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Transmembrane movements of lipids

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Summary

Membranes allow the rapid passage of uncharged lipids. Phospholipids on the other hand diffuse very slowly from one monolayer to another with a half-time of several hours. This slow spontaneous movement in a pure lipid bilayer can be selectively modulated in biological membranes by intrinsic proteins. In microsomes, and probably in bacterial membranes, non-specific phospholipid flippases allow the rapid redistribution of newly synthesized phospholipids. In eukaryotic plasma membranes, aminophospholipid translocase selectively pumps phosphatidylserine (PS) and phosphatidylethanolamine (PE) from the outer to the inner leaflet and establishes a permanent lipid asymmetry. The discovery of an aminophospholipid translocase in chromaffin granules proves that eukaryotic organelles may also contain lipid translocators.

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Literatur

  1. Allan, D., Thomas, P., and Michell, R. H., Rapid transbilayer diffusion of 1,2-diacylglycerol and its relevance to control of membrane curvature. Nature276 (1978) 2888–2890.

    Article  Google Scholar 

  2. Allan, D., and Quinn, P., Membrane phospholipid asymmetry in Semliki Forest virus grown in BHK cells. Biochim. biophys. Acta987 (1989) 199–204.

    Article  CAS  Google Scholar 

  3. Backer, J. M., and Dawidowicz, E. A., The rapid transmembrane movement of cholesterol in small unilamellar vesicles. Biochim. biophys. Acta551 (1979) 260–270.

    Article  CAS  PubMed  Google Scholar 

  4. Backer, J. M., and Dawidowicz, E. A., Transmembrane movement of cholesterol in small unilamellar vesicles detected by cholesterol oxidase. J. biol. Chem.256 (1981) 586–588.

    Article  CAS  PubMed  Google Scholar 

  5. Backer, J. M., and Dawidowicz, E. A., Reconstitution of a phospholipid flippase from rat liver microsomes. Nature327 (1987) 341–343.

    Article  PubMed  Google Scholar 

  6. Barsukov, L. I., Bergelson, L. D., Spiers, M., Hauser, J., and Semenza, G., Phospholipid topology and flip-flop of intestinal brush-border membrane. Biochim. biophys. Acta882 (1986) 87–99.

    Article  Google Scholar 

  7. Beaumelle, B. D., Vial, H. J., and Bienvenüe, A., Enhanced transbilayer mobility of phospholipids in malaria-infected monkey erythrocytes. A spin-label study. J. Cell Physiol.135 (1988) 94–100.

    Article  CAS  PubMed  Google Scholar 

  8. Bergmann, W. L., Dressler, V., Haest, C. W. M., and Deuticke, B., Reorientation rates and asymmetry of distribution of lysophospholipids between the inner and outer leaflet of the erythrocyte membrane. Biochim. biophys. Acta772 (1984) 328–336.

    Article  CAS  PubMed  Google Scholar 

  9. Berridge, M. J., Inositol triphosphate and diacylglycerol: two interacting second messengers. A. Rev. Biochem.56 (1987) 159–193.

    Article  CAS  Google Scholar 

  10. Bevers, E. M., Tilly, R. H., Tilly, J., Senden, J. M. G., Comfurius, P., and Zwaal, R. F. A., Exposure of endogenous phosphatidylserine at the outer surface of stimulated platelets is reversed by restoration of aminophospholipid translocase activity. Biochemistry28 (1989) 2382–2387.

    Article  CAS  PubMed  Google Scholar 

  11. Bishop, W. R. and Bell, R. M., Assembly of the endoplasmic reticulum phospholipid bilayer: the phosphatidylcholine transporter. Cell42 (1985) 51–60.

    Article  CAS  PubMed  Google Scholar 

  12. Bishop, D. G., Op den Kamp, J. A. F., and van Deenen, L. L. M., The distribution of lipids in the protoplast membranes ofBacillus subtilis. A study with phospholipase C and trinitrobenzene sulphonic acid. Eur. J. Biochem.80 (1977) 381–391.

    Article  CAS  PubMed  Google Scholar 

  13. Bitbol, M., and Devaux, P. F., Measurement of outward translocation of phospholipids across human erythrocyte membrane. Proc. natl Acad. Sci. USA85 (1988) 6783–6787.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bloj, B., and Zilversmit, D. B., Asymmetry and transposition rates of phosphatidylcholine in rat erythrocyte ghosts. Biochemistry15 (1976) 1277–1283.

    Article  CAS  PubMed  Google Scholar 

  15. Bloj, B., and Zilversmit, D. B., Complete exchangeability of cholesterol in phosphatidylcholine/cholesterol vesicles of different degrees of unsaturation. Biochemistry16 (1977) 3943–3948.

    Article  CAS  PubMed  Google Scholar 

  16. Brasaemble, D. L., Robertson, A. D., and Ahle, A. D., Transbilayer movement of cholesterol in the human erythrocyte membrane. J. Lipid Res.29 (1988) 481–489.

    Article  Google Scholar 

  17. Bretscher, M. S., Asymmetrical lipid bilayer structure for biological membranes. Nature New Biol.236 (1972) 11–12.

    Article  CAS  PubMed  Google Scholar 

  18. Bröring, K., Haest, C. W. M., and Deuticke, B., Translocation of oleic acid across the erythrocyte membrane. Evidence for a fast process. Biochim. biophys. Acta986 (1989) 321–331.

    Article  PubMed  Google Scholar 

  19. Buckland, R. M., Radda, G. K., and Shennan, C. D., Accessibility of phospholipids in the chromaffin granule membrane. Biochim. biophys. Acta513 (1978) 321–337.

    Article  CAS  PubMed  Google Scholar 

  20. Cabral, D. J., Small, D. M., Lilly, H. S., and Hamilton, J. A., Transbilayer movement of bile acid in model membranes. Biochemistry26 (1987) 1801–1804.

    Article  CAS  PubMed  Google Scholar 

  21. Calvez, J. Y., Zachowski, A., Herrmann, A., Morrot, G., and Devaux, P. F., Asymmetric distribution of phospholipids in spectrinpoor erythrocyte vesicles. Biochemistry27 (1988) 5666–5670.

    Article  CAS  PubMed  Google Scholar 

  22. Chap, H. J., Zwaal, R. F. A., and van Deenen, L. L. M., Action of highly purified phospholipases on blood platelets. Evidence for an asymmetric distribution of phospholipids in the surface membrane. Biochim. biophys. Acta467 (1977) 146–164.

    Article  CAS  PubMed  Google Scholar 

  23. Chiu, D., Lubin, B., and Shohet, S. B., Erythrocyte membrane lipid reorganization during the sickling process. Br. J. Haemat.41 (1979) 223–234.

    Article  CAS  Google Scholar 

  24. Classen, J., Haest, C. M. W., Tournois, H., and Deuticke, B., Gramicidin-induced enhancement of transbilayer reorientation of lipids in the erythrocyte membrane. Biochemistry26 (1987) 6604–6612.

    Article  CAS  PubMed  Google Scholar 

  25. Coleman, R., and Bell, R. M., Evidence that biosynthesis of phosphatidylethanolamine, phosphatidylcholine and triacylglycerol occurs on the cytoplasmic side of microsomal vesicles. J. Cell Biol.76 (1978) 245–253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Connor, J., and Schroit, A. J., Determination of lipid asymmetry in human red cells by resonance energy transfer. Biochemistry26 (1987) 5099–5105.

    Article  CAS  PubMed  Google Scholar 

  27. Connor, J., and Schroit, A. J., Transbilayer movement of phosphatidylserine in non human erythrocyte: evidence that the aminophospholipid transporter is a ubiquitous membrane protein. Biochemistry28 (1989) 9680–9685.

    Article  CAS  PubMed  Google Scholar 

  28. Crain, R. C., and Zilversmit, D. B., Two non-specific phospholipid exchange proteins from beef liver. 2. Use in studying the asymmetry and transbilayer movement of phosphatidylcholine, phosphatidyl-ethanolamine, and sphingomyelin in intact rat erythrocytes. Biochemistry19 (1980) 1440–1447.

    Article  CAS  PubMed  Google Scholar 

  29. Daleke, D. L., and Huestis, W. H., Incorporation and translocation of aminophospholipids in human erythrocytes. Biochemistry24 (1985) 5406–5416.

    Article  CAS  PubMed  Google Scholar 

  30. Daleke, D. L., and Huestis, W. H., Erythrocyte morphology reflects the transbilayer distribution of incorporated phospholipids. J. Cell Biol.108 (1989) 1375–1385.

    Article  CAS  PubMed  Google Scholar 

  31. De Kruijff, B., van Zoelen, E. J. J., and van Deenen, L. L. M., Glycophorin facilitates the transbilayer movement of phosphatidylcholine in vesicles. Biochim. biophys. Acta509 (1978) 537–542.

    Article  PubMed  Google Scholar 

  32. Deutsch, J. W., and Kelly, R. B., Lipids of synaptic vesicles: relevance to the mechanism of membrane fusion. Biochemistry20 (1981) 378–385.

    Article  CAS  PubMed  Google Scholar 

  33. Devaux, P. F., Morrot, G., Herrmann, A., and Zachowski, A., Protein involvement in plasma membrane lipid asymmetry. Stud. Biophys.127 (1988) 183–191.

    CAS  Google Scholar 

  34. Doody, M.C., Pownall, H. J., Kao, Y. J., and Smith, L. C., Mechanism and kinetics of transfer of a fluorescent fatty acid between single-walled phosphatidylcholine vesicles. Biochemistry19 (1980) 108–116.

    Article  CAS  PubMed  Google Scholar 

  35. Dressler, V., Haest, C. M. W., Plasa, G., Deuticke, B., and Erusalimsky, J. D., Stabilizing factors of phospholipid asymmetry in the erythrocyte membrane. Biochim. biophys. Acta775 (1984) 189–196.

    Article  CAS  PubMed  Google Scholar 

  36. Drickamer, L. K., The red cell membrane contains three different adenosine triphosphatases. J. biol. Chem.250 (1975) 1952–1954.

    Article  CAS  PubMed  Google Scholar 

  37. Elferink, J. G. R., The asymmetric distribution of chlorpromazine and its quaternary analogue over the erythrocyte membrane. Biochem. Pharmac.26 (1977) 2411–2416.

    Article  CAS  Google Scholar 

  38. Etemadi, A.-H., Membrane asymmetry. A survey and critical appraisal of the methodology. II. Methods for assessing the unequal distribution of lipids. Biochim. biophys. Acta604 (1980) 423–475.

    CAS  PubMed  Google Scholar 

  39. Fontaine, R. N., Harris, R. A., and Schroeder, F., Aminophospholipid asymmetry in murine synaptosomal plasma membrane. J. Neurochem.34 (1980) 269–277.

    Article  CAS  PubMed  Google Scholar 

  40. Fontaine, R. N., and Schroeder, F., Plasma membrane aminophospholipid distribution in transformed murine fibroblasts. Biochim. biophys. Acta558 (1979) 1–12.

    Article  CAS  PubMed  Google Scholar 

  41. Forgac, L., and Cantley, L., The plasma membrane (Mg2+)-dependent adenosine triphosphatase from the human erythrocyte is not an ion pump. J. Membr. Biol.80 (1984) 185–190.

    Article  CAS  PubMed  Google Scholar 

  42. Franck, P. F. H., Chiu, D. T.-Y., Op den Kamp, J. A. F., Lubin, B., van Deenen, L. L. M., and Roelofsen, B., Accelerated transbilayer movement of phosphatidylcholine in sickled erythrocytes. A reversible process. J. biol. Chem.258 (1983) 8435–8442.

    Article  Google Scholar 

  43. Franck, P. F. H., Op den Kamp, J. A. F., Lubin, B., Berendsen, W., Joosten, P., Briët, E., van Deenen, L. L. M., and Roelofsen, B., Abnormal transbilayer mobility of phosphatidylcholine in hereditary pyropoikilocytosis reflects the increased heat sensitivity of the membrane skeleton. Biochim. biophys. Acta815 (1985) 259–267.

    Article  CAS  PubMed  Google Scholar 

  44. Fujii, T., Tamura, A., and Yamane, T., Trans-bilayer movement of added phosphatidylcholine and lysophosphatidylcholine species with various acylchain lengths in plasma membrane of intact human erythrocytes. J. Biochem.98 (1986) 1221–1227.

    Article  Google Scholar 

  45. Ganong, B. R., and Bell, R. M., Transmembrane movement of phosphatidylglycerol and diacylglycerol sulfhydryl analogues. Biochemistry23 (1984) 4977–4983.

    Article  CAS  PubMed  Google Scholar 

  46. Gazzit, Y., Ohad, I., and Loyter, A., Changes in phospholipid susceptibility toward phospholipases induced by ATP depletion in avian and amphibian erythrocyte membranes. Biochim. biophys. Acta382 (1975) 65–72.

    Article  Google Scholar 

  47. Gordesky, S. E., Marinetti, G. V., and Love, R., The reaction of chemical probes with the erythrocyte membrane. J. Memb. Biol.20 (1975) 111–132.

    Article  CAS  Google Scholar 

  48. Greenhut, S. F., and Roseman, M. A., Cytochrome b5 induced flipflop of phospholipids in sonicated vesicles. Biochemistry24 (1985) 1252–1260.

    Article  CAS  PubMed  Google Scholar 

  49. Gupta, C. M., Alam, A., Mathur, P. N., and Dutta, G. P., A new look at nonparasitized red cells of malaria-infected monkeys. Nature299 (1982) 259–261.

    Article  CAS  PubMed  Google Scholar 

  50. Haldar, K., de Amorim, A. F., and Cross, G. A. M., Transport of fluorescent phospholipid analogues from the erythrocyte membrane to the parasite inPlasmodium falciparum-infected cells. J. Cell Biol.108 (1989) 2183–2192.

    Article  CAS  PubMed  Google Scholar 

  51. Herbette, L., Blaisie, J. K., Defoor, P., Fleischer, S., Bick, R. J., van Winkle, W. B., Tate, C. A., and Entman, M. L., Phospholipid asymmetry in the isolated sarcoplasmic reticulum membrane. Archs. Biochem. Biophys.234 (1984) 235–242.

    Article  CAS  Google Scholar 

  52. Herrmann, A., and Devaux, P. F., Alteration of the aminophospholipid translocase activity during in vivo and artifical aging of human erythrocytes. Biochim. biophys. Acta (1990) in press.

  53. Herrmann, A., Zachowski, A., and Devaux, P. F., The protein mediated phospholipid translocation of the endoplasmic reticulum has a low lipid specificity. Biochemistry29 (1990) 2023–2027.

    Article  CAS  PubMed  Google Scholar 

  54. Hidalgo, C., and Ikemoto, N., Disposition of proteins and aminophospholipids in the sarcoplasmic reticulum membrane. J. biol. Chem.252 (1977) 8446–8454.

    Article  CAS  PubMed  Google Scholar 

  55. Higgins, J. A., Biogenesis of endoplasmic reticulum phosphatidylcholine. Translocation of intermediate across the membrane bilayer during methylation of phosphatidylethanolamine. Biochim. biophys. Acta640 (1981) 1–15.

    Article  CAS  PubMed  Google Scholar 

  56. Hirata, F., and Axelrod, J., Enzymatic synthesis and rapid translocation of phosphatidylcholine by two methyl transferases in erythrocyte membranes. Proc. natl Acad. Sci. USA75 (1978) 2348–2352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Homan, R., and Pownall, H. J., Effect of pressure on phospholipid translocation in lipid bilayers. J. Am. chem. Soc.109 (1987) 4759–4760.

    Article  CAS  Google Scholar 

  58. Hope, M. J., and Cullis, P. R., Lipid asymmetry induced by transmembrane pH gradients in large unilamellar vesicles. J. biol. Chem.262 (1987) 4360–4366.

    Article  CAS  PubMed  Google Scholar 

  59. Hope, M. J., Redelmeier, T. E., Wong, K. F., Rodrigueza, W., and Cullis, P. R., Phospholipid asymmetry in large unilamellar vesicles induced by transmembrane pH gradients. Biochemistry28 (1989) 4181–4187.

    Article  CAS  PubMed  Google Scholar 

  60. Hubbell, W. L., Transbilayer coupling mechanism for the formation of lipid asymmetry in biological membranes. Application to the photoreceptor disc membrane. Biophys. J.57 (1990) 99–108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Hutson, J. L., and Higgins, J. A., Asymmetric synthesis followed by transmembrane movements of phosphatidylethanolamine in rat liver endoplasmic reticulum. Biochim. biophys. Acta687 (1982) 247–256.

    Article  CAS  PubMed  Google Scholar 

  62. Joliot, P., and Joliot, A., Electron transfer between the two photosystems. II. Equilibrium constants. Biochim. biophys. Acta765 (1984) 219–226.

    Article  CAS  Google Scholar 

  63. Johnson, L. W., Hughes, M. E., and Zilversmit, D. B., Use of phospholipid exchange protein to measure inside-outside transposition in phosphatidylcholine liposomes. Biochim. biophys. Acta375 (1974) 176–185.

    Article  Google Scholar 

  64. Kahlenberg, A., Walker, C., and Rohrlick, R., Evidence for an asymmetric distribution of phospholipids in the human erythrocyte membrane. Can. J. Biochem.52 (1974) 803–806.

    Article  CAS  PubMed  Google Scholar 

  65. Kawashima, Y., and Bell, R. M., Assembly of the endoplasmic reticulum phospholipid bilayer: the phosphatidylcholine and metabolites. J. biol. Chem.262 (1987) 16495–16502.

    Article  CAS  PubMed  Google Scholar 

  66. Kirby, C. J., and Green, C., Transbilayer migration (flip-flop) of cholesterol in erythrocyte membranes. Biochem. J.168 (1977) 575–577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kornberg, R. D., and Mc Connell, H. M., Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry10 (1971) 1111–1120.

    Article  CAS  PubMed  Google Scholar 

  68. Kumar, G., Kaira, V. K., and Brodie, A. F., Asymmetric distribution of phospholipids in membranes fromMycobacterium phlei. Archs Biochem. Biophys.198 (1979) 22–30.

    Article  CAS  Google Scholar 

  69. Kuypers, F., van Linde-Sibenius-Trip, M., Roelofsen, B., Tanner, M. J. A., Anstee, D. J., and Op den Kamp, J. A. F., Rhnull human erythrocytes have an abnormal membrane phospholipid organization. Biochem. J.2218 (1984) 931–934.

    Article  Google Scholar 

  70. Kuypers, F., van Linde-Sibenius-Trip, M., Roelofsen, B., Op den Kamp, J. A. F., Tanner, M. J. A., and Anstee, D. J., The phospholipid organization in the membranes of Mc Leod and Leach phenotype erythrocytes. FEBS Lett.184 (1985) 20–24.

    Article  CAS  PubMed  Google Scholar 

  71. Lange, Y., Cohen, C. M., and Poznansky, M. J., Transmembrane movement of cholesterol in human erythrocytes. Proc. natl Acad. Sci. USA74 (1977) 1538–1542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Lange, Y., Dolde, J., and Steck, T. L., The rate of transmembrane movement of cholesterol in human erythrocytes. J. biol. Chem.256 (1981) 5321–5323.

    Article  CAS  PubMed  Google Scholar 

  73. Lange, Y., and Slayton, J.M., Interaction of cholesterol and lysophosphatidylcholine in determining red cell shape. J. Lipid Res.23 (1982) 1121–1127.

    Article  CAS  PubMed  Google Scholar 

  74. Langley, K. E., and Kennedy, E. P., Energetics of rapid transmembrane movement and of compositional asymmetry of phosphatidylethanolamine in membranes ofBacillus megaterium. Proc. natl Acad. Sci. USA76 (1979) 6245–6249.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lubin, B., Chiu, D., Bastacky, J., Roelofsen, B., and van Deenen, L. L. M., Abnormalities in membrane phospholipid organization in sickled erythrocytes. J. clin. Invest.67 (1981) 1643–1649.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lupu, F., Caib, M., Scurei, C., and Simionescu, N., Changes in the organization of membrane lipids during human platelet activation. Study by fluorescent and freeze-fracture cytochemistry. Lab. Invest.54 (1986) 136–145.

    CAS  PubMed  Google Scholar 

  77. Maksymiw, R., Sui, S., Gaub, H., and Sackmann, E., Electrostatic coupling of spectrin dimers to phosphatidylserine containing lipid lamellae. Biochemistry26 (1987) 2983–2990.

    Article  CAS  PubMed  Google Scholar 

  78. Maneta-Peyret, L., Freyburger, G., Bessoule, J.-J., and Cassagne, C., Specific immunocytochemical visualization of phosphatidylserine. J. immun. Meth.12 (1989) 155–159.

    Article  Google Scholar 

  79. Martin, O. C., and Pagano, R. E., Transbilayer movement of fluorescent analogs of phosphatidylserine and phosphatidylethanolamine at the plasma membrane of cultured cells. J. biol. Chem.262 (1987) 5890–5898.

    Article  CAS  PubMed  Google Scholar 

  80. Mc Namee, M. G., and Mc Connell, H. M., Transmembrane potentials and phospholipid flip-flop in excitable membrane vesicles. Biochemistry12 (1973) 2951–2958.

    Article  CAS  PubMed  Google Scholar 

  81. Michaelson, D. M., Barkai, G., and Barenholz, Y., Asymmetry of lipid organization in cholinergic synaptic vesicle membranes. Biochem. J.211 (1983) 155–162.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Middelkoop, E., Transmembrane phospholipid asymmetry in erythroid cells: mechanisms of maintenance. Ph. D. thesis. University of Utrecht (The Netherlands), 1989.

    Google Scholar 

  83. Middelkoop, E., Lubin, B. H., Bevers, E. M., Op den Kamp, J. A. F., Comfurius, P., Chiu, D. T.-Y., Zwaal, R. F. A., van Deenen, L. L. M., and Roelofsen, B., Studies on sickled erythrocytes provide evidence that the asymmetric distribution of phosphatidylserine in the red cell membrane is maintained by both ATP-dependent translocation and interaction with membrane skeletal proteins. Biochim. biophys. Acta937 (1988) 281–288.

    Article  CAS  PubMed  Google Scholar 

  84. Middelkoop, E., Lubin, B. H., Op den Kamp, J. A. F., and Roelofsen, B., Flip-flop rates of individual molecular species of phosphatidylcholine in the human red cell membrane. Biochim. biophys. Acta855 (1986) 421–424.

    Article  CAS  PubMed  Google Scholar 

  85. Mombers, C., Verkleij, A. J., de Gier, J., and van Deenen, L. L. M., Interaction of spectrin-actin and synthetic phospholipids. II. The interaction with phosphatidylserine. Biochim. biophys. Acta551 (1979) 271–281.

    Article  CAS  PubMed  Google Scholar 

  86. Morrot, G., Hervé, P., Zachowski, A., Fellmann, P., and Devaux, P. F., Aminophospholipid translocase of human erythrocytes: phospholipid substrate specificity and effect of cholesterol. Biochemistry28 (1989) 3456–3462.

    Article  CAS  PubMed  Google Scholar 

  87. Morrot, G., Cribier, S., Devaux, P. F., Geldwerth, D., Davoust, J., Bureau, J. F., Fellmann, P., Hervé, P., and Frilley, B., Asymmetric lateral mobility of phospholipids in the human erythrocyte membrane. Proc. natl Acad. Sci. USA83 (1986) 6863–6867.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Murthy, M. S. R., and Pande, S. V., Mechanism of carnitine acylcarnitine translocase-catalyzed import of acylcarnitines in mitochondria. J. biol. Chem.259 (1984) 9082–9089.

    Article  CAS  PubMed  Google Scholar 

  89. Noorman, P. C., van Echteld, C. J. A., de Kruijff, B., and de Giers, J., Rapid transbilayer movement of phosphatidylcholine in unsaturated phosphatidylethanolamine containing model membrane. Biochim. biophys. Acta646 (1981) 483–487.

    Article  Google Scholar 

  90. Nordlund, J. R., Schmidt, C. F., Holloway, P. W., and Thompson, T. E., Effect of cytochrome b5 on the transbilayer distribution of phospholipids on model membranes. Biochemistry21 (1982) 2820–2825.

    Article  CAS  PubMed  Google Scholar 

  91. Norris, V., Phospholipid flip-out controls the cell cycle ofEscherichia coli. J. Theor. Biol.139 (1989) 117–128.

    Article  CAS  PubMed  Google Scholar 

  92. Olaisson, H., Mardh, S., and Arvisson, G., Phospholipid organization in H+K+-ATPase-containing membranes from pig gastric mucosa. J. biol. Chem.260 (1985) 11 262–11 267.

    Article  CAS  Google Scholar 

  93. Op den Kamp, J. A. F., Lipid asymmetry in membranes. A. Rev. Biochem.48 (1979) 47–71.

    Article  CAS  Google Scholar 

  94. Packham, N. K., and Jackson, J. B., Transport of local anaesthetics across chromatophore membranes. Biochim. biophys. Acta546 (1979) 142–146.

    Article  CAS  PubMed  Google Scholar 

  95. Pagano, R. E., and Longmuir, K. J., Phosphorylation, transbilayer movement, and facilitated intracellular transport of diacylglycerol are involved in the uptake of a fluorescent analog of phosphatidic acid by cultured fibroblasts. J. biol. Chem.260 (1985) 1909–1916.

    Article  CAS  PubMed  Google Scholar 

  96. Pagano, R. E., and Sleight, R. G., Defining lipid transport pathways in animal cells. Science229 (1985) 1051–1057.

    Article  CAS  PubMed  Google Scholar 

  97. Patzer, E. J., Wagner, R. R., and Barenholz, Y., Cholesterol oxidase as a probe for studying membrane organisation. Nature274 (1978) 394–395.

    Article  CAS  PubMed  Google Scholar 

  98. Pelletier, X., Mersel, M., Freysz, L., and Leray, C., Topological distribution of aminophospholipid fatty acids in trout intestinal brush-border membrane. Biochim. biophys. Acta902 (1987) 223–228.

    Article  CAS  PubMed  Google Scholar 

  99. Perret, B., Chap, H. J., and Douste-Blazy, L., Asymmetric distribution of arachidonic acid in the plasma membrane of human platelets. A determination using purified phospholipases and a rapid method for membrane isolation. Biochim. biophys. Acta556 (1979) 434–446.

    Article  CAS  PubMed  Google Scholar 

  100. Rawyler, A., van der Schaft, P. H., Roelofsen, B., and Op den Kamp, J. A. F., Phospholipid localization in the plasma membrane of Friend erythroleukemic cells and mouse erythrocytes. Biochemistry24 (1985) 1777–1783.

    Article  CAS  PubMed  Google Scholar 

  101. Record, M., El Tamer, A., Chap, H., and Douste-Blazy, L., Evidence for a highly asymmetric arrangement of ether- and diacyl-phospholipid subclasses in the plasma membrane of Krebs II ascites cells. Biochim. biophys. Acta778 (1984) 449–456.

    Article  CAS  PubMed  Google Scholar 

  102. Redelmeier, T. E., Hope, M. J., and Cullis, P. R., On the mechanism of transbilayer transport of phosphatidylglycerol in response to transmembrane pH gradients. Biochemistry29 (1990) 3046–3053.

    Article  CAS  PubMed  Google Scholar 

  103. Renooij, W., van Golde, L. M. G., Zwaal, R. F. A., and van Deenen, L. L. M., Topological asymmetry of phospholipid metabolism in rat erythrocyte membranes. Evidence for flip-flop of lecithin. Eur. J. Biochem.61 (1976) 53–58.

    Article  CAS  PubMed  Google Scholar 

  104. Rimon, G., Meyerstein, N., and Hennis, Y. I., Lateral mobility of phospholipids in the external and internal leaflets of normal and hereditary spherocytic human erythrocytes. Biochim. biophys. Acta775 (1984) 283–290.

    Article  CAS  PubMed  Google Scholar 

  105. Roelofsen, B., Op den Kamp, J. A. F., and van Dennen, L. L. M., Structural and dynamic aspects of red cell phospholipids; featuring phosphatidylcholine. Biomed. biochim. Acta46 (1987) 510–515.

    Google Scholar 

  106. Rothman, J. E., and Dawidowicz, E. A., Asymmetric exchange of vesicle phospholipids catalyzed by the phosphatidylcholine exchange protein. Measurement of inside-outside transitions. Biochemistry14 (1975) 2809–2816.

    Article  CAS  PubMed  Google Scholar 

  107. Rothman, J. E., and Kennedy, E. P., Asymmetrical distribution of phospholipids in the membrane ofBacillus megaterium. J. molec. Biol.110 (1977) 603–618.

    Article  CAS  PubMed  Google Scholar 

  108. Rothman, J. E., Tsai, D. K., Dawidowicz, E. A., and Lenard, J., Transbilayer phospholipid asymmetry and its maintenance in the membrane of influenza virus. Biochemistry15 (1976) 2361–2370.

    Article  CAS  PubMed  Google Scholar 

  109. Rousselet, A., Colbeau, A., Vignais, P. M., and Devaux, P. F., Study of the transverse diffusion of spin-labeled phospholipids in biological membranes. II. Inner mitochondrial membrane of rat liver: use of phosphatidylcholine exchange protein. Biochim. biophys. Acta426 (1976) 372–384.

    Article  CAS  PubMed  Google Scholar 

  110. Rousselet, A., Guthman, C., Matricon, J., Bienvenüe, A., and Devaux, P. F., Study on the transverse diffusion of spin labeled phospholipids in biological membranes. I. Human red blood cells. Biochim. biophys. Acta426 (1976) 357–371.

    Article  CAS  PubMed  Google Scholar 

  111. Sanchez-Yagüe, J., and Llanillo, M., Lipid composition of subcellular particles from sheep platelets. Location of phosphatidylethanolamine and phosphatidylserine in plasma membrane and platelet liposomes. Biochim. biophys. Acta856 (1986) 193–201.

    Article  PubMed  Google Scholar 

  112. Sandra, A., and Pagano, R. E., Phospholipid asymmetry in LM cell plasma membrane derivatives: polar head group and acyl chains distribution. Biochemistry17 (1978) 332–338.

    Article  CAS  PubMed  Google Scholar 

  113. Schick, P. K., Kurica, K. B., and Chacko, G. K., Location of phosphatidylethanolamine and phosphatidylserine in the human platelet membrane. J. clin. Invest.57 (1976) 1221–1226.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Schroit, A. J., Madsen, J., and Ruoho, A. E., Radioiodinated photoactivable phosphatidylcholine and phosphatidylserine: transfer properties and differential photoreactive interaction with human erythrocyte membrane proteins. Biochemistry26 (1987) 1812–1819.

    Article  CAS  PubMed  Google Scholar 

  115. Seigneuret, M., and Devaux, P. F., ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membranes: relation to shape changes. Proc. natl Acad. Sci. USA81 (1984) 3751–3755.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Seigneuret, M., Zachowski, A., Herrmann, A., and Devaux, P. F., Asymmetric lipid fluidity in human erythrocyte membrane: new spin-label evidence. Biochemistry23 (1984) 4271–4275.

    Article  CAS  PubMed  Google Scholar 

  117. Sessions, A., and Horwitz, A. F., Differentiation-related differences in the plasma membrane phospholipid asymmetry of myogenic and fibrogenic cells. Biochim. biophys. Acta728 (1983) 103–111.

    Article  CAS  PubMed  Google Scholar 

  118. Sharom, F. J., and Grant, C. W. M., A model for ganglioside behaviour in cell membranes. Biochim. biophys. Acta507 (1978) 280–293.

    Article  CAS  PubMed  Google Scholar 

  119. Shaw, J. M., Hutton, W. C., Lentz, B. R., and Thompson, T. E., Proton nuclear magnetic resonance study of the decay of transbilayer compositional asymmetry generated by a phosphatidylcholine exchange protein. Biochemistry16 (1977) 4156–4163.

    Article  CAS  PubMed  Google Scholar 

  120. Sheetz, M. P., and Singer, S. J., Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. natl Acad. Sci. USA71 (1974) 4457–4461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Shukla, S. D., and Hanahan, D. J., Membrane alteration in cellular aging: susceptibility of phospholipids in density (age)-separated human erythrocytes to phospholipase A2. Archs Biochem. Biophys.214 (1982) 335–341.

    Article  CAS  Google Scholar 

  122. Siegel, D. P., Banschbach, J., and Yeagle, P. L., Stabilization of HII phases by low levels of diglycerides and alkanes: a NMR, calorimetric and X-ray diffraction study. Biochemistry28 (1989) 5010–5019.

    Article  CAS  Google Scholar 

  123. Sleight, R. G., and Pagano, R. E., Transport of a fluorescent phosphatidylcholine analog from the plasma membrane to the Golgi apparatus. J. Cell Biol.99 (1984) 742–751.

    Article  CAS  PubMed  Google Scholar 

  124. Sperka-Gottlieb, C. D. M., Hermetter, A., Paltauf, F., and Daum, G., Lipid topology and physical properties of the outer mitochondrial membrane of the yeast,Saccharomyces cerevisiae. Biochim. biophys. Acta946 (1988) 227–234.

    Article  CAS  PubMed  Google Scholar 

  125. Sune, A., and Bienvenüe, A., Relationship between the transverse distribution of phospholipids in plasma membrane and shape change of human platelets. Biochemistry27 (1988) 6794–6800.

    Article  CAS  PubMed  Google Scholar 

  126. Sune, A., Vidal, M., Morin, P., Sainte-Marie, J., and Bienvenüe, A., Evidence for bidirectionnal transverse diffusion of spin-labeled phospholipids in the plasma membrane of guinea pig blood cells. Biochim. biophys. Acta946 (1988) 315–327.

    Article  CAS  PubMed  Google Scholar 

  127. Tanaka, K. I., and Ohnishi, S.-I., Heterogeneity in the fluidity of intact erythrocyte membrane and its homogenization upon hemolysis. Biochim. biophys. Acta426 (1976) 218–231.

    Article  CAS  PubMed  Google Scholar 

  128. Tanaka, Y., and Schroit, A. J., Insertion of fluorescent phosphatidylserine into the plasma membrane of red blood cells. Recognition by autologous macrophages. J. biol. Chem.258 (1983) 11335–11343.

    Article  CAS  PubMed  Google Scholar 

  129. Tilley, L., Cribier, S., Roelofsen, B., Op den Kamp, J. A. F., and van Deenen, L. L. M., ATP-dependent translocation of aminophospholipids across the human erythrocyte membrane. FEBS Lett.194 (1986) 21–27.

    Article  CAS  PubMed  Google Scholar 

  130. Tocanne, J.-F., Dupou-Cézanne, L., Lopez, A., and Tournier, J.-F., Lipid lateral diffusion and membrane organization. FEBS Lett.257 (1989) 10–16.

    Article  CAS  PubMed  Google Scholar 

  131. Vale, M. G. P., Localization of the aminophospholipids in sarcoplasmic reticulum membranes revealed by trinitrobenzene-sulfonate and fluorodinitrobenzene. Biochim. biophys. Acta471 (1977) 39–48.

    Article  CAS  PubMed  Google Scholar 

  132. Vance, D. E., Choy, P. C., Farren, S. B., Lim, P. H., and Schneider, W. J., Asymmetry of phospholipid biosynthesis. Nature270 (1977) 268–269.

    Article  CAS  PubMed  Google Scholar 

  133. Van den Besselaar, A. M. H. P., de Kruijff, B., van den Bosch, H., and van Deenen, L. L. M., Phosphatidylcholine mobility in liver microsomal membranes. Biochim. biophys. Acta510 (1978) 242–255.

    Article  PubMed  Google Scholar 

  134. Van den Meer, B. W., Fugate, R. D., and Sims, P. J., Complement proteins C5b-9 induce transbilayer migration of membrane phospholipids. Biophys. J.56 (1989) 935–946.

    Article  PubMed  PubMed Central  Google Scholar 

  135. Van der Schaft, P. H., Beaumelle, B., Vial, H., Roelofsen, B., Op den Kamp, J. A. F., and van Deenen, L. L. M., Phospholipid organization in monkey erythrocytes uponPlasmodium knowlesi infection. Biochim. biophys. Acta901 (1987) 1–14.

    Article  PubMed  Google Scholar 

  136. Van der Steen, A. T. M., de Kruijff, B., and de Gier, J., Glycophorin incorporation increases the bilayer permeability of large unilamellar vesicles in a lipid-dependent manner. Biochim. biophys. Acta691 (1982) 13–23.

    Article  Google Scholar 

  137. Van Dijck, P. W. M., van Zoelen, E. J. J., Seldenrijk, R., van Deenen, L. L. M., and de Gier, J., Calorimetric behavior of individual phospholipid classes from human and bovine erythrocyte membranes. Chem. Phys. Lipids17 (1986) 336–343.

    Article  Google Scholar 

  138. Van Duijn, G., Luiken, J., Verkleij, A. J., and de Kruijff, B., Relation between lipid polymorphism and transbilayer movement of lipids in rat liver microsomes. Biochim. biophys. Acta863 (1986) 193–204.

    Article  PubMed  Google Scholar 

  139. Van Meer, G., Plasma membrane cholesterol pools. TIBS12 (1987) 375–376.

    Google Scholar 

  140. Van Meer, G., Gahmberg, C. G., Op den Kamp, J. A. F., and van Deenen, L. L. M., Phospholipid distribution in human En(a-) red cell membranes which lack the major sialoglycoprotein, glycophorin A. FEBS Lett.135 (1981) 53–55.

    Article  PubMed  Google Scholar 

  141. Van Meer, G., and Op den Kamp, J. A. F., Transbilayer movement of various phosphatidylcholine species in intact human erythrocytes. J. Cell Biochem.19 (1982) 193–204.

    Article  PubMed  Google Scholar 

  142. Van Meer, G., Simons, K., Op den Kamp, J. A. F., and van Deenen, L. L. M., Phospholipid asymmetry in Semliki Forest virus grown in baby hamster kidney (BHK-21) cells. Biochemistry20 (1981) 1974–1981.

    Article  PubMed  Google Scholar 

  143. Venien, C., and Le Grimellec, C., Phospholipid asymmetry in renal brush-border membranes. Biochim. biophys. Acta942 (1988) 159–168.

    Article  CAS  PubMed  Google Scholar 

  144. Verkleij, A. J., Zwaal, R. F. A., Roelofsen, B., Comfurius, P., Kastelijn, D., and van Deenen, L. L. M., The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etching electron microscopy. Biochim. biophys. Acta323 (1973) 178–193.

    Article  CAS  PubMed  Google Scholar 

  145. Williamson, P., Algarin, L., Bateman, J., Choe, H. R., and Schlegel, R., Phospholipid asymmetry in human erythrocyte ghosts. J. Cell Physiol.123 (1985) 209–214.

    Article  CAS  PubMed  Google Scholar 

  146. Williamson, P., Bateman, J., Kozarsky, K., Mattocks, K., Hermanowicz, N., Choe, H. R., and Schlegel, R., Involvement of spectrin in the maintenance of phase-state asymmetry in the erythrocyte membrane. Cell30 (1982) 725–735.

    Article  CAS  PubMed  Google Scholar 

  147. Zachowski, A., Craescu, C. T., Galacteros F., and Devaux, P. F., Abnormality of phospholipid transverse diffusion in sickle erythrocytes. J. clin. Invest.75 (1985) 1713–1719.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Zachowski, A., Favre, E., Cribier, S., Hervé, P., and Devaux, P. F., Outside-inside translocation of aminophospholipids in the human erythrocyte membrane is mediated by a specific enzyme. Biochemistry25 (1986) 2585–2590.

    Article  CAS  PubMed  Google Scholar 

  149. Zachowski, A., Fellmann, P., and Devaux, P. F., Absence of transbilayer diffusion of spin-labeled sphingomyelin in human erythrocytes. Comparison with the diffusion of several spin-labeled glycerophospholipids. Biochim. biophys. Acta815 (1985) 510–514.

    Article  CAS  PubMed  Google Scholar 

  150. Zachowski, A., Henry, J.P., and Devaux, P. F., Control of transmembrane lipid asymmetry in chromaffin granules by an ATP-dependent protein. Nature340 (1989) 75–76.

    Article  CAS  PubMed  Google Scholar 

  151. Zachowski, A., Herrmann, A., Paraf, A., and Devaux, P. F., Aminophospholipid outside-inside translocation in lymphocyte plasma membranes is a protein-mediated phenomenon. Biochim. biophys. Acta897 (1987) 197–200.

    Article  CAS  PubMed  Google Scholar 

  152. Zilversmit, D. B., Phospholipid exchange proteins as membrane probes. Ann. N. Y. Acad. Sci.308 (1978) 149–163.

    Article  CAS  PubMed  Google Scholar 

  153. Zilversmit, D. B., and Hughes, M. E., Extensive exchange of rat liver microsomal phospholipids. Biochim. biophys. Acta469 (1977) 99–110.

    Article  CAS  PubMed  Google Scholar 

  154. Zwaal, R. F. A., and Bevers, E. M., in: Lipids and Membranes: Past Present and Future, pp. 231–257. Eds J. A. F. Op den Kamp, B. Roelofsen and K. W. A. Wirtz. Elsevier Science Publishers, Amsterdam 1986.

    Google Scholar 

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Zachowski, A., Devaux, P.F. Transmembrane movements of lipids. Experientia 46, 644–656 (1990). https://doi.org/10.1007/BF01939703

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