Die Rolle von Ras1 bei der Regulation des polaren Wachstums in Ustilago maydis

Kleine GTPasen der Ras-Familie sind molekulare Schalter, die an der Regulation einer Vielzahl von zellulären Prozessen beteiligt sind. In der hier vorliegenden Arbeit wurde die Rolle von Ras1 in dem phytopathogenen Pilz Ustilago maydis genauer untersucht. Im Vordergrund der Untersuchung standen die...

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1. Verfasser: Bauer, Annette
Beteiligte: Bölker, Michael (Prof. Dr.) (BetreuerIn (Doktorarbeit))
Format: Dissertation
Veröffentlicht: Philipps-Universität Marburg 2011
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1. http://archiv.ub.uni-marburg.de/diss/z2003/0133

2. http://archiv.ub.uni-marburg.de/diss/z2006/0915

3. Westwick J, Lambert Q, Clark G, Symons M, Van Aelst L, Pestell R, Der C (1997) Rac regulation of transformation, gene expression, and actin organization by multiple, PAK-independent pathways. Molecular and Cellular Biology 17(3): 1324-1335

4. Kae H, Kortholt A, Rehmann H, Insall RH, Van Haastert PJM, Spiegelman GB, Weeks G (2007) Cyclic AMP signalling in Dictyostelium: G-proteins activate separate Ras pathways using specific RasGEFs. EMBO Reports 8(5): 477-482

5. García-Muse T, Steinberg G, Pérez-Martín J (2003) Pheromone-induced G2 arrest in the phytopathogenic fungus Ustilago maydis. Eukaryotic Cell 2(3): 494

6. Banuett F, Herskowitz I (1996) Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122(10): 2965

7. Rodriguez-Viciana P, Warne P, Dhand R, Vanhaesebroeck B, Gout I, Fry M, Waterfield M, Downward J (1994) Phosphatidylinositol-3-OH kinase direct target of Ras. Nature 370: 527- 532

8. Kämper J, Reichmann M, Romeis T, Bölker M, Kahmann R (1995) Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81(1): 73-83

9. Banuett F (1992) Ustilago maydis, the delightful blight. Trends in Genetics 8(5): 174-180

10. Shimada Y, Gulli MP, Peter M (2000) Nuclear sequestration of the exchange factor Cdc24 by Far1 regulates cell polarity during yeast mating. Nature Cell Biology 2(2): 117-124

11. Gold S, Duncan G, Barrett K, Kronstad J (1994) cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes & Development 8(23): 2805-2816

12. Roberts R, Fink G (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 & Development 8(24): 2974-2985

13. Mahlert M, Leveleki L, Hlubek A, Sandrock B, Bolker M (2006) Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Molecular Microbiology 59(2): 567-578

14. Hlubek A, Schink KO, Mahlert M, Sandrock B, Bölker M (2008) Selective activation by the guanine nucleotide exchange factor Don1 is a main determinant of Cdc42 signalling specificity in Ustilago maydis. Molecular Microbiology 68((3)): 615–623

15. Zarnack K, Eichhorn H, Kahmann R, Feldbrügge M (2008) Pheromone-regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Molecular Microbiology 69(4): 1041-1053

16. Boyce K, Hynes M, Andrianopoulos A (2003) Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog. Journal of Cell Science 116(7): 1249-1260

17. Wennerberg K, Der CJ (2004) Rho-family GTPases: it's not only Rac and Rho (and I like it).

18. Bluhm BH, Zhao X, Flaherty JE, Xu JR, Dunkle LD (2007) RAS2 regulates growth and pathogenesis in Fusarium graminearum. Molecular Plant-Microbe Interactions 20(6): 627-

19. Rocks O, Peyker A, Kahms M, Verveer P, Koerner C, Lumbierres M, Kuhlmann J, Waldmann H, Wittinghofer A, Bastiaens P (2005) An Acylation Cycle Regulates Localization and Activity of Palmitoylated Ras Isoforms. Science 307(5716): 1746-1752

20. Berrier A, Mastrangelo A, Downward J, Ginsberg M, LaFlamme S (2000) Activated R-Ras, Rac1, PI 3-Kinase and PKC? Can Each Restore Cell Spreading Inhibited by Isolated Integrin ß1 Cytoplasmic Domains. The Journal of Cell Biology 151(7): 1549-1560

21. Lim K, Baines A, Fiordalisi J, Shipitsin M, Feig L, Cox A, Der C, Counter C (2005) Activation of RalA is critical for Ras-induced tumorigenesis of human cells. Cancer Cell 7(6): 533-545

22. Olivier J, Raabe T, Henkemeyer M, Dickson B, Mbamalu G, Margolis B, Schlessinger J, Hafen E, Pawson T (1993) A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell 73(1): 179–191

23. Shirsat N, Pignolo R, Kreider B, Rovera G (1990) A member of the ras gene superfamily is specifically expressed in T, B and myeloid hemopoietic cells. Oncogene 5: 769-772

24. Ponting C, Benjamin D (1996) A novel family of Ras-binding domains. Trends Biochem Sci 21(11): 422-425

25. Hancock J, Paterson H, Marshall C (1990) A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 63(133): 9

26. Nichols CB, Perfect ZH, Alspaugh JA (2007) A Ras1-Cdc24 signal transduction pathway mediates thermotolerance in the fungal pathogen Cryptococcus neoformans. Molecular Microbiology 63(4): 1118-1130

27. Fortwendel JR, Panepinto JC, Seitz AE, Askew DS, Rhodes JC (2004) Aspergillus fumigatus rasA and rasB regulate the timing and morphology of asexual development. Fungal Genetics and Biology 41(2): 129-139

28. Folch-Mallol JL, Martinez LM, Casas SJ, Yang R, Martinez-Anaya C, Lopez L, Hernandez A, Nieto-Sotelo J (2004) CELL AND DEVELOPMENTAL BIOLOGY-New roles for CDC25 in growth control, galactose regulation and cellular differentiation in Saccharomyces cerevisiae. Microbiology-Reading 150(9): 2865-2880

29. Mayorga M, Gold S (1998) Characterization and Molecular Genetic Complementation of Mutants Affecting Dimorphism in the Fungus Ustilago maydis. Fungal Genetics and Biology 24(3): 364-376

30. Haataja L, Groffen J, Heisterkamp N (1997) Characterization of RAC3, a Novel Member of the Rho Family. Journal of Biological Chemistry 272(33): 20384-20388

31. Gorfer M, Tarkka M, Hanif M, Pardo A, Laitiainen E, Raudaskoski M (2001) Characterization of Small GTPases Cdc 42 and Rac and the Relationship Between Cdc 42 and Actin Cytoskeleton in Vegetative and Ectomycorrhizal Hyphae of Suillus bovinus. Molecular Plant-Microbe Interactions 14(2): 135-144

32. Wittkowski K (2007) Charakterisierung von Ras-Guaninnukleotidaustauschfaktoren in

33. Prior IA, Hancock JF (2001) Compartmentalization of Ras proteins. Journal of Cell Science 114(9): 1603-1608

34. Onken B, Wiener H, Philips M, Chang E (2006) Compartmentalized signaling of Ras in fission yeast. Proceedings of the National Academy of Sciences 103(24): 9045

35. Christensen J (1963) Corn Smut Caused by Ustilago Maydis: American Phytopathological Society.

36. Mösch 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. Molecular Biology of the Cell 10(5): 1325

37. Ihara K, Muraguchi S, Kato M, Shimizu T, Shirakawa M, Kuroda S, Kaibuchi K, Hakoshima T (1998) Crystal Structure of Human RhoA in a Dominantly Active Form Complexed with a GTP Analogue. Journal of Biological Chemistry 273(16): 9656-9666

38. Wei Y, Zhang Y, Derewenda U, Liu X, Minor W, Nakamoto R, Somlyo A, Somlyo A, Derewenda Z (1997) Crystal structure of RhoA-GDP and its functional implications. Nature Structural Biology 4: 699-703

39. Mein besonderer Dank gilt Lars Hoffmann, der mir schon so lange zur Seite steht und immer für mich da ist und meinen Eltern, die mich während der ganzen Zeit unterstützt haben.

40. Chen C, Dickman M (2004) Dominant active Rac and dominant negative Rac revert the dominant active Ras phenotype in Colletotrichum trifolii by distinct signalling pathways. Molecular Microbiology 51(5): 1493-1507

41. Ein ganz besonderer Dank geht natürlich an die Mitglieder und ehemaligen Mitglieder der

42. Kahmann R, Basse C, Feldbrügge M (1999) Fungal-plant signalling in the Ustilago maydis- maize pathosystem. Current opinion in microbiology 2(6): 647-650

43. Schink KO (2010) Funktionelle Analyse von Rho-spezifischen Guaninnukleotidaustauschfaktoren in Ustilago maydis. Universitätsbibliothek Marburg, Schmidt A, Hall A (2002) Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes & Development 16(13): 1587-1609

44. Lamarche N, Hall A (1994) GAPs for rho-related GTPases. Trends Genet 10(12): 436-440

45. Ziman M, Johnson DI (1994) Genetic evidence for a functional interaction between Saccharomyces cerevisiae CDC24 and CDC42. Yeast 10(4): 463-474

46. Rolland F, de Winde JH, Lemaire K, Boles E, Thevelein JM, Winderickx J (2000) Glucose- induced cAMP signalling in yeast requires both a G-protein coupled receptor system for extracellular glucose detection and a separable hexose kinase-dependent sensing process. Molecular Microbiology 38(2): 348-358

47. Kübler E, Mösch HU, Rupp S, Lisanti MP (1997) Gpa2p, a G-protein -subunit, regulates growth and pseudohyphal development in Saccharomyces cerevisiae via a cAMP-dependent mechanism. Journal of Biological Chemistry 272(33): 20321

48. homologues participate in pathways controlling cell separation and cell polarity.

49. Brown J, Stowers L, Baer M, Trejo J, Coughlin S, Chant J (1996) Human Ste20 homologue hPAK1 links GTPases to the JNK MAP kinase pathway. Curr Biol 6: 598–605

50. Mitin N, Ramocki M, Zullo A, Der C, Konieczny S, Taparowsky E (2004) Identification and Characterization of Rain, a Novel Ras-interacting Protein with a Unique Subcellular Localization. Journal of Biological Chemistry 279(21): 22353-22361

51. Lobo S, Greentree W, Linder M, Deschenes R (2002) Identification of a Ras Palmitoyltransferase in Saccharomyces cerevisiae. Journal of Biological Chemistry 277(43): 41268-41273

52. Brachmann A, Weinzierl G, Kamper J, Kahmann R (2001) Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Molecular Microbiology 42(4): 1047-1063

53. Joyce D, Bouzahzah B, Fu M, Albanese C, D'Amico M, Steer J, Klein J, Lee R, Segall J, Westwick J (1999) Integration of Rac-dependent Regulation of Cyclin D1 Transcription through a Nuclear Factor-?B-dependent Pathway. Journal of Biological Chemistry 274(36): 25245-25249

54. Zheng Y, Bender A, Cerione RA (1995) Interactions among proteins involved in bud-site selection and bud-site assembly in Saccharomyces cerevisiae. Journal of Biological Chemistry 270(2): 626

55. McCormick F, Wittinghofer A (1996) Interactions between Ras proteins and their effectors.

56. Toda T, Uno I, Ishikawa T, Powers S, Kataoka T, Broek D, Cameron S, Broach J, Matsumoto K, Wigler M (1985) In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40(1): 27-36

57. Takai Y, Kaibuchi K, Kikuchi A (1992) Kawata T (1992): Small GTP-binding proteins. Int Rev Cytol 133: 187-230

58. Steinberg G, Schliwa M, Lehmler C, Bölker M, Kahmann R, McIntosh JR (1998) Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. Journal of Cell Science 111: 2235

59. Magee A, Newman C, Giannakouros T, Hancock J, Fawell E, Armstrong J (1992) Lipid modifications and function of the ras superfamily of proteins. Biochem Soc Trans 20(2): 497- 499

60. Park HO, Kang PJ, Rachfal AW (2002) Localization of the Rsr1/Bud1 GTPase involved in selection of a proper growth site in yeast. Journal of Biological Chemistry 277(30): 26721

61. Dai Q, Choy E, Chiu V, Romano J, Slivka S, Steitz S, Michaelis S, Philips M (1998) Mammalian Prenylcysteine Carboxyl Methyltransferase Is in the Endoplasmic Reticulum. Journal of Biological Chemistry 273(24): 15030-15034

62. Huang P, Han J, Hui L (2011) MAPK signaling in inflammation-associated cancer development. Protein & Cell 1(3): 218-226

63. Boyartchuk V, Ashby M, Rine J (1997) Modulation of Ras and a-factor function by carboxyl- terminal proteolysis. Science 275(5307): 1796-1800

64. Fukumoto Y, Kaibuchi K, Hori Y, Fujioka H, Araki S, Ueda T, Kikuchi A, Takai Y (1990) Molecular cloning and characterization of a novel type of regulatory protein (GDI) for the rho proteins, ras p21-like small GTP-binding proteins. Oncogene 5(9): 1321-1328

65. Milburn M, Tong L, deVos A, Brunger A, Yamaizumi Z, Nishimura S, Kim S (1990) Molecular switch for signal transduction: structural differences between active and inactive forms of protooncogenic ras proteins. Science 247(4945): 939

66. Tudzynski P, Scheffer J (2004) Pathogen profile Claviceps purpurea: molecular aspects of a unique pathogenic lifestyle. Molecular Plant Pathology 5(5): 377

67. Welch H, Coadwell W, Stephens L, Hawkins P (2003) Phosphoinositide 3-kinase-dependent activation of Rac. FEBS Lett 546(1): 93-97

68. Kaffarnik F (2003) PKA and MAPK phosphorylation of Prf 1 allows promoter discrimination in Ustilago maydis. The EMBO Journal 22(21): 5817-5826

69. Rebecchi M, Scarlata S (1998) PLECKSTRIN HOMOLOGY DOMAINS: A Common Fold with Diverse Functions. Annual Review of Biophysics and Biomolecular Structure 27(1): 503-528

70. Clarke S, Vogel J, Deschenes R, Stock J (1988) Posttranslational Modification of the Ha-ras Oncogene Protein: Evidence for a Third Class of Protein Carboxyl Methyltransferases. Proceedings of the National Academy of Sciences 85(13): 4643-4647

71. Barbieri MA, Kohn AD, Roth RA, Stahl PD (1998) Protein kinase B/akt and rab5 mediate Ras activation of endocytosis. Journal of Biological Chemistry 273(31): 19367

72. Zhang F, Casey P (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu Rev Biochem 65: 241-269

73. Casey P, Seabra M (1996) Protein prenyltransferases. J Biol Chem 271(10): 5289-5292

74. Sasaki T, Kikuchi A, Araki S, Hata Y, Isomura M, Kuroda S, Takai Y (1990) Purification and characterization from bovine brain cytosol of a protein that inhibits the dissociation of GDP from and the subsequent binding of GTP to smg p25A, a ras p21-like GTP-binding protein. Journal of Biological Chemistry 265(4): 2333-2337

75. Didsbury J, Weber R, Bokoch G, Evans T, Snyderman R (1989) rac, a novel ras-related family of proteins that are botulinum toxin substrates. Journal of Biological Chemistry 264(28): 16378-16382

76. Fang HM, Wang Y (2006) RA domain mediated interaction of Cdc35 with Ras1 is essential for increasing cellular cAMP level for Candida albicans hyphal development. Molecular Microbiology 61(2): 484-496

77. Feig L (2003) Ral-GTPases: approaching their 15 minutes of fame. Trends Cell Biol 13(8): 419–425

78. Patzak S (2007) Regulation der Zellknospung durch Rsr1 in Ustilago maydis. Diploma Thesis, Molekulargenetik, Philipps-Universität Marburg, Marburg

79. Fukata M, Kuroda S, Fujii K, Nakamura T, Shoji I, Matsuura Y, Okawa K, Iwamatsu A, Kikuchi A, Kaibuchi K (1997) Regulation of Cross-linking of Actin Filament by IQGAP1, a Target for Cdc42. Journal of Biological Chemistry 272(47): 29579-29583

80. Ren X, Schwartz M (1998) Regulation of inositol lipid kinases by Rho and Rac. Curr Opin Genet Dev 8(1): 63-67

81. Buchsbaum R, Connolly B, Feig L (2003) Regulation of p70 S6 Kinase by Complex Formation between the Rac Guanine Nucleotide Exchange Factor (Rac-GEF) Tiam1 and the Scaffold Spinophilin*. Journal of Biological Chemistry 278(21): 18833-18841

82. Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. The Journal of Cell Biology 144(6): 1235

83. Fukui Y, Kozasa T, Kaziro Y, Takeda T, Yamamoto M (1986) Role of a ras homolog in the life cycle of Schizosaccharomyces pombe. Cell 44(2): 329-336

84. Glomset J, Farnsworth C (1994) Role of protein modification reactions in programming interactions between ras-related GTPases and cell membranes. Annu Rev Cell Biol 10: 181- 205

85. Weeks G, Spiegelman GB (2003) Roles played by Ras subfamily proteins in the cell and developmental biology of microorganisms. Cellular signalling 15(10): 901-909

86. Lemmon M, Ferguson K (2000) Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 350(1)

87. Anand Apte B, Zetter B (1997) Signaling Mechanisms in Growth Factor Stimulated Cell Motility. Stem Cells 15(4): 259-267

88. Fenteany G, Janmey P, Stossel T (2000) Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Current Biology 10(14): 831-838

89. Jensen S, Geymonat M, Johnson AL, Segal M, Johnston LH (2002) Spatial regulation of the guanine nucleotide exchange factor Lte1 in Saccharomyces cerevisiae. Journal of Cell Science 115: 4977-4991

90. Golovanov A, Chuang T, DerMardirossian C, Barsukov I, Hawkins D, Badii R, Bokoch G, Lian L, Roberts G (2001) Structure-activity relationships in flexible protein domains: regulation of rho GTPases by RhoGDI and D4 GDI. J Mol Biol 305(1): 121-135

91. Pai E, Kabsch W, Krengel U, Holmes K, John J, Wittinghofer A (1989) Structure of the guanine- nucleotide-binding domain of the Ha-ras oncogene product p21 in the triphosphate conformation. Nature 341: 209-214

92. Nichols CB, Ferreyra J, Ballou ER, Alspaugh JA (2009) Subcellular localization directs signaling specificity of the Cryptococcus neoformans Ras1 protein. Eukaryotic Cell 8(2): 181

93. Li R, Bowerman B (2010) Symmetry breaking in biology. Cold Spring Harbor Perspectives in Biology 2(3)

94. Hall A (1990) The cellular functions of small GTP-binding proteins. Science 249(4969): 635

95. Leveleki L, Mahlert M, Sandrock B, Bolker M (2004) The PAK family kinase Cla 4 is required for budding and morphogenesis in Ustilago maydis. Molecular Microbiology 54(2): 396-406

96. Hartmann H, Kahmann R, Bölker M (1996) The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO J 15(7): 1632-1641

97. Truckses D, Bloomekatzs J, Thorner J (2004) The RA Domain of Ste50 Adaptor Protein Is Required for Delivery of Ste11 to the Plasma Membrane in the Filamentous Growth Signaling Pathway of the Yeast Saccharomyces cerevisiae Molecular and Cellular Biology 26(3): 912-928

98. Valencia A, Chardin P, Wittinghofer A, Sander C (1991) The ras protein family: evolutionary tree and role of conserved amino acids. Biochemistry 30(19): 4637-4648

99. Boettner B, Van Aelst L (2002) The RASputin effect. Genes & Development 16(16): 2033

100. Hrycyna C, Sapperstein S, Clarke S, Michaelis S (1991) The Saccharomyces cerevisiae STE14 gene encodes a methyltransferase that mediates C-terminal methylation of a-factor and RAS proteins. EMBO J 10(7): 1699-1709

101. Kawasaki T, Henmi K, Ono E, Hatakeyama S, Iwano M, Satoh H, Shimamoto K (1999) The small GTP-binding protein Rac is a regulator of cell death in plants. Proceedings of the National Academy of Sciences of the United States of America 96(19): 10922

102. Ridley A, Hall A (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70(3): 389-399

103. Mayorga M, Gold S (2001) The ubc 2 gene of Ustilago maydis encodes a putative novel adaptor protein required for filamentous growth, pheromone response and virulence. Molecular Microbiology 41(6): 1365-1379

104. Andrews D, Egan J, Mayorga M, Gold S (2000) The Ustilago maydis ubc 4 and ubc 5 Genes Encode Members of a MAP Kinase Cascade Required for Filamentous Growth. Molecular Plant-Microbe Interactions 13(7): 781-786

105. Rotblat B, Prior IA, Muncke C, Parton RG, Kloog Y, Henis YI, Hancock JF (2004) Three separable domains regulate GTP-dependent association of H-ras with the plasma membrane. Molecular and Cellular Biology 24(15): 6799

106. Papadaki P, Pizon V, Onken B, Chang EC (2002) Two ras pathways in fission yeast are differentially regulated by two ras guanine nucleotide exchange factors. Molecular and Cellular Biology 22(13): 4598

107. Tolias K, Hartwig J, Ishihara H, Shibasaki Y, Cantley L, Carpenter C (2000) Type Ia phosphatidylinositol-4-phosphate 5-kinase mediates Rac-dependent actin assembly. Current Biology 10(3): 153-156

108. Klosterman SJ, Martinez-Espinoza AD, Andrews DL, Seay JR, Gold SE (2008) Ubc2, an ortholog of the yeast Ste50p adaptor, possesses a basidiomycete-specific carboxy terminal extension essential for pathogenicity independent of pheromone response. Molecular Plant-Microbe Interactions 21(1): 110-121

109. Snetselaar K, Bolker M, Kahmann R (1996) Ustilago maydis Mating Hyphae Orient Their Growth toward Pheromone Sources. Fungal Genet Biol 20(4): 299-312

110. Takai Y, Sasaki T, Matozaki T (2001) Small GTP-Binding Proteins. Physiological Reviews 81(1): 153-208

111. Garnett M, Marais R (2004) Guilty as charged: B-RAF is a human oncogene. Cancer Cell 6(313): 9

112. Wang Y, Xu HP, Riggs M, Rodgers L, Wigler M (1991) byr2, a Schizosaccharomyces pombe gene encoding a protein kinase capable of partial suppression of the ras1 mutant phenotype. Molecular and Cellular Biology 11(7): 3554

113. 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 79(1): 131-141

114. Kataoka T, Powers S, McGill C, Fasano O, Strathern J, Broach J, Wigler M (1984) Genetic analysis of yeast RAS1 and RAS2 genes. Cell 37(2): 437-445

115. Homolog Canoe Acts as a Rap1 Effector During Dorsal Closure of the Drosophila Embryo. Genetics 165(1): 159-169

116. Li N, Batzer A, Daly R, Yajnik V, Skolnik E, Chardin P, Bar-Sagi D, Margolis B, Schlessinger J (1993) Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 363 85: 88

117. Snetselaar KM, KM, Mims C (1993) Infection of maize stigmas by Ustilago maydis: light and electron microscopy. Phytopathology 83: 843-850

118. Snetselaar K, Mims C (1992) Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia 84(2): 193-203

119. Roy S, Plowman S, Rotblat B, Prior IA, Muncke C, Grainger S, Parton RG, Henis YI, Kloog Y, Hancock JF (2005) Individual palmitoyl residues serve distinct roles in H-ras trafficking, microlocalization, and signaling. Molecular and Cellular Biology 25(15): 6722

120. Hurtado C, Beckerich J, Gaillardin C, Rachubinski R (2000) A Rac Homolog Is Required for Induction of Hyphal Growth in the Dimorphic Yeast Yarrowia lipolytica. Journal of Bacteriology 182(9): 2376-2386

121. Vallim M, Nichols C, Fernandes L, Cramer K, Alspaugh J (2005) A Rac Homolog Functions Downstream of Ras1 To Control Hyphal Differentiation and High-Temperature Growth in the Pathogenic Fungus Cryptococcus neoformans. Eukaryotic Cell 4(6): 1066-1078

122. Lorenz MC, Heitman J (1997) Yeast pseudohyphal growth is regulated by GPA2, a G protein homolog. The EMBO Journal 16(23): 7008-7018

123. Mösch H, Fink G (1997) Dissection of Filamentous Growth by Transposon Mutagenesis in Saccharomyces cerevisiae. Genetics 145(3): 671-684

124. Bishop A, Hall A (2000) Rho GTPases and their effector proteins. Biochem J 348(2): 241–255

125. Lee N, Kronstad J (2002) ras2 Controls Morphogenesis, Pheromone Response, and Pathogenicity in the Fungal Pathogen Ustilago maydis. Eukaryotic Cell 1(6): 954-966

126. Santangelo GM (2006) Glucose signaling in Saccharomyces cerevisiae. Microbiology and molecular biology reviews 70(1): 253

127. Müller P, Katzenberger J, Loubradou G, Kahmann R (2003) Guanyl Nucleotide Exchange Factor Sql2 and Ras2 Regulate Filamentous Growth in Ustilago maydis. Eukaryotic Cell 2(3): 609-617

128. Clark E, King W, Brugge J, Symons M, Hynes R (1998) Integrin-mediated Signals Regulated by Members of the Rho Family of GTPases. The Journal of Cell Biology 142(2): 573-586

129. Han L, Wong D, Dhaka A, Afar D, White M, Xie W, Herschman H, Witte O, Colicelli J (1997) Protein binding and signaling properties of RIN1 suggest a unique effector function. Proceedings of the National Academy of Sciences of the United States of America 94(10): 4954

130. Price L, Leng J, Schwartz M, Bokoch G (1998) Activation of Rac and Cdc42 by Integrins Mediates Cell Spreading. Molecular Biology of the Cell 9(7): 1863-1871

131. Fortwendel JR, Fuller KK, Stephens TJ, Bacon WC, Askew DS, Rhodes JC (2008) Aspergillus fumigatus RasA regulates asexual development and cell wall integrity. Eukaryotic Cell 7(9):

132. Xu K, Chong DC, Rankin SA, Zorn AM, Cleaver O (2009) Rasip1 is required for endothelial cell motility, angiogenesis and vessel formation. Developmental biology 329(2): 269-279

133. Dechant R, Binda M, Lee SS, Pelet S, Winderickx J, Peter M (2010) Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. The EMBO Journal 29(15): 2515-2526

134. Banuett F, Herskowitz I (1989) Different a Alleles of Ustilago maydis are Necessary for Maintenance of Filamentous Growth but not for Meiosis. Proceedings of the National Academy of Sciences 86(15): 5878-5882

135. Smith D, Garcia-Pedrajas M, Hong W, Yu Z, Gold S, Perlin M (2004) An ste20 Homologue in Ustilago maydis Plays a Role in Mating and Pathogenicity. Eukaryotic Cell 3(1): 180-189

136. Ziman M, O'Brien J, Ouellette L, Church W, Johnson D (1991) Mutational analysis of CDC42Sc, a Saccharomyces cerevisiae gene that encodes a putative GTP-binding protein involved in the control of cell polarity. Molecular and Cellular Biology 11(7): 3537-3544

137. Field J, Nikawa JI, Broek D, MacDonald B, Rodgers L, Wilson IA, Lerner RA, Wigler M (1988) Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Molecular and Cellular Biology 8(5): 2159

138. Feig L, Cooper G (1988) Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Molecular and Cellular Biology 8(8): 3235-3243

139. Gibbs J, Sigal I, Poe M, Scolnick E (1984) Intrinsic GTPase Activity Distinguishes Normal and Oncogenic ras p21 Molecules. Proceedings of the National Academy of Sciences 81(18): 5704- 5708

140. Mösch HU, Roberts RL, Fink GR (1996) Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America 93(11): 5352

141. Spellig T, Bölker M, Lottspeich F, Frank R, Kahmann R (1994) Pheromones trigger filamentous growth in Ustilago maydis. EMBO J 13(7): 1620-1627

142. Van Aelst L, Joneson T, Bar-Sagi D (1996) Identification of a novel Rac1-interacting protein involved in membrane ruffling. EMBO J 15(15): 3778-3786

143. Ramer SW, Davis RW (1993) A dominant truncation allele identifies a gene, STE20, that encodes a putative protein kinase necessary for mating in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America 90(2): 452

144. Neal SE, Eccleston JF, Webb MR (1990) Hydrolysis of GTP by p21NRAS, the NRAS protooncogene product, is accompanied by a conformational change in the wild-type protein: use of a single fluorescent probe at the catalytic site. Proceedings of the National Academy of Sciences of the United States of America 87(9): 3562

145. Bourne H, Sanders D, McCormick F (1990) The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348: 125-132

146. Bourne H, Sanders D, McCormick F (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349: 117-127

147. West M, Kung H, Kamata T (1990) A novel membrane factor stimulates guanine nucleotide exchange reaction of ras proteins. FEBS letters 259(2): 245-248

148. Schulz B, Banuett F, Dahl M, Schlesinger R, Schäfer W, Martin T, Herskowitz I, Kahmann R (1990) The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60(2): 295-306

149. Boelker M, Urban M, Kahmann R (1992) The a mating type locus of U. maydis specifies cell signaling components. Cell 68: 441–450

150. Mionnet C, Bogliolo S, Arkowitz RA (2008) Oligomerization regulates the localization of Cdc24, the Cdc42 activator in Saccharomyces cerevisiae. Journal of Biological Chemistry 283(25): 17515