Membrane phospholipid asymmetry counters the adverse effects of sterol overloading in the Golgi membrane of Drosophila

Genetics

Volumn 190, Issue 4, 2012, Pages 1299-1308

  Ma, Zhiguo ^a,b   Liu, Zhonghua ^a   Huang, Xun ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; MEMBRANE PHOSPHOLIPID; NEUROPEPTIDE; OXYSTEROL BINDING PROTEIN; STEROL; UNCLASSIFIED DRUG;

ARTICLE; CELL FUNCTION; CELL MIGRATION; CHOLESTEROL METABOLISM; CONTROLLED STUDY; GENETIC SCREENING; GOLGI COMPLEX; MEMBRANE; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARRIER PROTEINS; CHOLESTEROL; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; GENES, INSECT; GOLGI APPARATUS; HOMEOSTASIS; INTRACELLULAR MEMBRANES; INVERTEBRATE HORMONES; MALE; NEURONS; NEUROPEPTIDES; PHOSPHOLIPIDS; PROTEIN TRANSPORT; SECRETORY VESICLES; WING;

EUKARYOTA;

EID: 84859601572     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.137687     Document Type: Article

References (45)

1. Antonny, B., 2011 Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 80: 101-123.
2. Banerji, S., M. Ngo, C. F. Lane, C. A. Robinson, S. Minogue et al., 2010 Oxysterol binding protein-dependent activation of sphingomyelin synthesis in the Golgi apparatus requires phosphatidylinositol 4-kinase IIalpha. Mol. Biol. Cell 21: 4141-4150.
3. Chen, C. Y., M. F. Ingram, P. H. Rosal, and T. R. Graham, 1999 Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J. Cell Biol. 147: 1223-1236.
4. Daleke, D. L., 2007 Phospholipid flippases. J. Biol. Chem. 282: 821-825.
5. Dejgaard, S. Y., A. Murshid, A. Erman, O. Kizilay, D. Verbich et al., 2008 Rab18 and Rab43 have key roles in ER-Golgi trafficking. J. Cell Sci. 121: 2768-2781.
6. Dippold, H. C., M. M. Ng, S. E. Farber-Katz, S. K. Lee, M. L. Kerr et al., 2009 GOLPH3 bridges phosphatidylinositol-4- phosphate and actomyosin to stretch and shape the Golgi to promote budding. Cell 139: 337-351.
7. Du, X., J. Kumar, C. Ferguson, T. A. Schulz, Y. S. Ong et al., 2011 A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. J. Cell Biol. 192: 121-135.
8. Fadok, V. A., and P. M. Henson, 2003 Apoptosis: giving phosphatidylserine recognition an assist-with a twist. Curr. Biol. 13: R655-R657.
9. Ferraro, F., X. M. Ma, J. A. Sobota, B. A. Eipper, and R. E. Mains, 2007 Kalirin/Trio Rho guanine nucleotide exchange factors regulate a novel step in secretory granule maturation. Mol. Biol. Cell 18: 4813-4825.
10. Flamm, M., and D. Schachter, 1982 Acanthocytosis and cholesterol enrichment decrease lipid fluidity of only the outer human erythrocyte membrane leaflet. Nature 298: 290-292.
11. Gall, W. E., N. C. Geething, Z. Hua, M. F. Ingram, K. Liu et al., 2002 Drs2p-dependent formation of exocytic clathrin-coated vesicles in vivo. Curr. Biol. 12: 1623-1627.
12. Graham, T. R., 2004 Flippases and vesicle-mediated protein transport. Trends Cell Biol. 14: 670-677.
13. Hausser, A., P. Storz, S. Martens, G. Link, A. Toker et al., 2005 Protein kinase D regulates vesicular transport by phos-phorylating and activating phosphatidylinositol-4 kinase IIIbeta at the Golgi complex. Nat. Cell Biol. 7: 880-886.
14. Holthuis, J. C. M., 2004 Regulating membrane curvature, pp. 39-64 in Regulatory Mechanisms of Intracellular Membrane Transport, Vol. 10. Springer-Verlag, Berlin; Heidelberg, Germany.
15. 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.
16. Kobuna, H., T. Inoue, M. Shibata, K. Gengyo-Ando, A. Yamamoto et al., 2010 Multivesicular body formation requires OSBP-related proteins and cholesterol. PLoS Genet. 6: p ii: e1001055.
17. Li, X., M. P. Rivas, M. Fang, J. Marchena, B. Mehrotra 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.
18. Liu, K., K. Surendhran, S. F. Nothwehr, and T. R. Graham, 2008 P4-ATPase requirement for AP-1/clathrin function in protein transport from the trans-Golgi network and early endosomes. Mol. Biol. Cell 19: 3526-3535.
19. Lloyd, T. E., P. Verstreken, E. J. Ostrin, A. Phillippi, O. Lichtarge et al., 2000 A genome-wide search for synaptic vesicle cycle proteins in Drosophila. Neuron 26: 45-50.
20. Luan, H., W. C. Lemon, N. C. Peabody, J. B. Pohl, P. K. Zelensky et al., 2006 Functional dissection of a neuronal network required for cuticle tanning and wing expansion in Drosophila. J. Neurosci. 26: 573-584.
21. Luo, C. W., E. M. Dewey, S. Sudo, J. Ewer, S. Y. Hsu et al., 2005 Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2. Proc. Natl. Acad. Sci. USA 102: 2820-2825.
22. Lyssenko, N. N., Y. Miteva, S. Gilroy, W. Hanna-Rose, and R. A. Schlegel, 2008 An unexpectedly high degree of specialization and a widespread involvement in sterol metabolism among the C. elegans putative aminophospholipid translocases. BMC Dev. Biol. 8: 96.
23. Ma, Z., Z. Liu, and X. Huang, 2010 OSBP- and FAN-mediated sterol requirement for spermatogenesis in Drosophila. Development 137: 3775-3784.
24. Maxfield, F. R., and A. K. Menon, 2006 Intracellular sterol transport and distribution. Curr. Opin. Cell Biol. 18: 379-385.
25. Mayinger, P., 2009 Regulation of Golgi function via phosphoinositide lipids. Semin. Cell Dev. Biol. 20: 793-800.
26. Muthusamy, B. P., S. Raychaudhuri, P. Natarajan, F. Abe, K. Liu et al., 2009 Control of protein and sterol trafficking by antagonistic activities of a type IV P-type ATPase and oxysterol binding protein homologue. Mol. Biol. Cell 20: 2920-2931.
27. Natarajan, P., J. Wang, Z. Hua, and T. R. Graham, 2004 Drs2pcoupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc. Natl. Acad. Sci. USA 101: 10614-10619.
28. Natarajan, P., K. Liu, D. V. Patil, V. A. Sciorra, C. L. Jackson et al., 2009 Regulation of a Golgi flippase by phosphoinositides and an ArfGEF. Nat. Cell Biol. 11: 1421-1426.
29. Ngo, M., and N. D. Ridgway, 2009 Oxysterol binding proteinrelated protein 9 (ORP9) is a cholesterol transfer protein thatregulates Golgi structure and function. Mol. Biol. Cell 20: 1388-1399.
30. Nhek, S., M. Ngo, X. Yang, M. M. Ng, S. J. Field et al., 2010 Regulation of oxysterol-binding protein Golgi localization through protein kinase D-mediated phosphorylation. Mol. Biol. Cell 21: 2327-2337.
31. Olkkonen, V. M., 2004 Oxysterol binding protein and its homologues: new regulatory factors involved in lipid metabolism. Curr. Opin. Lipidol. 15: 321-327.
32. Park, J. H., A. J. Schroeder, C. Helfrich-Forster, F. R. Jackson, and J. Ewer, 2003 Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior. Development 130: 2645-2656.
33. Pomorski, T., and A. K. Menon, 2006 Lipid flippases and their biological functions. Cell. Mol. Life Sci. 63: 2908-2921.
34. Rao, S., C. Lang, E. S. Levitan, and D. L. Deitcher, 2001 Visualization of neuropeptide expression, transport, and exocytosis in Drosophila melanogaster. J. Neurobiol. 49: 159-172.
35. Raychaudhuri, S., and W. A. Prinz, 2010 The diverse functions of oxysterol-binding proteins. Annu. Rev. Cell Dev. Biol. 26: 157-177.
36. Soccio, R. E., and J. L. Breslow, 2004 Intracellular cholesterol transport. Arterioscler. Thromb. Vasc. Biol. 24: 1150-1160.
37. Stefan, C. J., A. G. Manford, D. Baird, J. Yamada-Hanff, Y. Mao et al., 2011 Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144: 389-401.
38. Storey, M. K., D. M. Byers, H. W. Cook, and N. D. Ridgway, 1998 Cholesterol regulates oxysterol binding protein (OSBP) phosphorylation and Golgi localization in Chinese hamster ovary cells: correlation with stimulation of sphingomyelin synthesis by 25-hydroxycholesterol. Biochem. J. 336(Pt. 1): 247-256.
39. Subtil, A., I. Gaidarov, K. Kobylarz, M. A. Lampson, J. H. Keen et al., 1999 Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. USA 96: 6775-6780.
40. Tanaka, K., K. Fujimura-Kamada, and T. Yamamoto, 2010 Functions of phospholipid flippases. J. Biochem. 149: 131-143.
41. 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.
42. Wang, Y., C. Thiele, and W. B. Huttner, 2000 Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic 1: 952-962.
43. Ye, B., Y. Zhang, W. Song, S. H. Younger, L. Y. Jan et al., 2007 Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130: 717-729.
44. Zhang, J., K. L. Schulze, P. R. Hiesinger, K. Suyama, S. Wang et al., 2007 Thirty-one flavors of Drosophila rab proteins. Genetics 176: 1307-1322.
45. Zhao, T., T. Gu, H. C. Rice, K. L. McAdams, K. M. Roark et al., 2008 A Drosophila gain-of-function screen for candidate genes involved in steroid-dependent neuroendocrine cell remodeling. Genetics 178: 883-901.