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PMID: 11160822 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Regulation of cell cycle progression by Swe1p and Hog1p following hypertonic stress.

Molecular biology of the cell ·Vol. 12 ·No. 1 ·2001-01-00 ·Pages 53-62

Alexander MR, Tyers M, Perret M, Craig BM, Fang KS, Gustin MC

Abstract

Exposure of yeast cells to an increase in external osmolarity induces a temporary growth arrest. Recovery from this stress is mediated by the accumulation of intracellular glycerol and the transcription of several stress response genes. Increased external osmolarity causes a transient accumulation of 1N and 2N cells and a concomitant depletion of S phase cells. Hypertonic stress triggers a cell cycle delay in G2 phase cells that appears distinct from the morphogenesis checkpoint, which operates in early S phase cells. Hypertonic stress causes a decrease in CLB2 mRNA, phosphorylation of Cdc28p, and inhibition of Clb2p-Cdc28p kinase activity, whereas Clb2 protein levels are unaffected. Like the morphogenesis checkpoint, the osmotic stress-induced G2 delay is dependent upon the kinase Swe1p, but is not tightly correlated with inhibition of Clb2p-Cdc28p kinase activity. Thus, deletion of SWE1 does not prevent the hypertonic stress-induced inhibition of Clb2p-Cdc28p kinase activity. Mutation of the Swe1p phosphorylation site on Cdc28p (Y19) does not fully eliminate the Swe1p-dependent cell cycle delay, suggesting that Swe1p may have functions independent of Cdc28p phosphorylation. Conversely, deletion of the mitogen-activated protein kinase HOG1 does prevent Clb2p-Cdc28p inhibition by hypertonic stress, but does not block Cdc28p phosphorylation or alleviate the cell cycle delay. However, Hog1p does contribute to proper nuclear segregation after hypertonic stress in cells that lack Swe1p. These results suggest a hypertonic stress-induced cell cycle delay in G2 phase that is mediated in a novel way by Swe1p in cooperation with Hog1p.

MeSH Terms
CDC28 Protein Kinase, S cerevisiae/drug effects,metabolism Cell Cycle/drug effects Cell Cycle Proteins Enzyme Activation/drug effects Fungal Proteins/pharmacology G2 Phase/drug effects Hypertonic Solutions/pharmacology Mitogen-Activated Protein Kinases/pharmacology Phosphorylation/drug effects Protein-Tyrosine Kinases/pharmacology Saccharomyces cerevisiae Proteins Yeasts/cytology,drug effects
Chemicals
Cell Cycle Proteins Fungal Proteins Hypertonic Solutions Saccharomyces cerevisiae Proteins SWE1 protein, S cerevisiae Protein-Tyrosine Kinases CDC28 Protein Kinase, S cerevisiae HOG1 protein, S cerevisiae Mitogen-Activated Protein Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Alexander M R
Rice University, Department of Biochemistry and Cell Biology, Houston Texas 77251, USA.
Tyers M
Perret M
Craig B M
Fang K S
Gustin M C
References (50)
50 references, click to expand
  1. The self-destructive personality of a cell cycle in transition.
    Curr Opin Cell Biol. 1995 Dec;7(6):781-9 PMID: 8608008
  2. Phosphorylation-independent inhibition of Cdc28p by the tyrosine kinase Swe1p in the morphogenesis checkpoint.
    Mol Cell Biol. 1999 Sep;19(9):5981-90 PMID: 10454545
  3. Transcriptional remodeling and G1 arrest in dioxygen stress in Saccharomyces cerevisiae.
    J Biol Chem. 1996 Oct 4;271(40):24885-93 PMID: 8798765
  4. At the heart of the budding yeast cell cycle.
    Trends Genet. 1996 Oct;12(10):405-12 PMID: 8909137
  5. Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast.
    Mol Biol Cell. 1996 Nov;7(11):1657-66 PMID: 8930890
  6. The spindle assembly checkpoint.
    Curr Opin Cell Biol. 1996 Dec;8(6):773-80 PMID: 8939672
  7. Cdc2 tyrosine phosphorylation is required for the DNA damage checkpoint in fission yeast.
    Genes Dev. 1997 Feb 15;11(4):504-11 PMID: 9042863
  8. The two isoenzymes for yeast NAD+-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation.
    EMBO J. 1997 May 1;16(9):2179-87 PMID: 9171333
  9. Ras-stimulated extracellular signal-related kinase 1 and RhoA activities coordinate platelet-derived growth factor-induced G1 progression through the independent regulation of cyclin D1 and p27.
    J Biol Chem. 1997 Dec 26;272(52):32966-71 PMID: 9407076
  10. Signalling in the yeasts: an informational cascade with links to the filamentous fungi.
    Microbiol Mol Biol Rev. 1998 Jun;62(2):249-74 PMID: 9618441
  11. Tyrosine phosphorylation of cdc2 is required for the replication checkpoint in Schizosaccharomyces pombe.
    Mol Cell Biol. 1998 Jul;18(7):3782-7 PMID: 9632761
  12. A morphogenesis checkpoint monitors the actin cytoskeleton in yeast.
    J Cell Biol. 1998 Sep 21;142(6):1487-99 PMID: 9744879
  13. Regulated nucleo/cytoplasmic exchange of HOG1 MAPK requires the importin beta homologs NMD5 and XPO1.
    EMBO J. 1998 Oct 1;17(19):5606-14 PMID: 9755161
  14. Control of Swe1p degradation by the morphogenesis checkpoint.
    EMBO J. 1998 Nov 16;17(22):6678-88 PMID: 9822611
  15. MAP kinase pathways in the yeast Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1264-300 PMID: 9841672
  16. Nuclear localization of Cdc25 is regulated by DNA damage and a 14-3-3 protein.
    Nature. 1999 Jan 14;397(6715):172-5 PMID: 9923681
  17. Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast.
    Genes Dev. 1999 Jan 15;13(2):176-87 PMID: 9925642
  18. Kinase activity-dependent nuclear export opposes stress-induced nuclear accumulation and retention of Hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae.
    Mol Biol Cell. 1999 Apr;10(4):1147-61 PMID: 10198063
  19. Heat-induced cell cycle arrest of Saccharomyces cerevisiae: involvement of the RAD6/UBC2 and WSC2 genes in its reversal.
    Mol Microbiol. 1999 May;32(4):729-39 PMID: 10361277
  20. In budding yeast, reactive oxygen species induce both RAS-dependent and RAS-independent cell cycle-specific arrest.
    Mol Microbiol. 1999 May;32(4):753-64 PMID: 10361279
  21. The elm1 kinase functions in a mitotic signaling network in budding yeast.
    Mol Cell Biol. 1999 Dec;19(12):7983-94 PMID: 10567524
  22. cdc25+ functions as an inducer in the mitotic control of fission yeast.
    Cell. 1986 Apr 11;45(1):145-53 PMID: 3955656
  23. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae.
    Science. 1988 Jul 15;241(4863):317-22 PMID: 3291120
  24. Conservation of mitotic controls in fission and budding yeasts.
    Cell. 1989 Apr 21;57(2):295-303 PMID: 2649252
  25. A review of mitosis in the fission yeast Schizosaccharomyces pombe.
    Exp Cell Res. 1989 Oct;184(2):273-86 PMID: 2680532
  26. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis.
    Nature. 1989 Nov 2;342(6245):39-45 PMID: 2682257
  27. mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2.
    Cell. 1991 Mar 22;64(6):1111-22 PMID: 1706223
  28. A potential positive feedback loop controlling CLN1 and CLN2 gene expression at the start of the yeast cell cycle.
    Cell. 1991 May 31;65(5):875-83 PMID: 2040016
  29. S-phase feedback control in budding yeast independent of tyrosine phosphorylation of p34cdc28.
    Nature. 1992 Jan 23;355(6358):365-8 PMID: 1731250
  30. Osmotic stress and the yeast cytoskeleton: phenotype-specific suppression of an actin mutation.
    J Cell Biol. 1992 Aug;118(3):561-71 PMID: 1639843
  31. Heat shock-mediated cell cycle blockage and G1 cyclin expression in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Feb;13(2):1034-41 PMID: 8380888
  32. An osmosensing signal transduction pathway in yeast.
    Science. 1993 Mar 19;259(5102):1760-3 PMID: 7681220
  33. Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins.
    EMBO J. 1993 May;12(5):1955-68 PMID: 8387915
  34. FAR1 links the signal transduction pathway to the cell cycle machinery in yeast.
    Cell. 1993 May 21;73(4):747-60 PMID: 8500168
  35. Control of the yeast cell cycle by the Cdc28 protein kinase.
    Curr Opin Cell Biol. 1993 Apr;5(2):166-79 PMID: 8507488
  36. Far1 and Fus3 link the mating pheromone signal transduction pathway to three G1-phase Cdc28 kinase complexes.
    Mol Cell Biol. 1993 Sep;13(9):5659-69 PMID: 8395009
  37. Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins.
    Cell. 1993 Sep 24;74(6):993-1007 PMID: 8402888
  38. Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins.
    EMBO J. 1993 Sep;12(9):3417-26 PMID: 8253069
  39. 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
  40. Direct inhibition of the yeast cyclin-dependent kinase Cdc28-Cln by Far1.
    Science. 1994 Aug 26;265(5176):1228-31 PMID: 8066461
  41. Characterization of the osmotic-stress response in Saccharomyces cerevisiae: osmotic stress and glucose repression regulate glycerol-3-phosphate dehydrogenase independently.
    Curr Genet. 1994 Jan;25(1):12-8 PMID: 8082159
  42. The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene.
    EMBO J. 1994 Sep 15;13(18):4382-9 PMID: 7523111
  43. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair.
    Genes Dev. 1994 Mar 15;8(6):652-65 PMID: 7926756
  44. Positioning of cell growth and division after osmotic stress requires a MAP kinase pathway.
    Yeast. 1994 Apr;10(4):425-39 PMID: 7941729
  45. A cell cycle checkpoint monitors cell morphogenesis in budding yeast.
    J Cell Biol. 1995 May;129(3):739-49 PMID: 7730408
  46. Cloning and characterization of GPD2, a second gene encoding sn-glycerol 3-phosphate dehydrogenase (NAD+) in Saccharomyces cerevisiae, and its comparison with GPD1.
    Mol Microbiol. 1995 Jul;17(1):95-107 PMID: 7476212
  47. The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A.
    Mol Cell Biol. 1995 Nov;15(11):6232-45 PMID: 7565776
  48. Cloning and characterization of seven cDNAs for hyperosmolarity-responsive (HOR) genes of Saccharomyces cerevisiae.
    Mol Gen Genet. 1995 Nov 15;249(2):127-38 PMID: 7500933
  49. Cell-cycle control linked to extracellular environment by MAP kinase pathway in fission yeast.
    Nature. 1995 Dec 14;378(6558):739-43 PMID: 7501024
  50. Purification and characterization of two isoenzymes of DL-glycerol-3-phosphatase from Saccharomyces cerevisiae. Identification of the corresponding GPP1 and GPP2 genes and evidence for osmotic regulation of Gpp2p expression by the osmosensing mitogen-activated protein kinase signal transduction pathway.
    J Biol Chem. 1996 Jun 7;271(23):13875-81 PMID: 8662716
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2001-01-00
Pages
53-62
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC30567
Subset
IM
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