Role of the cell wall integrity and filamentous growth mitogen-activated protein kinase pathways in cell wall remodeling during filamentous growth

Eukaryotic Cell

Volumn 8, Issue 8, 2009, Pages 1118-1133

  Birkaya, Barbara ^a   Maddi, Abhiram ^a   Joshi, Jyoti ^a   Free, Stephen J ^a   Cullen, Paul J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL WALL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

CELL WALL; GENE EXPRESSION REGULATION, FUNGAL; MITOGEN-ACTIVATED PROTEIN KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 68549111110     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00006-09     Document Type: Article

References (173)

1. Alberts, A. S., N. Bouquin, L. H. Johnston, and R. Treisman. 1998. Analysis of RhoA-binding proteins reveals an interaction domain conserved in heterotrimeric G protein beta subunits and the yeast response regulator protein Skn7. J. Biol. Chem. 273:8616-8622.
2. Amberg, D. C. 2000. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. Andrews, B. J., and I. Herskowitz. 1989. The yeast SWI4 protein contains a motif present in developmental regulators and is part of a complex involved in cell-cycle-dependent transcription. Nature 342:830-833.
4. Atha, D. H., and Ingham, K. C. 1981. Mechanism of precipitation of proteins by polyethylene glycols. Analysis in terms of excluded volume. J. Biol. Chem. 256:12108-12117.
5. Baetz, K., J. Moffat, J. Haynes, M. Chang, and B. Andrews. 2001. Tran-scriptional coregulation by the cell integrity mitogen-activated protein kinase Slt2 and the cell cycle regulator Swi4. Mol. Cell. Biol. 21:6515-6528.
6. Bardwell, L. 2006. Mechanisms of MAPK signalling specificity. Biochem. Soc. Trans. 34:837-841.
7. Baudin, A., O. Ozier-Kalogeropoulos, A. Denouel, F. Lacroute, and C. Cullin. 1993. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 21:3329-3330.
8. Bean, J. M., E. D. Siggia, and F. R. Cross. 2005. High functional overlap between MluI cell-cycle box binding factor and Swi4/6 cell-cycle box binding factor in the G1/S transcriptional program in Saccharomyces cerevisiae. Genetics 171: 49-61.
9. Bermejo, C., E. Rodriguez, R. Garcia, J. M. Rodriguez-Pena, M. L. Rodriguez de la Concepcion, C. Rivas, P. Arias, C. Nombela, F. Posas, and J. Arroyo. 2008. The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol. Biol. Cell 19:1113-1124.
10. Borneman, A. R., T. A. Gianoulis, Z. D. Zhang, H. Yu, J. Rozowsky, M. R. Seringhaus, L. Y. Wang, M. Gerstein, and M. Snyder. 2007. Divergence of transcription factor binding sites across related yeast species. Science 317: 815-819.
11. Bowman, S. M., A. Piwowar, M. Al Dabbous, J. Vierula, and S. J. Free. 2006. Mutational analysis of the glycosylphosphatidylinositol (GPI) anchor pathway demonstrates that GPI-anchored proteins are required for cell wall biogenesis and normal hyphal growth in Neurospora crassa. Eukaryot. Cell 5:587-600.
12. Brewster, J. L., T. de Valoir, N. D. Dwyer, E. Winter, and M. C. Gustin. 1993. An osmosensing signal transduction pathway in yeast. Science 259: 1760-1763.
13. Brown, J. L., and H. Bussey. 1993. The yeast KRE9 gene encodes an O glycoprotein involved in cell surface beta-glucan assembly. Mol. Cell. Biol. 13:6346-6356.
14. Bruhn, L., J. J. Hwang-Shum, and G. F. Sprague, Jr. 1992. The N-terminal 96 residues of MCM1, a regulator of cell type-specific genes in Saccharo-myces cerevisiae, are sufficient for DNA binding, transcription activation, and interaction with alpha 1. Mol. Cell. Biol. 12:3563-3572.
15. Buehrer, B. M., and B. Errede. 1997. Coordination of the mating and cell integrity mitogen-activated protein kinase pathways in Saccharomyces cer-evisiae. Mol. Cell. Biol. 17:6517-6525.
16. Calcagno, A. M., E. Bignell, T. R. Rogers, M. Canedo, F. A. Muhlschlegel, and K. Haynes. 2004. Candida glabrata Ste20 is involved in maintaining cell wall integrity and adaptation to hypertonic stress, and is required for wildtype levels of virulence. Yeast 21:557-568.
17. Cappellaro, C., V. Mrsa, and W. Tanner. 1998. New potential cell wall glucanases of Saccharomyces cerevisiae and their involvement in mating. J. Bacteriol. 180:5030-5037.
18. Carlson, M., and D. Botstein. 1982. Two differentially regulated mRNAs with different 5′ ends encode secreted with intracellular forms of yeast invertase. Cell 28:145-154.
19. Caro, L. H., G. J. Smits, P. van Egmond, J. W. Chapman, and F. M. Klis. 1998. Transcription of multiple cell wall protein-encoding genes in Saccharomyces cerevisiae is differentially regulated during the cell cycle. FEMS Microbiol. Lett. 161:345-349.
20. Caro, L. H., H. Tettelin, J. H. Vossen, A. F. Ram, H. van den Ende, and F. M. Klis. 1997. In silicio identification of glycosyl- phosphatidylinositolanchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13:1477-1489.
21. Carraway, K. L., V. P. Ramsauer, B. Haq, and C. A. Carothers Carraway. 2003. Cell signaling through membrane mucins. Bioessays 25:66-71.
22. Chaffin, W. L. 2008. Candida albicans cell wall proteins. Microbiol. Mol. Biol. Rev. 72:495-544.
23. Chang, V. K., M. J. Fitch, J. J. Donato, T. W. Christensen, A. M. Merchant, and B. K. Tye. 2003. Mcm1 binds replication origins. J. Biol. Chem. 278: 6093-6100.
24. Changwei, Z., X. Mingyong, and W. Ranran. 2007. Afr1p has a role in regulating the localization of Mpk1p at the shmoo tip in Saccharomyces cerevisiae. FEBS Lett. 581:2670-2674.
25. Chant, J., K. Corrado, J. R. Pringle, and I. Herskowitz. 1991. Yeast BUD5, encoding a putative GDP-GTP exchange factor, is necessary for bud site selection and interacts with bud formation gene BEM1. Cell 65:1213-1224.
26. Chant, J., and I. Herskowitz. 1991. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 65:1203-1212.
27. Chant, J., and J. R. Pringle. 1995. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J. Cell Biol. 129:751-765.
28. Cherry, J. M., C. Adler, C. Ball, S. A. Chervitz, S. S. Dwight, E. T. Hester, Y. Jia, G. Juvik, T. Roe, M. Schroeder, S. Weng, and D. Botstein. 1998. SGD: Saccharomyces genome database. Nucleic Acids Res. 26:73-79.
29. Cullen, P. J., W. Sabbagh, Jr., E. Graham, M. M. Irick, E. K. van Olden, C. Neal, J. Delrow, L. Bardwell, and G. F. Sprague, Jr. 2004. A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev. 18:1695-1708.
30. Cullen, P. J., J. Schultz, J. Horecka, B. J. Stevenson, Y. Jigami, and G. F. Sprague, Jr. 2000. Defects in protein glycosylation cause SHO1-dependent activation of a STE12 signaling pathway in yeast. Genetics 155:1005-1018.
31. Cullen, P. J., and G. F. Sprague, Jr. 2000. Glucose depletion causes haploid invasive growth in yeast. Proc. Natl. Acad. Sci. USA 97:13619-13624.
32. Cullen, P. J., and G. F. Sprague, Jr. 2002. The roles of bud-site-selection proteins during haploid invasive growth in yeast. Mol. Biol. Cell 13:2990-3004.
33. Cutler, N. S., X. Pan, J. Heitman, and M. E. Cardenas. 2001. The TOR signal transduction cascade controls cellular differentiation in response to nutrients. Mol. Biol. Cell 12:4103-4113.
34. Davenport, K. D., K. E. Williams, B. D. Ullmann, and M. C. Gustin. 1999. Activation of the Saccharomyces cerevisiae filamentation/invasion pathway by osmotic stress in high-osmolarity glycogen pathway mutants. Genetics 153:1091-1103.
35. Day, B., and T. Graham. 2007. The plant host pathogen interface: cell wall and membrane dynamics of pathogen-induced responses. Ann. N. Y. Acad. Sci. 1113:123-134.
36. de Godoy, L. M., J. V. Olsen, J. Cox, M. L. Nielsen, N. C. Hubner, F. Frohlich, T. C. Walther, and M. Mann. 2008. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455:1251-1254.
37. de Nobel, J. G., F. M. Klis, J. Priem, T. Munnik, and H. van den Ende. 1990. The glucanase-soluble mannoproteins limit cell wall porosity in Saccharomyces cerevisiae. Yeast 6:491-499.
38. Eisman, B., R. Alonso-Monge, E. Roman, D. Arana, C. Nombela, and J. Pla. 2006. The Cek1 and Hog1 mitogen-activated protein kinases play complementary roles in cell wall biogenesis and chlamydospore formation in the fungal pathogen Candida albicans. Eukaryot. Cell 5:347-358.
39. El Bakkoury, M., E. Dubois, and F. Messenguy. 2000. Recruitment of the yeast MADS-box proteins, ArgRI and Mcm1 by the pleiotropic factor ArgRIII is required for their stability. Mol. Microbiol. 35:15-31.
40. Gagnon-Arsenault, I., L. Parise, J. Tremblay, and Y. Bourbonnais. 2008. Activation mechanism, functional role and shedding of glycosylphosphatidylinositol-anchored Yps1p at the Saccharomyces cerevisiae cell surface. Mol. Microbiol. 69:982-993.
41. Galgoczy, D. J., A. Cassidy-Stone, M. Llinas, S. M. O'Rourke, I. Herskowitz, J. L. DeRisi, and A. D. Johnson. 2004. Genomic dissection of the cell-type-specification circuit in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101:18069-18074.
42. Garcia, R., J. M. Rodriguez-Pena, C. Bermejo, C. Nombela, and J. Arroyo. 2009. The high osmotic response and cell wall integrity pathways cooperate to regulate transcriptional responses to zymolyase-induced cell wall stress in Saccharomyces cerevisiae. J. Biol. Chem. 284:10901- 10911.
43. Garcia-Rodriguez, L. J., A. Duran, and C. Roncero. 2000. Calcofluor antifungal action depends on chitin and a functional high-osmolarity glycerol response (HOG) pathway: evidence for a physiological role of the Saccharomyces cerevisiae HOG pathway under noninducing conditions. J. Bacteriol. 182:2428-2437.
44. Garcia-Rodriguez, L. J., R. Valle, A. Duran, and C. Roncero. 2005. Cell integrity signaling activation in response to hyperosmotic shock in yeast. FEBS Lett. 579:6186-6190.
45. Gelperin, D. M., M. A. White, M. L. Wilkinson, Y. Kon, L. A. Kung, K. J. Wise, N. Lopez-Hoyo, L. Jiang, S. Piccirillo, H. Yu, M. Gerstein, M. E. Dumont, E. M. Phizicky, M. Snyder, and E. J. Grayhack. 2005. Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev. 19:2816-2826.
46. Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles, S. Veronneau, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
47. Gimeno, C. J., and G. R. Fink. 1994. Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol. Cell. Biol. 14:2100-2112.
48. Gimeno, C. J., and G. R. Fink. 1992. The logic of cell division in the life cycle of yeast. Science 257:626.
49. Gimeno, C. J., P. O. Ljungdahl, C. A. Styles, and G. R. Fink. 1992. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68:1077-1090.
50. Goldstein, A. L., and J. H. McCusker. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15:1541-1553.
51. Guo, B., C. A. Styles, Q. Feng, and G. R. Fink. 2000. A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc. Natl. Acad. Sci. USA 97:12158-12163.
52. Hagen, I., M. Ecker, A. Lagorce, J. M. Francois, S. Sestak, R. Rachel, G. Grossmann, N. C. Hauser, J. D. Hoheisel, W. Tanner, and S. Strahl. 2004. Sed1p and Srl1p are required to compensate for cell wall instability in Saccharomyces cerevisiae mutants defective in multiple GPI-anchored mannoproteins. Mol. Microbiol. 52:1413-1425.
53. Halme, A., S. Bumgarner, C. Styles, and G. R. Fink. 2004. Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell 116:405-415.
54. Hamada, K., S. Fukuchi, M. Arisawa, M. Baba, and K. Kitada. 1998. Screening for glycosylphosphatidylinositol (GPI)-dependent cell wall proteins in Saccharomyces cerevisiae. Mol. Gen. Genet. 258:53-59.
55. Hawle, P., D. Horst, J. P. Bebelman, X. X. Yang, M. Siderius, and S. M. van der Vies. 2007. Cdc37p is required for stress-induced high-osmolarity glycerol and protein kinase C mitogen-activated protein kinase pathway functionality by interaction with Hog1p and Slt2p (Mpk1p). Eukaryot. Cell 6:521-532.
56. Hedbacker, K., and M. Carlson. 2008. SNF1/AMPK pathways in yeast. Front. Biosci. 13:2408-2420.
57. Hoang, A. 2001. Caspofungin acetate: an antifungal agent. Am. J. Health Syst. Pharm. 58:1206-1217.
58. Hong, E. L., R. Balakrishnan, Q. Dong, K. R. Christie, J. Park, G. Binkley, M. C. Costanzo, S. S. Dwight, S. R. Engel, D. G. Fisk, J. E. Hirschman, B. C. Hitz, C. J. Krieger, M. S. Livstone, S. R. Miyasato, R. S. Nash, R. Oughtred, M. S. Skrzypek, S. Weng, E. D. Wong, K. K. Zhu, K. Dolinski, D. Botstein, and J. M. Cherry. 2008. Gene Ontology annotations at SGD: new data sources and annotation methods. Nucleic Acids Res. 36:D577D581.
59. Hwang-Shum, J. J., D. C. Hagen, E. E. Jarvis, C. A. Westby, and G. F. Sprague, Jr. 1991. Relative contributions of MCM1 and STE12 to transcriptional activation of aand alpha-specific genes from Saccharomyces cerevisiae. Mol. Gen. Genet. 227:197-204.
60. Jarvis, E. E., K. L. Clark, and G. F. Sprague, Jr. 1989. The yeast transcription activator PRTF, a homolog of the mammalian serum response factor, is encoded by the MCM1 gene. Genes Dev. 3:936-945.
61. Jiang, B., A. F. Ram, J. Sheraton, F. M. Klis, and H. Bussey. 1995. Regulation of cell wall beta-glucan assembly: PTC1 negatively affects PBS2 action in a pathway that includes modulation of EXG1 transcription. Mol. Gen. Genet. 248:260-269.
62. Jin, R., C. J. Dobry, P. J. McCown, and A. Kumar. 2008. Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Mol. Biol. Cell 19:284-296.
63. Johnson, D. I. 1999. Cdc42: an essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol. Mol. Biol. Rev. 63:54-105.
64. Jung, U. S., and D. E. Levin. 1999. Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol. Microbiol. 34:1049-1057.
65. Kaeberlein, M., and L. Guarente. 2002. Saccharomyces cerevisiae MPT5 and SSD1 function in parallel pathways to promote cell wall integrity. Genetics 160:83-95.
66. Kapteyn, J. C., R. C. Montijn, E. Vink, J. de la Cruz, A. Llobell, J. E. Douwes, H. Shimoi, P. N. Lipke, and F. M. Klis. 1996. Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked beta-1,3-/beta-1,6-glucan heteropolymer. Glycobiology 6:337-345.
67. Klebl, F., and W. Tanner. 1989. Molecular cloning of a cell wall exo-beta-1,3-glucanase from Saccharomyces cerevisiae. J. Bacteriol. 171:6259-6264.
68. Klis, F. M., A. Boorsma, and P. W. De Groot. 2006. Cell wall construction in Saccharomyces cerevisiae. Yeast 23:185-202.
69. Kollar, R., B. B. Reinhold, E. Petrakova, H. J. Yeh, G. Ashwell, J. Drgonova, J. C. Kapteyn, F. M. Klis, and E. Cabib. 1997. Architecture of the yeast cell wall. Beta(136)-glucan interconnects mannoprotein, beta(13)3-glucan, and chitin. J. Biol. Chem. 272:17762-17775.
70. Krause, S. A., and J. V. Gray. 2002. The protein kinase C pathway is required for viability in quiescence in Saccharomyces cerevisiae. Curr. Biol. 12:588-593.
71. Krisak, L., R. Strich, R. S. Winters, J. P. Hall, M. J. Mallory, D. Kreitzer, R. S. Tuan, and E. Winter. 1994. SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev. 8:2151-2161.
72. Kron, S. J., C. A. Styles, and G. R. Fink. 1994. Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 5:1003-1022.
73. Krysan, D. J., and L. Didone. 2008. A high-throughput screening assay for small molecules that disrupt yeast cell integrity. J. Biomol. Screen. 13:657-664.
74. Kuchin, S., V. K. Vyas, and M. Carlson. 2003. Role of the yeast Snf1 protein kinase in invasive growth. Biochem. Soc. Trans. 31:175-177.
75. Kuchin, S., V. K. Vyas, and M. Carlson. 2002. Snf1 protein kinase and the repressors Nrg1 and Nrg2 regulate FLO11, haploid invasive growth, and diploid pseudohyphal differentiation. Mol. Cell. Biol. 22:3994-4000.
76. Kumamoto, C. A. 2005. A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc. Natl. Acad. Sci. USA 102: 5576-5581.
77. Latge, J. P. 2007. The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 66:279-290.
78. Leberer, E., C. Wu, T. Leeuw, A. Fourest-Lieuvin, J. E. Segall, and D. Y. Thomas. 1997. Functional characterization of the Cdc42p binding domain of yeast Ste20p protein kinase. EMBO J. 16:83-97.
79. Lee, K. S., K. Irie, Y. Gotoh, Y. Watanabe, H. Araki, E. Nishida, K. Matsumoto, and D. E. Levin. 1993. A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol. Cell. Biol. 13:3067-3075.
80. Lesage, G., and H. Bussey. 2006. Cell wall assembly in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70:317-343.
81. Lesage, G., A. M. Sdicu, P. Menard, J. Shapiro, S. Hussein, and H. Bussey. 2004. Analysis of beta-1,3-glucan assembly in Saccharomyces cerevisiae using a synthetic interaction network and altered sensitivity to caspofungin. Genetics 167:35-49.
82. Levin, D. E. 2005. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69:262-291.
83. Levin, D. E., B. Bowers, C. Y. Chen, Y. Kamada, and M. Watanabe. 1994. Dissecting the protein kinase C/MAP kinase signalling pathway of Saccharomyces cerevisiae. Cell Mol. Biol. Res. 40:229-239.
84. Liu, H., C. A. Styles, and G. R. Fink. 1993. Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262:1741-1744.
85. Lo, H. J., J. R. Kohler, B. DiDomenico, D. Loebenberg, A. Cacciapuoti, and G. R. Fink. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90:939-949.
86. Lo, W. S., and A. M. Dranginis. 1998. The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol. Biol. Cell 9:161-171.
87. Lo, W. S., E. I. Raitses, and A. M. Dranginis. 1997. Development of pseudohyphae by embedded haploid and diploid yeast. Curr. Genet. 32: 197-202.
88. Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
89. Lopez-Villar, E., L. Monteoliva, M. R. Larsen, E. Sachon, M. Shabaz, M. Pardo, J. Pla, C. Gil, P. Roepstorff, and C. Nombela. 2006. Genetic and proteomic evidences support the localization of yeast enolase in the cell surface. Proteomics 6(Suppl. 1):S107-S118.
90. Lorenz, M. C., N. S. Cutler, and J. Heitman. 2000. Characterization of alcohol-induced filamentous growth in Saccharomyces cerevisiae. Mol. Biol. Cell 11:183-199.
91. Lorenz, M. C., and J. Heitman. 1998. Regulators of pseudohyphal differentiation in Saccharomyces cerevisiae identified through multicopy suppressor analysis in ammonium permease mutant strains. Genetics 150:1443-1457.
92. Madhani, H. D., and G. R. Fink. 1997. Combinatorial control required for the specificity of yeast MAPK signaling. Science 275:1314-1317.
93. Madhani, H. D., C. A. Styles, and G. R. Fink. 1997. MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation. Cell 91:673-684.
94. Maeda, T., M. Takekawa, and H. Saito. 1995. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269:554-558.
95. Maerz, S., C. Ziv, N. Vogt, K. Helmstaedt, N. Cohen, R. Gorovits, O. Yarden, and S. Seiler. 2008. The nuclear Dbf2-related kinase COT1 and the mitogen-activated protein kinases MAK1 and MAK2 genetically interact to regulate filamentous growth, hyphal fusion and sexual development in Neurospora crassa. Genetics 179:1313-1325.
96. Martineau, C. N., J. M. Beckerich, and M. Kabani. 2007. Flo11p-independent control of "mat" formation by hsp70 molecular chaperones and nucleotide exchange factors in yeast. Genetics 177:1679-1689.
97. McCaffrey, G., F. J. Clay, K. Kelsay, and G. F. Sprague, Jr. 1987. Identification and regulation of a gene required for cell fusion during mating of the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 7:2680-2690.
98. Morohashi, N., K. Nakajima, D. Kurihara, Y. Mukai, A. P. Mitchell, and M. Shimizu. 2007. A nucleosome positioned by alpha2/Mcm1 prevents HapI activator binding in vivo. Biochem. Biophys. Res. Commun. 364:583-588.
99. Mosch, H. U., and G. R. Fink. 1997. Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. Genetics 145:671-684.
100. Mosch, H. U., E. Kubler, S. Krappmann, G. R. Fink, and G. H. Braus. 1999. Crosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae. Mol. Biol. Cell 10:1325-1335.
101. Mosch, H. U., R. L. Roberts, and G. R. Fink. 1996. Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93: 5352-5356.
102. Moukadiri, I., L. Jaafar, and J. Zueco. 1999. Identification of two mannoproteins released from cell walls of a Saccharomyces cerevisiae mnn1 mnn9 double mutant by reducing agents. J. Bacteriol. 181:4741-4745.
103. Mrsa, V., M. Ecker, S. Strahl-Bolsinger, M. Nimtz, L. Lehle, and W. Tanner. 1999. Deletion of new covalently linked cell wall glycoproteins alters the electrophoretic mobility of phosphorylated wall components of Saccharomyces cerevisiae. J. Bacteriol. 181:3076-3086.
104. Nasmyth, K., and L. Dirick. 1991. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell 66:995-1013.
105. Nather, K., and C. A. Munro. 2008. Generating cell surface diversity in Candida albicans and other fungal pathogens. FEMS Microbiol. Lett. 285: 137-145.
106. Navarro-Garcia, F., R. Alonso-Monge, H. Rico, J. Pla, R. Sentandreu, and C. Nombela. 1998. A role for the MAP kinase gene MKC1 in cell wall construction and morphological transitions in Candida albicans. Microbiology 144:411-424.
107. Nimrichter, L., M. L. Rodrigues, E. G. Rodrigues, and L. R. Travassos. 2005. The multitude of targets for the immune system and drug therapy in the fungal cell wall. Microbes Infect. 7:789-798.
108. Nobile, C. J., and A. P. Mitchell. 2006. Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol. 8:1382-1391.
109. O'Rourke, S. M., I. Herskowitz, and E. K. O'Shea. 2002. Yeast go the whole HOG for the hyperosmotic response. Trends Genet. 18:405-412.
110. Oehlen, L. J., J. D. McKinney, and F. R. Cross. 1996. Ste12 and Mcm1 regulate cell cycle-dependent transcription of FAR1. Mol. Cell. Biol. 16: 2830-2837.
111. Ono, T., T. Suzuki, Y. Anraku, and H. Iida. 1994. The MID2 gene encodes a putative integral membrane protein with a Ca(2+)-binding domain and shows mating pheromone-stimulated expression in Saccharomyces cerevisiae. Gene 151:203-208.
112. Orlean, P. 1997. Biogenesis of yeast wall and surface components, p. 229-362. In J. R. Pringle, J. R. Broach, and E. W. Jones (ed.), The molecular and cellular biology of the yeast Saccharomyces. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
113. Orlean, P., H. Ammer, M. Watzele, and W. Tanner. 1986. Synthesis of an O-glycosylated cell surface protein induced in yeast by alpha factor. Proc. Natl. Acad. Sci. USA 83:6263-6266.
114. Palecek, S. P., A. S. Parikh, and S. J. Kron. 2000. Genetic analysis reveals that FLO11 upregulation and cell polarization independently regulate invasive growth in Saccharomyces cerevisiae. Genetics 156:1005-1023.
115. Pan, X., and J. Heitman. 2000. Sok2 regulates yeast pseudohyphal differentiation via a transcription factor cascade that regulates cell-cell adhesion. Mol. Cell. Biol. 20:8364-8372.
116. Pardo, M., M. Ward, S. Bains, M. Molina, W. Blackstock, C. Gil, and C. Nombela. 2000. A proteomic approach for the study of Saccharomyces cerevisiae cell wall biogenesis. Electrophoresis 21:3396-3410.
117. Park, H. O., and E. Bi. 2007. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 71:48-96.
118. Pesheva, M. G., M. K. Koprinarova, and P. Venkov. 2006. Enhanced protein export in Saccharomyces cerevisiae nud1 mutants is an active process. Curr. Microbiol. 53:496-501.
119. Peter, M., A. M. Neiman, H. O. Park, M. van Lohuizen, and I. Herskowitz. 1996. Functional analysis of the interaction between the small GTP binding protein Cdc42 and the Ste20 protein kinase in yeast. EMBO J. 15:7046-7059.
120. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
121. Pitoniak, A., B. Birkaya, H. S. Dionne, N. Vadiae, and P. J. Cullen. 13 May 2009, posting date. The signaling mucins Msb2 and Hkr1 differentially regulate the filamentation MAPK pathway and contribute to a multimodal response. Mol. Biol. Cell. doi:10.1091/mbc.E08-07-0760.
122. Posas, F., J. R. Chambers, J. A. Heyman, J. P. Hoeffler, E. de Nadal, and J. Arino. 2000. The transcriptional response of yeast to saline stress. J. Biol. Chem. 275:17249-17255.
123. Posas, F., and H. Saito. 1997. Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276:1702-1705.
124. Ragni, E., M. Sipiczki, and S. Strahl. 2007. Characterization of Ccw12p, a major key player in cell wall stability of Saccharomyces cerevisiae. Yeast 24:309-319.
125. Raitt, D. C., F. Posas, and H. Saito. 2000. Yeast Cdc42 GTPase and Ste20 PAK-like kinase regulate Sho1-dependent activation of the Hog1 MAPK pathway. EMBO J. 19:4623-4631.
126. Rajavel, M., B. Philip, B. M. Buehrer, B. Errede, and D. E. Levin. 1999. Mid2 is a putative sensor for cell integrity signaling in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:3969-3976.
127. Ramer, S. W., S. J. Elledge, and R. W. Davis. 1992. Dominant genetics using a yeast genomic library under the control of a strong inducible promoter. Proc. Natl. Acad. Sci. USA 89:11589-11593.
128. Reck-Peterson, S. L., P. J. Novick, and M. S. Mooseker. 1999. The tail of a yeast class V myosin, myo2p, functions as a localization domain. Mol. Biol. Cell 10:1001-1017.
129. Reiser, V., S. M. Salah, and G. Ammerer. 2000. Polarized localization of yeast Pbs2 depends on osmostress, the membrane protein Sho1 and Cdc42. Nat. Cell Biol. 2:620-627.
130. Reynolds, T. B., A. Jansen, X. Peng, and G. R. Fink. 2008. Mat formation in Saccharomyces cerevisiae requires nutrient and pH gradients. Eukaryot. Cell 7:122-130.
131. Rine, J., and I. Herskowitz. 1987. Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics 116:9-22.
132. Roberts, C. J., B. Nelson, M. J. Marton, R. Stoughton, M. R. Meyer, H. A. Bennett, Y. D. He, H. Dai, W. L. Walker, T. R. Hughes, M. Tyers, C. Boone, and S. H. Friend. 2000. Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles. Science 287:873-880.
133. Roberts, R. L., and G. R. Fink. 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 Dev. 8:2974-2985.
134. Rohde, J. R., and M. E. Cardenas. 2004. Nutrient signaling through TOR kinases controls gene expression and cellular differentiation in fungi. Curr. Top. Microbiol. Immunol. 279:53-72.
135. Roman, E., C. Nombela, and J. Pla. 2005. The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candida albicans. Mol. Cell. Biol. 25:10611-10627.
136. Ronen, R., H. Sharon, E. Levdansky, J. Romano, Y. Shadkchan, and N. Osherov. 2007. The Aspergillus nidulans pkcA gene is involved in polarized growth, morphogenesis and maintenance of cell wall integrity. Curr. Genet. 51:321-329.
137. Rose, M. D., P. Novick, J. H. Thomas, D. Botstein, and G. R. Fink. 1987. A Saccharomyces cerevisiae genomic plasmid bank based on a centromerecontaining shuttle vector. Gene 60:237-243.
138. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
139. Rua, D., B. T. Tobe, and S. J. Kron. 2001. Cell cycle control of yeast filamentous growth. Curr. Opin. Microbiol. 4:720-727.
140. Rupp, S., E. Summers, H. J. Lo, H. Madhani, and G. Fink. 1999. MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J. 18:1257-1269.
141. Russo, P., N. Kalkkinen, H. Sareneva, J. Paakkola, and M. Makarow. 1992. A heat shock gene from Saccharomyces cerevisiae encoding a secretory glycoprotein. Proc. Natl. Acad. Sci. USA 89:3671-3675.
142. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
143. Schneider, B. L., W. Seufert, B. Steiner, Q. H. Yang, and A. B. Futcher. 1995. Use of polymerase chain reaction epitope tagging for protein tagging in Saccharomyces cerevisiae. Yeast 11:1265-1274.
144. Sciorra, V. A., A. Audhya, A. B. Parsons, N. Segev, C. Boone, and S. D. Emr. 2005. Synthetic genetic array analysis of the PtdIns 4-kinase Pik1p identifies
145. Shimada, Y., P. Wiget, M. P. Gulli, E. Bi, and M. Peter. 2004. The nucleotide exchange factor Cdc24p may be regulated by auto-inhibition. EMBO J. 23:1051-1062.
146. Shitamukai, A., D. Hirata, S. Sonobe, and T. Miyakawa. 2004. Evidence for antagonistic regulation of cell growth by the calcineurin and high osmolarity glycerol pathways in Saccharomyces cerevisiae. J. Biol. Chem. 279:3651-3661.
147. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
148. Singh, P. K., and M. A. Hollingsworth. 2006. Cell surface-associated mucins in signal transduction. Trends Cell Biol. 16:467-476.
149. Smits, G. J., L. R. Schenkman, S. Brul, J. R. Pringle, and F. M. Klis. 2006. Role of cell cycle-regulated expression in the localized incorporation of cell wall proteins in yeast. Mol. Biol. Cell 17:3267-3280.
150. Smits, G. J., H. van den Ende, and F. M. Klis. 2001. Differential regulation of cell wall biogenesis during growth and development in yeast. Microbiology 147:781-794.
151. Sohn, K., J. Schwenk, C. Urban, J. Lechner, M. Schweikert, and S. Rupp. 2006. Getting in touch with Candida albicans: the cell wall of a fungal pathogen. Curr. Drug Targets 7:505-512.
152. Spellman, P. T., G. Sherlock, M. Q. Zhang, V. R. Iyer, K. Anders, M. B. Eisen, P. O. Brown, D. Botstein, and B. Futcher. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9:3273-3297.
153. Tan, S., Y. Hunziker, L. Pellegrini, and T. J. Richmond. 2000. Crystallization of the yeast MATalpha2/MCM1/DNA ternary complex: general methods and principles for protein/DNA cocrystallization. J. Mol. Biol. 297:947-959.
154. Tatebayashi, K., K. Tanaka, H. Y. Yang, K. Yamamoto, Y. Matsushita, T. Tomida, M. Imai, and H. Saito. 2007. Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J. 25:3521-3533.
155. Toh-e, A., S. Yasunaga, H. Nisogi, K. Tanaka, T. Oguchi, and Y. Matsui. 1993. Three yeast genes, PIR1, PIR2 and PIR3, containing internal tandem repeats, are related to each other, and PIR1 and PIR2 are required for tolerance to heat shock. Yeast 9:481-494.
156. Torres, J., C. J. Di Como, E. Herrero, and M. A. De La Torre-Ruiz. 2002. Regulation of the cell integrity pathway by rapamycin-sensitive TOR function in budding yeast. J. Biol. Chem. 277:43495-43504.
157. Vadaie, N., H. Dionne, D. S. Akajagbor, S. R. Nickerson, D. J. Krysan, and P. J. Cullen. 2008. Cleavage of the signaling mucin Msb2 by the aspartyl protease Yps1 is required for MAPK activation in yeast. J. Cell Biol. 181:1073-1081.
158. Vazquez de Aldana, C. R., J. Correa, P. San Segundo, A. Bueno, A. R. Nebreda, E. Mendez, and F. del Rey. 1991. Nucleotide sequence of the exo-1,3-beta-glucanase-encoding gene, EXG1, of the yeast Saccharomyces cerevisiae. Gene 97:173-182.
159. Verna, J., A. Lodder, K. Lee, A. Vagts, and R. Ballester. 1997. A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94:13804-13809.
160. Verstrepen, K. J., and F. M. Klis. 2006. Flocculation, adhesion and biofilm formation in yeasts. Mol. Microbiol. 60:5-15.
161. Vinod, P. K., N. Sengupta, P. J. Bhat, and K. V. Venkatesh. 2008. Integration of global signaling pathways, cAMP-PKA, MAPK and TOR in the regulation of FLO11. PLoS ONE 3:e1663.
162. Voynov, V., K. J. Verstrepen, A. Jansen, V. M. Runner, S. Buratowski, and G. R. Fink. 2006. Genes with internal repeats require the THO complex for transcription. Proc. Natl. Acad. Sci. USA 103:14423-14428.
163. Wendland, J. 2001. Comparison of morphogenetic networks of filamentous fungi and yeast. Fungal Genet. Biol. 34:63-82.
164. Westfall, P. J., and J. Thorner. 2006. Analysis of mitogen-activated protein kinase signaling specificity in response to hyperosmotic stress: use of an analog-sensitive HOG1 allele. Eukaryot. Cell 5:1215-1228.
165. Whiteway, M., and C. Bachewich. 2007. Morphogenesis in Candida albicans. Annu. Rev. Microbiol. 61:529-553.
166. Winzeler, E. A., D. D. Shoemaker, A. Astromoff, H. Liang, K. Anderson, B. Andre, R. Bangham, R. Benito, J. D. Boeke, H. Bussey, A. M. Chu, C. Connelly, K. Davis, F. Dietrich, S. W. Dow, M. El Bakkoury, F. Foury, S. H. Friend, E. Gentalen, G. Giaever, J. H. Hegemann, T. Jones, M. Laub, H. Liao, N. Liebundguth, D. J. Lockhart, A. Lucau-Danila, M. Lussier, N. M'Rabet, P. Menard, M. Mittmann, C. Pai, C. Rebischung, J. L. Revuelta, L. Riles, C. J. Roberts, P. Ross-MacDonald, B. Scherens, M. Snyder, S. Sookhai-Mahadeo, R. K. Storms, S. Veronneau, M. Voet, G. Volckaert, T. R. Ward, R. Wysocki, G. S. Yen, K. Yu, K. Zimmermann, P. Philippsen, M. Johnston, and R. W. Davis. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901-906.
167. Yashar, B., K. Irie, J. A. Printen, B. J. Stevenson, G. F. Sprague, Jr., K. Matsumoto, and B. Errede. 1995. Yeast MEK-dependent signal transduction: response thresholds and parameters affecting fidelity. Mol. Cell. Biol. 15:6545-6553.
168. Yin, Q. Y., P. W. de Groot, C. G. de Koster, and F. M. Klis. 2008. Mass spectrometry-based proteomics of fungal wall glycoproteins. Trends Microbiol. 16:20-26.
169. Yin, Q. Y., P. W. de Groot, H. L. Dekker, L. de Jong, F. M. Klis, and C. G. de Koster. 2005. Comprehensive proteomic analysis of Saccharomyces cerevisiae cell walls: identification of proteins covalently attached via glycosylphosphatidylinositol remnants or mild alkali-sensitive linkages. J. Biol. Chem. 280:20894-20901.
170. Zarzov, P., C. Mazzoni, and C. Mann. 1996. The SLT2(MPK1) MAP kinase is activated during periods of polarized cell growth in yeast. EMBO J. 15:83-91.
171. Zhang, M., D. Bennett, and S. E. Erdman. 2002. Maintenance of mating cell integrity requires the adhesin Fig2p. Eukaryot. Cell 1:811-822.
172. Zhao, X., R. Mehrabi, and J. R. Xu. 2007. Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot. Cell 6:1701-1714.
173. Zlotnik, H., M. P. Fernandez, B. Bowers, and E. Cabib. 1984. Saccharomyces cerevisiae mannoproteins form an external cell wall layer that determines wall porosity. J. Bacteriol. 159:1018-1026.