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Article

Hog1 Targets Whi5 and Msa1 Transcription Factors To Downregulate Cyclin Expression upon Stress

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Pages 1606-1618 | Received 21 Oct 2014, Accepted 20 Feb 2015, Published online: 20 Mar 2023

REFERENCES

  • Dirick L, Bohm T, Nasmyth K. 1995. Roles and regulation of Cln-Cdc28 kinases at the start of the cell cycle of Saccharomyces cerevisiae. EMBO J 14:4803–4813.
  • Dirick L, Nasmyth K. 1991. Positive feedback in the activation of G1 cyclins in yeast. Nature 351:754–757. http://dx.doi.org/10.1038/351754a0.
  • Skotheim JM, Di TS, Siggia ED, Cross FR. 2008. Positive feedback of G1 cyclins ensures coherent cell cycle entry. Nature 454:291–296. http://dx.doi.org/10.1038/nature07118.
  • Andrews BJ, Herskowitz I. 1989. The yeast SWI4 protein contains a motif present in developmental regulators and is part of a complex involved in cell-cycle-dependent transcription. Nature 342:830–833. http://dx.doi.org/10.1038/342830a0.
  • Nasmyth K, Dirick L. 1991. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell 66:995–1013. http://dx.doi.org/10.1016/0092-8674(91)90444-4.
  • Ogas J, Andrews BJ, Herskowitz I. 1991. Transcriptional activation of CLN1, CLN2, and a putative new G1 cyclin (HCS26) by SWI4, a positive regulator of G1-specific transcription. Cell 66:1015–1026. http://dx.doi.org/10.1016/0092-8674(91)90445-5.
  • Koch C, Moll T, Neuberg M, Ahorn H, Nasmyth K. 1993. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science 261:1551–1557. http://dx.doi.org/10.1126/science.8372350.
  • de Bruin RA, Kalashnikova TI, Chahwan C, McDonald WH, Wohlschlegel J, Yates J, III, Russell P, Wittenberg C. 2006. Constraining G1-specific transcription to late G1 phase: the MBF-associated corepressor Nrm1 acts via negative feedback. Mol Cell 23:483–496. http://dx.doi.org/10.1016/j.molcel.2006.06.025.
  • Cross FR, Hoek M, McKinney JD, Tinkelenberg AH. 1994. Role of Swi4 in cell cycle regulation of CLN2 expression. Mol Cell Biol 14:4779–4787.
  • Eser U, Falleur-Fettig M, Johnson A, Skotheim JM. 2011. Commitment to a cellular transition precedes genome-wide transcriptional change. Mol Cell 43:515–527. http://dx.doi.org/10.1016/j.molcel.2011.06.024.
  • Stuart D, Wittenberg C. 1994. Cell cycle-dependent transcription of CLN2 is conferred by multiple distinct cis-acting regulatory elements. Mol Cell Biol 14:4788–4801.
  • Lew DJ, Weinert T, Pringle JR. 1997. Cell cycle control in Saccharomyces cerevisiae. Cold Spring Harbor Monogr Arch 21:607–695. http://dx.doi.org/10.1101/087969364.21C.607.
  • Schwob E, Nasmyth K. 1993. CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev 7:1160–1175. http://dx.doi.org/10.1101/gad.7.7a.1160.
  • Costanzo M, Nishikawa JL, Tang X, Millman JS, Schub O, Breitkreuz K, Dewar D, Rupes I, Andrews B, Tyers M. 2004. CDK activity antagonizes Whi5, an inhibitor of G1/S transcription in yeast. Cell 117:899–913. http://dx.doi.org/10.1016/j.cell.2004.05.024.
  • de Bruin RA, McDonald WH, Kalashnikova TI, Yates J, III, Wittenberg C. 2004. Cln3 activates G1-specific transcription via phosphorylation of the SBF bound repressor Whi5. Cell 117:887–898. http://dx.doi.org/10.1016/j.cell.2004.05.025.
  • Huang D, Kaluarachchi S, van DD, Friesen H, Sopko R, Ye W, Bastajian N, Moffat J, Sassi H, Costanzo M, Andrews BJ. 2009. Dual regulation by pairs of cyclin-dependent protein kinases and histone deacetylases controls G1 transcription in budding yeast. PLoS Biol 7:e1000188. http://dx.doi.org/10.1371/journal.pbio.1000188.
  • Kosugi S, Hasebe M, Tomita M, Yanagawa H. 2009. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci U S A 106:10171–10176. http://dx.doi.org/10.1073/pnas.0900604106.
  • Taberner FJ, Quilis I, Igual JC. 2009. Spatial regulation of the start repressor Whi5. Cell Cycle 8:3013–3022. http://dx.doi.org/10.4161/cc.8.18.9621.
  • Mendenhall MD. 1993. An inhibitor of p34CDC28 protein kinase activity from Saccharomyces cerevisiae. Science 259:216–219. http://dx.doi.org/10.1126/science.8421781.
  • Schwob E, Bohm T, Mendenhall MD, Nasmyth K. 1994. The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell 79:233–244. http://dx.doi.org/10.1016/0092-8674(94)90193-7.
  • Feldman RM, Correll CC, Kaplan KB, Deshaies RJ. 1997. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91:221–230. http://dx.doi.org/10.1016/S0092-8674(00)80404-3.
  • Sheaff RJ, Roberts JM. 1996. End of the line: proteolytic degradation of cyclin-dependent kinase inhibitors. Chem Biol 3:869–873. http://dx.doi.org/10.1016/S1074-5521(96)90174-X.
  • Verma R, Annan RS, Huddleston MJ, Carr SA, Reynard G, Deshaies RJ. 1997. Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science 278:455–460. http://dx.doi.org/10.1126/science.278.5337.455.
  • Tanaka S, Umemori T, Hirai K, Muramatsu S, Kamimura Y, Araki H. 2007. CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 445:328–332. http://dx.doi.org/10.1038/nature05465.
  • Zegerman P, Diffley JF. 2007. Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 445:281–285. http://dx.doi.org/10.1038/nature05432.
  • Yang X, Lau KY, Sevim V, Tang C. 2013. Design principles of the yeast G1/S switch. PLoS Biol 11:e1001673. http://dx.doi.org/10.1371/journal.pbio.1001673.
  • Costanzo M, Schub O, Andrews B. 2003. G1 transcription factors are differentially regulated in Saccharomyces cerevisiae by the Swi6-binding protein Stb1. Mol Cell Biol 23:5064–5077. http://dx.doi.org/10.1128/MCB.23.14.5064-5077.2003.
  • Ho Y, Costanzo M, Moore L, Kobayashi R, Andrews BJ. 1999. Regulation of transcription at the Saccharomyces cerevisiae Start transition by Stb1, a Swi6-binding protein. Mol Cell Biol 19:5267–5278.
  • Li JM, Tetzlaff MT, Elledge SJ. 2008. Identification of MSA1, a cell cycle-regulated, dosage suppressor of drc1/sld2 and dpb11 mutants. Cell Cycle 7:3388–3398. http://dx.doi.org/10.4161/cc.7.21.6932.
  • Ashe M, de Bruin RA, Kalashnikova T, McDonald WH, Yates JR, Wittenberg C. 2008. The SBF-and MBF-associated protein Msa1 is required for proper timing of G1-specific transcription in Saccharomyces cerevisiae. J Biol Chem 283:6040–6049. http://dx.doi.org/10.1074/jbc.M708248200.
  • van der Felden J, Weisser S, Brückner S, Lenz P, Mösch HU. 2014. The transcription factors Tec1 and Ste12 interact with coregulators Msa1 and Msa2 to activate adhesion and multicellular development. Mol Cell Biol 34:2283–2293. http://dx.doi.org/10.1128/MCB.01599-13.
  • Hohmann S. 2009. Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae. FEBS Lett 583:4025–4029. http://dx.doi.org/10.1016/j.febslet.2009.10.069.
  • Saito H, Posas F. 2012. Response to hyperosmotic stress. Genetics 192:289–318. http://dx.doi.org/10.1534/genetics.112.140863.
  • de Nadal E, Ammerer G, Posas F. 2011. Controlling gene expression in response to stress. Nat Rev Genet 12:833–845. http://dx.doi.org/10.1038/nrg3055.
  • Alexander MR, Tyers M, Perret M, Craig BM, Fang KS, Gustin MC. 2001. Regulation of cell cycle progression by Swe1p and Hog1p following hypertonic stress. Mol Biol Cell 12:53–62. http://dx.doi.org/10.1091/mbc.12.1.53.
  • Bellí G, Gari E, Aldea M, Herrero E. 2001. Osmotic stress causes a G1 cell cycle delay and downregulation of Cln3/Cdc28 activity in Saccharomyces cerevisiae. Mol Microbiol 39:1022–1035. http://dx.doi.org/10.1046/j.1365-2958.2001.02297.x.
  • Clotet J, Escoté X, Adrover MA, Yaakov G, Gari E, Aldea M, de Nadal E, Posas F. 2006. Phosphorylation of Hsl1 by Hog1 leads to a G2 arrest essential for cell survival at high osmolarity. EMBO J 25:2338–2346. http://dx.doi.org/10.1038/sj.emboj.7601095.
  • Duch A, Felipe-Abrio I, Barroso S, Yaakov G, Garcia-Rubio M, Aguilera A, de Nadal E, Posas F. 2013. Coordinated control of replication and transcription by a SAPK protects genomic integrity. Nature 493:116–119. http://dx.doi.org/10.1038/nature11675.
  • Escoté X, Zapater M, Clotet J, Posas F. 2004. Hog1 mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1. Nat Cell Biol 6:997–1002. http://dx.doi.org/10.1038/ncb1174.
  • Yaakov G, Duch A, Garcia-Rubio M, Clotet J, Jimenez J, Aguilera A, Posas F. 2009. The stress-activated protein kinase Hog1 mediates S phase delay in response to osmostress. Mol Biol Cell 20:3572–3582. http://dx.doi.org/10.1091/mbc.E09-02-0129.
  • Adrover MA, Zi Z, Duch A, Schaber J, Gonzalez-Novo A, Jimenez J, Nadal-Ribelles M, Clotet J, Klipp E, Posas F. 2011. Time-dependent quantitative multicomponent control of the G1-S network by the stress-activated protein kinase Hog1 upon osmostress. Sci Signal 4:ra63. http://dx.doi.org/10.1126/scisignal.2002204.
  • Radmaneshfar E, Kaloriti D, Gustin MC, Gow NA, Brown AJ, Grebogi C, Romano MC, Thiel M. 2013. From START to FINISH: the influence of osmotic stress on the cell cycle. PLoS One 8:e68067. http://dx.doi.org/10.1371/journal.pone.0068067.
  • Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, Knop M. 2004. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21:947–962. http://dx.doi.org/10.1002/yea.1142.
  • Zapater M, Sohrmann M, Peter M, Posas F, de Nadal E. 2007. Selective requirement for SAGA in Hog1-mediated gene expression depending on the severity of the external osmostress conditions. Mol Cell Biol 27:3900–3910. http://dx.doi.org/10.1128/MCB.00089-07.
  • de Nadal E, Posas F. 2010. Multilayered control of gene expression by stress-activated protein kinases. EMBO J 29:4–13. http://dx.doi.org/10.1038/emboj.2009.346.
  • Miller C, Schwalb B, Maier K, Schulz D, Dumcke S, Zacher B, Mayer A, Sydow J, Marcinowski L, Dolken L, Martin DE, Tresch A, Cramer P. 2011. Dynamic transcriptome analysis measures rates of mRNA synthesis and decay in yeast. Mol Syst Biol 7:458. http://dx.doi.org/10.1038/msb.2010.112.
  • Romero-Santacreu L, Moreno J, Perez-Ortin JE, Alepuz P. 2009. Specific and global regulation of mRNA stability during osmotic stress in Saccharomyces cerevisiae. RNA 15:1110–1120. http://dx.doi.org/10.1261/rna.1435709.
  • Pelet S, Rudolf F, Nadal-Ribelles M, de Nadal E, Posas F, Peter M. 2011. Transient activation of the HOG MAPK pathway regulates bimodal gene expression. Science 332:732–735. http://dx.doi.org/10.1126/science.1198851.
  • Nadal-Ribelles M, Conde N, Flores O, Gonzalez-Vallinas J, Eyras E, Orozco M, de Nadal E, Posas F. 2012. Hog1 bypasses stress-mediated down-regulation of transcription by RNA polymerase II redistribution and chromatin remodeling. Genome Biol 13:R106. http://dx.doi.org/10.1186/gb-2012-13-11-r106.
  • Proft M, Struhl K. 2004. MAP kinase-mediated stress relief that precedes and regulates the timing of transcriptional induction. Cell 118:351–361. http://dx.doi.org/10.1016/j.cell.2004.07.016.
  • Alepuz PM, de Nadal E, Zapater M, Ammerer G, Posas F. 2003. Osmostress-induced transcription by Hot1 depends on a Hog1-mediated recruitment of the RNA Pol II. EMBO J 22:2433–2442. http://dx.doi.org/10.1093/emboj/cdg243.
  • Pokholok DK, Zeitlinger J, Hannett NM, Reynolds DB, Young RA. 2006. Activated signal transduction kinases frequently occupy target genes. Science 313:533–536. http://dx.doi.org/10.1126/science.1127677.
  • Vendrell A, Martinez-Pastor M, Gonzalez-Novo A, Pascual-Ahuir A, Sinclair DA, Proft M, Posas F. 2011. Sir2 histone deacetylase prevents programmed cell death caused by sustained activation of the Hog1 stress-activated protein kinase. EMBO Rep 12:1062–1068. http://dx.doi.org/10.1038/embor.2011.154.
  • Wagner MV, Smolka MB, De Bruin RA, Zhou H, Wittenberg C, Dowdy SF. 2009. Whi5 regulation by site specific CDK-phosphorylation in Saccharomyces cerevisiae. PLoS One 4:e4300. http://dx.doi.org/10.1371/journal.pone.0004300.
  • Travesa A, Kalashnikova TI, de Bruin RA, Cass SR, Chahwan C, Lee DE, Lowndes NF, Wittenberg C. 2013. Repression of G1/S transcription is mediated via interaction of the GTB motifs of Nrm1 and Whi5 with Swi6. Mol Cell Biol 33:1476–1486. http://dx.doi.org/10.1128/MCB.01333-12.
  • Duch A, de Nadal E, Posas F. 2012. The p38 and Hog1 SAPKs control cell cycle progression in response to environmental stresses. FEBS Lett 586:2925–2931. http://dx.doi.org/10.1016/j.febslet.2012.07.034.
  • Nadal-Ribelles M, Sole C, Xu Z, Steinmetz LM, de Nadal E, Posas F. 2014. Control of Cdc28 CDK1 by a stress-induced lncRNA. Mol Cell 53:549–561. http://dx.doi.org/10.1016/j.molcel.2014.01.006.

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