1932

Abstract

The endoplasmic reticulum (ER) has a broad localization throughout the cell and forms direct physical contacts with all other classes of membranous organelles, including the plasma membrane (PM). A number of protein tethers that mediate these contacts have been identified, and study of these protein tethers has revealed a multiplicity of roles in cell physiology, including regulation of intracellular Ca2+ dynamics and signaling as well as control of lipid traffic and homeostasis. In this review, we discuss the cross talk between the ER and the PM mediated by direct contacts. We review factors that tether the two membranes, their properties, and their dynamics in response to the functional state of the cell. We focus in particular on the role of ER–PM contacts in nonvesicular lipid transport between the two bilayers mediated by lipid transfer proteins.

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2017-06-20
2024-06-24
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Literature Cited

  1. Prinz WA. 1.  2014. Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J. Cell Biol. 205:759–69 [Google Scholar]
  2. Phillips MJ, Voeltz GK. 2.  2016. Structure and function of ER membrane contact sites with other organelles. Nat. Rev. Mol. Cell Biol. 17:69–82 [Google Scholar]
  3. Holthuis JC, Levine TP. 3.  2005. Lipid traffic: floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 6:209–20 [Google Scholar]
  4. Gallo A, Vannier C, Galli T. 4.  2016. Endoplasmic reticulum–plasma membrane associations: structures and functions. Annu. Rev. Cell Dev. Biol. 32:279–301 [Google Scholar]
  5. Stefan CJ, Manford AG, Emr SD. 5.  2013. ER-PM connections: sites of information transfer and inter-organelle communication. Curr. Opin. Cell Biol. 25:434–42 [Google Scholar]
  6. Metuzals J, Chang D, Hammar K, Reese TS. 6.  1997. Organization of the cortical endoplasmic reticulum in the squid giant axon. J. Neurocytol. 26:529–39 [Google Scholar]
  7. West M, Zurek N, Hoenger A, Voeltz GK. 7.  2011. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J. Cell Biol. 193:333–46 [Google Scholar]
  8. Porter KR, Palade GE. 8.  1957. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J. Biophys. Biochem. Cytol. 3:269–300 [Google Scholar]
  9. Rosenbluth J. 9.  1962. Subsurface cisterns and their relationship to the neuronal plasma membrane. J. Cell Biol. 13:405–21 [Google Scholar]
  10. Orci L, Ravazzola M, Le Coadic M, Shen WW, Demaurex N, Cosson P. 10.  2009. STIM1-induced precortical and cortical subdomains of the endoplasmic reticulum. PNAS 106:19358–62 [Google Scholar]
  11. Fernández-Busnadiego R, Saheki Y, De Camilli P. 11.  2015. Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum–plasma membrane contact sites. PNAS 112:E2004–13 [Google Scholar]
  12. Carrasco S, Meyer T. 12.  2011. STIM proteins and the endoplasmic reticulum–plasma membrane junctions. Annu. Rev. Biochem. 80:973–1000 [Google Scholar]
  13. Franzini-Armstrong C, Jorgensen AO. 13.  1994. Structure and development of E-C coupling units in skeletal muscle. Annu. Rev. Physiol. 56:509–34 [Google Scholar]
  14. Hogan PG, Rao A. 14.  2015. Store-operated calcium entry: mechanisms and modulation. Biochem. Biophys. Res. Commun. 460:40–49 [Google Scholar]
  15. Prakriya M, Lewis RS. 15.  2015. Store-operated calcium channels. Physiol. Rev. 95:1383–436 [Google Scholar]
  16. Schneider MF, Chandler WK. 16.  1973. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature 242:244–46 [Google Scholar]
  17. Endo M. 17.  2009. Calcium-induced calcium release in skeletal muscle. Physiol. Rev. 89:1153–76 [Google Scholar]
  18. Landstrom AP, Beavers DL, Wehrens XH. 18.  2014. The junctophilin family of proteins: from bench to bedside. Trends Mol. Med. 20:353–62 [Google Scholar]
  19. Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K. 19.  2000. Junctophilins: a novel family of junctional membrane complex proteins. Mol. Cell 6:11–22 [Google Scholar]
  20. Golini L, Chouabe C, Berthier C, Cusimano V, Fornaro M. 20.  et al. 2011. Junctophilin 1 and 2 proteins interact with the L-type Ca2+ channel dihydropyridine receptors (DHPRs) in skeletal muscle. J. Biol. Chem. 286:43717–25 [Google Scholar]
  21. Kakizawa S, Kishimoto Y, Hashimoto K, Miyazaki T, Furutani K. 21.  et al. 2007. Junctophilin-mediated channel crosstalk essential for cerebellar synaptic plasticity. EMBO J 26:1924–33 [Google Scholar]
  22. Fagni L, Chavis P, Ango F, Bockaert J. 22.  2000. Complex interactions between mGluRs, intracellular Ca2+ stores and ion channels in neurons. Trends Neurosci 23:80–88 [Google Scholar]
  23. Moriguchi S, Nishi M, Komazaki S, Sakagami H, Miyazaki T. 23.  et al. 2006. Functional uncoupling between Ca2+ release and after hyperpolarization in mutant hippocampal neurons lacking junctophilins. PNAS 103:10811–16 [Google Scholar]
  24. Holmes SE, O'Hearn E, Rosenblatt A, Callahan C, Hwang HS. 24.  et al. 2001. A repeat expansion in the gene encoding junctophilin-3 is associated with Huntington disease-like 2. Nat. Genet. 29:377–78 [Google Scholar]
  25. Putney JW Jr. 25.  1986. A model for receptor-regulated calcium entry. Cell Calcium 7:1–12 [Google Scholar]
  26. Hoth M, Penner R. 26.  1992. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355:353–56 [Google Scholar]
  27. Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M. 27.  et al. 2005. STIM1, an essential and conserved component of store-operated Ca2+ channel function. J. Cell Biol. 169:435–45 [Google Scholar]
  28. Liou J, Kim ML, Heo WD, Jones JT, Myers JW. 28.  et al. 2005. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr. Biol. 15:1235–41 [Google Scholar]
  29. Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ. 29.  et al. 2005. STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902–5 [Google Scholar]
  30. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH. 30.  et al. 2006. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–85 [Google Scholar]
  31. Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D. 31.  et al. 2006. CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312:1220–23 [Google Scholar]
  32. Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O. 32.  et al. 2006. Genome-wide RNAi screen of Ca2+ influx identifies genes that regulate Ca2+ release-activated Ca2+ channel activity. PNAS 103:9357–62 [Google Scholar]
  33. Nakatsu F, Baskin JM, Chung J, Tanner LB, Shui G. 33.  et al. 2012. PtdIns4P synthesis by PI4KIIIα at the plasma membrane and its impact on plasma membrane identity. J. Cell Biol. 199:1003–16 [Google Scholar]
  34. Korzeniowski MK, Popovic MA, Szentpetery Z, Varnai P, Stojilkovic SS, Balla T. 34.  2009. Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides. J. Biol. Chem. 284:21027–35 [Google Scholar]
  35. Picard C, McCarl CA, Papolos A, Khalil S, Luthy K. 35.  et al. 2009. STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N. Engl. J. Med. 360:1971–80 [Google Scholar]
  36. Lacruz RS, Feske S. 36.  2015. Diseases caused by mutations in ORAI1 and STIM1. Ann. NY Acad. Sci. 1356:45–79 [Google Scholar]
  37. Soboloff J, Rothberg BS, Madesh M, Gill DL. 37.  2012. STIM proteins: dynamic calcium signal transducers. Nat. Rev. Mol. Cell Biol. 13:549–65 [Google Scholar]
  38. Srikanth S, Jew M, Kim KD, Yee MK, Abramson J, Gwack Y. 38.  2012. Junctate is a Ca2+-sensing structural component of Orai1 and stromal interaction molecule 1 (STIM1). PNAS 109:8682–87 [Google Scholar]
  39. Woo JS, Srikanth S, Nishi M, Ping P, Takeshima H, Gwack Y. 39.  2016. Junctophilin-4, a component of the endoplasmic reticulum–plasma membrane junctions, regulates Ca2+ dynamics in T cells. PNAS 113:2762–67 [Google Scholar]
  40. Quintana A, Rajanikanth V, Farber-Katz S, Gudlur A, Zhang C. 40.  et al. 2015. TMEM110 regulates the maintenance and remodeling of mammalian ER–plasma membrane junctions competent for STIM–ORAI signaling. PNAS 112:E7083–92 [Google Scholar]
  41. Jing J, He L, Sun A, Quintana A, Ding Y. 41.  et al. 2015. Proteomic mapping of ER-PM junctions identifies STIMATE as a regulator of Ca2+ influx. Nat. Cell Biol. 17:1339–47 [Google Scholar]
  42. Sharma S, Quintana A, Findlay GM, Mettlen M, Baust B. 42.  et al. 2013. An siRNA screen for NFAT activation identifies septins as coordinators of store-operated Ca2+ entry. Nature 499:238–42 [Google Scholar]
  43. Srikanth S, Jung HJ, Kim KD, Souda P, Whitelegge J, Gwack Y. 43.  2010. A novel EF-hand protein, CRACR2A, is a cytosolic Ca2+ sensor that stabilizes CRAC channels in T cells. Nat. Cell Biol. 12:436–46 [Google Scholar]
  44. Palty R, Raveh A, Kaminsky I, Meller R, Reuveny E. 44.  2012. SARAF inactivates the store operated calcium entry machinery to prevent excess calcium refilling. Cell 149:425–38 [Google Scholar]
  45. Krapivinsky G, Krapivinsky L, Stotz SC, Manasian Y, Clapham DE. 45.  2011. POST, partner of stromal interaction molecule 1 (STIM1), targets STIM1 to multiple transporters. PNAS 108:19234–39 [Google Scholar]
  46. Moccia F, Zuccolo E, Soda T, Tanzi F, Guerra G. 46.  et al. 2015. Stim and Orai proteins in neuronal Ca2+ signaling and excitability. Front. Cell Neurosci. 9:153 [Google Scholar]
  47. Wang Y, Deng X, Mancarella S, Hendron E, Eguchi S. 47.  et al. 2010. The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science 330:105–9 [Google Scholar]
  48. Park CY, Shcheglovitov A, Dolmetsch R. 48.  2010. The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science 330:101–5 [Google Scholar]
  49. Anderie I, Schulz I, Schmid A. 49.  2007. Direct interaction between ER membrane-bound PTP1B and its plasma membrane-anchored targets. Cell Signal 19:582–92 [Google Scholar]
  50. Eden ER, White IJ, Tsapara A, Futter CE. 50.  2010. Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nat. Cell Biol. 12:267–72 [Google Scholar]
  51. Monteleone MC, Gonzalez Wusener AE, Burdisso JE, Conde C, Caceres A, Arregui CO. 51.  2012. ER-bound protein tyrosine phosphatase PTP1B interacts with Src at the plasma membrane/substrate interface. PLOS ONE 7:e38948 [Google Scholar]
  52. Bult A, Zhao F, Dirkx R Jr., Raghunathan A, Solimena M, Lombroso PJ. 52.  1997. STEP: a family of brain-enriched PTPs. Alternative splicing produces transmembrane, cytosolic and truncated isoforms. Eur. J. Cell Biol. 72:337–44 [Google Scholar]
  53. Bult A, Zhao F, Dirkx R Jr, Sharma E, Lukacsi E. 53.  et al. 1996. STEP61: A member of a family of brain-enriched PTPs is localized to the endoplasmic reticulum. J. Neurosci. 16:7821–31 [Google Scholar]
  54. Zhang Y, Venkitaramani DV, Gladding CM, Zhang Y, Kurup P. 54.  et al. 2008. The tyrosine phosphatase STEP mediates AMPA receptor endocytosis after metabotropic glutamate receptor stimulation. J. Neurosci. 28:10561–66 [Google Scholar]
  55. Snyder EM, Nong Y, Almeida CG, Paul S, Moran T. 55.  et al. 2005. Regulation of NMDA receptor trafficking by amyloid-β.. Nat. Neurosci. 8:1051–58 [Google Scholar]
  56. Frangioni JV, Oda A, Smith M, Salzman EW, Neel BG. 56.  1993. Calpain-catalyzed cleavage and subcellular relocation of protein phosphotyrosine phosphatase 1B (PTP-1B) in human platelets. EMBO J 12:4843–56 [Google Scholar]
  57. Whitters EA, Cleves AE, McGee TP, Skinner HB, Bankaitis VA. 57.  1993. SAC1p is an integral membrane protein that influences the cellular requirement for phospholipid transfer protein function and inositol in yeast. J. Cell Biol. 122:79–94 [Google Scholar]
  58. Nemoto Y, Kearns BG, Wenk MR, Chen H, Mori K. 58.  et al. 2000. Functional characterization of a mammalian Sac1 and mutants exhibiting substrate-specific defects in phosphoinositide phosphatase activity. J. Biol. Chem. 275:34293–305 [Google Scholar]
  59. Foti M, Audhya A, Emr SD. 59.  2001. Sac1 lipid phosphatase and Stt4 phosphatidylinositol 4-kinase regulate a pool of phosphatidylinositol 4-phosphate that functions in the control of the actin cytoskeleton and vacuole morphology. Mol. Biol. Cell 12:2396–411 [Google Scholar]
  60. Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD. 60.  2011. Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144:389–401 [Google Scholar]
  61. Manford A, Xia T, Saxena AK, Stefan C, Hu F. 61.  et al. 2010. Crystal structure of the yeast Sac1: implications for its phosphoinositide phosphatase function. EMBO J 29:1489–98 [Google Scholar]
  62. Mesmin B, Bigay J, Moser von Filseck J, Lacas-Gervais S, Drin G, Antonny B. 62.  2013. A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP. Cell 155:830–43 [Google Scholar]
  63. Dickson EJ, Jensen JB, Vivas O, Kruse M, Traynor-Kaplan AE, Hille B. 63.  2016. Dynamic formation of ER-PM junctions presents a lipid phosphatase to regulate phosphoinositides. J. Cell Biol. 213:33–48 [Google Scholar]
  64. Chung J, Torta F, Masai K, Lucast L, Czapla H. 64.  et al. 2015. Intracellular transport. PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts. Science 349:428–32 [Google Scholar]
  65. Moser von Filseck J, Copic A, Delfosse V, Vanni S, Jackson CL. 65.  et al. 2015. Intracellular transport. Phosphatidylserine transport by ORP/Osh proteins is driven by phosphatidylinositol 4-phosphate. Science 349:432–36 [Google Scholar]
  66. van Meer G, Voelker DR, Feigenson GW. 66.  2008. Membrane lipids: Where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9:112–24 [Google Scholar]
  67. Kaplan MR, Simoni RD. 67.  1985. Intracellular transport of phosphatidylcholine to the plasma membrane. J. Cell Biol. 101:441–45 [Google Scholar]
  68. Maxfield FR, Mondal M. 68.  2006. Sterol and lipid trafficking in mammalian cells. Biochem. Soc. Trans. 34:335–39 [Google Scholar]
  69. Hirschberg K, Miller CM, Ellenberg J, Presley JF, Siggia ED. 69.  et al. 1998. Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells. J. Cell Biol. 143:1485–503 [Google Scholar]
  70. Sleight RG, Pagano RE. 70.  1983. Rapid appearance of newly synthesized phosphatidylethanolamine at the plasma membrane. J. Biol. Chem. 258:9050–58 [Google Scholar]
  71. Gnamusch E, Kalaus C, Hrastnik C, Paltauf F, Daum G. 71.  1992. Transport of phospholipids between subcellular membranes of wild-type yeast cells and of the phosphatidylinositol transfer protein-deficient strain Saccharomyces cerevisiae Sec14. Biochim. Biophys. Acta 1111:120–26 [Google Scholar]
  72. Urbani L, Simoni RD. 72.  1990. Cholesterol and vesicular stomatitis virus G protein take separate routes from the endoplasmic reticulum to the plasma membrane. J. Biol. Chem. 265:1919–23 [Google Scholar]
  73. Baumann NA, Sullivan DP, Ohvo-Rekila H, Simonot C, Pottekat A. 73.  et al. 2005. Transport of newly synthesized sterol to the sterol-enriched plasma membrane occurs via nonvesicular equilibration. Biochemistry 44:5816–26 [Google Scholar]
  74. Brown RE. 74.  1992. Spontaneous lipid transfer between organized lipid assemblies. Biochim. Biophys. Acta 1113:375–89 [Google Scholar]
  75. Lev S. 75.  2012. Nonvesicular lipid transfer from the endoplasmic reticulum. Cold Spring Harb. Perspect. Biol. 4:a013300 [Google Scholar]
  76. Wirtz KW, Zilversmit DB. 76.  1968. Exchange of phospholipids between liver mitochondria and microsomes in vitro. J. Biol. Chem. 243:3596–602 [Google Scholar]
  77. Helmkamp GM Jr., Harvey MS, Wirtz KW, Van Deenen LL. 77.  1974. Phospholipid exchange between membranes. Purification of bovine brain proteins that preferentially catalyze the transfer of phosphatidylinositol. J. Biol. Chem. 249:6382–89 [Google Scholar]
  78. Thomas GM, Cunningham E, Fensome A, Ball A, Totty NF. 78.  et al. 1993. An essential role for phosphatidylinositol transfer protein in phospholipase C-mediated inositol lipid signaling. Cell 74:919–28 [Google Scholar]
  79. Aitken JF, van Heusden GP, Temkin M, Dowhan W. 79.  1990. The gene encoding the phosphatidylinositol transfer protein is essential for cell growth. J. Biol. Chem. 265:4711–17 [Google Scholar]
  80. Drin G. 80.  2014. Topological regulation of lipid balance in cells. Annu. Rev. Biochem. 83:51–77 [Google Scholar]
  81. Elbaz-Alon Y, Rosenfeld-Gur E, Shinder V, Futerman AH, Geiger T, Schuldiner M. 81.  2014. A dynamic interface between vacuoles and mitochondria in yeast. Dev. Cell 30:95–102 [Google Scholar]
  82. Honscher C, Mari M, Auffarth K, Bohnert M, Griffith J. 82.  et al. 2014. Cellular metabolism regulates contact sites between vacuoles and mitochondria. Dev. Cell 30:86–94 [Google Scholar]
  83. Lang AB, John Peter AT, Walter P, Kornmann B. 83.  2015. ER–mitochondrial junctions can be bypassed by dominant mutations in the endosomal protein Vps13. J. Cell Biol. 210:883–90 [Google Scholar]
  84. Lev S, Ben Halevy D, Peretti D, Dahan N. 84.  2008. The VAP protein family: from cellular functions to motor neuron disease. Trends Cell Biol 18:282–90 [Google Scholar]
  85. Murphy SE, Levine TP. 85.  2016. VAP, a versatile access point for the endoplasmic reticulum: review and analysis of FFAT-like motifs in the VAPome. Biochim. Biophys. Acta 1861:952–61 [Google Scholar]
  86. Loewen CJ, Levine TP. 86.  2005. A highly conserved binding site in vesicle-associated membrane protein-associated protein (VAP) for the FFAT motif of lipid-binding proteins. J. Biol. Chem. 280:14097–104 [Google Scholar]
  87. Kaiser SE, Brickner JH, Reilein AR, Fenn TD, Walter P, Brunger AT. 87.  2005. Structural basis of FFAT motif-mediated ER targeting. Structure 13:1035–45 [Google Scholar]
  88. Di Paolo G, De Camilli P. 88.  2006. Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–57 [Google Scholar]
  89. Balla T. 89.  2013. Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol. Rev. 93:1019–137 [Google Scholar]
  90. Michell RH. 90.  1975. Inositol phospholipids and cell surface receptor function. Biochim. Biophys. Acta 415:81–147 [Google Scholar]
  91. Bankaitis VA, Aitken JR, Cleves AE, Dowhan W. 91.  1990. An essential role for a phospholipid transfer protein in yeast Golgi function. Nature 347:561–62 [Google Scholar]
  92. Bankaitis VA, Malehorn DE, Emr SD, Greene R. 92.  1989. The Saccharomyces cerevisiae SEC14 gene encodes a cytosolic factor that is required for transport of secretory proteins from the yeast Golgi complex. J. Cell Biol. 108:1271–81 [Google Scholar]
  93. Grabon A, Khan D, Bankaitis VA. 93.  2015. Phosphatidylinositol transfer proteins and instructive regulation of lipid kinase biology. Biochim. Biophys. Acta 1851:724–35 [Google Scholar]
  94. Cunningham E, Tan SK, Swigart P, Hsuan J, Bankaitis V, Cockcroft S. 94.  1996. The yeast and mammalian isoforms of phosphatidylinositol transfer protein can all restore phospholipase C-mediated inositol lipid signaling in cytosol-depleted RBL-2H3 and HL-60 cells. PNAS 93:6589–93 [Google Scholar]
  95. Tanaka S, Hosaka K. 95.  1994. Cloning of a cDNA encoding a second phosphatidylinositol transfer protein of rat brain by complementation of the yeast sec14 mutation. J. Biochem. 115:981–84 [Google Scholar]
  96. Kim YJ, Hernandez ML, Balla T. 96.  2013. Inositol lipid regulation of lipid transfer in specialized membrane domains. Trends Cell Biol 23:270–78 [Google Scholar]
  97. Cockcroft S. 97.  2012. The diverse functions of phosphatidylinositol transfer proteins. Curr. Top Microbiol. Immunol. 362:185–208 [Google Scholar]
  98. Wirtz KWA. 98.  1991. Phospholipid transfer proteins. Annu. Rev. Biochem. 60:73–99 [Google Scholar]
  99. Milligan SC, Alb JG Jr., Elagina RB, Bankaitis VA, Hyde DR. 99.  1997. The phosphatidylinositol transfer protein domain of Drosophila retinal degeneration B protein is essential for photoreceptor cell survival and recovery from light stimulation. J. Cell Biol. 139:351–63 [Google Scholar]
  100. Chakrabarti P, Kolay S, Yadav S, Kumari K, Nair A. 100.  et al. 2015. A dPIP5K dependent pool of phosphatidylinositol 4,5 bisphosphate (PIP2) is required for G-protein coupled signal transduction in Drosophila photoreceptors. PLOS Genet 11:e1004948 [Google Scholar]
  101. Yadav S, Garner K, Georgiev P, Li M, Gomez-Espinosa E. 101.  et al. 2015. RDGBα, a PtdIns-PtdOH transfer protein, regulates G-protein-coupled PtdIns(4,5)P2 signalling during Drosophila phototransduction. J. Cell Sci. 128:3330–44 [Google Scholar]
  102. Yadav S, Cockcroft S, Raghu P. 102.  2016. The Drosophila photoreceptor as a model system for studying signalling at membrane contact sites. Biochem. Soc. Trans. 44:447–51 [Google Scholar]
  103. Kim S, Kedan A, Marom M, Gavert N, Keinan O. 103.  et al. 2013. The phosphatidylinositol-transfer protein Nir2 binds phosphatidic acid and positively regulates phosphoinositide signalling. EMBO Rep 14:891–99 [Google Scholar]
  104. Kim YJ, Guzman-Hernandez ML, Wisniewski E, Balla T. 104.  2015. Phosphatidylinositol-phosphatidic acid exchange by Nir2 at ER-PM contact sites maintains phosphoinositide signaling competence. Dev. Cell 33:549–61 [Google Scholar]
  105. Chang CL, Hsieh TS, Yang TT, Rothberg KG, Azizoglu DB. 105.  et al. 2013. Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep 5:813–25 [Google Scholar]
  106. Chang CL, Liou J. 106.  2015. Phosphatidylinositol 4,5-bisphosphate homeostasis regulated by Nir2 and Nir3 proteins at endoplasmic reticulum-plasma membrane junctions. J. Biol. Chem. 290:14289–301 [Google Scholar]
  107. Cockcroft S, Garner K, Yadav S, Gomez-Espinoza E, Raghu P. 107.  2016. RdgBα reciprocally transfers PA and PI at ER-PM contact sites to maintain PI(4,5)P2 homoeostasis during phospholipase C signalling in Drosophila photoreceptors. Biochem. Soc. Trans. 44:286–92 [Google Scholar]
  108. Garner K, Hunt AN, Koster G, Somerharju P, Groves E. 108.  et al. 2012. Phosphatidylinositol transfer protein, cytoplasmic 1 (PITPNC1) binds and transfers phosphatidic acid. J. Biol. Chem. 287:32263–76 [Google Scholar]
  109. Alva V, Lupas AN. 109.  2016. The TULIP superfamily of eukaryotic lipid-binding proteins as a mediator of lipid sensing and transport. Biochim. Biophys. Acta 1861:913–23 [Google Scholar]
  110. Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F. 110.  et al. 2014. Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510:552–55 [Google Scholar]
  111. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J. 111.  et al. 2009. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325:477–81 [Google Scholar]
  112. Toulmay A, Prinz WA. 112.  2012. A conserved membrane-binding domain targets proteins to organelle contact sites. J. Cell Sci. 125:49–58 [Google Scholar]
  113. Manford AG, Stefan CJ, Yuan HL, MacGurn JA, Emr SD. 113.  2012. ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev. Cell 23:1129–40 [Google Scholar]
  114. Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M. 114.  et al. 2013. PI(4,5)P2-dependent and Ca2+-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153:1494–509 [Google Scholar]
  115. Min SW, Chang WP, Sudhof TC. 115.  2007. E-Syts, a family of membranous Ca2+-sensor proteins with multiple C2 domains. PNAS 104:3823–28 [Google Scholar]
  116. Sudhof TC. 116.  2012. Calcium control of neurotransmitter release. Cold Spring Harb. Perspect. Biol. 4:a011353 [Google Scholar]
  117. Saheki Y, Bian X, Schauder CM, Sawaki Y, Surma MA. 117.  et al. 2016. Control of plasma membrane lipid homeostasis by the extended synaptotagmins. Nat. Cell Biol. 18:504–15 [Google Scholar]
  118. Yu H, Liu Y, Gulbranson DR, Paine A, Rathore SS, Shen J. 118.  2016. Extended synaptotagmins are Ca2+-dependent lipid transfer proteins at membrane contact sites. PNAS 113:4362–67 [Google Scholar]
  119. Idevall-Hagren O, A, Xie B, De Camilli P. 119.  2015. Triggered Ca2+ influx is required for extended synaptotagmin 1-induced ER-plasma membrane tethering. EMBO J 34:2291–305 [Google Scholar]
  120. Qiu X, Mistry A, Ammirati MJ, Chrunyk BA, Clark RW. 120.  et al. 2007. Crystal structure of cholesteryl ester transfer protein reveals a long tunnel and four bound lipid molecules. Nat. Struct. Mol. Biol. 14:106–13 [Google Scholar]
  121. Zhang Y, Wang H, Kage-Nakadai E, Mitani S, Wang X. 121.  2012. C. elegans secreted lipid-binding protein NRF-5 mediates PS appearance on phagocytes for cell corpse engulfment. Curr. Biol. 22:1276–84 [Google Scholar]
  122. AhYoung AP, Jiang J, Zhang J, Khoi Dang X, Loo JA. 122.  et al. 2015. Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. PNAS 112:E3179–88 [Google Scholar]
  123. Xu J, Bacaj T, Zhou A, Tomchick DR, Sudhof TC, Rizo J. 123.  2014. Structure and Ca2+-binding properties of the tandem C2 domains of E-Syt2. Structure 22:269–80 [Google Scholar]
  124. Craxton M. 124.  2004. Synaptotagmin gene content of the sequenced genomes. BMC Genom 5:43 [Google Scholar]
  125. Levy A, Zheng JY, Lazarowitz SG. 125.  2015. Synaptotagmin SYTA forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr. Biol. 25:2018–25 [Google Scholar]
  126. Perez-Sancho J, Vanneste S, Lee E, McFarlane HE, Esteban Del Valle A. 126.  et al. 2015. The Arabidopsis Synaptotagmin1 is enriched in endoplasmic reticulum-plasma membrane contact sites and confers cellular resistance to mechanical stresses. Plant Physiol 168:132–43 [Google Scholar]
  127. Aguilar PS, Engel A, Walter P. 127.  2007. The plasma membrane proteins Prm1 and Fig 1 ascertain fidelity of membrane fusion during yeast mating. Mol. Biol. Cell 18:547–56 [Google Scholar]
  128. Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R. 128.  et al. 2008. Arabidopsis Synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20:3374–88 [Google Scholar]
  129. Yamazaki T, Kawamura Y, Minami A, Uemura M. 129.  2008. Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20:3389–404 [Google Scholar]
  130. Omnus DJ, Manford AG, Bader JM, Emr SD, Stefan CJ. 130.  2016. Phosphoinositide kinase signaling controls ER-PM cross-talk. Mol. Biol. Cell 27:1170–80 [Google Scholar]
  131. Sclip A, Bacaj T, Giam LR, Sudhof TC. 131.  2016. Extended synaptotagmin (ESyt) triple knock-out mice are viable and fertile without obvious endoplasmic reticulum dysfunction. PLOS ONE 11:e0158295 [Google Scholar]
  132. Tremblay MG, Moss T. 132.  2016. Loss of all 3 extended synaptotagmins does not affect normal mouse development, viability or fertility. Cell Cycle 15:2360–66 [Google Scholar]
  133. Heo WD, Inoue T, Park WS, Kim ML, Park BO. 133.  et al. 2006. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314:1458–61 [Google Scholar]
  134. Leventis PA, Grinstein S. 134.  2010. The distribution and function of phosphatidylserine in cellular membranes. Annu. Rev. Biophys. 39:407–27 [Google Scholar]
  135. Saheki Y, De Camilli P. 135.  2012. Synaptic vesicle endocytosis. Cold Spring Harb. Perspect. Biol. 4:a005645 [Google Scholar]
  136. Hankins HM, Baldridge RD, Xu P, Graham TR. 136.  2015. Role of flippases, scramblases and transfer proteins in phosphatidylserine subcellular distribution. Traffic 16:35–47 [Google Scholar]
  137. Raychaudhuri S, Prinz WA. 137.  2010. The diverse functions of oxysterol-binding proteins. Annu. Rev. Cell Dev. Biol. 26:157–77 [Google Scholar]
  138. Beh CT, Rine J. 138.  2004. A role for yeast oxysterol-binding protein homologs in endocytosis and in the maintenance of intracellular sterol-lipid distribution. J. Cell Sci. 117:2983–96 [Google Scholar]
  139. Raychaudhuri S, Im YJ, Hurley JH, Prinz WA. 139.  2006. Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides. J. Cell Biol. 173:107–19 [Google Scholar]
  140. Schulz TA, Choi MG, Raychaudhuri S, Mears JA, Ghirlando R. 140.  et al. 2009. Lipid-regulated sterol transfer between closely apposed membranes by oxysterol-binding protein homologues. J. Cell Biol. 187:889–903 [Google Scholar]
  141. Im YJ, Raychaudhuri S, Prinz WA, Hurley JH. 141.  2005. Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 437:154–58 [Google Scholar]
  142. de Saint-Jean M, Delfosse V, Douguet D, Chicanne G, Payrastre B. 142.  et al. 2011. Osh4p exchanges sterols for phosphatidylinositol 4-phosphate between lipid bilayers. J. Cell Biol. 195:965–78 [Google Scholar]
  143. Maeda K, Anand K, Chiapparino A, Kumar A, Poletto M. 143.  et al. 2013. Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins. Nature 501:257–61 [Google Scholar]
  144. Tong J, Yang H, Yang H, Eom SH, Im YJ. 144.  2013. Structure of Osh3 reveals a conserved mode of phosphoinositide binding in oxysterol-binding proteins. Structure 21:1203–13 [Google Scholar]
  145. Moser von Filseck J, Vanni S, Mesmin B, Antonny B, Drin G. 145.  2015. A phosphatidylinositol–4-phosphate powered exchange mechanism to create a lipid gradient between membranes. Nat. Commun. 6:6671 [Google Scholar]
  146. Sohn M, Ivanova P, Brown HA, Toth DJ, Varnai P. 146.  et al. 2016. Lenz-Majewski mutations in PTDSS1 affect phosphatidylinositol 4-phosphate metabolism at ER-PM and ER-Golgi junctions. PNAS 113:4314–19 [Google Scholar]
  147. Dong R, Saheki Y, Swarup S, Lucast L, Harper JW, De Camilli P. 147.  2016. Endosome-ER contacts control actin nucleation and retromer function through VAP-dependent regulation of PI4P. Cell 166:408–23 [Google Scholar]
  148. Heino S, Lusa S, Somerharju P, Ehnholm C, Olkkonen VM, Ikonen E. 148.  2000. Dissecting the role of the Golgi complex and lipid rafts in biosynthetic transport of cholesterol to the cell surface. PNAS 97:8375–80 [Google Scholar]
  149. Georgiev AG, Sullivan DP, Kersting MC, Dittman JS, Beh CT, Menon AK. 149.  2011. Osh proteins regulate membrane sterol organization but are not required for sterol movement between the ER and PM. Traffic 12:1341–55 [Google Scholar]
  150. Gatta AT, Wong LH, Sere YY, Calderón-Noreña DM, Cockcroft S. 150.  et al. 2015. A new family of StART domain proteins at membrane contact sites has a role in ER-PM sterol transport. eLife 4:e07253 [Google Scholar]
  151. Alpy F, Tomasetto C. 151.  2014. START ships lipids across interorganelle space. Biochimie 96:85–95 [Google Scholar]
  152. Murley A, Sarsam RD, Toulmay A, Yamada J, Prinz WA, Nunnari J. 152.  2015. Ltc1 is an ER-localized sterol transporter and a component of ER-mitochondria and ER-vacuole contacts. J. Cell Biol. 209:539–48 [Google Scholar]
  153. Doerks T, Strauss M, Brendel M, Bork P. 153.  2000. GRAM, a novel domain in glucosyltransferases, myotubularins and other putative membrane-associated proteins. Trends Biochem. Sci. 25:483–85 [Google Scholar]
  154. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S. 154.  et al. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318–24 [Google Scholar]
  155. Sutton RB, Fasshauer D, Jahn R, Brunger AT. 155.  1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395:347–53 [Google Scholar]
  156. Wojnacki J, Galli T. 156.  2016. Membrane traffic during axon development. Dev. Neurobiol. 76:1185–200 [Google Scholar]
  157. Petkovic M, Jemaiel A, Daste F, Specht CG, Izeddin I. 157.  et al. 2014. The SNARE Sec 22b has a non-fusogenic function in plasma membrane expansion. Nat. Cell Biol. 16:434–44 [Google Scholar]
  158. Newman AP, Shim J, Ferro-Novick S. 158.  1990. BET1, BOS1, and SEC22 are members of a group of interacting yeast genes required for transport from the endoplasmic reticulum to the Golgi complex. Mol. Cell Biol. 10:3405–14 [Google Scholar]
  159. McNew JA, Parlati F, Fukuda R, Johnston RJ, Paz K. 159.  et al. 2000. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407:153–59 [Google Scholar]
  160. Nehls S, Snapp EL, Cole NB, Zaal KJ, Kenworthy AK. 160.  et al. 2000. Dynamics and retention of misfolded proteins in native ER membranes. Nat. Cell Biol. 2:288–95 [Google Scholar]
  161. Lavieu G, Orci L, Shi L, Geiling M, Ravazzola M. 161.  et al. 2010. Induction of cortical endoplasmic reticulum by dimerization of a coatomer-binding peptide anchored to endoplasmic reticulum membranes. PNAS 107:6876–81 [Google Scholar]
  162. Wolf W, Kilic A, Schrul B, Lorenz H, Schwappach B, Seedorf M. 162.  2012. Yeast Ist2 recruits the endoplasmic reticulum to the plasma membrane and creates a ribosome-free membrane microcompartment. PLOS ONE 7:e39703 [Google Scholar]
  163. Duran C, Qu Z, Osunkoya AO, Cui Y, Hartzell HC. 163.  2012. ANOs 3–7 in the anoctamin/Tmem16 Cl channel family are intracellular proteins. Am. J. Physiol. Cell Physiol. 302:C482–93 [Google Scholar]
  164. Picollo A, Malvezzi M, Accardi A. 164.  2015. TMEM16 proteins: unknown structure and confusing functions. J. Mol. Biol. 427:94–105 [Google Scholar]
  165. Mandikian D, Bocksteins E, Parajuli LK, Bishop HI, Cerda O. 165.  et al. 2014. Cell type specific spatial and functional coupling between mammalian brain Kv2.1 K+ channels and ryanodine receptors. J. Comp. Neurol. 522:3555–74 [Google Scholar]
  166. Kaufmann WA, Ferraguti F, Fukazawa Y, Kasugai Y, Shigemoto R. 166.  et al. 2009. Large-conductance calcium-activated potassium channels in purkinje cell plasma membranes are clustered at sites of hypolemmal microdomains. J. Comp. Neurol. 515:215–30 [Google Scholar]
  167. Breslow DK, Weissman JS. 167.  2010. Membranes in balance: mechanisms of sphingolipid homeostasis. Mol. Cell 40:267–79 [Google Scholar]
  168. Hama K. 168.  1965. Some observations on the fine structure of the lateral line organ of the Japanese sea eel Lyncozymba nystromi. J. Cell Biol. 24:193–210 [Google Scholar]
  169. Flickinger C, Fawcett DW. 169.  1967. The junctional specializations of Sertoli cells in the seminiferous epithelium. Anat. Record 158:207–21 [Google Scholar]
  170. Fuchs PA. 170.  2014. A ‘calcium capacitor’ shapes cholinergic inhibition of cochlear hair cells. J. Physiol. 592:3393–3401 [Google Scholar]
  171. Voss C, Schiller A, Taugner R. 171.  1980. Morphology and distribution of the synapses to the spinal motoneuron of the frog. Cell Tissue Res 213:253–71 [Google Scholar]
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