A Pil1-Sle1-Syj1-Tax4 Functional Pathway Links Eisosomes with PI(4,5)P2 Regulation

Overview

Journal J Cell Sci

Specialty Cell Biology

Date 2014 Jan 18

PMID 24434583

Citations 22

Authors

Ruth Kabeche

Assen Roguev

Nevan J Krogan

James B Moseley

Affiliations

Soon will be listed here.

Abstract

Stable compartments of the plasma membrane promote a wide range of cellular functions. In yeast cells, cytosolic structures called eisosomes generate prominent cortical invaginations of unknown function. Through a series of genetic screens in fission yeast, we found that the eisosome proteins Pil1 and Sle1 function with the synaptojanin-like lipid phosphatase Syj1 and its ligand Tax4. This genetic pathway connects eisosome function with the hydrolysis of phosphatidylinositol (4,5)-bisphosphate [PI(4,5)P2] in cells. Defects in PI(4,5)P2 regulation led to eisosome defects, and we found that the core eisosome protein Pil1 can bind to and tubulate liposomes containing PI(4,5)P2. Mutations in components of the Pil1-Sle1-Syj1-Tax4 pathway suppress the growth and morphology defects of TORC2 mutants, indicating that eisosome-dependent regulation of PI(4,5)P2 feeds into signal transduction pathways. We propose that the geometry of membrane invaginations generates spatial and temporal signals for lipid-mediated signaling events in cells.

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References

Morales-Johansson H, Jenoe P, Cooke F, Hall M . Negative regulation of phosphatidylinositol 4,5-bisphosphate levels by the INP51-associated proteins TAX4 and IRS4. J Biol Chem. 2004; 279(38):39604-10. DOI: 10.1074/jbc.M405589200. View

Snaith H, Thompson J, Yates 3rd J, Sawin K . Characterization of Mug33 reveals complementary roles for actin cable-dependent transport and exocyst regulators in fission yeast exocytosis. J Cell Sci. 2011; 124(Pt 13):2187-99. PMC: 3113670. DOI: 10.1242/jcs.084038. View

Bahler J, Wu J, Longtine M, Shah N, McKenzie 3rd A, Steever A . Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast. 1998; 14(10):943-51. DOI: 10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y. View

Ikai N, Nakazawa N, Hayashi T, Yanagida M . The reverse, but coordinated, roles of Tor2 (TORC1) and Tor1 (TORC2) kinases for growth, cell cycle and separase-mediated mitosis in Schizosaccharomyces pombe. Open Biol. 2012; 1(3):110007. PMC: 3352084. DOI: 10.1098/rsob.110007. View

Schmidt A, Bickle M, Beck T, Hall M . The yeast phosphatidylinositol kinase homolog TOR2 activates RHO1 and RHO2 via the exchange factor ROM2. Cell. 1997; 88(4):531-42. DOI: 10.1016/s0092-8674(00)81893-0. View

Malinska K, Malinsky J, Opekarova M, Tanner W . Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J Cell Sci. 2004; 117(Pt 25):6031-41. DOI: 10.1242/jcs.01493. View

Walther T, Brickner J, Aguilar P, Bernales S, Pantoja C, Walter P . Eisosomes mark static sites of endocytosis. Nature. 2006; 439(7079):998-1003. DOI: 10.1038/nature04472. View

Schmidt A, Kunz J, Hall M . TOR2 is required for organization of the actin cytoskeleton in yeast. Proc Natl Acad Sci U S A. 1996; 93(24):13780-5. PMC: 19424. DOI: 10.1073/pnas.93.24.13780. View

Olivera-Couto A, Aguilar P . Eisosomes and plasma membrane organization. Mol Genet Genomics. 2012; 287(8):607-20. DOI: 10.1007/s00438-012-0706-8. View

10.

Levin D . Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics. 2011; 189(4):1145-75. PMC: 3241422. DOI: 10.1534/genetics.111.128264. View

11.

Mitra P, Zhang Y, Rameh L, Ivshina M, McCollum D, Nunnari J . A novel phosphatidylinositol(3,4,5)P3 pathway in fission yeast. J Cell Biol. 2004; 166(2):205-11. PMC: 2172303. DOI: 10.1083/jcb.200404150. View

12.

Karotki L, Huiskonen J, Stefan C, Ziolkowska N, Roth R, Surma M . Eisosome proteins assemble into a membrane scaffold. J Cell Biol. 2011; 195(5):889-902. PMC: 3257569. DOI: 10.1083/jcb.201104040. View

13.

Torres J, Di Como C, Herrero E, de la Torre-Ruiz M . Regulation of the cell integrity pathway by rapamycin-sensitive TOR function in budding yeast. J Biol Chem. 2002; 277(45):43495-504. DOI: 10.1074/jbc.M205408200. View

14.

Brach T, Specht T, Kaksonen M . Reassessment of the role of plasma membrane domains in the regulation of vesicular traffic in yeast. J Cell Sci. 2011; 124(Pt 3):328-37. DOI: 10.1242/jcs.078519. View

15.

Moreno S, Klar A, Nurse P . Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991; 194:795-823. DOI: 10.1016/0076-6879(91)94059-l. View

16.

Aguilar P, Frohlich F, Rehman M, Shales M, Ulitsky I, Olivera-Couto A . A plasma-membrane E-MAP reveals links of the eisosome with sphingolipid metabolism and endosomal trafficking. Nat Struct Mol Biol. 2010; 17(7):901-8. PMC: 3073498. DOI: 10.1038/nsmb.1829. View

17.

Ziolkowska N, Karotki L, Rehman M, Huiskonen J, Walther T . Eisosome-driven plasma membrane organization is mediated by BAR domains. Nat Struct Mol Biol. 2011; 18(7):854-6. DOI: 10.1038/nsmb.2080. View

18.

Mayor S . Need tension relief fast? Try caveolae. Cell. 2011; 144(3):323-4. DOI: 10.1016/j.cell.2011.01.018. View

19.

Ryan C, Roguev A, Patrick K, Xu J, Jahari H, Tong Z . Hierarchical modularity and the evolution of genetic interactomes across species. Mol Cell. 2012; 46(5):691-704. PMC: 3380636. DOI: 10.1016/j.molcel.2012.05.028. View

20.

Helliwell S, Schmidt A, Ohya Y, Hall M . The Rho1 effector Pkc1, but not Bni1, mediates signalling from Tor2 to the actin cytoskeleton. Curr Biol. 1998; 8(22):1211-4. DOI: 10.1016/s0960-9822(07)00511-8. View