Regulation of transbilayer plasma membrane phospholipid asymmetry

Journal of Lipid Research

Volumn 44, Issue 2, 2003, Pages 233-242

  Daleke, David L ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Flippase; Floppase; Phosphatidylserine; Scramblase

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; AMINE; AMINOPHOSPHOLIPID; CALCIUM ION; CARRIER PROTEIN; CHOLINE; FLIPPASE; FLOPPASE; GLYCEROPHOSPHOLIPID; MEMBRANE PHOSPHOLIPID; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE; PROTEIN; SCRAMBLASE; SPECTRIN; SPHINGOLIPID; SPHINGOMYELIN; UNCLASSIFIED DRUG;

CELL ACTIVATION; CELL FUNCTION; CELL MEMBRANE; CELL STIMULATION; CELL SURFACE; CELLULAR DISTRIBUTION; CYTOPLASM; DIFFUSION; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME SPECIFICITY; ERYTHROCYTE MEMBRANE; HUMAN; LIPID BILAYER; LIPID MEMBRANE; LIPID TRANSPORT; NONHUMAN; PHOSPHOLIPID ASYMMETRY; PHOSPHOLIPID BILAYER; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SPIN LABELING; SURFACE PROPERTY; THERMODYNAMICS; TISSUE DISTRIBUTION;

ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL MEMBRANE; MEMBRANE PROTEINS; MOLECULAR STRUCTURE; PHOSPHOLIPID TRANSFER PROTEINS; PHOSPHOLIPIDS; SUBSTRATE SPECIFICITY;

EID: 0142218366     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.R200019-JLR200     Document Type: Review

References (157)

1. Bretscher, M. S. 1972. Asymmetric lipid bilayer structure for biological membranes. Nature (New Biol.). 236: 11-12.
2. Op den Kamp, J. A. F. 1979. Lipid asymmetry in membranes. Annu. Rev. Biochem. 48: 47-71.
3. Rothman, J. E., and J. Lenard. 1977. Membrane asymmetry. Science. 195: 743-753.
4. Bretscher, M. S. 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.
5. Gascard, P., D. Tran, M. Sauvage, J-C. Sulpice, K. Fukami, T. Takenawa, M. Claret, and F. Giraud. 1991. Asymmetric distribution of phosphoinositides and phosphatidic acid in the human erythrocyte membrane. Biochim. Biophys. Acta. 1069: 27-36.
6. Bütikofer, P., Z. W. Lin, D. T-Y. Chiu, and F. A. Kuypers. 1990. Transbilayer distribution and mobility of phosphatidylinositol in human red blood cells. J. Biol. Chem. 265: 16035-16038.
7. Boon, J. M., and B. D. Smith. 2002. Chemical control of phospholipid distribution across bilayer membranes. Med. Res. Rev. 22: 251-281.
8. Kolter, T., R. L. Proia, and K. Sandhoff. 2002. Combinatorial ganglioside biosynthesis. J. Biol. Chem. 277: 25859-25862.
9. Fadok, V. A., D. R. Voelker, P. A. Campbell, J. J. Cohen, D. L. Bratton, and P. M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148: 2207-2216.
10. Bevers, E. M., P. Comfurius, J. L. van Rijn, H. C. Hemker, and R. F. Zwaal. 1982. Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur. J. Biochem. 122: 429-436.
11. Lubin, B., D. Chiu, J. Bastacky, B. Roelofsen, and L. L. Van Deenen. 1981. Abnormalities in membrane phospholipid organization in sickled erythrocytes. J. Clin. Invest. 67: 1643-1649.
12. Schlegel, R. A., L. McEvoy, and P. Williamson. 1985. Membrane phospholipid asymmetry and the adherence of loaded red blood cells. Bibl. Haematol. 51: 150-156.
13. Wali, R. K., S. Jaffe, D. Kumar, N. Sorgente, and V. K. Kalra. 1987. Increased adherence of oxidant treated human and bovine erythrocytes to cultured endothelial cells. J. Cell. Physiol. 133: 25-36.
14. Fadok, V. A., D. L. Bratton, and P. M. Henson. 2001. Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences. J. Clin. Invest. 108: 957-962.
15. Fadok, V. A., D. L. Bratton, S. C. Frasch, M. L. Warner, and P. M. Henson. 1998. The role of phosphatidylserine in recognition of apoptotic cells by phagocytes. Cell Death Differ. 5: 551-562.
16. Wali, R. K., S. Jaffe, D. Kumar, and V. K. Kalra. 1988. Alterations in organization of phospholipids in erythrocytes as a factor in adherence to endothelial cells in diabetes mellitus. Diabetes. 37: 104-111.
17. Wilson, M. J., K. Richter-Lowney, and D. L. Daleke. 1993. Hyperglycemia induces a loss of phospholipid asymmetry in human erythrocytes. Biochemistry. 32: 11302-11310.
18. Pomorski, T., S. Hrafnsdottir, P. F. Devaux, and G. van Meer. 2001. Lipid distribution and transport across cellular membranes. Semin. Cell Dev. Biol. 12: 139-148.
19. Borst, P., N. Zelcer, and A. van Helvoort. 2000. ABC transporters in lipid transport. Biochim. Biophys. Acta. 1486: 128-144.
20. Borst, P., and R. O. Elferink. 2002. Mammalian abc transporters in health and disease. Annu. Rev. Biochem. 71: 537-592.
21. Bevers, E. M., P. Comfurius, D. W. Dekkers, and R. F. Zwaal. 1999. Lipid translocation across the plasma membrane of mammalian cells. Biochim. Biophys. Acta. 1439: 317-330.
22. Zwaal, R. F., and A. J. Schroit. 1997. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood. 89: 1121-1132.
23. Schlegel, R. A., and P. Williamson. 2001. Phosphatidylserine, a death knell. Cell Death Differ. 8: 551-563.
24. Bell, R. M., L. M. Ballas, and R. A. Coleman. 1981. Lipid topogenesis. J. Lipid Res. 22: 391-403.
25. Daleke, D. L., and W. H. Huestis. 1985. Incorporation and translocation of aminophospholipids in human erythrocytes. Biochemistry. 24: 5406-5416.
26. Ferrell, J. E., Jr., K. J. Lee, and W. H. Huestis. 1985. Membrane bilayer balance and erythrocyte shape: a quantitative assessment. Biochemistry. 24: 2849-2857.
27. Farge, E., and P. F. Devaux. 1992. Shape changes of giant liposomes induced by an asymmetric transmembrane distribution of phospholipids. Biophys. J. 61: 347-357.
28. Zachowski, A. 1993. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294: 1-14.
29. Bishop, W. R., and R. M. Bell. 1985. Assembly of the endoplasmic reticulum phospholipid bilayer: The phosphatidylcholine transporter. Cell. 42: 51-60.
30. Buton, X., G. Morrot, P. Fellmann, and M. Seigneuret. 1996. Ultrafast glycerophospholipid-selective transbilayer motion mediated by a protein in the endoplasmic reticulum membrane. J. Biol. Chem. 271: 6651-6657.
31. Hrafnsdottir, S., and A. K. Menon. 2000. Reconstitution and partial characterization of phospholipid flippase activity from detergent extracts of the Bacillus subtilis cell membrane. J. Bacteriol. 182: 4198-4206.
32. Gummadi, S. N., and A. K. Menon. 2002. Transbilayer movement of dipalmitoylphosphatidylcholine in proteoliposomes reconstituted from detergent extracts of endoplasmic reticulum. Kinetics of transbilayer transport mediated by a single flippase and identification of protein fractions enriched in flippase activity. J. Biol. Chem. 277: 25337-25343.
33. Holthuis, J. C., T. Pomorski, R. J. Raggers, H. Sprong, and G. Van Meer. 2001. The organizing potential of sphingolipids in intracellular membrane transport. Physiol. Rev. 81: 1689-1723.
34. Lannert, H., K. Gorgas, I. Meissner, F. T. Wieland, and D. Jeckel. 1998. Functional organization of the Golgi apparatus in glycosphingolipid biosynthesis. Lactosylceramide and subsequent glycosphingolipids are formed in the lumen of the late Golgi. J. Biol. Chem. 273: 2939-2946.
35. Burger, K. N., P. van der Bijl, and G. van Meer. 1996. Topology of sphingolipid galactosyltransferases in ER and Golgi: transbilayer movement of monohexosyl sphingolipids is required for higher glycosphingolipid biosynthesis. J. Cell Biol. 133: 15-28.
36. Buton, X., P. Herve, J. Kubelt, A. Tannert, K. N. Burger, P. Fellmann, P. Muller, A. Herrmann, M. Seigneuret, and P. F. Devaux. 2002. Transbilayer movement of monohexosylsphingolipids in endoplasmic reticulum and Golgi membranes. Biochemistry. 41: 13106-13115.
37. Mombers, C., A. J. Verkleij, J. de Gier, and L. L. M. van Deenen. 1979. The interaction of spectrin-actin and synthetic phospholipids. II. The interaction with phosphatidylserine. Biochim. Biophys. Acta. 551: 271-281.
38. Cohen, A. M., S. C. Liu, J. Lawler, L. Derick, and J. Palek. 1988. Identification of the protein 4.1 binding site to phosphatidylserine vesicles. Biochemistry. 27: 614-619.
39. Sato, S. B., and S. I. Ohnishi. 1983. Interaction of a peripheral protein of the erythrocyte membrane, band 4.1, with phosphatidylserine-containing liposomes and erythrocyte inside-out vesicles. Eur. J. Biochem. 130: 19-25.
40. Meers, P., and T. Mealy. 1993. Relationship between annexin V tryptophan exposure, calcium, and phospholipid binding. Biochemistry. 32: 5411-5418.
41. Manno, S., Y. Takakuwa, and N. Mohandas. 2002. Identification of a functional role for lipid asymmetry in biological membranes: Phosphatidylserine-skeletal protein interactions modulate membrane stability. Proc. Natl. Acad. Sci. USA. 99: 1943-1948.
42. Maksymiw, R., S. F. Sui, H. Gaub, and E. Sackmann. 1987. Electrostatic coupling of spectrin dimers to phosphatidylserine containing lipid lamellae. Biochemistry. 26: 2983-2990.
43. Gudi, S. R., A. Kumar, V. Bhakuni, S. M. Gokhale, and C. M. Gupta. 1990. Membrane skeleton-bilayer interaction is not the major determinant of membrane phospholipid asymmetry in human erythrocytes. Biochim. Biophys. Acta. 1023: 63-72.
44. O'Toole, P. J., C. Wolfe, S. Ladha, and R. J. Cherry. 1999. Rapid diffusion of spectrin bound to a lipid surface. Biochim. Biophys. Acta. 1419: 64-70.
45. O'Toole, P. J., I. E. Morrison, and R. J. Cherry. 2000. Investigations of spectrin-lipid interactions using fluoresceinphosphatidylethanolamine as a membrane probe. Biochim. Biophys. Acta. 1466: 39-46.
46. Calvez, J. Y., A. Zachowski, A. Herrmann, G. Morrot, and P. F. Devaux. 1988. Asymmetric distribution of phospholipids in spectrin-poor erythrocyte vesicles. Biochemistry. 27: 5666-5670.
47. Kuypers, F. A., B. H. Lubin, M. Yee, P. Agre, P. F. Devaux, and D. Geldwerth. 1993. The distribution of erythrocyte phospholipids in hereditary spherocytosis demonstrates a minimal role for erythrocyte spectrin on phospholipid diffusion and asymmetry. Blood. 81: 1051-1057.
48. de Jong, K., S. K. Larkin, S. Eber, P. F. Franck, B. Roelofsen, and F. A. Kuypers. 1999. Hereditary spherocytosis and elliptocytosis erythrocytes show a normal transbilayer phospholipid distribution. Blood. 94: 319-325.
49. Kornberg, R. D., and H. M. McConnell. 1971. Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry. 10: 1111-1120.
50. Fuji, T., and A. Tamura. 1983. Dynamic behaviour of amphiphilic lipids to penetrate into membrane of intact erythocytes and to induce change in the cell shape. Biomed. Biochim. Acta. 42: S81-S85.
51. Middelkoop, E., B. H. Lubin, J. A. F. Op den Kamp, and B. Roelofsen. 1986. Flip-flop rates of individual molecular species of phosphatidylcholine in the human red cell membrane. Biochim. Biophys. Acta. 855: 421-424.
52. Van Meer, G., and J. A. F. Op den Kamp. 1982. Transbilayer movement of various phosphatidylcholine species in intact human erythrocytes. J. Cell. Biochem. 19: 193-204.
53. Wali, R. K., S. Jaffe, D. Kumar, and V. K. Kalra. 1988. Alterations in organization of phospholipids in erythrocytes as factor in adherence to endothelial cells in diabetes mellitus. Diabetes. 37: 104-111.
54. Manodori, A. B., and F. A. Kuypers. 2002. Altered red cell turnover in diabetic mice. J. Lab. Clin. Med. 140: 161-165.
55. Seigneuret, M., and P. F. Devaux. 1984. ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc. Natl. Acad. Sci. USA. 81: 3751-3755.
56. Connor, J., and A. J. Schroit. 1987. Determination of lipid asymmetry in human red cells by resonance energy transfer. Biochemistry. 26: 5099-5105.
57. Sleight, R. G., and R. E. Pagano. 1985. Transbilayer movement of a fluorescent phosphatidylethanolamine analogue across the plasma membranes of cultured mammalian cells. J. Biol. Chem. 260: 1146-1154.
58. Colleau, M., P. Herve, P. Fellmann, and P. F. Devaux. 1991. Transmembrane diffusion of fluorescent phospholipids in human erythrocytes. Chem. Phys. Lipids. 57: 29-37.
59. Devaux, P. F., P. Fellmann, and P. Herve. 2002. Investigation on lipid asymmetry using lipid probes. Comparison between spin-labeled lipids and fluorescent lipids. Chem. Phys. Lipids. 116: 115-134.
60. Maier, O., V. Oberle, and D. Hoekstra. 2002. Fluorescent lipid probes: some properties and applications (a review). Chem. Phys. Lipids. 116: 3-18.
61. Daleke, D. L., and W. H. Huestis. 1989. Erythrocyte morphology reflects the transbilayer distribution of incorporated phospholipids. J. Cell Biol. 108: 1375-1385.
62. Anzai, K., Y. Yoshioka, and Y. Kirino. 1993. Novel radioactive phospholipid probes as a tool for measurement of phospholipid translocation across biomembranes. Biochim. Biophys. Acta. 1151: 69-75.
63. Tilley, L., S. Cribier, B. Roelofsen, J. A. F. Op den Kamp, and L. L. M. van Deenen. 1986. ATP-dependent translocation of aminophospholipids across the human erythrocyte membrane. FEBS Lett. 194: 21-27.
64. Bitbol, M., P. Fellmann, A. Zachowski, and P. F. Devaux. 1987. Ion regulation of phosphatidylserine and phosphatidylethanolamine outside-inside translocation in human erythrocytes. Biochim. Biophys. Acta. 904: 268-282.
65. Beleznay, Z., A. Zachowski, P. F. Devaux, M. P. Navazo, and P. Ott. 1993. ATP-dependent aminophospholipid translocation in erythrocyte vesicles: stoichiometry of transport. Biochemistry. 32: 3146-3152.
66. Connor, J., and A. J. Schroit. 1990. Aminophospholipid translocation in erythrocytes: evidence for the involvement of a specific transporter and an endofacial protein. Biochemistry. 29: 37-43.
67. Connor, J., C. H. Pak, R. F. Zwaal, and A. J. Schroit. 1992. Bidirectional transbilayer movement of phospholipid analogs in human red blood cells. Evidence for an ATP-dependent and protein-mediated process. J. Biol. Chem. 267: 19412-19417.
68. Connor, J., and A. J. Schroit. 1989. Transbilayer movement of phosphatidylserine in nonhuman erythrocytes: evidence that the aminophospholipid transporter is a ubiquitous membrane protein. Biochemistry. 28: 9680-9685.
69. Sune, A., P. Bette-Bobillo, A. Bienvenue, P. Fellmann, and P. F. Devaux. 1987. Selective outside-inside translocation of aminophospholipids in human platelets. Biochemistry. 2: 2972-2978.
70. Zachowski, A., A. Herrmann, A. Paraf, and P. F. Devaux. 1987. Phospholipid outside-inside translocation in lymphocyte plasma membranes is a protein-mediated phenomenon. Biochim. Biophys. Acta. 897: 197-200.
71. Julien, M., J. F. Tournier, and J. F. Tocanne. 1993. Differences in the transbilayer and lateral motions of fluorescent analogs of phosphatidylcholine and phosphatidylethanolamine in the apical plasma membrane of bovine aortic endothelial cells. Exp. Cell Res. 208: 387-397.
72. Martin, O. C., and R. E. Pagano. 1987. Transbilayer movement of fluorescent analogs of phosphatidylserine and phosphatidylethanolamine at the plasma membrane of cultured cells. Evidence for a protein-mediated and ATP-dependent process(es). J. Biol. Chem. 262: 5890-5898.
73. Pomorski, T., P. Muller, B. Zimmermann, K. Burger, P. F. Devaux, and A. Herrmann. 1996. Transbilayer movement of fluorescent and spin-labeled phospholipids in the plasma membrane of human fibroblasts: a quantitative approach. J. Cell Sci. 109: 687-698.
74. Cribier, S., J. Sainte-Marie, and P. F. Devaux. 1993. Quantitative comparison between aminophospholipid translocase activity in human erythrocytes and in K562 cells. Biochim. Biophys. Acta. 1148: 85-90.
75. Müller, P., T. Pomorski, S. Porwoli, R. Tauber, and A. Herrmann. 1996. Transverse movement of spin-labeled phospholipids in the plasma membrane of a hepatocytic cell line (HepG2): implications for biliary lipid secretion. Hepatology. 24: 1497-1503.
76. Müller, K., T. Pomorski, P. Muller, A. Zachowski, and A. Herrmann. 1994. Protein-dependent translocation of aminophospholipids and asymmetric transbilayer distribution of phospholipids in the plasma membrane of ram sperm cells. Biochemistry. 33: 9968-9974.
77. Zachowski, A., and Y. M. Gaudry-Talarmain. 1990. Phospholipid transverse diffusion in synaptosomes: evidence for the involvement of the aminophospholipid translocase. J. Neurochem. 55: 1352-1356.
78. Zachowski, A., J. P. Henry, and P. F. Devaux. 1989. Control of transmembrane lipid asymmetry in chromaffin granules by an ATP-dependent protein. Nature. 340: 75-76.
79. Pomorski, T., A. Herrmann, P. Muller, G. van Meer, and K. Burger. 1999. Protein-mediated inward translocation of phospholipids occurs in both the apical and basolateral plasma membrane domains of epithelial cells. Biochemistry. 38: 142-150.
80. Daleke, D. L., J. V. Lyles, E. Nemergut, and M. L. Zimmerman. 1995. Purification and substrate specificity of the human erythrocyte aminophospholipid transporter. NATO ASI Ser. H. 91: 49-59.
81. Morrot, G., P. Herve, A. Zachowski, P. Fellmann, and P. F. Devaux. 1989. Aminophospholipid translocase of human erythrocytes: phospholipid substrate specificity and effect of cholesterol. Biochemistry. 28: 3456-3462.
82. Zachowski, A., E. Favre, S. Cribier, P. Herve, and P. F. Devaux. 1986. Outside-inside translocation of aminophospholipids in the human erythrocyte membrane is mediated by a specific enzyme. (Published erratum appears in Biochemistry. 1986. 18;25(23): 7788) Biochemistry. 25: 2585-2590.
83. Zachowski, A., E. Favre, S. Cribier, P. Herve, and P. F. Devaux. 1986. Outside-inside translocation of aminophospholipids in the human erythrocyte membrane is mediated by a specific enzyme. (Published erratum appears in Biochemistry. 1986. 18;25(23): 7788) Biochemistry. 25: 2585-2590.
84. Johnson, J. E., M. L. Zimmerman, D. L. Daleke, and A. C. Newton. 1998. Lipid structure and not membrane structure is the major determinant in the regulation of protein kinase C by phosphatidylserine. Biochemistry. 37: 12020-12025.
85. Hoffmann, P. R., A. M. deCathelineau, C. A. Ogden, Y. Leverrier, D. L. Bratton, D. L. Daleke, A. J. Ridley, V. A. Fadok, and P. M. Henson. 2001. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J. Cell Biol. 155: 649-659.
86. Fadok, V. A., A. de Cathelineau, D. L. Daleke, P. M. Henson, and D. L. Bratton. 2001. Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. J. Biol. Chem. 276: 1071-1077.
87. Hall, M. P., and W. H. Huestis. 1994. Phosphatidylserine head-group diastereomers translocate equivalently across human erythrocyte membranes. Biochim. Biophys. Acta. 1190: 243-247.
88. Puri, V., and C. M. Gupta. 1998. Out-to-in translocation of butanetriol-containing phospholipid analogs in human erythrocyte membrane. Biochim. Biophys. Acta. 1373: 59-66.
89. Fellmann, P., P. Herve, T. Pomorski, P. Muller, D. Geldwerth, A. Herrmann, and P. F. Devaux. 2000. Transmembrane movement of diether phospholipids in human erythrocytes and human fibroblasts. Biochemistry. 39: 4994-5003.
90. Schroit, A. J., J. Madsen, and A. E. Ruoho. 1987. Radioiodinated, photoactivatable phosphatidylcholine and phosphatidylserine: transfer properties and differential photoreactive interaction with human erythrocyte membrane proteins. Biochemistry. 26: 1812-1819.
91. Loh, R. K., and W. H. Huestis. 1993. Human erythrocyte membrane lipid asymmetry: transbilayer distribution of rapidly diffusing phosphatidylserines. Biochemistry. 32: 11722-11726.
92. Zachowski, A., P. Fellmann, P. Herve, and P. F. Devaux. 1987. Labeling of human erythrocyte membrane proteins by photoactivatable radioiodinated phosphatidylcholine and phosphatidylserine. A search for the aminophospholipid translocase. FEBS Lett. 223: 315-320.
93. Nichols, J. W. 2002. Internalization and trafficking of fluorescent-labeled phospholipids in yeast. Semin. Cell Dev. Biol. 13: 179-184.
94. Grant, A. M., P. K. Hanson, L. Malone, and J. W. Nichols. 2001. NBD-labeled phosphatidylcholine and phosphatidylethanolamine are internalized by transbilayer transport across the yeast plasma membrane. Traffic. 2: 37-50.
95. Daleke, D. L., and J. V. Lyles. 2000. Identification and purification of aminophospholipid flippases. Biochim. Biophys. Acta. 1486: 108-127.
96. 2+-ATPase. A candidate aminophospholipid translocase. FEBS Lett. 266: 29-32.
97. Auland, M. E., B. D. Roufogalis, P. E. Devaux, and A. Zachowski. 1994. Reconstitution of ATP-dependent aminophospholipid translocation in proteoliposomes. Proc. Natl. Acad. Sci. USA. 91: 10938-10942.
98. Moriyama, Y., and N. Nelson. 1988. Purification and properties of a vanadate- and N-ethylmaleimide-sensitive ATPase from chromaffin granule membranes. J. Biol. Chem. 263: 8521-8527.
99. Moriyama, Y., N. Nelson, M. Maeda, and M. Futai. 1991. Vanadate-sensitive ATPase from chromaffin granule membranes formed a phosphoenzyme intermediate and was activated by phosphatidylserine. Arch. Biochem. Biophys. 286: 252-256.
100. Tang, X., M. S. Halleck, R. A. Schlegel, and P. Williamson. 1996. A subfamily of P-type ATPases with aminophospholipid transporting activity. [published erratum appears in Science 1996 Dec 6;274(5293):1597] Science. 272: 1495-1497.
101. Tang, X., M. S. Halleck, R. A. Schlegel, and P. Williamson. 1996. A subfamily of P-type ATPases with aminophospholipid transporting activity. [published erratum appears in Science 1996 Dec 6;274(5293):1597] Science. 272: 1495-1497.
102. Ding, J., Z. Wu, B. P. Crider, Y. Ma, X. Li, C. Slaughter, L. Gong, and X. S. Xie. 2000. 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: 23378-23386.
103. Mouro, I., M. S. Halleck, R. A. Schlegel, M. G. Mattei, P. Williamson, A. Zachowski, P. Devaux, J. P. Cartron, and Y. Colin. 1999. Cloning, expression, and chromosomal mapping of a human ATPase II gene, member of the third subfamily of P-type ATPases and orthologous to the presumed bovine and murine aminophospholipid translocase. Biochem. Biophys. Res. Commun. 257: 333-339.
104. Halleck, M. S., D. Pradhan, C. Blackman, C. Berkes, P. Williamson, and R. A. Schlegel. 1998. Multiple members of a third sub-family of P-type ATPases identified by genomic sequences and ESTs. Genome Res. 8: 354-361.
105. Axelsen, K. B., and M. G. Palmgren. 1998. Evolution of substrate specificities in the P-type ATPase superfamily. J. Mol. Evol. 46: 84-101.
106. Ripmaster, T. L., G. P. Vaughn, and J. L. Woolford, Jr. 1993. DRS1 to DRS7, novel genes required for ribosome assembly and function in Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 7901-7912.
107. Marx, U., T. Polakowski, T. Pomorski, C. Lang, H. Nelson, N. Nelson, and A. Herrmann. 1999. Rapid transbilayer movement of fluorescent phospholipid analogues in the plasma membrane of endocytosis-deficient yeast cells does not require the Drs2 protein. Eur. J. Biochem. 263: 254-263.
108. Gomes, E., M. K. Jakobsen, K. B. Axelsen, M. Geisler, and M. G. Palmgren. 2000. Chilling tolerance in Arabidopsis involves ALA1, a member of a new family of putative aminophospholipid translocases. Plant Cell. 12: 2441-2454.
109. Bull, L. N., M. J. van Eijk, L. Pawlikowska, J. A. DeYoung, J. A. Juijn, M. Liao, L. W. Klomp, N. Lomri, R. Berger, B. F. Scharschmidt, A. S. Knisely, R. H. Houwen, and N. B. Freimer. 1998. A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis. Nat. Genet. 18: 219-224.
110. Siegmund, A., A. Grant, C. Angeletti, L. Malone, J. W. Nichols, and H. K. Rudolph. 1998. Loss of Drs2p does not abolish transfer of fluorescence-labeled phospholipids across the plasma membrane of Saccharomyces cerevisiae. J. Biol. Chem. 273: 34399-34405.
111. Paterson, J., M. Zimmerman, J. Lyles, C-W. Lee, M. Halleck, P. Williamson, R. Schlegel, and D. L. Daleke. 2001. Lipid specificity of candidate flippases (Abstract). Biophys. J. 80: 256.
112. Meguro, M., A. Kashiwagi, K. Mitsuya, M. Nakao, I. Kondo, S. Saitoh, and M. Oshimura. 2001. A novel maternally expressed gene, ATP10C, encodes a putative aminophospholipid translocase associated with Angelman syndrome. Nat. Genet. 28: 19-20.
113. Dhar, M., L. S. Webb, L. Smith, L. Hauser, D. Johnson, and D. B. West. 2000. A novel ATPase on mouse chromosome 7 is a candidate gene for increased body fat. Physiol. Genomics. 4: 93-100.
114. Bitbol, M., and P. F. Devaux. 1988. Measurement of outward translocation of phospholipids across human erythrocyte membrane. Proc. Natl. Acad. Sci. USA. 85: 6783-6787.
115. Prasad, R., S. L. Panwar, and Smriti. 2002. Drug resistance in yeasts-an emerging scenario. Adv. Microb. Physiol. 46: 155-201.
116. Smriti, S. S., Krishamurthy, and R. Prasad. 1999. Membrane fluidity affects functions of Cdr1p, a multidrug ABC transporter of Candida albicans. FEMS Microbiol. Lett. 173: 475-81.
117. Zhou, Z., K. A. White, A. Polissi, C. Georgopoulos, and C. R. Raetz. 1998. Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J. Biol. Chem. 273: 12466-12475.
118. Doerrler, W. T., and C. R. Raetz. 2002. ATPase activity of the MsbA lipid flippase of Escherichia coli. J. Biol. Chem. 277: 36697-36705.
119. Rust, S., M. Rosier, H. Funke, J. Real, Z. Amoura, J. C. Piette, J. F. Deleuze, H. B. Brewer, N. Duverger, P. Denefle, and G. Assmann. 1999. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat. Genet. 22: 352-355.
120. Bodzioch, M., E. Orso, J. Klucken, T. Langmann, A. Bottcher, W. Diederich, W. Drobnik, S. Barlage, C. Buchler, M. Porsch-Ozcurumez, W. E. Kaminski, H. W. Hahmann, K. Oette, G. Rothe, C. Aslanidis, K. J. Lackner, and G. Schmitz. 1999. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 22: 347-351.
121. Brooks-Wilson, A., M. Marcil, S. M. Clee, L. H. Zhang, K. Roomp, M. van Dam, L. Yu, C. Brewer, J. A. Collins, H. O. Molhuizen, O. Loubser, B. F. Ouelette, K. Fichter, K. J. Ashbourne-Excoffon, C. W. Sensen, S. Scherer, S. Mott, M. Denis, D. Martindale, J. Frohlich, K. Morgan, B. Koop, S. Pimstone, J. J. Kastelein, and M. R. Hayden. 1999. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 22: 336-345.
122. Hamon, Y., C. Broccardo, O. Chambenoit, M. F. Luciani, F. Toti, S. Chaslin, J. M. Freyssinet, P. F. Devaux, J. McNeish, D. Marguet, and G. Chimini. 2000. ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat. Cell Biol. 2: 399-406.
123. Smith, J. D., C. Waelde, A. Horwitz, and P. Zheng. 2002. Evaluation of the role of phosphatidylserine translocase activity in ABCA1-mediated lipid efflux. J. Biol. Chem. 277: 17797-17803.
124. Luciani, M. F., and G. Chimini. 1996. The ATP binding cassette transporter ABC1, is required for the engulfment of corpses generated by apoptotic cell death. EMBO J. 15: 226-235.
125. van Helvoort, A., A. J. Smith, H. Sprong, I. Fritzsche, A. H. Schinkel, P. Borst, and G. van Meer. 1996. MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell. 87: 507-517.
126. Bosch, I., K. Dunussi-Joannopoulos, R. L. Wu, S. T. Furlong, and J. Croop. 1997. Phosphatidylcholine and phosphatidylethanolamine behave as substrates of the human MDR1 P-glycoprotein. Biochemistry. 36: 5685-5694.
127. Raggers, R. J., I. Vogels, and G. van Meer. 2001. Multidrug-resistance P-glycoprotein (MDR1) secretes platelet-activating factor. Biochem. J. 357: 859-865.
128. Romsicki, Y., and F. J. Sharom. 2001. Phospholipid flippase activity of the reconstituted P-glycoprotein multidrug transporter. Biochemistry. 40: 6937-6947.
129. Smit, J. J., A. H. Schinkel, R. P. Oude Elferink, A. K. Groen, E. Wagenaar, L. van Deemter, C. A. Mol, R. Ottenhoff, N. M. van der Lugt, and M. A. van Roon. 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.
130. Ruetz, S., and P. Gros. 1994. Phosphatidylcholine translocase: a physiological role for the mdr2 gene. Cell. 77: 1071-1081.
131. Nies, A. T., Z. Gatmaitan, and I. M. Arias. 1996. ATP-dependent phosphatidylcholine translocation in rat liver canalicular plasma membrane vesicles. J. Lipid Res. 37: 1125-1136.
132. Smit, J. J., A. H. Schinkel, C. A. Mol, D. Majoor, W. J. Mooi, A. P. Jongsma, C. R. Lincke, and P. Borst. 1994. Tissue distribution of the human MDR3 P-glycoprotein. Lab. Invest. 71: 638-649.
133. Deeley, R. G., and S. P. Cole. 1997. Function, evolution and structure of multidrug resistance protein (MRP). Semin. Cancer Biol. 8: 193-204.
134. Pulaski, L., G. Jedlitschky, I. Leier, U. Buchholz, and D. Keppler. 1996. Identification of the multidrug-resistance protein (MRP) as the glutathione-S-conjugate export pump of erythrocytes. Eur. J. Biochem. 241: 644-648.
135. Kamp, D., and C. W. Haest. 1998. Evidence for a role of the multidrug resistance protein (MRP) in the outward translocation of NBD-phospholipids in the erythrocyte membrane. Biochim. Biophys. Acta. 1372: 91-101.
136. Dekkers, D. W., P. Comfurius, R. G. van Gool, E. M. Bevers, and R. F. Zwaal. 2000. Multidrug resistance protein 1 regulates lipid asymmetry in erythrocyte membranes. Biochem. J. 350: 531-535.
137. Dekkers, D. W., P. Comfurius, A. J. Schroit, E. M. Bevers, and R. F. Zwaal. 1998. Transbilayer movement of NBD-labeled phospholipids in red blood cell membranes: outward-directed transport by the multidrug resistance protein 1 (MRP1). Biochemistry. 37: 14833-14837.
138. Raggers, R. J., A. van Helvoort, R. Evers, and G. van Meer. 1999. The human multidrug resistance protein MRP1 translocates sphingolipid analogs across the plasma membrane. J. Cell Sci. 112: 415-422.
139. Weng, J., N. L. Mata, S. M. Azarian, R. T. Tzekov, D. G. Birch, and G. H. Travis. 1999. Insights into the function of Rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice. Cell. 98: 13-23.
140. Allikmets, R., N. F. Shroyer, N. Singh, J. M. Seddon, R. A. Lewis, P. S. Bernstein, A. Peiffer, N. A. Zabriskie, Y. Li, A. Hutchinson, M. Dean, J. R. Lupski, and M. Leppert. 1997. Mutation of the Stargardt disease gene (ABCR) in age-related macular degeneration. Science. 277: 1805-1807.
141. Allikmets, R., N. Singh, H. Sun, N. F. Shroyer, A. Hutchinson, A. Chidambaram, B. Gerrard, L. Baird, D. Stauffer, A. Peiffer, A. Rattner, P. Smallwood, Y. Li, K. L. Anderson, R. A. Lewis, J. Nathans, M. Leppert, M. Dean, and J. R. Lupski. 1997. A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat. Genet. 15: 236-246.
142. Backer, J. M., and E. A. Dawidowicz. 1985. Membrane assembly: evidence for a phospholipid "flipase" in rat liver microsomes (Abstract). J. Cell Biol. 101: 261.
143. Herrmann, A., A. Zachowski, and P. F. Devaux. 1990. Protein-mediated phospholipid translocation in the endoplasmic reticulum with a low lipid specificity. Biochemistry. 29: 2023-2027.
144. McEvoy, L., P. Williamson, and R. A. Schlegel. 1986. Membrane phospholipid asymmetry as a determinant of erythrocyte recognition by macrophages. Proc. Natl. Acad. Sci. USA. 83: 3311-3315.
145. Connor, J., C. C. Pak, and A. J. Schroit. 1994. Exposure of phosphatidylserine in the outer leaflet of human red blood cells. Relationship to cell density, cell age, and clearance by mononuclear cells. J. Biol. Chem. 269: 2399-2404.
146. 2+-dependent transbilayer movement of phospholipid. J. Biol. Chem. 271: 17205-17210.
147. Comfurius, P., P. Williamson, E. F. Smeets, R. A. Schlegel, E. M. Bevers, and R. F. Zwaal. 1996. Reconstitution of phospholipid scramblase activity from human blood platelets. Biochemistry. 35: 7631-7634.
148. Zhou, Q., J. Zhao, J. G. Stout, R. A. Luhm, T. Wiedmer, and P. J. Sims. 1997. Molecular cloning of human plasma membrane phospholipid scramblase. A protein mediating transbilayer movement of plasma membrane phospholipids. J. Biol. Chem. 272: 18240-18244.
149. Wiedmer, T., Q. Zhou, D. Y. Kwoh, and P. J. Sims. 2000. Identification of three new members of the phospholipid scramblase gene family. Biochim. Biophys. Acta. 1467: 244-253.
150. Zhou, Q., J. Zhao, T. Wiedmer, and P. J. Sims. 2002. Normal hemostasis but defective hematopoietic response to growth factors in mice deficient in phospholipid scramblase 1. Blood. 99: 4030-4038.
151. Sims, P. J., and T. Wiedmer. 2001. Unraveling the mysteries of phospholipid scrambling. Thromb. Haemost. 86: 266-275.
152. Sun, J., J. Zhao, M. A. Schwartz, J. Y. Wang, T. Wiedmer, and P. J. Sims. 2001. c-Abl tyrosine kinase binds and phosphorylates phospholipid scramblase 1. J. Biol. Chem. 276: 28984-28990.
153. Frasch, S. C., P. M. Henson, J. M. Kailey, D. A. Richter, M. S. Janes, V. A. Fadok, and D. L. Bratton. 2000. Regulation of phospholipid scramblase activity during apoptosis and cell activation by protein kinase Cdelta. J. Biol. Chem. 275: 23065-23073.
154. Sun, J., M. Nanjundan, L. J. Pike, T. Wiedmer, and P. J. Sims. 2002. Plasma membrane phospholipid scramblase 1 is enriched in lipid rafts and interacts with the epidermal growth factor receptor. Biochemistry. 41: 6338-6345.
155. Bevers, E. M., P. Comfurius, and R. F. Zwaal. 1983. Changes in membrane phospholipid distribution during platelet activation. Biochim. Biophys. Acta. 736: 57-66.
156. 2+ induces transbilayer redistribution of all major phospholipids in human erythrocytes. Biochemistry. 31: 6355-6360.
157. 2+-induced scrambling of various fluorescently labelled lipid analogues in red blood cells. Biochem. J. 362: 741-747.