Surprising roles for phospholipid binding proteins revealed by high throughput genetics

Biochemistry and Cell Biology

Volumn 88, Issue 4, 2010, Pages 565-574

  LeBlanc, Marissa A ^a   McMaster, Christopher R ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Metabolism; Phospholipid; Sterol; Synthetic genetic analysis; Vesicular trafficking

Indexed keywords

BIOLOGICAL ANALYSIS; CELL VIABILITY; ENDOSOMES; ESSENTIAL GENE; GENETIC ANALYSIS; HIGH THROUGHPUT; HIGH-THROUGHPUT METHOD; IN-CELL; IN-VIVO; ISOGENIC STRAIN; LIPID-BINDING PROTEINS; MAMMALIAN CELLS; METABOLIC PATHWAYS; OXYSTEROL BINDING PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLINOSITOL; PHOSPHOLIPID BINDING; SACCHAROMYCES CEREVISIAE; SYNTHETIC GENETIC ANALYSIS; TRANSFER PROTEIN; VESICULAR TRAFFICKING; VESICULAR TRANSPORT;

ALCOHOLS; GROWTH KINETICS; MAMMALS; METABOLISM; PHOSPHOLIPIDS; YEAST;

PROTEINS;

PHOSPHATIDYLCHOLINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PHOSPHOLIPID BINDING PROTEIN; PROTEIN KES1; PROTEIN SEC14; UNCLASSIFIED DRUG;

CELL GROWTH; CELL MIGRATION; CYTOLOGY; ENDOSOME; GENE FUNCTION; GENETIC ANALYSIS; HUMAN; PHOSPHOLIPID METABOLISM; PROTEIN FUNCTION; PROTEIN TRANSPORT; REVIEW; TRANS GOLGI NETWORK;

ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; GENETIC TECHNIQUES; GOLGI APPARATUS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PHOSPHOLIPID TRANSFER PROTEINS; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 77954889740     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O09-171     Document Type: Review

References (53)

1. Audhya, A., Foti, M., and Emr, S.D. 2000. Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol. Biol. Cell, 11(8): 2673-2689. PMID:10930462.
2. Bankaitis, V.A., Aitken, J.R., Cleves, A.E., and Dowhan, W. 1990. An essential role for a phospholipid transfer protein in yeast Golgi function. Nature, 347(6293): 561-562. doi:10.1038/347561a0. PMID:2215682.
3. Beh, C.T., and Rine, J. 2004. A role for yeast oxysterol-binding protein homologs in endocytosis and in the maintenance of intracellular sterol-lipid distribution. J. Cell Sci. 117(Pt 14): 2983-2996. doi:10.1242/jcs.01157. PMID:15173322.
4. Beh, C.T., Cool, L., Phillips, J., and Rine, J. 2001. Overlapping functions of the yeast oxysterol-binding protein homologues. Genetics, 157(3): 1117-1140. PMID:11238399.
5. Cleves, A.E., McGee, T.P., Whitters, E.A., Champion, K.M., Aitken, J.R., Dowhan, W., et al. 1991. Mutations in the CDP-cho-line pathway for phospholipid biosynthesis bypass the requirement for an essential phospholipid transfer protein. Cell, 64(4): 789-800. doi:10.1016/0092-8674(91)90508-V. PMID:1997207.
6. Curwin, A.J., and McMaster, C.R. 2008. Structure and function of the enigmatic Sec14 domain-containing proteins and the etiology of human disease. Future Lipidol. 3(4): 399-410. doi:10. 2217/17460875.3.4.399.
7. Curwin, A.J., Fairn, G.D., and McMaster, C.R. 2009. Phospholipid transfer protein Sec14 is required for trafficking from endo-somes and regulates distinct trans-Golgi export pathways. J. Biol. Chem. 284(11): doi:10.1074/jbc.M808732200. PMID:19129178.
8. Davierwala, A.P., Haynes, J., Li, Z., Brost, R.L., Robinson, M.D., Yu, L., et al. 2005. The synthetic genetic interaction spectrum of essential genes. Nat. Genet. 37(10): 1147-1152. doi:10.1038/ ng1640. PMID:16155567.
9. Drin, G., Casella, J.F., Gautier, R., Boehmer, T., Schwartz, T.U., and Antonny, B. 2007. A general amphipathic alpha-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 14(2): 138-146. doi:10.1038/nsmb1194. PMID:17220896.
10. Fairn, G.D., and McMaster, C.R. 2005. Identification and assessment of the role of a nominal phospholipid binding region of ORP1S (oxysterol-binding-protein-related protein 1 short) in the regulation of vesicular transport. Biochem. J. 387(Pt 3): 889-896. doi:10.1042/BJ20041915. PMID:15617515.
11. Fairn, G.D., Curwin, A.J., Stefan, C.J., and McMaster, C.R. 2007. The oxysterol binding protein Kes1p regulates Golgi apparatus phosphatidylinositol-4-phosphate function. Proc. Natl. Acad. Sci. U.S.A. 104(39): doi:10.1073/pnas.0705571104. PMID:17881569.
12. Fang, M., Kearns, B.G., Gedvilaite, A., Kagiwada, S., Kearns, M., Fung, M.K., and Bankaitis, V.A. 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(23): 6447-6459. PMID:8978672.
13. Fernández-Murray, J.P., and McMaster, C.R. 2005. Glycerophosphocholine catabolism as a new route for choline formation for phosphatidylcholine synthesis by the Kennedy pathway. J. Biol. Chem. 280(46): 38290-38296. doi:10.1074/jbc.M507700200. PMID:16172116.
14. Guarente, L. 1993. Synthetic enhancement in gene interaction: a genetic tool come of age. Trends Genet. 9(10): 362-366. doi:10.1016/0168-9525(93)90042-G. PMID:8273152.
15. Gurunathan, S., David, D., and Gerst, J.E. 2002. Dynamin and clathrin are required for the biogenesis of a distinct class of secretory vesicles in yeast. EMBO J. 21(4): 602-614. doi:10.1093/ emboj/21.4.602. PMID:11847108.
16. Harsay, E., and Schekman, R. 2002. A subset of yeast vacuolar protein sorting mutants is blocked in one branch of the exocytic pathway. J. Cell Biol. 156(2): 271-285. doi:10.1083/jcb.200109077. PMID:11807092.
17. Henneberry, A.L., Lagace, T.A., Ridgway, N.D., and McMaster, C.R. 2001. Phosphatidylcholine synthesis influences the diacylglycerol homeostasis required for SEC14p-dependent Golgi function and cell growth. Mol. Biol. Cell, 12(3): 511-520. PMID:11251067.
18. Hosomi, A., Arita, M., Sato, Y., Kiyose, C., Ueda, T., Igarashi, O., et al. 1997. Affinity for alpha-tocopherol transfer protein as a determinant of the biological activities of vitamin E analogs. FEBS Lett. 409(1): 105-108. doi:10.1016/S0014-5793(97) 00499-7. PMID:9199513.
19. Ile, K.E., Schaaf, G., and Bankaitis, V.A. 2006. Phosphatidylinositol transfer proteins and cellular nanoreactors for lipid signaling. Nat. Chem. Biol. 2(11): 576-583. doi:10.1038/nchembio835. PMID:17051233.
20. Im, Y.J., Raychaudhuri, S., Prinz, W.A., and Hurley, J.H. 2005. Structural mechanism for sterol sensing and transport by OSBPrelated proteins. Nature, 437(7055): 154-158. doi:10.1038/nature03923. PMID:16136145.
21. Knodler, A., and Mayinger, P. 2005. Analysis of phosphoinositide binding proteins using liposomes as an affinity matrix. Biotechniques, 38(6): 858-862, 860, 862. doi:10.2144/05386BM02. PMID:16018544.
22. Kozminski, K.G., Alfaro, G., Dighe, S., and Beh, C.T. 2006. Homologues of oxysterol-binding proteins affect Cdc42p-and Rho1p-mediated cell polarization in Saccharomyces cerevisiae. Traffic, 7(9): 1224-1242. doi:10.1111/j.1600-0854.2006.00467.x. PMID:17004323.
23. Lehto, M., Laitinen, S., Chinetti, G., Johansson, M., Ehnholm, C., Staels, B., et al. 2001. The OSBP-related protein family in humans. J. Lipid Res. 42(8): 1203-1213. PMID:11483621.
24. Levine, T.P., and Munro, S. 1998. The pleckstrin homology domain of oxysterol-binding protein recognises a determinant specific to Golgi membranes. Curr. Biol. 8(13): 729-739. doi:10. 1016/S0960-9822(98)70296-9. PMID:9651677.
25. Levine, T.P., and Munro, S. 2002. Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr. Biol. 12(9): 695-704. doi:10.1016/S0960-9822(02)00779-0. PMID:12007412.
26. Li, X., Routt, S.M., Xie, Z., Cui, X., Fang, M., Kearns, M.A., et al. 2000. Identification of a novel family of nonclassic yeast phosphatidylinositol transfer proteins whose function modulates phospholipase D activity and Sec14p-independent cell growth. Mol. Biol. Cell, 11(6): 1989-2005. PMID:10848624.
27. Li, X., Rivas, M.P., Fang, M., Marchena, J., Mehrotra, B., Chaudhary, A., 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(1): 63-77. doi:10.1083/jcb.200201037. PMID:11916983.
28. Lustgarten, V., and Gerst, J.E. 1999. Yeast VSM1 encodes a vSNARE binding protein that may act as a negative regulator of constitutive exocytosis. Mol. Cell. Biol. 19(6): 4480-4494. PMID:10330187.
29. Manor, D., and Morley, S. 2007. The alpha-tocopherol transfer protein. Vitam. Horm. 76: 45-65. doi:10.1016/S0083-6729(07)76003-X. PMID:17628171.
30. Mousley, C.J., Tyeryar, K.R., Vincent-Pope, P., and Bankaitis, V.A. 2007. The Sec14-superfamily and the regulatory interface between phospholipid metabolism and membrane trafficking. Biochim. Biophys. Acta, 1771(6): 727-736. PMID:17512778.
31. Murray, J.P., and McMaster, C.R. 2005. Nte1p-mediated deacylation of phosphatidylcholine functionally interacts with Sec14p. J. Biol. Chem. 280(9): 8544-8552. doi:10.1074/jbc.M413999200. PMID:15611060.
32. Novick, P., Osmond, B.C., and Botstein, D. 1989. Suppressors of yeast actin mutations. Genetics, 121(4): 659-674. PMID: 2656401.
33. Qian, J., Atkinson, J., and Manor, D. 2006. Biochemical consequences of heritable mutations in the alpha-tocopherol transfer protein. Biochemistry, 45(27): 8236-8242. doi:10.1021/bi060522c. PMID:16819822.
34. Raychaudhuri, S., Im, Y.J., Hurley, J.H., and Prinz, W.A. 2006. Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides. J. Cell Biol. 173(1): doi:10.1083/jcb.200510084. PMID:16585271.
35. Rivas, M.P., Kearns, B.G., Xie, Z., Guo, S., Sekar, M.C., Hosaka, K., et al. 1999. Pleiotropic alterations in lipid metabolism in yeast sac1 mutants: relationship to "bypass Sec14p" and inositol auxotrophy. Mol. Biol. Cell, 10(7): 2235-2250. PMID:10397762.
36. Robinson, M., Poon, P.P., Schindler, C., Murray, L.E., Kama, R., Gabriely, G., et al. 2006. The Gcs1 Arf-GAP mediates Snc1,2 v-SNARE retrieval to the Golgi in yeast. Mol. Biol. Cell, 17(4): 1845-1858. doi:10.1091/mbc.E05-09-0832. PMID:16452633.
37. Saito, K., Tautz, L., and Mustelin, T. 2007. The lipid-binding SEC14 domain. Biochim. Biophys. Acta, 1771(6): 719-726. PMID:17428729.
38. Schaaf, G., Ortlund, E.A., Tyeryar, K.R., Mousley, C.J., Ile, K.E., Garrett, T.A., et al. 2008. Functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the sec14 superfamily. Mol. Cell, 29(2): 191-206. doi:10.1016/j.molcel.2007.11.026. PMID:18243114.
39. Schuldiner, M., Collins, S.R., Thompson, N.J., Denic, V., Bhamidipati, A., Punna, T., et al. 2005. Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell, 123(3): 507-519. doi:10.1016/j. cell.2005.08.031. PMID:16269340.
40. Sciorra, V.A., Audhya, A., Parsons, A.B., Segev, N., Boone, C., and Emr, S.D. 2005. Synthetic genetic array analysis of the PtdIns 4-kinase Pik1p identifies components in a Golgi-specific Ypt31/rab-GTPase signaling pathway. Mol. Biol. Cell, 16(2): 776-793. doi:10.1091/mbc.E04-08-0700. PMID:15574876.
41. Segrè, D., Deluna, A., Church, G.M., and Kishony, R. 2005. Modular epistasis in yeast metabolism. Nat. Genet. 37(1): 77-83. PMID:15592468.
42. Sha, B., Phillips, S.E., Bankaitis, V.A., and Luo, M. 1998. Crystal structure of the Saccharomyces cerevisiae phosphatidylinositol transfer protein. Nature, 391(6666): 506-510. doi:10.1038/35179. PMID:9461221.
43. Sreenivas, A., Patton-Vogt, J.L., Bruno, V., Griac, P., and Henry, S.A. 1998. A role for phospholipase D (Pld1p) in growth, secretion, and regulation of membrane lipid synthesis in yeast. J. Biol. Chem. 273(27): doi:10.1074/jbc.273.27.16635. PMID:9642212.
44. Strahl, T., Hama, H., DeWald, D.B., and Thorner, J. 2005. Yeast phosphatidylinositol 4-kinase, Pik1, has essential roles at the Golgi and in the nucleus. J. Cell Biol. 171(6): 967-979. doi:10. 1083/jcb.200504104. PMID:16365163.
45. Tong, A.H., and Boone, C. 2006. Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol. Cell. Biol. 313: 171-192.
46. Tong, A.H., Evangelista, M., Parsons, A.B., Xu, H., Bader, G.D., Pagé, N., et al. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science, 294(5550): 2364-2368. doi:10.1126/science.1065810. PMID:11743205.
47. Tong, A.H., Lesage, G., Bader, G.D., Ding, H., Xu, H., Xin, X., et al. 2004. Global mapping of the yeast genetic interaction net-work. Science, 303(5659): 808-813. doi:10.1126/science.1091317. PMID:14764870.
48. Walch-Solimena, C., and Novick, P. 1999. The yeast phosphatidy-linositol-4-OH kinase pik1 regulates secretion at the Golgi. Nat. Cell Biol. 1(8): 523-525. doi:10.1038/70319. PMID:10587649.
49. Wang, P., Duan, W., Munn, A.L., and Yang, H. 2005. Molecular characterization of Osh6p, an oxysterol binding protein homolog in the yeast Saccharomyces cerevisiae. FEBS J. 272(18): 4703-4715. doi:10.1111/j.1742-4658.2005.04886.x. PMID:16156791.
50. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., Andre, B., et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science, 285(5429): 901-906. doi:10.1126/science.285.5429.901. PMID:10436161.
51. Xie, Z., Fang, M., Rivas, M.P., Faulkner, A.J., Sternweis, P.C., Engebrecht, J.A., and Bankaitis, V.A. 1998. Phospholipase D activity is required for suppression of yeast phosphatidylinositol transfer protein defects. Proc. Natl. Acad. Sci. U.S.A. 95(21): 12346-12351. doi:10.1073/pnas.95.21.12346. PMID:9770489.
52. Xie, Z., Fang, M., and Bankaitis, V.A. 2001. Evidence for an intrinsic toxicity of phosphatidylcholine to Sec14p-dependent pro-tein transport from the yeast Golgi complex. Mol. Biol. Cell, 12(4): 1117-1129. PMID:11294911.
53. Xu, Y., Liu, Y., Ridgway, N.D., and McMaster, C.R. 2001. Novel members of the human oxysterol-binding protein family bind phospholipids and regulate vesicle transport. J. Biol. Chem. 276(21): 18407-18414. doi:10.1074/jbc.M101204200. PMID:11279184.