1932

Abstract

Inside eukaryotic cells, membrane contact sites (MCSs), regions where two membrane-bound organelles are apposed at less than 30 nm, generate regions of important lipid and calcium exchange. This review principally focuses on the structure and the function of MCSs between the endoplasmic reticulum (ER) and the plasma membrane (PM). Here we describe how tethering structures form and maintain these junctions and, in some instances, participate in their function. We then discuss recent insights into the mechanisms by which specific classes of proteins mediate nonvesicular lipid exchange between the ER and PM and how such phenomena, already known to be crucial for maintaining organelle identity, are also emerging as regulators of cell growth and development.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-111315-125024
2016-10-06
2024-06-22
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/32/1/annurev-cellbio-111315-125024.html?itemId=/content/journals/10.1146/annurev-cellbio-111315-125024&mimeType=html&fmt=ahah

Literature Cited

  1. Antonucci DE, Lim ST, Vassanelli S, Trimmer JS. 2001. Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons. Neuroscience 108:169–81 [Google Scholar]
  2. Baumann NA, Sullivan DP, Ohvo-Rekilä H, Simonot C, Pottekat A. et al. 2005. Transport of newly synthesized sterol to the sterol-enriched plasma membrane occurs via nonvesicular equilibration. Biochemistry 44:155816–26 [Google Scholar]
  3. Blom T, Somerharju P, Ikonen E. 2011. Synthesis and biosynthetic trafficking of membrane lipids. Cold Spring Harb. Perspect. Biol. 3:8a004713 [Google Scholar]
  4. Bos MP, Robert V, Tommassen J. 2007. Biogenesis of the gram-negative bacterial outer membrane. Annu. Rev. Microbiol. 61:191–214 [Google Scholar]
  5. Burgoyne T, Patel S, Eden ER. 2015. Calcium signaling at ER membrane contact sites. Biochim. Biophys. Acta 1853:92012–17 [Google Scholar]
  6. Carrasco S, Meyer T. 2011. STIM proteins and the endoplasmic reticulum–plasma membrane junctions. Annu. Rev. Biochem. 80:973–1000 [Google Scholar]
  7. Chang CL, Hsieh TS, Yang TT, Rothberg KG, Azizoglu DB. et al. 2013. Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum–plasma membrane junctions. Cell Rep. 5:3813–25 [Google Scholar]
  8. Chung J, Torta F, Masai K, Lucast L, Czapla H. et al. 2015. PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER–plasma membrane contacts. Science 349:6246428–32 [Google Scholar]
  9. Creutz CE, Snyder SL, Schulz TA. 2004. Characterization of the yeast tricalbins: membrane-bound multi-C2-domain proteins that form complexes involved in membrane trafficking. Cell. Mol. Life Sci. 61:101208–20 [Google Scholar]
  10. D'Angelo G, Vicinanza M, De Matteis MA. 2008. Lipid-transfer proteins in biosynthetic pathways. Curr. Opin. Cell Biol. 20:4360–70 [Google Scholar]
  11. De Saint-Jean M, Delfosse V, Douguet D, Chicanne G, Payrastre B. et al. 2011. Osh4p exchanges sterols for phosphatidylinositol 4-phosphate between lipid bilayers. J. Cell Biol. 195:6965–78 [Google Scholar]
  12. Deutsch E, Weigel AV, Akin EJ, Fox P, Hansen G. et al. 2012. Kv2.1 cell surface clusters are insertion platforms for ion channel delivery to the plasma membrane. Mol. Biol. Cell 23:152917–29 [Google Scholar]
  13. Di Paolo G, De Camilli P. 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature 443:7112651–57 [Google Scholar]
  14. Endo M. 2009. Calcium-induced calcium release in skeletal muscle. Physiol. Rev. 89:41153–76 [Google Scholar]
  15. Ercan E, Momburg F, Engel U, Temmerman K, Nickel W, Seedorf M. 2009. A conserved, lipid-mediated sorting mechanism of yeast Ist2 and mammalian STIM proteins to the peripheral ER. Traffic 10:121802–18 [Google Scholar]
  16. Fernández-Busnadiego R, Saheki Y, De Camilli P. 2015. Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum–plasma membrane contact sites. PNAS 112:16E2004–13 [Google Scholar]
  17. Fischer MA, Temmerman K, Ercan E, Nickel W, Seedorf M. 2009. Binding of plasma membrane lipids recruits the yeast integral membrane protein Ist2 to the cortical ER. Traffic 10:81084–97 [Google Scholar]
  18. Fox PD, Haberkorn CJ, Akin EJ, Seel PJ, Krapf D, Tamkun MM. 2015. Induction of stable ER–plasma-membrane junctions by Kv2.1 potassium channels. J. Cell Sci. 128:112096–105 [Google Scholar]
  19. Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. 2011. ER tubules mark sites of mitochondrial division. Science 334:6054358–62 [Google Scholar]
  20. Garbino A, van Oort RJ, Dixit SS, Landstrom AP, Ackerman MJ, Wehrens XH. 2009. Molecular evolution of the junctophilin gene family. Physiol. Genom. 37:3175–86 [Google Scholar]
  21. Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M. et al. 2013. PI(4,5)P2-dependent and Ca2+-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153:71494–509 [Google Scholar]
  22. Golovina VA. 2005. Visualization of localized store-operated calcium entry in mouse astrocytes. Close proximity to the endoplasmic reticulum. J. Physiol. 564:3737–49 [Google Scholar]
  23. Haj FG, Sabet O, Kinkhabwala A, Wimmer-Kleikamp S, Roukos V. et al. 2012. Regulation of signaling at regions of cell-cell contact by endoplasmic reticulum–bound protein-tyrosine phosphatase 1B. PLOS ONE 7:5e36633 [Google Scholar]
  24. Hanada K, Kumagai K, Yasuda S, Miura Y, Kawano M. et al. 2003. Molecular machinery for non-vesicular trafficking of ceramide. Nature 426:6968803–9 [Google Scholar]
  25. Hartzell HC, Yu K, Xiao Q, Chien LT, Qu Z. 2009. Anoctamin/TMEM16 family members are Ca2+-activated Cl channels. J. Physiol. 587:102127–39 [Google Scholar]
  26. Hayashi M, Raimondi A, O'Toole E, Paradise S, Collesi C. et al. 2008. Cell- and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1–null neurons. PNAS 105:62175–80 [Google Scholar]
  27. Helle SC, Kanfer G, Kolar K, Lang A, Michel AH, Kornmann B. 2013. Organization and function of membrane contact sites. Biochim. Biophys. Acta 1833:112526–41 [Google Scholar]
  28. Henne WM, Liou J, Emr SD. 2015. Molecular mechanisms of inter-organelle ER-PM contact sites. Curr. Opin. Cell Biol. 35:123–30 [Google Scholar]
  29. Herdman C, Tremblay MG, Mishra PK, Moss T. 2014. Loss of extended synaptotagmins ESyt2 and ESyt3 does not affect mouse development or viability, but in vitro cell migration and survival under stress are affected. Cell Cycle 13:162616–25 [Google Scholar]
  30. Holthuis JC, Levine TP. 2005. Lipid traffic: floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 6:3209–20 [Google Scholar]
  31. Holthuis JC, Menon AK. 2014. Lipid landscapes and pipelines in membrane homeostasis. Nature 510:750348–57 [Google Scholar]
  32. Idevall-Hagren O, A, Xie B, De Camilli P. 2015. Triggered Ca2+ influx is required for extended synaptotagmin 1–induced ER–plasma membrane tethering. EMBO J. 34:172291–305 [Google Scholar]
  33. Im YJ, Raychaudhuri S, Prinz WA, Hurley JH. 2005. Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 437:7055154–58 [Google Scholar]
  34. Ito K, Komazaki S, Sasamoto K, Yoshida M, Nishi M. et al. 2001. Deficiency of triad junction and contraction in mutant skeletal muscle lacking junctophilin type 1. J. Cell Biol. 154:51059–67 [Google Scholar]
  35. Jacquier N, Choudhary V, Mari M, Toulmay A, Reggiori F, Schneiter R. 2011. Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Sci. 124:142424–37 [Google Scholar]
  36. Jahn R, Fasshauer D. 2012. Molecular machines governing exocytosis of synaptic vesicles. Nature 490:7419201–7 [Google Scholar]
  37. Jahn R, Scheller RH. 2006. SNAREs—engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7:9631–43 [Google Scholar]
  38. Jiménez JL, Davletov B. 2007. Beta-strand recombination in tricalbin evolution and the origin of synaptotagmin-like C2 domains. Proteins 68:3770–78 [Google Scholar]
  39. Kagiwada S, Hashimoto M. 2007. The yeast VAP homolog Scs2p has a phosphoinositide-binding ability that is correlated with its activity. Biochem. Biophys. Res. Commun. 364:4870–76 [Google Scholar]
  40. Kaiser SE, Brickner JH, Reilein AR, Fenn TD, Walter P, Brunger AT. 2005. Structural basis of FFAT motif–mediated ER targeting. Structure 13:71035–45 [Google Scholar]
  41. Kannan M, Riekhof WR, Voelker DR. 2015. Transport of phosphatidylserine from the endoplasmic reticulum to the site of phosphatidylserine decarboxylase2 in yeast. Traffic 16:2123–34 [Google Scholar]
  42. Kaplan MR, Simoni RD. 1985a. Intracellular transport of phosphatidylcholine to the plasma membrane. J. Cell Biol. 101:2441–45 [Google Scholar]
  43. Kaplan MR, Simoni RD. 1985b. Transport of cholesterol from the endoplasmic reticulum to the plasma membrane. J. Cell Biol. 101:2446–53 [Google Scholar]
  44. Kawano M, Kumagai K, Nishijima M, Hanada K. 2006. Efficient trafficking of ceramide from the endoplasmic reticulum to the Golgi apparatus requires a VAMP-associated protein–interacting FFAT motif of CERT. J. Biol. Chem. 281:4030279–88 [Google Scholar]
  45. Kopec KO, Alva V, Lupas AN. 2010. Homology of SMP domains to the TULIP superfamily of lipid-binding proteins provides a structural basis for lipid exchange between ER and mitochondria. Bioinformatics 26:161927–31 [Google Scholar]
  46. Kopec KO, Alva V, Lupas AN. 2011. Bioinformatics of the TULIP domain superfamily. Biochem. Soc. Trans. 39:41033–38 [Google Scholar]
  47. Kralt A, Carretta M, Mari M, Reggiori F, Steen A. et al. 2015. Intrinsically disordered linker and plasma membrane–binding motif sort Ist2 and Ssy1 to junctions. Traffic 16:2135–47 [Google Scholar]
  48. Kudo N, Kumagai K, Tomishige N, Yamaji T, Wakatsuki S. et al. 2008. Structural basis for specific lipid recognition by CERT responsible for nonvesicular trafficking of ceramide. PNAS 105:2488–93 [Google Scholar]
  49. Lahiri S, Toulmay A, Prinz WA. 2015. Membrane contact sites, gateways for lipid homeostasis. Curr. Opin. Cell Biol. 33:82–87 [Google Scholar]
  50. Lalanne F, Ponsin G. 2000. Mechanism of the phospholipid transfer protein–mediated transfer of phospholipids from model lipid vesicles to high density lipoproteins. Biochim. Biophys. Acta 1487:182–91 [Google Scholar]
  51. Landstrom AP, Beavers DL, Wehrens XH. 2014. The junctophilin family of proteins: from bench to bedside. Trends Mol. Med. 20:6353–62 [Google Scholar]
  52. Lee I, Hong W. 2006. Diverse membrane-associated proteins contain a novel SMP domain. FASEB J. 20:2202–6 [Google Scholar]
  53. Lek A, Evesson FJ, Sutton RB, North KN, Cooper ST. 2012. Ferlins: regulators of vesicle fusion for auditory neurotransmission, receptor trafficking and membrane repair. Traffic 13:2185–94 [Google Scholar]
  54. Lev S. 2010. Non-vesicular lipid transport by lipid-transfer proteins and beyond. Nat. Rev. Mol. Cell Biol. 11:10739–50 [Google Scholar]
  55. Lev S, Ben Halevy D, Peretti D, Dahan N. 2008. The VAP protein family: from cellular functions to motor neuron disease. Trends Cell Biol. 18:6282–90 [Google Scholar]
  56. Levine T. 2004. Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions. Trends Cell Biol. 14:9483–90 [Google Scholar]
  57. Levine T, Rabouille C. 2005. Endoplasmic reticulum: one continuous network compartmentalized by extrinsic cues. Curr. Opin. Cell Biol. 17:4362–68 [Google Scholar]
  58. Levy A, Zheng JY, Lazarowitz SG. 2015. Synaptotagmin SYTA forms ER–plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr. Biol. 25:152018–25 [Google Scholar]
  59. Li F, Pincet F, Perez E, Eng WS, Melia TJ. et al. 2007. Energetics and dynamics of SNAREpin folding across lipid bilayers. Nat. Struct. Mol. Biol. 14:10890–96 [Google Scholar]
  60. Lim ST, Antonucci DE, Scannevin RH, Trimmer JS. 2000. A novel targeting signal for proximal clustering of the Kv2.1 K+ channel in hippocampal neurons. Neuron 25:385–97 [Google Scholar]
  61. Liou J, Fivaz M, Inoue T, Meyer T. 2007. Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca2+ store depletion. PNAS 104:229301–6 [Google Scholar]
  62. Liu W, Montana V, Parpura V, Mohideen U. 2011. Single-molecule measurements of dissociation rates and energy landscapes of binary trans snare complexes in parallel versus antiparallel orientation. Biophys. J. 101:81854–62 [Google Scholar]
  63. Loewen CJ, Levine TP. 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. 280:1414097–104 [Google Scholar]
  64. Loewen CJ, Roy A, Levine TP. 2003. A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 22:92025–35 [Google Scholar]
  65. Loewen CJ, Young BP, Tavassoli S, Levine TP. 2007. Inheritance of cortical ER in yeast is required for normal septin organization. J. Cell Biol. 179:3467–83 [Google Scholar]
  66. Maeda K, Anand K, Chiapparino A, Kumar A, Poletto M. et al. 2013. Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins. Nature 501:7466257–61 [Google Scholar]
  67. Mandikian D, Bocksteins E, Parajuli LK, Bishop HI, Cerda O. et al. 2014. Cell type–specific spatial and functional coupling between mammalian brain Kv2.1 K+ channels and ryanodine receptors. J. Comp. Neurol. 522:153555–74 [Google Scholar]
  68. Manford AG, Stefan CJ, Yuan HL, Macgurn JA, Emr SD. 2012. ER–to–plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev. Cell 23:61129–40 [Google Scholar]
  69. Mannella C, Buttle K, Rath B, Marko M. 1998. Electron microscopic tomography of rat-liver mitochondria and their interactions with the endoplasmic reticulum. Biofactors 8:225–28 [Google Scholar]
  70. Mesmin B, Bigay J, Moser von Filseck J, Lacas-Gervais S, Drin G, Antonny B. 2013. A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP. Cell 155:4830–43 [Google Scholar]
  71. Min S, Chang W, Südhof T. 2007. E-Syts, a family of membranous Ca2+-sensor proteins with multiple C2 domains. PNAS 104:3823–28 [Google Scholar]
  72. Moser von Filseck J, Čopič A, Delfosse V, Vanni S, Jackson CL. et al. 2015a. Phosphatidylserine transport by ORP/Osh proteins is driven by phosphatidylinositol 4-phosphate. Science 349:6246432–36 [Google Scholar]
  73. Moser von Filseck J, Vanni S, Mesmin B, Antonny B, Drin G. 2015b. A phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes. Nat. Commun. 6:6671 [Google Scholar]
  74. Murphy SE, Levine TP. 2016. VAP, a versatile access point for the endoplasmic reticulum: review and analysis of FFAT-like motifs in the VAPome. Biochim. Biophys. Acta 18618 Part B952–61 [Google Scholar]
  75. Nguyen TT, Lewandowska A, Choi JY, Markgraf DF, Junker M. et al. 2012. Gem1 and ERMES do not directly affect phosphatidylserine transport from ER to mitochondria or mitochondrial inheritance. Traffic 13:6880–90 [Google Scholar]
  76. Nishimura Y, Hayashi M, Inada H, Tanaka T. 1999. Molecular cloning and characterization of mammalian homologues of vesicle-associated membrane protein–associated (VAMP-associated) proteins. Biochem. Biophys. Res. Commun. 254:121–26 [Google Scholar]
  77. Novikoff AB. 1964. GERL, its form and function in neurons of rat spinal ganglia. Biol. Bull. 127:358 [Google Scholar]
  78. Petkovic M, Jemaiel A, Daste F, Specht CG, Izeddin I. et al. 2014. The SNARE Sec22b has a non-fusogenic function in plasma membrane expansion. Nat. Cell Biol. 16:5434–44 [Google Scholar]
  79. Porter KR, Palade GE. 1957. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J. Biophys. Biochem. Cytol. 3:269–300 [Google Scholar]
  80. Prinz WA. 2010. Lipid trafficking sans vesicles: where, why, how?. Cell 143:6870–74 [Google Scholar]
  81. Prinz WA. 2014. Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J. Cell Biol. 205:6759–69 [Google Scholar]
  82. Raiborg C, Wenzel EM, Pedersen NM, Olsvik H, Schink KO. et al. 2015. Repeated ER-endosome contacts promote endosome translocation and neurite outgrowth. Nature 520:7546234–38 [Google Scholar]
  83. Raychaudhuri S, Im YJ, Hurley JH, Prinz WA. 2006. Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein–related proteins and phosphoinositides. J. Cell Biol. 173:1107–19 [Google Scholar]
  84. Raychaudhuri S, Prinz WA. 2010. The diverse functions of oxysterol-binding proteins. Annu. Rev. Cell Dev. Biol. 26:157–77 [Google Scholar]
  85. Reinisch KM, De Camilli P. 2016. SMP-domain proteins at membrane contact sites: structure and function. Biochim. Biophys. Acta 18618 Part B924–27 [Google Scholar]
  86. Rizo J, Südhof TC. 1998. C2-domains, structure and function of a universal Ca2+-binding domain. J. Biol. Chem. 273:2615879–82 [Google Scholar]
  87. Rosenbluth J. 1962. Subsurface cisterns and their relationship to the neuronal plasma membrane. J. Cell Biol. 13:405–21 [Google Scholar]
  88. Rowland AA, Chitwood PJ, Phillips MJ, Voeltz GK. 2014. ER contact sites define the position and timing of endosome fission. Cell 159:51027–41 [Google Scholar]
  89. Schaaf G, Ortlund EA, Tyeryar KR, Mousley CJ, Ile KE. et al. 2008. Functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the sec14 superfamily. Mol. Cell 29:2191–206 [Google Scholar]
  90. Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F. et al. 2014. Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510:7506552–55 [Google Scholar]
  91. Schekman R. 2002. Lasker Basic Medical Research Award. SEC mutants and the secretory apparatus. Nat. Med. 8:101055–58 [Google Scholar]
  92. Schrader M, Godinho LF, Costello JL, Islinger M. 2015. The different facets of organelle interplay: an overview of organelle interactions. Front. Cell Dev. Biol. 3:56 [Google Scholar]
  93. Schulz TA, Choi MG, Raychaudhuri S, Mears JA, Ghirlando R. et al. 2009. Lipid-regulated sterol transfer between closely apposed membranes by oxysterol-binding protein homologues. J. Cell Biol. 187:6889–903 [Google Scholar]
  94. Shore G, Tata J. 1977. Two fractions of rough endoplasmic reticulum from rat liver. I. Recovery of rapidly sedimenting endoplasmic reticulum in association with mitochondria. J. Cell Biol. 72:714–25 [Google Scholar]
  95. Skehel PA, Martin KC, Kandel ER, Bartsch D. 1995. A VAMP-binding protein from Aplysia required for neurotransmitter release. Science 269:52301580–83 [Google Scholar]
  96. Sleight RG, Pagano RE. 1983. Rapid appearance of newly synthesized phosphatidylethanolamine at the plasma membrane. J. Biol. Chem. 258:159050–58 [Google Scholar]
  97. Soboloff J, Rothberg BS, Madesh M, Gill DL. 2012. STIM proteins: dynamic calcium signal transducers. Nat. Rev. Mol. Cell Biol. 13:9549–65 [Google Scholar]
  98. Sprong H, van der Sluijs P, van Meer G. 2001. How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2:7504–13 [Google Scholar]
  99. Steck TL, Ye J, Lange Y. 2002. Probing red cell membrane cholesterol movement with cyclodextrin. Biophys. J. 83:42118–25 [Google Scholar]
  100. Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD. 2011. Osh proteins regulate phosphoinositide metabolism at ER–plasma membrane contact sites. Cell 144:3389–401 [Google Scholar]
  101. Stefan CJ, Manford AG, Emr SD. 2013. ER-PM connections: sites of information transfer and inter-organelle communication. Curr. Opin. Cell Biol. 25:4434–42 [Google Scholar]
  102. Sutton RB, Fasshauer D, Jahn R, Brunger AT. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395:6700347–53 [Google Scholar]
  103. Suzuki E, Hirosawa K. 1994. Immunolocalization of a Drosophila phosphatidylinositol transfer protein (rdgB) in normal and rdgA mutant photoreceptor cells with special reference to the subrhabdomeric cisternae. J. Electron Microsc. 43:4183–89 [Google Scholar]
  104. Takeshima H, Hoshijima M, Song LS. 2015. Ca2+ microdomains organized by junctophilins. Cell Calcium 58:4349–56 [Google Scholar]
  105. Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K. 2000. Junctophilins: a novel family of junctional membrane complex proteins. Mol. Cell 6:111–22 [Google Scholar]
  106. Urbani L, Simoni RD. 1990. Cholesterol and vesicular stomatitis virus G protein take separate routes from the endoplasmic reticulum to the plasma membrane. J. Biol. Chem. 265:41919–23 [Google Scholar]
  107. Van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9:2112–24 [Google Scholar]
  108. Vance JE. 1990. Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 265:137248–56 [Google Scholar]
  109. Vance JE, Aasman EJ, Szarka R. 1991. Brefeldin A does not inhibit the movement of phosphatidylethanolamine from its sites for synthesis to the cell surface. J. Biol. Chem. 266:138241–47 [Google Scholar]
  110. Warnock DE, Lutz MS, Blackburn WA, Young WW, Baenziger JU. 1994. Transport of newly synthesized glucosylceramide to the plasma membrane by a non-Golgi pathway. PNAS 91:72708–12 [Google Scholar]
  111. Weninger K, Bowen ME, Chu S, Brunger AT. 2003. Single-molecule studies of SNARE complex assembly reveal parallel and antiparallel configurations. PNAS 100:2514800–5 [Google Scholar]
  112. West M, Zurek N, Hoenger A, Voeltz GK. 2011. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J. Cell Biol. 193:2333–46 [Google Scholar]
  113. Wolf W, Kilic A, Schrul B, Lorenz H, Schwappach B, Seedorf M. 2012. Yeast Ist2 recruits the endoplasmic reticulum to the plasma membrane and creates a ribosome-free membrane microcompartment. PLOS ONE 7:7e39703 [Google Scholar]
  114. Wu MM, Buchanan J, Luik RM, Lewis RS. 2006. Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J. Cell Biol. 174:6803–13 [Google Scholar]
  115. Xu J, Bacaj T, Zhou A, Tomchick DR, Südhof TC, Rizo J. 2014. Structure and Ca2+-binding properties of the tandem C2 domains of E-Syt2. Structure 22:2269–80 [Google Scholar]
  116. Yoder MD, Thomas LM, Tremblay JM, Oliver RL, Yarbrough LR, Helmkamp GM. 2001. Structure of a multifunctional protein. Mammalian phosphatidylinositol transfer protein complexed with phosphatidylcholine. J. Biol. Chem. 276:129246–52 [Google Scholar]
  117. Zhang L, Yan F, Zhang S, Lei D, Charles MA. et al. 2012. Structural basis of transfer between lipoproteins by cholesteryl ester transfer protein. Nat. Chem. Biol. 8:4342–49 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-111315-125024
Loading
/content/journals/10.1146/annurev-cellbio-111315-125024
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error