Linking phospholipid flippases to vesicle-mediated protein transport

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1791, Issue 7, 2009, Pages 612-619

  Muthusamy, Baby Periyanayaki ^a   Natarajan, Paramasivam ^a   Zhou, Xiaoming ^a   Graham, Todd R ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Cdc50p; Clathrin; Drs2p; Flippase; Kes1p; Membrane asymmetry; P4 ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE P4; CARRIER PROTEIN; CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 50P; ERGOSTEROL; FLIPPASE; PHOSPHOLIPID TRANSFER PROTEIN; PROTEIN DRS2P; UNCLASSIFIED DRUG;

ARTICLE; ARTIFICIAL MEMBRANE; ASYMMETRIC SYNTHESIS; BIOGENESIS; CAENORHABDITIS ELEGANS; CELL BUDDING; CELL MEMBRANE TRANSPORT; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; EXOCYTOSIS; LIPID METABOLISM; LIVER DISEASE; MEMBRANE FORMATION; MEMBRANE VESICLE; NONHUMAN; PHOSPHOLIPID BILAYER; PHOSPHOLIPID TRANSFER; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; STEROL METABOLISM; TRANSPORT VESICLE; YEAST CELL;

ADENOSINE TRIPHOSPHATASES; ATP-BINDING CASSETTE TRANSPORTERS; PHOSPHOLIPID TRANSFER PROTEINS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSPORT VESICLES;

ARABIDOPSIS THALIANA; CAENORHABDITIS ELEGANS; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 67649270577     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.03.004     Document Type: Article

References (99)

1. Balasubramanian K., and Schroit A.J. Aminophospholipid asymmetry: a matter of life and death. Annu. Rev. Physiol. 65 (2003) 701-734
2. Op den Kamp J.A. Lipid asymmetry in membranes. Annu. Rev. Biochem. 48 (1979) 47-71
3. Hoffmann P.R., Kench J.A., Vondracek A., Kruk E., Daleke D.L., Jordan M., Marrack P., Henson P.M., and Fadok V.A. Interaction between phosphatidylserine and the phosphatidylserine receptor inhibits immune responses in vivo. J. Immunol. 174 (2005) 1393-1404
4. Yeung T., Gilbert G.E., Shi J., Silvius J., Kapus A., and Grinstein S. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319 (2008) 210-213
5. Emoto K., and Umeda M. An essential role for a membrane lipid in cytokinesis. Regulation of contractile ring disassembly by redistribution of phosphatidylethanolamine. J. Cell Biol. 149 (2000) 1215-1224
6. Zwaal R.F., Comfurius P., and van Deenen L.L. Membrane asymmetry and blood coagulation. Nature 268 (1977) 358-360
7. Darland-Ransom M., Wang X., Sun C.L., Mapes J., Gengyo-Ando K., Mitani S., and Xue D. Role of C. elegans TAT-1 protein in maintaining plasma membrane phosphatidylserine asymmetry. Science 320 (2008) 528-531
8. Mercer J., and Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320 (2008) 531-535
9. Cerbon J., and Calderon V. Generation, modulation and maintenance of the plasma membrane asymmetric phospholipid composition in yeast cells during growth: their relation to surface potential and membrane protein activity. Biochim. Biophys. Acta 1235 (1995) 100-106
10. Kato U., Emoto K., Fredriksson C., Nakamura H., Ohta A., Kobayashi T., Murakami-Murofushi K., Kobayashi T., and Umeda M. A novel membrane protein, Ros3p, is required for phospholipid translocation across the plasma membrane in Saccharomyces cerevisiae. J. Biol. Chem. 277 (2002) 37855-37862
11. Chen S., Wang J., Muthusamy B.P., Liu K., Zare S., Andersen R.J., and Graham T.R. Roles for the Drs2p-Cdc50p complex in protein transport and phosphatidylserine asymmetry of the yeast plasma membrane. Traffic 7 (2006) 1503-1517
12. Tang X., Halleck M.S., Schlegel R.A., and Williamson P. A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 272 (1996) 1495-1497
13. Paulusma C.C., and Oude Elferink R.P. The type 4 subfamily of P-type ATPases, putative aminophospholipid translocases with a role in human disease. Biochim. Biophys. Acta 1741 (2005) 11-24
14. Dhar M.S., Sommardahl C.S., Kirkland T., Nelson S., Donnell R., Johnson D.K., and Castellani L.W. Mice heterozygous for Atp10c, a putative amphipath, represent a novel model of obesity and type 2 diabetes. J. Nutr. 134 (2004) 799-805
15. Flamant S., Pescher P., Lemercier B., Clement-Ziza M., Kepes F., Fellous M., Milon G., Marchal G., and Besmond C. Characterization of a putative type IV aminophospholipid transporter P-type ATPase. Mamm Genome 14 (2003) 21-30
16. Paterson J.K., Renkema K., Burden L., Halleck M.S., Schlegel R.A., Williamson P., and Daleke D.L. Lipid specific activation of the murine P4-ATPase Atp8a1 (ATPase II). Biochemistry 45 (2006) 5367-5376
17. Ding J., Wu Z., Crider B.P., Ma Y., Li X., Slaughter C., Gong L., and Xie X.S. Identification and functional expression of four isoforms of ATPase II, the putative aminophospholipid translocase. Effect of isoform variation on the ATPase activity and phospholipid specificity. J. Biol. Chem. 275 (2000) 23378-23386
18. Soupene E., and Kuypers F.A. Identification of an erythroid ATP-dependent aminophospholipid transporter. Br. J. Haematol. 133 (2006) 436-438
19. Pomorski T., Lombardi R., Riezman H., Devaux P.F., van Meer G., and Holthuis J.C. Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol. Biol. Cell 14 (2003) 1240-1254
20. Alder-Baerens N., Lisman Q., Luong L., Pomorski T., and Holthuis J.C. Loss of P4 ATPases Drs2p and Dnf3p disrupts aminophospholipid transport and asymmetry in yeast post-Golgi secretory vesicles. Mol. Biol. Cell 17 (2006) 1632-1642
21. Natarajan P., Wang J., Hua Z., and Graham T.R. Drs2p-coupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 10614-10619
22. Elvington S.M., Bu F., and Nichols J.W. Fluorescent, acyl chain-labeled phosphatidylcholine analogs reveal novel transport pathways across the plasma membrane of yeast. J. Biol. Chem. 280 (2005) 40957-40964
23. Graham T.R. Flippases and vesicle-mediated protein transport. Trends Cell Biol. 14 (2004) 670-677
24. Kuhlbrandt W. Biology, structure and mechanism of P-type ATPases. Nat Rev Mol. Cell. Biol. 5 (2004) 282-295
25. Toyoshima C., and Mizutani T. Crystal structure of the calcium pump with a bound ATP analogue. Nature 430 (2004) 529-535
26. Saito K., Fujimura-Kamada K., Furuta N., Kato U., Umeda M., and Tanaka K. Cdc50p, a protein required for polarized growth, associates with the Drs2p P-type ATPase implicated in phospholipid translocation in Saccharomyces cerevisiae. Mol. Biol. Cell 15 (2004) 3418-3432
27. Furuta N., Fujimura-Kamada K., Saito K., Yamamoto T., and Tanaka K. Endocytic recycling in yeast is regulated by putative phospholipid translocases and the Ypt31p/32p-Rcy1p pathway. Mol. Biol. Cell 18 (2007) 295-312
28. Hua Z., Fatheddin P., and Graham T.R. An essential subfamily of Drs2p-related P-type ATPases is required for protein trafficking between Golgi complex and endosomal/vacuolar system. Mol. Biol. Cell 13 (2002) 3162-3177
29. Hanson P.K., Malone L., Birchmore J.L., and Nichols J.W. Lem3p is essential for the uptake and potency of alkylphosphocholine drugs, edelfosine and miltefosine. J. Biol. Chem. 278 (2003) 36041-36050
30. Stevens H.C., Malone L., and Nichols J.W. The putative aminophospholipid translocases, DNF1 and DNF2, are not required for 7-Nitrobenz-2-oxa-1,3-diazol-4-yl-phosphatidylserine flip across the plasma membrane of Saccharomyces cerevisiae. J. Biol. Chem. 283 (2008) 35060-35069
31. Riekhof W.R., Wu J., Gijon M.A., Zarini S., Murphy R.C., and Voelker D.R. Lysophosphatidylcholine metabolism in Saccharomyces cerevisiae: the role of P-type ATPases in transport and a broad specificity acyltransferase in acylation. J. Biol. Chem. 282 (2007) 36853-36861
32. Perez-Victoria F.J., Sanchez-Canete M.P., Castanys S., and Gamarro F. Phospholipid translocation and miltefosine potency require both L. donovani miltefosine transporter and the new protein LdRos3 in Leishmania parasites. J. Biol. Chem. 281 (2006) 23766-23775
33. Daleke D.L., and Huestis W.H. Incorporation and translocation of aminophospholipids in human erythrocytes. Biochemistry 24 (1985) 5406-5416
34. Smriti, Nemergut E.C., and Daleke D.L. ATP-dependent transport of phosphatidylserine analogues in human erythrocytes. Biochemistry 46 (2007) 2249-2259
35. Niggli V., and Sigel E. Anticipating antiport in P-type ATPases. Trends Biochem. Sci. 33 (2008) 156-160
36. Obara K., Miyashita N., Xu C., Toyoshima I., Sugita Y., Inesi G., and Toyoshima C. Structural role of countertransport revealed in Ca(2+) pump crystal structure in the absence of Ca(2+). Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 14489-14496
37. Parsons A.B., Lopez A., Givoni I.E., Williams D.E., Gray C.A., Porter J., Chua G., Sopko R., Brost R.L., Ho C.H., Wang J., Ketela T., Brenner C., Brill J.A., Fernandez G.E., Lorenz T.C., Payne G.S., Ishihara S., Ohya Y., Andrews B., Hughes T.R., Frey B.J., Graham T.R., Andersen R.J., and Boone C. Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell 126 (2006) 611-625
38. Seigneuret M., and Devaux P.F. ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc. Natl. Acad. Sci. U. S. A. 81 (1984) 3751-3755
39. Devaux P.F. Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30 (1991) 1163-1173
40. Farge E., Ojcius D.M., Subtil A., and Dautry-Varsat A. Enhancement of endocytosis due to aminophospholipid transport across the plasma membrane of living cells. Am. J. Physiol. 276 (1999) C725-733
41. Chen C.Y., Ingram M.F., Rosal P.H., and Graham T.R. Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J. Cell Biol. 147 (1999) 1223-1236
42. Donaldson J.G., and Jackson C.L. Regulators and effectors of the ARF GTPases. Curr. Opin. Cell Biol. 12 (2000) 475-482
43. Chen C.Y., and Graham T.R. An arf1Delta synthetic lethal screen identifies a new clathrin heavy chain conditional allele that perturbs vacuolar protein transport in Saccharomyces cerevisiae. Genetics 150 (1998) 577-589
44. Gall W.E., Higginbotham M.A., Chen C., Ingram M.F., Cyr D.M., and Graham T.R. The auxilin-like phosphoprotein Swa2p is required for clathrin function in yeast. Curr. Biol. 10 (2000) 1349-1358
45. Liu K., Surendhran K., Nothwehr S.F., and Graham T.R. P4-ATPase requirement for AP-1/clathrin function in protein transport from the trans-Golgi network and early endosomes. Mol. Biol. Cell 19 (2008) 3526-3535
46. Gall W.E., Geething N.C., Hua Z., Ingram M.F., Liu K., Chen S.I., and Graham T.R. Drs2p-dependent formation of exocytic clathrin-coated vesicles in vivo. Curr. Biol. 12 (2002) 1623-1627
47. Mulholland J., Wesp A., Riezman H., and Botstein D. Yeast actin cytoskeleton mutants accumulate a new class of Golgi-derived secretary vesicle. Mol. Biol. Cell 8 (1997) 1481-1499
48. Harsay E., and Bretscher A. Parallel secretory pathways to the cell surface in yeast. J. Cell Biol. 131 (1995) 297-310
49. Schmid S.L. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66 (1997) 511-548
50. Hinners I., and Tooze S.A. Changing directions: clathrin-mediated transport between the Golgi and endosomes. J. Cell. Sci. 116 (2003) 763-771
51. Costaguta G., Stefan C.J., Bensen E.S., Emr S.D., and Payne G.S. Yeast Gga coat proteins function with clathrin in Golgi to endosome transport. Mol. Biol. Cell 12 (2001) 1885-1896
52. Black M.W., and Pelham H.R. A selective transport route from Golgi to late endosomes that requires the yeast GGA proteins. J. Cell Biol. 151 (2000) 587-600
53. Duncan M.C., and Payne G.S. ENTH/ANTH domains expand to the Golgi. Trends Cell Biol. 13 (2003) 211-215
54. Copic A., Starr T.L., and Schekman R. Ent3p and Ent5p exhibit cargo-specific functions in trafficking proteins between the trans-Golgi network and the endosomes in yeast. Mol. Biol. Cell 18 (2007) 1803-1815
55. Odorizzi G., Cowles C.R., and Emr S.D. The AP-3 complex: a coat of many colours. Trends Cell Biol. 8 (1998) 282-288
56. Yeung B.G., Phan H.L., and Payne G.S. Adaptor complex-independent clathrin function in yeast. Mol. Biol. Cell 10 (1999) 3643-3659
57. Sakane H., Yamamoto T., and Tanaka K. The functional relationship between the Cdc50p-Drs2p putative aminophospholipid translocase and the Arf GAP Gcs1p in vesicle formation in the retrieval pathway from yeast early endosomes to the TGN. Cell Struct. Funct. 31 (2006) 87-108
58. Wang C.W., Hamamoto S., Orci L., and Schekman R. Exomer: a coat complex for transport of select membrane proteins from the trans-Golgi network to the plasma membrane in yeast. J. Cell Biol. 174 (2006) 973-983
59. Trautwein M., Schindler C., Gauss R., Dengjel J., Hartmann E., and Spang A. Arf1p, Chs5p and the ChAPs are required for export of specialized cargo from the Golgi. EMBO J. 25 (2006) 943-954
60. Valdivia R.H., Baggott D., Chuang J.S., and Schekman R.W. The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev. Cell 2 (2002) 283-294
61. Losev E., Reinke C.A., Jellen J., Strongin D.E., Bevis B.J., and Glick B.S. Golgi maturation visualized in living yeast. Nature 441 (2006) 1002-1006
62. Matsuura-Tokita K., Takeuchi M., Ichihara A., Mikuriya K., and Nakano A. Live imaging of yeast Golgi cisternal maturation. Nature 441 (2006) 1007-1010
63. Liu K., Hua Z., Nepute J.A., and Graham T.R. Yeast P4-ATPases Drs2p and Dnf1p are essential cargos of the NPFXD/Sla1p endocytic pathway. Mol. Biol. Cell 18 (2007) 487-500
64. Chantalat S., Park S.K., Hua Z., Liu K., Gobin R., Peyroche A., Rambourg A., Graham T.R., and Jackson C.L. The Arf activator Gea2p and the P-type ATPase Drs2p interact at the Golgi in Saccharomyces cerevisiae. J. Cell. Sci. 117 (2004) 711-722
65. Koenig J.H., and Ikeda K. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9 (1989) 3844-3860
66. Lewis M.J., Nichols B.J., Prescianotto-Baschong C., Riezman H., and Pelham H.R. Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol. Biol. Cell 11 (2000) 23-38
67. Robinson M., Poon P.P., Schindler C., Murray L.E., Kama R., Gabriely G., Singer R.A., Spang A., Johnston G.C., and Gerst J.E. The Gcs1 Arf-GAP mediates Snc1,2 v-SNARE retrieval to the Golgi in yeast. Mol. Biol. Cell 17 (2006) 1845-1858
68. Galan J.M., Wiederkehr A., Seol J.H., Haguenauer-Tsapis R., Deshaies R.J., Riezman H., and Peter M. Skp1p and the F-box protein Rcy1p form a non-SCF complex involved in recycling of the SNARE Snc1p in yeast. Mol. Cell. Biol. 21 (2001) 3105-3117
69. Chen S.H., Chen S., Tokarev A.A., Liu F., Jedd G., and Segev N. Ypt31/32 GTPases and their novel F-box effector protein Rcy1 regulate protein recycling. Mol. Biol. Cell 16 (2005) 178-192
70. Hirst J., Lui W.W., Bright N.A., Totty N., Seaman M.N., and Robinson M.S. A family of proteins with gamma-adaptin and VHS domains that facilitate trafficking between the trans-Golgi network and the vacuole/lysosome. J. Cell Biol. 149 (2000) 67-80
71. Deloche O., and Schekman R.W. Vps10p cycles between the TGN and the late endosome via the plasma membrane in clathrin mutants. Mol. Biol. Cell 13 (2002) 4296-4307
72. Singer-Kruger B., Lasic M., Burger A.M., Hausser A., Pipkorn R., and Wang Y. Yeast and human Ysl2p/hMon2 interact with Gga adaptors and mediate their subcellular distribution. EMBO J. 27 (2008) 1423-1435
73. Huh W.K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., and O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 425 (2003) 686-691
74. Wicky S., Schwarz H., and Singer-Kruger B. Molecular interactions of yeast Neo1p, an essential member of the Drs2 family of aminophospholipid translocases, and its role in membrane trafficking within the endomembrane system. Mol. Cell. Biol. 24 (2004) 7402-7418
75. Lee M.C., Miller E.A., Goldberg J., Orci L., and Schekman R. Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20 (2004) 87-123
76. Letourneur F., Gaynor E.C., Hennecke S., Demolliere C., Duden R., Emr S.D., Riezman H., and Cosson P. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79 (1994) 1199-1207
77. Sato K., Nishikawa S., and Nakano A. Membrane protein retrieval from the Golgi apparatus to the endoplasmic reticulum (ER): characterization of the RER1 gene product as a component involved in ER localization of Sec12p. Mol. Biol. Cell 6 (1995) 1459-1477
78. Boehm J., Letourneur F., Ballensiefen W., Ossipov D., Demolliere C., and Schmitt H.D. Sec12p requires Rer1p for sorting to coatomer (COPI)-coated vesicles and retrieval to the ER. J. Cell. Sci. 110 Pt 8 (1997) 991-1003
79. Hua Z., and Graham T.R. Requirement for neo1p in retrograde transport from the Golgi complex to the endoplasmic reticulum. Mol. Biol. Cell 14 (2003) 4971-4983
80. Fei W., Alfaro G., Muthusamy B.P., Klaassen Z., Graham T.R., Yang H., and Beh C.T. Genome-wide analysis of sterol-lipid storage and trafficking in Saccharomyces cerevisiae. Eukaryot Cell 7 (2008) 401-414
81. Groen A., Kunne C., Jongsma G., van den Oever K., Mok K.S., Petruzzelli M., Vrins C.L., Bull L., Paulusma C.C., and Oude Elferink R.P. Abcg5/8 independent biliary cholesterol excretion in Atp8b1-deficient mice. Gastroenterology 134 (2008) 2091-2100
82. Kishimoto T., Yamamoto T., and Tanaka K. Defects in structural integrity of ergosterol and the Cdc50p-Drs2p putative phospholipid translocase cause accumulation of endocytic membranes, onto which actin patches are assembled in yeast. Mol. Biol. Cell 16 (2005) 5592-5609
83. Lyssenko N.N., Miteva Y., Gilroy S., Hanna-Rose W., and Schlegel R.A. An unexpectedly high degree of specialization and a widespread involvement in sterol metabolism among the C. elegans putative aminophospholipid translocases. BMC Dev. Biol. 8 (2008) 96
84. B.P. Muthusamy, S. Raychaudhuri, P. Natarajan, F. Abe, K. Liu, W.A. Prinz and T.R. Graham, Control of protein and sterol trafficking by antagonistc activtities of a P4-ATPase and oxysterol binding protein homologue. Manuscript submitted (2009).
85. Beh C.T., Cool L., Phillips J., and Rine J. Overlapping functions of the yeast oxysterol-binding protein homologues. Genetics 157 (2001) 1117-1140
86. Schulz T.A., and Prinz W.A. Sterol transport in yeast and the oxysterol binding protein homologue (OSH) family. Biochim. Biophys. Acta 1771 (2007) 769-780
87. Fang M., Kearns B.G., Gedvilaite A., Kagiwada S., Kearns M., Fung M.K., and Bankaitis V.A. 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 (1996) 6447-6459
88. Jiang B., Brown J.L., Sheraton J., Fortin N., and Bussey H. A new family of yeast genes implicated in ergosterol synthesis is related to the human oxysterol binding protein. Yeast 10 (1994) 341-353
89. Morozova N., Liang Y., Tokarev A.A., Chen S.H., Cox R., Andrejic J., Lipatova Z., Sciorra V.A., Emr S.D., and Segev N. TRAPPII subunits are required for the specificity switch of a Ypt-Rab GEF. Nat. Cell Biol. 8 (2006) 1263-1269
90. Mousley C.J., Tyeryar K.R., Vincent-Pope P., and Bankaitis V.A. The Sec14-superfamily and the regulatory interface between phospholipid metabolism and membrane trafficking. Biochim. Biophys. Acta 1771 (2007) 727-736
91. Li X., Rivas M.P., Fang M., Marchena J., Mehrotra B., Chaudhary A., Feng L., Prestwich G.D., and Bankaitis V.A. Analysis of oxysterol binding protein homologue Kes1p function in regulation of Sec14p-dependent protein transport from the yeast Golgi complex. J. Cell Biol. 157 (2002) 63-77
92. Nakano K., Yamamoto T., Kishimoto T., Noji T., and Tanaka K. Protein kinases Fpk1p and Fpk2p are novel regulators of phospholipid asymmetry. Mol. Biol. Cell 19 (2008) 1783-1797
93. Im Y.J., Raychaudhuri S., Prinz W.A., and Hurley J.H. Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature 437 (2005) 154-158
94. Raychaudhuri S., Im Y.J., Hurley J.H., and Prinz W.A. Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides. J. Cell Biol. 173 (2006) 107-119
95. Lange Y., Ye J., and Steck T.L. Scrambling of phospholipids activates red cell membrane cholesterol. Biochemistry 46 (2007) 2233-2238
96. Gomes E., Jakobsen M.K., Axelsen K.B., Geisler M., and Palmgren M.G. Chilling tolerance in Arabidopsis involves ALA1, a member of a new family of putative aminophospholipid translocases. Plant Cell 12 (2000) 2441-2454
97. Paulusma C.C., Groen A., Kunne C., Ho-Mok K.S., Spijkerboer A.L., Rudi de Waart D., Hoek F.J., Vreeling H., Hoeben K.A., van Marle J., Pawlikowska L., Bull L.N., Hofmann A.F., Knisely A.S., and Oude Elferink R.P. Atp8b1 deficiency in mice reduces resistance of the canalicular membrane to hydrophobic bile salts and impairs bile salt transport. Hepatology 44 (2006) 195-204
98. Poulsen L.R., Lopez-Marques R.L., McDowell S.C., Okkeri J., Licht D., Schulz A., Pomorski T., Harper J.F., and Palmgren M.G. The Arabidopsis P4-ATPase ALA3 localizes to the golgi and requires a beta-subunit to function in lipid translocation and secretory vesicle formation. Plant Cell 20 (2008) 658-676
99. Ruaud A.F., Nilsson L., Richard F., Larsen M.K., Bessereau J.L., and Tuck S. The C. elegans P4-ATPase TAT-1 regulates lysosome biogenesis and endocytosis. Traffic 10 (2008) 88-100