Pheromone-induced anisotropy in yeast plasma membrane phosphatidylinositol- 4,5-bisphosphate distribution is required for MAPK signaling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 26, 2010, Pages 11805-11810

  Garrenton, Lindsay S ^a,c   Stefan, Christopher J ^b   McMurray, Michael A ^a   Emr, Scott D ^b   Thorner, Jeremy ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b School of Integrative Plant Sciences   (United States)

^c GENENTECH INC   (United States)

Author keywords

factor; Phosphoinositides; Scaffold protein; Yeast mating response

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PHEROMONE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PLECKSTRIN;

ACTIN FILAMENT; ANISOTROPY; ARTICLE; CELL MEMBRANE; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; ENZYME LOCALIZATION; FLUOROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; SIGNAL TRANSDUCTION; STIMULUS; YEAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL MEMBRANE; CELL SURFACE EXTENSIONS; FLUORESCENCE POLARIZATION; FLUORESCENT DYES; MAP KINASE SIGNALING SYSTEM; PHEROMONES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN PRECURSORS; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 77955370261     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1005817107     Document Type: Article

References (36)

1. 2) and proteins: Interactions, organization, and information flow. Annu Rev Biophys Biomol Struct 31:151-175.
2. Janmey PA, Lindberg U (2004) Cytoskeletal regulation: Rich in lipids. Nat Rev Mol Cell Biol 5:658-666.
3. Simonsen A, Wurmser AE, Emr SD, Stenmark H (2001) The role of phosphoinositides in membrane transport. Curr Opin Cell Biol 13:485-492.
4. Downes CP, Gray A, Lucocq JM (2005) Probing phosphoinositide functions in signaling and membrane trafficking. Trends Cell Biol 15:259-268.
5. Janetopoulos C, Devreotes P (2006) Phosphoinositide signaling plays a key role in cytokinesis. J Cell Biol 174:485-490.
6. Bagorda A, Mihaylov VA, Parent CA (2006) Chemotaxis: Moving forward and holding on to the past. Thromb Haemost 95:12-21.
7. Martin-Belmonte F, et al. (2007) PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128:383-397.
8. 2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314:1458-1461.
9. Ziel JW, Hagedorn EJ, Audhya A, Sherwood DR (2009) UNC-6 (netrin) orients the invasive membrane of the anchor cell in C. elegans. Nat Cell Biol 11:183-189.
10. Strahl T, Thorner J (2007) Synthesis and function of membrane phosphoinositides in budding yeast, Saccharomyces cerevisiae. Biochim Biophys Acta 1771:353-404.
11. Garrenton LS, Young SL, Thorner J (2006) Function of the MAPK scaffold protein, Ste5, requires a cryptic PH domain. Genes Dev 20:1946-1958.
12. Hurley JH, Meyer T (2001) Subcellular targeting by membrane lipids. Curr Opin Cell Biol 13:146-152.
13. Lemmon MA, Ferguson KM (2000) Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 350:1-18.
14. Inouye C, Dhillon N, Thorner J (1997) Ste5 RING-H2 domain: Role in Ste4-promoted oligomerization for yeast pheromone signaling. Science 278:103-106.
15. Stefan CJ, Audhya A, Emr SD (2002) The yeast synaptojanin-like proteins control the cellular distribution of phosphatidylinositol (4,5)-bisphosphate. Mol Biol Cell 13: 542-557.
16. Hilgemann DW (2007) Local PIP(2) signals: When, where, and how? Pflugers Arch 455:55-67.
17. Winters MJ, Lamson RE, Nakanishi H, Neiman AM, Pryciak PM (2005) A membrane binding domain in the ste5 scaffold synergizes with gbetagamma binding to control localization and signaling in pheromone response. Mol Cell 20:21-32.
18. Audhya A, Emr SD (2002) Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev Cell 2:593-605.
19. Strahl T, Hama H, DeWald DB, Thorner J (2005) Yeast phosphatidylinositol 4-kinase, Pik1, has essential roles at the Golgi and in the nucleus. J Cell Biol 171:967-979.
20. Orlando K, et al. (2008) Regulation of Gic2 localization and function by phosphatidylinositol 4,5-bisphosphate during the establishment of cell polarity in budding yeast. J Biol Chem 283: 14205-14212.
21. QiM, Elion EA (2005) Formin-induced actin cables are required for polarized recruitment of the Ste5 scaffold and high level activation of MAPK Fus3. J Cell Sci 118:2837-2848.
22. Ayscough KR, et al. (1997) High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J Cell Biol 137:399-416.
23. Bardwell L (2005) A walk-through of the yeast mating pheromone response pathway. Peptides 26:339-350.
24. Slessareva JE, Routt SM, Temple B, Bankaitis VA, Dohlman HG (2006) Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein alpha subunit at the endosome. Cell 126:191-203.
25. Flatauer LJ, Zadeh SF, Bardwell L (2005) Mitogen-activated protein kinases with distinct requirements for Ste5 scaffolding influence signaling specificity in Saccharomyces cerevisiae. Mol Cell Biol 25:1793-1803.
26. Sette C, Inouye CJ, Stroschein SL, Iaquinta PJ, Thorner J (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.
27. Good M, Tang G, Singleton J, Reményi A, Lim WA (2009) The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation. Cell 136:1085-1097.
28. Stolz LE, Huynh CV, Thorner J, York JD (1998) Identification and characterization of an essential family of inositol polyphosphate 5-phosphatases (INP51, INP52 and INP53 gene products) in the yeast Saccharomyces cerevisiae. Genetics 148:1715-1729.
29. Emoto K, Inadome H, Kanaho Y, Narumiya S, Umeda M (2005) Local change in phospholipid composition at the cleavage furrow is essential for completion of cytokinesis. J Biol Chem 280:37901-37907.
30. 2 functions at the cleavage furrow during cytokinesis. Curr Biol 15:1407-1412.
31. Ciejek E, Thorner J (1979) Recovery of S. cerevisiae a cells from G1 arrest by alpha factor pheromone requires endopeptidase action. Cell 18:623-635.
32. Sherman F, Fink GR, Hicks JB (1986) Laboratory Course Manual for Methods in Yeast Genetics (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY).
33. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY), 2nd Ed.
34. Sprague GF, Jr (1991) Assay of yeast mating reaction. Methods Enzymol 194:77-93.
35. Reneke JE, Blumer KJ, Courchesne WE, Thorner J (1988) The carboxy-terminal segment of the yeast alpha-factor receptor is a regulatory domain. Cell 55:221-234.
36. Stern M, Jensen R, Herskowitz I (1984) Five SWI genes are required for expression of the HO gene in yeast. J Mol Biol 178:853-868.