Swi4. Mol Cell Biol 21:6515-6528
2. Becker J, Walter W, Yan W, Craig EA (1996) Functional interaction of cytosolic hsp70 and a DnaJ-related protein, Ydj1p, in protein translocation in vivo. Mol Cell Biol 16:4378-4386
3. Brachmann CB et al (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115-132
4. Brodsky JL, Chiosis G (2006) Hsp70 molecular chaperones: Emerging roles in human disease and identification of small molecule modulators. Curr Top Med Chem 6:1215-1225
5. Dodou E, Treisman R (1997) The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-activated protein kinase pathway. Mol Cell Biol 17:1848-1859
6. Dragovic Z, Broadley SA, Shomura Y, Bracher A, Hartl FU (2006) Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J 25:2519-2528
7. Farrell A, Morgan DO (2000) Cdc37 promotes the stability of protein kinases Cdc28 and Cak1. Mol Cell Biol 20:749-754
8. Garcia R et al (2004) The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J Biol Chem 279:15183-15195
9. Goeckeler JL, Stephens A, Lee P, Caplan AJ, Brodsky JL (2002) Overexpression of yeast Hsp110 homolog Sse1p suppresses ydj1-151 thermosensitivity and restores Hsp90-dependent activity. Mol Biol Cell 13:2760-2770
10. Hawle P, Horst D, Bebelman JP, Yang XX, Siderius M, van der Vies SM (2007) Cdc37p is required for stress-induced high-osmolarity glycerol and protein kinase C mitogen-activated protein kinase pathway functionality by interaction with Hog1p and Slt2p (Mpk1p). Eukaryot Cell 6:521-532
11. Igual JC, Johnson AL, Johnston LH (1996) Coordinated regulation of gene expression by the cell cycle transcription factor Swi4 and the protein kinase C MAP kinase pathway for yeast cell integrity. EMBO J 15:5001-5013
12. Jung US, Sobering AK, Romeo MJ, Levin DE (2002) Regulation of the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP kinase. Mol Microbiol 46:781-789
13. Kabani M, Beckerich JM, Brodsky JL (2002) Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Mol Cell Biol 22:4677-4689
14. Kim KY, Cosano IC, Levin DE, Molina M, Martin H (2007) Dissecting the transcriptional activation function of the cell wall integrity MAP kinase. Yeast 24:335-342
15. Kim KY, Truman AW, Levin DE (2008) Yeast Mpk1 mitogen-activated protein kinase activates transcription through Swi4/Swi6 by a noncatalytic mechanism that requires upstream signal. Mol Cell Biol 28:2579-2589
16. Koch C, Moll T, Neuberg M, Ahorn H, Nasmyth K (1993) A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science 261:1551-1557
17. Lagorce A et al (2003) Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J Biol Chem 278:20345-20357
18. Lee P, Shabbir A, Cardozo C, Caplan AJ (2004) Sti1 and Cdc37 can stabilize Hsp90 in chaperone complexes with a protein kinase. Mol Biol Cell 15:1785-1792
19. Levin DE (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69:262-291
20. Levin DE, Bartlett-Heubusch E (1992) Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect. J Cell Biol 116:1221-1229
21. Liu XD, Morano KA, Thiele DJ (1999) The yeast Hsp110 family member, Sse1, is an Hsp90 cochaperone. J Biol Chem 274:26654-26660
22. Madden K, Sheu YJ, Baetz K, Andrews B, Snyder M (1997) SBF cell cycle regulator as a target of the yeast PKC-MAP kinase pathway. Science 275:1781-1784
23. Mandal AK et al (2007) Cdc37 has distinct roles in protein kinase quality control that protect nascent chains from degradation and promote posttranslational maturation. J Cell Biol 176:319-328
24. Mayer MP, Bukau B (1999) Molecular chaperones: The busy life of Hsp90. Curr Biol 9:R322-R325
25. Mayer MP, Bukau B (2005) Hsp70 chaperones: Cellular functions and molecular mechanism. Cell Mol Life Sci 62:670-684
26. Millson SH, Truman AW, King V, Prodromou C, Pearl LH, Piper PW (2005) A two-hybrid screen of the yeast proteome for Hsp90 interactors uncovers a novel Hsp90 chaperone requirement in the activity of a stress-activated mitogen-activated protein kinase, Slt2p (Mpk1p). Eukaryot Cell 4:849-860
27. Moll T, Dirick L, Auer H, Bonkovsky J, Nasmyth K (1992) SWI6 is a regulatory subunit of two different cell cycle START-dependent transcription factors in Saccharomyces cerevisiae. J Cell Sci Suppl 16:87-96
28. Morano KA, Santoro N, Kock KA, Thiele DJ (1999) A trans -activation domain in yeast heat shock transcription factor is essential for cell cycle progression during stress. Mol Cell Biol 19:402-411
29. Mukai H, Kuno T, Tanaka H, Hirata D, Miyakawa T, Tanaka C (1993) Isolation and characterization of SSE1 and SSE2, new members of the yeast HSP70 multigene family. Gene 132:57-66
30. Nicolet CM, Craig EA (1989) Isolation and characterization of STI1, a stress-inducible gene from Saccharomyces cerevisiae. Mol Cell Biol 9:3638-3646
31. Paravicini G et al (1992) The osmotic integrity of the yeast cell requires a functional PKC1 gene product. Mol Cell Biol 12:4896-4905
32. Pearl LH, Prodromou C (2001) Structure, function, and mechanism of the Hsp90 molecular chaperone. Adv Protein Chem 59:157-186
33. Piper PW, Truman AW, Millson SH, Nuttall J (2006) Hsp90 chaperone control over transcriptional regulation by the yeast Slt2(Mpk1) p and human ERK5 mitogen-activated protein kinases (MAPKs). Biochem Soc Trans 34:783-785
34. Raviol H, Sadlish H, Rodriguez F, Mayer MP, Bukau B (2006) Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J 25:2510-2518
35. Rothstein R (1991) Targeting, disruption, replacement, and allele rescue: Integrative DNA transformation in yeast. In: Guthrie C, Fink G (eds) Methods in enzymology. Academic Press, San Diego, pp 281-301
36. Shaner L, Morano KA (2007) All in the family: Atypical Hsp70 chaperones are conserved modulators of Hsp70 activity. Cell Stress Chaperones 12:1-8
37. Shaner L, Sousa R, Morano KA (2006) Characterization of hsp70 binding and nucleotide exchange by the yeast hsp110 chaperone Sse1. Biochemistry 45:15075-15084
38. Shaner L, Trott A, Goeckeler JL, Brodsky JL, Morano KA (2004) The function of the yeast molecular chaperone Sse1 is mechanistically distinct from the closely related hsp70 family. J Biol Chem 279:21992-22001
39. Shaner L, Wegele H, Buchner J, Morano KA (2005) The yeast Hsp110 Sse1 functionally interacts with the Hsp70 chaperones Ssa and Ssb. J Biol Chem 280:41262-41269
40. Torres L et al (1991) A protein kinase gene complements the lytic phenotype of Saccharomyces cerevisiae lyt2 mutants. Mol Microbiol 5:2845-2854
41. Trott A, Shaner L, Morano KA (2005) The molecular cchaperone Sse1 and the growth control protein kinase Sch9 collaborate to regulate protein kinase A activity in Saccharomyces cerevisiae. Genetics 170:1009-1021
42. Truman AW et al (2006) Expressed in the yeast Saccharomyces cerevisiae, human ERK5 is a client of the Hsp90 chaperone that complements loss of the Slt2p (Mpk1p) cell integrity stress-activated protein kinase. Eukaryot Cell 5:1914-1924
43. Truman AW, Millson SH, Nuttall JM, Mollapour M, Prodromou C, Piper PW (2007) In the yeast heat shock response, Hsf1-directed induction of Hsp90 facilitates the activation of the Slt2 (Mpk1) mitogen-activated protein kinase required for cell integrity. Eukaryot Cell 6:744-752
44. Watanabe Y, Irie K, Matsumoto K (1995) Yeast RLM1 encodes a serum response factor-like protein that may function downstream of the Mpk1 (Slt2) mitogen-activated protein kinase pathway. Mol Cell Biol 15:5740-5749
45. Wright CM, Fewell SW, Sullivan ML, Pipas JM, Watkins SC, Brodsky JL (2007) The Hsp40 molecular chaperone Ydj1p, along with the protein kinase C pathway, affects cell-wall integrity in the yeast Saccharomyces cerevisiae. Genetics 175:1649-1664
46. Yam AY, Albanese V, Lin HT, Frydman J (2005) Hsp110 cooperates with different cytosolic HSP70 systems in a pathway for de novo folding. J Biol Chem 280:41252-41261
47. Zarzov P, Mazzoni C, Mann C (1996) The SLT2(MPK1) MAP kinase is activated during periods of polarized cell growth in yeast. EMBO J 15:83-91