Phosphorylation of the RGS protein Sst2 by the MAP kinase Fus3 and use of Sst2 as a model to analyze determinants of substrate sequence specificity

Biochemistry

Volumn 44, Issue 22, 2005, Pages 8159-8166

  Parnell, Stephen C ^a   Marotti Jr , Louis A ^a,b   Kiang, Lee ^a,c   Torres, Matthew P ^a   Borchers, Christoph H ^a   Dohlman, Henrik G ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYMES; MASS SPECTROMETRY; MATHEMATICAL MODELS; SYNTHESIS (CHEMICAL); YEAST;

MUTANTS; PEPTIDES; PHOSPHORYLATION; SYNTHETIC PEPTIDES;

PROTEINS;

AMINO ACID; HISTIDINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE FUS3; MUTANT PROTEIN; PROLINE; RGS PROTEIN; RGS PROTEIN SST2; SERINE; SYNTHETIC PEPTIDE; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; MOLECULAR RECOGNITION; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE;

ALANINE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CONSENSUS SEQUENCE; FEEDBACK, BIOCHEMICAL; GTPASE-ACTIVATING PROTEINS; HISTIDINE; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDE MAPPING; PHENYLALANINE; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE PROTEINS; SERINE; SUBSTRATE SPECIFICITY; TRYPTOPHAN;

SACCHAROMYCES CEREVISIAE;

EID: 20144383113     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0503091     Document Type: Article

References (37)

1. Dohlman, H. G. (2002) G proteins and pheromone signaling, Annu. Rev. Physiol. 64, 129-152.
2. Apanovitch, D. M., Slep, K. C., Sigler, P. B., and Dohlman, H. G. (1998) Sst2 is a GTPase-activating protein for Opal: purification and characterization of a cognate RGS-Ga protein pair in yeast, Biochemistry 37, 4815-4822.
3. Yi, T. M., Kitano, H., and Simon, M. I. (2003) A quantitative characterization of the yeast heterotrimeric G protein cycle. Proc. Natl. Acad. Sci. U.S.A. 100, 10764-10769.
4. Dohlman, H. G., and Thorner, J. W. (2001) Regulation of G protein-initiated signal transduction in yeast: paradigms and principles, Annu. Rev. Biochem. 70, 703-754.
5. Elion, E. A., Satterberg, B., and Kranz, J. E. (1993) FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1, Mol. Biol. Cell 4, 495-510.
6. Breitkreutz, A., Boucher, L., and Tyers, M. (2001) MAPK specificity in the yeast pheromone response independent of transcriptional activation, Curr. Biol. 11, 1266-1271.
7. Hung, W., Olson, K. A., Breitkreutz, A., and Sadowski, I. (1997) Characterization of the basal and pheromone-stimulated phosphorylation states of Ste12p, Eur. J. Biochem. 245, 241-251.
8. Breitkreutz, A., and Tyers, M. (2002) MAPK signaling specificity: it takes two to tango, Trends Cell Biol. 12, 254-257.
9. Cook, J. G., Bardwell, L., Kron, S. J., and Thorner, J. (1996) Two novel targets of the MAP kinase Kss1 are negative regulators of invasive growth in the yeast Saccharomyces cerevisiae. Genes Dev. 10, 2831-2848.
10. Zhou, Z., Gartner, A., Cade, R., Ammerer, G., and Errede, B. (1993) Pheromone-induced signal transduction in Saccharomyces cerevisiae requires the sequential function of three protein kinases, Mol. Cell. Biol. 13, 2069-2080.
11. Maleri, S., Ge, Q., Hackett, E. A., Wang, Y., Dohlman, H. G., and Errede, B. (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.
12. Bardwell, L., Cook, J. G., Inouye, C. J., and Thorner, J. (1994) Signal propagation and regulation in the mating pheromone response pathway of the yeast Saccharomyces cerevisiae, Dev. Biol. 166, 363-379.
13. Doi, K., Gartner, A., Ammerer, G., Errede, B., Shinkawa, H., Sugimoto, K., and Matsumoto, K. (1994) MSG5, a novel protein phosphatase promotes adaptation to pheromone response in S. cerevisiae, EMBO J. 13, 61-70.
14. Tyers, M., and Futcher, B. (1993) Farl and Fus3 link the mating pheromone signal transduction pathway to three G1-phase Cdc28 kinase complexes, Mol. Cell. Biol. 13, 5659-5669.
15. Peter, M., Gartner, A., Horecka, J., Ammerer, G., and Herskowitz, I. (1993) FAR1 links the signal transduction pathway to the cell cycle machinery in yeast, Cell 73, 747-760.
16. Cherkasova, V. A., McCully, R., Wang, Y., Hinnebusch, A., and Elion, E. A. (2003) A novel functional link between MAP kinase cascades and the Ras/cAMP pathway that regulates survival, Curr. Biol. 13, 1220-1226.
17. Feng, Y., and Davis, N. G. (2000) Feedback phosphorylation of the yeast a-factor receptor requires activation of the downstream signaling pathway from G protein through mitogen-activated protein kinase, Mol. Cell. Biol. 20, 563-574.
18. Li, E., Cismowski, M. J., and Stone, D. E. (1998) Phosphorylation of the pheromone-responsive Gbeta protein of Saccharomyces cerevisiae does not affect its mating-specific signaling function, Mol. Gen. Genet. 258, 608-618.
19. Oehlen, B., and Cross, F. R. (1994) Signal transduction in the budding yeast Saccharomyces cerevisiae, Curr. Opin. Cell Biol. 6, 836-841.
20. Garrison, T. R., Zhang, Y., Pausch, M., Apanovitch, D., Aebersold, R., and Dohlman, H. G. (1999) Feedback phosphorylation of an RGS protein by MAP kinase in yeast. J. Biol. Chem. 274, 36387-36391.
21. Clark-Lewis, I., Sanghera, J. S., and Pelech, S. L. (1991) Definition of a consensus sequence for peptide substrate recognition by p44mpk, the meiosis-activated myelin basic protein kinase, J. Biol. Chem. 266, 15180-15184.
22. Gonzalez, F. A., Raden, D. L., and Pavis, R. J. (1991) Identification of substrate recognition determinants for human ERK1 and ERK2 protein kinases, J. Biol. Chem. 266, 22159-22163.
23. Tesmer, J. J., Berman, D. M., Gilman, A. G., and Sprang, S. R. (1997) Structure of RGS4 bound to A1F4-activated G(iα1): stabilization of the transition state for GTP hydrolysis, Cell 89, 251-261.
24. Dohlman, H. G., Song, J., Ma, D., Coarchesne, W. E., and Thorner, J. (1996) Sst2, a negative regulator of pheromone signaling in the yeast Saccharomyces cerevisiae: expression, localization, and genetic interaction and physical association with Gpa1 (the G-protein α subunit), Mol. Cell. Biol. 16, 5194-5209.
25. Gietz, R. D., and Woods, R. A. (2002) Transformation of yeast by the LiAc/ss carrier DNA/PEG method. Methods Enzymol. 350, 87-96.
26. Dohlman, H. G., Apaniesk, D., Cheo, Y., Song, J., and Nusskern, D. (1995) Inhibition of G-protein signaling by dominant gain-of-function mutations in Sst2p, a pheromone desensitization factor in Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 3635-3643.
27. Kallal, L., and Fishel, R. (2000) The GTP hydrolysis defect of the Saccharomyces cerevisiae mutant G-protein Gpa1(G50V), Yeast 16, 387-400.
28. Errede, B., Gartner, A., Zhou, Z., Nasmyth, K., and Ammerer, G. (1993) MAP kinase-related FUS3 from S. cerevisiae is activated by STE7 in vitro, Nature 362, 261-264.
29. Horchers, C., Peter, J. F., Hall, M. C., Kunkel, T. A., and Tomer, K. B. (2000) Identification of in-gel digested proteins by complementary peptide mass fingerprinting and tandem mass spectrometry data obtained on an electrospray ionization quadrupole time-of-flight mass spectrometer, Anal. Chem. 72, 1163-1168.
30. Hoffman, G., Garrison, T. R., and Dohlman, H. G. (2002) Analysis of RGS proteins in Saccharomyces cerevisiae, Methods Enzymol. 344, 617-631.
31. Hao, N., Yildirim, N., Wang, Y., Elston, T. C., and Dohlman, H. G. (2003) Regulators of G protein signaling and transient activation of signaling: experimental and computational analysis reveals negative and positive feedback controls on G protein activity, J. Biol. Chem. 278, 46506-46515.
32. Prowse, C. N., Hagopian, J. C., Cobb, M. H., Ahn, N. G., and Lew, J. (2000) Catalytic reaction pathway for the mitogen-activated protein kinase ERK2, Biochemistry 39, 6258-6266.
33. Songyang, Z., Lu, K. P., Kwon, Y. T., Tsai, L. H., Filhol, O., Cochet, C., Brickey, D. A., Soderling, T. R., Bartleson, C., Graves, D. J., DeMaggio, A. J., Hoekstra, M. F., Blenis, J., Hunter, T., and Cantley, L. C. (1996) A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and Erk1, Mol. Cell. Biol. 16, 6486-6493.
34. Songyang, Z. (2001) Analysis of protein kinase specificity by peptide libraries and prediction of in vivo substrates, Methods Enzymol. 332, 171-183.
35. Northwood, I. C., Gonzalez, F. A., Wartmann, M., Raden, D. L., and Davis, R. J. (1991) Isolation and characterization of two growth factor-stimulated protein kinases that phosphorylate the epidermal growth factor receptor at threonine 669. J. Biol. Chem. 266, 15266-15276.
36. Alvarez, E., Northwood, I. C., Gonzalez, F. A., Latour, D. A., Seth, A., Abate, C., Curran, T., and Davis, R. J. (1991) Pro-Leu-Ser/Thr-Pro is a consensus primary sequence for substrate protein phosphorylation. Characterization of the phosphorylation of c-myc and c-jun proteins by an epidermal growth factor receptor threonine 669 protein kinase, J. Biol. Chem. 266, 15277-15285.
37. Gruhler, A., Olsen, J. V., Mohammed, S., Mortensen, P., Faergeman, N. J., Mann, M., and Jensen, O. N. (2005) Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway, Mol. Cell. Proteomics 4, 310-327.