Rvs161p and Sphingolipids Are Required for Actin Repolarization Following Salt Stress

Overview

Journal Eukaryot Cell

Publisher American Society for Microbiology

Specialty Molecular Biology

Date 2002 Dec 13

PMID 12477802

Citations 29

Authors

Axelle Balguerie

Michel Bagnat

Marc Bonneu

Michel Aigle

Annick M Breton

Affiliations

Soon will be listed here.

Abstract

In Saccharomyces cerevisiae, the actin cytoskeleton is depolarized by NaCl stress. In this study, the response was maximal after 30 min, and then actin patches repolarized. Rvs161p was required for actin repolarization because the rvs161delta mutant did not repolarize actin patches after growth in a salt medium. Mutations suppressing the rvs161delta-related salt sensitivity all occurred in genes required for sphingolipid biosynthesis: FEN1, SUR4, SUR2, SUR1, and IPT1. These suppressors also suppressed act1-1-related salt sensitivity and the defect in actin repolarization of the rvs161delta mutant, providing a link between sphingolipids and actin polarization. Indeed, deletion of the suppressor genes suppressed the rvs161delta defect in actin repolarization in two ways: either actin was not depolarized at the wild-type level in a set of suppressor mutants, or actin was repolarized in the absence of Rvs161p in the other suppressor mutants. Rvs161p was localized as cortical patches that concentrated at polarization sites, i.e., bud emergence and septa, and was found to be associated with lipid rafts. An important link between sphingolipids and actin polarization is that Rvs161p was required for actin repolarization and was found to be located in lipid rafts.

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References

SCHNEITER R . Brave little yeast, please guide us to thebes: sphingolipid function in S. cerevisiae. Bioessays. 1999; 21(12):1004-10. DOI: 10.1002/(SICI)1521-1878(199912)22:1<1004::AID-BIES4>3.0.CO;2-Y. View

Janes P, Ley S, Magee A . Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J Cell Biol. 1999; 147(2):447-61. PMC: 2174214. DOI: 10.1083/jcb.147.2.447. View

Bagnat M, Keranen S, Shevchenko A, Simons K . Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci U S A. 2000; 97(7):3254-9. PMC: 16225. DOI: 10.1073/pnas.97.7.3254. View

Rozelle A, Machesky L, Yamamoto M, Driessens M, Insall R, Roth M . Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr Biol. 2000; 10(6):311-20. DOI: 10.1016/s0960-9822(00)00384-5. View

Brown D, London E . Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem. 2000; 275(23):17221-4. DOI: 10.1074/jbc.R000005200. View

Chung N, Jenkins G, Hannun Y, Heitman J, Obeid L . Sphingolipids signal heat stress-induced ubiquitin-dependent proteolysis. J Biol Chem. 2000; 275(23):17229-32. DOI: 10.1074/jbc.C000229200. View

Zanolari B, Friant S, Funato K, Sutterlin C, Stevenson B, Riezman H . Sphingoid base synthesis requirement for endocytosis in Saccharomyces cerevisiae. EMBO J. 2000; 19(12):2824-33. PMC: 203373. DOI: 10.1093/emboj/19.12.2824. View

Roper K, Corbeil D, Huttner W . Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol. 2000; 2(9):582-92. DOI: 10.1038/35023524. View

Philip B, Levin D . Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol Cell Biol. 2000; 21(1):271-80. PMC: 88800. DOI: 10.1128/MCB.21.1.271-280.2001. View

10.

Lang T, Bruns D, Wenzel D, Riedel D, Holroyd P, Thiele C . SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 2001; 20(9):2202-13. PMC: 125434. DOI: 10.1093/emboj/20.9.2202. View

11.

Chamberlain L, Burgoyne R, Gould G . SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc Natl Acad Sci U S A. 2001; 98(10):5619-24. PMC: 33262. DOI: 10.1073/pnas.091502398. View

12.

Ikonen E . Roles of lipid rafts in membrane transport. Curr Opin Cell Biol. 2001; 13(4):470-7. DOI: 10.1016/s0955-0674(00)00238-6. View

13.

Martin T . PI(4,5)P(2) regulation of surface membrane traffic. Curr Opin Cell Biol. 2001; 13(4):493-9. DOI: 10.1016/s0955-0674(00)00241-6. View

14.

Breton A, Schaeffer J, Aigle M . The yeast Rvs161 and Rvs167 proteins are involved in secretory vesicles targeting the plasma membrane and in cell integrity. Yeast. 2001; 18(11):1053-68. DOI: 10.1002/yea.755. View

15.

Chung N, Mao C, Heitman J, Hannun Y, Obeid L . Phytosphingosine as a specific inhibitor of growth and nutrient import in Saccharomyces cerevisiae. J Biol Chem. 2001; 276(38):35614-21. DOI: 10.1074/jbc.M105653200. View

16.

Friant S, Lombardi R, Schmelzle T, Hall M, Riezman H . Sphingoid base signaling via Pkh kinases is required for endocytosis in yeast. EMBO J. 2001; 20(23):6783-92. PMC: 125749. DOI: 10.1093/emboj/20.23.6783. View

17.

Bagnat M, Chang A, Simons K . Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast. Mol Biol Cell. 2001; 12(12):4129-38. PMC: 60781. DOI: 10.1091/mbc.12.12.4129. View

18.

Itoh K, Sakakibara M, Yamasaki S, Takeuchi A, Arase H, Miyazaki M . Cutting edge: negative regulation of immune synapse formation by anchoring lipid raft to cytoskeleton through Cbp-EBP50-ERM assembly. J Immunol. 2002; 168(2):541-4. DOI: 10.4049/jimmunol.168.2.541. View

19.

Young M, Karpova T, Brugger B, Moschenross D, Wang G, Schneiter R . The Sur7p family defines novel cortical domains in Saccharomyces cerevisiae, affects sphingolipid metabolism, and is involved in sporulation. Mol Cell Biol. 2002; 22(3):927-34. PMC: 133540. DOI: 10.1128/MCB.22.3.927-934.2002. View

20.

Sikorski R, Hieter P . A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989; 122(1):19-27. PMC: 1203683. DOI: 10.1093/genetics/122.1.19. View