Mitogen-activated protein kinases with distinct requirements for Ste5 scaffolding influence signaling specificity in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 25, Issue 5, 2005, Pages 1793-1803

  Flatauer, Laura J ^a   Zadeh, Sheena F ^a   Bardwell, Lee ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; SCAFFOLD PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL CYCLE; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; STIMULUS RESPONSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CYCLE; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; OSMOTIC PRESSURE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 14044266923     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.5.1793-1803.2005     Document Type: Article

References (50)

1. Andersson, J., D. M. Simpson, M. Qi, Y. Wang, and E. A. Elion. 2004. Differential input by Ste5 scaffold and Msg5 phosphatase route a MAPK cascade to multiple outcomes. EMBO J. 23:2564-2576.
2. Bardwell, A. J., L. J. Flatauer, K. Matsukuma, J. Thorner, and L. Bardwell. 2001. A conserved docking site in MEKs mediates high-affinity binding to MAP kinases and cooperates with a scaffold protein to enhance signal transmission. J. Biol. Chem. 276:10374-10386.
3. Bardwell, L. 2005. A walk-through of the yeast mating pheromone response pathway. Peptides 26:339-350.
4. Bardwell, L., J. G. Cook, E. C. Chang, B. R. Cairns, and J. Thorner. 1996. Signaling in the yeast pheromone response pathway: specific and high-affinity interaction of the mitogen-activated protein (MAP) kinases Kss1 and Fus3 with the upstream MAP kinase kinase Ste7. Mol. Cell. Biol. 16:3637-3650.
5. Bardwell, L., J. G. Cook, J. X. Zhu-Shimoni, D. Voora, and J. Thorner. 1998. Differential regulation of transcription: repression by unactivated mitogen-activated protein kinase Kss1 requires the Dig1 and Dig2 proteins. Proc. Natl. Acad. Sci. USA 95:15400-15405.
6. Bartel, P. L., and S. Fields. 1995. Analyzing protein-protein interactions using the two-hybrid system. Methods Enzymol. 254:241-263.
7. Boguslawski, G. 1992. PBS2, a yeast gene encoding a putative protein kinase, interacts with the RAS2 pathway and affects the osmotic sensitivity of Saccharomyces cerevisiae. J. Gen. Microbiol. 138:2425-2432.
8. Breitkreutz, A., L. Boucher, and M. Tyers. 2001. MAPK specificity in the yeast pheromone response independent of transcriptional activation. Curr. Biol. 11:1266-1271.
9. Cairns, B. R., S. W. Ramer, and R. D. Kornherg. 1992. Order of action of components in the yeast pheromone response pathway revealed with a dominant allele of the STE11 kinase and the multiple phosphorylation of the STE7 kinase. Genes Dev. 6:1305-1318.
10. 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.
11. Cook, J. G., L. Bardwell, and J. Thorner. 1997. Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous growth signaling pathway. Nature 390:85-88.
12. 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.
13. 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.
14. 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.
15. Elion, E. A. 2001. The Ste5p scaffold. J. Cell Sci. 114:3967-3978.
16. Errede, B., A. Gartner, Z. Zhou, K. Naysmith, and G. Ammerer. 1993. MAP kinase-related FUS3 from S. cerevisiae is activated by STE7 in vitro. Nature 362:261-264.
17. Ferrell, J. E., Jr., and K. A. Cimprich. 2003. Enforced proximity in the function of a famous scaffold. Mol. Cell 11:289-291.
18. Hagen, D. C., G. McCaffrey, and G. F. Sprague, Jr. 1991. Pheromone response elements are necessary and sufficient for basal and pheromone-induced transcription of the FUS1 gene of Saccharomyces cerevisiae. Mol. Cell. Biol. 11:2952-2961.
19. Hall, J. P., V. Cherkasova, E. Elion, M. C. Gustin, and E. Winter. 1996. The osmoregulatory pathway represses mating pathway activity in Saccharomyces cerevisiae: isolation of a FUS3 mutant that is insensitive to the repression mechanism. Mol. Cell. Biol. 16:6715-6723.
20. Harris, K., R. E. Lamson, B. Nelson, T. R. Hughes, M. J. Marton, C. J. Roberts, C. Boone, and P. M. Pryciak. 2001. Role of scaffolds in MAP kinase pathway specificity revealed by custom design of pathway-dedicated signaling proteins. Curr. Biol. 11:1815-1824.
21. Hartwell, L. H. 1980. Mutants of Saccharomyces cerevisiae unresponsive to cell division control by polypeptide mating hormone. J. Cell Biol. 85:811-822.
22. 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 protein-protein interactions. Genetics 147:479-492.
23. 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.
24. Jansen, G., F. Buhring, C. P. Hollenberg, and M. Ramezani Rad. 2001. Mutations in the SAM domain of STE50 differentially influence the MAPK-mediated pathways for mating, filamentous growth and osmotolerance in Saccharomyces cerevisiae. Mol. Genet. Genomics 265:102-117.
25. Kusari, A. B., D. M. Molina, W. Sabbagh, Jr., C. S. Lau, and L. Bardwell. 2004. A conserved protein interaction network involving the yeast MAP kinases Fus3 and Kss1. J. Cell Biol. 164:267-277.
26. 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.
27. Liu, H., C. A. Styles, and G. R. Fink. 1996. Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics 144:967-978.
28. Lodish, H., A. Berk, P. Matsudaira, C. A. Kaiser, M. Krieger, M. P. Scott, S. L. Zipursky, and J. Darnell. 2003. Molecular cell biology, 5th ed. W. H. Freeman, New York, N. Y.
29. Madhani, H. D., and G. R. Fink. 1997. Combinatorial control required for the specificity of yeast MAPK signaling. Science 275:1314-1317.
30. Madhani, H. D., and G. R. Fink. 1998. The riddle of MAP kinase signaling specificity. Trends Genet. 14:151-155.
31. 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.
32. Maleri, S., Q. Ge, E. A. Hackett, Y. Wang, H. G. Dohlman, and B. Errede. 2004. Persistent activation by constitutive Ste7 promotes Kss1-mediated invasive growth but fails to support Fus3-dependent mating in yeast. Mol. Cell. Biol. 24:9221-9238.
33. Neiman, A. M., and I. Herskowitz. 1994. Reconstitution of a yeast protein kinase cascade in vitro: activation of the yeast MEK homolog STE7 by STE11. Proc. Natl. Acad. Sci. USA 91:3398-3402.
34. O'Rourke, S. M., and I. Herskowitz. 1998. The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes Dev. 12:2874-2886.
35. Park, S. H., A. Zarrinpar, and W. A. Lim. 2003. Rewiring MAP kinase pathways using alternative scaffold assembly mechanisms. Science 299:1061-1064.
36. Pawson, T., and P. Nash. 2000. Protein-protein interactions define specificity in signal transduction. Genes Dev. 14:1027-1047.
37. 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.
38. Pryciak, P. M., and F. A. Huntress. 1998. Membrane recruitment of the kinase cascade scaffold protein Ste5 by the Gβγ complex underlies activation of the yeast pheromone response pathway. Genes Dev. 12:2684-2697.
39. 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.
40. 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.
41. Sabbagh, W., Jr., L. J. Flatauer, A. J. Bardwell, and L. Bardwell. 2001. Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation. Mol. Cell 8:683-691.
42. Schuller, C., J. L. Brewster, M. R. Alexander, M. C. Gustin, and H. Ruis. 1994. The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J. 13:4382-4389.
43. Sette, C., C. J. Inouye, S. L. Stroschein, P. J. Iaquinta, and J. Thorner. 2000. Mutational analysis suggests that activation of the yeast pheromone response mitogen-activated protein kinase pathway involves conformational changes in the Ste5 scaffold protein. Mol. Biol. Cell 11:4033-4049.
44. Siekhaus, D. E., and D. G. Drubin. 2003. Spontaneous receptor-independent heterotrimeric G-protein signalling in an RGS mutant. Nat. Cell Biol. 5:231-235.
45. Stevenson, B. J., N. Rhodes, B. Errede, and G. F. Sprague, Jr. 1992. Constitutive mutants of the protein kinase STE11 activate the yeast pheremone response pathway in the absence of the G protein. Genes Dev. 6:1293-1304.
46. van Drogen, F., S. M. O'Rourke, V. M. Stucke, M. Jaquenoud, A. M. Neiman, and M. Peter. 2000. Phosphorylation of the MEKK Ste11p by the PAK-like kinase Ste20p is required for MAP kinase signaling in vivo. Curr. Biol. 10:630-639.
47. van Drogen, F., and M. Peter. 2002. MAP kinase cascades: scaffolding signal specificity. Curr. Biol. 12:R53-R55.
48. Wang, Y., and E. A. Elion. 2003. Nuclear export and plasma membrane recruitment of the Ste5 scaffold are coordinated with oligomerization and association with signal transduction components. Mol. Biol. Cell 14:2543-2558.
49. Whitmarsh, A. J., and R. J. Davis. 1998. Structural organization of MAP-kinase signaling modules by scaffold proteins in yeast and mammals. Trends Biochem. Sci. 23:481-485.
50. Zarrinpar, A., R. P. Bhattacharyya, M. P. Nittler, and W. A. Lim. 2004. Sho1 and Pbs2 act as coscaffolds linking components in the yeast high osmolarity MAP kinase pathway. Mol. Cell 14:825-832.