Evolutionary reshaping of fungal mating pathway scaffold proteins

mBio

Volumn 2, Issue 1, 2011, Pages

  Côte, Pierre ^a,b   Sulea, Traian ^b   Dignard, Daniel ^b   Wu, Cunle ^a,b   Whiteway, Malcolm ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FAR1 LIKE PROTEIN; FUNGAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN HST7; PROTEIN STE11P; PROTEIN STE7P; SCAFFOLD PROTEIN; STE5 LIKE PROTEIN; UNCLASSIFIED DRUG; NUCLEAR MATRIX PROTEIN;

ARTICLE; BINDING SITE; CANDIDA ALBICANS; CELL CYCLE REGULATION; CELL POLARITY; CONTROLLED STUDY; DIMERIZATION; FUNGAL CELL; FUNGAL REPRODUCTION; GENE EXPRESSION; MATING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RING FINGER MOTIF; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; CHEMISTRY; CLASSIFICATION; EVOLUTION; FUNGAL GENE; FUNGUS; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

BASIDIOMYCOTA; CANDIDA; CANDIDA ALBICANS; PEZIZOMYCETES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCOTINA;

AMINO ACID SEQUENCE; BIOLOGICAL EVOLUTION; CANDIDA ALBICANS; FUNGAL PROTEINS; FUNGI; GENES, MATING TYPE, FUNGAL; MOLECULAR SEQUENCE DATA; NUCLEAR MATRIX-ASSOCIATED PROTEINS; PHYLOGENY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 79955125042     PISSN: None     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00230-10     Document Type: Article

References (65)

1. Bhattacharyya, R. P., A. Remenyi, B. J. Yeh, and W. A. Lim. 2006. Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu. Rev. Biochem. 75:655-680.
2. Dard, N., and M. Peter. 2006. Scaffold proteins in MAP kinase signaling: more than simple passive activating platforms. Bioessays 28:146-156.
3. Cortese, M. S., V. N. Uversky, and A. K. Dunker. 2008. Intrinsic disorder in scaffold proteins: getting more from less. Prog. Biophys. Mol. Biol. 98:85-106.
4. Elion, E. A. 2001. The Ste5p scaffold. J. Cell Sci. 114:3967-3978.
5. Printen, J. A., and G. F. Sprague, Jr. 1994. Protein-protein interactions in the yeast pheromone response pathway: Ste5p interacts with all members of the MAP kinase cascade. Genetics 138:609-619.
6. Marcus, S., A. Polverino, M. Barr, and M. Wigler. 1994. Complexes between STE5 and components of the pheromone-responsive mitogenactivated protein kinase module. Proc. Natl. Acad. Sci. U. S. A. 91: 7762-7766.
7. Choi, K. Y., B. Satterberg, D. M. Lyons, and E. A. Elion. 1994. Ste5 tethers multiple protein kinases in the MAP kinase cascade required for mating in S. cerevisiae. Cell 78:499-512.
8. Whiteway, M. S., C. Wu, T. Leeuw, K. Clark, A. Fourest-Lieuvin, D. Y. Thomas, and E. Leberer. 1995. Association of the yeast pheromone response G protein beta gamma subunits with the MAP kinase scaffold Ste5p. Science 269:1572-1575.
9. Pryciak, P. M., and F. A. Huntress. 1998. Membrane recruitment of the kinase cascade scaffold protein Ste5 by the Gbetagamma complex underlies activation of the yeast pheromone response pathway. Genes Dev. 12: 2684-2697.
10. Chen, R. E., and J. Thorner. 2007. Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1773:1311-1340.
11. Bhattacharyya, R. P., A. Remenyi, M. C. Good, C. J. Bashor, A. M. Falick, and W. A. Lim. 2006. The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311:822-826.
12. Winters, M. J., R. E. Lamson, H. Nakanishi, A. M. Neiman, and P. M. Pryciak. 2005.Amembrane binding domain in the ste5 scaffold synergizes with gbetagamma binding to control localization and signaling in pheromone response. Mol. Cell 20:21-32.
13. Borden, K. L. 2000. RING domains: master builders of molecular scaffolds? J. Mol. Biol. 295:1103-1112.
14. Shaw, G. 1996. The pleckstrin homology domain: an intriguing multifunctional protein module. Bioessays 18:35-46.
15. Good, M., G. Tang, J. Singleton, A. Remenyi, and W. A. Lim. 2009. The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation. Cell 136:1085-1097.
16. Yablonski, D., I. Marbach, and A. Levitzki. 1996. Dimerization of Ste5, a mitogen-activated protein kinase cascade scaffold protein, is required for signal transduction. Proc. Natl. Acad. Sci. U. S. A. 93:13864-13869.
17. Kranz, J. E., B. Satterberg, and E. A. Elion. 1994. The MAP kinase Fus3 associates with and phosphorylates the upstream signaling component Ste5. Genes Dev. 8:313-327.
18. Deshaies, R. J., and C. A. Joazeiro. 2009. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78:399-434.
19. Garrenton, L. S., S. L. Young, and J. Thorner. 2006. Function of the MAPK scaffold protein, Ste5, requires a cryptic PH domain. Genes Dev. 20:1946-1958.
20. Inouye, C., N. Dhillon, and J. Thorner. 1997. Ste5 RING-H2 domain: role in Ste4-promoted oligomerization for yeast pheromone signaling. Science 278:103-106.
21. Wiget, P., Y. Shimada, A. C. Butty, E. Bi, and M. Peter. 2004. Sitespecific regulation of the GEF Cdc24p by the scaffold protein Far1p during yeast mating. EMBO J. 23:1063-1074.
22. Leberer, E., D. Dignard, D. Harcus, L. Hougan, M. Whiteway, and D. Y. Thomas. 1993. Cloning of Saccharomyces cerevisiae STE5 as a suppressor of a Ste20 protein kinase mutant: structural and functional similarity of Ste5 to Far1. Mol. Gen. Genet. 241:241-254.
23. Butty, A. C., P. M. Pryciak, L. S. Huang, I. Herskowitz, and M. Peter. 1998. The role of Far1p in linking the heterotrimeric G protein to polarity establishment proteins during yeast mating. Science 282:1511-1516.
24. Elion, E. A., B. Satterberg, and J. E. Kranz. 1993. FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1. Mol. Biol. Cell 4:495-510.
25. Peter, M., A. Gartner, J. Horecka, G. Ammerer, and I. Herskowitz. 1993. FAR1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell 73:747-760.
26. Tyers, M., and B. Futcher. 1993. Far1 and Fus3 link the mating pheromone signal transduction pathway to three G1-phase Cdc28 kinase complexes. Mol. Cell. Biol. 13:5659-5669.
27. Elion, E. A. 2000. Pheromone response, mating and cell biology. Curr. Opin. Microbiol. 3:573-581.
28. Mendenhall, M. D. 1998. Cyclin-dependent kinase inhibitors of Saccharomyces cerevisiae and Schizosaccharomyces pombe. Curr. Top. Microbiol. Immunol. 227:1-24.
29. Chang, F., and I. Herskowitz. 1990. Identification of a gene necessary for cell cycle arrest by a negative growth factor of yeast: FAR1 is an inhibitor of a G1 cyclin, CLN2. Cell 63:999-1011.
30. Lyons, D. M., S. K. Mahanty, K. Y. Choi, M. Manandhar, and E. A. Elion. 1996. The SH3-domain protein Bem1 coordinates mitogenactivated protein kinase cascade activation with cell cycle control in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:4095-4106.
31. Shimada, Y., M. P. Gulli, and M. Peter. 2000. Nuclear sequestration of the exchange factor Cdc24 by Far1 regulates cell polarity during yeast mating. Nat. Cell Biol. 2:117-124.
32. 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.
33. Côte, P., and M. Whiteway. 2008. The role of Candida albicans FAR1 in regulation of pheromone-mediated mating, gene expression and cell cycle arrest. Mol. Microbiol. 68:392-404.
34. Atir-Lande, A., T. Gildor, and D. Kornitzer. 2005. Role for the SCFCDC4 ubiquitin ligase in Candida albicans morphogenesis. Mol. Biol. Cell 16: 2772-2785.
35. Tsong, A. E., M. G. Miller, R. M. Raisner, and A. D. Johnson. 2003. Evolution of a combinatorial transcriptional circuit: a case study in yeasts. Cell 115:389-399.
36. Yi, S., N. Sahni, K. J. Daniels, C. Pujol, T. Srikantha, and D. R. Soll. 2008. The same receptor,Gprotein, and mitogen-activated protein kinase pathway activate different downstream regulators in the alternative white and opaque pheromone responses of Candida albicans. Mol. Biol. Cell 19:957-970.
37. Zhao, R., K. J. Daniels, S. R. Lockhart, K. M. Yeater, L. L. Hoyer, and D. R. Soll. 2005. Unique aspects of gene expression during Candida albicans mating and possible G(1) dependency. Eukaryot. Cell 4:1175-1190.
38. Fischer, D. 2006. Servers for protein structure prediction. Curr. Opin. Struct. Biol. 16:178-182.
39. Ginalski, K., A. Elofsson, D. Fischer, and L. Rychlewski. 2003. 3D-Jury: a simple approach to improve protein structure predictions. Bioinformatics 19:1015-1018.
40. Wapinski, I., A. Pfeffer, N. Friedman, and A. Regev. 2007. Natural history and evolutionary principles of gene duplication in fungi. Nature 449:54-61.
41. Toda, T., M. Shimanuki, and M. Yanagida. 1991. Fission yeast genes that confer resistance to staurosporine encode an AP-1-like transcription factor and a protein kinase related to the mammalian ERK1/MAP2 and budding yeast FUS3 and KSS1 kinases. Genes Dev. 5:60-73.
42. Neiman, A. M., B. J. Stevenson, H. P. Xu, G. F. Sprague, Jr., I. Herskowitz, M. Wigler, and S. Marcus. 1993. Functional homology of protein kinases required for sexual differentiation in Schizosaccharomyces pombe and Saccharomyces cerevisiae suggests a conserved signal transduction module in eukaryotic organisms. Mol. Biol. Cell 4:107-120.
43. Butler, G., et al. 2009. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657-662.
44. Whittaker, C. A., and R. O. Hynes. 2002. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell 13:3369-3387.
45. Inouye, C., N. Dhillon, T. Durfee, P. C. Zambryski, and J. Thorner. 1997. Mutational analysis of STE5 in the yeast Saccharomyces cerevisiae: application of a differential interaction trap assay for examining proteinprotein interactions. Genetics 147:479-492.
46. Wu, C., G. Jansen, J. Zhang, D. Y. Thomas, and M. Whiteway. 2006. Adaptor protein Ste50p links the Ste11p MEKK to the HOG pathway through plasma membrane association. Genes Dev. 20:734-746.
47. Remenyi, A., M. C. Good, R. P. Bhattacharyya, and W. A. Lim. 2005. The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol. Cell 20:951-962.
48. Stynen, B., P. Van Dijck, and H. Tournu. 2010. A CUG codon adapted two-hybrid system for the pathogenic fungus Candida albicans. Nucleic Acids Res. 38:e184.
49. Schwartz, M. A., and H. D. Madhani. 2004. Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. Annu. Rev. Genet. 38: 725-748.
50. Ponting, C. P., L. Aravind, J. Schultz, P. Bork, and E. V. Koonin. 1999. Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. J. Mol. Biol. 289:729-745.
51. Bi, X., R. A. Corpina, and J. Goldberg. 2002. Structure of the Sec23/ 24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419: 271-277.
52. Humbert, S., H. van Vuuren, Y. Lutz, J. H. Hoeijmakers, J. M. Egly, and V. Moncollin. 1994. p44 and p34 subunits of the BTF2/TFIIH transcription factor have homologies with SSL1, a yeast protein involved in DNA repair. EMBO J. 13:2393-2398.
53. Takagi, Y., C. A. Masuda, W. H. Chang, H. Komori, D. Wang, T. Hunter, C. A. Joazeiro, and R. D. Kornberg. 2005. Ubiquitin ligase activity of TFIIH and the transcriptional response to DNA damage. Mol. Cell 18:237-243.
54. Verma, R., R. Oania, J. Graumann, and R. J. Deshaies. 2004. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 118:99-110.
55. Fu, H., N. Reis, Y. Lee, M. H. Glickman, and R. D. Vierstra. 2001. Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome. EMBO J. 20:7096-7107.
56. Bounpheng, M. A., J. J. Dimas, S. G. Dodds, and B. A. Christy. 1999. Degradation of Id proteins by the ubiquitin-proteasome pathway. FASEB J. 13:2257-2264.
57. Voges, D., P. Zwickl, and W. Baumeister. 1999. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68:1015-1068.
58. Daniels, K. J., T. Srikantha, S. R. Lockhart, C. Pujol, and D. R. Soll. 2006. Opaque cells signal white cells to form biofilms in Candida albicans. EMBO J. 25:2240-2252.
59. Sahni, N., S. Yi, K. J. Daniels, G. Huang, T. Srikantha, and D. R. Soll. 2010. Tec1 mediates the pheromone response of the white phenotype of Candida albicans: insights into the evolution of new signal transduction pathways. PLoS Biol. 8:e1000363.
60. Wolfe, K. H., and D. C. Shields. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708-713.
61. Peisajovich, S. G., J. E. Garbarino, P. Wei, and W. A. Lim. 2010. Rapid diversification of cell signaling phenotypes by modular domain recombination. Science 328:368-372.
62. Magee, B. B., M. Legrand, A. M. Alarco, M. Raymond, and P. T. Magee. 2002. Many of the genes required for mating in Saccharomyces cerevisiae are also required for mating in Candida albicans. Mol. Microbiol. 46:1345-1351.
63. Nicholls, S., M. Straffon, B. Enjalbert, A. Nantel, S. Macaskill, M. Whiteway, and A. J. Brown. 2004. Msn2- and Msn4-like transcription factors play no obvious roles in the stress responses of the fungal pathogen Candida albicans. Eukaryot. Cell 3:1111-1123.
64. Dignard, D., and M. Whiteway. 2006. SST2, a regulator of G-protein signaling for the Candida albicans mating response pathway. Eukaryot. Cell 5:192-202.
65. Yi, S., N. Sahni, K. J. Daniels, K. L. Liu, G. Huang, A. M. Garnaas, C. Pujol, T. Srikantha, D. R. Soll. 2011. Utilization of the mating scaffold protein in the evolution of a new signal transduction pathway for biofilm development. mBio 2(1):e00237-10. doi:10.1128/mBio.00237-10.