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PMID: 15371544 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Disruption of yeast forkhead-associated cell cycle transcription by oxidative stress.

Molecular biology of the cell ·Vol. 15 ·No. 12 ·2004-12-00 ·Pages 5659-69

Shapira M, Segal E, Botstein D

Abstract

The effects of oxidative stress on yeast cell cycle depend on the stress-exerting agent. We studied the effects of two oxidative stress agents, hydrogen peroxide (HP) and the superoxide-generating agent menadione (MD). We found that two small coexpressed groups of genes regulated by the Mcm1-Fkh2-Ndd1 transcription regulatory complex are sufficient to account for the difference in the effects of HP and MD on the progress of the cell cycle, namely, G1 arrest with MD and an S phase delay followed by a G2/M arrest with HP. Support for this hypothesis is provided by fkh1fkh2 double mutants, which are affected by MD as we find HP affects wild-type cells. The apparent involvement of a forkhead protein in HP-induced cell cycle arrest, similar to that reported for Caenorhabditis elegans and human, describes a potentially novel stress response pathway in yeast.

MeSH Terms
Cell Cycle/drug effects,genetics Cell Cycle Proteins/genetics,metabolism Forkhead Transcription Factors Gene Expression Profiling Gene Expression Regulation, Fungal/drug effects Hydrogen Peroxide/pharmacology Oxidative Stress/drug effects Saccharomyces cerevisiae/cytology,drug effects,genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Transcription Factors/genetics,metabolism Transcription, Genetic/drug effects,genetics Vitamin K 3/pharmacology
Chemicals
Cell Cycle Proteins Fkh1 protein, S cerevisiae Fkh2 protein, S cerevisiae Forkhead Transcription Factors Saccharomyces cerevisiae Proteins Transcription Factors Vitamin K 3 Hydrogen Peroxide
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Shapira Michael
Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA. [email protected]
Segal Eran
Botstein David
References (67)
67 references, click to expand
  1. Two alternative cell cycle checkpoint pathways differentially control DNA damage-dependent induction of MAG1 and DDI1 expression in yeast.
    Mol Genet Genomics. 2001 Nov;266(3):436-44 PMID: 11713673
  2. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation.
    Sci STKE. 2000 Oct 10;2000(53):pe1 PMID: 11752613
  3. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway.
    Science. 2002 Mar 29;295(5564):2450-2 PMID: 11884717
  4. Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase.
    Proc Natl Acad Sci U S A. 2002 Apr 2;99(7):4245-50 PMID: 11929995
  5. Diverse and specific gene expression responses to stresses in cultured human cells.
    Mol Biol Cell. 2004 May;15(5):2361-74 PMID: 15004229
  6. Chemistry of dioxygen.
    Methods Enzymol. 1984;105:3-22 PMID: 6328186
  7. Parallel pathways of gene regulation: homologous regulators SWI5 and ACE2 differentially control transcription of HO and chitinase.
    Genes Dev. 1992 Jan;6(1):93-104 PMID: 1730413
  8. Quinone chemistry and toxicity.
    Toxicol Appl Pharmacol. 1992 Jan;112(1):2-16 PMID: 1733045
  9. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1.
    Nature. 2000 Apr 13;404(6779):782-7 PMID: 10783894
  10. Differential regulation of glutaredoxin gene expression in response to stress conditions in the yeast Saccharomyces cerevisiae.
    Biochim Biophys Acta. 2000 Jan 31;1490(1-2):33-42 PMID: 10786615
  11. A large-scale study of Yap1p-dependent genes in normal aerobic and H2O2-stress conditions: the role of Yap1p in cell proliferation control in yeast.
    Mol Microbiol. 2000 May;36(4):830-45 PMID: 10844671
  12. Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth.
    Nature. 2000 Jul 6;406(6791):90-4 PMID: 10894548
  13. Forkhead-like transcription factors recruit Ndd1 to the chromatin of G2/M-specific promoters.
    Nature. 2000 Jul 6;406(6791):94-8 PMID: 10894549
  14. The forkhead protein Fkh2 is a component of the yeast cell cycle transcription factor SFF.
    EMBO J. 2000 Jul 17;19(14):3750-61 PMID: 10899128
  15. Oxidative stress and cell cycle checkpoint function.
    Free Radic Biol Med. 2000 May 1;28(9):1387-404 PMID: 10924858
  16. Forkhead transcription factors, Fkh1p and Fkh2p, collaborate with Mcm1p to control transcription required for M-phase.
    Curr Biol. 2000 Jul 27-Aug 10;10(15):896-906 PMID: 10959837
  17. Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and saccharomyces cerevisiae responses to oxidative stress.
    Annu Rev Microbiol. 2000;54:439-61 PMID: 11018134
  18. Oxidants, oxidative stress and the biology of ageing.
    Nature. 2000 Nov 9;408(6809):239-47 PMID: 11089981
  19. Genomic expression programs in the response of yeast cells to environmental changes.
    Mol Biol Cell. 2000 Dec;11(12):4241-57 PMID: 11102521
  20. The Stanford Microarray Database.
    Nucleic Acids Res. 2001 Jan 1;29(1):152-5 PMID: 11125075
  21. The TRANSFAC system on gene expression regulation.
    Nucleic Acids Res. 2001 Jan 1;29(1):281-3 PMID: 11125113
  22. Oxidation of methionine in proteins: roles in antioxidant defense and cellular regulation.
    IUBMB Life. 2000 Oct-Nov;50(4-5):301-7 PMID: 11327324
  23. Order of function of the budding-yeast mitotic exit-network proteins Tem1, Cdc15, Mob1, Dbf2, and Cdc5.
    Curr Biol. 2001 May 15;11(10):784-8 PMID: 11378390
  24. Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae.
    Mol Biol Cell. 1992 Jul;3(7):805-18 PMID: 1387566
  25. Saccharomyces cerevisiae has an inducible response to menadione which differs from that to hydrogen peroxide.
    J Gen Microbiol. 1993 Mar;139(3):501-7 PMID: 8473859
  26. DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein.
    Science. 2002 Apr 19;296(5567):530-4 PMID: 11964479
  27. FOXO forkhead transcription factors induce G(2)-M checkpoint in response to oxidative stress.
    J Biol Chem. 2002 Jul 26;277(30):26729-32 PMID: 12048180
  28. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress.
    Nature. 2002 Sep 19;419(6904):316-21 PMID: 12239572
  29. Forkhead transcription factors: key players in development and metabolism.
    Dev Biol. 2002 Oct 1;250(1):1-23 PMID: 12297093
  30. Nonparametric methods for identifying differentially expressed genes in microarray data.
    Bioinformatics. 2002 Nov;18(11):1454-61 PMID: 12424116
  31. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation.
    Cell. 2002 Nov 15;111(4):471-81 PMID: 12437921
  32. A genome-wide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage.
    Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16934-9 PMID: 12482937
  33. The Forkhead Box m1b transcription factor is essential for hepatocyte DNA replication and mitosis during mouse liver regeneration.
    Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16881-6 PMID: 12482952
  34. Module networks: identifying regulatory modules and their condition-specific regulators from gene expression data.
    Nat Genet. 2003 Jun;34(2):166-76 PMID: 12740579
  35. Oxidative DNA damage: mechanisms, mutation, and disease.
    FASEB J. 2003 Jul;17(10):1195-214 PMID: 12832285
  36. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans.
    Nature. 2003 Jul 17;424(6946):277-83 PMID: 12845331
  37. Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression.
    Nature. 2003 Jul 31;424(6948):561-5 PMID: 12891360
  38. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase.
    Science. 2004 Mar 26;303(5666):2011-5 PMID: 14976264
  39. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase.
    Science. 1993 Sep 17;261(5128):1551-7 PMID: 8372350
  40. DUN1 encodes a protein kinase that controls the DNA damage response in yeast.
    Cell. 1993 Dec 17;75(6):1119-27 PMID: 8261511
  41. 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
  42. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage.
    Cell. 1995 Sep 8;82(5):841-7 PMID: 7671311
  43. The Swi5 transcription factor of Saccharomyces cerevisiae has a role in exit from mitosis through induction of the cdk-inhibitor Sic1 in telophase.
    Genetics. 1997 Jan;145(1):85-96 PMID: 9017392
  44. A novel Mcm1-dependent element in the SWI4, CLN3, CDC6, and CDC47 promoters activates M/G1-specific transcription.
    Genes Dev. 1997 May 15;11(10):1277-88 PMID: 9171372
  45. Flow cytometric analysis of DNA content in budding yeast.
    Methods Enzymol. 1997;283:322-32 PMID: 9251030
  46. Identification of RNR4, encoding a second essential small subunit of ribonucleotide reductase in Saccharomyces cerevisiae.
    Mol Cell Biol. 1997 Oct;17(10):6105-13 PMID: 9315670
  47. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans.
    Nature. 1997 Oct 30;389(6654):994-9 PMID: 9353126
  48. Exploring the metabolic and genetic control of gene expression on a genomic scale.
    Science. 1997 Oct 24;278(5338):680-6 PMID: 9381177
  49. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans.
    Science. 1997 Nov 14;278(5341):1319-22 PMID: 9360933
  50. SGD: Saccharomyces Genome Database.
    Nucleic Acids Res. 1998 Jan 1;26(1):73-9 PMID: 9399804
  51. Activation of the OxyR transcription factor by reversible disulfide bond formation.
    Science. 1998 Mar 13;279(5357):1718-21 PMID: 9497290
  52. Hydrogen peroxide causes RAD9-dependent cell cycle arrest in G2 in Saccharomyces cerevisiae whereas menadione causes G1 arrest independent of RAD9 function.
    J Biol Chem. 1998 Apr 10;273(15):8564-71 PMID: 9535829
  53. A genome-wide transcriptional analysis of the mitotic cell cycle.
    Mol Cell. 1998 Jul;2(1):65-73 PMID: 9702192
  54. The H2O2 stimulon in Saccharomyces cerevisiae.
    J Biol Chem. 1998 Aug 28;273(35):22480-9 PMID: 9712873
  55. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway.
    Genes Dev. 1998 Sep 15;12(18):2956-70 PMID: 9744871
  56. Residues in the Swi5 zinc finger protein that mediate cooperative DNA binding with the Pho2 homeodomain protein.
    Mol Cell Biol. 1998 Nov;18(11):6436-46 PMID: 9774660
  57. Regulation of Cdc28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1191-243 PMID: 9841670
  58. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization.
    Mol Biol Cell. 1998 Dec;9(12):3273-97 PMID: 9843569
  59. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide.
    Free Radic Biol Med. 1999 Aug;27(3-4):322-8 PMID: 10468205
  60. Java Treeview--extensible visualization of microarray data.
    Bioinformatics. 2004 Nov 22;20(17):3246-8 PMID: 15180930
  61. DNA polymerase epsilon links the DNA replication machinery to the S phase checkpoint.
    Cell. 1995 Jan 13;80(1):29-39 PMID: 7813016
  62. Silent repair accounts for cell cycle specificity in the signaling of oxidative DNA lesions.
    EMBO J. 2001 Jun 1;20(11):2896-906 PMID: 11387222
  63. Mechanisms controlling differential promoter-occupancy by the yeast forkhead proteins Fkh1p and Fkh2p: implications for regulating the cell cycle and differentiation.
    Genes Dev. 2001 Sep 15;15(18):2445-56 PMID: 11562353
  64. Serial regulation of transcriptional regulators in the yeast cell cycle.
    Cell. 2001 Sep 21;106(6):697-708 PMID: 11572776
  65. Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p.
    Mol Biol Cell. 2001 Oct;12(10):2987-3003 PMID: 11598186
  66. Forkhead transcription factors contribute to execution of the mitotic programme in mammals.
    Nature. 2001 Oct 18;413(6857):744-7 PMID: 11607034
  67. Rme1, which controls CLN2 expression in Saccharomyces cerevisiae, is a nuclear protein that is cell cycle regulated.
    Mol Genet Genomics. 2001 Nov;266(3):374-84 PMID: 11713667
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2004-12-00
Epub
2004-00-15
Pages
5659-69
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC532044
Subset
IM
Grants
NIGMS NIH HHS · R01 GM046406 · United States
NIGMS NIH HHS · R37 GM046406 · United States
NIGMS NIH HHS · GM-46406 · United States
Corrections
ErratumIn
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