Cell Wall Stress Depolarizes Cell Growth via Hyperactivation of Rho1

doi:10.1083/jcb.147.1.163

This Article

	Full Text
	Full Text (PDF, 533K)
	PPT slides of all figures
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Delley, P.-A.
	Articles by Hall, M. N.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Delley, P.-A.
	Articles by Hall, M. N.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/1999//163 $5.00
The Journal of Cell Biology, Volume 147, Number 1, , 1999 163-174

Original Article

Cell Wall Stress Depolarizes Cell Growth via Hyperactivation of Rho1

Pierre-Alain Delley^a and Michael N. Hall^a

^a Department of Biochemistry, Biozentrum, University of Basel, CH-4056 Basel, Switzerland
Department of Biochemistry, Biozentrum, University of Basel, Klingelbergstrasse 70, CH-4056 Basel, Switzerland.41-61-267-214941-61-267-2162

hall{at}ubaclu.unibas.ch

Cells sense and physiologically respond to environmental stressvia signaling pathways. Saccharomyces cerevisiae cells respondto cell wall stress by transiently depolarizing the actin cytoskeleton.We report that cell wall stress also induces a transient depolarizeddistribution of the cell wall biosynthetic enzyme glucan synthaseFKS1 and its regulatory subunit RHO1, possibly as a mechanismto repair general cell wall damage. The redistribution of FKS1is dependent on the actin cytoskeleton. Depolarization of theactin cytoskeleton and FKS1 is mediated by the plasma membraneprotein WSC1, the RHO1 GTPase switch, PKC1, and a yet-to-bedefined PKC1 effector branch. WSC1 behaves like a signal transduceror a stress-specific actin landmark that both controls and respondsto the actin cytoskeleton, similar to the bidirectional signalingbetween integrin receptors and the actin cytoskeleton in mammaliancells. The PKC1-activated mitogen-activated protein kinase cascadeis not required for depolarization, but rather for repolarizationof the actin cytoskeleton and FKS1. Thus, activated RHO1 canmediate both polarized and depolarized cell growth via the sameeffector, PKC1, suggesting that RHO1 may function as a rheostatrather than as a simple on-off switch.

Key Words: actin cytoskeleton • yeast • PKC1 • integrins • WSC1

1.used in this paper: GTPase, guanosine triphosphatase; HA,hemagglutinin; LAT-A, latrunculin A; MAP, mitogen-activatedprotein

CiteULike

Complore

Connotea

Del.icio.us Add to Digg

Digg

Facebook

Technorati

Twitter What's this?

This article has been cited by other articles:

Mollapour, M., Shepherd, A., Piper, P. W. (2009). Presence of the Fps1p aquaglyceroporin channel is essential for Hog1p activation, but suppresses Slt2(Mpk1)p activation, with acetic acid stress of yeast. Microbiology 155: 3304-3311 [Abstract] [Full Text]
Yoshida, S., Bartolini, S., Pellman, D. (2009). Mechanisms for concentrating Rho1 during cytokinesis. Genes Dev. 23: 810-823 [Abstract] [Full Text]
Crutchley, J., King, K. M., Keaton, M. A., Szkotnicki, L., Orlando, D. A., Zyla, T. R., Bardes, E. S.G., Lew, D. J. (2009). Molecular Dissection of the Checkpoint Kinase Hsl1p. Mol. Biol. Cell 20: 1926-1936 [Abstract] [Full Text]
Badrane, H., Nguyen, M. H., Cheng, S., Kumar, V., Derendorf, H., Iczkowski, K. A., Clancy, C. J. (2008). The Candida albicans phosphatase Inp51p interacts with the EH domain protein Irs4p, regulates phosphatidylinositol-4,5-bisphosphate levels and influences hyphal formation, the cell integrity pathway and virulence. Microbiology 154: 3296-3308 [Abstract] [Full Text]
Juanes, M. A., Queralt, E., Bano, M. C., Igual, J. C. (2007). Rot1 plays an antagonistic role to Clb2 in actin cytoskeleton dynamics throughout the cell cycle. J. Cell Sci. 120: 2390-2401 [Abstract] [Full Text]
Reyes, A., Sanz, M., Duran, A., Roncero, C. (2007). Chitin synthase III requires Chs4p-dependent translocation of Chs3p into the plasma membrane. J. Cell Sci. 120: 1998-2009 [Abstract] [Full Text]
Zakrzewska, A., Boorsma, A., Delneri, D., Brul, S., Oliver, S. G., Klis, F. M. (2007). Cellular Processes and Pathways That Protect Saccharomyces cerevisiae Cells against the Plasma Membrane-Perturbing Compound Chitosan. Eukaryot Cell 6: 600-608 [Abstract] [Full Text]
Park, H.-O., Bi, E. (2007). Central Roles of Small GTPases in the Development of Cell Polarity in Yeast and Beyond. Microbiol. Mol. Biol. Rev. 71: 48-96 [Abstract] [Full Text]
Gross, S. R., Kinzy, T. G. (2007). Improper Organization of the Actin Cytoskeleton Affects Protein Synthesis at Initiation. Mol. Cell. Biol. 27: 1974-1989 [Abstract] [Full Text]
Stewart, M. S., Krause, S. A., McGhie, J., Gray, J. V. (2007). Mpt5p, a Stress Tolerance- and Lifespan-Promoting PUF Protein in Saccharomyces cerevisiae, Acts Upstream of the Cell Wall Integrity Pathway. Eukaryot Cell 6: 262-270 [Abstract] [Full Text]
Piao, H. L., Machado, I. M.P., Payne, G. S. (2007). NPFXD-mediated Endocytosis Is Required for Polarity and Function of a Yeast Cell Wall Stress Sensor. Mol. Biol. Cell 18: 57-65 [Abstract] [Full Text]
Serrano, R., Martin, H., Casamayor, A., Arino, J. (2006). Signaling Alkaline pH Stress in the Yeast Saccharomyces cerevisiae through the Wsc1 Cell Surface Sensor and the Slt2 MAPK Pathway. J. Biol. Chem. 281: 39785-39795 [Abstract] [Full Text]
Lottersberger, F., Panza, A., Lucchini, G., Piatti, S., Longhese, M. P. (2006). The Saccharomyces cerevisiae 14-3-3 Proteins Are Required for the G1/S Transition, Actin Cytoskeleton Organization and Cell Wall Integrity. Genetics 173: 661-675 [Abstract] [Full Text]
Grosshans, B. L., Grotsch, H., Mukhopadhyay, D., Fernandez, I. M., Pfannstiel, J., Idrissi, F.-Z., Lechner, J., Riezman, H., Geli, M. I. (2006). TEDS Site Phosphorylation of the Yeast Myosins I Is Required for Ligand-induced but Not for Constitutive Endocytosis of the G Protein-coupled Receptor Ste2p. J. Biol. Chem. 281: 11104-11114 [Abstract] [Full Text]
Ren, G., Vajjhala, P., Lee, J. S., Winsor, B., Munn, A. L. (2006). The BAR Domain Proteins: Molding Membranes in Fission, Fusion, and Phagy. Microbiol. Mol. Biol. Rev. 70: 37-120 [Abstract] [Full Text]
Meier, K. D., Deloche, O., Kajiwara, K., Funato, K., Riezman, H. (2006). Sphingoid Base Is Required for Translation Initiation during Heat Stress in Saccharomyces cerevisiae. Mol. Biol. Cell 17: 1164-1175 [Abstract] [Full Text]
Parrish, W. R., Stefan, C. J., Emr, S. D. (2005). PtdIns(3)P accumulation in triple lipid-phosphatase-deletion mutants triggers lethal hyperactivation of the Rho1p/Pkc1p cell-integrity MAP kinase pathway. J. Cell Sci. 118: 5589-5601 [Abstract] [Full Text]
Queralt, E., Igual, J. C. (2005). Functional Connection Between the Clb5 Cyclin, the Protein Kinase C Pathway and the Swi4 Transcription Factor in Saccharomyces cerevisiae. Genetics 171: 1485-1498 [Abstract] [Full Text]
Mizunuma, M., Hirata, D., Miyakawa, T. (2005). Implication of Pkc1p protein kinase C in sustaining Cln2p level and polarized bud growth in response to calcium signaling in Saccharomyces cerevisiae. J. Cell Sci. 118: 4219-4229 [Abstract] [Full Text]
Noma, S., Iida, K., Iida, H. (2005). Polarized Morphogenesis Regulator Spa2 Is Required for the Function of Putative Stretch-Activated Ca2+-Permeable Channel Component Mid1 in Saccharomyces cerevisiae. Eukaryot Cell 4: 1353-1363 [Abstract] [Full Text]
Claret, S., Gatti, X., Doignon, F., Thoraval, D., Crouzet, M. (2005). The Rgd1p Rho GTPase-Activating Protein and the Mid2p Cell Wall Sensor Are Required at Low pH for Protein Kinase C Pathway Activation and Cell Survival in Saccharomyces cerevisiae. Eukaryot Cell 4: 1375-1386 [Abstract] [Full Text]
Levin, D. E. (2005). Cell Wall Integrity Signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69: 262-291 [Abstract] [Full Text]
Imazu, H., Sakurai, H. (2005). Saccharomyces cerevisiae Heat Shock Transcription Factor Regulates Cell Wall Remodeling in Response to Heat Shock. Eukaryot Cell 4: 1050-1056 [Abstract] [Full Text]
Williams, M. E., Torabinejad, J., Cohick, E., Parker, K., Drake, E. J., Thompson, J. E., Hortter, M., DeWald, D. B. (2005). Mutations in the Arabidopsis Phosphoinositide Phosphatase Gene SAC9 Lead to Overaccumulation of PtdIns(4,5)P2 and Constitutive Expression of the Stress-Response Pathway. Plant Physiol. 138: 686-700 [Abstract] [Full Text]
Fadri, M., Daquinag, A., Wang, S., Xue, T., Kunz, J. (2005). The Pleckstrin Homology Domain Proteins Slm1 and Slm2 Are Required for Actin Cytoskeleton Organization in Yeast and Bind Phosphatidylinositol-4,5-Bisphosphate and TORC2. Mol. Biol. Cell 16: 1883-1900 [Abstract] [Full Text]
Vilella, F., Herrero, E., Torres, J., de la Torre-Ruiz, M. A. (2005). Pkc1 and the Upstream Elements of the Cell Integrity Pathway in Saccharomyces cerevisiae, Rom2 and Mtl1, Are Required for Cellular Responses to Oxidative Stress. J. Biol. Chem. 280: 9149-9159 [Abstract] [Full Text]
Irazoqui, J. E., Howell, A. S., Theesfeld, C. L., Lew, D. J. (2005). Opposing Roles for Actin in Cdc42p Polarization. Mol. Biol. Cell 16: 1296-1304 [Abstract] [Full Text]
Zajac, A., Sun, X., Zhang, J., Guo, W. (2005). Cyclical Regulation of the Exocyst and Cell Polarity Determinants for Polarized Cell Growth. Mol. Biol. Cell 16: 1500-1512 [Abstract] [Full Text]
Cortes, J. C. G., Carnero, E., Ishiguro, J., Sanchez, Y., Duran, A., Ribas, J. C. (2005). The novel fission yeast (1,3){beta}-D-glucan synthase catalytic subunit Bgs4p is essential during both cytokinesis and polarized growth. J. Cell Sci. 118: 157-174 [Abstract] [Full Text]
Koo, J. C., Lee, B., Young, M. E., Koo, S. C., Cooper, J. A., Baek, D., Lim, C. O., Lee, S. Y., Yun, D.-J., Cho, M. J. (2004). Pn-AMP1, a Plant Defense Protein, Induces Actin Depolarization in Yeasts. Plant Cell Physiol 45: 1669-1680 [Abstract] [Full Text]
Cortes, J. C. G., Katoh-Fukui, R., Moto, K., Ribas, J. C., Ishiguro, J. (2004). Schizosaccharomyces pombe Pmr1p Is Essential for Cell Wall Integrity and Is Required for Polarized Cell Growth and Cytokinesis. Eukaryot Cell 3: 1124-1135 [Abstract] [Full Text]
Morales-Johansson, H., Jenoe, P., Cooke, F. T., Hall, M. N. (2004). Negative Regulation of Phosphatidylinositol 4,5-Bisphosphate Levels by the INP51-associated Proteins TAX4 and IRS4. J. Biol. Chem. 279: 39604-39610 [Abstract] [Full Text]
Zhang, X., Lester, R. L., Dickson, R. C. (2004). Pil1p and Lsp1p Negatively Regulate the 3-Phosphoinositide-dependent Protein Kinase-like Kinase Pkh1p and Downstream Signaling Pathways Pkc1p and Ypk1p. J. Biol. Chem. 279: 22030-22038 [Abstract] [Full Text]
Garcia, R., Bermejo, C., Grau, C., Perez, R., Rodriguez-Pena, J. M., Francois, J., Nombela, C., Arroyo, J. (2004). The Global Transcriptional Response to Transient Cell Wall Damage in Saccharomyces cerevisiae and Its Regulation by the Cell Integrity Signaling Pathway. J. Biol. Chem. 279: 15183-15195 [Abstract] [Full Text]
Uesono, Y., Ashe, M. P., Toh-e, A. (2004). Simultaneous yet Independent Regulation of Actin Cytoskeletal Organization and Translation Initiation by Glucose in Saccharomyces cerevisiae. Mol. Biol. Cell 15: 1544-1556 [Abstract] [Full Text]
Mackin, N. A., Sousou, T. J., Erdman, S. E. (2004). The PXL1 Gene of Saccharomyces cerevisiae Encodes a Paxillin-like Protein Functioning in Polarized Cell Growth. Mol. Biol. Cell 15: 1904-1917 [Abstract] [Full Text]
Schneper, L., Krauss, A., Miyamoto, R., Fang, S., Broach, J. R. (2004). The Ras/Protein Kinase A Pathway Acts in Parallel with the Mob2/Cbk1 Pathway To Effect Cell Cycle Progression and Proper Bud Site Selection. Eukaryot Cell 3: 108-120 [Abstract] [Full Text]
Harrison, J. C., Zyla, T. R., Bardes, E. S. G., Lew, D. J. (2004). Stress-specific Activation Mechanisms for the "Cell Integrity" MAPK Pathway. J. Biol. Chem. 279: 2616-2622 [Abstract] [Full Text]
Lommel, M., Bagnat, M., Strahl, S. (2004). Aberrant Processing of the WSC Family and Mid2p Cell Surface Sensors Results in Cell Death of Saccharomyces cerevisiae O-Mannosylation Mutants. Mol. Cell. Biol. 24: 46-57 [Abstract] [Full Text]
Reinoso-Martin, C., Schuller, C., Schuetzer-Muehlbauer, M., Kuchler, K. (2003). The Yeast Protein Kinase C Cell Integrity Pathway Mediates Tolerance to the Antifungal Drug Caspofungin through Activation of Slt2p Mitogen-Activated Protein Kinase Signaling. Eukaryot Cell 2: 1200-1210 [Abstract] [Full Text]
Wiederkehr, A., Du, Y., Pypaert, M., Ferro-Novick, S., Novick, P. (2003). Sec3p Is Needed for the Spatial Regulation of Secretion and for the Inheritance of the Cortical Endoplasmic Reticulum. Mol. Biol. Cell 14: 4770-4782 [Abstract] [Full Text]
deHart, A. K.A., Schnell, J. D., Allen, D. A., Tsai, J.-Y., Hicke, L. (2003). Receptor Internalization in Yeast Requires the Tor2-Rho1 Signaling Pathway. Mol. Biol. Cell 14: 4676-4684 [Abstract] [Full Text]
Alic, N., Higgins, V. J., Pichova, A., Breitenbach, M., Dawes, I. W. (2003). Lipid Hydroperoxides Activate the Mitogen-activated Protein Kinase Mpk1p in Saccharomyces cerevisiae. J. Biol. Chem. 278: 41849-41855 [Abstract] [Full Text]
Valdivia, R. H., Schekman, R. (2003). The yeasts Rho1p and Pkc1p regulate the transport of chitin synthase III (Chs3p) from internal stores to the plasma membrane. Proc. Natl. Acad. Sci. USA 100: 10287-10292 [Abstract] [Full Text]
Dong, Y., Pruyne, D., Bretscher, A. (2003). Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast. JCB 161: 1081-1092 [Abstract] [Full Text]
Mosley, A. L., Lakshmanan, J., Aryal, B. K., Ozcan, S. (2003). Glucose-mediated Phosphorylation Converts the Transcription Factor Rgt1 from a Repressor to an Activator. J. Biol. Chem. 278: 10322-10327 [Abstract] [Full Text]
Balguerie, A., Bagnat, M., Bonneu, M., Aigle, M., Breton, A. M. (2002). Rvs161p and Sphingolipids Are Required for Actin Repolarization following Salt Stress. Eukaryot Cell 1: 1021-1031 [Abstract] [Full Text]
Cortes, J. C. G., Ishiguro, J., Duran, A., Ribas, J. C. (2002). Localization of the (1,3){beta}-D-glucan synthase catalytic subunit homologue Bgs1p/Cps1p from fission yeast suggests that it is involved in septation, polarized growth, mating, spore wall formation and spore germination. J. Cell Sci. 115: 4081-4096 [Abstract] [Full Text]
Torres, J., Di Como, C. J., Herrero, E., de la Torre-Ruiz, M. A. (2002). Regulation of the Cell Integrity Pathway by Rapamycin-sensitive TOR Function in Budding Yeast. J. Biol. Chem. 277: 43495-43504 [Abstract] [Full Text]
Zhang, M., Bennett, D., Erdman, S. E. (2002). Maintenance of Mating Cell Integrity Requires the Adhesin Fig2p. Eukaryot Cell 1: 811-822 [Abstract] [Full Text]
Sekiya-Kawasaki, M., Abe, M., Saka, A., Watanabe, D., Kono, K., Minemura-Asakawa, M., Ishihara, S., Watanabe, T., Ohya, Y. (2002). Dissection of Upstream Regulatory Components of the Rho1p Effector, 1,3-{beta}-Glucan Synthase, in Saccharomyces cerevisiae. Genetics 162: 663-676 [Abstract] [Full Text]
McMillan, J. N., Theesfeld, C. L., Harrison, J. C., Bardes, E. S. G., Lew, D. J. (2002). Determinants of Swe1p Degradation in Saccharomyces cerevisiae. Mol. Biol. Cell 13: 3560-3575 [Abstract] [Full Text]
Roelants, F. M., Torrance, P. D., Bezman, N., Thorner, J. (2002). Pkh1 and Pkh2 Differentially Phosphorylate and Activate Ypk1 and Ykr2 and Define Protein Kinase Modules Required for Maintenance of Cell Wall Integrity. Mol. Biol. Cell 13: 3005-3028 [Abstract] [Full Text]
Angeles de la Torre-Ruiz, M., Torres, J., Arino, J., Herrero, E. (2002). Sit4 Is Required for Proper Modulation of the Biological Functions Mediated by Pkc1 and the Cell Integrity Pathway in Saccharomyces cerevisiae. J. Biol. Chem. 277: 33468-33476 [Abstract] [Full Text]
Huang, D., Moffat, J., Andrews, B. (2002). Dissection of a Complex Phenotype by Functional Genomics Reveals Roles for the Yeast Cyclin-Dependent Protein Kinase Pho85 in Stress Adaptation and Cell Integrity. Mol. Cell. Biol. 22: 5076-5088 [Abstract] [Full Text]
Hohmann, S. (2002). Osmotic Stress Signaling and Osmoadaptation in Yeasts. Microbiol. Mol. Biol. Rev. 66: 300-372 [Abstract] [Full Text]
Chai, B., Hsu, J.-m., Du, J., Laurent, B. C. (2002). Yeast RSC Function Is Required for Organization of the Cellular Cytoskeleton via an Alternative PKC1 Pathway. Genetics 161: 575-584 [Abstract] [Full Text]
Schmelzle, T., Helliwell, S. B., Hall, M. N. (2002). Yeast Protein Kinases and the RHO1 Exchange Factor TUS1 Are Novel Components of the Cell Integrity Pathway in Yeast. Mol. Cell. Biol. 22: 1329-1339 [Abstract] [Full Text]
Cooper, K. F., Strich, R. (2002). Saccharomycescerevisiae C-Type Cyclin Ume3p/Srb11p Is Required for Efficient Induction and Execution of Meiotic Development. Eukaryot Cell 1: 66-74 [Abstract] [Full Text]
Schmitz, H.-P., Huppert, S., Lorberg, A., Heinisch, J. J. (2002). Rho5p downregulates the yeast cell integrity pathway. J. Cell Sci. 115: 3139-3148 [Abstract] [Full Text]
Baetz, K., Moffat, J., Haynes, J., Chang, M., Andrews, B. (2001). Transcriptional Coregulation by the Cell Integrity Mitogen-Activated Protein Kinase Slt2 and the Cell Cycle Regulator Swi4. Mol. Cell. Biol. 21: 6515-6528 [Abstract] [Full Text]
Drees, B. L., Sundin, B., Brazeau, E., Caviston, J. P., Chen, G.-C., Guo, W., Kozminski, K. G., Lau, M. W., Moskow, J. J., Tong, A., Schenkman, L. R., McKenzie, A. III, Brennwald, P., Longtine, M., Bi, E., Chan, C., Novick, P., Boone, C., Pringle, J. R., Davis, T. N., Fields, S., Drubin, D. G. (2001). A protein interaction map for cell polarity development. JCB 154: 549-576 [Abstract] [Full Text]
Nanduri, J., Tartakoff, A. M. (2001). Perturbation of the Nucleus: A Novel Hog1p-independent, Pkc1p-dependent Consequence of Hypertonic Shock in Yeast. Mol. Biol. Cell 12: 1835-1841 [Abstract] [Full Text]
Gladfelter, A. S., Moskow, J. J., Zyla, T. R., Lew, D. J. (2001). Isolation and Characterization of Effector-Loop Mutants of CDC42 in Yeast. Mol. Biol. Cell 12: 1239-1255 [Abstract] [Full Text]
Beauvais, A., Bruneau, J. M., Mol, P. C., Buitrago, M. J., Legrand, R., Latgé, J. P. (2001). Glucan Synthase Complex of Aspergillus fumigatus. J. Bacteriol. 183: 2273-2279 [Abstract] [Full Text]
Smits, G. J., van den Ende, H., Klis, F. M. (2001). Differential regulation of cell wall biogenesis during growth and development in yeast. Microbiology 147: 781-794 [Full Text]
WARNER, J.R., VILARDELL, J., SOHN, J.H. (2001). Economics of Ribosome Biosynthesis. Cold Spring Harb Symp Quant Biol 66: 567-574 [Abstract]
Audhya, A., Foti, M., Emr, S. D. (2000). Distinct Roles for the Yeast Phosphatidylinositol 4-Kinases, Stt4p and Pik1p, in Secretion, Cell Growth, and Organelle Membrane Dynamics. Mol. Biol. Cell 11: 2673-2689 [Abstract] [Full Text]
Li, Y., Moir, R. D., Sethy-Coraci, I. K., Warner, J. R., Willis, I. M. (2000). Repression of Ribosome and tRNA Synthesis in Secretion-Defective Cells Is Signaled by a Novel Branch of the Cell Integrity Pathway. Mol. Cell. Biol. 20: 3843-3851 [Abstract] [Full Text]
Andrews, P., Stark, M. (2000). Dynamic, Rho1p-dependent localization of Pkc1p to sites of polarized growth. J. Cell Sci. 113: 2685-2693 [Abstract]
Pruyne, D, Bretscher, A (2000). Polarization of cell growth in yeast. J. Cell Sci. 113: 571-585 [Abstract]
Stefan, C. J., Audhya, A., Emr, S. D. (2002). The Yeast Synaptojanin-like Proteins Control the Cellular Distribution of Phosphatidylinositol (4,5)-Bisphosphate. Mol. Biol. Cell 13: 542-557 [Abstract] [Full Text]