Interactions between the bud emergence proteins Bem1p and Bem2p and Rho- type GTPases in yeast

doi:10.1083/jcb.127.5.1395

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Interactions between the bud emergence proteins Bem1p and Bem2p and Rho- type GTPases in yeast

J Peterson, Y Zheng, L Bender, A Myers, R Cerione and A Bender
Department of Biology, Indiana University, Bloomington 47405.

The SH3 domain-containing protein Bem1p is needed for normal bud emergence and mating projection formation, two processes that require asymmetric reorganizations of the cortical cytoskeleton in Saccharomyces cerevisiae. To identify proteins that functionally and/or physically interact with Bem1p, we screened for mutations that display synthetic lethality with a mutant allele of the BEM1 gene and for genes whose products display two-hybrid interactions with the Bem1 protein. CDC24, which is required for bud emergence and encodes a GEF (guanine- nucleotide exchange factor) for the essential Rho-type GTPase Cdc42p, was identified during both screens. The COOH-terminal 75 amino acids of Cdc24p, outside of the GEF domain, can interact with a portion of Bem1p that lacks both SH3 domains. Bacterially expressed Cdc24p and Bem1p bind to each other in vitro, indicating that no other yeast proteins are required for this interaction. The most frequently identified gene that arose from the bem1 synthetic-lethal screen was the bud-emergence gene BEM2 (Bender and Pringle. 1991. Mol. Cell Biol. 11:1295-1395), which is allelic with IPL2 (increase in ploidy; Chan and Botstein, 1993. Genetics. 135:677-691). Here we show that Bem2p contains a GAP (GTPase-activating protein) domain for Rho-type GTPases, and that this portion of Bem2p can stimulate in vitro the GTPase activity of Rho1p, a second essential yeast Rho-type GTPase. Cells deleted for BEM2 become large and multinucleate. These and other genetic, two-hybrid, biochemical, and phenotypic data suggest that multiple Rho-type GTPases control the reorganization of the cortical cytoskeleton in yeast and that the functions of these GTPases are tightly coupled. Also, these findings raise the possibility that Bem1p may regulate or be a target of action of one or more of these GTPases.
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Ho, H.-L., Lee, H.-Y., Liao, H.-C., Chen, M.-Y. (2008). Involvement of Saccharomyces cerevisiae Avo3p/Tsc11p in Maintaining TOR Complex 2 Integrity and Coupling to Downstream Signaling. Eukaryot Cell 7: 1328-1343 [Abstract] [Full Text]
Mionnet, C., Bogliolo, S., Arkowitz, R. A. (2008). Oligomerization Regulates the Localization of Cdc24, the Cdc42 Activator in Saccharomyces cerevisiae. J. Biol. Chem. 283: 17515-17530 [Abstract] [Full Text]
Sumimoto, H., Kamakura, S., Ito, T. (2007). Structure and Function of the PB1 Domain, a Protein Interaction Module Conserved in Animals, Fungi, Amoebas, and Plants. Sci Signal 2007: re6-re6 [Abstract] [Full Text]
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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]
Yamaguchi, Y., Ota, K., Ito, T. (2007). A Novel Cdc42-interacting Domain of the Yeast Polarity Establishment Protein Bem1: IMPLICATIONS FOR MODULATION OF MATING PHEROMONE SIGNALING. J. Biol. Chem. 282: 29-38 [Abstract] [Full Text]
France, Y. E., Boyd, C., Coleman, J., Novick, P. J. (2006). The polarity-establishment component Bem1p interacts with the exocyst complex through the Sec15p subunit. J. Cell Sci. 119: 876-888 [Abstract] [Full Text]
Levin, D. E. (2005). Cell Wall Integrity Signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69: 262-291 [Abstract] [Full Text]
Wang, Y., Chen, W., Simpson, D. M., Elion, E. A. (2005). Cdc24 Regulates Nuclear Shuttling and Recruitment of the Ste5 Scaffold to a Heterotrimeric G Protein in Saccharomyces cerevisiae. J. Biol. Chem. 280: 13084-13096 [Abstract] [Full Text]
Winters, M. J., Pryciak, P. M. (2005). Interaction with the SH3 Domain Protein Bem1 Regulates Signaling by the Saccharomyces cerevisiae p21-Activated Kinase Ste20. Mol. Cell. Biol. 25: 2177-2190 [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]
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]
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]
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]
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]
Hurtado, C. A. R., Rachubinski, R. A. (2002). Isolation and Characterization of YlBEM1, a Gene Required for Cell Polarization and Differentiation in the Dimorphic Yeast Yarrowia lipolytica. Eukaryot Cell 1: 526-537 [Abstract] [Full Text]
Hohmann, S. (2002). Osmotic Stress Signaling and Osmoadaptation in Yeasts. Microbiol. Mol. Biol. Rev. 66: 300-372 [Abstract] [Full Text]
Elion, E. A. (2002). The Ste5p scaffold. J. Cell Sci. 114: 3967-3978 [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]
Nakano, K., Imai, J., Arai, R., Toh-e, A., Matsui, Y., Mabuchi, I. (2002). The small GTPase Rho3 and the diaphanous/formin For3 function in polarized cell growth in fission yeast. J. Cell Sci. 115: 4629-4639 [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]
Wang, B.-D., Kuo, T.-T. (2001). Induction of a Mitosis Delay and Cell Lysis by High-Level Secretion of Mouse {alpha}-Amylase from Saccharomyces cerevisiae. Appl. Environ. Microbiol. 67: 3693-3701 [Abstract] [Full Text]
Cid, V. J., Adamikova, L., Sanchez, M., Molina, M., Nombela, C. (2001). Cell cycle control of septin ring dynamics in the budding yeast. Microbiology 147: 1437-1450 [Abstract] [Full Text]
Gulli, M.-P., Peter, M. (2001). Temporal and spatial regulation of Rho-type guanine-nucleotide exchange factors: the yeast perspective. Genes Dev. 15: 365-379 [Full Text]
Philip, B., Levin, D. E. (2001). Wsc1 and Mid2 Are Cell Surface Sensors for Cell Wall Integrity Signaling That Act through Rom2, a Guanine Nucleotide Exchange Factor for Rho1. Mol. Cell. Biol. 21: 271-280 [Abstract] [Full Text]
Lenburg, M. E., O'Shea, E. K. (2001). Genetic Evidence for a Morphogenetic Function of the Saccharomyces cerevisiae Pho85 Cyclin-Dependent Kinase. Genetics 157: 39-51 [Abstract] [Full Text]
Singer, J. M., Hermann, G. J., Shaw, J. M. (2000). Suppressors of mdm20 in Yeast Identify New Alleles of ACT1 and TPM1 Predicted to Enhance Actin-Tropomyosin Interactions. Genetics 156: 523-534 [Abstract] [Full Text]
Jaquenoud, M., Peter, M. (2000). Gic2p May Link Activated Cdc42p to Components Involved in Actin Polarization, Including Bni1p and Bud6p (Aip3p). Mol. Cell. Biol. 20: 6244-6258 [Abstract] [Full Text]
Bi, E., Chiavetta, J. B., Chen, H., Chen, G.-C., Chan, C. S. M., Pringle, J. R. (2000). Identification of Novel, Evolutionarily Conserved Cdc42p-interacting Proteins and of Redundant Pathways Linking Cdc24p and Cdc42p to Actin Polarization in Yeast. Mol. Biol. Cell 11: 773-793 [Abstract] [Full Text]
Martin, H., Rodriguez-Pachon, J. M., Ruiz, C., Nombela, C., Molina, M. (2000). Regulatory Mechanisms for Modulation of Signaling through the Cell Integrity Slt2-mediated Pathway in Saccharomyces cerevisiae. J. Biol. Chem. 275: 1511-1519 [Abstract] [Full Text]
Wendland, J, Philippsen, P (2000). Determination of cell polarity in germinated spores and hyphal tips of the filamentous ascomycete Ashbya gossypii requires a rhoGAP homolog. J. Cell Sci. 113: 1611-1621 [Abstract]
Fujiwara, T., Tanaka, K., Inoue, E., Kikyo, M., Takai, Y. (1999). Bni1p Regulates Microtubule-Dependent Nuclear Migration through the Actin Cytoskeleton in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 8016-8027 [Abstract] [Full Text]
Takemoto, Y., Furuta, M., Sato, M., Kubo, M., Hashimoto, Y. (1999). Isolation and characterization of a novel HS1 SH3 domain binding protein, HS1BP3. Int Immunol 11: 1957-1964 [Abstract] [Full Text]
Toya, M., Iino, Y., Yamamoto, M. (1999). Fission Yeast Pob1p, Which Is Homologous to Budding Yeast Boi Proteins and Exhibits Subcellular Localization Close to Actin Patches, Is Essential for Cell Elongation and Separation. Mol. Biol. Cell 10: 2745-2757 [Abstract] [Full Text]
Kirsch, K. H., Georgescu, M.-M., Ishimaru, S., Hanafusa, H. (1999). CMS: An adapter molecule involved in cytoskeletal rearrangements. Proc. Natl. Acad. Sci. USA 96: 6211-6216 [Abstract] [Full Text]
Nern, A., Arkowitz, R. A. (1999). A Cdc24p-Far1p-G{beta}{gamma} Protein Complex Required for Yeast Orientation during Mating. JCB 144: 1187-1202 [Abstract] [Full Text]
Johnson, D. I. (1999). Cdc42: An Essential Rho-Type GTPase Controlling Eukaryotic Cell Polarity. Microbiol. Mol. Biol. Rev. 63: 54-105 [Abstract] [Full Text]
Gustin, M. C., Albertyn, J., Alexander, M., Davenport, K. (1998). MAP Kinase Pathways in the Yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62: 1264-1300 [Abstract] [Full Text]
Butty, A., Pryciak, P. M., Huang, L. S., Herskowitz, I., Peter, M. (1998). The Role of Far1p in Linking the Heterotrimeric G Protein to Polarity Establishment Proteins During Yeast Mating. Science 282: 1511-1516 [Abstract] [Full Text]
Lamarche-Vane, N., Hall, A. (1998). CdGAP, a Novel Proline-rich GTPase-activating Protein for Cdc42 and Rac. J. Biol. Chem. 273: 29172-29177 [Abstract] [Full Text]
Sawin, K. E., Nurse, P. (1998). Regulation of Cell Polarity by Microtubules in Fission Yeast. JCB 142: 457-471 [Abstract] [Full Text]
Sheu, Y.-J., Santos, B., Fortin, N., Costigan, C., Snyder, M. (1998). Spa2p Interacts with Cell Polarity Proteins and Signaling Components Involved in Yeast Cell Morphogenesis. Mol. Cell. Biol. 18: 4053-4069 [Abstract] [Full Text]
Morozov, I., Lotan, O., Joseph, G., Gorzalczany, Y., Pick, E. (1998). Mapping of Functional Domains in p47phox Involved in the Activation of NADPH Oxidase by "Peptide Walking". J. Biol. Chem. 273: 15435-15444 [Abstract] [Full Text]
Madrid, R., Gomez, M. J., Ramos, J., Rodriguez-Navarro, A. (1998). Ectopic Potassium Uptake in trk1 trk2 Mutants of Saccharomyces cerevisiae Correlates with a Highly Hyperpolarized Membrane Potential. J. Biol. Chem. 273: 14838-14844 [Abstract] [Full Text]
Kim, J., Hirsch, J. P. (1998). A Nucleolar Protein That Affects Mating Efficiency in Saccharomyces cerevisiae by Altering the Morphological Response to Pheromone. Genetics 149: 795-805 [Abstract] [Full Text]
Rethinaswamy, A., Birnbaum, M. J., Glover, C. V.�C. (1998). Temperature-sensitive Mutations of the CKA1 Gene Reveal a Role for Casein Kinase II in Maintenance of Cell Polarity in Saccharomyces cerevisiae. J. Biol. Chem. 273: 5869-5877 [Abstract] [Full Text]
Li, R., Zhang, B., Zheng, Y. (1997). Structural Determinants Required for the Interaction between Rho GTPase and the GTPase-activating Domain of p190. J. Biol. Chem. 272: 32830-32835 [Abstract] [Full Text]
Chen, G.-C., Kim, Y.-J., Chan, C. S.M. (1997). The Cdc42 GTPase-associated proteins Gic1 and Gic2 are required for polarized cell growth in Saccharomyces�cerevisiae. Genes Dev. 11: 2958-2971 [Abstract] [Full Text]
Brown, J. L., Jaquenoud, M., Gulli, M.-P., Chant, J., Peter, M. (1997). Novel Cdc42-binding proteins Gic1 and Gic2 control cell polarity in�yeast. Genes Dev. 11: 2972-2982 [Abstract] [Full Text]
Manning, B. D., Padmanabha, R., Snyder, M. (1997). The Rho-GEF Rom2p Localizes to Sites of Polarized Cell Growth and Participates in Cytoskeletal Functions in Saccharomyces cerevisiae. Mol. Biol. Cell 8: 1829-1844 [Abstract] [Full Text]
Arkowitz, R. A., Lowe, N. (1997). A Small Conserved Domain in the Yeast Spa2p Is Necessary and Sufficient for Its Polarized Localization. JCB 138: 17-36 [Abstract] [Full Text]
Wassmann, K., Ammerer, G. (1997). Overexpression of the G1-cyclin Gene CLN2 Represses the Mating Pathway in Saccharomyces cerevisiae at the Level of the MEKK Ste11. J. Biol. Chem. 272: 13180-13188 [Abstract] [Full Text]
Park, H.-O., Bi, E., Pringle, J. R., Herskowitz, I. (1997). Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast�cell�polarity. Proc. Natl. Acad. Sci. USA 94: 4463-4468 [Abstract] [Full Text]
Hermann, G. J., King, E. J., Shaw, J. M. (1997). The Yeast Gene, MDM20, Is Necessary for Mitochondrial Inheritance and Organization of the Actin Cytoskeleton. JCB 137: 141-153 [Abstract] [Full Text]
Stevenson, B J, Ferguson, B, De Virgilio, C, Bi, E, Pringle, J R, Ammerer, G, Sprague, G F (1995). Mutation of RGA1, which encodes a putative GTPase-activating protein for the polarity-establishment protein Cdc42p, activates the pheromone-response pathway in the yeast Saccharomyces cerevisiae.. Genes Dev. 9: 2949-2963 [Abstract]
Leeuw, T., Fourest-Lieuvin, A., Wu, C., Chenevert, J., Clark, K., Whiteway, M., Thomas, D. Y., Leberer, E. (1995). Pheromone Response in Yeast: Association of Bem1p with Proteins of the MAP Kinase Cascade and Actin. Science 270: 1210-1213 [Abstract]
Herskowitz, I., Park, H.-O., Sanders, S., Valtz, N., Peter, M. (1995). Programming of Cell Polarity in Budding Yeast by Endogenous and Exogenous Signals. Cold Spring Harb Symp Quant Biol 60: 717-727 [Abstract]
Pringle, J.R., Bi, E., Harkins, H.A., Zahner, J.E., De Virgilio, C., Chant, J., Corrado, K., Fares, H. (1995). Establishment of Cell Polarity in Yeast. Cold Spring Harb Symp Quant Biol 60: 729-744 [Abstract]
Bose, I., Irazoqui, J. E., Moskow, J. J., Bardes, E. S. G., Zyla, T. R., Lew, D. J. (2001). Assembly of Scaffold-mediated Complexes Containing Cdc42p, the Exchange Factor Cdc24p, and the Effector Cla4p Required for Cell Cycle-regulated Phosphorylation of Cdc24p. J. Biol. Chem. 276: 7176-7186 [Abstract] [Full Text]