Eisosomes and plasma Membrane organization

Molecular Genetics and Genomics

Volumn 287, Issue 8, 2012, Pages 607-620

  Olivera Couto, Agustina ^a   Aguilar, Pablo S ^a  

^a INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

Author keywords

Curvature; Fungi; Membrane; Nanodomains; Scaffold

Indexed keywords

MEMBRANE PROTEIN; PROTEIN CAN1; PROTEIN FUR4; PROTEIN LSP1; PROTEIN PIL1; PROTEIN SLM1; PROTEIN SLM2; PROTEIN TAT2; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

BIOGENESIS; CELL MEMBRANE; CELL ORGANELLE; EISOSOME; ENDOCYTOSIS; FUNGAL CELL; GENE DELETION; GENE INTERACTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; YEAST;

CELL MEMBRANE; ENDOCYTOSIS; FUNGI; MEMBRANE MICRODOMAINS; ORGANELLES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

FUNGI;

EID: 84864689387     PISSN: 16174615     EISSN: 16174623     Source Type: Journal    
DOI: 10.1007/s00438-012-0706-8     Document Type: Review

References (101)

1. Aguilar PS, Frohlich F, Rehman M, Shales M, Ulitsky I, Olivera-Couto A, Braberg H, Shamir R, Walter P, Mann M, Ejsing CS, Krogan NJ, Walther TC (2010) A plasma-membrane E-MAP reveals links of the eisosome with sphingolipid metabolism and endosomal trafficking. Nat Struct Mol Biol 17:901-908
2. Alvarez FJ, Douglas LM, Rosebrock A, Konopka JB (2008) The Sur7 protein regulates plasma membrane organization and prevents intracellular cell wall growth in Candida albicans. Mol Biol Cell 19:5214-5225
3. Aronova S, Wedaman K, Aronov PA, Fontes K, Ramos K, Hammock BD, Powers T (2008) Regulation of ceramide biosynthesis by TOR complex 2. Cell Metab 7:148-158
4. Audhya A, Loewith R, Parsons AB, Gao L, Tabuchi M, Zhou H, Boone C, Hall MN, Emr SD (2004) Genome-wide lethality screen identifies new PI4, 5P2 effectors that regulate the actin cytoskeleton. EMBO J 23:3747-3757
5. Bagnat M, Simons K (2002) Cell surface polarization during yeast mating. Proc Natl Acad Sci USA 99:14183-14188
6. Bagnat M, Keranen S, Shevchenko A, Simons K (2000) Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci USA 97:3254-3259
7. Bastiani M, Parton RG (2010) Caveolae at a glance. J Cell Sci 123:3831-3836
8. Berchtold D, Walther TC (2009) TORC2 plasma membrane localization is essential for cell viability and restricted to a distinct domain. Mol Biol Cell 20:1565-1575
9. Berchtold D, Piccolis M, Chiaruttini N, Riezman I, Riezman H, Roux A, Walther TC, Loewith R (2012) Plasma membrane stress induces relocalization of Slm proteins and activation of TORC2 to promote sphingolipid synthesis. Nat Cell Biol 14:542-547
10. Bernardo SM, Lee SA (2010) Candida albicans SUR7 contributes to secretion, biofilm formation, and macrophage killing. BMC Microbiol 10:133
11. Brach T, Specht T, Kaksonen M (2011) Reassessment of the role of plasma membrane domains in the regulation of vesicular traffic in yeast. J Cell Sci 124:328-337
12. Chen L, Davis NG (2000) Recycling of the yeast a-factor receptor. J Cell Biol 151:731-738
13. de Bony J, Lopez A, Gilleron M, Welby M, Laneelle G, Rousseau B, Beaucourt JP, Tocanne JF (1989) Transverse and lateral distribution of phospholipids and glycolipids in the membrane of the bacterium Micrococcus luteus. Biochemistry 28:3728-3737
14. Demel RA, Jansen JW, van Dijck PW, van Deenen LL (1977) The preferential interaction of cholesterol with different classes of phospholipids. Biochim Biophys Acta 465:1-10
15. Deng C, Xiong X, Krutchinsky AN (2009) Unifying fluorescence microscopy and mass spectrometry for studying protein complexes in cells. Mol Cell Proteomics 8:1413-1423
16. Douglas LM, Wang HX, Keppler-Ross S, Dean N, Konopka JB (2012) Sur7 promotes plasma membrane organization and is needed for resistance to stressful conditions and to the invasive growth and virulence of Candida albicans. MBio 3 (1). doi: 10.1128/mBio.00254-11
17. Douglass AD, Vale RD (2005) Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121:937-950
18. Fiedler D, Braberg H, Mehta M, Chechik G, Cagney G, Mukherjee P, Silva AC, Shales M, Collins SR, van Wageningen S, Kemmeren P, Holstege FC, Weissman JS, Keogh MC, Koller D, Shokat KM, Krogan NJ (2009) Functional organization of the S. cerevisiae phosphorylation network. Cell 136:952-963
19. Fishov I, Woldringh CL (1999) Visualization of membrane domains in Escherichia coli. Mol Microbiol 32:1166-1172
20. Friant S, Lombardi R, Schmelzle T, Hall MN, Riezman H (2001) Sphingoid base signaling via Pkh kinases is required for endocytosis in yeast. EMBO J 20:6783-6792
21. Frohlich F, Moreira K, Aguilar PS, Hubner NC, Mann M, Walter P, Walther TC (2009) A genome-wide screen for genes affecting eisosomes reveals Nce102 function in sphingolipid signaling. J Cell Biol 185:1227-1242
22. Galindo A, Hervas-Aguilar A, Rodriguez-Galan O, Vincent O, Arst HN Jr, Tilburn J, Penalva MA (2007) PalC, one of two Bro1 domain proteins in the fungal pH signalling pathway, localizes to cortical structures and binds Vps32. Traffic 8:1346-1364
23. Galindo A, Calcagno-Pizarelli AM, Arst HN Jr, Penalva MA (2012) An ordered pathway for the assembly of ESCRT-containing fungal ambient pH signalling complexes at the plasma membrane. J Cell Sci 125:1784-1795. doi:10.1242/jcs.098897
24. Georgiev AG, Sullivan DP, Kersting MC, Dittman JS, Beh CT, Menon AK (2011) Osh proteins regulate membrane sterol organization but are not required for sterol movement between the ER and PM. Traffic 12:1341-1355
25. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425:737-741
26. Grossmann G, Opekarova M, Malinsky J, Weig-Meckl I, Tanner W (2007) Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J 26:1-8
27. Grossmann G, Malinsky J, Stahlschmidt W, Loibl M, Weig-Meckl I, Frommer WB, Opekarova M, Tanner W (2008) Plasma membrane microdomains regulate turnover of transport proteins in yeast. J Cell Biol 183:1075-1088
28. Guan XL, Souza CM, Pichler H, Dewhurst G, Schaad O, Kajiwara K, Wakabayashi H, Ivanova T, Castillon GA, Piccolis M, Abe F, Loewith R, Funato K, Wenk MR, Riezman H (2009) Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Mol Biol Cell 20:2083-2095
29. Hancock JF (2006) Lipid rafts: contentious only from simplistic standpoints. Nat Rev Mol Cell Biol 7:456-462
30. Hansen CG, Nichols BJ (2010) Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 20:177-186
31. Hayer A, Stoeber M, Bissig C, Helenius A (2010) Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 11:361-382
32. Herrador A, Herranz S, Lara D, Vincent O (2010) Recruitment of the ESCRT machinery to a putative seven-transmembrane-domain receptor is mediated by an arrestin-related protein. Mol Cell Biol 30:897-907
33. Hosiner D, Sponder G, Graschopf A, Reipert S, Schweyen RJ, Schuller C, Aleschko M (2011) Pun1p is a metal ion-inducible, calcineurin/Crz1p-regulated plasma membrane protein required for cell wall integrity. Biochim Biophys Acta 1808:1108-1119
34. Jin H, McCaffery JM, Grote E (2008) Ergosterol promotes pheromone signaling and plasma membrane fusion in mating yeast. J Cell Biol 180:813-826
35. Johannes L, Mayor S (2010) Induced domain formation in endocytic invagination, lipid sorting, and scission. Cell 142:507-510
36. Kabeche R, Baldissard S, Hammond J, Howard L, Moseley JB (2011) The filament-forming protein Pil1 assembles linear eisosomes in fission yeast. Mol Biol Cell 22:4059-4067
37. Kaiser HJ, Orlowski A, Rog T, Nyholm TK, Chai W, Feizi T, Lingwood D, Vattulainen I, Simons K (2011) Lateral sorting in model membranes by cholesterol-mediated hydrophobic matching. Proc Natl Acad Sci USA 108:16628-16633
38. Kaksonen M, Toret CP, Drubin DG (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7:404-414
39. Kamada Y, Fujioka Y, Suzuki NN, Inagaki F, Wullschleger S, Loewith R, Hall MN, Ohsumi Y (2005) Tor2 directly phosphorylates the AGC kinase Ypk2 to regulate actin polarization. Mol Cell Biol 25:7239-7248
40. Kamble C, Jain S, Murphy E, Kim K (2011) Requirements of Slm proteins for proper eisosome organization, endocytic trafficking and recycling in the yeast Saccharomyces cerevisiae. J Biosci 36:79-96
41. Karotki L, Huiskonen JT, Stefan CJ, Ziolkowska NE, Roth R, Surma MA, Krogan NJ, Emr SD, Heuser J, Grunewald K, Walther TC (2011) Eisosome proteins assemble into a membrane scaffold. J Cell Biol 195:889-902
42. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K, Murakoshi H, Kasai RS, Kondo J, Fujiwara T (2005) Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 34:351-378
43. Kusumi A, Suzuki KG, Kasai RS, Ritchie K, Fujiwara TK (2011) Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem Sci 36:604-615
44. Lagorce A, Hauser NC, Labourdette D, Rodriguez C, Martin-Yken H, Arroyo J, Hoheisel JD, Francois J (2003) Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J Biol Chem 278:20345-20357
45. Lauwers E, Andre B (2006) Association of yeast transporters with detergent-resistant membranes correlates with their cell-surface location. Traffic 7:1045-1059
46. London E, Brown DA (2000) Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim Biophys Acta 1508:182-195
47. Lopez D, Kolter R (2010) Functional microdomains in bacterial membranes. Genes Dev 24:1893-1902
48. Luo G, Gruhler A, Liu Y, Jensen ON, Dickson RC (2008) The sphingolipid long-chain base-Pkh1/2-Ypk1/2 signaling pathway regulates eisosome assembly and turnover. J Biol Chem 283:10433-10444
49. Malinska K, Malinsky J, Opekarova M, Tanner W (2003) Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol Biol Cell 14:4427-4436
50. Malinska K, Malinsky J, Opekarova M, Tanner W (2004) Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J Cell Sci 117:6031-6041
51. Markin VS (1981) Lateral organization of membranes and cell shapes. Biophys J 36:1-19
52. Matsumoto K, Kusaka J, Nishibori A, Hara H (2006) Lipid domains in bacterial membranes. Mol Microbiol 61:1110-1117
53. McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438:605-611
54. Moor H, Muhlethaler K (1963) Fine structure in frozen-etched yeast cells. J Cell Biol 17:609-628
55. Moreira KE, Walther TC, Aguilar PS, Walter P (2009) Pil1 controls eisosome biogenesis. Mol Biol Cell 20:809-818
56. Mouritsen OG, Bloom M (1984) Mattress model of lipid-protein interactions in membranes. Biophys J 46:141-153
57. Mueller NS, Wedlich-Soldner R, Spira F (2012) From mosaic to patchwork: Matching lipids and proteins in membrane organization. Mol Membr Biol. doi:10.3109/09687688.2012.687461
58. Mulholland J, Preuss D, Moon A, Wong A, Drubin D, Botstein D (1994) Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J Cell Biol 125:381-391
59. Munro S (2003) Lipid rafts: elusive or illusive? Cell 115:377-388
60. Murphy ER, Boxberger J, Colvin R, Lee SJ, Zahn G, Loor F, Kim K (2011) Pil1, an eisosome organizer, plays an important role in the recruitment of synaptojanins and amphiphysins to facilitate receptor-mediated endocytosis in yeast. Eur J Cell Biol 90:825-833
61. Nakano K, Yamamoto T, Kishimoto T, Noji T, Tanaka K (2008) Protein kinases Fpk1p and Fpk2p are novel regulators of phospholipid asymmetry. Mol Biol Cell 19:1783-1797
62. Niles BJ, Mogri H, Hill A, Vlahakis A, Powers T (2012) Plasma membrane recruitment and activation of the AGC kinase Ypk1 is mediated by target of rapamycin complex 2 (TORC2) and its effector proteins Slm1 and Slm2. Proc Natl Acad Sci USA 109:1536-1541
63. Oh Y, Bi E (2011) Septin structure and function in yeast and beyond. Trends Cell Biol 21:141-148
64. Okuzaki D, Satake W, Hirata A, Nojima H (2003) Fission yeast meu14+ is required for proper nuclear division and accurate forespore membrane formation during meiosis II. J Cell Sci 116:2721-2735
65. Olivera-Couto A, Grana M, Harispe L, Aguilar PS (2011) The eisosome core is composed of BAR domain proteins. Mol Biol Cell 22:2360-2372
66. Penalva MA, Tilburn J, Bignell E, Arst HN Jr (2008) Ambient pH gene regulation in fungi: making connections. Trends Microbiol 16:291-300
67. Poveda JA, Fernandez AM, Encinar JA, Gonzalez-Ros JM (2008) Protein-promoted membrane domains. Biochim Biophys Acta 1778:1583-1590
68. Prosser DC, Drivas TG, Maldonado-Baez L, Wendland B (2011) Existence of a novel clathrin-independent endocytic pathway in yeast that depends on Rho1 and formin. J Cell Biol 195:657-671
69. Rankin BR, Moneron G, Wurm CA, Nelson JC, Walter A, Schwarzer D, Schroeder J, Colon-Ramos DA, Hell SW (2011) Nanoscopy in a living multicellular organism expressing GFP. Biophys J 100:L63-L65
70. Reijnst P, Walther A, Wendland J (2011) Dual-colour fluorescence microscopy using yEmCherry-/GFP-tagging of eisosome components Pil1 and Lsp1 in Candida albicans. Yeast 28:331-338
71. Robinson JM, Karnovsky MJ (1980) Evaluation of the polyene antibiotic filipin as a cytochemical probe for membrane cholesterol. J Histochem Cytochem 28:161-168
72. Roelants FM, Torrance PD, Bezman N, Thorner J (2002) Pkh1 and Pkh2 differentially phosphorylate and activate Ypk1 and Ykr2 and define protein kinase modules required for maintenance of cell wall integrity. Mol Biol Cell 13:3005-3028
73. Roelants FM, Baltz AG, Trott AE, Fereres S, Thorner J (2010) A protein kinase network regulates the function of aminophospholipid flippases. Proc Natl Acad Sci USA 107:34-39
74. Roux A, Cuvelier D, Nassoy P, Prost J, Bassereau P, Goud B (2005) Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J 24:1537-1545
75. Schroeder RJ, Ahmed SN, Zhu Y, London E, Brown DA (1998) Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J Biol Chem 273:1150-1157
76. Schuck S, Honsho M, Ekroos K, Shevchenko A, Simons K (2003) Resistance of cell membranes to different detergents. Proc Natl Acad Sci USA 100:5795-5800
77. Seger S, Rischatsch R, Philippsen P (2011) Formation and stability of eisosomes in the filamentous fungus Ashbya gossypii. J Cell Sci 124:1629-1634
78. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569-572
79. Simons K, Sampaio JL (2011) Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol 3:a004697
80. Sivadon P, Peypouquet MF, Doignon F, Aigle M, Crouzet M (1997) Cloning of the multicopy suppressor gene SUR7: evidence for a functional relationship between the yeast actin-binding protein Rvs167 and a putative membranous protein. Yeast 13:747-761
81. Snaith HA, Thompson J, Yates JR 3rd, Sawin KE (2011) Characterization of Mug33 reveals complementary roles for actin cabledependent transport and exocyst regulators in fission yeast exocytosis. J Cell Sci 124:2187-2199
82. Sorre B, Callan-Jones A, Manneville JB, Nassoy P, Joanny JF, Prost J, Goud B, Bassereau P (2009) Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proc Natl Acad Sci USA 106:5622-5626
83. Spira F, Mueller NS, Beck G, von Olshausen P, Beig J, Wedlich-Soldner R (2012) Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat Cell Biol 14(6):640-648. doi:10.1038/ncb2487
84. Stradalova V, Stahlschmidt W, Grossmann G, Blazikova M, Rachel R, Tanner W, Malinsky J (2009) Furrow-like invaginations of the yeast plasma membrane correspond to membrane compartment of Can1. J Cell Sci 122:2887-2894
85. Streiblova E (1968) Surface structure of yeast protoplasts. J Bacteriol 95:700-707
86. Sun Y, Taniguchi R, Tanoue D, Yamaji T, Takematsu H, Mori K, Fujita T, Kawasaki T, Kozutsumi Y (2000) Sli2 (Ypk1), a homologue of mammalian protein kinase SGK, is a downstream kinase in the sphingolipid-mediated signaling pathway of yeast. Mol Cell Biol 20:4411-4419
87. Tabuchi M, Audhya A, Parsons AB, Boone C, Emr SD (2006) The phosphatidylinositol 4, 5-biphosphate and TORC2 binding proteins Slm1 and Slm2 function in sphingolipid regulation. Mol Cell Biol 26:5861-5875
88. Takeo K (1984) Lack of invaginations of the plasma membrane during budding and cell division of Saccharomyces cerevisiae and Schizosaccharomyces pombe. FEMS Microbiol Lett 22:97-100
89. Tanos B, Rodriguez-Boulan E (2008) The epithelial polarity program: machineries involved and their hijacking by cancer. Oncogene 27:6939-6957
90. Valdez-Taubas J, Pelham HR (2003) Slow diffusion of proteins in the yeast plasma membrane allows polarity to be maintained by endocytic cycling. Curr Biol 13:1636-1640
91. van Meer G, Stelzer EH, Wijnaendts-van-Resandt RW, Simons K (1987) Sorting of sphingolipids in epithelial (Madin-Darby canine kidney) cells. J Cell Biol 105:1623-1635
92. Vangelatos I, Roumelioti K, Gournas C, Suarez T, Scazzocchio C, Sophianopoulou V (2010) Eisosome organization in the filamentous ascomycete Aspergillus nidulans. Eukaryot Cell 9:1441-1454
93. Walther TC, Brickner JH, Aguilar PS, Bernales S, Pantoja C, Walter P (2006) Eisosomes mark static sites of endocytosis. Nature 439:998-1003
94. Walther TC, Aguilar PS, Frohlich F, Chu F, Moreira K, Burlingame AL, Walter P (2007) Pkh-kinases control eisosome assembly and organization. EMBO J 26:4946-4955
95. Wang HX, Douglas LM, Aimanianda V, Latge JP, Konopka JB (2011) The Candida albicans Sur7 protein is needed for proper synthesis of the fibrillar component of the cell wall that confers strength. Eukaryot Cell 10:72-80
96. Xu T, Shively CA, Jin R, Eckwahl MJ, Dobry CJ, Song Q, Kumar A (2010) A profile of differentially abundant proteins at the yeast cell periphery during pseudohyphal growth. J Biol Chem 285:15476-15488
97. Young ME, Karpova TS, Brugger B, Moschenross DM, Wang GK, Schneiter R, Wieland FT, Cooper JA (2002) The Sur7p family defines novel cortical domains in Saccharomyces cerevisiae, affects sphingolipid metabolism, and is involved in sporulation. Mol Cell Biol 22:927-934
98. Yu JW, Mendrola JM, Audhya A, Singh S, Keleti D, De Wald DB, Murray D, Emr SD, Lemmon MA (2004) Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol Cell 13:677-688
99. Zhang X, Lester RL, Dickson RC (2004) Pil1p and Lsp1p negatively regulate the 3-phosphoinositide-dependent protein kinase-like kinase Pkh1p and downstream signaling pathways Pkc1p and Ypk1p. J Biol Chem 279:22030-22038
100. Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7:9-19
101. Ziolkowska NE, Karotki L, Rehman M, Huiskonen JT, Walther TC (2011) Eisosome-driven plasma membrane organization is mediated by BAR domains. Nat Struct Mol Biol 18:854-856