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Abstract

The human red blood cell membrane consists of lipids (41%), proteins (52%), and carbohydrates (7%) (Dodge et al. 1963). Membrane lipids (5.2 mg/ml packed cells or 5.2·10-13 g/cell) can be divided into three classes: neutral lipids (25.2%), phospholipids (62.7%) and glycosphingolipids (about 12%). Neutral lipids of human erythrocytes represent cholesterol almost exclusively (Nelson 1972). The ratio of cholesterol to phospholipid is about 0.8 (Broekhuyse 1974). Phospholipids (4.3 umol/mlcells) consist of sphingomyelin (SM, 26%) and glycerophospho-lipids. Glycerophospholipids can be divided into 3 main fractions — phosphatidylcholine (PC, 30%), phosphatidylethanolamine (PE, 27%), and phosphatidylserine (PS, 13%) as well as several minor fractions — phosphatidic acid, lyso-PC, phosphati-dylinositol (PI), and PI mono and diphosphates (Nelson 1972; Broekhuyse 1974). The fatty acid pattern differs among the phospholipid classes and according to the position of the glycerol backbone. PE and PS contain higher fractions of polyunsaturated fatty acids than PC (Gercken et al. 1972). Saturated fatty acids with 16 to 24 carbon atoms are preferentially located at the 1 position of glycerol whereas unsaturated fatty acids with up to 6 double bonds are at the 2 position (Van Deenen 1969). In case of PE, species with vinyl ether bonds at the 1 position of glycerol (plasmalogens) make up the majority (Nelson 1972). SM mainly contains long-chain saturated or monounsaturated fatty acids with up to 24 C atoms (Gercken et al. 1972).

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References

  • Abumrad N, Harmon C, Ibrahimi A (1998) Membrane transport of long-chain fatty acids: evidence for a facilitated process. J Lipid Res 39:2309–2318

    Google Scholar 

  • Abumrad N, Coburn C, Ibrahimi A (1999) Membrane proteins implicated in long-chain fatty acid uptake by mammalian cells: CD36, FATP and FABPm. Biochim Biophys Acta 1441:4–13

    Article  Google Scholar 

  • Andrick C, Bröring K, Deuticke B, Haest CWM (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

    Article  Google Scholar 

  • Basse F, Sainte-Marie J, Maurin L, Bienvenue A (1992) Effect of benzylalcohol on phospholipid flip-flop in the human erythrocyte membrane. Eur J Biochem 205:155–162

    Article  Google Scholar 

  • Basse F, Stout JG, Sims PJ, Wiedmer TW (1996) Isolation of an erythrocyte membrane protein that mediates Ca2+-dependent transbilayer movement of phospholipid. J Biol Chem 271:17205–17210

    Article  Google Scholar 

  • Beleznay Z, Zachowski A, Devaux PF, Ott P (1997) Characterization of the correlation between ATP-dependent aminophospholipid translocation and Mg2+-ATPase activity in red blood cell membranes. Eur J Biochem 243:58–65

    Article  Google Scholar 

  • Bergmann WL, Dressler V, Haest CWM, Deuticke B (1984a) Reorientation rates and asymmetry of distribution of lysophospholipids between the inner and outer leaflet of the erythrocyte membrane. Biochim Biophys Acta 772:328–336

    Article  Google Scholar 

  • Bergmann WL, Dressier V, Haest CWM, Deuticke B (1984b) Cross-linking of SH-groups in the erythrocyte membrane enhances transbilayer reorientation of phospholipids. Biochim Biophys Acta 769:390–398

    Article  Google Scholar 

  • Bevers EM, Comfurius P, Dekkers DWC, Harmsma M, Zwaal RFA (1998) Transmembrane phospholipid distribution in blood cells: control mechanisms and pathological significance. J Biol Chem 379:973–986

    Google Scholar 

  • Bevers EM, Comfurius P, Dekkers DWC, Zwaal RFA (1999) Lipid translocation across the plasma membrane of mammalian cells. Biochim Biophys Acta 1439:317–330

    Article  Google Scholar 

  • Bitbol M, Devaux PF (1988) Measurement of outward translocation of phospholipids across human erythrocyte membrane. Proc Natl Acad Sci 85:6783–6787

    Article  ADS  Google Scholar 

  • Blumenfeld N, Zachowski A, Galacteros F, Beuzard Y, Devaux PF (1991) Transmembrane mobility of phospholipids in sickle erythrocytes: Effect of deoxygenation on diffusion and asymmetry. Blood 77:849–854

    Google Scholar 

  • Bojesen IN and Bojesen E (1999) Sheep erythrocyte membrane binding and transfer of long-chain fatty acids. J Membrane Biol 171:141–149

    Article  Google Scholar 

  • Bonomini M, Sirolli V, Settefrati N, Dottori S, Di Liberato L, Arduini A (1999) Increased erythrocyte phosphatidylserine exposure in chronic renal failure. J Am Soc Nephrol 10:1982–1990

    Google Scholar 

  • Borst P, Evers R, Kool M, Wijnholds J (1999) The multidrug resistance protein family. Biochim Biophys Acta 1461:347–357

    Article  Google Scholar 

  • Brasaemle DL, Robertson AD, Attie AD (1988) Transbilayer movement of cholesterol in the human erythrocyte membrane. J Lipid Res 29:481–489

    Google Scholar 

  • Bratosin D, Matzurier J, Tissier JP, Estaquier J, Huart JJ, Ameisen JC, Aminoff D, Montreuil J (1998) Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages. A review. Biochimie 80:173–195

    Article  Google Scholar 

  • Bretcher MS (1972) Asymmetrical lipid bilayer structure for biological membranes. Nature New Biology 236:11–12

    Article  Google Scholar 

  • Broekhuyse RM (1974) Improved lipid extraction of erythrocytes. Clin Chim Acta 51:341–343

    Article  Google Scholar 

  • Bröring K, Haest CWM, Deuticke B (1989) Translocation of oleic acid across the erythrocyte membrane. Evidence for a fast process. Biochim Biophys Acta 986:321–331

    Article  Google Scholar 

  • Bucki R, Giraud F, Sulpice JC (2000) Phosphatidylinositol 4,5-bisphosphate domain inducers promote phospholipid transverse redistribution in biological membranes. Biochemistry 39:5838–5844

    Article  Google Scholar 

  • Cabantchik ZI, Greger R (1992) Chemical probes for anion transporters of mammalian cell membranes. Am J Physiol 262:C803–C827

    Google Scholar 

  • Cabrai DJ, Small DM, Lilly HS, Hamilton JA (1987) Transbilayer movement of bile acids in model membranes. Biochemistry 26:1801–1804

    Article  Google Scholar 

  • Cines DB, Pollack ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, Pober JS, Wick TM, Konkle BA, Schwartz BS, Barnathan ES, McCrae KR, Hug BA, Schmidt AM, Stern DM (1998) Endothelial cells in physiology and in the pathology of vascular disorders. Blood 91:3527–3561

    Google Scholar 

  • Classen J, Haest CWM, Tournois H, Deuticke B (1987) Gramicidin-induced enhancement of transbilayer reorientation of lipids in the erythrocyte membrane. Biochemistry 26:6604–6612

    Article  Google Scholar 

  • Classen J, Deuticke B, Haest CWM (1989) Nonmediated flip-flop of phospholipid analogues in the erythrocyte membrane as probed by palmitoylcarnitine: Basic properties and influence of membrane modification. J Membrane Biol 111:169–178

    Article  Google Scholar 

  • Connor J, Schroit AJ (1988) Transbilayer movement of phosphatidylserine in erythrocytes: Inhibition of transport and preferential labeling of a 31 000-Dalton protein by sulfhy-dryl reactive reagents. Biochemistry 27:848–851

    Article  Google Scholar 

  • Connor J, Pak CH, Zwaal RFA, Schroit AJ (1992) Bidirectional transbilayer movement of phospholipid analogs in human red cells. J Biol Chem 267:19412–19417

    Google Scholar 

  • Connor J, Pak CC, Schroit AJ (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

    Google Scholar 

  • Czarnecka H, Yokoyama S (1996) Regulation of cellular efflux by lecithin:cholesterol acyl-transferase reaction through nonspecific lipid exchange. J Biol Chem 271:2023–2028

    Article  Google Scholar 

  • Daleke DL, Huestis WH (1985) Incorporation and translocation of aminophospholipids in human erythrocytes. Biochemistry 24:5406–5416

    Article  Google Scholar 

  • Daleke DL, Lyles JV (2000) Identification and purification of aminophospholipid flippases. Biochim Biophys Acta 1486:108–127

    Article  Google Scholar 

  • De Jong K, Larkin SK, Styles LA, Bookchin RM, Kuypers FA (2001) Characterization of the phosphatidylserine-exposing subpopulation of sickle cells. Blood 98:860–867

    Article  Google Scholar 

  • Dekkers DWC, Comfurius P, Schroit AJ, Bevers EM, Zwaal RFA (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

    Article  Google Scholar 

  • Dekkers DWC, Comfurius P, Van Gool RGJ, Bevers EM, Zwaal RFA (2000) Multidrug resistance protein 1 regulates lipid asymmetry in erythrocyte membranes. Biochem J 350:531–535

    Article  Google Scholar 

  • Deuticke B, Heller KB, Haest CWM (1987) Progressive oxidative membrane damage in erythrocytes after pulse treatment with t-butylhydroperoxide. Biochim Biophys Acta 899:113–124

    Article  Google Scholar 

  • Deuticke B, Henseleit U, Haest CWM, Heller KB, Dubbelman TMAR (1989) Enhancement of transbilayer mobility of a membrane lipid probe accompanies formation of membrane leaks during photodynamic treatment of erythrocytes. Biochim Biophys Acta 982:53–61

    Article  Google Scholar 

  • Deuticke B, Grebe R, Haest CWM (1990) Action of drugs on the erythrocyte membrane. In: Harris HR (ed) Blood cell biochemistry. Plenum Press, New York, pp 475–529

    Google Scholar 

  • Deuticke B, Klonk S, Haest CWM (1992) The red cell membrane in health and disease. Erythrocyte membrane barrier function: Role of bilayer polarity and skeletal proteins. Biochem Soc Trans 20:769–773

    Google Scholar 

  • Devaux PF (1991) Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30:1163–1173

    Article  Google Scholar 

  • Ding J, Wu Z, Crider BP, Ma Y, Li X, Slaughter C, Gong L, Xie XS (2000) Identification and functional expression of four isoforms of ATPase II, the putative aminophospholipid translocase. J Biol Chem 275:23378–23386

    Article  Google Scholar 

  • Dodge JT, Mitchell C, Hanahan D (1963) The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes. Arch Biochem Biophys 100:119–130

    Article  Google Scholar 

  • Dolis D, Moreau C, Zachowski A, Devaux PF (1997) Aminophospholipid translocase and proteins involved in transmembrane traffic. Biophys Chem 68:221–231

    Article  Google Scholar 

  • Dressler V, Schwister K, Haest CWM, Deuticke B (1983) Dielectric breakdown of the erythrocyte membrane enhances transbilayer mobility of phospholipids. Biochim Bio-phys Acta 732:304–307

    Article  Google Scholar 

  • Eastman SJ, Hope MJ, Cullis PR (1991) Transbilayer transport of phosphatidic acid in response to transmembrane pH gradients. Biochemistry 30:1740–1745

    Article  Google Scholar 

  • Fadok VA, Bratton DL, Frasch SC, Warner ML, Henson PM (1998) The role of phosphati-dylserine in recognition of apoptotic cells by phagocytes. Cell Death Differ 5:551–562

    Article  Google Scholar 

  • Farquahar JW, Ahrens EH Jr (1963) Effects of dietary fats on human erythrocyte fatty acid patterns. J Clin Invest 42:675–685

    Article  Google Scholar 

  • Ferrell JE, Lee KJ, Huestis WH (1985) Membrane bilayer balance and erythrocyte shape: A quantitative assessment. Biochemistry 24:2849–2857

    Article  Google Scholar 

  • Florin-Christensen J, Suarez CE, Florin-Christensen M, Wainszelbaum M, Brown WC, McElwain TF, Palmer GH (2001) A unique phospholipid organization in bovine erythrocyte membranes. Proc Natl Acad Sci USA 98:7736–7741

    Article  ADS  Google Scholar 

  • Franck PFH, Op den Kamp JAF, Lubin B, Berendsen W, Joosten P, Briet E, Van Deenen LLM, Roelofsen B (1985) Abnormal transbilayer mobility of phosphatidylcholine in hereditary pyropoikilocytosis reflects the increased heat sensitivity of membrane skeleton. Biochim Biophys Acta 815:259–267

    Article  Google Scholar 

  • Frasch SC, Henson PM, Kailey JM, Richter DA, Janes MS, Fadok VA, Bratton DL (2000) Regulation of phospholipid scramblase activity during apoptosis and cell activation by protein kinase CA. J Biol Chem 275:23065–23073

    Article  Google Scholar 

  • Fujii T, Tamura A, Yamane T (1985) Trans-bilayer movement of added phosphatidylcholine and lysophosphatidylcholine species with various acyl chain lengths in plasma membrane of intact human erythrocytes. J Biochem 98:1221–1227

    Google Scholar 

  • Gahmberg CG, Hakomori S (1973) External labelling of cell surface galactose and galacto-seamine in glycolipid and glycoprotein of human erythrocytes. J Biol Chem 248:4311–4317

    Google Scholar 

  • Galbiati F, Razani B, Lisanti MP (2001) Emerging themes in lipid rafts and caveolae. Cell 106:403–411

    Article  Google Scholar 

  • Ganong BR, Bell RM (1984) Transmembrane movement of phosphatidylglycerol and dia-cylglycerol sulfhydryl analogues. Biochemistry 23:4977–4983

    Article  Google Scholar 

  • Gascard P, Tran D, Sauvage M, Sulpice JC, Fukami K, Takenawa T, Claret M, Giraud F (1991) Asymmetric distribution of phosphoinositides and phophatidic acid in the human erythrocyte membrane. Biochim Biophys Acta 1069:27–36

    Article  Google Scholar 

  • Geldwerth D, Cherif-Zahar B, Helley D, Gane P, Freyssinet JM, Colin Y, Devaux PF, Car-tron JP (1997) Phosphatidylserine exposure and aminophospholipid translocase activity in Rh-deficient erythrocytes. Mol Membr Biol 14:125–132

    Article  Google Scholar 

  • Gercken G, Tiling T, Brockmann U, Schröter W (1972) Fatty acid composition of phospholipids in erythrocytes of adults, normal newborn infants and neonates with Rh erythroblastosis. Pediat Res 6:487–494

    Article  Google Scholar 

  • Gordesky SE, Marinetti GV (1973) The asymmetric arrangement of phospholipids in the human erythrocyte membrane. Biochem Biophys Res Commun 50:1027–1031

    Article  Google Scholar 

  • Haest CWM, Andrick C (1989) Newly synthetized phosphatidylcholine is very rapidly translocated from the inner to the outer membrane leaflet in human erythrocytes. Stu-dia Biophysica 134:77–82

    Google Scholar 

  • Haest CWM, Plasa G, Kamp D, Deuticke B (1978) Spectrin as a stabilizer of the phospholipid asymmetry in the human erythrocyte membrane. Biochim Biophys Acta 509:21–32

    Article  Google Scholar 

  • Haest CWM, Kunze I, Classen J, Schneider E, Deuticke B (1986) Flip-flop rates and origin of phospholipid asymmetry in the native and modified red cell membrane can be studied by phospholipid analogues. In: Klein R, Schmitz B (eds) Topics in lipid research. The Royal Society of Chemistry, Burlington House, London, pp 235–242

    Google Scholar 

  • Haest CWM, Kamp D, Deuticke B (1997) Transbilayer reorientation of phospholipid probes in the human erythrocyte membrane. Lessons from studies on electroporated and resealed cells. Biochim Biophys Acta 1325:17–33

    Article  Google Scholar 

  • Haldar K, De Amorim AF, Cross GA (1989) Transport of fluorescent phospholipid analogues from the erythrocyte membrane to the parasite in Plasmodium falciparum-infected cells. J Cell Biol 108:2183–2192

    Article  Google Scholar 

  • Hall MP, Huestis WH (1994) Phosphatidylserine headgroup diastereomers translocate equivalently across human erythrocyte membranes. Biochim Biophys Acta 1190:243–247

    Article  Google Scholar 

  • Halleck MS, Lawler JF Jr, Blackshaw S, Gao L, Nagarajan P, Hacker C, Scott P, Newman JT, Nakanishi Y, Ando H, Weinstock D, Williamson P, Schlegel R (1999) Differential expression of putative transbilayer amphipath transporters. Physiol Genomics 1:139–150

    Google Scholar 

  • Hamon Y, Broccardo C, Chambenoit O, Luciani MF, Toti F, Chaslin S, Freyssinet JM, Devaux PF, McNeish J, Marguet D, Chimini G (2000) ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nature Cell Biol 2:399–406

    Article  Google Scholar 

  • Herrmann A, Devaux PF (1990) Alteration of the aminophospholipid translocase activity during in vivo and artificial aging of human erythrocytes. Biochim Biophys Acta 1027:41–46

    Article  Google Scholar 

  • Hipfner DR, Deeley RG, Cole SPC (1999) Structural, mechanistic and clinical aspects of MRP1. Biochim Biophys Acta 1461:359–376

    Article  Google Scholar 

  • Homan R, Pownall HJ (1988) Transbilayer diffusion of phospholipids: dependence on head group structure and acyl chain length. Biochim Biophys Acta 938:155–166

    Article  Google Scholar 

  • Hooijberg JH, Pinedo HM, Vrasdonk C, Priebe W, Lankelma J, Broxterman HJ (2000) The effect of glutathione on the ATPase activity of MRP1 in its natural membranes. FEBS Letters 469:47–51

    Article  Google Scholar 

  • Jain SK (1985) In Vivo externalization of phosphatidylserine and phosphatidylethanolamine in the membrane bilayer and hypercoagulability by the lipid peroxidation of erythrocytes in rats. J Clin Invest 76:281–286

    Article  Google Scholar 

  • Kamp D, Haest CWM (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

    Article  Google Scholar 

  • Kamp D, Sieberg T, Haest CWM (2001) Inhibition and stimulation of phospholipid scrambling activity. Consequences for lipid asymmetry, echinocytosis and microvesiculation of erythrocytes. Biochemistry 40:9438–9446

    Article  Google Scholar 

  • Kavecansky J, Joiner CH, Schroeder F (1994) Erythrocyte membrane lateral sterol domains: a dehydroergosterol fluorescence polarization study. Biochemistry 33:2880–2890

    Article  Google Scholar 

  • Kirby CJ, Green C (1977) Transmembrane migration (‘Flip-Flop’) of cholesterol in erythrocyte membranes. Biochem J 168:575–577

    Google Scholar 

  • Kleinfeld AM (2000) Lipid phase fatty acid flip-flop, is it fast enough for cellular transport? J Membrane Biol 175:79–86

    Article  Google Scholar 

  • Kleinfeld AM, Chu P, Romero C (1997) Transport of long-chain native fatty acids across lipid bilayer membranes indicates that transbilayer flip-flop is rate limiting. Biochemistry 36:14146–14158

    Article  Google Scholar 

  • Kleinfeld AM, Storms S, Watts M (1998) Transport of long-chain fatty acids across human erythrocyte ghost membranes. Biochemistry 37:8011–8019

    Article  Google Scholar 

  • Kleinhorst A, Oslender A, Haest CWM, Deuticke B (1998) Band 3-mediated flip-flop and phosphatase-catalyzed cleavage of a long-chain alkyl phosphate anion in the human erythrocyte membrane. J Membrane Biol 165:111–124

    Article  Google Scholar 

  • König J, Nies AT, Cui Y, Leier I, Keppler D (1999) Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim Biophys Acta 1461:377–394

    Article  Google Scholar 

  • Koefoed P, Brahm J (1994) The permeability of the human red cell membrane to steroid sex hormones. Biochim Biophys Acta 1195:55–62

    Article  Google Scholar 

  • Kornberg RD, McConnell HM (1971) Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry 14:2809–2816

    Google Scholar 

  • Krupka RM (1989) Role of substrate binding forces in exchange-only transport systems: II. Implications for the mechanism of the anion exchanger of red cells. J Membrane Biol 109:159–171

    Article  Google Scholar 

  • Kuypers FA, Van Linde-Sibenius-Trip M, Roelofsen B, Tanner MJA, Anstee DJ, Op den Kamp JAF (1984) Rhnull human erythrocytes have an abnormal membrane phospholipid organization. Biochem J 221:931–934

    Google Scholar 

  • Kuypers FA, Van Linde-Sibenius-Trip M, Roelofsen B, Op den Kamp JAF, Tanner MJA, Anstee DJ (1985) The phospholipid organisation in the membranes of McLeod and Leach phenotype erythrocytes. FEBS Letters 184:20–24

    Article  Google Scholar 

  • Kuypers FA, Yuan J, Lewis RA, Snyder LM, Kiefer CR, Bunyaratvej A, Fucharoen S, Ma L, Styles L, De Jong K, Schrier SL (1998) Membrane phospholipid asymmetry in human thalassemia. Blood 91:3044–3051

    Google Scholar 

  • Lange Y (1992) Tracking cell cholesterol with cholesterol oxidase. J Lipid Res 33:315–321

    Google Scholar 

  • Lange Y, Cohen CM, Poznansky MJ (1977) Transmembrane movement of cholesterol in human erythrocytes. Proc Natl Acad Sci 74:1538–1542

    Article  ADS  Google Scholar 

  • Lange Y, Dolde J, Steck TL (1981) The rate of transmembrane movement of cholesterol in the human erythrocyte membrane. J Biol Chem 256:5321–5323

    Google Scholar 

  • Le Maire M, Moller JV, Champeil P (1987) Binding of a nonionic detergent to membranes: Flip-flop rate and location on the bilayer. Biochemistry 26:4803–4810

    Article  Google Scholar 

  • Lubin B, Chiu D, Bastacky J, Roelofsen B, Van Deenen LLM (1981) Abnormalities in membrane phospholipid organization in sickled erythrocytes. J Clin Invest 67:1643–1649

    Article  Google Scholar 

  • Manodori AB, Barabino GA, Lubin BH, Kuypers FA (2000) Adherence of phosphatidyl-serine-exposing erythrocytes to endothelial matrix thrombospondin. Blood 95:1293–1300

    Google Scholar 

  • Marsh D, Horvath LI (1998) Structure, dynamics and composition of the lipid-protein interface. Perspectives from spin-labelling. Biochim Biophys Acta 1376:267–296

    Article  Google Scholar 

  • Martin OC, Pagano RE (1987) Transbilayer movement of fluorescent analogs of phosphat-diylserine and phosphatidylethanolamine at the plasma membrane of cultured cells. J Biol Chem 262:5890–5898

    Google Scholar 

  • Middelkoop E, Lubin BH, Op den Kamp JAF, Roelofsen B (1986) Flip-flop rates of individual molecular species of phosphatidylcholine in the human red cell membrane. Biochim Biophys Acta 855:421–424

    Article  Google Scholar 

  • Mohandas N, Wyatt J, Mel SF, Rossi ME, Shohet SB (1982) Lipid translocation across the human erythrocyte membrane. Regulatory factors. J Biol Chem 257:6537–6543

    Google Scholar 

  • Moll GN, Vial HJ, Ancelin ML, Roelofsen B, Comfurius P, Slotboom AJ, Zwaal RF, Op den Kamp JA, Van Deenen LL (1990) Phospholipid asymmetry in the plasma membrane of malaria infected cells. Biochem Cell Biol 68:579–585

    Article  Google Scholar 

  • Moore DJ, Giosioso S, Sills RH, Mendelsohn R (1999) Some relationships between membrane phospholipid domains, conformational order, and cell shape in intact human erythrocytes. Biochim Biophys Acta 1415:342–348

    Article  Google Scholar 

  • Müller P, Zachowski A, Beuzard Y, Devaux PF (1993) Transmembrane mobility and distribution of phospholipids in the membrane of mouse β-thalassemic red blood cells. Biochim Biophys Acta 1151:7–12

    Article  Google Scholar 

  • Nelson GJ (1972) Lipid composition and metabolism of erythrocytes. In: Nelson GJ (ed) Blood lipids and lipoproteins: Quantitation, composition, and metabolism. Wiley-Interscience, New York, pp 317–386

    Google Scholar 

  • Nijhof W, Van der Schaft PH, Wierenga PK, Roelofsen B, Op den Kamp JAF, Van Deenen LLM (1986) The transbilayer distribution of phosphatidylethanolamine in erythroid plasma membranes during erythropoiesis. Biochim Biophys Acta 862:273–277

    Article  Google Scholar 

  • Op den Kamp JAF (1979) Lipid asymmetry in membranes. Annu Rev Biochem 48:47–71

    Article  Google Scholar 

  • Oram JF (2000) Tangier disease and ABCA1. Biochim Biophys Acta 1529:321–330

    Article  Google Scholar 

  • Ortwein R, Oslender-Kohnen A, Deuticke B (1994) Band 3, the anion exchanger of the erythrocyte membrane, is also a flippase. Biochim Biophys Acta 1191:317–323

    Article  Google Scholar 

  • Pantaler E, Kamp D, Haest CWM (2000) Acceleration of flip-flop in the erythrocyte membrane by detergents differing in polar head group and alkyl chain length. Biochim Biophys Acta 1509:397–408

    Article  Google Scholar 

  • Peters R (1988) Lateral mobility of proteins and lipids in the red cell membrane and the activation of adenylate cyclase by β-adrenergic receptors. FEBS Letters 234:1–7

    Article  Google Scholar 

  • Pomorski T, Herrmann A, Zachowski A, Devaux PF, Müller P (1994) Rapid determination of the transbilayer distribution of NBD-phospholipids in erythrocyte membranes by di-thionite. Mol Membr Biol 11:39–44

    Article  Google Scholar 

  • Qian YM, Song WC, Cui H, Cole SP, Deeley RG (2001) Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J Biol Chem 276:6404–6411

    Article  Google Scholar 

  • Rao GA, Siler K, Larkin EC (1979) Diet-induced alterations in the discoid shape and phospholipid compositions of rat erythrocytes. Lipids 14:30–38

    Article  Google Scholar 

  • Rawyler A, Van der Schaft PH, Roelofsen B, Op den Kamp JAF (1985) Phospholipid localization in the plasma membrane of Friend erythroleukemic cells and mouse erythrocytes. Biochemistry 24:1777–1783

    Article  Google Scholar 

  • Renooij W, Van Golde LMG, Zwaal RFA, Roelofsen B, Van Deenen LLM (1974) Preferential incorporation of fatty acids at the inside of human erythrocyte membranes. Biochim Biophys Acta 363:287–292

    Article  Google Scholar 

  • Renooij W, Van Golde LMG, Zwaal RFA, Van Deenen LLM (1976) Topological asymmetry of phospholipid metabolism in rat erythrocyte membranes. Eur J Biochem 61:53–58

    Article  Google Scholar 

  • Rosso J, Zachowski A, Devaux PF (1988) Influence of chlorpromazine on the transverse mobility of phospholipids in the human erythrocyte membrane: relation to shape changes. Biochim Biophys Acta 942:271–279

    Article  Google Scholar 

  • Salzer U, Prohaska R (2001) Stomatin, flotillin-1, and flotillin-2 are major integral proteins of erythrocyte lipid rafts. Blood 97:1141–1143

    Article  Google Scholar 

  • Savili J, Fadok V (2000) Corpse clearance defines the meaning of cell death. Nature 407:784–788

    Article  ADS  Google Scholar 

  • Schneider E, Haest CWM, Deuticke B (1986a) Transbilayer reorientation of platelet-activating factor in the erythrocyte membrane. FEBS Letters 198:311–314

    Article  Google Scholar 

  • Schneider E, Haest CWM, Plasa G, Deuticke B (1986b) Bacterial toxins, amphotericin B and local anesthetics enhance transbilayer mobility of phospholipids in erythrocyte membranes. Consequences for phospholipid asymmetry. Biochim Biophys Acta 855:325–336

    Article  Google Scholar 

  • Schroeder F, Nemecz G, Wood WG, Joiner C, Morrot G, Ayaut-Jarrier M, Devaux PF (1991) Transmembrane distribution of sterol in human erythrocyte. Biochim Biophys Acta 1066:183–192

    Article  Google Scholar 

  • Schwichtenhövel C, Deuticke B, Haest CWM (1992) Alcohols produce reversible and irreversible acceleration of phospholipid flip-flop in the human erythrocyte membrane. Biochim Biophys Acta 1111:35–44

    Article  Google Scholar 

  • 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 USA 81:3751–3755

    Article  ADS  Google Scholar 

  • Serra MV, Kamp D, Haest CWM (1996) Pathways for flip-flop of mono- and di-anionic phospholipids in the erythrocyte membrane. Biochim Biophys Acta 1282:263–273

    Article  Google Scholar 

  • Sherman IW, Prudhomme J, Tait JT (1997) Altered membrane phospholipid asymmetry in Plasmodium falciparum-intected erythrocytes. Parasitology Today 13:242–243

    Article  Google Scholar 

  • Shohet SB (1972) Hemolysis and changes in erythrocyte membrane lipids. New Engl J Med 286:577–583

    Article  Google Scholar 

  • Sims PJ, Wiedmer T (2001) Unraveling the mysteries of phospholipid scrambling. Thromb Haemost 86:266–275

    Google Scholar 

  • Somerharju P, Virtanen JA, Cheng KH (1999) Lateral organisation of membrane lipids. The superlattice model. Biochim Biophys Acta 1440:32–48

    Article  Google Scholar 

  • Stout JG, Zhou Q, Wiedmer T, Sims PJ (1998) Change in conformation of plasma membrane phospholipid scramblase induced by occupancy of its Ca2+ binding site. Biochemistry 37:14860–14866

    Article  Google Scholar 

  • Subsczynski WK, Wisniewska A, Yin JJ, Hyde JS, Kusumi A (1994) Hydrophobic barriers of lipid bilayer membranes formed by reduction of water penetration by alkyl chain unsaturation and cholesterol. Biochemistry 33:7670–7681

    Article  Google Scholar 

  • Sun J, Zhao J, Schwartz MA, Wang JYJ, Wiedmer T (2001) C-Abl tyrosine kinase binds and phosphorylates phospholipid scramblase 1. J Biol Chem 276:28984–28990

    Article  Google Scholar 

  • Tait JF, Gibson D (1994) Measurement of membrane phospholipid asymmetry in normal and sickle-cell erythrocytes by means of annexin V binding. J Lab Clin Med 123:741–748

    Google Scholar 

  • Tang X, Halleck MS, Schlegel RA, Williamson P (1996) A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 272:1495–1497

    Article  ADS  Google Scholar 

  • Van Deenen LLM (1969) Membrane lipids and lipophilic proteins. In: Tosteson DC (ed) The molecular basis of membrane function. Printice-Hall, Englewood Cliffs, pp 47–78

    Google Scholar 

  • Van der Schaft PH, Roelofsen B, Op den Kamp JAF, Van Deenen LLM (1987a) Phospholipid asymmetry during erythropoiesis. A study on Friend erythroleukemic cells and mouse reticulocytes. Biochim Biophys Acta 900:103–115

    Article  Google Scholar 

  • Van der Schaft PH, Beaumelle B, Vial H, Roelofsen B, Op den Kamp JAF, Van Deenen LLM (1987b) Phospholipid organization in monkey erythrocytes upon Plasmodium knowlesi infection. Biochim Biophys Acta 901:1–14

    Article  Google Scholar 

  • 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 freeze-etch electron microscopy. Biochim Biophys Acta 323:178–193

    Article  Google Scholar 

  • Vondenhof A (1993) Mechanismen der Phospholipid-Translokation in der Erythrozyten-membran. Ph.D. thesis, RWTH Aachen

    Google Scholar 

  • Vondenhof A, Oslender A, Deuticke B, Haest CWM (1994) Band 3, an accidental flippase for anionic phospholipids. Biochemistry 33:4517–4520

    Article  Google Scholar 

  • Voswinkel St, Haest CWM, Deuticke B (2001) Complex effects of papain on function and inhibitor sensitivity of the red cell anion exchanger AE1 suggest the presence of different transport subsites. J Membrane Biol 179:205–221

    Article  Google Scholar 

  • Wali RK, Jaffe S, Kumar D, Kaira VK (1988) Alterations in organization of phospholipids in erythrocytes as factor in adherence to endothelial cells in diabetic mellitus. Diabetes 37:104–111

    Article  Google Scholar 

  • Welti R, Glaser M (1994) Lipid domains in model and biological membranes. Chem Phys Lipids 73:121–137

    Article  Google Scholar 

  • Wiedmer T, Zhou Q, Kwoh DY, Sims P (2000) Identification of three new members of the phospholipid scramblase gene family. Biochim Biophys Acta 1467:244–253

    Article  Google Scholar 

  • Woon LA, Holland JW, Kable EP, Roufagalis BD (1999) Ca2+ sensitivity of phospholipid scrambling in human red cell ghosts. Cell Calcium 25:313–320

    Article  Google Scholar 

  • Yang L, Andrews DA, Low PS (2000) Lysophosphatidic acid opens Ca++ channels in human erythrocytes. Blood 95:2420–2425

    Google Scholar 

  • Yeagle P (1987) The membranes of cells. Academic Press, Orlando

    Google Scholar 

  • Zachowski A (1993) Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem J 294:1–14

    Google Scholar 

  • Zachowski A, Devaux PF (1990) Transmembrane movements of lipids. Experientia 46:644–656

    Article  Google Scholar 

  • Zachowski A, Favre E, Cribier S, Herve P, Devaux PF (1986) Outside-inside translocation of aminophospholipids in the human erythrocyte membrane is mediated by a specific enzyme. Biochemistry 25:2585–2590

    Article  Google Scholar 

  • Zhou Q, Zhao J, Stout JG, Luhm RA, Wiedmer T, Sims PJ (1997) Molecular cloning of human plasma membrane phospholipid scramblase. J Biol Chem 272:18240–18244

    Article  Google Scholar 

  • Zhao J, Zhou Q, Wiedmer T, Sims PJ (1998) Palmitoylation of phospholipid scramblase is required for normal function in promoting Ca2+-activated transbilayer movement of membrane phospholipids. Biochemistry 37:6361–6366

    Article  Google Scholar 

  • Zuvic-Butorac M, Müller P, Pomorski T, Libera J, Herrmann A, Schara M (1999) Lipid domains in the exoplasmic and cytoplasmic leaflet of the human erythrocyte membrane: a spin label approach. Eur Biophys J 28:302–311

    Article  Google Scholar 

  • Zwaal RFA, Flückinger R, Moser S, Zahler P (1974) Lecithinase activities at the external surface of ruminant erythrocyte membranes. Biochim Biophys Acta 373:416–424

    Article  Google Scholar 

  • Zwaal RFA, Schroit AJ (1997) Pathophysiological implications of membrane phospholipid asymmetry in blood cells. Blood 89:1121–1132

    Google Scholar 

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Haest, C.W.M. (2003). Distribution and Movement of Membrane Lipids. In: Bernhardt, I., Ellory, J.C. (eds) Red Cell Membrane Transport in Health and Disease. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-05181-8_1

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