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Article

The Transcription Factors Tec1 and Ste12 Interact with Coregulators Msa1 and Msa2 To Activate Adhesion and Multicellular Development

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Pages 2283-2293 | Received 04 Dec 2013, Accepted 24 Mar 2014, Published online: 20 Mar 2023

REFERENCES

  • Levine M, Davidson EH. 2005. Gene regulatory networks for development. Proc. Natl. Acad. Sci. U. S. A. 102:4936–4942. http://dx.doi.org/10.1073/pnas.0408031102.
  • Busser BW, Bulyk ML, Michelson AM. 2008. Toward a systems-level understanding of developmental regulatory networks. Curr. Opin. Genet. Dev. 18:521–529. http://dx.doi.org/10.1016/j.gde.2008.09.003.
  • Reményi A, Schöler HR, Wilmanns M. 2004. Combinatorial control of gene expression. Nat. Struct. Mol. Biol. 11:812–815. http://dx.doi.org/10.1038/nsmb820.
  • Hahn S, Young ET. 2011. Transcriptional regulation in Saccharomyces cerevisiae: transcription factor regulation and function, mechanisms of initiation, and roles of activators and coactivators. Genetics 189:705–736. http://dx.doi.org/10.1534/genetics.111.127019.
  • Cullen PJ, Sprague GFJr. 2012. The regulation of filamentous growth in yeast. Genetics 190:23–49. http://dx.doi.org/10.1534/genetics.111.127456.
  • Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR. 1992. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68:1077–1090. http://dx.doi.org/10.1016/0092-8674(92)90079-R.
  • Reynolds TB, Fink GR. 2001. Bakers' yeast, a model for fungal biofilm formation. Science 291:878–881. http://dx.doi.org/10.1126/science.291.5505.878.
  • Brückner S, Mösch H-U. 2012. Choosing the right lifestyle: adhesion and development in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 36:25–58. http://dx.doi.org/10.1111/j.1574-6976.2011.00275.x.
  • Zaman S, Lippman SI, Zhao X, Broach JR. 2008. How Saccharomyces responds to nutrients. Annu. Rev. Genet. 42:27–81. http://dx.doi.org/10.1146/annurev.genet.41.110306.130206.
  • Chen RE, Thorner J. 2007. Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1773:1311–1340. http://dx.doi.org/10.1016/j.bbamcr.2007.05.003.
  • Dolan JW, Kirkman C, Fields S. 1989. The yeast Ste12 protein binds to the DNA sequence mediating pheromone induction. Proc. Natl. Acad. Sci. U. S. A. 86:5703–5707. http://dx.doi.org/10.1073/pnas.86.15.5703.
  • Errede B, Ammerer G. 1989. Ste12, a protein involved in cell-type-specific transcription and signal transduction in yeast, is part of protein-DNA complexes. Genes Dev. 3:1349–1361. http://dx.doi.org/10.1101/gad.3.9.1349.
  • Liu H, Styles CA, Fink GR. 1993. Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262:1741–1744. http://dx.doi.org/10.1126/science.8259520.
  • Roberts RL, Fink GR. 1994. 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. 8:2974–2985. http://dx.doi.org/10.1101/gad.8.24.2974.
  • Gavrias V, Andrianopoulos A, Gimeno CJ, Timberlake WE. 1996. Saccharomyces cerevisiae TEC1 is required for pseudohyphal growth. Mol. Microbiol. 19:1255–1263. http://dx.doi.org/10.1111/j.1365-2958.1996.tb02470.x.
  • Mösch H-U, Fink GR. 1997. Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. Genetics 145:671–684.
  • Lo WS, Dranginis AM. 1998. The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol. Biol. Cell 9:161–171. http://dx.doi.org/10.1091/mbc.9.1.161.
  • Rupp S, Summers E, Lo HJ, Madhani H, Fink GR. 1999. MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J. 18:1257–1269. http://dx.doi.org/10.1093/emboj/18.5.1257.
  • Zeitlinger J, Simon I, Harbison CT, Hannett NM, Volkert TL, Fink GR, Young RA. 2003. Program-specific distribution of a transcription factor dependent on partner transcription factor and MAPK signaling. Cell 113:395–404. http://dx.doi.org/10.1016/S0092-8674(03)00301-5.
  • Bao MZ, Schwartz MA, Cantin GT, Yates JRIII, Madhani HD. 2004. Pheromone-dependent destruction of the Tec1 transcription factor is required for MAP kinase signaling specificity in yeast. Cell 119:991–1000. http://dx.doi.org/10.1016/j.cell.2004.11.052.
  • Brückner S, Köhler T, Braus GH, Heise B, Bolte M, Mösch H-U. 2004. Differential regulation of Tec1 by Fus3 and Kss1 confers signaling specificity in yeast development. Curr. Genet. 46:331–342. http://dx.doi.org/10.1007/s00294-004-0545-1.
  • Chou S, Huang L, Liu H. 2004. Fus3-regulated Tec1 degradation through SCFCdc4 determines MAPK signaling specificity during mating in yeast. Cell 119:981–990. http://dx.doi.org/10.1016/j.cell.2004.11.053.
  • Brückner S, Kern S, Birke R, Saugar I, Ulrich H-D, Mösch H-U. 2011. The TEA transcription factor Tec1 links TOR and MAPK pathways to coordinate yeast development. Genetics 189:479–494. http://dx.doi.org/10.1534/genetics.111.133629.
  • Madhani HD, Fink GR. 1997. Combinatorial control required for the specificity of yeast MAPK signaling. Science 275:1314–1317. http://dx.doi.org/10.1126/science.275.5304.1314.
  • Borneman AR, Gianoulis TA, Zhang ZD, Yu H, Rozowsky J, Seringhaus MR, Wang LY, Gerstein M, Snyder M. 2007. Divergence of transcription factor binding sites across related yeast species. Science 317:815–819. http://dx.doi.org/10.1126/science.1140748.
  • Mueller CG, Nordheim A. 1991. A protein domain conserved between yeast MCM1 and human SRF directs ternary complex formation. EMBO J. 10:4219–4229.
  • Primig M, Winkler H, Ammerer G. 1991. The DNA binding and oligomerization domain of MCM1 is sufficient for its interaction with other regulatory proteins. EMBO J. 10:4209–4218.
  • Yuan YO, Stroke IL, Fields S. 1993. Coupling of cell identity to signal response in yeast: interaction between the alpha 1 and Ste12 proteins. Genes Dev. 7:1584–1597. http://dx.doi.org/10.1101/gad.7.8.1584.
  • Chou S, Lane S, Liu H. 2006. Regulation of mating and filamentation genes by two distinct Ste12 complexes in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:4794–4805. http://dx.doi.org/10.1128/MCB.02053-05.
  • Cook JG, Bardwell L, Kron SJ, Thorner J. 1996. Two novel targets of the MAP kinase Kss1 are negative regulators of invasive growth in the yeast Saccharomyces cerevisiae. Genes Dev. 10:2831–2848. http://dx.doi.org/10.1101/gad.10.22.2831.
  • Cook JG, Bardwell L, Thorner J. 1997. Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous-growth signalling pathway. Nature 390:85–88. http://dx.doi.org/10.1038/36355.
  • Tedford K, Kim S, Sa D, Stevens K, Tyers M. 1997. Regulation of the mating pheromone and invasive growth responses in yeast by two MAP kinase substrates. Curr. Biol. 7:228–238. http://dx.doi.org/10.1016/S0960-9822(06)00118-7.
  • Bardwell L, Cook JG, Voora D, Baggott DM, Martinez AR, Thorner J. 1998. Repression of yeast Ste12 transcription factor by direct binding of unphosphorylated Kss1 MAPK and its regulation by the Ste7 MEK. Genes Dev. 12:2887–2898. http://dx.doi.org/10.1101/gad.12.18.2887.
  • Bardwell L, Cook JG, Zhu-Shimoni JX, Voora D, Thorner J. 1998. 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. 95:15400–15405. http://dx.doi.org/10.1073/pnas.95.26.15400.
  • Andrianopoulos A, Timberlake WE. 1991. ATTS, a new and conserved DNA binding domain. Plant Cell 3:747–748. http://dx.doi.org/10.1105/tpc.3.8.747.
  • Anbanandam A, Albarado DC, Nguyen CT, Halder G, Gao X, Veeraraghavan S. 2006. Insights into transcription enhancer factor 1 (TEF-1) activity from the solution structure of the TEA domain. Proc. Natl. Acad. Sci. U. S. A. 103:17225–17230. http://dx.doi.org/10.1073/pnas.0607171103.
  • Köhler T, Wesche S, Taheri N, Braus GH, Mösch H-U. 2002. Dual role of the Saccharomyces cerevisiae TEA/ATTS family transcription factor Tec1p in regulation of gene expression and cellular development. Eukaryot. Cell 1:673–686. http://dx.doi.org/10.1128/EC.1.5.673-686.2002.
  • Heise B, van der Felden J, Kern S, Malcher M, Brückner S, Mösch H-U. 2010. The TEA transcription factor Tec1 confers promoter-specific gene regulation by Ste12-dependent and -independent mechanisms. Eukaryot. Cell 9:514–531. http://dx.doi.org/10.1128/EC.00251-09.
  • Ashe M, de Bruin RA, Kalashnikova T, McDonald WH, Yates JRIII, 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.
  • Golemis EA, Brent R. 1992. Fused protein domains inhibit DNA binding by LexA. Mol. Cell. Biol. 12:3006–3014.
  • 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.
  • Guthrie C, Fink GR. 1991. Guide to yeast genetics and molecular biology. Methods Enzymol. 194:1–863.
  • Fashena SJ, Serebriiskii IG, Golemis EA. 2000. LexA-based two-hybrid systems. Methods Enzymol. 328:14–26. http://dx.doi.org/10.1016/S0076-6879(00)28387-0.
  • Hackett EA, Esch RK, Maleri S, Errede B. 2006. A family of destabilized cyan fluorescent proteins as transcriptional reporters in S. cerevisiae. Yeast 23:333–349. http://dx.doi.org/10.1002/yea.1358.
  • Jansen G, Wu CL, Schade B, Thomas DY, Whiteway M. 2005. Drag&Drop cloning in yeast. Gene 344:43–51. http://dx.doi.org/10.1016/j.gene.2004.10.016.
  • Mösch H-U, Roberts RL, Fink GR. 1996. Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 93:5352–5356. http://dx.doi.org/10.1073/pnas.93.11.5352.
  • Sheff MA, Thorn KS. 2004. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21:661–670. http://dx.doi.org/10.1002/yea.1130.
  • Jungbluth M, Renicke C, Taxis C. 2010. Targeted protein depletion in Saccharomyces cerevisiae by activation of a bidirectional degron. BMC Syst. Biol. 4:176. http://dx.doi.org/10.1186/1752-0509-4-176.
  • Yaffe MP, Schatz G. 1984. Two nuclear mutations that block mitochondrial protein import in yeast. Proc. Natl. Acad. Sci. U. S. A. 81:4819–4823. http://dx.doi.org/10.1073/pnas.81.15.4819.
  • Aparicio O, Geisberg JV, Sekinger E, Yang A, Moqtaderi Z, Struhl K. 2005. Chromatin immunoprecipitation for determining the association of proteins with specific genomic sequences in vivo. Curr. Protoc. Mol. Biol. 2005: Chapter 21:Unit 21.23. http://dx.doi.org/10.1002/0471142727.mb2103s69.
  • Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9:3273–3297. http://dx.doi.org/10.1091/mbc.9.12.3273.
  • Kirkman-Correia C, Stroke IL, Fields S. 1993. Functional domains of the yeast STE12 protein, a pheromone-responsive transcriptional activator. Mol. Cell. Biol. 13:3765–3772.
  • 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.
  • Cullen PJ, Sabbagh WJr, Graham E, Irick MM, van Olden EK, Neal C, Delrow J, Bardwell L, Sprague GFJr. 2004. A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev. 18:1695–1708. http://dx.doi.org/10.1101/gad.1178604.
  • Chavel CA, Dionne HM, Birkaya B, Joshi J, Cullen PJ. 2010. Multiple signals converge on a differentiation MAPK pathway. PLoS Genet. 6:e1000883. http://dx.doi.org/10.1371/journal.pgen.1000883.
  • Madhani HD, Galitski T, Lander ES, Fink GR. 1999. Effectors of a developmental mitogen-activated protein kinase cascade revealed by expression signatures of signaling mutants. Proc. Natl. Acad. Sci. U. S. A. 96:12530–12535. http://dx.doi.org/10.1073/pnas.96.22.12530.
  • Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, Shah K, Shokat KM, Morgan DO. 2003. Targets of the cyclin-dependent kinase Cdk1. Nature 425:859–864. http://dx.doi.org/10.1038/nature02062.
  • Peter M, Gartner A, Horecka J, Ammerer G, Herskowitz I. 1993. FAR1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell 73:747–760. http://dx.doi.org/10.1016/0092-8674(93)90254-N.
  • Doncic A, Falleur-Fettig M, Skotheim JM. 2011. Distinct interactions select and maintain a specific cell fate. Mol. Cell 43:528–539. http://dx.doi.org/10.1016/j.molcel.2011.06.025.
  • Liu H, Köhler J, Fink GR. 1994. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266:1723–1726. http://dx.doi.org/10.1126/science.7992058.
  • Pesole G, Lotti M, Alberghina L, Saccone C. 1995. Evolutionary origin of nonuniversal CUGSer codon in some Candida species as inferred from a molecular phylogeny. Genetics 141:903–907.
  • Schweizer A, Rupp S, Taylor BN, Rollinghoff M, Schroppel K. 2000. The TEA/ATTS transcription factor CaTec1p regulates hyphal development and virulence in Candida albicans. Mol. Microbiol. 38:435–445. http://dx.doi.org/10.1046/j.1365-2958.2000.02132.x.
  • Hedges SB. 2002. The origin and evolution of model organisms. Nat. Rev. Genet. 3:838–849. http://dx.doi.org/10.1038/nrg929.
  • Borneman AR, Leigh-Bell JA, Yu H, Bertone P, Gerstein M, Snyder M. 2006. Target hub proteins serve as master regulators of development in yeast. Genes Dev. 20:435–448. http://dx.doi.org/10.1101/gad.1389306.
  • Taylor JW, Berbee ML. 2006. Dating divergences in the Fungal Tree of Life: review and new analyses. Mycologia 98:838–849. http://dx.doi.org/10.3852/mycologia.98.6.838.
  • Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, Hernday AD, Tuch BB, Andes DR, Johnson AD. 2012. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148:126–138. http://dx.doi.org/10.1016/j.cell.2011.10.048.
  • Hilman D, Gat U. 2011. The evolutionary history of YAP and the hippo/YAP pathway. Mol. Biol. Evol. 28:2403–2417. http://dx.doi.org/10.1093/molbev/msr065.
  • Zhao B, Tumaneng K, Guan KL. 2011. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 13:877–883. http://dx.doi.org/10.1038/ncb2303.
  • Varelas X, Wrana JL. 2012. Coordinating developmental signaling: novel roles for the Hippo pathway. Trends Cell Biol. 22:88–96. http://dx.doi.org/10.1016/j.tcb.2011.10.002.
  • Wray GA. 2007. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8:206–216. http://dx.doi.org/10.1038/nrg2063.
  • Tuch BB, Li H, Johnson AD. 2008. Evolution of eukaryotic transcription circuits. Science 319:1797–1799. http://dx.doi.org/10.1126/science.1152398.
  • Wohlbach DJ, Thompson DA, Gasch AP, Regev A. 2009. From elements to modules: regulatory evolution in Ascomycota fungi. Curr. Opin. Genet. Dev. 19:571–578. http://dx.doi.org/10.1016/j.gde.2009.09.007.

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