Ras and rho small G proteins: Insights from the Schizophyllum commune genome sequence and comparisons to other fungi

Biotechnology and Genetic Engineering Reviews

Volumn 28, Issue , 2012, Pages 61-100

  Raudaskoski, Marjatta ^a   Kothe, Erika ^b   Fowler, Thomas J ^c   Jung, Elke Martina ^b   Horton, J Stephen ^d  

^a UNIVERSITY OF TURKU   (Finland)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c SOUTHERN ILLINOIS UNIVERSITY EDWARDSVILLE   (United States)

^d UNION COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; PROTEINS;

ANIMAL CELLS; FILAMENTOUS FUNGUS; FRUITING BODIES; GENOME COMPARISON; GENOME SEQUENCES; HYPHAL GROWTH; SCHIZOPHYLLUM COMMUNE; SEXUAL REPRODUCTION; SIGNALLING PATHWAYS; SMALL G PROTEINS;

FUNGI;

CYCLIC AMP; EFFECTOR CASPASE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; P21 ACTIVATED KINASE; PROTEIN TYROSINE PHOSPHATASE; RAP PROTEIN; RAS PROTEIN; REGULATOR PROTEIN; RHO FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ASPERGILLUS; CRYPTOCOCCUS NEOFORMANS; CYTOLOGY; FRUITING BODY; FUNGUS; GENE FUNCTION; GENE SEQUENCE; GENOME; HUMAN; LACCARIA; MEDICAL RESEARCH; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FAMILY; PROTEIN FUNCTION; REPRODUCTION; REVIEW; SACCHAROMYCES CEREVISIAE; SCHIZOPHYLLUM COMMUNE; SCHIZOSACCHAROMYCES POMBE; SIGNAL TRANSDUCTION; USTILAGO MAYDIS;

ANIMALIA; BASIDIOMYCOTA; FUNGI; SCHIZOPHYLLUM COMMUNE;

EID: 84860894952     PISSN: 02648725     EISSN: None     Source Type: Journal    
DOI: 10.5661/bger-28-61     Document Type: Review

References (172)

1. ADAMO, J.E., ROSSI, G. and BRENNWALD, P. (1999) The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Molecular Biology of the Cell 10, 4121-33.
2. AITTALEB, M, BOGUTH, C.A. and TESMER, J.J. (2010) Structure and function of heterotrimeric G protein-regulated Rho guanine nucleotide exchange factors. Molecular Pharmacology 77, 111-25.
3. ALSPAUGH, J.A., CAVALLO, L.M., PERFECT, J.R. and HEITMAN, J. (2000) RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans. Molecular Microbiology 36, 352-65.
4. ALTSCHULER, D.L., MURO, A., SCHIJMAN, A, ALMONACID, F.B. and TORRES, H.N. (1990) Neurospora crassa cDNA clones coding for a new member of the ras protein family. FEBS Letters 273, 103-6.
5. ARIAS-ROMERO, L.E., and CHERNOFF, J. (2008) A tale of two Paks. Biology of the Cell 100, 97-108.
6. ASPURIA, P.-J. and TAMANOI, F. (2004) The Rheb family of GTP-binding proteins. Cellular Signalling 16, 1105-12.
7. ASPURIA P.-J., SATO, T. and TAMANOI, F. (2007) The TSC/Rheb/TOR signaling pathway in fission yeast and mammalian cells: temperature sensitive and constitutive active mutants of TOR. Cell Cycle 6, 1692-5.
8. BAARLINK, C. and GROSSE, R. (2008) A GBD uncovered: the FHOD1 N terminus is formin'. Structure 16, 1287-8.
9. BASSAM, R. A., NOUVEL, I., LEUNG, K.F., HUME, A.N. and SEABRA, M.C. (2010) A novel statin-mediated "prenylation block-and-release" assay provides insight into the membrane targeting mechanisms of small GTPases. Biochemical and Biophysical Research Communications 397, 34-41.
10. BAUER, Y., KNECHTLE, P., WENDLAND, J., HELFER, H. and PHILIPPSEN, P. (2004) A Ras-like GTPase is involved in hyphal growth guidance in the filamentous fungus Ashbya gossypii. Molecular Biology of the Cell 15, 4622-32.
11. BOS, J.L,, REHMANN, H. and WITTINGHOFER, A. (2007) GEFs and GAPs: critical elements in the control of small G proteins. Cell 129, 865-77.
12. BOSE, I., IRAZOQUI, J.E., MOSKOW, J.J. ET AL. (2001) Assembly of scaffold-mediated complexes containing Cdc42p, the exchange factor Cdc24p, and the effector Cla4p required for cell cycle-regulated phosphorylation of Cdc24p. Journal of Biological Chemistry 276, 7176-86.
13. BOULTER, E., GARCIA-MATA, R., GUILLUY, C. ET AL. (2010) Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nature Cell Biology 12, 477-83.
14. BOYCE, K.J., HYNES, M.J. and ANDRIANOPOULOS, A. (2001) The CDC42 homolog of the dimorphic fungus Penicillium marneffei is required for correct cell polarization during growth but not development. Journal of Bacteriology 183, 3447-57.
15. BOYCE, K.J., HYNES, M.J. and ANDRIANOPOULOS, A. (2002) Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog. Journal of Cell Science 116, 1249-60.
16. BOYCE, K.J., HYNES, M.J. and ANDRIANOPOULOS, A. (2005) The Ras and Rho GTPases genetically interact to co-ordinately regulate cell polarity during development in Penicillium marneffei. Molecular Microbiology 55, 1487-501.
17. BRENNWALD, P. and ROSSI, G. (2007) Spatial regulation of exocytosis and cell polarity: yeast as a model for animal cells. FEBS Letters 581, 2119-24.
18. BROACH, J.R. (1991) RAS genes in Saccharomyces cerevisiae: signal transduction in search of a pathway. Trends in Genetics 7, 28-33.
19. BROEK, D., TODA, T., MICHAELI, T. ET AL. (1987) The S. cerevisiae CDC25 gene product regulates the RAS/adenylate cyclase pathway. Cell 48, 789-99.
20. BROWN, M.D. and SACKS, D.B. (2006) IQGAP1 in cellular signaling: bridging the GAP. Trends in Cell Biology 16, 242-9.
21. CANSADO, J. T., SOTO, M. G. and PÉREZ, P. (2010) Rga4, a Rho-GAP from fission yeast. Finding specificity within promiscuity. Communicative & Integrative Biology 3, 436-9.
22. CERIONE. R.A. and ZHENG, Y. (1996) The Dbl family of oncogenes. Current Opinion in Cell Biology 8, 216-22.
23. CHANG, E.C., BARR, M., WANG, Y. ET AL. (1994) Cooperative interaction of S. pombe proteins required for mating and morphogenesis. Cell 79, 131-41
24. CHANG, F., DRUBIN, D. and NURSE, P. (1997) cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. Cell Biology 137, 169-82.
25. CHEN, C. and DICKMAN, M.B. (2005) cAMP blocks MAPK activation and sclerotial development via Rap-1 in a PKA-independent manner in Sclerotinia sclerotiorum. Molecular Microbiology 55, 299-311.
26. CHEN, C., HA, Y., MIN, J., MEMMOTT, S.D. and DICKMAN, M.B. (2006) Cdc42 is required for proper growth and development in the fungal pathogen Colletotrichum trifolii. Eukaryotic Cell 5, 155-66.
27. CHEN, J., ZHENG, W., ZHENG, S. ET AL. (2008) Rac1 is required for pathogenicity and Chm1-dependent conidiogenesis in rice fungal pathogen Magnaporthe grisea. PLoS Pathogen 4(11), e1000202.
28. CHESARONE, M.A. and GOODE, B,L. (2009) Actin nucleation and elongation factors: mechanisms and interplay. Current Opinion in Cell Biology 21, 28-37.
29. COLE, K.C., MCLAUGHLIN, H.W. and JOHNSON, D.I. (2007) Use of bimolecular fluorescence complementation to study in vivo interactions between Cdc42p and Rdi1p of Saccharomyces cerevisiae. Eukaryotic Cell 6, 378-87.
30. CRÉCHET, J.B., POULLET, P. MISTOU, M.Y. ET AL. (1990) Enhancement of the GDP-GTP exchange of RAS proteins by the carboxyl-terminal domain of SCD25. Science 248, 866-8.
31. D'ANGELO, I., WELTI, S., BONNEAU, F. and SCHEFFZEK, K. (2006) A novel bipartite phospholipid-binding module in the neurofibromatosis type 1 protein. EMBO Report 7, 174-9.
32. DEFEO-JONES, D., SCOLNICK, E.M., KOLLER, R. and DHAR, R. (1983) Ras-related gene sequences identified and isolated from Saccharomyces cerevisiae. Nature 306, 707-9.
33. DERMARDIROSSIAN, C. and BOKOCH, G. M. (2005) GDIs: central regulatory molecules in Rho GTPase activation. Trends in Cell Biology 15, 356-63.
34. DOIGNON, F., WEINACHTER, C., ROUMANIE, O. and CROUZET, M.(1999) The yeast Rgd1p is a GTPase activating protein of the Rho3 and rho4 proteins. FEBS Letters 459, 458-62.
35. DOVAS, A. and COUCHMAN, J.R.(2005) RhoGDI: multiple functions in the regulation of Rho family GTPase activities. Biochemical Journal 390, 1-9.
36. ENG, K., NAQVI, N.I., WONG, K.C. and BALASUBRAMANIAN, M.K. (1998) Rng2p, a protein required for cytokinesis in fission yeast, is a component of the actomyosin ring and the spindle pole body. Current Biology 8, 611-21.
37. EPP, J. A. and CHANT, J. (1997) An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast. Current Biology 7, 921-9.
38. EVANGELISTA, M., BLUNDELL, K., LONGTINE, M.S. ET AL. (1997) Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276, 118-22.
39. EVANGELISTA, M., PRUYNE, D., AMBERG, D.C., BOONE, C. and BRETSCHER, A. (2002) Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nature Cell Biology 4, 32-41.
40. FEIERBACH, B. and CHANG, F. (2001) Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Current Biology 11, 1656-65.
41. FERNÁNDEZ-MEDARDE, A. and SANTOS, E. (2011) The RasGrf family of mammalian guanine nucleotide exchange factors. Biochimica et Biophysica Acta 1815, 170-88.
42. FILLINGER, S., CHAVEROCHE, M.K., SHIMIZU, K., KELLER, N. and D'ENFERT, C. (2002) cAMP and ras signalling independently control spore germination in the filamentous fungus Aspergillus nidulans. Molecular Microbiology 44, 1001-16.
43. FORTWENDEL, J.R., PANEPINTO, J.C., SEITZ, A.E., ASKEW, D.S. and RHODES, J.C. (2004) Aspergillus fumigatus rasA and rasB regulate the timing and morphology of asexual development. Fungal Genetics and Biology 41, 129-39.
44. FORTWENDEL, J.R., FULLER, K.K., STEPHENS, T.J. ET AL. (2008) Aspergillus fumigatus RasA regulates asexual development and cell wall integrity. Eukaryotic Cell 7, 1530-9.
45. FORTWENDEL, J.R., JUVVADI, P.R., ROGG, L.E. and STEINBACH, W.J. (2011) Regulatable Ras Activity Is Critical for Proper Establishment and Maintenance of Polarity in Aspergillus fumigatus. Eukaryotic Cell 10, 611-5.
46. FRISCHE, E.W. and ZWARTKRUIS, F.J. (2010) Rap1, a mercenary among the Ras-like GTPases. Developmental Biology 340, 1-9.
47. FUENTES, G. and VALENCIA, A. (2009) Ras classical effectors: new tales from in silico complexes. Trends in Biochemical Sciences 34, 533-9.
48. FUKUDA, M. (2010) How can mammalian Rab small GTPases be comprehensively analyzed?: Development of new tools to comprehensively analyze mammalian Rabs in membrane traffic. Histology and Histopathology 25, 1473-80.
49. FUKUI, Y., KOZASA, T., KAZIRO, Y., TAKEDA, T., and YAMAMOTO, M. (1986) Role of a ras homolog in the life cycle of Schizosaccharomyces pombe. Cell 44, 329-36.
50. GAO, L. and BRETSCHER, A. (2008) Analysis of unregulated formin activity reveals how yeast can balance F-actin assembly between different microfilament-based organizations. Molecular Biology of the Cell 19, 1474-84.
51. GARCÍA, P., TAJADURA, V., GARCÍA, I., and SÁNCHEZ, Y. (2006) Role of Rho GTPases and Rho-GEFs in the regulation of cell shape and integrity in fission yeast. Yeast 23, 1031-43.
52. GIBBS, J. B. and MARSHALL, M.S. (1989) The ras oncogene - an important regulatory element in lower eucaryotic organisms. Microbiology Review 53, 171-85.
53. GORFER, M., TARKKA, M.,HANIF, M. ET AL. (2001) Characterization of small GTPases Cdc42 and Rac and the relationship between Ccdc42 and actin cytoskeleton in vegetative and ectomycorrhizal hyphae of Suillus bovinus. Molecular Plant Microbe Interactions 14, 135-44.
54. GREENBERG, L. and HATINI, V. (2011) Systematic expression and loss-of-function analysis defines spatially restricted requirements for Drosophila RhoGEFs and RhoGAPs in leg morphogenesis. Mechanisms of Development 128, 5-17.
55. HARASHIMA, T., ANDERSON, S., YATES, J.R. and HEITMAN, J. (2006) The kelch proteins Gpb1 and Gpb2 inhibit Ras activity via association with the yeast RasGAP neurofibromin homologs Ira1 and Ira2. Molecular Cell 22, 819-30
56. HARRIS, S.D. (2011) Cdc42/Rho GTPases in fungi: variations on a common theme. Molecular Microbiology 79, 1123-7.
57. HARRIS, S.D., HAMER, L., SHARPLESS, K.E. and HAMER, J.E. (1997) The Aspergillus nidulans sepA gene encodes an FH1/2 protein involved in cytokinesis and the maintenance of cellular polarity. EMBO Journal 16, 3474-83.
58. HART, M.J., CALLOW, M.G., SOUZA, B. and POLAKIS, P. (1996) IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs. EMBO Journal 15, 2997-3005.
59. HE, B. and GUO, W. (2009) The exocyst elated domain, is a potential effector for cdc42Hs complex in polarized exocytosis. Current Opinion in Cell Biology 21, 537-42.
60. HEINRICH, M., KÖHLER, T., and MÖSCH, H.U. (2007) Role of Cdc42-Cla4 interaction in the pheromone response of Saccharomyces cerevisiae. Eukaryotic Cell 6, 317-27.
61. HORI, K., KAJIWARA, S., SAITO, T. ET AL. (1991) Cloning, sequence analysis and transcriptional expression of a ras gene of the edible basidiomycete Lentinus edodes. Gene 105, 91-6.
62. HUGHES, D.A., FUKUI, Y., YAMAMOTO, M. (1990) Homologous activators of ras in fission and budding yeast. Nature 344, 355-7.
63. IMAMURA, H., TANAKA, K., HIHARA, T. ET AL. (1997) Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO Journal 16, 2745-55.
64. ISHIBASHI, O. and SHISHIDO, K. (1993) Nucleotide sequence of a ras gene from the basidiomycete Coprinus cinereus. Gene 125, 233-4.
65. IWAKI, N., KARATSU, K. and MIYAMOTO, M. (2003) Role of guanine nucleotide exchange factors for Rho family GTPases in the regulation of cell morphology and actin cytoskeleton in fission yeast. Biochemical and Biophysical Research Communications 312, 414-20.
66. JACINTO, E. (2008) What controls TOR? IUBMB Life 60, 483-96.
67. JAFFE, A.B. and HALL, A. (2005) Rho GTPases: biochemistry and biology. Annual Review of Cell and Developmental Biology 21, 247-69.
68. JOHNSON, D.I. (1999) Cdc42: an essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiology and Molecular Biology Reviews 63, 54-105.
69. JOHNSON, D. I. and PRINGLE, J.R. (1990) Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. Journal of Cell Biology 111, 143-52.
70. JUSTA-SCHUCH, D., HEILIG, Y., RICHTHAMMER, C. and SEILER, S. (2010) Septum formation is regulated by the RHO4-specific exchange factors BUD3 and RGF3 and by the landmark protein BUD4 in Neurospora crassa. Molecular Microbiology 76, 220-35.
71. KAHMANN, R. and SCHIRAWSKI, J. (2007) Mating in the smut fungi: From a to b to downstream cascades. In: Sex in Fungi. Eds. Heitman, J., Kronstad, J.W., Taylor, J.W., and Casselton, L.A., pp 377-87. Washington, DC: ASM Press.
72. KANG, P.J., BÉVEN, L., HARIHARAN, S., and PARK, H.O. (2010) The Rsr1/Bud1 GTPase interacts with itself and the Cdc42 GTPase during bud-site selection and polarity establishment in budding yeast. Molecular Biology of the Cell 21, 3007-16.
73. KATAOKA, T., POWER, S., MCGILL, C. ET AL. (1984) Genetic analysis of yeast ras1 and ras2 genes. Cell 37, 437-45.
74. KATOH, K., KUMA, K., YOH, H. and MIYATA, T. (2005) MAFFT version5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511-8.
75. KOCH, G., TANAKA, K., MASUDA, T. ET AL. (1997) Association of the Rho family small GTP-binding proteins with Rho GDP dissociation inhibitor (Rho GDI) in Saccharomyces cerevisiae. Oncogene 15, 417-22.
76. KOZMINSKI, K.G., BEVEN, L., ANGERMAN, E., ET AL. (2003) Interaction between a Ras and a Rho GTPase couples selection of a growth site to the development of cell polarity in yeast. Molecular Biology of the Cell 14, 4958-70.
77. KURODA, S., FUKATA, M., KOBAYASHI, K. ET AL. (1996) Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1. Journal of Biological Chemistry 271, 23363-7.
78. KWON, M.J., ARENTSHORST, M., ROOS, E.D. ET AL. (2011) Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi. Molecular Microbiology 79,1151-67.
79. LEBERER, E., HARCUS, D., DIGNARD, D. ET AL. (2001) Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signalling pathways in the pathogenic fungus Candida albicans. Molecular Microbiology 42, 673-87.
80. LEE, N., and KRONSTAD, J.W. (2002) ras2 controls morphogenesis, pheromone response and pathogenicity in the fungal pathogen Ustilago maydis. Eukaryotic Cell 1, 954-66.
81. MAENG, S., KO, Y.J., KIM, G.B. ET AL. (2010) Comparative transcriptome analysis reveals novel roles of the Ras and cyclic AMP signaling pathways in environmental stress response and antifungal drug sensitivity in Cryptococcus neoformans. Eukaryotic Cell 9, 360-78.
82. MASUDA, T., TANAKA, K., NONAKA, H. ET AL. (1994) Molecular cloning and characterization of yeast rho GDP dissociation inhibitor. Journal of Biological Chemistry 269, 19713-8.
83. MENOTTA, M., AMICUCCI, A. and BASILI, G. ET AL. (2008) Molecular and functional characterization of a Rho GDP dissociation inhibitor in the filamentous fungus Tuber borchii. BMC Microbiology 8, 57.
84. MILLER, P. and JOHNSON, D.I. (1994) Cdc42p GTPase is involved in controlling polarized cell growth in Schizosaccharomyces pombe. Molecular and Cellular Biology 14, 1075-83
85. MOON, S.Y. and ZHENG, Y.(2003) Rho GTPase-activating proteins in cell regulation. Trends in Cell Biology 13,13-22.
86. MÜLLER, P., KATZENBERGER, J.D., LOUBRADOU, G. and KAHMANN, R. (2003) Guanyl nucleotide exchange factor Sql2 and Ras2 regulate filamentous growth in Ustilago maydis. Eukaryotic Cell 2, 609-17.
87. NAKANO, K. IMAI, J., ARAI, R. ET AL. (2002) The small GTPase Rho3 and the diaphanous/formin For3 function in polarized cell growth in fission yeast. Journal of Cell Science 115, 4629-39.
88. NAKANO, K., MUTOH, T., ARAI, R. and MABUCHI, I. (2003) The small GTPase Rho4 is involved in controlling cell morphology and septation in fission yeast. Genes to Cells 8, 357-70.
89. NAKANO, K., MUTOH, T. and MABUCHI, I. (2001) Characterization of GTPase-activating proteins for the function of the Rho-family small GTPases in the fission yeast Schizosaccharomyces pombe. Genes to Cells 6, 1031-42.
90. NICHOLS, C.B., PERFECT, Z.H., and ALSPAUGH, J.A. (2007) A Ras1-Cdc24 signal transduction pathway mediates thermotolerance in the fungal pathogen Cryptococcus neoformans. Molecular Microbiology 63, 1118-30.
91. OHM, R.A., DE JONG, J.F., LUGONES, L.G. ET AL. (2010) Genome sequence of the model mushroom Schizophyllum commune. Nature Biotechnology 28, 957-63.
92. ORY, S. and GASMAN, S. (2011) Rho GTPases and exocytosis: What are the molecular links? Seminars in Cell and Developmental Biology 22, 27-32.
93. OSHEROV, N. and MAY, G. (2000) Conidial germination in Aspergillus nidulans requires RAS signaling and protein synthesis. Genetics 155, 647-56.
94. OSMAN, M.A. and CERIONE, R.A. (1998) Iqg1p, a yeast homologue of the mammalian IQGAPs, mediates cdc42p effects on the actin cytoskeleton. Journal of Cell Biology 142, 443-55.
95. OTTILIE, S., MILLER, P.J., JOHNSON, D.I. ET AL. (1995) Fission yeast pak1+ encodes a protein kinase that interacts with Cdc42p and is involved in the control of cell polarity and mating. EMBO Journal 14, 5908-19.
96. OZAKI, K., TANAKA, K., IMAMURA, H. ET AL. (1996) Rom1p and Rom2p are GDP/GTP exchange proteins (GEPs) for the Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO Journal 15, 2196-207
97. PADMANABHAN, A., BAKKA, K., SEVUGAN, M. ET AL. (2011) IQGAP-related Rng2p organizes cortical nodes and ensures position of cell division in fission yeast. Current Biology 21, 467-72.
98. PADRICK, S.B. and ROSEN, M.K. (2010) Physical mechanisms of signal integration by WASP family proteins. Annual Review of Biochemistry 79, 707-35.
99. PALMER, G.E. and HORTON, J.S. (2006) Mushrooms by magic: making connections between signal transduction and fruiting body development in the basidiomycete fungus Schizophyllum commune. FEMS Microbiology Letters 262, 1-8.
100. PAPADAKI, P., PIZON, V., ONKEN, B. and CHANG, E.C. (2002) Two ras pathways in fission yeast are differentially regulated by two ras guanine nucleotide exchange factors. Molecular Cell Biology 22, 4598-606
101. PARK, H.-O. and BI, E. (2007) Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiology and Molecular Biology Reviews 71, 48-96
102. PARK, H.-O., BI, E., PRINGLE, J.R. and HERSKOWITZ, I. (1997) Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast cell polarity. Proceedings of the National Academy of Sciences of the United States of America 94, 4463-8.
103. PEREZ, P. and RINCÓN S.A. (2010) Rho GTPases: regulation of cell polarity and growth in yeasts. Biochemical Journal 426, 243-53.
104. PETERSEN, J., NIELSEN, O., EGEL, R. and HAGAN, I.M. (1998) FH3: A domain found in formins targets the fission yeast formin Fus1 to the projection tip during conjugation. Journal of Cell Biology 141, 1217-28
105. POLLARD, T.D. and WU, J.-Q. (2010) Understanding cytokinesis: lessons from fission yeast. Nature Reviews Molecular Cell Biology 11, 149-55.
106. PRICE, M.S., NICHOLS, C.B. and ALSPAUGH, J.A. (2008) The Cryptococcus neoformans Rho-GDP dissociation inhibitor mediates intracellular survival and virulence. Infection and Immunity 76, 5729-37.
107. QYANG, Y., YANG, P., DU, H. ET AL. (2002) The p21-activated kinase, Shk1, is required for proper regulation of microtubule dynamics in the fission yeast, Schizosaccharomyces pombe. Molecular Microbiology 44, 325-34.
108. RAAIJMAKERS, J.H. and BOS, J.L. (2009) Specificity in Ras and Rap signaling. Journal of Biological Chemistry 284, 10995-9.
109. RAJASHEKAR, B., KOHLER, A. JOHANSSON, T. ET AL. (2009) Expansion of signal pathways in the ectomycorrhizal fungus Laccaria bicolor- evolution of nucleotide sequences and expression patterns in families of protein kinases and RAS small GTPases. New Phytologist 183, 365-79.
110. RASMUSSEN, C.G. and GLASS, N.L. (2005) A Rho-type GTPase, rho-4, is required for septation in Neurospora crassa. Eukaryotic Cell 4, 1913-25.
111. RAUDASKOSKI, M. (1998) The relationship between B-mating-type genes and nuclear migration in Schizophyllum commune. Fungal Genetics and Biology 24, 207-27
112. RAUDASKOSKI, M. and KOTHE, E. (2010) Basidiomycete mating type genes and pheromone signaling. Eukaryotic Cell 9, 847-59.
113. RAUDASKOSKI, M., PARDO, A.G., TARKKA, M. ET AL. (2001) Small GTPases, cytoskeleton and signal transduction in filamentous homobasidiomycetes. In: Cell Biology of Plant and Fungal Tip Growth. NATO Science Series I. Life and behavioral sciences, Volume 328. Eds. Geitman, A., Cresti, M., Heath, I.B. pp 123-36. Washington, DC: IOS Press.
114. ROBINSON, L.C., GIBBS, J.B, MARSHALL, M.S, SIGAL, I.S. and TATCHELL, K.(1987) CDC25: a component of the RAS-adenylate cyclase pathway in Saccharomyces cerevisiae. Science 235, 1218-21.
115. ROLKE, Y. and TUDZYNSKI, P. (2008) The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: interaction and impact on polarity, development and pathogenicity. Molecular Microbiology 68, 405-23.
116. ROSSMAN, K.L., DER, C.J. and SONDEK, J. (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nature Reviews Molecular Cell Biology 6, 167-80.
117. ROUMANIE, O., WEINACHTER, C., LARRIEU, I., CROUZET, M. and DOIGNON, F. (2001) Functional characterization of the Bag7, Lrg1 and Rgd2 RhoGAP proteins from Saccharomyces cerevisiae. FEBS Letters 506, 149-56.
118. RUNEBERG, P., RAUDASKOSKI, M. and VIRTANEN, I. (1986) Cytoskeletal elements in the hyphae of the homobasidiomycete Schizophyllum commune visualized with indirect immunofluorescence and NBD-phallacidin. European Journal of Cell Biology 41, 25-32.
119. SANTOS, B., MARTÍN-CUADRADO, A.B., VÁZQUEZ DE ALDANA, C.R., DEL REY, F. and PÉREZ, P. (2005) Rho4 GTPase is involved in secretion of glucanases during fission yeast cytokinesis. Eukaryotic Cell 4, 1639-45.
120. SCHEFFER, J., CHEN, C., HEIDRICH, P., DICKMAN, M.B. and TUDZYNSKI, P. (2005) A CDC42 homologue in Claviceps purpurea is involved in vegetative differentiation and is essential for pathogenicity. Eukaryotic Cell 4, 1228-38
121. SCHMIDT, A. and HALL, M.N. (1998) Signalling to the actin cytoskeleton. Annual Review of Cell and Developmental Biology 14, 305-38.
122. SCHUBERT, D., RAUDASKOSKI, M., KNABE, N. and KOTHE, E. (2006) Ras GTPase activating protein Gap1 of the homobasidiomycete Schizophyllum commune regulates hyphal growth orientation and sexual development. Eukaryotic Cell 5, 683-95.
123. SCHWALB, M.N. (1974) Effect of adenosine 3′,5′-cyclic monophosphate on the morphogenesis of fruit bodies of Schizophyllum commune. Archives of Microbiology 96, 17-20.
124. SELLS. M., BARRATT, J.T., CAVISTON, J. ET AL. (1998) Characterization of Pak2p, a pleckstrin-homology domain-containing p21-activated protein kinase from fission yeast. Journal of Biological Chemistry 273, 18490-8.
125. SHEN, G., WHITTINGTON, A. and WANG, P. (2011) Wsp1, aGBD/CRIB domain-containing WASP homolog, is required for growth, morphogenesis, and virulence of Cryptococcus neoformans. Eukaryotic Cell 10, 521-9.
126. SI, H., JUSTA-SCHUCH, D., SEILER, S. and HARRIS, S.D. (2010) Regulation of septum formation by the Bud3-Rho4 GTPase module in Aspergillus nidulans. Genetics 185, 165-76.
127. SIROTKIN, V., BELTZNER, C.C., MARCHAND, J.B. and POLLARD, T.D. (2005) Interactions of WASp, myosin-I and verprolin with Arp2/3 complex during actin patch assembly in fission yeast. Journal of Cell Biology 170, 637-48.
128. SLAUGHTER, B.D., DAS, A., SCHWARTZ, J.W., RUBINSTEIN ,B. and LI, R. (2009) Dual modes of cdc42 recycling fine-tune polarized morphogenesis. Developmental Cell 17, 823-35.
129. SMITH, G. R., GIVAN, S.A., CULLEN, P. and SPRAGUE, JR., G.F. (2002) GTPase-Activating Proteins for Cdc42. Eukaryotic Cell 1, 469-80.
130. SOM, T. and KOLAPARTHI, V.S. (1994) Developmental decisions in Aspergillus nidulans are modulated by Ras activity. Molecular and Cellular Biology 14, 5333-48.
131. SOTO, T., VILLAR-TAJADURA, M.A., MADRID, M. ET AL. (2010) Rga4 modulates the activity of the fission yeast cell integrity MAPK pathway by acting as a Rho2 GTPase-activating protein. Journal of Biological Chemistry 285, 11516-25.
132. SPRINGETT, G.M., KAWASAKI, H. and SPRIGGS D.R. (2004) Non-kinase second-messenger signaling: new pathways with new promise. Bioessays 26, 730-8.
133. STEVENSON, B.J., FERGUSON, B., DE VIRGILIO, C. ET AL. (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 and Development 9, 2949-63.
134. STORK P.J. (2003) Does Rap1 deserve a bad Rap? Trends in Biochemical Sciences 28, 267-75.
135. SUNDARAM, S., KIM, S.J., SUZUKI, H. ET AL. (2001) Isolation and characterization of a symbiosis-regulated ras from the ectomycorrhizal fungus Laccaria bicolor. Molecular Plant Microbe Interactions 14, 618-28.
136. SZCZEPANOWSKA, J. (2009) Involvement of Rac/Cdc42/PAK pathway in cytoskeletal rearrangements. Acta Biochimica Polonica 56, 225-34.
137. TABIN, C.J., BRADLEY, S.M., BARGMANN, C.I. ET AL. (1982) Mechanism of activation of a human oncogene. Nature 300, 143-9.
138. TAKAINE, M., NUMATA, O. and NAKANO, K. (2009) Fission yeast IQGAP arranges actin filaments into the cytokinetic contractile ring. EMBO Journal 28, 3117-31.
139. TAKEMOTO, D. KAMAKURA, S., SAIKIA, S. ET AL. (2011) Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex. Proceedings of the National Academy of Sciences of the United States of America 108, 2861-6.
140. TAKENAWA, T. (2010) Phosphoinositide-binding interface proteins involved in shaping cell membranes. Proceedings of the Japanese Academy, Series B: Physical and Biological Sciences 86, 509-23.
141. TAKENAWA, T. and SUETSUGA, S. (2007) The WASP-WAVE protein network:connecting the membrane to the cytoskeleton. Nature Reviews Molecular Cell Biology 8, 37-48.
142. TANAKA, K., MATSUMOTO, K. and TOH-E, A. (1989) IRA1, an inhibitory regulator of the RAS-cyclic AMP pathway in Saccharomyces cerevisiae. Molecular and Cellular Biology 9, 757-68.
143. TANAKA, K., NAKAFUKU, M., TAMANOI, F. ET AL. (1990) IRA2, a second gene of Saccharomyces cerevisiae that encodes a protein with a domain homologous to mammalian ras GTPase-activating protein. Molecular and Cellular Biology 10, 4303-13.
144. TATEBE, H., NAKANO, K., MAXIMO, R. and SHIOZAKI, K. (2008) Pom1 DYRK regulates localization of the Rga4 GAP to ensure bipolar activation of Cdc42 in fission yeast. Current Biology 18, 322-30.
145. TCHERKEZIAN, J. and LAMARCHE-VANE, N. (2007) Current knowledge of the large RhoGAP family of proteins. Biology of the Cell 99, 67-86
146. TIEDJE, C., SAKWA, I., JUST, U. and HÖFKEN, T. (2008) The Rho GDI Rdi1 regulates Rho GTPases by distinct mechanisms. Molecular Biology of the Cell 19, 2885-96.
147. TISI, R., BELOTTI, F., PAIARDI, C., BRUNETTI, F. and MARTEGANI, E. (2008) The budding yeast RasGEF Cdc25 reveals an unexpected nuclear localization. Biochimica et Biophysica Acta 1783, 2363-74.
148. TRAHEY, M. and MCCORM ICK, F. (1987) A cytoplasmic protein stimulates normal N-ras p21 GTPase, but does not affect oncogenic mutants. Science 238, 542-5.
149. TRATNER, I., FOURTICQ-ESQUEÖUTE, A., TILLIT, J. and BALDACCI, G. (1997) Cloning and characterization of the S. pombe gene efc25+, a new putative guanine nucleotide exchange factor. Gene 193, 203-10.
150. UNO, I., MITSUZAWA, H., MATSUMOTO, K. ET AL. (1985) Reconstitution of the GTP-dependent adenylate cyclase from products of the yeast CYR1 and RAS2 genes in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 82, 7855-59.
151. UNO, I., YAMAGUCHI, M. and ISHIKAWA, T. (1974) The effect of light on fruiting body formation and adenosine 3′, 5′-cyclic monophosphate metabolism in Coprinus macrorhizus. Proceedings of the National Academy of Sciences of the United States of America 71, 479-83.
152. VALLIM, M.A., NICHOLS, C.B., FERNANDES, L, CRAMER, K.L. and ALSPAUGH, J.A. (2005) A Rac homolog functions downstream of Ras1 to control hyphal differentiation and high-temperature growth in the pathogenic fungus Cryptococcus neoformans. Eukaryotic Cell 6,1066-78.
153. VASARA, T., SALOHEIMO, M., KERÄNEN, S. and PENTTILÄ, M. (2001a) Trichoderma reesei rho3 a homologue of yeast RH03 suppresses the growth defect of yeast sec15-1 mutation. Current Genetics 40, 119-27.
154. VASARA, T., SALUSJÄRVI, L., RAUDASKOSKI, M. ET AL. (2001b) Interactions of the Trichoderma reesei rho3 with the secretory pathway in yeast and T. reesei. Molecular Microbiology 42, 1349-61.
155. VEGA, F.M. and RIDLEY, A.J. (2007) SnapShot: Rho Family GTPases. Cell 129, 130.
156. VIGIL, D., CHERFILS, J., ROSSMAN, K.L. and DER, C.J. (2010) Ras superfamily GEFs and GAPs: validated and tractable targets for cancer therapy? Nature Reviews Cancer 10, 842-57.
157. VILLAR-TAJADURA, M.A., COLL, P.M., MADRID, M. ET AL. (2008) Rga2 is a Rho2 GAP that regulates morphogenesis and cell integrity in S. pombe. Molecular Microbiology 70, 867-81.
158. VIRAG, A., LEE, M.P., SI, H. and HARRIS, S.D. (2007) Regulation of hyphal morphogenesis by cdc42 and rac1 homologues in Aspergillus nidulans. Molecular Microbiology 66, 1579-96.
159. VLAHOU, G. and RIVERO, F. (2006) Rho GTPase signaling in Dictyostelium discoideum: insights from the genome. European Journal of Cell Biology 85, 947-59.
160. WANG, T. and BRETSCHER, A. (1995) The rho-GAP encoded by BEM2 regulates cytoskeletal structure in budding yeast. Molecular Biology of the Cell 6, 1011-24.
161. WANG, Y., BOGUSKI, M., RIGGS, M., RODGERS, L. and WIGLER, M. (1991) sar1, a gene from Schizosaccharomyces pombe encoding a protein that regulates ras1. Cell Regulation 2, 453-65.
162. WAUGH, M.S., NICHOLS, C.B., DECESARE, C.M. ET AL. (2002) Ras1 and Ras2 contribute shared and unique roles in physiology and virulence of Cryptococcus neoformans. Microbiology 148, 191-201.
163. WAUGH, M.S., VALLIM, M.A., HEITMAN, J. and ALSPAUGH, J.A. (2003) Ras1 controls pheromone expression and response during mating in Cryptococcus neoformans. Fungal Genetics and Biology 38,110-21.
164. WEBER, M., SALO, V., UUSKALLIO, M., and RAUDASKOSKI, M. (2005) Ectopic expression of a constitutively active Cdc42 small GTPase alters the morphology of haploid and dikaryotic hyphae in the filamentous homobasidiomycete Schizophyllum commune. Fungal Genetics and Biology 42, 624-37.
165. WEI, W., MOSTELLER, R.D., SANYAL, P. ET AL. (1992) Identification of a mammalian gene structurally and functionally related to the CDC25 gene of Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America 89, 7100-4.
166. WORTHYLAKE. D.K., ROSSMAN, K.L. and SONDEK, J. (2000) Crystal structure of Rac1 in complex with the guanine nucleotide exchange region of Tiam1. Nature 408, 682-8.
167. WU, H., ROSSI, G. and BRENNWALD, P. (2008) The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends in Cell Biology 18, 397-404.
168. YAMAGISHI, K., KIMURA, T., SUZUKI, M., SHINMOTO, H. and YAMAKI, K.J. (2004) Elevation of intracellular cAMP levels by dominant active heterotrimeric G protein alpha subunits ScGP-A and ScGP-C in homobasidiomycete, Schizophyllum commune. Bioscience, Biotechnology and Biochemistry 68, 1017-26.
169. YAMAGUCHI, Y., OTA, K. and ITO, T. (2007) A novel Cdc42-interacting domain of the yeast polarity establishment protein Bem1. Implications for modulation of mating pheromone signaling. Journal of Biological Chemistry 282, 29-38.
170. YOUNG, K.G. and COPELAND, J.W. (2010) Formins in cell signaling. Biochimica et Biophysica Acta 1803, 183-90.
171. ZAMAN, S., LIPPMAN, S.I., ZHAO, X. and BROACH, J.R. (2008) How Saccharomyces responds to nutrients. Annual Review of Genetics 42, 27-81.
172. ZHENG, Y., CERIONE, R. and BENDER, A. (1994) Control of the yeast bud-site assembly GTPase Cdc42. Catalysis of guanine nucleotide exchange by Cdc24 and stimulation of GTPase activity by Bem3. Journal of Biological Chemistry 269, 2369-72.