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PMID: 12455951 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway, and protein tyrosine phosphatases are essential under heat stress.

Eukaryotic cell ·Vol. 1 ·No. 2 ·2002-04-00 ·Pages 163-73

Winkler A, Arkind C, Mattison CP, Burkholder A, Knoche K, Ota I

Abstract

The yeast high-osmolarity glycerol (HOG) mitogen-activated protein kinase (MAPK) pathway has been characterized as being activated solely by osmotic stress. In this work, we show that the Hog1 MAPK is also activated by heat stress and that Sho1, previously identified as a membrane-bound osmosensor, is required for heat stress activation of Hog1. The two-component signaling protein, Sln1, the second osmosensor in the HOG pathway, was not involved in heat stress activation of Hog1, suggesting that the Sho1 and Sln1 sensors discriminate between stresses. The possible function of Hog1 activation during heat stress was examined, and it was found that the hog1 delta strain does not recover as rapidly from heat stress as well as the wild type. It was also found that protein tyrosine phosphatases (PTPs) Ptp2 and Ptp3, which inactivate Hog1, have two functions during heat stress. First, they are essential for survival at elevated temperatures, preventing lethality due to Hog1 hyperactivation. Second, they block inappropriate cross talk between the HOG and the cell wall integrity MAPK pathways, suggesting that PTPs are important for maintaining specificity in MAPK signaling pathways.

MeSH Terms
Heat-Shock Response Intracellular Signaling Peptides and Proteins MAP Kinase Signaling System Membrane Proteins/metabolism Mitogen-Activated Protein Kinase Kinases/metabolism Mitogen-Activated Protein Kinases/genetics,metabolism,physiology Models, Biological Protein Tyrosine Phosphatase, Non-Receptor Type 11 Protein Tyrosine Phosphatases/metabolism,physiology Saccharomyces cerevisiae Proteins/genetics,metabolism Yeasts/classification,enzymology,metabolism
Chemicals
Intracellular Signaling Peptides and Proteins Membrane Proteins SHO1 protein, S cerevisiae Saccharomyces cerevisiae Proteins HOG1 protein, S cerevisiae Mitogen-Activated Protein Kinases Mitogen-Activated Protein Kinase Kinases PBS2 protein, S cerevisiae Protein Tyrosine Phosphatase, Non-Receptor Type 11 Protein Tyrosine Phosphatases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Winkler Astrid
Department of Chemistry and Biochemistry, University of Colorado, Boulder, Colorado 80309, USA.
Arkind Christopher
Mattison Christopher P
Burkholder Anne
Knoche Kathryn
Ota Irene
References (46)
46 references, click to expand
  1. A specific protein-protein interaction accounts for the in vivo substrate selectivity of Ptp3 towards the Fus3 MAP kinase.
    Genes Dev. 1999 Nov 1;13(21):2811-27 PMID: 10557209
  2. 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 Jun;14(6):4135-44 PMID: 8196651
  3. A novel regulatory mechanism of MAP kinases activation and nuclear translocation mediated by PKA and the PTP-SL tyrosine phosphatase.
    J Cell Biol. 1999 Dec 13;147(6):1129-36 PMID: 10601328
  4. Two protein tyrosine phosphatases, Ptp2 and Ptp3, modulate the subcellular localization of the Hog1 MAP kinase in yeast.
    Genes Dev. 2000 May 15;14(10):1229-35 PMID: 10817757
  5. Response of Saccharomyces cerevisiae to severe osmotic stress: evidence for a novel activation mechanism of the HOG MAP kinase pathway.
    Mol Microbiol. 2000 Jul;37(2):382-97 PMID: 10931333
  6. Yeast Cdc42 GTPase and Ste20 PAK-like kinase regulate Sho1-dependent activation of the Hog1 MAPK pathway.
    EMBO J. 2000 Sep 1;19(17):4623-31 PMID: 10970855
  7. Polarized localization of yeast Pbs2 depends on osmostress, the membrane protein Sho1 and Cdc42.
    Nat Cell Biol. 2000 Sep;2(9):620-7 PMID: 10980703
  8. The Saccharomyces cerevisiae Sln1p-Ssk1p two-component system mediates response to oxidative stress and in an oxidant-specific fashion.
    Free Radic Biol Med. 2000 Nov 15;29(10):1043-50 PMID: 11084293
  9. Ptc1, a type 2C Ser/Thr phosphatase, inactivates the HOG pathway by dephosphorylating the mitogen-activated protein kinase Hog1.
    Mol Cell Biol. 2001 Jan;21(1):51-60 PMID: 11113180
  10. Thermosensory transduction in Escherichia coli: inhibition of the thermoresponse by L-serine.
    Proc Natl Acad Sci U S A. 1979 Jan;76(1):91-5 PMID: 370831
  11. Conditional inversion of the thermoresponse in Escherichia coli.
    J Bacteriol. 1984 Jul;159(1):360-7 PMID: 6376475
  12. Yeast shuttle and integrative vectors with multiple cloning sites suitable for construction of lacZ fusions.
    Gene. 1986;45(3):299-310 PMID: 3026915
  13. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites.
    Gene. 1988 Dec 30;74(2):527-34 PMID: 3073106
  14. The recognition component of the N-end rule pathway.
    EMBO J. 1990 Oct;9(10):3179-89 PMID: 2209542
  15. Thermosensing ability of Trg and Tap chemoreceptors in Escherichia coli.
    J Bacteriol. 1991 Feb;173(3):1120-4 PMID: 1991711
  16. A gene encoding a putative tyrosine phosphatase suppresses lethality of an N-end rule-dependent mutant.
    Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2355-9 PMID: 1549598
  17. A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C.
    Mol Cell Biol. 1993 May;13(5):3067-75 PMID: 8386319
  18. Mutations in a protein tyrosine phosphatase gene (PTP2) and a protein serine/threonine phosphatase gene (PTC1) cause a synthetic growth defect in Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Sep;13(9):5408-17 PMID: 8395005
  19. A yeast protein similar to bacterial two-component regulators.
    Science. 1993 Oct 22;262(5133):566-9 PMID: 8211183
  20. MSG5, a novel protein phosphatase promotes adaptation to pheromone response in S. cerevisiae.
    EMBO J. 1994 Jan 1;13(1):61-70 PMID: 8306972
  21. A two-component system that regulates an osmosensing MAP kinase cascade in yeast.
    Nature. 1994 May 19;369(6477):242-5 PMID: 8183345
  22. The sevenmaker gain-of-function mutation in p42 MAP kinase leads to enhanced signalling and reduced sensitivity to dual specificity phosphatase action.
    FEBS Lett. 1994 Sep 26;352(2):201-5 PMID: 7925974
  23. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor.
    Science. 1995 Jul 28;269(5223):554-8 PMID: 7624781
  24. The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response.
    Genes Dev. 1995 Jul 1;9(13):1559-71 PMID: 7628692
  25. A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway.
    J Biol Chem. 1995 Dec 15;270(50):30157-61 PMID: 8530423
  26. Cell-cycle control linked to extracellular environment by MAP kinase pathway in fission yeast.
    Nature. 1995 Dec 14;378(6558):739-43 PMID: 7501024
  27. Heat shock transcription factors: structure and regulation.
    Annu Rev Cell Dev Biol. 1995;11:441-69 PMID: 8689565
  28. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor.
    Cell. 1996 Sep 20;86(6):865-75 PMID: 8808622
  29. Cdc48p interacts with Ufd3p, a WD repeat protein required for ubiquitin-mediated proteolysis in Saccharomyces cerevisiae.
    EMBO J. 1996 Sep 16;15(18):4884-99 PMID: 8890162
  30. The osmoregulatory pathway represses mating pathway activity in Saccharomyces cerevisiae: isolation of a FUS3 mutant that is insensitive to the repression mechanism.
    Mol Cell Biol. 1996 Dec;16(12):6715-23 PMID: 8943326
  31. Regulation of the Saccharomyces cerevisiae HOG1 mitogen-activated protein kinase by the PTP2 and PTP3 protein tyrosine phosphatases.
    Mol Cell Biol. 1997 Mar;17(3):1289-97 PMID: 9032256
  32. Characterization of a serum response factor-like protein in Saccharomyces cerevisiae, Rlm1, which has transcriptional activity regulated by the Mpk1 (Slt2) mitogen-activated protein kinase pathway.
    Mol Cell Biol. 1997 May;17(5):2615-23 PMID: 9111331
  33. Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK.
    Science. 1997 Jun 13;276(5319):1702-5 PMID: 9180081
  34. Two protein-tyrosine phosphatases inactivate the osmotic stress response pathway in yeast by targeting the mitogen-activated protein kinase, Hog1.
    J Biol Chem. 1997 Jul 11;272(28):17749-55 PMID: 9211927
  35. Differential regulation of FUS3 MAP kinase by tyrosine-specific phosphatases PTP2/PTP3 and dual-specificity phosphatase MSG5 in Saccharomyces cerevisiae.
    Genes Dev. 1997 Jul 1;11(13):1690-702 PMID: 9224718
  36. A proteinaceous gene regulatory thermometer in Salmonella.
    Cell. 1997 Jul 11;90(1):55-64 PMID: 9230302
  37. puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila.
    Genes Dev. 1998 Feb 15;12(4):557-70 PMID: 9472024
  38. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications.
    Yeast. 1998 Jan 30;14(2):115-32 PMID: 9483801
  39. Signal transduction through MAP kinase cascades.
    Adv Cancer Res. 1998;74:49-139 PMID: 9561267
  40. Requirement of STE50 for osmostress-induced activation of the STE11 mitogen-activated protein kinase kinase kinase in the high-osmolarity glycerol response pathway.
    Mol Cell Biol. 1998 Oct;18(10):5788-96 PMID: 9742096
  41. The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae.
    Genes Dev. 1998 Sep 15;12(18):2874-86 PMID: 9744864
  42. MAP kinase pathways in the yeast Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1264-300 PMID: 9841672
  43. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human.
    Physiol Rev. 1999 Jan;79(1):143-80 PMID: 9922370
  44. The extracellular domain of the Saccharomyces cerevisiae Sln1p membrane osmolarity sensor is necessary for kinase activity.
    J Bacteriol. 1999 Apr;181(8):2527-34 PMID: 10198019
  45. Differential regulation of the cell wall integrity mitogen-activated protein kinase pathway in budding yeast by the protein tyrosine phosphatases Ptp2 and Ptp3.
    Mol Cell Biol. 1999 Nov;19(11):7651-60 PMID: 10523653
  46. Crosstalk between cAMP-dependent kinase and MAP kinase through a protein tyrosine phosphatase.
    Nat Cell Biol. 1999 Sep;1(5):305-11 PMID: 10559944
Article Info
Journal
Eukaryotic cell
Abbr.
Eukaryot Cell
ISSN
1535-9778
DOI
10.1128/EC.1.2.163-173.2002
Published
2002-04-00
Pages
163-73
Language
English
Region
United States
NLM ID
101130731
PMCID
PMC118028
Subset
IM
External Links
PubMed source DOI: 10.1128/EC.1.2.163-173.2002 PMC Full Text View journal details
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