1932

Abstract

The fungal plasma membrane is organized into specialized domains that vary in size, stability, and composition. Membrane compartment of Can1(MCC)/eisosome domains that were recently discovered in the budding yeast are interesting because they represent a novel type of membrane domain that is important for plasma membrane organization, sphingolipid homeostasis, and cell wall morphogenesis. The MCC portion was identified as stable punctate patches that correspond to furrows in the plasma membrane that are about 300 nm long and 50 nm deep. These domains contain integral membrane proteins, including the tetraspan proteins Sur7 and Nce102. The eisosome portion includes proteins peripherally associated with the cytoplasmic side of the MCC, including the Bin/amphiphysin/Rvs-domain proteins Pil1 and Lsp1, which assemble into filaments that curve the membrane to form the furrows. By comparing MCC/eisosome domains in diverse fungi, researchers are identifying common features that further our understanding of their unique biogenesis, structure, and function.

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2014-09-08
2024-05-23
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Literature Cited

  1. Aguilar PS, Frohlich F, Rehman M, Shales M, Ulitsky I. 1.  et al. 2010. A plasma-membrane E-MAP reveals links of the eisosome with sphingolipid metabolism and endosomal trafficking. Nat. Struct. Mol. Biol. 17:901–8 [Google Scholar]
  2. Alvarez FJ, Douglas LM, Konopka JB. 2.  2007. Sterol-rich plasma membrane domains in fungi. Eukaryot. Cell 6:755–63 [Google Scholar]
  3. Alvarez FJ, Douglas LM, Konopka JB. 3.  2009. The Sur7 protein resides in punctate membrane subdomains and mediates spatial regulation of cell wall synthesis in Candida albicans. Commun. Integr. Biol. 2:76–77 [Google Scholar]
  4. Alvarez FJ, Douglas LM, Rosebrock A, Konopka JB. 4.  2008. The Sur7 protein regulates plasma membrane organization and prevents intracellular cell wall growth in Candida albicans. Mol. Biol. Cell 19:5214–25Analysis of Sur7 in C. albicans revealed roles in cell wall and PM organization. [Google Scholar]
  5. Athanasopoulos A, Boleti H, Scazzocchio C, Sophianopoulou V. 5.  2013. Eisosome distribution and localization in the meiotic progeny of Aspergillus nidulans. Fungal Genet. Biol. 53:84–96 [Google Scholar]
  6. Badrane H, Nguyen MH, Blankenship JR, Cheng S, Hao B. 6.  et al. 2012. Rapid redistribution of phosphatidylinositol-(4,5)-bisphosphate and septins during the Candida albicans response to caspofungin. Antimicrob. Agents Chemother. 56:4614–24 [Google Scholar]
  7. Barug D, de Groot K. 7.  1985. Effect of the imidazole derivative lombazole on the ultrastructure of Staphylococcus epidermidis and Candida albicans. Antimicrob. Agents Chemother. 28:643–47 [Google Scholar]
  8. Baxter BK, Didone L, Oga D, Schor S, Krysan DJ. 8.  2011. Identification, in vitro activity and mode of action of phosphoinositide-dependent-1 kinase inhibitors as antifungal molecules. ACS Chem. Biol. 6:502–10 [Google Scholar]
  9. Berchtold D, Piccolis M, Chiaruttini N, Riezman I, Riezman H. 9.  et al. 2012. Plasma membrane stress induces relocalization of Slm proteins and activation of TORC2 to promote sphingolipid synthesis. Nat. Cell Biol. 14:542–47 [Google Scholar]
  10. Berchtold D, Walther TC. 10.  2009. TORC2 plasma membrane localization is essential for cell viability and restricted to a distinct domain. Mol. Biol. Cell 20:1565–75 [Google Scholar]
  11. Bernardo SM, Lee SA. 11.  2010. Candida albicans SUR7 contributes to secretion, biofilm formation, and macrophage killing. BMC Microbiol. 10:133 doi: 10.1186/1471-2180-10-133 [Google Scholar]
  12. Brach T, Specht T, Kaksonen M. 12.  2011. Reassessment of the role of plasma membrane domains in the regulation of vesicular traffic in yeast. J. Cell Sci. 124:328–37 [Google Scholar]
  13. Breslow DK, Collins SR, Bodenmiller B, Aebersold R, Simons K. 13.  et al. 2010. Orm family proteins mediate sphingolipid homeostasis. Nature 463:1048–53 [Google Scholar]
  14. Buser C, Drubin DG. 14.  2013. Ultrastructural imaging of endocytic sites in Saccharomyces cerevisiae by transmission electron microscopy and immunolabeling. Microsc. Microanal. 19:381–92 [Google Scholar]
  15. Caudron F, Barral Y. 15.  2009. Septins and the lateral compartmentalization of eukaryotic membranes. Dev. Cell 16:493–506 [Google Scholar]
  16. deHart AK, Schnell JD, Allen DA, Hicke L. 16.  2002. The conserved Pkh-Ypk kinase cascade is required for endocytosis in yeast. J. Cell Biol. 156:241–48 [Google Scholar]
  17. Deng C, Xiong X, Krutchinsky AN. 17.  2009. Unifying fluorescence microscopy and mass spectrometry for studying protein complexes in cells. Mol. Cell Proteomics 8:1413–23 [Google Scholar]
  18. Dickson RC, Sumanasekera C, Lester RL. 18.  2006. Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog. Lipid Res. 45:447–65 [Google Scholar]
  19. Douglas LM, Alvarez FJ, McCreary C, Konopka JB. 19.  2005. Septin function in yeast model systems and pathogenic fungi. Eukaryot. Cell 4:1503–12 [Google Scholar]
  20. Douglas LM, Wang HX, Keppler-Ross S, Dean N, Konopka JB. 20.  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:e00254–11 [Google Scholar]
  21. Douglas LM, Wang HX, Konopka JB. 21.  2013. The MARVEL domain protein Nce102 regulates actin organization and invasive growth of Candida albicans. mBio 4:e00723–13 [Google Scholar]
  22. Douglas LM, Wang HX, Li L, Konopka JB. 22.  2011. Membrane compartment occupied by Can1 (MCC) and eisosome subdomains of the fungal plasma membrane. Membranes 1:394–411 [Google Scholar]
  23. Drgonova J, Drgon T, Tanaka K, Kollar R, Chen GC. 23.  et al. 1996. Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272:277–79 [Google Scholar]
  24. Dujon B. 24.  2006. Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet. 22:375–87 [Google Scholar]
  25. Dupont S, Beney L, Ritt JF, Lherminier J, Gervais P. 25.  2010. Lateral reorganization of plasma membrane is involved in the yeast resistance to severe dehydration. Biochim. Biophys. Acta 1798:975–85 [Google Scholar]
  26. Epstein S, Riezman H. 26.  2013. Sphingolipid signaling in yeast: potential implications for understanding disease. Front. Biosci. 5:97–108 [Google Scholar]
  27. Fadri M, Daquinag A, Wang S, Xue T, Kunz J. 27.  2005. The pleckstrin homology domain proteins Slm1 and Slm2 are required for actin cytoskeleton organization in yeast and bind phosphatidylinositol-4,5-bisphosphate and TORC2. Mol. Biol. Cell 16:1883–900 [Google Scholar]
  28. Frohlich F, Moreira K, Aguilar PS, Hubner NC, Mann M. 28.  et al. 2009. A genome-wide screen for genes affecting eisosomes reveals Nce102 function in sphingolipid signaling. J. Cell Biol. 185:1227–42 [Google Scholar]
  29. Furuse M, Tsukita S. 29.  2006. Claudins in occluding junctions of humans and flies. Trends Cell Biol. 16:181–88 [Google Scholar]
  30. Gervasio OL, Phillips WD, Cole L, Allen DG. 30.  2011. Caveolae respond to cell stretch and contribute to stretch-induced signaling. J. Cell Sci. 124:3581–90 [Google Scholar]
  31. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A. 31.  et al. 2003. Global analysis of protein expression in yeast. Nature 425:737–41 [Google Scholar]
  32. Gross H, Kuebler O, Bas E, Moor H. 32.  1978. Decoration of specific sites on freeze-fractured membranes. J. Cell Biol. 79:646–56 [Google Scholar]
  33. Grossmann G, Malinsky J, Stahlschmidt W, Loibl M, Weig-Meckl I. 33.  et al. 2008. Plasma membrane microdomains regulate turnover of transport proteins in yeast. J. Cell Biol. 183:1075–88 [Google Scholar]
  34. Grossmann G, Opekarova M, Malinsky J, Weig-Meckl I, Tanner W. 34.  2007. Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J. 26:1–8Revealed a distinct lipid composition in MCC domains. [Google Scholar]
  35. Guan XL, Souza CM, Pichler H, Dewhurst G, Schaad O. 35.  et al. 2009. Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Mol. Biol. Cell 20:2083–95 [Google Scholar]
  36. Han S, Lone MA, Schneiter R, Chang A. 36.  2010. Orm1 and Orm2 are conserved endoplasmic reticulum membrane proteins regulating lipid homeostasis and protein quality control. Proc. Natl. Acad. Sci. USA 107:5851–56 [Google Scholar]
  37. Heitman J, Filler SG, Edwards JEJ, Mitchell AP. 37.  2006. Molecular Principles of Fungal Pathogenesis Washington, DC: ASM
  38. Hemler ME. 38.  2005. Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 6:801–11 [Google Scholar]
  39. Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L. 39.  et al. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180–83 [Google Scholar]
  40. Hosiner D, Sponder G, Graschopf A, Reipert S, Schweyen RJ. 40.  et al. 2011. Pun1p is a metal ion-inducible, calcineurin/Crz1p-regulated plasma membrane protein required for cell wall integrity. Biochim. Biophys. Acta 1808:1108–19 [Google Scholar]
  41. Jin H, McCaffery JM, Grote E. 41.  2008. Ergosterol promotes pheromone signaling and plasma membrane fusion in mating yeast. J. Cell Biol. 180:813–26 [Google Scholar]
  42. Kabeche R, Baldissard S, Hammond J, Howard L, Moseley JB. 42.  2011. The filament-forming protein Pil1 assembles linear eisosomes in fission yeast. Mol. Biol. Cell 22:4059–67Identified unique properties of eisosomes in fission yeast S. pombe. [Google Scholar]
  43. Kabeche R, Roguev A, Krogan NJ, Moseley JB. 43.  2014. A Pil1-Sle1-Syj1-Tax4 functional pathway links eisosomes with PI(4,5)P2 regulation. J. Cell Sci. 127:1318–26 [Google Scholar]
  44. Kamble C, Jain S, Murphy E, Kim K. 44.  2011. Requirements of Slm proteins for proper eisosome organization, endocytic trafficking and recycling in the yeast Saccharomyces cerevisiae. J. Biosci. 36:79–96 [Google Scholar]
  45. Karotki L, Huiskonen JT, Stefan CJ, Ziolkowska NE, Roth R. 45.  et al. 2011. Eisosome proteins assemble into a membrane scaffold. J. Cell Biol. 195:889–902Determined structure of eisosomes and proposed a model for their formation. [Google Scholar]
  46. Khalaj V, Azizi M, Enayati S, Khorasanizadeh D, Ardakani EM. 46.  2012. NCE102 homologue in Aspergillus fumigatus is required for normal sporulation, not hyphal growth or pathogenesis. FEMS Microbiol. Lett. 329:138–45 [Google Scholar]
  47. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X. 47.  et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440:637–43 [Google Scholar]
  48. Lauss M, Kriegner A, Vierlinger K, Noehammer C. 48.  2007. Characterization of the drugged human genome. Pharmacogenomics 8:1063–73 [Google Scholar]
  49. Loibl M, Grossmann G, Stradalova V, Klingl A, Rachel R. 49.  et al. 2010. C terminus of Nce102 determines the structure and function of microdomains in the Saccharomyces cerevisiae plasma membrane. Eukaryot. Cell 9:1184–92 [Google Scholar]
  50. Luo G, Costanzo M, Boone C, Dickson RC. 50.  2011. Nutrients and the Pkh1/2 and Pkc1 protein kinases control mRNA decay and P-body assembly in yeast. J. Biol. Chem. 286:8759–70 [Google Scholar]
  51. Luo G, Gruhler A, Liu Y, Jensen ON, Dickson RC. 51.  2008. The sphingolipid long-chain base-Pkh1/2-Ypk1/2 signaling pathway regulates eisosome assembly and turnover. J. Biol. Chem. 283:10433–44 [Google Scholar]
  52. Malinska K, Malinsky J, Opekarova M, Tanner W. 52.  2003. Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol. Biol. Cell 14:4427–36Discovery of MCC as a special PM domain. [Google Scholar]
  53. Malinska K, Malinsky J, Opekarova M, Tanner W. 53.  2004. Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J. Cell Sci. 117:6031–41 [Google Scholar]
  54. Malinsky J, Opekarova M, Tanner W. 54.  2010. The lateral compartmentation of the yeast plasma membrane. Yeast 27:473–78 [Google Scholar]
  55. Martin SW, Konopka JB. 55.  2004. Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot. Cell 3:675–84 [Google Scholar]
  56. Martinez MJ, Roy S, Archuletta AB, Wentzell PD, Anna-Arriola SS. 56.  et al. 2004. Genomic analysis of stationary-phase and exit in Saccharomyces cerevisiae: gene expression and identification of novel essential genes. Mol. Biol. Cell 15:5295–305 [Google Scholar]
  57. Mascaraque V, Hernáez ML, Jiménez-Sánchez M, Hansen R, Gil C. 57.  et al. 2013. Phosphoproteomic analysis of protein kinase C signaling in Saccharomyces cerevisiae reveals Slt2 mitogen-activated protein kinase (MAPK)-dependent phosphorylation of eisosome core components. Mol. Cell Proteomics 12:557–74 [Google Scholar]
  58. Moor H, Muhlethaler K. 58.  1963. Fine structure in frozen-etched yeast cells. J. Cell Biol. 17:609–28 [Google Scholar]
  59. Moreira KE, Schuck S, Schrul B, Frohlich F, Moseley JB. 59.  et al. 2012. Seg1 controls eisosome assembly and shape. J. Cell Biol. 198:405–20 [Google Scholar]
  60. Moreira KE, Walther TC, Aguilar PS, Walter P. 60.  2009. Pil1 controls eisosome biogenesis. Mol. Biol. Cell 20:809–18 [Google Scholar]
  61. Mulholland J, Preuss D, Moon A, Wong A, Drubin D, Botstein D. 61.  1994. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J. Cell Biol. 125:381–91 [Google Scholar]
  62. Munro S. 62.  2003. Lipid rafts: elusive or illusive?. Cell 115:377–88 [Google Scholar]
  63. Murphy ER, Boxberger J, Colvin R, Lee SJ, Zahn G. 63.  et al. 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. 90:825–33 [Google Scholar]
  64. Murphy ER, Kim KT. 64.  2012. Insights into eisosome assembly and organization. J. Biosci. 37:295–300 [Google Scholar]
  65. Niles BJ, Mogri H, Hill A, Vlahakis A, Powers T. 65.  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 109:1536–41 [Google Scholar]
  66. Niles BJ, Powers T. 66.  2012. Plasma membrane proteins Slm1 and Slm2 mediate activation of the AGC kinase Ypk1 by TORC2 and sphingolipids in S. cerevisiae.. Cell Cycle 11:3745–49 [Google Scholar]
  67. Obara K, Yamamoto H, Kihara A. 67.  2012. Membrane protein Rim21 plays a central role in sensing ambient pH in Saccharomyces cerevisiae. J. Biol. Chem. 287:38473–81 [Google Scholar]
  68. Odds FC. 68.  1988. Candida and Candidosis Philadelphia: Bailliere Tindall
  69. Odds FC, Brown AJ, Gow NA. 69.  2003. Antifungal agents: mechanisms of action. Trends Microbiol. 11:272–79 [Google Scholar]
  70. Oh Y, Bi E. 70.  2011. Septin structure and function in yeast and beyond. Trends Cell Biol. 21:141–48 [Google Scholar]
  71. Okuzaki D, Satake W, Hirata A, Nojima H. 71.  2003. Fission yeast meu14+ is required for proper nuclear division and accurate forespore membrane formation during meiosis II. J. Cell Sci. 116:2721–35 [Google Scholar]
  72. Olivera-Couto A, Aguilar PS. 72.  2012. Eisosomes and plasma membrane organization. Mol. Genet. Genomics 287:607–20 [Google Scholar]
  73. Olivera-Couto A, Grana M, Harispe L, Aguilar PS. 73.  2011. The eisosome core is composed of BAR domain proteins. Mol. Biol. Cell 22:2360–72 [Google Scholar]
  74. Pfaller MA, Diekema DJ. 74.  2010. Epidemiology of invasive mycoses in North America. Crit. Rev. Microbiol. 36:1–53 [Google Scholar]
  75. Qadota H, Python CP, Inoue SB, Arisawa M, Anraku Y. 75.  et al. 1996. Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-β-glucan synthase. Science 272:279–81 [Google Scholar]
  76. Reijnst P, Walther A, Wendland J. 76.  2011. Dual-colour fluorescence microscopy using yEmCherry-/GFP-tagging of eisosome components Pil1 and Lsp1 in Candida albicans. Yeast 28:331–38 [Google Scholar]
  77. Roelants FM, Breslow DK, Muir A, Weissman JS, Thorner J. 77.  2011. Protein kinase Ypk1 phosphorylates regulatory proteins Orm1 and Orm2 to control sphingolipid homeostasis in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 108:19222–27 [Google Scholar]
  78. Roh DH, Bowers B, Schmidt M, Cabib E. 78.  2002. The septation apparatus, an autonomous system in budding yeast. Mol. Biol. Cell 13:2747–59 [Google Scholar]
  79. Schmidt M, Varma A, Drgon T, Bowers B, Cabib E. 79.  2003. Septins, under Cla4p regulation, and the chitin ring are required for neck integrity in budding yeast. Mol. Biol. Cell 14:2128–41 [Google Scholar]
  80. Seger S, Rischatsch R, Philippsen P. 80.  2011. Formation and stability of eisosomes in the filamentous fungus Ashbya gossypii. J. Cell Sci. 124:1629–34 [Google Scholar]
  81. Sivadon P, Peypouquet MF, Doignon F, Aigle M, Crouzet M. 81.  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 13:747–61 [Google Scholar]
  82. Smith AE, Zhang Z, Thomas CR, Moxham KE, Middelberg AP. 82.  2000. The mechanical properties of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 97:9871–74 [Google Scholar]
  83. Snaith HA, Thompson J, Yates JR 3rd, Sawin KE. 83.  2011. Characterization of Mug33 reveals complementary roles for actin cable-dependent transport and exocyst regulators in fission yeast exocytosis. J. Cell Sci. 124:2187–99 [Google Scholar]
  84. Spira F, Mueller NS, Beck G, von Olshausen P, Beig J, Wedlich-Soldner R. 84.  2012. Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat. Cell Biol. 14:640–48 [Google Scholar]
  85. Stradalova V, Stahlschmidt W, Grossmann G, Blazikova M, Rachel R. 85.  et al. 2009. Furrow-like invaginations of the yeast plasma membrane correspond to membrane compartment of Can1. J. Cell Sci. 122:2887–94Discovery that MCC/eisosome domains correspond to furrows in the PM. [Google Scholar]
  86. Sudbery PE. 86.  2011. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9:737–48 [Google Scholar]
  87. Sun Y, Carroll S, Kaksonen M, Toshima JY, Drubin DG. 87.  2007. PtdIns(4,5)P2 turnover is required for multiple stages during clathrin- and actin-dependent endocytic internalization. J. Cell Biol. 177:355–67 [Google Scholar]
  88. Sun Y, Miao Y, Yamane Y, Zhang C, Shokat KM. 88.  et al. 2012. Orm protein phosphoregulation mediates transient sphingolipid biosynthesis response to heat stress via the Pkh-Ypk and Cdc55-PP2A pathways. Mol. Biol. Cell 23:2388–98 [Google Scholar]
  89. Swain E, Baudry K, Stukey J, McDonough V, Germann M, Nickels JT Jr. 89.  2002. Sterol-dependent regulation of sphingolipid metabolism in Saccharomyces cerevisiae. J. Biol. Chem. 277:26177–84 [Google Scholar]
  90. Takeo K. 90.  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 [Google Scholar]
  91. Utsugi T, Minemura M, Hirata A, Abe M, Watanabe D, Ohya Y. 91.  2002. Movement of yeast 1,3-β-glucan synthase is essential for uniform cell wall synthesis. Genes Cells 7:1–9 [Google Scholar]
  92. Vangelatos I, Roumelioti K, Gournas C, Suarez T, Scazzocchio C, Sophianopoulou V. 92.  2010. Eisosome organization in the filamentous ascomycete Aspergillus nidulans. Eukaryot. Cell 9:1441–54 [Google Scholar]
  93. Vernay A, Schaub S, Guillas I, Bassilana M, Arkowitz RA. 93.  2012. A steep phosphoinositide bis-phosphate gradient forms during fungal filamentous growth. J. Cell Biol. 198:711–30 [Google Scholar]
  94. Walther TC, Aguilar PS, Frohlich F, Chu F, Moreira K. 94.  et al. 2007. Pkh-kinases control eisosome assembly and organization. EMBO J. 26:4946–55 [Google Scholar]
  95. Walther TC, Brickner JH, Aguilar PS, Bernales S, Pantoja C, Walter P. 95.  2006. Eisosomes mark static sites of endocytosis. Nature 439:998–1003Demonstrated that Pil1 and Lsp1 form eisosomes that underlie the MCC. [Google Scholar]
  96. Wang HX, Douglas LM, Aimanianda V, Latge JP, Konopka JB. 96.  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 [Google Scholar]
  97. Warenda AJ, Konopka JB. 97.  2002. Septin function in Candida albicans morphogenesis. Mol. Biol. Cell 13:2732–46 [Google Scholar]
  98. Xu T, Shively CA, Jin R, Eckwahl MJ, Dobry CJ. 98.  et al. 2010. A profile of differentially abundant proteins at the yeast cell periphery during pseudohyphal growth. J. Biol. Chem. 285:15476–88 [Google Scholar]
  99. Xu Z, Wei W, Gagneur J, Clauder-Münster S, Smolik M. 99.  et al. 2011. Antisense expression increases gene expression variability and locus interdependency. Mol. Syst. Biol. 7:468 [Google Scholar]
  100. Yoshikawa K, Tanaka T, Furusawa C, Nagahisa K, Hirasawa T, Shimizu H. 100.  2009. Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS Yeast Res. 9:32–44 [Google Scholar]
  101. Young ME, Karpova TS, Brugger B, Moschenross DM, Wang GK. 101.  et al. 2002. The Sur7p family defines novel cortical domains in Saccharomyces cerevisiae, affects sphingolipid metabolism, and is involved in sporulation. Mol. Cell. Biol. 22:927–34 [Google Scholar]
  102. Yu H, Braun P, Yildirim MA, Lemmens I, Venkatesan K. 102.  et al. 2008. High-quality binary protein interaction map of the yeast interactome network. Science 322:104–10 [Google Scholar]
  103. Zhang X, Lester RL, Dickson RC. 103.  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. 279:22030–38 [Google Scholar]
  104. Zhao H, Michelot A, Koskela EV, Tkach V, Stamou D. 104.  et al. 2013. Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep. 4:1213–23 [Google Scholar]
  105. Zimmerberg J, McLaughlin S. 105.  2004. Membrane curvature: how BAR domains bend bilayers. Curr. Biol. 14:R250–52 [Google Scholar]
  106. Ziolkowska NE, Christiano R, Walther TC. 106.  2012. Organized living: formation mechanisms and functions of plasma membrane domains in yeast. Trends Cell Biol. 22:151–58 [Google Scholar]
  107. Ziolkowska NE, Karotki L, Rehman M, Huiskonen JT, Walther TC. 107.  2011. Eisosome-driven plasma membrane organization is mediated by BAR domains. Nat. Struct. Mol. Biol. 18:854–56Crystal structure revealed Lsp1 forms a BAR domain, which suggested a mechanism for eisosome formation. [Google Scholar]
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