Membrane contact sites: Complex zones for membrane association and lipid Exchange

Lipid Insights

Volumn 2015, Issue , 2015, Pages 55-63

  Quon, Evan ^a   Beh, Christopher T ^a,b  

^a SIMON FRASER UNIVERSITY   (Canada)

^b SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Endoplasmic reticulum; Lipid transfer proteins; Membrane contact sites; Membrane lipids; Membrane tethering proteins; Nonvesicular transport; Plasma membrane

Indexed keywords

ARTICLE; BINDING SITE; CELL MEMBRANE; CELL VACUOLE; COMPLEX FORMATION; ENDOPLASMIC RETICULUM; HUMAN; ION TRANSPORT; LIPID METABOLISM; LIPID TRANSPORT; MEMBRANE BINDING; MEMBRANE STRUCTURE; NONHUMAN;

EID: 85013477437     PISSN: None     EISSN: 11786353     Source Type: Journal    
DOI: 10.4137/Lpi.s37190     Document Type: Article

References (115)

1. Levine T. Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions. Trends Cell Biol. 2004;14(9):483-490.
2. Lev S. Non-vesicular lipid transport by lipid-transfer proteins and beyond. Nat Rev Mol Cell Biol. 2010;11(10):739-750.
3. Lev S. Nonvesicular lipid transfer from the endoplasmic reticulum. Cold Spring Harb Perspect Biol. 2012;4(10):a013300.
4. West M, Zurek N, Hoenger A, Voeltz GK. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J Cell Biol. 2011;193(2):333-346.
5. Porter KR, Palade GE. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J Biophys Biochem Cytol. 1957;3(2): 269-300.
6. Henkart M, Landis DM, Reese TS. Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons. J Cell Biol. 1976; 70(2 pt 1):338-347.
7. Levine TP, Munro S. Dual targeting of Osh1p, a yeast homologue of oxysterolbinding protein, to both the Golgi and the nucleus-vacuole junction. Mol Biol Cell. 2001;12(6):1633-1644.
8. Hönscher C, Ungermann C. A close-up view of membrane contact sites between the endoplasmic reticulum and the endolysosomal system: from yeast to man. Crit Rev Biochem Mol Biol. 2014;9238(3):1-7.
9. Helle SCJ, Kanfer G, Kolar K, Lang A, Michel AH, Kornmann B. Organization and function of membrane contact sites. Biochim Biophys Acta. 2013;1833(11): 2526-2541.
10. Lang A, John Peter AT, Kornmann B. ER-mitochondria contact sites in yeast: beyond the myths of ERMES. Curr Opin Cell Biol. 2015;35:7-12.
11. Yamaji T, Kumagai K, Tomishige N, Hanada K. Two sphingolipid transfer proteins, CERT and FAPP2: their roles in sphingolipid metabolism. IUBMB Life. 2008;60(8):511-518.
12. Alpy F, Tomasetto C. START ships lipids across interorganelle space. Biochimie. 2014;96(1):85-95.
13. Kvam E, Goldfarb DS. Nvj1p is the outer-nuclear-membrane receptor for oxysterol-binding protein homolog Osh1p in Saccharomyces cerevisiae. J Cell Sci. 2004;117(pt 21):4959-4968.
14. Loewen CJR, Roy A, Levine TP. A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 2003;22(9): 2025-2035.
15. Schulz TA, Choi MG, Raychaudhuri S, et al. Lipid-regulated sterol transfer between closely apposed membranes by oxysterol-binding protein homologues. J Cell Biol.2009;187(6):889-903.
16. Toulmay A, Prinz WA. Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr Opin Cell Biol. 2011;23(4):458-463.
17. Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD. Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell. 2011;144(3):389-401.
18. Chung J, Torta F, Masai K, et al. PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts. Science. 2015;349(6246):428-432.
19. Moser von Filseck J, Opi A, Delfosse V, et al. Phosphatidylserine transport by ORP/Osh proteins is driven by phosphatidylinositol 4-phosphate. Science. 2015; 349(6246):432-436.
20. Moser von Filseck J, Vanni S, Mesmin B, Antonny B, Drin G. A phosphatidylinositol- 4-phosphate powered exchange mechanism to create a lipid gradient between membranes. Nat Commun. 2015;6:6671.
21. Alfaro G, Johansen J, Dighe SA, Duamel G, Kozminski KG, Beh CT. The sterol-binding protein Kes1/Osh4p is a regulator of polarized exocytosis. Traffic. 2011;12(11):1521-1536.
22. Menon AK, Levine TP. Cell biology: countercurrents in lipid flow. Nature. 2015;525(7568):191-192.
23. Georgiev AG, Sullivan DP, Kersting MC, Dittman JS, Beh CT, Menon AK. Osh proteins regulate membrane sterol organization but are not required for sterol movement between the ER and PM. Traffic. 2011;12(10):1341-1355.
24. Beh CT, McMaster CR, Kozminski KG, Menon AK. A detour for yeast oxysterol binding proteins. J Biol Chem. 2012;287(14):11481-11488.
25. LeBlanc MA, McMaster CR. Lipid binding requirements for oxysterol-binding protein Kes1 inhibition of autophagy and endosome-trans-Golgi trafficking pathways. J Biol Chem. 2010;285(44):33875-33884.
26. Vance JE. Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem. 1990;265(13):7248-7256.
27. Voelker DR. Bridging gaps in phospholipid transport. Trends Biochem Sci. 2005;30(7):396-404.
28. Horvath SE, Daum G. Lipids of mitochondria. Prog Lipid Res. 2013;52(4):590-614.
29. Flis VV, Daum G. Lipid transport between the endoplasmic. Cold Spring Harb Perspect Biol. 2013;5(6):a013235.
30. Klug L, Daum G. Yeast lipid metabolism at a glance. FEMS Yeast Res. 2014; 14(3):369-388.
31. Pichler H, Gaigg B, Hrastnik C, et al. A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids. Eur J Biochem. 2001;268(8):2351-2361.
32. Prinz WA. Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J Cell Biol. 2014;205(6):759-769.
33. Schneggenburger R, Rosenmund C. Molecular mechanisms governing Ca(2+) regulation of evoked and spontaneous release. Nat Neurosci. 2015;18(7): 935-941.
34. López-Crisosto C, Bravo-Sagua R, Rodriguez-Peña M, et al. ER-to-mitochondria miscommunication and metabolic diseases. Biochim Biophys Acta. 2015; 1852(10 pt A):2096-2105.
35. Park CY, Hoover PJ, Mullins FM, et al. STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell. 2009;136(5):876-890.
36. Liou J, Kim ML, Heo WD, et al. STIM is a Ca2+ sensor essential for Ca2+- store-depletion triggered Ca2+ influx. Curr Biol. 2005;15(13):1235-1241.
37. Feske S, Gwack Y, Prakriya M, et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature. 2006;441(7090):179-185.
38. Korzeniowski MK, Popovic MA, Szentpetery Z, Varnai P, Stojilkovic SS, Balla T. Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides. J Biol Chem. 2009;284(31):21027-21035.
39. Henne WM, Liou J, Emr SD. Molecular mechanisms of inter-organelle ER-PM contact sites. Curr Opin Cell Biol. 2015;35:123-130.
40. McLean LR, Phillips MC. Mechanism of cholesterol and phosphatidylcholine exchange or transfer between unilamellar vesicles. Biochemistry. 1981;20(10): 2893-2900.
41. Ferrell JE, Lee KJ, Huestis WH. Lipid transfer between phosphatidylcholine vesicles and human erythrocytes: exponential decrease in rate with increasing acyl chain length. Biochemistry. 1985;24(12):2857-2864.
42. Phillips MC, Johnson WJ, Rothblat GH. Mechanisms and consequences of cellular cholesterol exchange and transfer. Biochim Biophys Acta. 1987;906(2):223-276.
43. Prinz WA. Lipid trafficking sans vesicles: where, why, how? Cell. 2010;143(6): 870-874.
44. Petkovic M, Jemaiel A, Daste F, et al. The SNARE Sec22b has a non-fusogenic function in plasma membrane expansion. Nat Cell Biol. 2014;16(5):434-444.
45. Merklinger E, Schloetel JG, Spitta L, Thiele C, Lang T. No evidence for spontaneous lipid transfer at ER-PM membrane contact sites. J Membr Biol. 2015;248(1): 1-16.
46. Schauder CM, Wu X, Saheki Y, et al. Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature. 2014;510(7506):552-555.
47. Lee I, Hong W. Diverse membrane-associated proteins contain a novel SMP domain. FASEB J. 2006;20(2):202-206.
48. Min SW, Chang WP, Südhof TC. E-Syts, a family of membranous Ca2+-sensor proteins with multiple C2 domains. Proc Natl Acad Sci U S A. 2007;104(10): 3823-3828.
49. Giordano F, Saheki Y, Idevall-Hagren O, et al. PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell. 2013;153(7):1494-1509.
50. Kopec KO, Alva V, Lupas AN. Homology of SMP domains to the TULIP superfamily of lipid-binding proteins provides a structural basis for lipid exchange between ER and mitochondria. Bioinformatics. 2010;26(16):1927-1931.
51. Chang C-L, Hsieh T-S, Yang TT, et al. Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep. 2013;5(3):813-825.
52. Kornmann B, Currie E, Collins SR, et al. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science. 2009;325(5939):477-481.
53. AhYoung AP, Jiang J, Zhang J, et al. Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc Natl Acad Sci U S A. 2015;122(25):3179-3188.
54. Stocco DM, Clark BJ. Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem Pharmacol. 1996;51(806):197-205.
55. Stocco DM. StAR protein and the regulation of steroid hormone biosynthesis. Annu Rev Physiol. 2001;63:193-213.
56. Soccio RE, Breslow JL. StAR-related lipid transfer (START) proteins: mediators of intracellular lipid metabolism. J Biol Chem. 2003;278(25):22183-22186.
57. Alpy F, Stoeckel ME, Dierich A, et al. The steroidogenic acute regulatory protein homolog MLN64, a late endosomal cholesterol-binding protein. J Biol Chem. 2001;276(6):4261-4269.
58. Alpy F, Latchumanan VK, Kedinger V, et al. Functional characterization of the MENTAL domain. J Biol Chem. 2005;280(18):17945-17952.
59. Alpy F, Rousseau A, Schwab Y, et al. STARD3 or STARD3NL and VAP form a novel molecular tether between late endosomes and the ER. J Cell Sci. 2013; 126(23):5500-5512.
60. Murcia M, Faráldo-Gómez JD, Maxfield FR, Roux B. Modeling the structure of the StART domains of MLN64 and StAR proteins in complex with cholesterol. J Lipid Res. 2006;47(12):2614-2630.
61. Kishida T, Kostetskii I, Zhang Z, et al. Targeted mutation of the MLN64 START domain causes only modest alterations in cellular sterol metabolism. J Biol Chem. 2004;279(18):19276-19285.
62. Romanowski MJ, Soccio RE, Breslow JL, Burley SK. Crystal structure of the Mus musculus cholesterol-regulated START protein 4 (StarD4) containing a StARrelated lipid transfer domain. Proc Natl Acad Sci U S A. 2002;99(10):6949-6954.
63. Gatta AT, Wong LH, Sere YY, et al. A new family of StART domain proteins at membrane contact sites has a role in ER-PM sterol transport. Elife. 2015;4:1-21.
64. Murley A, Sarsam RD, Toulmay A, Yamada J, Prinz WA, Nunnari J. Ltc1 is an ER-localized sterol transporter and a component of ER-mitochondria and ERvacuole contacts. J Cell Biol. 2015;1:539-548.
65. Elbaz-Alon Y, Eisenberg-Bord M, Shinder V, et al. Lam6 regulates the extent of contacts between organelles. Cell Rep. 2015;12(1):7-14.
66. Manford AG, Stefan CJ, Yuan HL, Macgurn JA, Emr SD. ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev Cell. 2012;23(6):1129-1140.
67. Toulmay A, Prinz WA. A conserved membrane-binding domain targets proteins to organelle contact sites. J Cell Sci. 2012;125(1):49-58.
68. Creutz CE, Snyder SL, Schulz TA. Characterization of the yeast tricalbins: membrane-bound multi-C2-domain proteins that form complexes involved in membrane trafficking. Cell Mol Life Sci. 2004;61(10):1208-1220.
69. Tarassov K, Messier V, Landry CR, et al. An in vivo map of the yeast protein interactome. Science. 2008;320(5882):1465-1470.
70. Babu M, Vlasblom J, Pu S, et al. Interaction landscape of membrane-protein complexes in Saccharomyces cerevisiae. Nature. 2012;489(7417):585-589.
71. Elbaz Y, Schuldiner M. Staying in touch: the molecular era of organelle contact sites. Trends Biochem Sci. 2011;36(11):616-623.
72. Zachowski A. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem J. 1993;294(pt 1):1-14.
73. Pomorski T, Holthuis JCM, Herrmann A, van Meer G. Tracking down lipid flippases and their biological functions. J Cell Sci. 2004;117(pt 6):805-813.
74. Simons K, Sampaio JL. Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol. 2011;3(10):a004697.
75. Voeltz GK, Rolls MM, Rapoport TA. Structural organization of the endoplasmic reticulum. EMBO Rep. 2002;3(10):944-950.
76. van Meer G, Sprong H. Membrane lipids and vesicular traffic. Curr Opin Cell Biol. 2004;16(4):373-378.
77. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell. 2006;124(3): 573-586.
78. Hu J, Shibata Y, Voss C, et al. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science. 2008;319(5867):1247-1250.
79. Yang YS, Strittmatter SM. The reticulons: a family of proteins with diverse functions. Genome Biol. 2007;8(12):234.
80. Hu J, Shibata Y, Zhu PP, et al. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell. 2009;138(3):549-561.
81. Anwar K, Klemm RW, Condon A, et al. The dynamin-like GTPase Sey1p mediates homotypic ER fusion in S. cerevisiae. J Cell Biol. 2012;197(2):209-217.
82. Rogers JV, Arlow T, Inkellis ER, Koo TS, Rose MD. ER-associated SNAREs and Sey1p mediate nuclear fusion at two distinct steps during yeast mating. Mol Biol Cell. 2013;24(24):3896-3908.
83. Voss C, Lahiri S, Young BP, Loewen CJ, Prinz WA. ER-shaping proteins facilitate lipid exchange between the ER and mitochondria in S. cerevisiae. J Cell Sci. 2012;125(pt 20):4791-4799.
84. Bollen IC, Higgins JA. Phospholipid asymmetry in rough- and smoothendoplasmic- reticulum membranes of untreated and phenobarbital-treated rat liver. Biochem J. 1980;189(3):475-480.
85. Fairn GD, Schieber NL, Ariotti N, et al. High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine. J Cell Biol. 2011;194(2): 257-275.
86. Leventis PA, Grinstein S. The distribution and function of phosphatidylserine in cellular membranes. Annu Rev Biophys. 2010;39(1):407-427.
87. McLaughlin S, Murray D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature. 2005;438(7068):605-611.
88. Sun Y, Thapa N, Hedman AC, Anderson RA. Phosphatidylinositol 4,5-bisphosphate: targeted production and signaling. Bioessays. 2013;35(6):513-522.
89. Fischer MA, Temmerman K, Ercan E, Nickel W, Seedorf M. Binding of plasma membrane lipids recruits the yeast integral membrane protein Ist2 to the cortical ER. Traffic. 2009;10(8):1084-1097.
90. Ercan E, Momburg F, Engel U, Temmerman K, Nickel W, Seedorf M. A conserved, lipid-mediated sorting mechanism of yeast Ist2 and mammalian STIM proteins to the peripheral ER. Traffic. 2009;10(12):1802-1818.
91. Loewen CJR, Young BP, Tavassoli S, Levine TP. Inheritance of cortical ER in yeast is required for normal septin organization. J Cell Biol. 2007;179(3): 467-483.
92. Wilson JD, Thompson SL, Barlowe C. Yet1p-Yet3p interacts with Scs2p-Opi1p to regulate ER localization of the Opi1p repressor. Mol Biol Cell. 2011;22(9): 1430-1439.
93. Chao JT, Wong AKO, Tavassoli S, et al. Polarization of the endoplasmic reticulum by ER-septin tethering. Cell. 2014;158(3):620-632.
94. Kagiwada S, Hashimoto M. The yeast VAP homolog Scs2p has a phosphoinositide-binding ability that is correlated with its activity. Biochem Biophys Res Commun. 2007;364(4):870-876.
95. Tong J, Yang H, Yang H, Eom SH, Im YJ. Structure of Osh3 reveals a conserved mode of phosphoinositide binding in oxysterol-binding proteins. Structure. 2013;21(7):1203-1213.
96. Im YJ, Raychaudhuri S, Prinz WA, Hurley JH. Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature. 2005;437(7055): 154-158.
97. Maleth J, Choi S, Muallem S, Ahuja M. Translocation between PI(4,5)P2-poor and PI(4,5)P2-rich microdomains during store depletion determines STIM1 conformation and Orai1 gating. Nat Commun. 2014;5(5843):1-10.
98. Hammond GRV, Fischer MJ, Anderson KE, et al. PI4P and PI(4,5)P2 are essential but independent lipid determinants of membrane identity. Science. 2012; 337(6095):727-730.
99. Hughes WE, Woscholski R, Cooke FT, et al. SAC1 encodes a regulated lipid phosphoinositide phosphatase, defects in which can be suppressed by the homologous Inp52p and Inp53p phosphatases. J Biol Chem. 2000;275(2):801-808.
100. Loewen CJR, Gaspar ML, Jesch SA, et al. Phospholipid metabolism regulated by a transcription factor sensing phosphatidic acid. Science. 2004;304(5677): 1644-1647.
101. Beh CT, Rine J. A role for yeast oxysterol-binding protein homologs in endocytosis and in the maintenance of intracellular sterol-lipid distribution. J Cell Sci. 2004;117(pt 14):2983-2996.
102. Baumann NA, Sullivan DP, Ohvo-Rekilä H, et al. Transport of newly synthesized sterol to the sterol-enriched plasma membrane occurs via nonvesicular equilibration. Biochemistry. 2005;44:5816-5826.
103. Steck TL, Ye J, Lange Y. Probing red cell membrane cholesterol movement with cyclodextrin. Biophys J. 2002;83(4):2118-2125.
104. Choubey A, Kalia RK, Malmstadt N, Nakano A, Vashishta P. Cholesterol translocation in a phospholipid membrane. Biophys J. 2013;104(11):2429-2436.
105. Muthusamy BP, Raychaudhuri S, Natarajan P, et al. Control of protein and sterol trafficking by antagonistic activities of a type IV P-type ATPase and oxysterol binding protein homologue. Mol Biol Cell. 2009;20(12):2920-2931.
106. Menon AK. Flippases. Trends Cell Biol. 1995;5(9):355-360.
107. van Meer G, Halter D, Sprong H, Somerharju P, Egmond MR. ABC lipid transporters: extruders, flippases, or flopless activators? FEBS Lett. 2006;580(4): 1171-1177.
108. Pomorski T, Menon AK. Lipid flippases and their biological functions. Cell Mol Life Sci. 2006;63(24):2908-2921.
109. Devaux PF, Herrmann A, Ohlwein N, Kozlov MM. How lipid flippases can modulate membrane structure. Biochim Biophys Acta. 2008;1778(7-8):1591-1600.
110. Puts CF, Lenoir G, Krijgsveld J, Williamson P, Holthuis JCM. A P4-ATPase protein interaction network reveals a link between aminophospholipid transport and phosphoinositide metabolism research articles. J Proteome Res. 2010;9: 833-842.
111. Daleke DL. Phospholipid flippases. J Biol Chem. 2007;282(2):821-825.
112. Malvezzi M, Chalat M, Janjusevic R, et al. Ca2+-dependent phospholipid scrambling by a reconstituted TMEM16 ion channel. Nat Commun. 2013;4:1-9.
113. Kim YJ, Wisniewski E, Kim YJ, Wisniewski E, Balla T. Phosphatidylinositolphosphatidic acid exchange by Nir2 at ER-PM contact sites maintains article phosphatidylinositol-phosphatidic acid exchange by Nir2 at ER-PM contact sites maintains phosphoinositide signaling competence. Dev Cell. 2015;33(5): 549-561.
114. Kim S, Kedan A, Marom M, et al. The phosphatidylinositol-transfer protein Nir2 binds phosphatidic acid and positively regulates phosphoinositide signalling. EMBO Rep. 2013;14(10):891-899.
115. Trivedi D, Padinjat R. RdgB proteins: functions in lipid homeostasis and signal transduction. Biochim Biophys Acta. 2007;1771:692-699.