This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Philip, B.
Right arrow Articles by Levin, D. E.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Philip, B.
Right arrow Articles by Levin, D. E.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, January 2001, p. 271-280, Vol. 21, No. 1
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.1.271-280.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Wsc1 and Mid2 Are Cell Surface Sensors for Cell Wall Integrity Signaling That Act through Rom2, a Guanine Nucleotide Exchange Factor for Rho1

Bevin Philip and David E. Levin*

Department of Biochemistry & Molecular Biology, School of Public Health, The Johns Hopkins University, Baltimore, Maryland 21205

Received 10 July 2000/Returned for modification 16 August 2000/Accepted 12 October 2000

Wsc1 and Mid2 are highly O-glycosylated cell surface proteins that reside in the plasma membrane of Saccharomyces cerevisiae. They have been proposed to function as mechanosensors of cell wall stress induced by wall remodeling during vegetative growth and pheromone-induced morphogenesis. These proteins are required for activation of the cell wall integrity signaling pathway that consists of the small G-protein Rho1, protein kinase C (Pkc1), and a mitogen-activated protein kinase cascade. We show here by two-hybrid experiments that the C-terminal cytoplasmic domains of Wsc1 and Mid2 interact with Rom2, a guanine nucleotide exchange factor (GEF) for Rho1. At least with regard to Wsc1, this interaction is mediated by the Rom2 N-terminal domain. This domain is distinct from the Rho1-interacting domain, suggesting that the GEF can interact simultaneously with a sensor and with Rho1. We also demonstrate that extracts from wsc1 and mid2 mutants are deficient in the ability to catalyze GTP loading of Rho1 in vitro, providing evidence that the function of the sensor-Rom2 interaction is to stimulate nucleotide exchange toward this G-protein. In a related line of investigation, we identified the PMT2 gene in a genetic screen for mutations that confer an additive cell lysis defect with a wsc1 null allele. Pmt2 is a member of a six-protein family in yeast that catalyzes the first step in O mannosylation of target proteins. We demonstrate that Mid2 is not mannosylated in a pmt2 mutant and that this modification is important for signaling by Mid2.

* Corresponding author. Mailing address: Department of Biochemistry & Molecular Biology, The Johns Hopkins University, School of Public Health, 615 N. Wolfe St., Baltimore, MD 21205. Phone: (410) 955-9825. Fax: (410) 955-2926. E-mail: levin{at}welch.jhu.edu.

Molecular and Cellular Biology, January 2001, p. 271-280, Vol. 21, No. 1
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.1.271-280.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Fuchs, B. B., Mylonakis, E. (2009). Our Paths Might Cross: the Role of the Fungal Cell Wall Integrity Pathway in Stress Response and Cross Talk with Other Stress Response Pathways. Eukaryot Cell 8: 1616-1625 [Abstract] [Full Text]  
  • 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]  
  • Zhang, L., Feng, D., Fang, W., Ouyang, H., Luo, Y., Du, T., Jin, C. (2009). Comparative proteomic analysis of an Aspergillus fumigatus mutant deficient in glucosidase I (AfCwh41). Microbiology 155: 2157-2167 [Abstract] [Full Text]  
  • Krause, S. A., Xu, H., Gray, J. V. (2008). The Synthetic Genetic Network around PKC1 Identifies Novel Modulators and Components of Protein Kinase C Signaling in Saccharomyces cerevisiae. Eukaryot Cell 7: 1880-1887 [Abstract] [Full Text]  
  • Ma, J., Dobry, C. J., Krysan, D. J., Kumar, A. (2008). Unconventional Genomic Architecture in the Budding Yeast Saccharomyces cerevisiae Masks the Nested Antisense Gene NAG1. Eukaryot Cell 7: 1289-1298 [Abstract] [Full Text]  
  • Jackson-Hayes, L., Hill, T. W., Loprete, D. M., Fay, L. M., Gordon, B. S., Nkashama, S. A., Patel, R. K., Sartain, C. V. (2008). Two GDP-mannose transporters contribute to hyphal form and cell wall integrity in Aspergillus nidulans. Microbiology 154: 2037-2047 [Abstract] [Full Text]  
  • Wright, D. J., Munro, E., Corbett, M., Bentley, A. J., Fullwood, N. J., Murray, S., Price, C. (2008). The Saccharomyces cerevisiae Actin Cytoskeletal Component Bsp1p Has an Auxiliary Role in Actomyosin Ring Function and in the Maintenance of Bud-Neck Structure. Genetics 178: 1903-1914 [Abstract] [Full Text]  
  • Fuchs, B. B., Tegos, G. P., Hamblin, M. R., Mylonakis, E. (2007). Susceptibility of Cryptococcus neoformans to Photodynamic Inactivation Is Associated with Cell Wall Integrity. Antimicrob. Agents Chemother. 51: 2929-2936 [Abstract] [Full Text]  
  • Fujioka, T., Mizutani, O., Furukawa, K., Sato, N., Yoshimi, A., Yamagata, Y., Nakajima, T., Abe, K. (2007). MpkA-Dependent and -Independent Cell Wall Integrity Signaling in Aspergillus nidulans. Eukaryot Cell 6: 1497-1510 [Abstract] [Full Text]  
  • Zhong, Q., Li, G., Gvozdenovic-Jeremic, J., Greenberg, M. L. (2007). Up-regulation of the Cell Integrity Pathway in Saccharomyces cerevisiae Suppresses Temperature Sensitivity of the pgs1{Delta} Mutant. J. Biol. Chem. 282: 15946-15953 [Abstract] [Full Text]  
  • Wright, C. M., Fewell, S. W., Sullivan, M. L., Pipas, J. M., Watkins, S. C., Brodsky, J. L. (2007). The Hsp40 Molecular Chaperone Ydj1p, Along With the Protein Kinase C Pathway, Affects Cell-Wall Integrity in the Yeast Saccharomyces cerevisiae. Genetics 175: 1649-1664 [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]  
  • Hernandez-Blanco, C., Feng, D. X., Hu, J., Sanchez-Vallet, A., Deslandes, L., Llorente, F., Berrocal-Lobo, M., Keller, H., Barlet, X., Sanchez-Rodriguez, C., Anderson, L. K., Somerville, S., Marco, Y., Molina, A. (2007). Impairment of Cellulose Synthases Required for Arabidopsis Secondary Cell Wall Formation Enhances Disease Resistance. Plant Cell 19: 890-903 [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]  
  • Proszynski, T. J., Klemm, R., Bagnat, M., Gaus, K., Simons, K. (2006). Plasma membrane polarization during mating in yeast cells. JCB 173: 861-866 [Abstract] [Full Text]  
  • Lesage, G., Bussey, H. (2006). Cell Wall Assembly in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70: 317-343 [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]  
  • 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]  
  • Fernandes, H., Roumanie, O., Claret, S., Gatti, X., Thoraval, D., Doignon, F., Crouzet, M. (2006). The Rho3 and Rho4 small GTPases interact functionally with Wsc1p, a cell surface sensor of the protein kinase C cell-integrity pathway in Saccharomyces cerevisiae.. Microbiology 152: 695-708 [Abstract] [Full Text]  
  • Castrejon, F., Gomez, A., Sanz, M., Duran, A., Roncero, C. (2006). The RIM101 Pathway Contributes to Yeast Cell Wall Assembly and Its Function Becomes Essential in the Absence of Mitogen-Activated Protein Kinase Slt2p. Eukaryot Cell 5: 507-517 [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]  
  • Zanelli, C. F., Valentini, S. R. (2005). Pkc1 Acts Through Zds1 and Gic1 to Suppress Growth and Cell Polarity Defects of a Yeast eIF5A Mutant. Genetics 171: 1571-1581 [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]  
  • Denis, V., Cyert, M. S. (2005). Molecular Analysis Reveals Localization of Saccharomyces cerevisiae Protein Kinase C to Sites of Polarized Growth and Pkc1p Targeting to the Nucleus and Mitotic Spindle. Eukaryot Cell 4: 36-45 [Abstract] [Full Text]  
  • Somerville, C., Bauer, S., Brininstool, G., Facette, M., Hamann, T., Milne, J., Osborne, E., Paredez, A., Persson, S., Raab, T., Vorwerk, S., Youngs, H. (2004). Toward a Systems Approach to Understanding Plant Cell Walls. Science 306: 2206-2211 [Abstract] [Full Text]  
  • Staleva, L., Hall, A., Orlow, S. J. (2004). Oxidative Stress Activates FUS1 and RLM1 Transcription in the Yeast Saccharomyces cerevisiae in an Oxidant-dependent Manner. Mol. Biol. Cell 15: 5574-5582 [Abstract] [Full Text]  
  • Frieman, M. B., Cormack, B. P. (2004). Multiple sequence signals determine the distribution of glycosylphosphatidylinositol proteins between the plasma membrane and cell wall in Saccharomyces cerevisiae. Microbiology 150: 3105-3114 [Abstract] [Full Text]  
  • Vay, H. A., Philip, B., Levin, D. E. (2004). Mutational analysis of the cytoplasmic domain of the Wsc1 cell wall stress sensor. Microbiology 150: 3281-3288 [Abstract] [Full Text]  
  • Wang, K., Vavassori, S., Schweizer, L. M., Schweizer, M. (2004). Impaired PRPP-synthesizing capacity compromises cell integrity signalling in Saccharomyces cerevisiae. Microbiology 150: 3327-3339 [Abstract] [Full Text]  
  • Weber, Y., Prill, S. K.-H., Ernst, J. F. (2004). Pmt-Mediated O Mannosylation Stabilizes an Essential Component of the Secretory Apparatus, Sec20p, in Candida albicans. Eukaryot Cell 3: 1164-1168 [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]  
  • Oka, T., Hamaguchi, T., Sameshima, Y., Goto, M., Furukawa, K. (2004). Molecular characterization of protein O-mannosyltransferase and its involvement in cell-wall synthesis in Aspergillus nidulans. Microbiology 150: 1973-1982 [Abstract] [Full Text]  
  • Proszynski, T. J., Simons, K., Bagnat, M. (2004). O-Glycosylation as a Sorting Determinant for Cell Surface Delivery in Yeast. Mol. Biol. Cell 15: 1533-1543 [Abstract] [Full Text]  
  • Merchan, S., Bernal, D., Serrano, R., Yenush, L. (2004). Response of the Saccharomyces cerevisiae Mpk1 Mitogen-Activated Protein Kinase Pathway to Increases in Internal Turgor Pressure Caused by Loss of Ppz Protein Phosphatases. Eukaryot Cell 3: 100-107 [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]  
  • 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]  
  • Huang, G., Zhang, M., Erdman, S. E. (2003). Posttranslational Modifications Required for Cell Surface Localization and Function of the Fungal Adhesin Aga1p. Eukaryot Cell 2: 1099-1114 [Abstract] [Full Text]  
  • Bonilla, M., Cunningham, K. W. (2003). Mitogen-activated Protein Kinase Stimulation of Ca2+ Signaling Is Required for Survival of Endoplasmic Reticulum Stress in Yeast. Mol. Biol. Cell 14: 4296-4305 [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]  
  • Green, R., Lesage, G., Sdicu, A.-M., Menard, P., Bussey, H. (2003). A synthetic analysis of the Saccharomyces cerevisiae stress sensor Mid2p, and identification of a Mid2p-interacting protein, Zeo1p, that modulates the PKC1-MPK1 cell integrity pathway. Microbiology 149: 2487-2499 [Abstract] [Full Text]  
  • Abe, M., Qadota, H., Hirata, A., Ohya, Y. (2003). Lack of GTP-bound Rho1p in secretory vesicles of Saccharomyces cerevisiae. JCB 162: 85-97 [Abstract] [Full Text]  
  • Girrbach, V., Strahl, S. (2003). Members of the Evolutionarily Conserved PMT Family of Protein O-Mannosyltransferases Form Distinct Protein Complexes among Themselves. J. Biol. Chem. 278: 12554-12562 [Abstract] [Full Text]  
  • Torok, Z., Tsvetkova, N. M., Balogh, G., Horvath, I., Nagy, E., Penzes, Z., Hargitai, J., Bensaude, O., Csermely, P., Crowe, J. H., Maresca, B., Vigh, L. (2003). Heat shock protein coinducers with no effect on protein denaturation specifically modulate the membrane lipid phase. Proc. Natl. Acad. Sci. USA 100: 3131-3136 [Abstract] [Full Text]  
  • Page, N., Gerard-Vincent, M., Menard, P., Beaulieu, M., Azuma, M., Dijkgraaf, G. J. P., Li, H., Marcoux, J., Nguyen, T., Dowse, T., Sdicu, A.-M., Bussey, H. (2003). A Saccharomyces cerevisiae Genome-Wide Mutant Screen for Altered Sensitivity to K1 Killer Toxin. Genetics 163: 875-894 [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]  
  • Willer, T., Amselgruber, W., Deutzmann, R., Strahl, S. (2002). Characterization of POMT2, a novel member of the PMT protein O-mannosyltransferase family specifically localized to the acrosome of mammalian spermatids. Glycobiology 12: 771-783 [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]  
  • 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]  
  • Hahn, J.-S., Thiele, D. J. (2002). Regulation of the Saccharomyces cerevisiae Slt2 Kinase Pathway by the Stress-inducible Sdp1 Dual Specificity Phosphatase. J. Biol. Chem. 277: 21278-21284 [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]  
  • West, C. M., Zhang, P., McGlynn, A. C., Kaplan, L. (2002). Outside-In Signaling of Cellulose Synthesis by a Spore Coat Protein in Dictyostelium. Eukaryot Cell 1: 281-292 [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]  
  • Sobering, A. K., Jung, U. S., Lee, K. S., Levin, D. E. (2002). Yeast Rpi1 Is a Putative Transcriptional Regulator That Contributes to Preparation for Stationary Phase. Eukaryot Cell 1: 56-65 [Abstract] [Full Text]  
  • de Bettignies, G., Thoraval, D., Morel, C., Peypouquet, M. F., Crouzet, M. (2001). Overactivation of the Protein Kinase C-Signaling Pathway Suppresses the Defects of Cells Lacking the Rho3/Rho4-GAP Rgd1p in Saccharomyces cerevisiae. Genetics 159: 1435-1448 [Abstract] [Full Text]  
  • Santos, J. L., Shiozaki, K. (2001). Fungal Histidine Kinases. Sci Signal 2001: re1-re1 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»