Skip to main content
SpringerLink
Log in

Dse1 may control cross talk between the pheromone and filamentation pathways in yeast

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

The filamentous/invasive growth pathway is activated by nutrient limitation in the haploid form of the yeast Saccharomyces cerevisiae, whereas exposure to mating-pheromone causes cells to differentiate into gametes. Although these two pathways respond to very different stimuli and generate very different responses, they utilize many of the same signaling components. This implies the need for robust mechanisms to maintain signal fidelity. Dse1 was identified in an allele-specific suppressor screen for proteins that interact with the pheromone-responsive Gβγ, and found to bind both to a Gβγ-affinity column, and to the shared MEKK, Ste11. Although overexpression of Dse1 stimulated invasive growth and transcription of both filamentation and mating-specific transcriptional reporters, deletion of DSE1 had no effect on these outputs. In contrast, pheromone hyper-induced transcription of the filamentation reporter in cells lacking Dse1 and in cells expressing a mutant form of Gβ that exhibits diminished interaction with Dse1. Thus, the interaction of Dse1 with both Gβ and Ste11 may be designed to control cross talk between the pheromone and filamentation pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1994) Protocols in molecular biology. Wiley, New York

    Google Scholar 

  • Bar EE, Ellicott AT, Stone DE (2003) Gβγ recruits Rho1 to the site of polarized growth during mating in budding yeast. J Biol Chem 278:21798–21804

    Article  PubMed  CAS  Google Scholar 

  • Bardwell L (2004) A walk-through of the yeast mating pheromone response pathway. Peptides 25:1465–1476

    Article  PubMed  CAS  Google Scholar 

  • Caldwell GA, Naider F, Becker JM (1995) Fungal lipopeptide mating pheromones: a model system for the study of protein prenylation. Microbiol Rev 59:406–422

    PubMed  CAS  Google Scholar 

  • Caponigro G, Abedi MR, Hurlburt AP, Maxfield A, Judd W, Kamb A (1998) Transdominant genetic analysis of a growth control pathway. Proc Natl Acad Sci USA 95:7508–7513

    Article  PubMed  CAS  Google Scholar 

  • Choi KY, Satterberg B, Lyons DM, Elion EA (1994) Ste5 tethers multiple protein kinases in the MAP kinase cascade required for mating in S. cerevisiae. Cell 78:499–512

    Article  PubMed  CAS  Google Scholar 

  • Cismowski MJ, Metodiev M, Draper E, Stone DE (2001) Biochemical analysis of yeast Gα mutants that enhance adaptation to pheromone. Biochem Biophys Res Commun 284:247–254

    Article  PubMed  CAS  Google Scholar 

  • Cole GM, Stone DE, Reed SI (1990) Stoichiometry of G protein subunits affects the Saccharomyces cerevisiae mating pheromone signal transduction pathway. Mol Cell Biol 10:510–517

    PubMed  CAS  Google Scholar 

  • Colman-Lerner A, Chin TE, Brent R (2001) Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates. Cell 107:739–750

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Doolin MT, Johnson AL, Johnston LH, Butler G (2001) Overlapping and distinct roles of the duplicated yeast transcription factors Ace2p and Swi5p. Mol Microbiol 40:422–432

    Article  PubMed  CAS  Google Scholar 

  • Drogen F, O’Rourke SM, Stucke VM, Jaquenoud M, Neiman AM, Peter M (2000) Phosphorylation of the MEKK Ste11p by the PAK-like kinase Ste20p is required for MAP kinase signaling in vivo. Curr Biol 10:630–639

    Article  PubMed  CAS  Google Scholar 

  • Elion EA (2000) Pheromone response, mating and cell biology. Curr Opin Microbiol 3:573–581

    Article  PubMed  CAS  Google Scholar 

  • Elion EA (2001) The Ste5p scaffold. J Cell Sci 114:3967–3978

    PubMed  CAS  Google Scholar 

  • Flatauer LJ, Zadeh SF, Bardwell L (2005) Mitogen-activated protein kinases with distinct requirements for Ste5 scaffolding influence signaling specificity in Saccharomyces cerevisiae. Mol Cell Biol 25:1793–1803

    Article  PubMed  CAS  Google Scholar 

  • Frydlova I, Malcova I, Vasicova P, Hasek J (2009) Deregulation of DSE1 gene expression results in aberrant budding within the birth scar and cell wall integrity pathway activation in Saccharomyces cerevisiae. Eukaryot Cell 8:586–594

    Article  PubMed  CAS  Google Scholar 

  • Fuller RS, Sterne RE, Thorner J (1988) Enzymes required for yeast prohormone processing. Annu Rev Physiol 50:345–362

    Article  PubMed  CAS  Google Scholar 

  • Gietz D, St Jean A, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20:1425

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gustin MC, Albertyn J, Alexander M, Davenport K (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62:1264–1300

    PubMed  CAS  Google Scholar 

  • Hagen DC, McCaffrey G, Sprague GF Jr (1986) Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a factor: gene sequence and implications for the structure of the presumed receptor. Proc Natl Acad Sci USA 83:1418–1422

    Article  PubMed  CAS  Google Scholar 

  • Harris K et al (2001) Role of scaffolds in MAP kinase pathway specificity revealed by custom design of pathway-dedicated signaling proteins. Curr Biol 11:1815–1824

    Article  PubMed  CAS  Google Scholar 

  • Huh WK et al (2003) Global analysis of protein localization in budding yeast. Nature 425:686–691

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153:163–168

    PubMed  CAS  Google Scholar 

  • King L, Butler G (1998) Ace2p, a regulator of CTS1 (chitinase) expression, affects pseudohyphal production in Saccharomyces cerevisiae. Curr Genet 34:183–191

    Article  PubMed  CAS  Google Scholar 

  • Kovacech B, Nasmyth K, Schuster T (1996) EGT2 gene transcription is induced predominantly by Swi5 in early G1. Mol Cell Biol 16:3264–3274

    PubMed  CAS  Google Scholar 

  • Kron SJ, Gow NA (1995) Budding yeast morphogenesis: signalling, cytoskeleton and cell cycle. Curr Opin Cell Biol 7:845–855

    Article  PubMed  CAS  Google Scholar 

  • Kron SJ, Styles CA, Fink GR (1994) Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol Biol Cell 5:1003–1022

    PubMed  CAS  Google Scholar 

  • Lamson RE, Winters MJ, Pryciak PM (2002) Cdc42 regulation of kinase activity and signaling by the yeast p21-activated kinase Ste20. Mol Cell Biol 22:2939–2951

    Article  PubMed  CAS  Google Scholar 

  • Li E, Meldrum E, Stratton HF, Stone DE (1998) Substitutions in the pheromone-responsive Gβ protein of Saccharomyces cerevisiae confer a defect in recovery from pheromone treatment. Genetics 148:947–961

    PubMed  CAS  Google Scholar 

  • Mackay V, Manney TR (1974) Mutations affecting sexual conjugation and related processes in Saccharomyces cerevisiae. II. Genetic analysis of nonmating mutants. Genetics 76:273–288

    PubMed  CAS  Google Scholar 

  • Madhani HD, Fink GR (1997) Combinatorial control required for the specificity of yeast MAPK signaling. Science 275:1314–1317

    Article  PubMed  CAS  Google Scholar 

  • Maleri S, Ge Q, Hackett EA, Wang Y, Dohlman HG, Errede B (2004) Persistent activation by constitutive Ste7 promotes Kss1-mediated invasive growth but fails to support Fus3-dependent mating in yeast. Mol Cell Biol 24:9221–9238

    Article  PubMed  CAS  Google Scholar 

  • Marcus S, Polverino A, Barr M, Wigler M (1994) Complexes between STE5 and components of the pheromone-responsive mitogen-activated protein kinase module. Proc Natl Acad Sci USA 91:7762–7766

    Article  PubMed  CAS  Google Scholar 

  • McClean MN, Mody A, Broach JR, Ramanathan S (2007) Cross-talk and decision making in MAP kinase pathways. Nat Genet 39:409–414

    Article  PubMed  CAS  Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Mosch HU, 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 USA 93:5352–5356

    Article  PubMed  CAS  Google Scholar 

  • Mosch HU, Kubler E, Krappmann S, Fink GR, Braus GH (1999) Crosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae. Mol Biol Cell 10:1325–1335

    PubMed  CAS  Google Scholar 

  • Nakafuku M, Itoh H, Nakamura S, Kaziro Y (1987) Occurrence in Saccharomyces cerevisiae of a gene homologous to the cDNA coding for the alpha subunit of mammalian G proteins. Proc Natl Acad Sci USA 84:2140–2144

    Article  PubMed  CAS  Google Scholar 

  • Palecek SP, Parikh AS, Kron SJ (2002) Sensing, signalling and integrating physical processes during Saccharomyces cerevisiae invasive and filamentous growth. Microbiology 148:893–907

    PubMed  CAS  Google Scholar 

  • Pan X, Heitman J (2000) Sok2 regulates yeast pseudohyphal differentiation via a transcription factor cascade that regulates cell–cell adhesion. Mol Cell Biol 20:8364–8372

    Article  PubMed  CAS  Google Scholar 

  • Peter M, Neiman AM, Park HO, van Lohuizen M, Herskowitz I (1996) Functional analysis of the interaction between the small GTP binding protein Cdc42 and the Ste20 protein kinase in yeast. EMBO J 15:7046–7059

    PubMed  CAS  Google Scholar 

  • Pryciak PM, Huntress FA (1998) Membrane recruitment of the kinase cascade scaffold protein Ste5 by the Gβγ complex underlies activation of the yeast pheromone response pathway. Genes Dev 12:2684–2697

    Article  PubMed  CAS  Google Scholar 

  • Reed SI, Hadwiger JA, Lorincz AT (1985) Protein kinase activity associated with the product of the yeast cell division cycle gene CDC28. Proc Natl Acad Sci USA 82:4055–4059

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Roberts RL, Mosch HU, Fink GR (1997) 14–3-3 proteins are essential for RAS/MAPK cascade signaling during pseudohyphal development in S. cerevisiae. Cell 89:1055–1065

    Article  PubMed  CAS  Google Scholar 

  • Sabbagh W Jr, Flatauer LJ, Bardwell AJ, Bardwell L (2001) Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation. Mol Cell 8:683–691

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Schaeffer HJ, Weber MJ (1999) Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol Cell Biol 19:2435–2444

    PubMed  CAS  Google Scholar 

  • Schwartz MA, Madhani HD (2004) Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. Annu Rev Genet 38:725–748

    Article  PubMed  CAS  Google Scholar 

  • Spiegel AM (1987) Signal transduction by guanine nucleotide binding proteins. Mol Cell Endocrinol 49:1–16

    Article  PubMed  CAS  Google Scholar 

  • Spiegel A et al (1988) Signal transduction by guanine nucleotide-binding proteins. Recent Prog Horm Res 44:337–375

    PubMed  CAS  Google Scholar 

  • Stevenson BJ, Rhodes N, Errede B, Sprague GF Jr (1992) Constitutive mutants of the protein kinase STE11 activate the yeast pheromone response pathway in the absence of the G protein. Genes Dev 6:1293–1304

    Article  PubMed  CAS  Google Scholar 

  • Stratton HF, Zhou J, Reed SI, Stone DE (1996) The mating-specific Gα protein of Saccharomyces cerevisiae downregulates the mating signal by a mechanism that is dependent on pheromone and independent of Gβγ sequestration. Mol Cell Biol 16:6325–6337

    PubMed  CAS  Google Scholar 

  • Trueheart J, Boeke JD, Fink GR (1987) Two genes required for cell fusion during yeast conjugation: evidence for a pheromone-induced surface protein. Mol Cell Biol 7:2316–2328

    PubMed  CAS  Google Scholar 

  • Whiteway M et al (1989) The STE4 and STE18 genes of yeast encode potential beta and gamma subunits of the mating factor receptor-coupled G protein. Cell 56:467–477

    Article  PubMed  CAS  Google Scholar 

  • Whiteway M, Hougan L, Thomas DY (1990) Overexpression of the STE4 gene leads to mating response in haploid Saccharomyces cerevisiae. Mol Cell Biol 10:217–222

    PubMed  CAS  Google Scholar 

  • Whitmarsh AJ, Davis RJ (1998) Structural organization of MAP-kinase signaling modules by scaffold proteins in yeast and mammals. Trends Biochem Sci 23:481–485

    Article  PubMed  CAS  Google Scholar 

  • Yashar B et al (1995) Yeast MEK-dependent signal transduction: response thresholds and parameters affecting fidelity. Mol Cell Biol 15:6545–6553

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank William Lu for technical assistance, and Beverly Errede and Peter Pryciak for strains and plasmids. This work was supported by National Science Foundation grant #MCB-0453964.

Author information

Author notes

  1. Edward Draper

    Present address: Center for Molecular Biology of Oral Diseases, University of Illinois at Chicago, 801 South Paulina Avenue, Chicago, IL, 60612, USA

  2. Eli E. Bar

    Present address: Neuropathology Laboratory 558 Ross Research Building, The Johns Hopkins University, 720 Rutland Avenue, Baltimore, MD, 21205, USA

Authors and Affiliations

  1. Laboratory for Molecular Biology (M/C 567), Department of Biological Sciences, University of Illinois at Chicago, 900 South Ashland Ave, Chicago, IL, 60607, USA

    Edward Draper, Oleksii Dubrovskyi, Eli E. Bar & David E. Stone

Authors
  1. Edward Draper
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Oleksii Dubrovskyi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eli E. Bar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David E. Stone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David E. Stone.

Additional information

Communicated by S. Hohmann.

E. Draper and O. Dubrovskyi contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Draper, E., Dubrovskyi, O., Bar, E.E. et al. Dse1 may control cross talk between the pheromone and filamentation pathways in yeast. Curr Genet 55, 611–621 (2009). https://doi.org/10.1007/s00294-009-0274-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-009-0274-6

Keywords

Search

Navigation