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PMID: 15385622 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Oxidative stress activates FUS1 and RLM1 transcription in the yeast Saccharomyces cerevisiae in an oxidant-dependent Manner.

Molecular biology of the cell ·Vol. 15 ·No. 12 ·2004-12-00 ·Pages 5574-82

Staleva L, Hall A, Orlow SJ

Abstract

Mating in haploid Saccharomyces cerevisiae occurs after activation of the pheromone response pathway. Biochemical components of this pathway are involved in other yeast signal transduction networks. To understand more about the coordination between signaling pathways, we used a "chemical genetic" approach, searching for compounds that would activate the pheromone-responsive gene FUS1 and RLM1, a reporter for the cell integrity pathway. We found that catecholamines (l-3,4-hydroxyphenylalanine [l-dopa], dopamine, adrenaline, and noradrenaline) elevate FUS1 and RLM1 transcription. N-Acetyl-cysteine, a powerful antioxidant in yeast, completely reversed this effect, suggesting that FUS1 and RLM1 activation in response to catecholamines is a result of oxidative stress. The oxidant hydrogen peroxide also was found to activate transcription of an RLM1 reporter. Further genetic analysis combined with immunoblotting revealed that Kss1, one of the mating mitogen-activated protein kinases (MAPKs), and Mpk1, an MAPK of the cell integrity pathway, participated in l-dopa-induced stimulation of FUS1 and RLM1 transcription. We also report that Mpk1 and Hog1, the high osmolarity MAPK, were phosphorylated upon induction by hydrogen peroxide. Together, our results demonstrate that cells respond to oxidative stress via different signal transduction machinery dependent upon the nature of the oxidant.

MeSH Terms
Cell Membrane Permeability Gene Expression Regulation, Fungal/drug effects Hydrogen Peroxide/metabolism,pharmacology Levodopa/pharmacology MADS Domain Proteins MAP Kinase Signaling System/drug effects Membrane Proteins/genetics,metabolism Mitogen-Activated Protein Kinases/genetics,metabolism Mutation/genetics Oxidants/pharmacology Oxidative Stress/drug effects Pheromones/pharmacology Phosphorylation/drug effects Saccharomyces cerevisiae/drug effects,genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Transcription Factors/genetics,metabolism Transcription, Genetic/drug effects
Chemicals
FUS1 protein, S cerevisiae MADS Domain Proteins Membrane Proteins Oxidants Pheromones RLM1 protein, S cerevisiae SLG1 protein, S cerevisiae Saccharomyces cerevisiae Proteins Transcription Factors Levodopa Hydrogen Peroxide FUS3 protein, S cerevisiae HOG1 protein, S cerevisiae KSS1 protein, S cerevisiae Mitogen-Activated Protein Kinases SLT2 protein, S cerevisiae
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Staleva Liliana
Department of Dermatology, New York University School of Medicine, New York, NY 10016, USA.
Hall Andrea
Orlow Seth J
References (58)
58 references, click to expand
  1. The MAPKKK Ste11 regulates vegetative growth through a kinase cascade of shared signaling components.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12679-84 PMID: 10535982
  2. 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
  3. Mitogen-activated protein kinase Mkp1 of Pneumocystis carinii complements the slt2Delta defect in the cell integrity pathway of Saccharomyces cerevisiae.
    Mol Microbiol. 1999 Nov;34(3):451-62 PMID: 10564487
  4. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway.
    Mol Microbiol. 1999 Dec;34(5):1049-57 PMID: 10594829
  5. Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae.
    J Biol Chem. 2000 Jan 14;275(2):1511-9 PMID: 10625705
  6. Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles.
    Science. 2000 Feb 4;287(5454):873-80 PMID: 10657304
  7. Defects in protein glycosylation cause SHO1-dependent activation of a STE12 signaling pathway in yeast.
    Genetics. 2000 Jul;155(3):1005-18 PMID: 10880465
  8. Reactive oxygen species stimulate p44/42 mitogen-activated protein kinase and induce p27(Kip1): role in angiotensin II-mediated hypertrophy of proximal tubular cells.
    J Am Soc Nephrol. 2000 Aug;11(8):1387-97 PMID: 10906152
  9. Effects of dopamine and L-DOPA on survival of PC12 cells.
    J Neurosci Res. 2000 Oct 1;62(1):112-9 PMID: 11002293
  10. H2O2 sensing through oxidation of the Yap1 transcription factor.
    EMBO J. 2000 Oct 2;19(19):5157-66 PMID: 11013218
  11. 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
  12. Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1.
    Mol Cell Biol. 2001 Jan;21(1):271-80 PMID: 11113201
  13. Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation.
    Mol Cell. 2001 Sep;8(3):683-91 PMID: 11583629
  14. Mutations in WSC genes for putative stress receptors result in sensitivity to multiple stress conditions and impairment of Rlm1-dependent gene expression in Saccharomyces cerevisiae.
    Mol Genet Genomics. 2001 Sep;266(1):142-55 PMID: 11589572
  15. Regulation of the Saccharomyces cerevisiae Slt2 kinase pathway by the stress-inducible Sdp1 dual specificity phosphatase.
    J Biol Chem. 2002 Jun 14;277(24):21278-84 PMID: 11923319
  16. A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13804-9 PMID: 9391108
  17. The riddle of MAP kinase signaling specificity.
    Trends Genet. 1998 Apr;14(4):151-5 PMID: 9594663
  18. 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
  19. Repression of yeast Ste12 transcription factor by direct binding of unphosphorylated Kss1 MAPK and its regulation by the Ste7 MEK.
    Genes Dev. 1998 Sep 15;12(18):2887-98 PMID: 9744865
  20. Routing MAP kinase cascades.
    Science. 1998 Sep 11;281(5383):1625-6 PMID: 9767029
  21. Identification of Kel1p, a kelch domain-containing protein involved in cell fusion and morphology in Saccharomyces cerevisiae.
    J Cell Biol. 1998 Oct 19;143(2):375-89 PMID: 9786949
  22. 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
  23. Neurotrophic effects of L-DOPA in postnatal midbrain dopamine neuron/cortical astrocyte cocultures.
    J Neurochem. 1997 Oct;69(4):1398-408 PMID: 9326268
  24. Coordination of the mating and cell integrity mitogen-activated protein kinase pathways in Saccharomyces cerevisiae.
    Mol Cell Biol. 1997 Nov;17(11):6517-25 PMID: 9343415
  25. MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation.
    Cell. 1997 Nov 28;91(5):673-84 PMID: 9393860
  26. MAP kinase pathways in the yeast Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1264-300 PMID: 9841672
  27. Differential regulation of transcription: repression by unactivated mitogen-activated protein kinase Kss1 requires the Dig1 and Dig2 proteins.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15400-5 PMID: 9860980
  28. Signaling to the actin cytoskeleton.
    Annu Rev Cell Dev Biol. 1998;14:305-38 PMID: 9891786
  29. Relative dependence of different outputs of the Saccharomyces cerevisiae pheromone response pathway on the MAP kinase Fus3p.
    Genetics. 1999 Apr;151(4):1425-44 PMID: 10101167
  30. A constitutively active G-protein-coupled receptor causes mating self-compatibility in the mushroom Coprinus.
    EMBO J. 1999 May 17;18(10):2756-63 PMID: 10329622
  31. Saccharomyces cerevisiae mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway.
    J Bacteriol. 1999 Jun;181(11):3330-40 PMID: 10348843
  32. The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae.
    Mol Microbiol. 1999 May;32(4):671-80 PMID: 10361272
  33. Evidence for an antiapoptotic role of dopamine in developing retinal tissue.
    J Neurochem. 1999 Aug;73(2):485-92 PMID: 10428043
  34. Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: implications for Parkinson's disease.
    J Neurochem. 1999 Sep;73(3):1127-37 PMID: 10461904
  35. D(2) dopamine receptors induce mitogen-activated protein kinase and cAMP response element-binding protein phosphorylation in neurons.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11607-12 PMID: 10500224
  36. The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans.
    Eukaryot Cell. 2003 Apr;2(2):351-61 PMID: 12684384
  37. Differential mutagenic, antimutagenic and cytotoxic responses induced by apomorphine and its oxidation product, 8-oxo-apomorphine-semiquinone, in bacteria and yeast.
    Mutat Res. 2003 Aug 5;539(1-2):29-41 PMID: 12948812
  38. Saccharomyces cerevisiae glutaredoxin 5-deficient cells subjected to continuous oxidizing conditions are affected in the expression of specific sets of genes.
    J Biol Chem. 2004 Mar 26;279(13):12386-95 PMID: 14722110
  39. Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxidative-stress-response genes.
    Proc Natl Acad Sci U S A. 2004 Apr 27;101(17):6564-9 PMID: 15087496
  40. Activation of cytosolic phospholipase A2 in Her14 fibroblasts by hydrogen peroxide: a p42/44(MAPK)-dependent and phosphorylation-independent mechanism.
    Biochim Biophys Acta. 2004 Mar 22;1636(2-3):183-95 PMID: 15164766
  41. The Hog1 MAP kinase pathway and the Mec1 DNA damage checkpoint pathway independently control the cellular responses to hydrogen peroxide.
    DNA Repair (Amst). 2004 Jul 2;3(7):769-76 PMID: 15177185
  42. Role of CaMKII in hydrogen peroxide activation of ERK1/2, p38 MAPK, HSP27 and actin reorganization in endothelial cells.
    FEBS Lett. 2004 Aug 13;572(1-3):307-13 PMID: 15304367
  43. Transcription and regulatory signals at the mating type locus in yeast.
    Cell. 1984 Jul;37(3):969-78 PMID: 6378388
  44. A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle.
    Cell. 1990 Jul 27;62(2):213-24 PMID: 2196995
  45. Pheromone-dependent phosphorylation of the yeast STE12 protein correlates with transcriptional activation.
    Genes Dev. 1991 May;5(5):741-50 PMID: 2026326
  46. An osmosensing signal transduction pathway in yeast.
    Science. 1993 Mar 19;259(5102):1760-3 PMID: 7681220
  47. 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
  48. FAR1 links the signal transduction pathway to the cell cycle machinery in yeast.
    Cell. 1993 May 21;73(4):747-60 PMID: 8500168
  49. FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1.
    Mol Biol Cell. 1993 May;4(5):495-510 PMID: 8334305
  50. 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
  51. A two-component system that regulates an osmosensing MAP kinase cascade in yeast.
    Nature. 1994 May 19;369(6477):242-5 PMID: 8183345
  52. Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth.
    Genes Dev. 1994 Dec 15;8(24):2974-85 PMID: 8001818
  53. L-dopa cytotoxicity to PC12 cells in culture is via its autoxidation.
    J Neurochem. 1995 Feb;64(2):825-32 PMID: 7830076
  54. Parallel signal processing among mammalian MAPKs.
    Trends Biochem Sci. 1995 Mar;20(3):117-22 PMID: 7709430
  55. L-DOPA up-regulates glutathione and protects mesencephalic cultures against oxidative stress.
    J Neurochem. 1996 Feb;66(2):501-10 PMID: 8592119
  56. The SLT2(MPK1) MAP kinase is activated during periods of polarized cell growth in yeast.
    EMBO J. 1996 Jan 2;15(1):83-91 PMID: 8598209
  57. 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
  58. The evolution of the MAP kinase pathways: coduplication of interacting proteins leads to new signaling cascades.
    J Mol Evol. 1999 Nov;49(5):567-82 PMID: 10552038
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2004-12-00
Epub
2004-00-22
Pages
5574-82
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC532035
Subset
IM
Grants
NEI NIH HHS · R01 EY010223 · United States
NEI NIH HHS · EY10223 · United States
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