Multiple Means to the Same End: The Genetic Basis of Acquired Stress Resistance in Yeast
In nature, stressful environments often occur in combination or close succession, and thus the ability to prepare for impending stress likely provides a significant fitness advantage. Organisms exposed to a mild dose of stress can become tolerant to what would otherwise be a lethal dose of subsequent stress; however, the mechanism of this acquired stress tolerance is poorly understood. To explore this, we exposed the yeast gene-deletion libraries, which interrogate all essential and non-essential genes, to successive stress treatments and identified genes necessary for acquiring subsequent stress resistance. Cells were exposed to one of three different mild stress pretreatments (salt, DTT, or heat shock) and then challenged with a severe dose of hydrogen peroxide (H2O2). Surprisingly, there was little overlap in the genes required for acquisition of H2O2 tolerance after different mild-stress pretreatments, revealing distinct mechanisms of surviving H2O2 in each case. Integrative network analysis of these results with respect to protein–protein interactions, synthetic–genetic interactions, and functional annotations identified many processes not previously linked to H2O2 tolerance. We tested and present several models that explain the lack of overlap in genes required for H2O2 tolerance after each of the three pretreatments. Together, this work shows that acquired tolerance to the same severe stress occurs by different mechanisms depending on prior cellular experiences, underscoring the context-dependent nature of stress tolerance.
Vyšlo v časopise:
Multiple Means to the Same End: The Genetic Basis of Acquired Stress Resistance in Yeast. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002353
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002353
Souhrn
In nature, stressful environments often occur in combination or close succession, and thus the ability to prepare for impending stress likely provides a significant fitness advantage. Organisms exposed to a mild dose of stress can become tolerant to what would otherwise be a lethal dose of subsequent stress; however, the mechanism of this acquired stress tolerance is poorly understood. To explore this, we exposed the yeast gene-deletion libraries, which interrogate all essential and non-essential genes, to successive stress treatments and identified genes necessary for acquiring subsequent stress resistance. Cells were exposed to one of three different mild stress pretreatments (salt, DTT, or heat shock) and then challenged with a severe dose of hydrogen peroxide (H2O2). Surprisingly, there was little overlap in the genes required for acquisition of H2O2 tolerance after different mild-stress pretreatments, revealing distinct mechanisms of surviving H2O2 in each case. Integrative network analysis of these results with respect to protein–protein interactions, synthetic–genetic interactions, and functional annotations identified many processes not previously linked to H2O2 tolerance. We tested and present several models that explain the lack of overlap in genes required for H2O2 tolerance after each of the three pretreatments. Together, this work shows that acquired tolerance to the same severe stress occurs by different mechanisms depending on prior cellular experiences, underscoring the context-dependent nature of stress tolerance.
Zdroje
1. GaschAP 2007 Comparative genomics of the environmental stress response in ascomycete fungi. Yeast
2. ParsellDALindquistS 1993 The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27 437 496
3. CraigEAGambillBDNelsonRJ 1993 Heat shock proteins: molecular chaperones of protein biogenesis. Microbiol Rev 57 402 414
4. EstruchF 2000 Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24 469 486
5. JamiesonDJ 1998 Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14 1511 1527
6. HohmannSMagerPWillemH 2003 Yeast Stress Responses. Heidelberg Springer-Verlag
7. MagerWHFerreiraPM 1993 Stress response of yeast. Biochem J 290 (Pt1) 1 13
8. HahnGMNingSCElizagaMKappDSAndersonRL 1989 A comparison of thermal responses of human and rodent cells. Int J Radiat Biol 56 817 825
9. LouYYousefAE 1997 Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Appl Environ Microbiol 63 1252 1255
10. MaleckKLevineAEulgemTMorganASchmidJ 2000 The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26 403 410
11. SchenkPMKazanKWilsonIAndersonJPRichmondT 2000 Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci U S A 97 11655 11660
12. ChinnusamyVSchumakerKZhuJK 2004 Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55 225 236
13. DurrantWEDongX 2004 Systemic acquired resistance. Annu Rev Phytopathol 42 185 209
14. CharngYYLiuHCLiuNYHsuFCKoSS 2006 Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol 140 1297 1305
15. HeckerMPane-FarreJVolkerU 2006 SigB-Dependent General Stress Response in Bacillus subtilis and Related Gram-Positive Bacteria. Annu Rev Microbiol
16. JeongWSJunMKongAN 2006 Nrf2: a potential molecular target for cancer chemoprevention by natural compounds. Antioxid Redox Signal 8 99 106
17. KenslerTWWakabayashiNBiswalS 2007 Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47 89 116
18. MatsumotoHHamadaNTakahashiAKobayashiYOhnishiT 2007 Vanguards of paradigm shift in radiation biology: radiation-induced adaptive and bystander responses. J Radiat Res (Tokyo) 48 97 106
19. ScholzHFranzMHeberleinU 2005 The hangover gene defines a stress pathway required for ethanol tolerance development. Nature 436 845 847
20. LuDMaulikNMoraruIIKreutzerDLDasDK 1993 Molecular adaptation of vascular endothelial cells to oxidative stress. Am J Physiol 264 C715 722
21. RaffaghelloLLeeCSafdieFMWeiMMadiaF 2008 Starvation-dependent differential stress resistance protects normal but not cancer cells against high-dose chemotherapy. Proc Natl Acad Sci U S A 105 8215 8220
22. ZhaoHSapolskyRMSteinbergGK 2006 Interrupting reperfusion as a stroke therapy: ischemic postconditioning reduces infarct size after focal ischemia in rats. J Cereb Blood Flow Metab 26 1114 1121
23. ZhaoH 2009 Ischemic postconditioning as a novel avenue to protect against brain injury after stroke. J Cereb Blood Flow Metab 29 873 885
24. CaustonHCRenBKohSSHarbisonCTKaninE 2001 Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12 323 337
25. GaschAPSpellmanPTKaoCMCarmel-HarelOEisenMB 2000 Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11 4241 4257
26. Martinez-PastorMTMarchlerGSchullerCMarchler-BauerARuisH 1996 The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). Embo J 15 2227 2235
27. SchmittAPMcEnteeK 1996 Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 93 5777 5782
28. GornerWDurchschlagEMartinez-PastorMTEstruchFAmmererG 1998 Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev 12 586 597
29. AmorosMEstruchF 2001 Hsf1p and Msn2/4p cooperate in the expression of Saccharomyces cerevisiae genes HSP26 and HSP104 in a gene- and stress type-dependent manner. Mol Microbiol 39 1523 1532
30. EstruchFCarlsonM 1993 Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant of Saccharomyces cerevisiae. Mol Cell Biol 13 3872 3881
31. BerryDBGaschAP 2008 Stress-activated genomic expression changes serve a preparative role for impending stress in yeast. Mol Biol Cell 19 4580 4587
32. TempleMDPerroneGGDawesIW 2005 Complex cellular responses to reactive oxygen species. Trends Cell Biol 15 319 326
33. ThorpeGWFongCSAlicNHigginsVJDawesIW 2004 Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxidative-stress-response genes. Proc Natl Acad Sci U S A 101 6564 6569
34. KelleyRIdekerT 2009 Genome-wide fitness and expression profiling implicate Mga2 in adaptation to hydrogen peroxide. PLoS Genet 5 e1000488 doi:10.1371/journal.pgen.1000488
35. TuckerCLFieldsS 2004 Quantitative genome-wide analysis of yeast deletion strain sensitivities to oxidative and chemical stress. Comp Funct Genomics 5 216 224
36. LeeWSt OngeRPProctorMFlahertyPJordanMI 2005 Genome-wide requirements for resistance to functionally distinct DNA-damaging agents. PLoS Genet 1 e24 doi:10.1371/journal.pgen.0010024
37. GiaeverGChuAMNiLConnellyCRilesL 2002 Functional profiling of the Saccharomyces cerevisiae genome. Nature 418 387 391
38. WinzelerEAShoemakerDDAstromoffALiangHAndersonK 1999 Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285 901 906
39. YanZCostanzoMHeislerLEPawJKaperF 2008 Yeast Barcoders: a chemogenomic application of a universal donor-strain collection carrying bar-code identifiers. Nat Methods 5 719 725
40. de la Torre-RuizMAMozo-VillariasAPujolNPetkovaMI 2010 How budding yeast sense and transduce the oxidative stress signal and the impact in cell growth and morphogenesis. Curr Protein Pept Sci 11 669 679
41. Yeger-LotemERivaLSuLJGitlerADCashikarAG 2009 Bridging high-throughput genetic and transcriptional data reveals cellular responses to alpha-synuclein toxicity. Nat Genet 41 316 323
42. JinYHDunlapPEMcBrideSJAl-RefaiHBushelPR 2008 Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet 4 e1000053 doi:10.1371/journal.pgen.1000053
43. TaiSLSnoekILuttikMAAlmeringMJWalshMC 2007 Correlation between transcript profiles and fitness of deletion mutants in anaerobic chemostat cultures of Saccharomyces cerevisiae. Microbiology 153 877 886
44. WarringerJEricsonEFernandezLNermanOBlombergA 2003 High-resolution yeast phenomics resolves different physiological features in the saline response. Proc Natl Acad Sci U S A 100 15724 15729
45. ChangMBellaouiMBooneCBrownGW 2002 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 99 16934 16939
46. BirrellGWBrownJAWuHIGiaeverGChuAM 2002 Transcriptional response of Saccharomyces cerevisiae to DNA-damaging agents does not identify the genes that protect against these agents. Proc Natl Acad Sci U S A 99 8778 8783
47. LewisJAElkonIMMcGeeMAHigbeeAJGaschAP 2010 Exploiting natural variation in Saccharomyces cerevisiae to identify genes for increased ethanol resistance. Genetics 186 1197 1205
48. Flattery-O'BrienJCollinsonLPDawesIW 1993 Saccharomyces cerevisiae has an inducible response to menadione which differs from that to hydrogen peroxide. J Gen Microbiol 139 501 507
49. WestfallPJPattersonJCChenREThornerJ 2008 Stress resistance and signal fidelity independent of nuclear MAPK function. Proc Natl Acad Sci U S A 105 12212 12217
50. SchullerCBrewsterJLAlexanderMRGustinMCRuisH 1994 The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. Embo J 13 4382 4389
51. ClotetJEscoteXAdroverMAYaakovGGariE 2006 Phosphorylation of Hsl1 by Hog1 leads to a G2 arrest essential for cell survival at high osmolarity. Embo J 25 2338 2346
52. AlexanderMRTyersMPerretMCraigBMFangKS 2001 Regulation of cell cycle progression by Swe1p and Hog1p following hypertonic stress. Mol Biol Cell 12 53 62
53. BelliGGariEAldeaMHerreroE 2001 Osmotic stress causes a G1 cell cycle delay and downregulation of Cln3/Cdc28 activity in Saccharomyces cerevisiae. Mol Microbiol 39 1022 1035
54. EscoteXZapaterMClotetJPosasF 2004 Hog1 mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1. Nat Cell Biol 6 997 1002
55. EscoteXMirandaMRodriguez-PorrataBMasACorderoR 2011 The stress-activated protein kinase Hog1 develops a critical role after resting state. Mol Microbiol
56. WuC 1995 Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11 441 469
57. GaschAP 2002 The Environmental Stress Response: a common yeast response to environmental stresses. HohmannSMagerP Yeast Stress Responses Heidelberg Springer-Verlag 11 70
58. HedbackerKCarlsonM 2008 SNF1/AMPK pathways in yeast. Front Biosci 13 2408 2420
59. LiaoXButowRA 1993 RTG1 and RTG2: two yeast genes required for a novel path of communication from mitochondria to the nucleus. Cell 72 61 71
60. LipsonDRazTKieuAJonesDRGiladiE 2009 Quantification of the yeast transcriptome by single-molecule sequencing. Nat Biotechnol 27 652 658
61. AveryAMAverySV 2001 Saccharomyces cerevisiae expresses three phospholipid hydroperoxide glutathione peroxidases. J Biol Chem 276 33730 33735
62. HochstrasserM 1996 Ubiquitin-dependent protein degradation. Annu Rev Genet 30 405 439
63. FinleyDOzkaynakEVarshavskyA 1987 The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell 48 1035 1046
64. TkaczJSLampenO 1975 Tunicamycin inhibition of polyisoprenyl N-acetylglucosaminyl pyrophosphate formation in calf-liver microsomes. Biochem Biophys Res Commun 65 248 257
65. GalaoRPChariAAlves-RodriguesILobaoDMasA 2010 LSm1-7 complexes bind to specific sites in viral RNA genomes and regulate their translation and replication. Rna 16 817 827
66. NoueiryAODiezJFalkSPChenJAhlquistP 2003 Yeast Lsm1p-7p/Pat1p deadenylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation. Mol Cell Biol 23 4094 4106
67. Restrepo-HartwigMAhlquistP 1999 Brome mosaic virus RNA replication proteins 1a and 2a colocalize and 1a independently localizes on the yeast endoplasmic reticulum. J Virol 73 10303 10309
68. HollienJWeissmanJS 2006 Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313 104 107
69. HollienJLinJHLiHStevensNWalterP 2009 Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186 323 331
70. DeckerCJParkerR 2006 CAR-1 and trailer hitch: driving mRNP granule function at the ER? J Cell Biol 173 159 163
71. RandJDGrantCM 2006 The thioredoxin system protects ribosomes against stress-induced aggregation. Mol Biol Cell 17 387 401
72. PrinzAHartmannEKaliesKU 2000 Sec61p is the main ribosome receptor in the endoplasmic reticulum of Saccharomyces cerevisiae. Biol Chem 381 1025 1029
73. JonikasMCCollinsSRDenicVOhEQuanEM 2009 Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323 1693 1697
74. WiedmannBPrehnS 1999 The nascent polypeptide-associated complex (NAC) of yeast functions in the targeting process of ribosomes to the ER membrane. FEBS Lett 458 51 54
75. ChenYFeldmanDEDengCBrownJADe GiacomoAF 2005 Identification of mitogen-activated protein kinase signaling pathways that confer resistance to endoplasmic reticulum stress in Saccharomyces cerevisiae. Mol Cancer Res 3 669 677
76. PastorMMProftMPascual-AhuirA 2009 Mitochondrial function is an inducible determinant of osmotic stress adaptation in yeast. J Biol Chem 284 30307 30317
77. TagkopoulosILiuYCTavazoieS 2008 Predictive behavior within microbial genetic networks. Science 320 1313 1317
78. MitchellARomanoGHGroismanBYonaADekelE 2009 Adaptive prediction of environmental changes by microorganisms. Nature 460 220 224
79. PierceSEDavisRWNislowCGiaeverG 2007 Genome-wide analysis of barcoded Saccharomyces cerevisiae gene-deletion mutants in pooled cultures. Nat Protoc 2 2958 2974
80. SmithAMHeislerLEMellorJKaperFThompsonMJ 2009 Quantitative phenotyping via deep barcode sequencing. Genome Res 19 1836 1842
81. BreslowDKCameronDMCollinsSRSchuldinerMStewart-OrnsteinJ 2008 A comprehensive strategy enabling high-resolution functional analysis of the yeast genome. Nat Methods 5 711 718
82. LeeMVTopperSEHublerSLHoseJWengerCD 2011 A dynamic model of proteome changes reveals new roles for transcript alteration in yeast. Mol Syst Biol 7 514
83. EisenMBSpellmanPTBrownPOBotsteinD 1998 Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95 14863 14868
84. RobinsonMDGrigullJMohammadNHughesTR 2002 FunSpec: a web-based cluster interpreter for yeast. B M C Bioinformatics 3 35
85. ShannonPMarkielAOzierOBaligaNSWangJT 2003 Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13 2498 2504
86. StarkCBreitkreutzBJRegulyTBoucherLBreitkreutzA 2006 BioGRID: a general repository for interaction datasets. Nucleic Acids Res 34 D535 539
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 11
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Evidence-Based Annotation of Gene Function in MR-1 Using Genome-Wide Fitness Profiling across 121 Conditions
- De Novo Origins of Human Genes
- TRY-5 Is a Sperm-Activating Protease in Seminal Fluid
- Cyclin D/CDK4 and Cyclin E/CDK2 Induce Distinct Cell Cycle Re-Entry Programs in Differentiated Muscle Cells