1932

Abstract

To maintain an asymmetric distribution of ions across membranes, protein pumps displace ions against their concentration gradient by using chemical energy. Here, we describe a functionally analogous but topologically opposite process that applies to the lipid transfer protein (LTP) oxysterol-binding protein (OSBP). This multidomain protein exchanges cholesterol for the phosphoinositide phosphatidylinositol 4-phosphate [PI(4)P] between two apposed membranes. Because of the subsequent hydrolysis of PI(4)P, this counterexchange is irreversible and contributes to the establishment of a cholesterol gradient along organelles of the secretory pathway. The facts that some natural anti-cancer molecules block OSBP and that many viruses hijack the OSBP cycle for the formation of intracellular replication organelles highlight the importance and potency of OSBP-mediated lipid exchange. The architecture of some LTPs is similar to that of OSBP, suggesting that the principles of the OSBP cycle—burning PI(4)P for the vectorial transfer of another lipid—might be general.

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2018-06-20
2024-12-05
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Literature Cited

  1. 1.  Taylor FR, Saucier SE, Shown EP, Parish EJ, Kandutsch AA 1984. Correlation between oxysterol binding to a cytosolic binding protein and potency in the repression of hydroxymethylglutaryl coenzyme A reductase. J. Biol. Chem. 259:12382–87
    [Google Scholar]
  2. 2.  Luu W, Sharpe LJ, Capell-Hattam I, Gelissen IC, Brown AJ 2016. Oxysterols: old tale, new twists. Annu. Rev. Pharmacol. Toxicol. 56:447–67
    [Google Scholar]
  3. 3.  Ridgway ND, Dawson PA, Ho YK, Brown MS, Goldstein JL 1992. Translocation of oxysterol binding protein to Golgi apparatus triggered by ligand binding. J. Cell Biol. 116:307–19
    [Google Scholar]
  4. 4.  Suchanek M, Hynynen R, Wohlfahrt G, Lehto M, Johansson M et al. 2007. The mammalian oxysterol-binding protein-related proteins (ORPs) bind 25-hydroxycholesterol in an evolutionarily conserved pocket. Biochem. J. 405:473–80
    [Google Scholar]
  5. 5.  Nishimura T, Inoue T, Shibata N, Sekine A, Takabe W et al. 2005. Inhibition of cholesterol biosynthesis by 25-hydroxycholesterol is independent of OSBP. Genes Cells 10:793–801
    [Google Scholar]
  6. 6.  Olsen BN, Schlesinger PH, Baker NA 2009. Perturbations of membrane structure by cholesterol and cholesterol derivatives are determined by sterol orientation. J. Am. Chem. Soc. 131:4854–65
    [Google Scholar]
  7. 7.  Theunissen JJH, Jackson RL, Kempen HJM, Demel RA 1986. Membrane properties of oxysterols. Interfacial orientation, influence on membrane permeability and redistribution between membranes. Biochim. Biophys. Acta 860:66–74
    [Google Scholar]
  8. 8.  Infante RE, Abi-Mosleh L, Radhakrishnan A, Dale JD, Brown MS, Goldstein JL 2008. Purified NPC1 protein. I. Binding of cholesterol and oxysterols to a 1278-amino acid membrane protein. J. Biol. Chem. 283:1052–63
    [Google Scholar]
  9. 9.  Li J, Pfeffer SR 2016. Lysosomal membrane glycoproteins bind cholesterol and contribute to lysosomal cholesterol export. eLife 5:19316
    [Google Scholar]
  10. 10.  Huang P, Nedelcu D, Watanabe M, Jao C, Kim Y et al. 2016. Cellular cholesterol directly activates Smoothened in Hedgehog signaling. Cell 166:1176–87
    [Google Scholar]
  11. 11.  Luchetti G, Sircar R, Kong JH, Nachtergaele S, Sagner A et al. 2016. Cholesterol activates the G-protein coupled receptor Smoothened to promote Hedgehog signaling. eLife 5:1055
    [Google Scholar]
  12. 12.  Im YJ, Raychaudhuri S, Prinz WA, Hurley JH 2005. Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 437:154–58
    [Google Scholar]
  13. 13.  Lagace TA, Byers DM, Cook HW, Ridgway ND 1999. Chinese hamster ovary cells overexpressing the oxysterol binding protein (OSBP) display enhanced synthesis of sphingomyelin in response to 25-hydroxycholesterol. J. Lipid Res. 40:109–16
    [Google Scholar]
  14. 14.  Wakana Y, Kotake R, Oyama N, Murate M, Kobayashi T et al. 2015. CARTS biogenesis requires VAP-lipid transfer protein complexes functioning at the endoplasmic reticulum-Golgi interface. Mol. Biol. Cell 26:4686–99
    [Google Scholar]
  15. 15.  Fang M, Kearns BG, Gedvilaite A, Kagiwada S, Kearns M et al. 1996. Kes1p shares homology with human oxysterol binding protein and participates in a novel regulatory pathway for yeast Golgi-derived transport vesicle biogenesis. EMBO J 15:6447–59
    [Google Scholar]
  16. 16.  Jiang B, Brown JL, Sheraton J, Fortin N, Bussey H 1994. A new family of yeast genes implicated in ergosterol synthesis is related to the human oxysterol binding protein. Yeast 10:341–53
    [Google Scholar]
  17. 17.  Alphey L, Jimenez J, Glover D 1998. A Drosophila homologue of oxysterol binding protein (OSBP)–implications for the role of OSBP. Biochim. Biophys. Acta 1395:159–64
    [Google Scholar]
  18. 18.  Jaworski CJ, Moreira E, Li A, Lee R, Rodriguez IR 2001. A family of 12 human genes containing oxysterol-binding domains. Genomics 78:185–96
    [Google Scholar]
  19. 19.  Lehto M, Laitinen S, Chinetti G, Johansson M, Ehnholm C et al. 2001. The OSBP-related protein family in humans. J. Lipid Res. 42:1203–13
    [Google Scholar]
  20. 20.  Laitinen S, Olkkonen VM, Ehnholm C, Ikonen E 1999. Family of human oxysterol binding protein (OSBP) homologues. A novel member implicated in brain sterol metabolism. J. Lipid Res. 40:2204–11
    [Google Scholar]
  21. 21.  Beh CT, Cool L, Phillips J, Rine J 2001. Overlapping functions of the yeast oxysterol-binding protein homologues. Genetics 157:1117–40
    [Google Scholar]
  22. 22.  Olkkonen VM. 2015. OSBP-related protein family in lipid transport over membrane contact sites. Lipid Insights 8:Suppl. 11–9
    [Google Scholar]
  23. 23.  Levine TP, Munro S 1998. The pleckstrin homology domain of oxysterol-binding protein recognises a determinant specific to Golgi membranes. Curr. Biol. 8:13729–39
    [Google Scholar]
  24. 24.  Levine TP, Munro S 2002. Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr. Biol. 12:695–704
    [Google Scholar]
  25. 25.  Loewen CJR, Roy A, Levine TP 2003. A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J 22:2025–35
    [Google Scholar]
  26. 26.  Wyles JP, McMaster CR, Ridgway ND 2002. Vesicle-associated membrane protein-associated protein-A (VAP-A) interacts with the oxysterol-binding protein to modify export from the endoplasmic reticulum. J. Biol. Chem. 277:29908–18
    [Google Scholar]
  27. 27.  Hanada K, Kumagai K, Yasuda S, Miura Y, Kawano M et al. 2003. Molecular machinery for non-vesicular trafficking of ceramide. Nature 426:803–9
    [Google Scholar]
  28. 28.  Levine TP. 2004. Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions. Trends Cell Biol 14:483–90
    [Google Scholar]
  29. 29.  DiNitto JP, Lambright DG 2006. Membrane and juxtamembrane targeting by PH and PTB domains. Biochim. Biophys. Acta 1761:850–67
    [Google Scholar]
  30. 30.  Godi A, Di Campli A, Konstantakopoulos A, Di Tullio G, Alessi DR et al. 2004. FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat. Cell Biol. 6:393–404
    [Google Scholar]
  31. 31.  Liu Y, Kahn RA, Prestegard JH 2014. Interaction of Fapp1 with Arf1 and PI4P at a membrane surface: an example of coincidence detection. Structure 22:421–30
    [Google Scholar]
  32. 32.  Prashek J, Truong T, Yao X 2013. Crystal structure of the pleckstrin homology domain from the ceramide transfer protein: implications for conformational change upon ligand binding. PLOS ONE 8:e79590
    [Google Scholar]
  33. 33.  He J, Scott JL, Heroux A, Roy S, Lenoir M et al. 2011. Molecular basis of phosphatidylinositol 4-phosphate and ARF1 GTPase recognition by the FAPP1 pleckstrin homology (PH) domain. J. Biol. Chem. 286:18650–57
    [Google Scholar]
  34. 34.  Lenoir M, Coskun Ü, Grzybek M, Cao X, Buschhorn SB et al. 2010. Structural basis of wedging the Golgi membrane by FAPP pleckstrin homology domains. EMBO Rep 11:279–84
    [Google Scholar]
  35. 35.  Sugiki T, Takeuchi K, Yamaji T, Takano T, Tokunaga Y et al. 2012. Structural basis for the Golgi association by the pleckstrin homology domain of the ceramide trafficking protein (CERT). J. Biol. Chem. 287:33706–18
    [Google Scholar]
  36. 36.  D'Angelo G, Polishchuk E, Di Tullio G, Santoro M, Di Campli A et al. 2007. Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide. Nature 449:715862–67
    [Google Scholar]
  37. 37.  Lenoir M, Grzybek M, Majkowski M, Rajesh S, Kaur J et al. 2015. Structural basis of dynamic membrane recognition by trans-Golgi network specific FAPP proteins. J. Mol. Biol. 427:966–81
    [Google Scholar]
  38. 38.  Manneville J-B, Casella J-F, Ambroggio EE, Gounon P, Bertherat J et al. 2008. COPI coat assembly occurs on liquid-disordered domains and the associated membrane deformations are limited by membrane tension. PNAS 105:16946–51
    [Google Scholar]
  39. 39.  Balla A, Tuymetova G, Tsiomenko A, Várnai P, Balla T 2005. A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type-III alpha: studies with the PH domains of the oxysterol binding protein and FAPP1. Mol. Biol. Cell 16:1282–95
    [Google Scholar]
  40. 40.  Dong R, Saheki Y, Swarup S, Lucast L, Harper JW, De Camilli P 2016. Endosome-ER contacts control actin nucleation and retromer function through VAP-dependent regulation of PI4P. Cell 166:408–23
    [Google Scholar]
  41. 41.  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 1861:952–61
    [Google Scholar]
  42. 42.  Bigay J, Antonny B 2012. Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev. Cell 23:886–95
    [Google Scholar]
  43. 43.  Holthuis JCM, Menon AK 2014. Lipid landscapes and pipelines in membrane homeostasis. Nature 510:48–57
    [Google Scholar]
  44. 44.  Jackson CL, Walch L, Verbavatz J-M 2016. Lipids and their trafficking: an integral part of cellular organization. Dev. Cell 39:139–53
    [Google Scholar]
  45. 45.  Kaiser SE, Brickner JH, Reilein AR, Fenn TD, Walter P, Brunger AT 2005. Structural basis of FFAT motif-mediated ER targeting. Structure 13:1035–45
    [Google Scholar]
  46. 46.  Furuita K, Jee J, Fukada H, Mishima M, Kojima C 2010. Electrostatic interaction between oxysterol-binding protein and VAMP-associated protein A revealed by NMR and mutagenesis studies. J. Biol. Chem. 285:12961–70
    [Google Scholar]
  47. 47.  Weir ML, Xie H, Klip A, Trimble WS 2001. VAP-A binds promiscuously to both v- and tSNAREs. Biochem. Biophys. Res. Commun. 286:616–21
    [Google Scholar]
  48. 48.  Amarilio R, Ramachandran S, Sabanay H, Lev S 2005. Differential regulation of endoplasmic reticulum structure through VAP-Nir protein interaction. J. Biol. Chem. 280:5934–44
    [Google Scholar]
  49. 49.  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. 254:21–26
    [Google Scholar]
  50. 50.  Loewen CJR, Gaspar ML, Jesch SA, Delon C, Ktistakis NT et al. 2004. Phospholipid metabolism regulated by a transcription factor sensing phosphatidic acid. Science 304:1644–47
    [Google Scholar]
  51. 51.  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 155:830–43
    [Google Scholar]
  52. 52.  Weber-Boyvat M, Kentala H, Peränen J, Olkkonen VM 2015. Ligand-dependent localization and function of ORP–VAP complexes at membrane contact sites. Cell Mol. Life Sci. 72:1967–87
    [Google Scholar]
  53. 53.  Felberbaum R, Wilson NR, Cheng D, Peng J, Hochstrasser M 2012. Desumoylation of the endoplasmic reticulum membrane VAP family protein Scs2 by Ulp1 and SUMO regulation of the inositol synthesis pathway. Mol. Cell. Biol. 32:64–75
    [Google Scholar]
  54. 54.  Goto A, Liu X, Robinson C-A, Ridgway ND 2012. Multisite phosphorylation of oxysterol-binding protein regulates sterol binding and activation of sphingomyelin synthesis. Mol. Biol. Cell 23:3624–35
    [Google Scholar]
  55. 55.  Weber-Boyvat M, Kentala H, Lilja J, Vihervaara T, Hanninen R et al. 2015. OSBP-related protein 3 (ORP3) coupling with VAMP-associated protein A regulates R-Ras activity. Exp. Cell Res. 331:278–91
    [Google Scholar]
  56. 56.  Kumagai K, Kawano-Kawada M, Hanada K 2014. Phosphoregulation of the ceramide transport protein CERT at serine 315 in the interaction with VAMP-associated protein (VAP) for inter-organelle trafficking of ceramide in mammalian cells. J. Biol. Chem. 289:10748–60
    [Google Scholar]
  57. 57.  Drin G, Casella J-F, Gautier R, Boehmer T, Schwartz TU, Antonny B 2007. A general amphipathic α-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 14:138–46
    [Google Scholar]
  58. 58.  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. 173:107–19
    [Google Scholar]
  59. 59.  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. 195:965–78
    [Google Scholar]
  60. 60.  Moser von Filseck J, Vanni S, Mesmin B, Antonny B, Drin G 2015. A phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes. Nat. Commun. 6:6671
    [Google Scholar]
  61. 61.  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. 187:889–903
    [Google Scholar]
  62. 62.  Charman M, Colbourne TR, Pietrangelo A, Kreplak L, Ridgway ND 2014. Oxysterol-binding protein (OSBP)-related protein 4 (ORP4) is essential for cell proliferation and survival. J. Biol. Chem. 289:15705–17
    [Google Scholar]
  63. 63.  Liu X, Ridgway ND 2014. Characterization of the sterol and phosphatidylinositol 4-phosphate binding properties of Golgi-associated OSBP-related protein 9 (ORP9). PLOS ONE 9:e108368
    [Google Scholar]
  64. 64.  Goto A, Charman M, Ridgway ND 2016. Oxysterol-binding protein activation at endoplasmic reticulum-Golgi contact sites reorganizes phosphatidylinositol 4-phosphate pools. J. Biol. Chem. 291:1336–47
    [Google Scholar]
  65. 65.  Zhao K, Ridgway ND 2017. Oxysterol-binding protein-related protein 1L regulates cholesterol egress from the endo-lysosomal system. Cell Rep 19:1807–18
    [Google Scholar]
  66. 66.  Manik MK, Yang H, Tong J, Im YJ 2017. Structure of yeast OSBP-related protein Osh1 reveals key determinants for lipid transport and protein targeting at the nucleus-vacuole junction. Structure 25:617–29
    [Google Scholar]
  67. 67.  Godi A, Pertile P, Meyers R, Marra P, Di Tullio G et al. 1999. ARF mediates recruitment of PtdIns-4-OH kinase-β and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex. Nat. Cell. Biol. 1:280–87
    [Google Scholar]
  68. 68.  Minogue S, Waugh MG, De Matteis MA, Stephens DJ, Berditchevski F, Hsuan JJ 2006. Phosphatidylinositol 4-kinase is required for endosomal trafficking and degradation of the EGF receptor. J. Cell Sci. 119:571–81
    [Google Scholar]
  69. 69.  Balla A, Tuymetova G, Barshishat M, Geiszt M, Balla T 2002. Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J. Biol. Chem. 277:20041–50
    [Google Scholar]
  70. 70.  Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX et al. 2003. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114:299–310
    [Google Scholar]
  71. 71.  Mesmin B, Bigay J, Polidori J, Jamecna D, Lacas-Gervais S, Antonny B 2017. Sterol transfer, PI4P consumption, and control of membrane lipid order by endogenous OSBP. EMBO J 36:3156–74
    [Google Scholar]
  72. 72.  Wrenn SP, Kaler EW, Lee SP 1999. A fluorescence energy transfer study of lecithin-cholesterol vesicles in the presence of phospholipase C. J. Lipid Res. 40:1483–94
    [Google Scholar]
  73. 73.  Wilhelm LP, Wendling C, Védie B, Kobayashi T, Chenard MP et al. 2017. STARD3 mediates endoplasmic reticulum-to-endosome cholesterol transport at membrane contact sites. EMBO J 36:1412–33
    [Google Scholar]
  74. 74.  Charman M, Goto A, Ridgway ND 2017. Oxysterol binding protein recruitment and activity at the ER-Golgi interface are independent of Sac1. Traffic 18:519–29
    [Google Scholar]
  75. 75.  Beh CT, McMaster CR, Kozminski KG, Menon AK 2012. A detour for yeast oxysterol binding proteins. J. Biol. Chem. 287:11481–88
    [Google Scholar]
  76. 76.  Maxfield FR, van Meer G 2010. Cholesterol, the central lipid of mammalian cells. Curr. Opin. Cell Biol. 22:422–29
    [Google Scholar]
  77. 77.  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 144:389–401
    [Google Scholar]
  78. 78.  Blagoveshchenskaya A, Cheong FY, Rohde HM, Glover G, Knödler A et al. 2008. Integration of Golgi trafficking and growth factor signaling by the lipid phosphatase SAC1. J. Cell Biol. 180:803–12
    [Google Scholar]
  79. 79.  Manford A, Xia T, Saxena AK, Stefan C, Hu F et al. 2010. Crystal structure of the yeast Sac1: implications for its phosphoinositide phosphatase function. EMBO J 29:1489–98
    [Google Scholar]
  80. 80.  Cai Y, Deng Y, Horenkamp F, Reinisch KM, Burd CG 2014. Sac1-Vps74 structure reveals a mechanism to terminate phosphoinositide signaling in the Golgi apparatus. J. Cell Biol. 206:485–91
    [Google Scholar]
  81. 81.  Dickson EJ, Jensen JB, Vivas O, Kruse M, Traynor-Kaplan AE, Hille B 2016. Dynamic formation of ER-PM junctions presents a lipid phosphatase to regulate phosphoinositides. J. Cell Biol. 213:33–48
    [Google Scholar]
  82. 82.  Zewe JP, Wills RC, Sangappa S, Goulden BD, Hammond GR 2018. SAC1 degrades its lipid substrate PtdIns4P in the endoplasmic reticulum to maintain a steep chemical gradient with donor membranes. eLife 7:e35588
    [Google Scholar]
  83. 83.  Ma Z, Liu Z, Huang X 2010. OSBP- and FAN-mediated sterol requirement for spermatogenesis in Drosophila. Development 137:3775–84
    [Google Scholar]
  84. 84.  Iaea DB, Dikiy I, Kiburu I, Eliezer D, Maxfield FR 2015. STARD4 membrane interactions and sterol binding. Biochemistry 54:4623–36
    [Google Scholar]
  85. 85.  Dittman JS, Menon AK 2017. Speed limits for nonvesicular intracellular sterol transport. Trends Biochem. Sci. 42:90–97
    [Google Scholar]
  86. 86.  Hein MY, Hubner NC, Poser I, Cox J, Nagaraj N et al. 2015. A human interactome in three quantitative dimensions organized by stoichiometries and abundances. Cell 163:712–23
    [Google Scholar]
  87. 87.  Georgiev AG, Sullivan DP, Kersting MC, Dittman JS, Beh CT, Menon AK 2011. Osh proteins regulate membrane sterol organization but are not required for sterol movement between the ER and PM. Traffic 12:1341–55
    [Google Scholar]
  88. 88.  Gatta AT, Wong LH, Sere YY, Calderón-Noreña DM, Cockcroft S et al. 2015. A new family of StART domain proteins at membrane contact sites has a role in ER-PM sterol transport. eLife 4:400
    [Google Scholar]
  89. 89.  Altan-Bonnet N. 2017. Lipid tales of viral replication and transmission. Trends Cell Biol 27:201–13
    [Google Scholar]
  90. 90.  Hsu N-Y, Ilnytska O, Belov G, Santiana M, Chen Y-H et al. 2010. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141:799–811
    [Google Scholar]
  91. 91.  Berger KL, Kelly SM, Jordan TX, Tartell MA, Randall G 2011. Hepatitis C virus stimulates the phosphatidylinositol 4-kinase III alpha-dependent phosphatidylinositol 4-phosphate production that is essential for its replication. J. Virol. 85:8870–83
    [Google Scholar]
  92. 92.  Dorobantu CM, Albulescu L, Harak C, Feng Q, van Kampen M et al. 2015. Modulation of the host lipid landscape to promote RNA virus replication: the picornavirus encephalomyocarditis virus converges on the pathway used by hepatitis C virus. PLOS Pathog 11:e1005185
    [Google Scholar]
  93. 93.  Arita M. 2014. Phosphatidylinositol-4 kinase III beta and oxysterol-binding protein accumulate unesterified cholesterol on poliovirus-induced membrane structure. Microbiol. Immunol. 58:239–56
    [Google Scholar]
  94. 94.  Roulin PS, Lötzerich M, Torta F, Tanner LB, van Kuppeveld FJM et al. 2014. Rhinovirus uses a phosphatidylinositol 4-phosphate/cholesterol counter-current for the formation of replication compartments at the ER-Golgi interface. Cell Host Microbe 16:677–90
    [Google Scholar]
  95. 95.  Strating JRPM, van der Linden L, Albulescu L, Bigay J, Arita M et al. 2015. Itraconazole inhibits enterovirus replication by targeting the oxysterol-binding protein. Cell Rep 10:600–15
    [Google Scholar]
  96. 96.  Burgett AWG, Poulsen TB, Wangkanont K, Anderson DR, Kikuchi C et al. 2011. Natural products reveal cancer cell dependence on oxysterol-binding proteins. Nat. Chem. Biol. 7:639–47
    [Google Scholar]
  97. 97.  Moreira EF, Jaworski C, Li A, Rodriguez IR 2001. Molecular and biochemical characterization of a novel oxysterol-binding protein (OSBP2) highly expressed in retina. J. Biol. Chem. 276:18570–78
    [Google Scholar]
  98. 98.  Niko Y, Didier P, Mély Y, Konishi G-I, Klymchenko AS 2016. Bright and photostable push-pull pyrene dye visualizes lipid order variation between plasma and intracellular membranes. Sci. Rep. 6:18870
    [Google Scholar]
  99. 99.  Mazeres S, Fereidouni F, Joly E 2017. Using spectral decomposition of the signals from laurdan-derived probes to evaluate the physical state of membranes in live cells. F1000Research 6:763
    [Google Scholar]
  100. 100.  Leventis PA, Grinstein S 2010. The distribution and function of phosphatidylserine in cellular membranes. Annu. Rev. Biophys. 39:407–27
    [Google Scholar]
  101. 101.  Moser von Filseck J, Čopič A, Delfosse V, Vanni S, Jackson CL et al. 2015. Phosphatidylserine transport by ORP/Osh proteins is driven by phosphatidylinositol 4-phosphate. Science 349:432–36
    [Google Scholar]
  102. 102.  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 349:428–32
    [Google Scholar]
  103. 103.  Maeda K, Anand K, Chiapparino A, Kumar A, Poletto M et al. 2013. Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins. Nature 501:257–61
    [Google Scholar]
  104. 104.  Tani M, Kuge O 2014. Involvement of Sac1 phosphoinositide phosphatase in the metabolism of phosphatidylserine in the yeast Saccharomyces cerevisiae. Yeast 31:145–58
    [Google Scholar]
  105. 105.  Galmes R, Houcine A, van Vliet AR, Agostinis P, Jackson CL, Giordano F 2016. ORP5/ORP8 localize to endoplasmic reticulum-mitochondria contacts and are involved in mitochondrial function. EMBO Rep 17:800–10
    [Google Scholar]
  106. 106.  Kono N, Arai H 2015. Intracellular transport of fat-soluble vitamins A and E. Traffic 16:19–34
    [Google Scholar]
  107. 107.  Kono N, Ohto U, Hiramatsu T, Urabe M, Uchida Y et al. 2013. Impaired α-TTP-PIPs interaction underlies familial vitamin E deficiency. Science 340:1106–10
    [Google Scholar]
  108. 108.  Wong LH, Čopič A, Levine TP 2017. Advances on the transfer of lipids by lipid transfer proteins. Trends Biochem. Sci. 42:516–30
    [Google Scholar]
  109. 109.  Tong J, Yang H, Yang H, Eom SH, Im YJ 2013. Structure of Osh3 reveals a conserved mode of phosphoinositide binding in oxysterol-binding proteins. Structure 21:1203–13
    [Google Scholar]
  110. 110.  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 105:488–93
    [Google Scholar]
  111. 111.  Windisch B, Bray D, Duke T 2006. Balls and chains—a mesoscopic approach to tethered protein domains. Biophys. J. 91:2383–92
    [Google Scholar]
  112. 112.  Buser CA, Sigal CT, Resh MD, McLaughlin S 1994. Membrane binding of myristylated peptides corresponding to the NH2 terminus of Src. Biochemistry 33:13093–101
    [Google Scholar]
  113. 113.  Milo R, Phillips R 2015. Cell Biology by the Numbers New York: Garland Sci.
    [Google Scholar]
  114. 114.  Wijdeven RH, Janssen H, Nahidiazar L, Janssen L, Jalink K et al. 2016. Cholesterol and ORP1L-mediated ER contact sites control autophagosome transport and fusion with the endocytic pathway. Nat. Commun. 7:11808
    [Google Scholar]
  115. 115.  Rocha N, Kuijl C, van der Kant R, Janssen L, Houben D et al. 2009. Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150Glued and late endosome positioning. J. Cell Biol. 185:1209–25
    [Google Scholar]
  116. 116.  Wenk MR, Lucast L, Di Paolo G, Romanelli AJ, Suchy SF et al. 2003. Phosphoinositide profiling in complex lipid mixtures using electrospray ionization mass spectrometry. Nat. Biotechnol. 21:813–17
    [Google Scholar]
  117. 117.  Vihervaara T, Uronen R-L, Wohlfahrt G, Björkhem I, Ikonen E, Olkkonen VM 2011. Sterol binding by OSBP-related protein 1L regulates late endosome motility and function. Cell Mol. Life Sci. 68:537–51
    [Google Scholar]
  118. 118.  Balla T. 2013. Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol. Rev. 93:1019–137
    [Google Scholar]
  119. 119.  Wattenberg BW, Silbert DF 1983. Sterol partitioning among intracellular membranes. Testing a model for cellular sterol distribution. J. Biol. Chem. 258:2284–89
    [Google Scholar]
  120. 120.  Nasuhoglu C, Feng S, Mao J, Yamamoto M, Yin HL et al. 2002. Nonradioactive analysis of phosphatidylinositides and other anionic phospholipids by anion-exchange high-performance liquid chromatography with suppressed conductivity detection. Anal. Biochem. 301:243–54
    [Google Scholar]
  121. 121.  Hammond GRV, Fischer MJ, Anderson KE, Holdich J, Koteci A et al. 2012. PI4P and PI(4,5)P2 are essential but independent lipid determinants of membrane identity. Science 337:727–30
    [Google Scholar]
  122. 122.  Barylko B, Mao YS, Wlodarski P, Jung G, Binns DD et al. 2009. Palmitoylation controls the catalytic activity and subcellular distribution of phosphatidylinositol 4-kinase IIα. J. Biol. Chem. 284:9994–10003
    [Google Scholar]
  123. 123.  Fairn GD, Curwin AJ, Stefan CJ, McMaster CR 2007. The oxysterol binding protein Kes1p regulates Golgi apparatus phosphatidylinositol-4-phosphate function. PNAS 104:15352–57
    [Google Scholar]
  124. 124.  Altan-Bonnet N, Balla T 2012. Phosphatidylinositol 4-kinases: hostages harnessed to build panviral replication platforms. Trends Biochem. Sci. 37:293–302
    [Google Scholar]
  125. 125.  Waugh MG, Minogue S, Chotai D, Berditchevski F, Hsuan JJ 2006. Lipid and peptide control of phosphatidylinositol 4-kinase IIα activity on Golgi-endosomal rafts. J. Biol. Chem. 281:3757–63
    [Google Scholar]
  126. 126.  Li X, Rivas MP, Fang M, Marchena J, Mehrotra B et al. 2002. Analysis of oxysterol binding protein homologue Kes1p function in regulation of Sec14p-dependent protein transport from the yeast Golgi complex. J. Cell Biol. 157:63–77
    [Google Scholar]
  127. 127.  Foti M, Audhya A, Emr SD 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]
  128. 128.  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. 265:1919–23
    [Google Scholar]
  129. 129.  Puchkov D, Haucke V 2013. Greasing the synaptic vesicle cycle by membrane lipids. Trends Cell Biol 23:493–503
    [Google Scholar]
  130. 130.  Deng Y, Rivera-Molina FE, Toomre DK, Burd CG 2016. Sphingomyelin is sorted at the trans Golgi network into a distinct class of secretory vesicle. PNAS 113:6677–82
    [Google Scholar]
  131. 131.  Brügger B, Sandhoff R, Wegehingel S, Gorgas K, Malsam J et al. 2000. Evidence for segregation of sphingomyelin and cholesterol during formation of COPI-coated vesicles. J. Cell Biol. 151:507–18
    [Google Scholar]
  132. 132.  Kim YJ, Guzman-Hernandez ML, Wisniewski E, Balla T 2015. Phosphatidylinositol-phosphatidic acid exchange by Nir2 at ER-PM contact sites maintains phosphoinositide signaling competence. Dev. Cell 33:549–61
    [Google Scholar]
  133. 133.  Yadav S, Garner K, Georgiev P, Li M, Gomez-Espinosa E 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]
  134. 134.  Chang C-L, Liou J 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]
  135. 135.  Lees JA, Messa M, Sun EW, Wheeler H, Torta F et al. 2017. Lipid transport by TMEM24 at ER–plasma membrane contacts regulates pulsatile insulin secretion. Science 355:eaah6171
    [Google Scholar]
  136. 136.  Erecińska M, Silver IA 1989. ATP and brain function. J. Cereb. Blood Flow Metab. 9:2–19
    [Google Scholar]
  137. 137.  Wang P-Y, Weng J, Anderson RGW 2005. OSBP is a cholesterol-regulated scaffolding protein in control of ERK 1/2 activation. Science 307:1472–76
    [Google Scholar]
  138. 138.  Mousley CJ, Yuan P, Gaur NA, Trettin KD, Nile AH et al. 2012. A sterol-binding protein integrates endosomal lipid metabolism with TOR signaling and nitrogen sensing. Cell 148:702–15
    [Google Scholar]
  139. 139.  Huang J, Mousley CJ, Dacquay L, Maitra N, Drin G et al. 2018. A lipid transfer protein signaling axis exerts dual control of cell-cycle and membrane trafficking systems. Dev. Cell 44:378–91
    [Google Scholar]
  140. 140.  Zhong W, Yi Q, Xu B, Li S, Wang T et al. 2016. ORP4L is essential for T-cell acute lymphoblastic leukemia cell survival. Nat. Commun. 7:12702
    [Google Scholar]
  141. 141.  Lorente-Rodríguez A, Barlowe C 2011. Requirement for Golgi-localized PI(4)P in fusion of COPII vesicles with Golgi compartments. Mol. Biol. Cell 22:216–29
    [Google Scholar]
  142. 142.  Ling Y, Hayano S, Novick P 2014. Osh4p is needed to reduce the level of phosphatidylinositol-4-phosphate on secretory vesicles as they mature. Mol. Biol. Cell 25:3389–400
    [Google Scholar]
  143. 143.  Du X, Kumar J, Ferguson C, Schulz TA, Ong YS et al. 2011. A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. J. Cell Biol. 192:121–35
    [Google Scholar]
  144. 144.  Maekawa M, Fairn GD 2015. Complementary probes reveal that phosphatidylserine is required for the proper transbilayer distribution of cholesterol. J. Cell Sci. 128:1422–33
    [Google Scholar]
  145. 145.  Singh RP, Brooks BR, Klauda JB 2009. Binding and release of cholesterol in the Osh4 protein of yeast. Proteins 75:468–77
    [Google Scholar]
  146. 146.  Barelli H, Antonny B 2016. Lipid unsaturation and organelle dynamics. Curr. Opin. Cell Biol. 41:25–32
    [Google Scholar]
  147. 147.  Naguib A, Bencze G, Engle DD, Chio C II, Herzka T et al. 2015. P53 mutations change phosphatidylinositol acyl chain composition. Cell Rep 10:8–19
    [Google Scholar]
  148. 148.  Fernández-Busnadiego R, Saheki Y, De Camilli P 2015. Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites. PNAS 112:E2004–13
    [Google Scholar]
  149. 149.  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 510:552–55
    [Google Scholar]
  150. 150.  AhYoung AP, Jiang J, Zhang J, Khoi Dang X, Loo JA et al. 2015. Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. PNAS 112:E3179–88
    [Google Scholar]
  151. 151.  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 23:1129–40
    [Google Scholar]
  152. 152.  Peretti D, Dahan N, Shimoni E, Hirschberg K, Lev S 2008. Coordinated lipid transfer between the endoplasmic reticulum and the Golgi complex requires the VAP proteins and is essential for Golgi-mediated transport. Mol. Biol. Cell 19:3871–84
    [Google Scholar]
  153. 153.  Schmid EM, Bakalar MH, Choudhuri K, Weichsel J, Ann H et al. 2016. Size-dependent protein segregation at membrane interfaces. Nat. Phys. 12:704–11
    [Google Scholar]
  154. 154.  Gay A, Rye D, Radhakrishnan A 2015. Switch-like responses of two cholesterol sensors do not require protein oligomerization in membranes. Biophys. J. 108:1459–69
    [Google Scholar]
  155. 155.  Maekawa M, Yang Y, Fairn GD 2016. Perfringolysin O theta toxin as a tool to monitor the distribution and inhomogeneity of cholesterol in cellular membranes. Toxins 8:3E67
    [Google Scholar]
  156. 156.  Shiba T, Kawasaki M, Takatsu H, Nogi T, Matsugaki N et al. 2003. Molecular mechanism of membrane recruitment of GGA by ARF in lysosomal protein transport. Nat. Struct. Biol. 10:386–93
    [Google Scholar]
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