Tracking down lipid flippases and their biological functions

Journal of Cell Science

Volumn 117, Issue 6, 2004, Pages 805-813

  Pomorski, Thomas ^a   Holthuis, Joost C M ^b   Hermann, Andreas ^a   van Meer, Gerrit ^b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

ABC transporter; Lipid flippase; Membrane dynamics; P type ATPase; Vesicle budding

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARRIER PROTEIN; LIPID TRANSFER PROTEIN; MEMBRANE PROTEIN; PHOSPHOLIPID;

CELL COMPOSITION; CELL MEMBRANE; CELL ORGANELLE; CELL VACUOLE; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; EUKARYOTIC CELL; GOLGI COMPLEX; LEISHMANIA; LIPID BILAYER; LIPID TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVIEW; SECRETORY VESICLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CARRIER PROTEINS; CELL MEMBRANE; FUNGAL PROTEINS; HUMANS; INTRACELLULAR MEMBRANES; LEISHMANIA; LIPID METABOLISM; LIPIDS; MEMBRANE PROTEINS; MEMBRANES, ARTIFICIAL; MICE; YEASTS;

EUKARYOTA; MAMMALIA;

EID: 1642378564     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01055     Document Type: Review

References (91)

1. Araujo-Santos, J. M., Gamarro, F., Castanys, S., Herrmann, A. and Pomorski, T. (2003). Rapid transport of phospholipids across the plasma membrane of Leishmania infantum. Biochem. Biophys. Res. Commun. 306, 250-255.
2. 2+-dependent transbilayer movement of phospholipid. J. Biol. Chem. 271, 17205-17210.
3. Bell, R. M., Ballas, L. M. and Coleman, R. A. (1981). Lipid topogenesis. J. Lipid Res. 22, 391-403.
4. Berge, K. E., Tian, H., Graf, G. A., Yu, L., Grishin, N. V., Schultz, J., Kwiterovich, P., Shan, B., Barnes, R. and Hobbs, H. H. (2000). Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. Science 290, 1771-1775.
5. Bezombes, C., Maestre, N., Laurent, G., Levade, T., Bettaieb, A. and Jaffrezou, J. P. (1998). Restoration of TNF-alpha-induced ceramide generation and apoptosis in resistant human leukemia KG1a cells by the P-glycoprotein blocker PSC833. FASEB J. 12, 101-109.
6. Bishop, W. R. and Bell, R. M. (1985). Assembly of the endoplasmic reticulum phospholipid bilayer: the phosphatidylcholine transporter. Cell 42, 51-60.
7. Bretscher, M. S. (1972). Asymmetrical lipid bilayer structure for biological membranes. Nat. New Biol. 236, 11-12.
8. Bretscher, M. S. (1973). Membrane structure: some general principles. Science 181, 622-629.
9. Burger, K. N., van der Bijl, P. and van Meer, G. (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.
10. Buton, X., Morrot, G., Fellmann, P. and Seigneuret, M. (1996). Ultrafast glycerophospholipid-selective transbilayer motion mediated by a protein in the endoplasmic reticulum membrane. J. Biol. Chem. 271, 6651-6657.
11. Buton, X., Hervé, P., Kubelt, J., Tannert, A., Burger, K. N., Fellmann, P., Muller, P., Herrmann, A., Seigneuret, M. and Devaux, P. F. (2002). Transbilayer movement of monohexosyl sphingolipids in endoplasmic reticulum and Golgi membranes. Biochemistry 41, 13106-13115.
12. Catty, P., de Kerchove d'Exaerde, A. and Goffeau, A. (1997). The complete inventory of the yeast Saccharomyces cerevisiae P-type transport ATPases. FEBS Lett. 409, 325-332.
13. Chambenoit, Y., Hamon, D., Marguet, D., Rigneault, H., Rosseneu, M. and Chimini, G. (2001). Specific docking of apolipoprotein A-1 at the cell surface requires a functional ABCA1 transporter. J. Biol. Chem. 276, 9955-9960.
14. Chen, C. Y., Ingram, M. F., Rosal, P. H. and Graham, T. R. (1999). Role of Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J. Cell Biol. 147, 1223-1236.
15. Chojnacki, T. and Dallner, G. (1988). The biological role of dolichol. Biochem. J. 251, 1-9.
16. Comfurius, P., Williamson, P., Smeets, E. F., Schlegel, R. A., Bevers, E. M. and Zwaal, R. F. (1996). Reconstitution of phospholipid scramblase activity from human blood platelets. Biochemistry 35, 7631-7634.
17. Connor, J., Pak, C. H., Zwaal, R. F. and Schroit, A. J. (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.
18. Decottignies, A., Grant, A. M., Nichols, J. W., de Wet, H., McIntosh, D. B. and Goffeau, A. (1998). ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J. Biol. Chem. 273, 12612-12622.
19. Dekkers, D. W., Comfurius, P., van Gool, R. G., Bevers, E. M. and Zwaal, R. F. (2000). Multidrug resistance protein 1 regulates lipid asymmetry in erythrocyte membranes. Biochem. J. 350, 531-535.
20. De Kruijff, B. and van Zoelen, E. J. (1978). Effect of the phase transition on the transbilayer movement of dimyristoyl phosphatidylcholine in unilamellar vesicles. Biochim. Biophys. Acta 511, 105-115.
21. Devaux, P. F., Fellmann, P. and Herve, P. (2002). Investigation on lipid asymmetry using lipid probes: Comparison between spin-labeled lipids and fluorescent lipids. Chem. Phys. Lipids 116, 115-134.
22. Fadok, V. A., Bratton, D. L., Rose, D. M., Pearson, A., Ezekewitz, R. A., Henson, P. M. (2000). A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405, 85-90.
23. Farge, E. and Devaux, P. F. (1992). Shape changes of giant liposomes induced by an asymmetric transmembrane distribution of phospholipids. Biophys. J. 61, 347-357.
24. Farge, E., Ojcius, D. M., Subtil, A. and Dautry-Varsat, A. (1999). Enhancement of endocytosis due to aminophospholipid transport across the plasma membrane of living cells. Am. J. Physiol. 276, C725-C733.
25. Flesch, F. M., Brouwers, J. F., Nievelstein, P. F., Verkleij, A. J., van Golde, L. M., Colenbrander, B. and Gadella, B. M. (2001). Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J. Cell Sci. 114, 3543-3555.
26. Gadella, B. M. and Harrison, R. A. (2002). Capacitation induces cyclic adenosine 3′,5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod. 67, 340-350.
27. Gaffet, P., Bettache, N. and Bienvenue, A. (1995). Transverse redistribution of phospholipids during human platelet activation: evidence for a vectorial outflux specific to aminophospholipids. Biochemistry 34, 6762-6769.
28. Gall, W. E., Geething, N. C., Hua, Z., Ingram, M. F., Liu, K., Chen, S. I. and Graham, T. R. (2002). Drs2p-dependent formation of exocytic clathrin-coated vesicles in vivo. Curr. Biol. 12, 1623-1627.
29. Gomès, E., Jakobsen, M. K., Axelsen, K. B., Geisler, M. and Palmgren, M. G. (2000). Chilling tolerance in Arabidopsis involves ALA1, a member of a new family of putative aminophospholipid translocases. Plant Cell 12, 2441-2454.
30. Graf, G. A., Li, W. P., Gerard, R. D., Gelissen, I., White, A., Cohen, J. C. and Hobbs, H. H. (2002). Coexpression of ATP-binding cassette proteins ABCG5 and ABCG8 permits their transport to the apical surface. J. Clin. Invest. 110, 659-669.
31. Grant, A. M., Hanson, P. K., Malone, L. and Nichols, J. W. (2001). NBD-labeled phosphatidylcholine and phosphatidylethanolamine are internalized by transbilayer transport across the yeast plasma membrane. Traffic 2, 37-50.
32. Hakomori, S. (2003). Structure, organization, and function of glycosphingolipids in membrane. Curr. Opin. Hematol. 10, 16-24.
33. Halleck, M. S., Pradhan, D., Blackman, C., Berkes, C., Williamson, P. and Schlegel, R. A. (1998). Multiple members of a third subfamily of P-type ATPases identified by genomic sequences and ESTs. Genome Res. 8, 354-361.
34. Halleck, M. S., Lawler, J. F. Jr, Blackshaw, S., Gao, L., Nagarajan, P., Hacker, C., Pyle, S., Newman, J. T., Nakanishi, Y., Ando, H., Weinstock, D., Williamson, P. and Schlegel, R. A. (1999). Differential expression of putative transbilayer amphipath transporters. Physiol. Genomics 1, 139-150.
35. Hamilton, J. A. (2003). Fast flip-flop of cholesterol and fatty acids in membranes: implications for membrane transport proteins. Curr. Opin. Lipidol. 14, 263-271.
36. Hamon, Y., Broccardo, C., Chambenoit, O., Luciani, M. F., Toti, F., Chaslin, S., Freyssinet, J. M., Devaux, P. F., McNeish, J., Marguet, D. and Chimini, G. (2000). ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat. Cell Biol. 2, 399-406.
37. Hanson, P. K., Malone, L., Birchmore, J. L. and Nichols, J. W. (2003). Lem3p is essential for the uptake and potency of alkylphosphocholine drugs, edelfosine and miltefosine. J. Biol. Chem. 278, 36041-36050.
38. Harder, T. and van Meer, G. (2003). Lipid-based membrane domains: Physics meets immunology. Traffic 4, 812-820.
39. Helenius, J., Ng, D. T., Marolda, C. L., Walter, P., Valvano, M. A. and Aebi, M. (2002). Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein. Nature 415, 447-450.
40. Herrmann, A., Zachowski, A. and Devaux, P. F. (1990). Protein-mediated phospholipid translocation in the endoplasmic reticulum with low lipid specificity. Biochemistry 29, 2023-2027.
41. Herzing, L. B., Kim, S. J., Cook, E. H. Jr and Ledbetter, D. H. (2001). The human aminophospholipid-transporting ATPase gene ATP10C maps adjacent to UBE3A and exhibits similar imprinted expression. Am. J. Hum. Genet. 68, 1501-1505.
42. Hua, Z., Fatheddin, P. and Graham, T. R. (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. Hua, Z. and Graham, T. R. (2003). Requirement for Neo1p in Retrograde Transport from the Golgi Complex to the Endoplasmic Reticulum. Mol. Biol. Cell 12, 4971-4983.
44. John, K., Schreiber, S., Kubelt, J., Herrmann, A. and 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.
45. Kamp, D. and Haest, C. W. (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.
46. Kato, U., Emoto, K., Fredriksson, C., Nakamura, H., Ohta, A., Kobayashi, T., Murakami-Murofushi, K., Kobayashi, T. and 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.
47. Kean, L. S., Grant, A. M., Angeletti, C., Mahe, Y., Kuchler, K., Fuller, R. S. and Nichols, J. W. (1997). Plasma membrane translocation of fluorescent-labeled phosphatidylethanolamine is controlled by transcription regulators, PDR1 and PDR3. J. Cell Biol. 138, 255-270.
48. Kol, M. A., de Kroon, A. I., Rijkers, D. T., Killian, J. A. and de Kruijff, B. (2001). Membrane-spanning peptides induce phospholipid flop: a model for phospholipid translocation across the inner membrane of E. coli. Biochemistry 40, 10500-10506.
49. Kol, M. A., van Laak, A. N., Rijkers, D. T., Killian, J. A., de Kroon, A. I. and de Kruijff, B. (2003). Phospholipid flop induced by transmembrane peptides in model membranes is modulated by lipid composition. Biochemistry 42, 231-237.
50. Kornberg, R. D. and McConnell, H. M. (1971). Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry 10, 1111-1120.
51. Lannert, H., Bünning, C., Jeckel, D. and Wieland, F. T. (1994). Lactosylceramide is synthesized in the lumen of the Golgi apparatus. FEBS Lett. 342, 91-96.
52. Lentz, B. R. (2003). Exposure of platelet membrane phosphatidylserine regulates blood coagulation. Prog. Lipid Res. 5, 423-438.
53. Marx, U., Polakowski, T., Pomorski, T., Lang, C., Nelson, H., Nelson, N. and Herrmann, A. (1999). Rapid transbilayer movement of fluorescent phospholipid analogues in the plama membrane of endocytosis-deficient yeast cells does not require the Drs2 protein. Europ. J. Biochem. 263, 254-263.
54. Marx, U., Lassmann, G., Holzhutter, H. G., Wustner, D., Muller, P., Hohlig, A., Kubelt, J. and Herrmann, A. (2000). Rapid flip-flop of phospholipids in endoplasmic reticulum membranes studied by a stopped-flow approach. Biophys J. 78, 2628-2640.
55. Mathivet, L., Cribier, S. and Devaux, P. F. (1996). Shape change and physical properties of giant phospholipid vesicles prepared in the presence of an AC electric field. Biophys J. 70, 1112-1121.
56. Meguro, M., Kashiwagi, A., Mitsuya, K., Nakao, M., Kondo, I., Saitoh, S. and Oshimura, M. (2001). A novel maternally expressed gene, ATP10C, encodes a putative aminophospholipid translocase associated with Angelman syndrome. Nat. Genet. 28, 19-20.
57. Menon, A. K., Watkins, W. E., III and Hrafnsdóttir, S. (2000). Specific proteins are required to translocate phosphatidylcholine bidirectionally across the endoplasmic reticulum. Curr. Biol. 10, 241-252.
58. Morrot, G., Herve, P., Zachowski, A., Fellmann, P. and Devaux, P. F. (1989). Aminophospholipid translocase of human erythrocytes: phospholipid substrate specificity and effect of cholesterol. Biochemistry 28, 3456-3462.
59. Mui, B. L., Dobereiner, H. G., Madden, T. D. and Cullis, P. R. (1995). Influence of transbilayer area asymmetry on the morphology of large unilamellar vesicles. Biophys J. 69, 930-941.
60. Pérez-Victoria, F. J., Gamarro, F., Ouellette, M. and Castanys, S. (2003). Functional cloning of the miltefosine transporter: a novel P-type phospholipid translocase from Leishmania involved in drug resistance. J. Biol. Chem. 278, 49965-49971.
61. Pohl, A., Lage, H., Muller, P., Pomorski, T. and Herrmann, A. (2002). Transport of phosphatidylserine via MDR1 (multidrug resistance 1) P-glycoprotein in a human gastric carcinoma cell line. Biochem. J. 365, 259-268.
62. Pomorski, T., Herrmann, A., Muller, P., van Meer, G. and Burger, K. (1999) Protein-mediated inward translocation of phospholipids occurs in both the apical and basolateral plasma membrane domains of epithelial cells. Biochemistry 38, 142-150.
63. Pomorski, T., Lombardi, R., Riezman, H., Devaux, P. F., van Meer, G. and Holthuis, J. C. M. (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.
64. Raggers, R. J., van Helvoort, A., Evers, R. and van Meer, G. (1999). The human multidrug resistance protein MRP1 translocates sphingolipid analogs across the plasma membrane. J. Cell Sci. 112, 415-422.
65. Raggers, R. J., Pomorski, T., Holthuis, J. C. M., Kälin, N. and van Meer, G. (2000). Lipid Traffic: The ABC of transbilayer movement. Traffic 1, 226-234.
66. Raggers, R. J., Vogels, I. and van Meer, G. (2001). Multidrug-resistance P-glycoprotein (MDR1) secretes platelet-activating factor. Biochem. J. 357, 859-865.
67. Rauch, C. and Farge, E. (2000). Endocytosis switch controlled by transmembrane osmotic pressure and phospholipid number asymmetry. Biophys J. 78, 3036-3047.
68. Ruetz, S. and Gros, P. (1994). Phosphatidylcholine translocase: a physiological role for the mdr2 gene. Cell 77, 1071-1081.
69. Rush, J. S. and Waechter, C. J. (1998). Topological studies on the enzymes catalyzing the biosynthesis of Glc-P-dolichol and the triglucosyl cap of Glc3Man9GlcNAc2-P-P-dolichol in microsomal vesicles from pig brain: use of the processing glucosidases I/II as latency markers. Glycobiology 8, 1207-1213.
70. Schmitz, G., Langmann, T. and Heimerl, S. (2001). Role of ABCG1 and other ABCG family members in lipid metabolism. J. Lipid Res. 42, 1513-1520.
71. Seigneuret, M. and Devaux, P. F. (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.
72. Sheetz, M. P. and Singer, S. J. (1974). Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA 71, 4457-4461.
73. Siegmund, A., Grant, A., Angeletti, C., Malone, L., Nichols, J. W. and Rudolph, H. K. (1998). Loss of Drs2p does not abolish NBD-labeled phospholipid transfer across the plasma membrane of Saccharomyces cerevisiae. J. Biol. Chem. 273, 34399-34405.
74. Sims, P. J. and Wiedmer, T. (2001). Unraveling the mysteries of phospholipid scrambling. Thromb. Haemost. 86, 266-275.
75. Small, D. M. (2003). Role of ABC transporters in secretion of cholesterol from liver into bile. Proc. Natl. Acad. Sci. USA 100, 4-6.
76. Smeets, E. F., Comfurius, P., Bevers, E. M. and Zwaal, R. F. (1994). Calcium-induced transbilayer scrambling of fluorescent phospholipid analogs in platelets and erythrocytes. Biochim. Biophys. Acta 1195, 281-286.
77. Smit, J. J., Schinkel, A. H., Oude Elferink, R. P., Gruen, A. K., Wagenaar, E., van Deemter, L., Mol, C. A., Ottenhoff, R., van der Lugt, N. M., van Roon, M. A. et al. (1993). Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipids from bile and to liver disease. Cell 75, 451-462.
78. Smith, A. J., Timmermans-Hereijgers, J. L., Roelofsen, B., Wirtz, K. W., van Blitterswijk, W. J., Smit, J. J., Schinkel, A. H. and Borst, P. (1994). The human MDR3 P-glycoprotein promotes translocation of phosphatidylcholine through the plasma membrane of fibroblasts from transgenic mice. FEBS Lett. 354, 263-266.
79. Tang, X., Halleck, M. S., Schlegel, R. A. and Williamson, P. (1996). A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 272, 1495-1497.
80. Tannert, A., Wustner, D., Bechstein, J., Muller, P., Devaux, P. F. and Herrmann, A. (2003). Aminophospholipids have no access to the lumenal side of the biliary canaliculus - Implications for the specific lipid composition of the bile fluid. J. Biol. Chem. 278, 40631-40639.
81. Thompson, R. and Jansen, P. L. (2000). Genetic defects in hepatocanalicular transport. Semin. Liver Dis. 20, 365-372.
82. Ujhazy, P., Ortiz, D., Misra, S., Li, S., Moseley, J., Jones, H. and Arias, I. M. (2001). Familial intrahepatic cholestasis 1: studies of localization and function. Hepatology 34, 768-775.
83. van Helvoort, A., Smith, A. J., Sprong, H., Fritzsche, I., Schinkel, A. H., Borst, P. and van Meer, G. (1996). MDR1 P-glycoprotein is a lipid translocase of broad specifity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell 87, 507-517.
84. Voelker, D. R. (2003). New perspectives on the regulation of intermembrane glycerophospholipid traffic. J. Lipid Res. 44, 441-449.
85. Wang, N., Silver, D. L., Thiele, C. and Tall, A. R. (2001). ATP-binding cassette transporter A1 (ABCA1) functions as a cholesterol efflux regulatory protein. J. Biol. Chem. 276, 23742-23747.
86. Wang, N., Lan, D., Gerbod-Giannone, M., Linsel-Nitschke, P., Jehle, A. W., Chen, W., Martinez, L. O. and Tall, A. R. (2003). ATP-binding cassette transporter A7 (ABCA7) binds apolipoprotein A-I and mediates cellular phospholipid but not cholesterol efflux. J. Biol. Chem. 278, 42906-42912.
87. Williamson, P., Bevers, E. M., Smeets, E. F., Comfurius, P., Schlegel, R. A. and Zwaal, R. F. (1995). Continuous analysis of the mechanism of activated transbilayer lipid movement in platelets. Biochemistry 34, 10448-10455.
88. Yu, L., Hammer, R. E., Li-Hawkins, J., von Bergmann, K., Lutjohann, D., Cohen, J. C. and Hobbs, H. H. (2002). Disruption of Abcg5 and Abcg8 in mice reveals their crucial role in biliary cholesterol secretion. Proc. Natl. Acad. Sci. USA 99, 16237-16242.
89. Zachowski, A. (1993). Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294, 1-14.
90. Zha, X., Genest, J., Jr and McPherson, R. (2001). Endocytosis is enhanced in Tangier fibroblasts: possible role of ATP-binding cassette protein A1 in endosomal vesicular transport. J. Biol. Chem. 276, 39476-39483.
91. Zhou, Q., Zhao, J., Wiedmer, T. and Sims P. J. (2002). Normal hemostasis but defective hematopoietic response to growth factors in mice deficient in phospholipid scramblase 1. Blood 99, 4030-4038.