Skip to main content
SpringerLink
Log in

Functional interaction between Cdc42 and the stress MAPK signaling pathway during the regulation of fission yeast polarized growth

  • Review
  • Published:
International Microbiology Aims and scope Submit manuscript

Abstract

Cell polarization can be defined as the generation and maintenance of directional cellular organization. The spatial distribution and protein or lipid composition of the cell are not symmetric but organized in specialized domains which allow cells to grow and acquire a certain shape that is closely linked to their physiological function. The establishment and maintenance of polarized growth requires the coordination of diverse processes including cytoskeletal dynamics, membrane trafficking, and signaling cascade regulation. Some of the major players involved in the selection and maintenance of sites for polarized growth are Rho GTPases, which recognize the polarization site and transmit the signal to regulatory proteins of the cytoskeleton. Additionally, cytoskeletal organization, polarized secretion, and endocytosis are controlled by signaling pathways including those mediated by mitogen-activated protein kinases (MAPKs). Rho GTPases and the MAPK signaling pathways are strongly conserved from yeast to mammals, suggesting that the basic mechanisms of polarized growth have been maintained throughout evolution. For this reason, the study of how polarized growth is established and regulated in simple organisms such as the fission yeast Schizosaccharomyces pombe has contributed to broaden our knowledge about these processes in multicellular organisms. We review here the function of the Cdc42 GTPase and the stress activated MAPK (SAPK) signaling pathways during fission yeast polarized growth, and discuss the relevance of the crosstalk between both 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

Similar content being viewed by others

References

  • Aicart-Ramos C, Valero RA, Rodriguez-Crespo I (2011) Protein palmitoylation and subcellular trafficking. Biochim Biophys Acta 1808:2981–2994

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Tabarés I, Grallert A, Ortiz JM, Hagan IM (2007) Schizosaccharomyces pombe protein phosphatase 1 in mitosis, endocytosis and a partnership with Wsh3/Tea4 to control polarised growth. J Cell Sci 120:3589–3601

    Article  PubMed  CAS  Google Scholar 

  • Arellano M, Durán A, Pérez P (1996) Rho 1 GTPase activates the (1-3)beta-D-glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. EMBO J 15:4584–4591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arellano M, Valdivieso MH, Calonge TM, Coll PM, Duran A, Perez P (1999) Schizosaccharomyces pombe protein kinase C homologues, pck1p and pck2p, are targets of rho1p and rho2p and differentially regulate cell integrity. J Cell Sci 112:3569–3578

    Article  CAS  PubMed  Google Scholar 

  • Asp E, Nilsson D, Sunnerhagen P (2008) Fission yeast mitogen-activated protein kinase Sty1 interacts with translation factors. Eukaryot Cell 7:328–338

    Article  CAS  PubMed  Google Scholar 

  • Attanapola SL, Alexander CJ, Mulvihill DP (2009) Ste20-kinase-dependent TEDS-site phosphorylation modulates the dynamic localisation and endocytic function of the fission yeast class I myosin, Myo1. J Cell Sci 122:3856–3861

    Article  CAS  PubMed  Google Scholar 

  • Bähler J, Pringle JR (1998) Pom1p, a fission yeast protein kinase that provides positional information for both polarized growth and cytokinesis. Genes Dev 12:1356–1370

    Article  PubMed  PubMed Central  Google Scholar 

  • Bendezu FO, Martin SG (2011) Actin cables and the exocyst form two independent morphogenesis pathways in the fission yeast. Mol Biol Cell 22:44–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bendezu FO, Vincenzetti V, Vavylonis D, Wyss R, Vogel H, Martin SG (2015) Spontaneous Cdc42 polarization independent of GDI-mediated extraction and actin-based trafficking. PLoS Biol 13:e1002097

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Berlanga JJ, Rivero D, Martin R, Herrero S, Moreno S, de Haro C (2010) Role of mitogen-activated protein kinase Sty1 in regulation of eukaryotic initiation factor 2alpha kinases in response to environmental stress in Schizosaccharomyces pombe. Eukaryot Cell 9:194–207

    Article  CAS  PubMed  Google Scholar 

  • Bicho CC, Kelly DA, Snaith HA, Goryachev AB, Sawin KE (2010) A catalytic role for Mod5 in the formation of the Tea1 cell polarity landmark. Curr Biol 20:1752–1757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bluthgen N, Legewie S (2008) Systems analysis of MAPK signal transduction. Essays in Biochem 45:95–107

    Article  Google Scholar 

  • Bos JL, Rehmann H, Wittinghofer A (2007) GEFs and GAPs: critical elements in the control of small G proteins. Cell 129:865–877

    Article  CAS  PubMed  Google Scholar 

  • Buck V, Quinn J, Soto Pino T, Martin H, Saldanha J, Makino K, Morgan BA, Millar JB (2001) Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol Biol Cell 12:407–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabib E, Drgonová J, Drgon T (1998) Role of small G proteins in yeast cell polarization and wall biosynthesis. Annu Rev Biochem 67:307–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calonge TM, Nakano K, Arellano M, Arai R, Katayama S, Toda T, Mabuchi I, Perez P (2000) Schizosaccharomyces pombe rho2p GTPase regulates cell wall alpha-glucan biosynthesis through the protein kinase pck2p. Mol Biol Cell 11:4393–4401

  • Chang EC, Barr M, Wang Y, Jung V, Xu HP, Wigler MH (1994) Cooperative interaction of S. pombe proteins required for mating and morphogenesis. Cell Cycle 79:131–141

    CAS  Google Scholar 

  • Chang E, Bartholomeusz G, Pimental R, Chen J, Lai H, Wang LH, Yang P, Marcus S (1999) Direct binding and in vivo regulation of the fission yeast p21-activated kinase shk1 by the SH3 domain protein scd2. Mol Cell Biol 19:8066–8074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bahler J (2003) Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14:214–229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coffman VC, Sees JA, Kovar DR, Wu JQ (2013) The formins Cdc12 and For3 cooperate during contractile ring assembly in cytokinesis. J Cell Biol 203:101–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coll PM, Trillo Y, Ametzazurra A, Perez P (2003) Gef1p, a new guanine nucleotide exchange factor for Cdc42p, regulates polarity in Schizosaccharomyces pombe. Mol Biol Cell 14:313–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das M, Wiley DJ, Medina S, Vincent HA, Larrea M, Oriolo A, Verde F (2007) Regulation of cell diameter, For3p localization, and cell symmetry by fission yeast Rho-GAP Rga4p. Mol Biol Cell 18:2090–2101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das M, Drake T, Wiley DJ, Buchwald P, Vavylonis D, Verde F (2012) Oscillatory dynamics of Cdc42 GTPase in the control of polarized growth. Science 337:239–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das M, Nunez I, Rodriguez M, Wiley DJ, Rodriguez J, Sarkeshik A, Yates JR 3rd, Buchwald P, Verde F (2015) Phosphorylation-dependent inhibition of Cdc42 GEF Gef1 by 14-3-3 protein Rad24 spatially regulates Cdc42 GTPase activity and oscillatory dynamics during cell morphogenesis. Mol Biol Cell 26:3520–3534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doi A, Kita A, Kanda Y, Uno T, Asami K, Satoh R, Nakano K, Sugiura R (2015) Geranylgeranyltransferase Cwg2-Rho4/Rho5 module is implicated in the Pmk1 MAP kinase-mediated cell wall integrity pathway in fission yeast. Genes Cells 20:310–323

    Article  CAS  PubMed  Google Scholar 

  • Dudin O, Merlini L, Bendezu FO, Groux R, Vincenzetti V, Martin SG (2017) A systematic screen for morphological abnormalities during fission yeast sexual reproduction identifies a mechanism of actin aster formation for cell fusion. PLoS Genet 13:e1006721

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Estravis M, Rincon SA, Santos B, Perez P (2011) Cdc42 regulates multiple membrane traffic events in fission yeast. Traffic 12:1744–1758

    Article  CAS  PubMed  Google Scholar 

  • Estravis M, Rincon SA, Portales E, Perez P, Santos B (2017) Cdc42 activation state affects its localization and protein levels in fission yeast. Microbiology

  • Etienne-Manneville S (2004) Cdc42--the Centre of polarity. J Cell Sci 117:1291–1300

    Article  CAS  PubMed  Google Scholar 

  • Feierbach B, Chang F (2001) Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr Biol 11:1656–1665

    Article  CAS  PubMed  Google Scholar 

  • Gachet Y, Hyams JS (2005) Endocytosis in fission yeast is spatially associated with the actin cytoskeleton during polarised cell growth and cytokinesis. J Cell Sci 118:4231–4242

    Article  CAS  PubMed  Google Scholar 

  • Gacto M, Soto T, Vicente-Soler J, Villa T, Cansado J (2003) Learning from yeasts: intracellular sensing of stress conditions. Int Microbio l6:211–219

    Article  CAS  Google Scholar 

  • Gallo Castro D, Martin SG (2018) Differential GAP requirement for Cdc42-GTP polarization during proliferation and sexual reproduction. J Cell Biol 217:4215–4229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garcia Cortes JC, Ramos M, Osumi M, Perez P, Ribas JC (2016) The cell biology of fission yeast Septation. Microbiol Mol Biol Rev 80:779–791

    Article  PubMed  PubMed Central  Google Scholar 

  • Garcia P, Tajadura V, Sanchez Y (2009) The Rho1p exchange factor Rgf1p signals upstream from the Pmk1 mitogen-activated protein kinase pathway in fission yeast. Mol Biol Cell 20:721–731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haupt A, Ershov D, Minc N (2018) A positive feedback between growth and polarity provides directional persistency and flexibility to the process of tip growth. Curr Biol 28:3342–3351 e3343

    Article  CAS  PubMed  Google Scholar 

  • Hodge RG, Ridley AJ (2016) Regulating Rho GTPases and their regulators. Nat Rev Mol Cell Biol 17:496–510

    Article  CAS  PubMed  Google Scholar 

  • Hoffman CS, Wood V, Fantes PA (2015) An ancient yeast for young geneticists: a primer on the Schizosaccharomyces pombe model system. Genetics 201:403–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Chew TG, Ge W, Balasubramanian MK (2007) Polarity determinants Tea1p, Tea4p, and Pom1p inhibit division-septum assembly at cell ends in fission yeast. Dev Cell 12:987–996

    Article  CAS  PubMed  Google Scholar 

  • Huisman SM, Brunner D (2011) Cell polarity in fission yeast: a matter of confining, positioning, and switching growth zones. Semin Cell Dev Biol 22:799–805

    Article  CAS  PubMed  Google Scholar 

  • Kelly FD, Nurse P (2011) Spatial control of Cdc42 activation determines cell width in fission yeast. Mol Biol Cell 22:3801–3811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H, Yang P, Catanuto P, Verde F, Lai H, Du H, Chang F, Marcus S (2003) The kelch repeat protein, Tea1, is a potential substrate target of the p21-activated kinase, Shk1, in the fission yeast, Schizosaccharomyces pombe. J Biol Chem 278:30074–30082

    Article  CAS  Google Scholar 

  • Kokkoris K, Gallo Castro D, Martin SG (2014) The Tea4-PP1 landmark promotes local growth by dual Cdc42 GEF recruitment and GAP exclusion. J Cell Sci 127:2005–2016

    CAS  PubMed  Google Scholar 

  • Kovar DR, Sirotkin V, Lord M (2011) Three's company: the fission yeast actin cytoskeleton. Trends Cell Biol 21:177–187

    Article  CAS  PubMed  Google Scholar 

  • Lawrence CL, Maekawa H, Worthington JL, Reiter W, Wilkinson CR, Jones N (2007) Regulation of Schizosaccharomyces pombe Atf1 protein levels by Sty1-mediated phosphorylation and heterodimerization with Pcr1. J Biol Chem 282, United States:5160–5170

    Article  CAS  PubMed  Google Scholar 

  • Loo TH, Balasubramanian M (2008) Schizosaccharomyces pombe Pak-related protein, Pak1p/Orb2p, phosphorylates myosin regulatory light chain to inhibit cytokinesis. J Cell Biol 183:785–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Aviles S, Grande M, Gonzalez M, Helgesen AL, Alemany V, Sanchez-Piris M, Bachs O, Millar JB, Aligue R (2005) Inactivation of the Cdc25 phosphatase by the stress-activated Srk1 kinase in fission yeast. Mol Cell 17:49–59

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Kuno T, Kita A, Asayama Y, Sugiura R (2006) Rho2 is a target of the farnesyltransferase Cpp1 and acts upstream of Pmk1 mitogen-activated protein kinase signaling in fission yeast. Mol Biol Cell 17:5028–5037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcus S, Polverino A, Chang E, Robbins D, Cobb MH, Wigler MH (1995) Shk1, a homolog of the Saccharomyces cerevisiae Ste20 and mammalian p65PAK protein kinases, is a component of a Ras/Cdc42 signaling module in the fission yeast Schizosaccharomyces pombe. Proc Natl Acad Sci U S A 92:6180–6184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin SG (2015) Spontaneous cell polarization: feedback control of Cdc42 GTPase breaks cellular symmetry. Bioessays 37:1193–1201

    Article  CAS  PubMed  Google Scholar 

  • Martin SG, Berthelot-Grosjean M (2009) Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle. Nature 459:852–856

    Article  CAS  PubMed  Google Scholar 

  • Martin SG, McDonald WH, Yates JR 3rd, Chang F (2005) Tea4p links microtubule plus ends with the formin for3p in the establishment of cell polarity. Dev Cell 8:479–491

    Article  CAS  PubMed  Google Scholar 

  • Martin V, Rodriguez-Gabriel MA, McDonald WH, Watt S, Yates JR 3rd, Bahler J, Russell P (2006) Cip1 and Cip2 are novel RNA-recognition-motif proteins that counteract Csx1 function during oxidative stress. Mol Biol Cell 17:1176–1183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin SG, Rincon SA, Basu R, Perez P, Chang F (2007) Regulation of the formin for3p by cdc42p and bud6p. Mol Biol Cell 18:4155–4167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mata J, Nurse P (1997) Tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell 89:939–949

    Article  CAS  PubMed  Google Scholar 

  • Millar JB, Buck V, Wilkinson MG (1995) Pyp1 and Pyp2 PTPases dephosphorylate an osmosensing MAP kinase controlling cell size at division in fission yeast. Genes Dev 9:2117–2130

    Article  CAS  PubMed  Google Scholar 

  • Morigasaki S, Ikner A, Tatebe H, Shiozaki K (2013) Response regulator-mediated MAPKKK heteromer promotes stress signaling to the Spc1 MAPK in fission yeast. Mol Biol Cell 24:1083–1092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moseley JB, Mayeux A, Paoletti A, Nurse P (2009) A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 459:857–860

    Article  CAS  PubMed  Google Scholar 

  • Mutavchiev DR, Leda M, Sawin KE (2016) Remodeling of the fission yeast Cdc42 cell-polarity module via the Sty1 p38 stress-activated protein kinase pathway. Curr Biol 26:2921–2928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano K, Toya M, Yoneda A, Asami Y, Yamashita A, Kamasawa N, Osumi M, Yamamoto M (2011) Pob1 ensures cylindrical cell shape by coupling two distinct rho signaling events during secretory vesicle targeting. Traffic 12:726–739

    Article  CAS  PubMed  Google Scholar 

  • Nguyen AN, Shiozaki K (1999) Heat-shock-induced activation of stress MAP kinase is regulated by threonine- and tyrosine-specific phosphatases. Genes Dev 13:1653–1663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen AN, Ikner AD, Shiozaki M, Warren SM, Shiozaki K (2002) Cytoplasmic localization of Wis1 MAPKK by nuclear export signal is important for nuclear targeting of Spc1/Sty1 MAPK in fission yeast. Mol Biol Cell 13:2651–2663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Opalko HE, Moseley JB (2017) Dynamic regulation of Cdr1 kinase localization and phosphorylation during osmotic stress. J Biol Chem 292:18457–18468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez P, Cansado J (2010) Cell integrity signaling and response to stress in fission yeast. Curr Protein Pept Sci 11:680–692

    Article  CAS  PubMed  Google Scholar 

  • Perez P, Rincon SA (2010) Rho GTPases: regulation of cell polarity and growth in yeasts. Biochem J 426:243–253

    Article  CAS  PubMed  Google Scholar 

  • Perez P, Portales E, Santos B (2015) Rho4 interaction with exocyst and septins regulates cell separation in fission yeast. Microbiology 161:948–959

    Article  CAS  PubMed  Google Scholar 

  • Petersen J, Hagan IM (2005) Polo kinase links the stress pathway to cell cycle control and tip growth in fission yeast. Nature 435:507–512

    Article  CAS  PubMed  Google Scholar 

  • Pollard TD (2007) Regulation of actin filament assembly by Arp2/3 complex and formins. Ann Rev Biophys Biomol Struct 36:451–477

    Article  CAS  Google Scholar 

  • Quinn J, Findlay VJ, Dawson K, Millar JB, Jones N, Morgan BA, Toone WM (2002) Distinct regulatory proteins control the graded transcriptional response to increasing H(2)O(2) levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell 13:805–816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Revilla-Guarinos MT, Martin-Garcia R, Villar-Tajadura MA, Estravis M, Coll PM, Perez P (2016) Rga6 is a fission yeast rho GAP involved in Cdc42 regulation of polarized growth. Mol Biol Cell 27:1524–1535

    Article  CAS  PubMed Central  Google Scholar 

  • Rincon SA, Santos B, Perez P (2006) Fission yeast Rho5p GTPase is a functional paralogue of Rho1p that plays a role in survival of spores and stationary-phase cells. Eukaryot Cell 5:435–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson AM, Hagan IM (2008) Stress-regulated kinase pathways in the recovery of tip growth and microtubule dynamics following osmotic stress in S. Pombe. J Cell Sci 121:4055–4068

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Gabriel MA, Burns G, McDonald WH, Martin V, Yates JR 3rd, Bahler J, Russell P (2003) RNA-binding protein Csx1 mediates global control of gene expression in response to oxidative stress. EMBO J 22:6256–6266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salat-Canela C, Paulo E, Sánchez-Mir L, Carmona M, Ayté J, Oliva B, Hidalgo E (2017) Deciphering the role of the signal- and Sty1 kinase-dependent phosphorylation of the stress-responsive transcription factor Atf1 on gene activation. J Biol Chem 292:13635–13644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez-Marinas M, Gimenez-Zaragoza D, Martin-Ramos E, Llanes J, Cansado J, Pujol MJ, Bachs O, Aligue R (2018) Cmk2 kinase is essential for survival in arsenite by modulating translation together with RACK1 orthologue Cpc2 in Schizosaccharomyces pombe. Free Radic Biol Med 129:116–126

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Mir L, Franco A, Martin-Garcia R, Madrid M, Vicente-Soler J, Soto T, Gacto M, Perez P, Cansado J (2014a) Rho2 palmitoylation is required for plasma membrane localization and proper signaling to the fission yeast cell integrity MAPK pathway. Mol Cell Biol 34:2747–2759

    Article  CAS  Google Scholar 

  • Sanchez-Mir L, Soto T, Franco A, Madrid M, Viana RA, Vicente J, Gacto M, Perez P, Cansado J (2014b) Rho1 GTPase and PKC ortholog Pck1 are upstream activators of the cell integrity MAPK pathway in fission yeast. PLoS One 9:e88020

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Santos B, Gutierrez J, Calonge TM, Perez P (2003) Novel rho GTPase involved in cytokinesis and cell wall integrity in the fission yeast Schizosaccharomyces pombe. Eukaryot Cell 2:521–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos B, Martin-Cuadrado AB, Vazquez de Aldana CR, del Rey F, Perez P (2005) Rho4 GTPase is involved in secretion of glucanases during fission yeast cytokinesis. Eukaryot Cell 4:1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sells MA, Barratt JT, Caviston J, Ottilie S, Leberer E, Chernoff J (1998) Characterization of Pak2p, a pleckstrin homology domain-containing, p21-activated protein kinase from fission yeast. J Biol Chem 273:18490–18498

    Article  CAS  PubMed  Google Scholar 

  • Shiozaki K, Russell P (1996) Conjugation, meiosis, and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. Genes Dev 10:2276–2288

    Article  CAS  PubMed  Google Scholar 

  • Snaith HA, Samejima I, Sawin KE (2005) Multistep and multimode cortical anchoring of tea1p at cell tips in fission yeast. EMBO J 24:3690–3699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soto T, Beltran FF, Paredes V, Madrid M, Millar JBA, Vicente-Soler J, Cansado J, Gacto M (2002) Cold induces stress-activated protein kinase-mediated response in the fission yeast Schizosaccharomyces pombe. Eur J Biochem 269:5056–5065

    Article  CAS  PubMed  Google Scholar 

  • Soto T, Nunez A, Madrid M, Vicente J, Gacto M, Cansado J (2007) Transduction of centrifugation-induced gravity forces through mitogen-activated protein kinase pathways in the fission yeast Schizosaccharomyces pombe. Microbiology 153:1519–1529

    Article  CAS  PubMed  Google Scholar 

  • Tatebe H, Shimada K, Uzawa S, Morigasaki S, Shiozaki K (2005) Wsh3/Tea4 is a novel cell-end factor essential for bipolar distribution of Tea1 and protects cell polarity under environmental stress in S. pombe. Curr Biol 15:1006–1015

    Article  CAS  PubMed  Google Scholar 

  • Tatebe H, Nakano K, Maximo R, Shiozaki K (2008) Pom1 DYRK regulates localization of the Rga4 GAP to ensure bipolar activation of Cdc42 in fission yeast. Curr Biol 18:322–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tay YD, Leda M, Goryachev AB, Sawin KE (2018) Local and global Cdc42 guanine nucleotide exchange factors for fission yeast cell polarity are coordinated by microtubules and the Tea1-Tea4-Pom1 axis. J Cell Sci 131. https://doi.org/10.1242/jcs.216580

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Terenna CR, Makushok T, Velve-Casquillas G, Baigl D, Chen Y, Bornens M, Paoletti A, Piel M, Tran PT (2008) Physical mechanisms redirecting cell polarity and cell shape in fission yeast. Curr Biol 18:1748–1753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiedje C, Sakwa I, Just U, Hofken T (2008) The Rho GDI Rdi1 regulates Rho GTPases by distinct mechanisms. Mol Biol Cell 19:2885–2896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran PT, Marsh L, Doye V, Inoué S, Chang F (2001) A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153:397–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tu H, Barr M, Dong DL, Wigler M (1997) Multiple regulatory domains on the Byr2 protein kinase. Mol Cell Biol 17:5876–5887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vetter IR, Wittinghofer A (2001) The guanine nucleotide-binding switch in three dimensions. Science 294:1299–1304

    Article  CAS  PubMed  Google Scholar 

  • Viana RA, Pinar M, Soto T, Coll PM, Cansado J, Pérez P (2013) Negative functional interaction between cell integrity MAPK pathway and Rho1 GTPase in fission yeast. Genetics 195:421–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vjestica A, Merlini L, Nkosi PJ, Martin SG (2018) Gamete fusion triggers bipartite transcription factor assembly to block re-fertilization. Nature 560:397–400

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Tang X, Balasubramanian MK (2003) Rho3p regulates cell separation by modulating exocyst function in Schizosaccharomyces pombe. Genetics 164:1323–1331

  • Wedlich-Soldner R, Li R (2003) Spontaneous cell polarization: undermining determinism. Nat Cell Biol 5:267–270

    Article  CAS  PubMed  Google Scholar 

  • Wennerberg K, Rossman KL, Der CJ (2005) The Ras superfamily at a glance. J Cell Sci 118:843–846

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson MG, Samuels M, Takeda T, Toone WM, Shieh JC, Toda T, Millar JB, Jones N (1996) The Atf1 transcription factor is a target for the Sty1 stress-activated MAP kinase pathway in fission yeast. Genes Dev 10:2289–2301

    Article  CAS  PubMed  Google Scholar 

  • Winter D, Podtelejnikov AV, Mann M, Li R (1997) The complex containing actin-related proteins Arp2 and Arp3 is required for the motility and integrity of yeast actin patches. Curr Biol 7:519–529

    Article  CAS  PubMed  Google Scholar 

  • Wood E, Nurse P (2013) Pom1 and cell size homeostasis in fission yeast. Cell Cycle 12:3228–3236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang P, Qyang Y, Bartholomeusz G, Zhou X, Marcus S (2003) The novel Rho GTPase-activating protein family protein, Rga8, provides a potential link between Cdc42/p21-activated kinase and Rho signaling pathways in the fission yeast, Schizosaccharomyces pombe. J Biol Chem 278:48821–48830

    Article  CAS  Google Scholar 

  • Yonetani A, Chang F (2010) Regulation of cytokinesis by the formin cdc12p. Curr Biol 20:561–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank D. M. Posner for language revision. This work was supported by grants BIO2015-69958-P and BFU2017-82423-P from the Ministry of Science, Innovation and Universities (MICIU) and grants CSI068P17 and Escalera de Excelencia CLU-2017-03 from the Regional Government of Castilla y León (JCyL/FEDER) and the European Regional Development Fund (ERDF). The authors wish to acknowledge the many other studies on fission yeast cell polarity and apologize for not citing every important contribution in this review due to space limitations.

Author information

Authors and Affiliations

  1. Instituto de Biología Funcional y Genómica, Consejo Superior de Investigaciones Científicas and Universidad de Salamanca, 37007, Salamanca, Spain

    Pilar Pérez

  2. Yeast Physiology Group, Department of Genetics and Microbiology, Facultad de Biología, Universidad de Murcia, 30071, Murcia, Spain

    Teresa Soto, Elisa Gómez-Gil & Jose Cansado

Authors
  1. Pilar Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teresa Soto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elisa Gómez-Gil
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jose Cansado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Pilar Pérez or Jose Cansado.

Ethics declarations

Conflict of interest

The authors declare that they have conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez, P., Soto, T., Gómez-Gil, E. et al. Functional interaction between Cdc42 and the stress MAPK signaling pathway during the regulation of fission yeast polarized growth. Int Microbiol 23, 31–41 (2020). https://doi.org/10.1007/s10123-019-00072-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10123-019-00072-6

Keywords

Search

Navigation