Dynamic transbilayer lipid asymmetry

Cold Spring Harbor Perspectives in Biology

Volumn 3, Issue 5, 2011, Pages 1-11

  van Meer, Gerrit ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE LIPID;

BACTERIUM; BIOLOGICAL MODEL; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; LIPID BILAYER; LIPID METABOLISM; METABOLISM; MITOCHONDRIAL MEMBRANE; PHYSIOLOGY; REVIEW; TRANSPORT AT THE CELLULAR LEVEL; TRANSPORT VESICLE; ULTRASTRUCTURE; VIRUS;

BACTERIA; BIOLOGICAL TRANSPORT; CELL MEMBRANE; LIPID BILAYERS; LIPID METABOLISM; MEMBRANE LIPIDS; MITOCHONDRIAL MEMBRANES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; TRANSPORT VESICLES; VIRUSES;

EID: 80052549175     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a004671     Document Type: Article

References (121)

1. Alaimo C, Catrein I, Morf L, Marolda CL, Callewaert N, Valvano MA, Feldman MF, Aebi M. 2006. Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. Embo J 25: 967-976.
2. Allan D, Quinn P. 1989. Membrane phospholipid asymmetry in Semliki Forest virus grown in BHK cells. Biochim Biophys Acta 987: 199-204.
3. Andrick C, Broring K, Deuticke B, Haest CW. 1991. Fast translocation of phosphatidylcholine to the outer membrane leaflet after its synthesis at the inner membrane surface in human erythrocytes. Biochim Biophys Acta 1064: 235-241.
4. Andrieu N, Salvayre R, Levade T. 1996. Comparative study of the metabolic pools of sphingomyelin and phosphatidylcholine sensitive to tumor necrosis factor. Eur J Biochem 236: 738-745.
5. Bai J, Pagano RE. 1997. Measurement of spontaneous transfer and transbilayer movement of BODIPY-labeled lipids in lipid vesicles. Biochemistry 36: 8840-8848.
6. Bakrac B, Kladnik A, Macek P, McHaffie G, Werner A, Lakey JH, Anderluh G. 2010. A toxin-based probe reveals cytoplasmic exposure of Golgi sphingomyelin. J Biol Chem 285: 22186-22195.
7. Berden JA, Barker RW, Radda GK. 1975. NMR studies on phospholipid bilayers. Some factors affecting lipid distribution. Biochim Biophys Acta 375: 186-208.
8. Bevers EM, Williamson PL. 2010. Phospholipid scramblase: An update. FEBS Lett 584: 2724-2730.
9. Bevers EM, Comfurius P, Zwaal RF. 1983. Changes in membrane phospholipid distribution during platelet activation. Biochim Biophys Acta 736: 57-66.
10. Boadu E, Bilbey NJ, Francis GA. 2008. Cellular cholesterol substrate pools for adenosine-triphosphate cassette transporter A1-dependent high-density lipoprotein formation. Curr Opin Lipidol 19: 270-276.
11. Bretscher MS. 1972. Phosphatidyl-ethanolamine: Differential labelling in intact cells and cell ghosts of human erythrocytes by a membrane-impermeable reagent. J Mol Biol 71: 523-528.
12. Buckland RM, Radda GK, Shennan CD. 1978. Accessibility of phospholipids in the chromaffin granule membrane. Biochim Biophys Acta 513: 321-337.
13. Buton X, Herve P, Kubelt J, Tannert A, Burger KN, Fellmann P, Muller P, Herrmann A, Seigneuret M, Devaux PF. 2002. Transbilayer movement of monohexosylsphingolipids in endoplasmic reticulum and Golgi membranes. Biochemistry 41: 13106-13115.
14. Buton X, Morrot G, Fellmann P, Seigneuret M. 1996. Ultrafast glycerophospholipid-selective transbilayer motion mediated by a protein in the endoplasmic reticulum membrane. J Biol Chem 271: 6651-6657.
15. Catty P, de Kerchove d'Exaerde A, Goffeau A. 1997. The complete inventory of the yeast Saccharomyces cerevisiae P-type transport ATPases. FEBS Lett 409: 325-332.
16. Chap HJ, Zwaal RF, van Deenen LL. 1977. Action of highly purified phospholipases on blood platelets. Evidence for an asymmetric distribution of phospholipids in the surface membrane. Biochim Biophys Acta 467: 146-164.
17. Chen CY, Ingram MF, Rosal PH, Graham TR. 1999. Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J Cell Biol 147: 1223-1236.
18. Cheng HT, Megha, London E. 2009. Preparation and properties of asymmetric vesicles that mimic cell membranes: Effect upon lipid raft formation and transmembrane helix orientation. J Biol Chem 284: 6079-6092.
19. Collins MD. 2008. Interleaflet coupling mechanisms in bilayers of lipids and cholesterol. Biophys J 94: L32-L34.
20. CollinsMD, Keller SL. 2008. Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers. Proc Natl Acad Sci 105: 124-128.
21. Contreras FX, Basanez G, Alonso A, Herrmann A, Goni FM. 2005. Asymmetric addition of ceramides but not dihydroceramides promotes transbilayer (flip-flop) lipid motion in membranes. Biophys J 88: 348-359.
22. Contreras FX, Villar AV, Alonso A, Kolesnick RN, Goni FM. 2003. Sphingomyelinase activity causes transbilayer lipid translocation in model and cell membranes. J Biol Chem 278: 37169-37174.
23. Crain RC, Zilversmit DB. 1980. Two nonspecific phospholipid exchange proteins from beef liver. 2. Use in studying the asymmetry and transbilayer movement of phosphatidylcholine, phosphatidylethanolamine, and sphingomyelin in intact rat erythrocytes. Biochemistry 19: 1440-1447.
24. Devaux P, McConnell HM. 1972. Lateral diffusion in spinlabeled phosphatidylcholine multilayers. J Am Chem Soc 94: 4475-4481.
25. Doerrler WT, Gibbons HS, Raetz CR. 2004. MsbAdependent translocation of lipids across the inner membrane of Escherichia coli. J Biol Chem 279: 45102-45109.
26. Dragsten PR, Blumenthal R, Handler JS. 1981. Membrane asymmetry in epithelia: is the tight junction a barrier to diffusion in the plasma membrane? Nature 294: 718-722.
27. Eckford PD, Sharom FJ. 2010. The reconstituted Escherichia coli MsbA protein displays lipid flippase activity. Biochem J 429: 195-203.
28. Ernest S, Bello-Reuss E. 1999. Secretion of platelet-activating factor is mediated by MDR1 P-glycoprotein in cultured human mesangial cells. J Am Soc Nephrol 10: 2306-2313.
29. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148: 2207-2216.
30. Farge E, Ojcius DM, Subtil A, Dautry-Varsat A. 1999. Enhancement of endocytosis due to aminophospholipid transport across the plasma membrane of living cells. Am J Physiol 276: C725-C733.
31. Gallet PF, Zachowski A, Julien R, Fellmann P, Devaux PF, Maftah A. 1999. Transbilayer movement and distribution of spin-labelled phospholipids in the inner mitochondrial membrane. Biochim Biophys Acta 1418: 61-70.
32. Gascard P, Tran D, Sauvage M, Sulpice JC, Fukami K, Takenawa T, Claret M, Giraud F. 1991. Asymmetric distribution of phosphoinositides and phosphatidic acid in the human erythrocyte membrane. Biochim Biophys Acta 1069: 27-36.
33. 2+-induced isotropic motion and phosphatidylcholine flip-flop in phosphatidylcholine-cardiolipin bilayers. Biochim Biophys Acta 598: 554-560.
34. Griffiths G, Back R, Marsh M. 1989. A quantitative analysis of the endocytic pathway in baby hamster kidney cells. J Cell Biol 109: 2703-2720.
35. Halter D, Neumann S, van Dijk SM, Wolthoorn J, de Maziere AM, Vieira OV, Mattjus P, Klumperman J, van Meer G, Sprong H. 2007. Pre-and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis. J Cell Biol 179: 101-115.
36. Hamilton JA. 2003. Fast flip-flop of cholesterol and fatty acids in membranes: implications for membrane transport proteins. Curr Opin Lipidol 14: 263-271.
37. Harvat EM, Zhang YM, Tran CV, Zhang Z, FrankMW, Rock CO, Saier MHJr. 2005. Lysophospholipid flipping across the Escherichia coli inner membrane catalyzed by a transporter (LplT) belonging to the major facilitator superfamily. J Biol Chem 280: 12028-12034.
38. Helenius J, Ng DT, Marolda CL, Walter P, Valvano MA, Aebi M. 2002. Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein. Nature 415: 447-450.
39. Herrmann A, Zachowski A, Devaux PF. 1990. Proteinmediated phospholipid translocation in the endoplasmic reticulum with a low lipid specificity. Biochemistry 29: 2023-2027.
40. Hope MJ, Redelmeier TE, Wong KF, Rodrigueza W, Cullis PR. 1989. Phospholipid asymmetry in large unilamellar vesicles induced by transmembrane pH gradients. Biochemistry 28: 4181-4187.
41. Hua Z, Graham TR. 2003. Requirement for neo1p in retrograde transport from the Golgi complex to the endoplasmic reticulum. Mol Biol Cell 14: 4971-4983.
42. Hua Z, Fatheddin P, Graham TR. 2002. 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: 3162-3177.
43. Huang J, Buboltz JT, Feigenson GW. 1999. Maximum solubility of cholesterol in phosphatidylcholine and phosphatidylethanolamine bilayers. Biochim Biophys Acta 1417: 89-100.
44. Ikeda M, Kihara A, Denpoh A, Igarashi Y. 2008. The Rim101 pathway is involved in Rsb1 expression induced by altered lipid asymmetry. Mol Biol Cell 19: 1922-1931.
45. John K, Schreiber S, Kubelt J, Herrmann A, Muller P. 2002. Transbilayer movement of phospholipids at the main phase transition of lipid membranes: Implications for rapid flip-flop in biological membranes. Biophys J 83: 3315-3323.
46. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, Arredondo FD, Hanlon R, Fudal I, Rouxel T, et al. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142: 284-295.
47. Kälin N, Fernandes J, Hrafnsdottir S, vanMeer G. 2004. Natural phosphatidylcholine is actively translocated across the plasma membrane to the surface of mammalian cells. J Biol Chem 279: 33228-33236.
48. Kato U, Emoto K, Fredriksson C, Nakamura H, Ohta A, Kobayashi T, Murakami-Murofushi K, Umeda M. 2002. A novel membrane protein, Ros3p, is required for phospholipid translocation across the plasma membrane in Saccharomyces cerevisiae. J Biol Chem 277: 37855-37862.
49. Kawai K, Fujita M, Nakao M. 1974. Lipid components of two different regions of an intestinal epithelial cell membrane of mouse. Biochim Biophys Acta 369: 222-233.
50. Kiessling V, Crane JM, Tamm LK. 2006. Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking. Biophys J 91: 3313-3326.
51. Kiessling V, Wan C, Tamm LK. 2009. Domain coupling in asymmetric lipid bilayers. Biochim Biophys Acta 1788: 64-71.
52. Kol MA, van Laak AN, Rijkers DT, Killian JA, de Kroon AI, de Kruijff B. 2003. Phospholipid flop induced by transmembrane peptides in model membranes is modulated by lipid composition. Biochemistry 42: 231-237.
53. Kolesnick RN. 1989. Sphingomyelinase action inhibits phorbol ester-induced differentiation of human promyelocytic leukemic (HL-60) cells. J Biol Chem 264: 7617-7623.
54. Kolter T, Sandhoff K. 2010. Lysosomal degradation of membrane lipids. FEBS Lett 584: 1700-1712.
55. Kornberg RD, McConnell HM. 1971. Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry 10: 1111-1120.
56. Krasilnikov OV, Yuldasheva LN. 2009. Transmembrane cholesterol migration in planar lipid membranes measured with Vibrio cholerae cytolysin as molecular tool. Biochimie 91: 620-623.
57. Kubelt J, Menon AK, Muller P, Herrmann A. 2002. Transbilayermovement of fluorescent phospholipid analogues in the cytoplasmic membrane of Escherichia coli. Biochemistry 41: 5605-5612.
58. Lange Y, Dolde J, Steck TL. 1981. The rate of transmembrane movement of cholesterol in the human erythrocyte. J Biol Chem 256: 5321-5323.
59. Lenoir G, Williamson P, Puts CF, Holthuis JC. 2009. Cdc50p plays a vital role in the ATPase reaction cycle of the putative aminophospholipid transporter Drs2p. J Biol Chem 284: 17956-17967.
60. Leventis PA, Grinstein S. 2010. The distribution and function of phosphatidylserine in cellular membranes. Annu Rev Biophys 39: 407-427.
61. Levy E, Spahis S, Sinnett D, Peretti N, Maupas-Schwalm F, Delvin E, Lambert M, Lavoie MA. 2007. Intestinal cholesterol transport proteins: An update and beyond. Curr Opin Lipidol 18: 310-318.
62. Lin T, Genestier L, Pinkoski MJ, Castro A, Nicholas S, Mogil R, Paris F, Fuks Z, Schuchman EH, Kolesnick RN, et al. 2000. Role of acidic sphingomyelinase in Fas/CD95-mediated cell death. J Biol Chem 275: 8657-8663.
63. Linsel-Nitschke P, Jehle AW, Shan J, Cao G, Bacic D, Lan D, Wang N, Tall AR. 2005. Potential role of ABCA7 in cellular lipid efflux to apoA-I. J Lipid Res 46: 86-92.
64. Lloyd-Evans E, Morgan AJ, He X, SmithDA, Elliot-Smith E, Sillence DJ, Churchill GC, Schuchman EH, Galione A, Platt FM. 2008. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat Med 14: 1247-1255.
65. López-Montero I, Rodriguez N, Cribier S, Pohl A, Velez M, Devaux PF. 2005. Rapid transbilayer movement of ceramides in phospholipid vesicles and in human erythrocytes. J Biol Chem 280: 25811-25819.
66. Menon I, Huber T, Sanyal S, Banerjee S, Barré P, Canis S, Warren JD, Hwa J, Sakmar TP, Menon AK. 2011. Opsin is a phospholipid flippase. Curr Biol 21: 149-153.
67. Mitsutake S, Suzuki C, Akiyama M, Tsuji K, Yanagi T, Shimizu H, Igarashi Y. 2010. ABCA12 dysfunction causes a disorder in glucosylceramide accumulation during keratinocyte differentiation. J Dermatol Sci 60: 128-129.
68. Mondal M, Mesmin B, Mukherjee S, Maxfield FR. 2009. Sterols are mainly in the cytoplasmic leaflet of the plasma membrane and the endocytic recycling compartment in CHO cells. Mol Biol Cell 20: 581-588.
69. Montal M, Mueller P. 1972. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc Natl Acad Sci 69: 3561-3566.
70. Morita SY, Kobayashi A, Takanezawa Y, Kioka N, Handa T, Arai H, Matsuo M, Ueda K. 2007. Bile salt-dependent efflux of cellular phospholipids mediated by ATP binding cassette protein B4. Hepatology 46: 188-199.
71. Nagao K, Kimura Y, Mastuo M, Ueda K. 2010. Lipid outward translocation by ABC proteins. FEBS Lett 584: 2717-2723.
72. Nakano K, Yamamoto T, Kishimoto T, Noji T, Tanaka K. 2008. Protein kinases Fpk1p and Fpk2p are novel regulators of phospholipid asymmetry. Mol Biol Cell 19: 1783-1797.
73. Okazaki T, Bell RM, Hannun YA. 1989. Sphingomyelin turnover induced by vitamin D3 in HL-60 cells. Role in cell differentiation. J Biol Chem 264: 19076-19080.
74. Op den Kamp JAF. 1979. Lipid asymmetry in membranes. Annu Rev Biochem 48: 47-71.
75. Pagano RE, Martin OC, Schroit AJ, Struck DK. 1981. Formation of asymmetric phospholipid membranes via spontaneous transfer of fluorescent lipid analogues between vesicle populations. Biochemistry 20: 4920-4927.
76. Paulusma CC, Elferink RP. 2010. P4 ATPases-the physiological relevance of lipid flipping transporters. FEBS Lett 584: 2708-2716.
77. Pomorski T, Lombardi R, Riezman H, Devaux PF, vanMeer G, Holthuis JC. 2003. 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: 1240-1254.
78. Raggers RJ, Vogels I, van Meer G. 2001. Multidrug-resistance P-glycoprotein (MDR1) secretes platelet-activating factor. Biochem J 357: 859-865.
79. Rawyler A, van der Schaft PH, Roelofsen B, Op den Kamp JA. 1985. Phospholipid localization in the plasma membrane of Friend erythroleukemic cells and mouse erythrocytes. Biochemistry 24: 1777-1783.
80. Renooij W, Van Golde LM. 1977. The transposition of molecular classes of phosphatidylcholine across the rat erythrocyte membrane and their exchange between the red cell membrane and plasma lipoproteins. Biochim Biophys Acta 470: 465-474.
81. RenooijW, Van Golde LM, Zwaal RF, Van Deenen LL. 1976. Topological asymmetry of phospholipid metabolism in rat erythrocyte membranes. Evidence for flip-flop of lecithin. Eur J Biochem 61: 53-58.
82. Roelants FM, Baltz AG, Trott AE, Fereres S, Thorner J. 2010. A protein kinase network regulates the function of aminophospholipid flippases. ProcNatl Acad Sci 107: 34-39.
83. Rothman JE, Kennedy EP. 1977. Rapid transmembrane movement of newly synthesized phospholipids during membrane assembly. Proc Natl Acad Sci 74: 1821-1825.
84. Rothman JE, Tsai DK, Dawidowicz EA, Lenard J. 1976. Transbilayer phospholipid asymmetry and its maintenance in the membrane of influenza virus. Biochemistry 15: 2361-2370.
85. Rousselet A, Guthmann C, Matricon J, Bienvenue A, Devaux PF. 1976. Study of the transverse diffusion of spin labeled phospholipids in biological membranes. I. Human red bloods cells. Biochim Biophys Acta 426: 357-371.
86. Rush JS, Gao N, Lehrman MA, Matveev S, Waechter CJ. 2009. Suppression of Rft1 expression does not impair the transbilayer movement of Man5GlcNAc2-P-P-dolichol in sealed microsomes from yeast. J Biol Chem 284: 19835-19842.
87. Saito K, Fujimura-Kamada K, Furuta N, Kato U, Umeda M, Tanaka K. 2004. 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: 3418-3432.
88. Sandra A, Pagano RE. 1978. Phospholipid asymmetry inLM cell plasma membrane derivatives: polar head group and acyl chain distributions. Biochemistry 17: 332-338.
89. Sanyal S, Menon AK. 2009. Flipping lipids: Why an' what's the reason for? ACS Chem Biol 4: 895-909.
90. Sanyal S, Frank CG, Menon AK. 2008. Distinct flippases translocate glycerophospholipids and oligosaccharide diphosphate dolichols across the endoplasmic reticulum. Biochemistry 47: 7937-7946.
91. Schick PK, Kurica KB, Chacko GK. 1976. Location of phosphatidylethanolamine and phosphatidylserine in the human platelet plasma membrane. J Clin Invest 57: 1221-1226.
92. Schoenwaelder SM, Yuan Y, Josefsson EC, White MJ, Yao Y, Mason KD, O'Reilly LA, Henley KJ, Ono A, Hsiao S, et al. 2009. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 114: 663-666.
93. Schroeder F, Nemecz G, Wood WG, Joiner C, Morrot G, Ayraut-Jarrier M, Devaux PF. 1991. Transmembrane distribution of sterol in the human erythrocyte. Biochim Biophys Acta 1066: 183-192.
94. Seigneuret M, Devaux PF. 1984. ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc Natl Acad Sci 81: 3751-3755.
95. Shaw JM, Moore NF, Patzer EJ, Correa-Freire MC, Wagner RR, Thompsom TE. 1979. Compositional asymmetry and transmembrane movement of phosphatidylcholine in vesicular stomatitis virus membranes. Biochemistry 18: 538-543.
96. Simard JR, Pillai BK, Hamilton JA. 2008. Fatty acid flip-flop in a model membrane is faster than desorption into the aqueous phase. Biochemistry 47: 9081-9089.
97. Simons K, vanMeer G. 1988. Lipid sorting in epithelial cells. Biochemistry 27: 6197-6202.
98. Smit JJ, Schinkel AH, Oude Elferink RP, Groen AK, Wagenaar E, van Deemter L, Mol CA, Ottenhoff R, van der Lugt NM, van Roon MA, et al. 1993. Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell 75: 451-462.
99. Soupene E, Kuypers FA. 2006. Identification of an erythroid ATP-dependent aminophospholipid transporter. Br J Haematol 133: 436-438.
100. Stapelbroek JM, Peters TA, van Beurden DH, Curfs JH, Joosten A, Beynon AJ, van Leeuwen BM, van der Velden LM, Bull L, Oude Elferink RP, et al. 2009. ATP8B1 is essential for maintaining normal hearing. Proc Natl Acad Sci 106: 9709-9714.
101. StoffelW, SorgoW. 1976. Asymmetry of the lipid-bilayer of Sindbis virus. Chem Phys Lipids 17: 324-335.
102. Stoffel W, Anderson R, Stahl J. 1975. Studies on the asymmetric arrangement of membrane-lipid-enveloped virions as a model system. Hoppe-Seylers Z Physiol Chem 356: 1123-1129.
103. Sundler R, Alberts AW, Vagelos PR. 1978. Phospholipases as probes for membrane sideness. Selective analysis of the outer monolayer of asymmetric bilayer vesicles. J Biol Chem 253: 5299-5304.
104. Takabe K, Kim RH, Allegood JC, Mitra P, Ramachandran S, Nagahashi M, Harikumar KB, Hait NC, Milstien S, Spiegel S. 2010. Estradiol induces export of sphingosine 1-phosphate from breast cancer cells via ABCC1 and ABCG2. J Biol Chem 285: 10477-10486.
105. Tang X, Halleck MS, Schlegel RA, Williamson P. 1996. A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 272: 1495-1497.
106. Tefsen B, Geurtsen J, Beckers F, Tommassen J, de Cock H. 2005. Lipopolysaccharide transport to the bacterial outer membrane in spheroplasts. J Biol Chem 280: 4504-4509.
107. Tepper AD, Ruurs P, Wiedmer T, Sims PJ, Borst J, van Blitterswijk WJ. 2000. Sphingomyelin hydrolysis to ceramide during the execution phase of apoptosis results from phospholipid scrambling and alters cell-surface morphology. J Cell Biol 150: 155-164.
108. Tsai KH, Lenard J. 1975. Asymmetry of influenza virus membrane bilayer demonstrated with phospholipase C. Nature 253: 554-555.
109. van Helvoort A, Smith AJ, Sprong H, Fritzsche I, Schinkel AH, Borst P, van Meer G. 1996. MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell 87: 507-517.
110. vanMeer G, Op denKamp JA. 1982. Transbilayermovement of various phosphatidylcholine species in intact human erythrocytes. J Cell Biochem 19: 193-204.
111. van Meer G, Simons K. 1982. Viruses budding from either the apical or the basolateral plasma membrane domain of MDCK cells have unique phospholipid compositions. EMBO J 1: 847-852.
112. vanMeer G, Simons K. 1986. The function of tight junctions in maintaining differences in lipid composition between the apical and the basolateral cell surface domains of MDCK cells. EMBO J 5: 1455-1464.
113. van Meer G, Simons K, Op den Kamp JA, van Deenen LM. 1981. Phospholipid asymmetry in Semliki Forest virus grown on baby hamster kidney (BHK-21) cells. Biochemistry 20: 1974-1981.
114. van Meer G, Halter D, Sprong H, Somerharju P, Egmond MR. 2006. ABC lipid transporters: Extruders, flippases, or flopless activators? FEBS Lett 580: 1171-1177.
115. vanMeer G, Poorthuis BJ, Wirtz KW, Op den Kamp JA, van Deenen LL. 1980. Transbilayer distribution and mobility of phosphatidylcholine in intact erythrocyte membranes. A study with phosphatidylcholine exchange protein. Eur J Biochem 103: 283-288.
116. Verkleij AJ, Zwaal RFA, Roelofsen B, Comfurius P, Kastelijn D, van Deenen LLM. 1973. The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freezeetch electron microscopy. Biochim Biophys Acta 323: 178-193.
117. Wan C, Kiessling V, Tamm LK. 2008. Coupling of cholesterol-rich lipid phases in asymmetric bilayers. Biochemistry 47: 2190-2198.
118. Wanders RJ, Visser WF, van RoermundCW, Kemp S, Waterham HR. 2007. The peroxisomal ABC transporter family. Pflugers Arch 453: 719-734.
119. Watkins WE, Menon AK. 2002. Reconstitution of phospholipid flippase activity from E. coli inner membrane: A test of the protein translocon as a candidate flippase. Biol Chem 383: 1435-1440.
120. Züllig S, Neukomm LJ, Jovanovic M, Charette SJ, Lyssenko NN, Halleck MS, Reutelingsperger CP, Schlegel RA, Hengartner MO. 2007. Aminophospholipid translocase TAT-1 promotes phosphatidylserine exposure during C. elegans apoptosis. Curr Biol 17: 994-999.
121. Zwaal RF, Comfurius P, van Deenen LL. 1977. Membrane asymmetry and blood coagulation. Nature 268: 358-360.