Lipid-regulated sterol transfer between closely apposed membranes by oxysterol-binding protein homologues

Journal of Cell Biology

Volumn 187, Issue 6, 2009, Pages 889-903

  Schulz, Timothy A ^a   Choi, Mal Gi ^a   Raychaudhuri, Sumana ^a   Mears, Jason A ^a   Ghirlando, Rodolfo ^a   Hinshaw, Jenny E ^a   Prinz, William A ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; LIPID; OXYSTEROL BINDING PROTEIN; PHOSPHATIDYLINOSITIDE; PROTEIN OSH4P; STEROL; UNCLASSIFIED DRUG; CARRIER PROTEIN; HYBRID PROTEIN; KES1 PROTEIN, S CEREVISIAE; LIPOSOME; MEMBRANE LIPID; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL; SACCHAROMYCES CEREVISIAE PROTEIN; STEROID RECEPTOR;

ARTICLE; BINDING SITE; CELL ORGANELLE; LIPID COMPOSITION; MEMBRANE TRANSPORT; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; REGULATORY MECHANISM; CHEMICAL STRUCTURE; CHEMISTRY; ENDOPLASMIC RETICULUM; GENETICS; KINETICS; METABOLISM; MUTATION; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; TRANSPORT AT THE CELLULAR LEVEL;

BINDING SITES; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; ENDOPLASMIC RETICULUM; KINETICS; LIPOSOMES; MEMBRANE LIPIDS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTATION; PHOSPHATIDYLINOSITOLS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, STEROID; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; STEROLS;

EID: 74049122402     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200905007     Document Type: Article

References (51)

1. Beh, C.T., and J. Rine. 2004. A role for yeast oxysterol-binding protein homologs in endocytosis and in the maintenance of intracellular sterol-lipid distribution. J. Cell Sci. 117:2983-2996. doi:10.1242/jcs.01157
2. Beh, C.T., L. Cool, J. Phillips, and J. Rine. 2001. Overlapping functions of the yeast oxysterol-binding protein homologues. Genetics. 157:1117-1140.
3. Crowley, J.H., F.W. Leak Jr., K.V. Shianna, S. Tove, and L.W. Parks. 1998. A mutation in a purported regulatory gene affects control of sterol uptake in Saccharomyces cerevisiae. J. Bacteriol. 180:4177-4183.
4. Espenshade, P.J., and A.L. Hughes. 2007. Regulation of sterol synthesis in eukaryotes. Annu. Rev. Genet. 41:401-427. doi:10.1146/annurev.genet. 41.110306.130315
5. Fairn, G.D., and C.R. McMaster. 2005. The roles of the human lipid-binding proteins ORP9S and ORP10S in vesicular transport. Biochem. Cell Biol. 83:631-636. doi:10.1139/o05-064
6. Fairn, G.D., and C.R. McMaster. 2008. Emerging roles of the oxysterol-binding protein family in metabolism, transport, and signaling. Cell. Mol. Life Sci. 65:228-236. doi:10.1007/s00018-007-7325-2
7. Fairn, G.D., A.J. Curwin, C.J. Stefan, and C.R. McMaster. 2007. The oxysterol binding protein Kes1p regulates Golgi apparatus phosphatidylinositol- 4-phosphate function. Proc. Natl. Acad. Sci. USA. 104:15352-15357. doi:10.1073/pnas.0705571104
8. Fang, M., B.G. Kearns, A. Gedvilaite, S. Kagiwada, M. Kearns, M.K. Fung, and V.A. Bankaitis. 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. 15:6447-6459.
9. Fritz, F., E.M. Howard, M.M. Hoffman, and P.D. Roepe. 1999. Evidence for altered ion transport in Saccharomyces cerevisiae overexpressing human MDR 1 protein. Biochemistry. 38:4214-4226. doi:10.1021/bi981929n
10. Hanada, K., K. Kumagai, N. Tomishige, and M. Kawano. 2007. CERT and intracellular trafficking of ceramide. Biochim. Biophys. Acta. 1771:644-653.
11. Holthuis, J.C., and T.P. Levine. 2005. Lipid traffic: floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 6:209-220. doi:10.1038/nrm1591
12. Hynynen, R., S. Laitinen, R. Käkelä, K. Tanhuanpää, S. Lusa, C. Ehnholm, P. Somerharju, E. Ikonen, and V.M. Olkkonen. 2005. Overexpression of OSBP-related protein 2 (ORP2) induces changes in cellular cholesterol metabolism and enhances endocytosis. Biochem. J. 390:273-283. doi:10.1042/BJ20042082
13. Ikonen, E. 2006. Mechanisms for cellular cholesterol transport: defects and human disease. Physiol. Rev. 86:1237-1261. doi:10.1152/physrev.00022. 2005
14. Im, Y.J., S. Raychaudhuri, W.A. Prinz, and J.H. Hurley. 2005. Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature. 437:154-158. doi:10.1038/nature03923
15. John, K., J. Kubelt, P. Müller, D. Wüstner, and A. Herrmann. 2002. Rapid transbilayer movement of the fluorescent sterol dehydroergosterol in lipid membranes. Biophys. J. 83:1525-1534. doi:10.1016/S0006-3495(02) 73922-2
16. Kreye, S., J. Malsam, and T.H. Söllner. 2008. In vitro assays to measure SNARE-mediated vesicle fusion. Methods Mol. Biol. 440:37-50. doi:10.1007/978-1-59745-178-9-3
17. Ladinsky, M.S., D.N. Mastronarde, J.R. McIntosh, K.E. Howell, and L.A. Staehelin. 1999. Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J. Cell Biol. 144:1135-1149. doi:10.1083/jcb.144.6.1135
18. Lange, Y., and T.L. Steck. 1997. Quantitation of the pool of cholesterol associated with acyl-CoA:cholesterol acyltransferase in human fibroblasts. J. Biol. Chem. 272:13103-13108. doi:10.1074/jbc.272.20.13103
19. Lebowitz, J., M.S. Lewis, and P. Schuck. 2002. Modern analytical ultracentrifugation in protein science: a tutorial review. Protein Sci. 11:2067-2079. doi:10.1110/ps.0207702
20. Levine, T., and C. Loewen. 2006. Inter-organelle membrane contact sites: through a glass, darkly. Curr. Opin. Cell Biol. 18:371-378. doi:10.1016/j.ceb.2006.06.011
21. Levine, T.P., and S. Munro. 2001. Dual targeting of Osh1p, a yeast homologue of oxysterol-binding protein, to both the Golgi and the nucleus-vacuole junction. Mol. Biol. Cell. 12:1633-1644.
22. Li, Y., and W.A. Prinz. 2004. ATP-binding cassette (ABC) transporters mediate nonvesicular, raft-modulated sterol movement from the plasma membrane to the endoplasmic reticulum. J. Biol. Chem. 279:45226-45234. doi:10.1074/jbc.M407600200
23. Li, X., M.P. Rivas, M. Fang, J. Marchena, B. Mehrotra, A. Chaudhary, L. Feng, G.D. Prestwich, and V.A. Bankaitis. 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. doi:10.1083/jcb.200201037
24. Loewen, C.J., A. Roy, and T.P. Levine. 2003. A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 22:2025-2035. doi:10.1093/emboj/cdg201
25. Maxfield, F.R., and I. Tabas. 2005. Role of cholesterol and lipid organization in disease. Nature. 438:612-621. doi:10.1038/nature04399
26. Mousley, C.J., K.R. Tyeryar, P. Vincent-Pope, and V.A. Bankaitis. 2007. The Sec14-superfamily and the regulatory interface between phospholipid metabolism and membrane trafficking. Biochim. Biophys. Acta. 1771:727-736.
27. Ngo, M., and N.D. Ridgway. 2009. Oxysterol binding protein-related protein 9 (ORP9) is a cholesterol transfer protein that regulates Golgi structure and function. Mol. Biol. Cell. 20:1388-1399.
28. Olkkonen, V.M. 2004. Oxysterol binding protein and its homologues: new regulatory factors involved in lipid metabolism. Curr. Opin. Lipidol. 15:321-327. doi:10.1097/00041433-200406000-00013
29. Peretti, D., N. Dahan, E. Shimoni, K. Hirschberg, and S. Lev. 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. 19:3871-3884.
30. Perktold, A., B. Zechmann, G. Daum, and G. Zellnig. 2007. Organelle association visualized by three-dimensional ultrastructural imaging of the yeast cell. FEMS Yeast Res. 7:629-638. doi:10.1111/j.1567-1364.2007.00226.x
31. Perry, R.J., and N.D. Ridgway. 2006. Oxysterol-binding protein and vesicle-associated membrane protein-associated protein are required for sterol-dependent activation of the ceramide transport protein. Mol. Biol. Cell. 17:2604-2616. doi:10.1091/mbc.E06-01-0060
32. Pichler, H., B. Gaigg, C. Hrastnik, G. Achleitner, S.D. Kohlwein, G. Zellnig, A. Perktold, and G. Daum. 2001. A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids. Eur. J. Biochem. 268:2351-2361. doi:10.1046/j.1432- 1327.2001.02116.x
33. Proszynski, T.J., R.W. Klemm, M. Gravert, P.P. Hsu, Y. Gloor, J. Wagner, K. Kozak, H. Grabner, K. Walzer, M. Bagnat, et al. 2005. A genome-wide visual screen reveals a role for sphingolipids and ergosterol in cell surface delivery in yeast. Proc. Natl. Acad. Sci. USA. 102:17981-17986. doi:10.1073/pnas.0509107102
34. Radhakrishnan, A., J.L. Goldstein, J.G. McDonald, and M.S. Brown. 2008. Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: a delicate balance. Cell Metab. 8:512-521. doi:10.1016/j.cmet.2008.10.008
35. Raychaudhuri, S., Y.J. Im, J.H. Hurley, and W.A. Prinz. 2006. Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein - related proteins and phosphoinositides. J. Cell Biol. 173:107-119. doi:10.1083/jcb.200510084
36. Glued and late endosome positioning. J. Cell Biol. 185:1209-1225. doi:10.1083/jcb.200811005
37. Schaaf, G., E.A. Ortlund, K.R. Tyeryar, C.J. Mousley, K.E. Ile, T.A. Garrett, J. Ren, M.J. Woolls, C.R. Raetz, M.R. Redinbo, and V.A. Bankaitis. 2008. Functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the sec14 superfamily. Mol. Cell. 29:191-206. doi:10.1016/j.molcel.2007.11.026
38. Schuck, P. 2003. On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem. 320:104-124. doi:10.1016/S0003-2697(03)00289-6
39. Suchanek, M., R. Hynynen, G. Wohlfahrt, M. Lehto, M. Johansson, H. Saarinen, A. Radzikowska, C. Thiele, and V.M. Olkkonen. 2007. The mammalian oxysterol-binding protein-related proteins (ORPs) bind 25-hydroxycholesterol in an evolutionarily conserved pocket. Biochem. J. 405:473-480. doi:10.1042/BJ20070176
40. Sullivan, D.P., H. Ohvo-Rekilä, N.A. Baumann, C.T. Beh, and A.K. Menon. 2006. Sterol trafficking between the endoplasmic reticulum and plasma membrane in yeast. Biochem. Soc. Trans. 34:356-358. doi:10.1042/ BST0340356
41. Takeshima, H., S. Komazaki, M. Nishi, M. Iino, and K. Kangawa. 2000. Junctophilins: a novel family of junctional membrane complex proteins. Mol. Cell. 6:11-22. doi:10.1016/S1097-2765(00)00003-4
42. van Meer, G., D.R. Voelker, and G.W. Feigenson. 2008. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9:112-124. doi:10.1038/nrm2330
43. Várnai, P., B. Tóth, D.J. Tóth, L. Hunyady, and T. Balla. 2007. Visualization and manipulation of plasma membrane-endoplasmic reticulum contact sites indicates the presence of additional molecular components within the STIM1-Orai1 complex. J. Biol. Chem. 282:29678-29690. doi:10.1074/jbc.M704339200
44. Vicinanza, M., G. D'Angelo, A. Di Campli, and M.A. De Matteis. 2008. Phosphoinositides as regulators of membrane trafficking in health and disease. Cell. Mol. Life Sci. 65:2833-2841.
45. Wang, P., W. Duan, A.L. Munn, and H. Yang. 2005a. Molecular characterization of Osh6p, an oxysterol binding protein homolog in the yeast Saccharomyces cerevisiae. FEBS J. 272:4703-4715. doi:10.1111/j.1742-4658. 2005.04886.x
46. Wang, P., Y. Zhang, H. Li, H.K. Chieu, A.L. Munn, and H. Yang. 2005b. AAA ATPases regulate membrane association of yeast oxysterol binding proteins and sterol metabolism. EMBO J. 24:2989-2999. doi:10.1038/sj.emboj.7600764
47. Wang, P.Y., J. Weng, and R.G.W. Anderson. 2005c. OSBP is a cholesterol-regulated scaffolding protein in control of ERK 1/2 activation. Science. 307:1472-1476. doi:10.1126/science.1107710
48. 2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J. Cell Biol. 174:803-813. doi:10.1083/jcb. 200604014
49. Yan, D., and V.M. Olkkonen. 2008. Characteristics of oxysterol binding proteins. Int. Rev. Cytol. 265:253-285. doi:10.1016/S0074-7696(07)65007-4
50. Zinser, E., and G. Daum. 1995. Isolation and biochemical characterization of organelles from the yeast, Saccharomyces cerevisiae. Yeast. 11:493-536. doi:10.1002/yea.320110602
51. Zweytick, D., E. Leitner, S.D. Kohlwein, C. Yu, J. Rothblatt, and G. Daum. 2000. Contribution of Are1p and Are2p to steryl ester synthesis in the yeast Saccharomyces cerevisiae. Eur. J. Biochem. 267:1075-1082. doi:10.1046/j.1432-1327.2000.01103.x