The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium: Evidence for rapid flip and flop movement

European Journal of Biochemistry

Volumn 267, Issue 5, 2000, Pages 1473-1483

  Hessel, Elke ^a   Herrmann, Andreas ^b   Müller, Peter ^b   Schnetkamp, Paul P M ^c   Hofmann, Klaus Peter ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

Disc membrane; Flip flop; Phospholipid asymmetry; Photoreceptor

Indexed keywords

PHOSPHOLIPID; RHODOPSIN;

ARTICLE; BILAYER MEMBRANE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; LIPID ANALYSIS; LIPID COMPOSITION; NONHUMAN; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; RETINA ROD OUTER SEGMENT;

ADENOSINE TRIPHOSPHATE; ANIMALS; CATTLE; ELECTRON SPIN RESONANCE SPECTROSCOPY; ETHYLMALEIMIDE; LIPID BILAYERS; PHOSPHOLIPIDS; ROD OUTER SEGMENTS; SPIN LABELS;

BOVINAE;

EID: 0034012727     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.2000.01147.x     Document Type: Article

References (51)

1. 1. Boesze-Battaglia, K. & Albert, A. (1992) Phospholipid distribution among bovine rod outer segment plasma membrane and disc membranes. Exp. Eye Rex. 54, 821-823.
2. 2. Fliesler, S.J. & Anderson, R.E. (1983) Chemistry and metabolism of lipids in the vertebrate retina. Prog. Lipid Res. 22, 79-131.
3. 3. Lamba, O.P., Borchman, D. & O'Brien, P.J. (1994) Fourier transform infrared study of the rod outer segment disk and plasma membranes of vertebrate retina. Biochemistry 33, 1704-1712.
4. 4. Brown, M.F. (1994) Modulation of rhodopsin function by properties of the membrane bilayer. Chem. Phys. Lipids 73, 159-180.
5. 5. Bush, R.A., Malnoe, A., Reḿe, C.E. & Williams, T.P. (1994) Dietary deficiency of n-3 fatty acids alters rhodopsin content and function in the rat retina. Invest. Ophthalmol. Visual Sci. 35, 91-100.
6. 6. Anderson, R.E., Maude, M.B., Narfström, K. & Nilsson, S.E.G. (1997) Lipids of plasma, retina, and retinal pigment epithelium in Swedish briard dogs with a slowly progressive retinal dystrophy. Exp. Eye Res. 64, 181-187.
7. 7. Helmreich, E.J. & Hofmann, K.P. (1996) Structure and function of proteins in G-protein-coupled signal transfer. Biochim. Biophys. Acta 1286. 285-322.
8. 8. Hofmann, K.P. & Heck, M. (1996) Light-induced protein-protein interactions on the rod photoreceptor disc membrane. In Biomembranes HA (Lee, A.G., ed.), pp. 141-198. JAI Press Inc, Greenwich, CT, USA
9. 9. Seitz, H.R., Heck, M., Hofmann, K.P., Alt, T., Pellaud, J. & Seelig, A. (1999) Molecular determinants of the reversible membrane anchorage of the G-protein transducin. Biochemistry 38, 7950-7960.
10. 10. Kisselev, O.G., Meyer, C.K., Heck, M., Ernst, O.P. & Hofmann, K.P. (1999) Signal transfer from rhodopsin to the G-protein: evidence for a two-site sequential fit mechanism. Proc. Natl Acad. Sci. USA 96, 4898-4903.
11. 11. Dacmen, F.J. & Bonting, S.L. (1969) Internal protonation in retinylidene phosphatidylethanolamine and the red-shift in rhodopsin. Nature 222, 879-881.
12. 12. De-Grip, W.J., Bonting, S.L. & Daemen, F.J. (1975) Biochemical aspects of the visual process. XXXI. Chemical modification studies on rod outer segment retinol dehydrogenase. Exp. Eye Res. 21, 549-555.
13. 13. Sun, H., Molday, R.S. & Nathans, J. (1999) Retinal stimulates ATP hydrolysis by purified and reconstituted ABCR, the photoreceptor-specific ATP-binding cassette transporter responsible for stargardt disease. J. Biol. Chem. 274, 8269-8281.
14. 14. Weng, J., Mata, N.L., Azarian, S.M., Tzekov, R.T., Birch, D.G. & Travis, G.H. (1999) Insights into the function of rim protein in photoreceptors and etiology of stargardt's disease from the phenotype in aber knockout mice. Cell 98, 13-23.
15. 15. Bevers, E., Comfurius, E.P., Dekkers, D.W.C., Harmsma, M. & Zwaal, F.A. (1982) Transmembrane phospholipid distribution in blood cells: control mechanisms and pathophysiological significance. Biochemistry 122, 429-436.
16. 16. Fadok, V.A., Voelker, D.R., Campbell, P.A., Cohen, J.J., Bratton, D.L. & Henson, P.M. (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207-2216.
17. 17. Zwaal, R.F.A. & Schroit, A.J. (1997) Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 89, 1121-1132.
18. 18. Bishop, W.R. & Bell, R.M. (1985) Assembly of the endoplasmic reticulum phospholipid bilayer: the phosphatidycholine transporter. Cell 42, 51-60.
19. 19. Herrmann, A., Zachowski, A. & Devaux, P.F. (1990) Protein-mediated phospholipid translocation in the endoplasmic reticulum with a low lipid specificity. Biochemistry 29, 2023-2027.
20. 20. Buton, X., Morrot, G., Fellmann, P. & Seigneuret, M. (1996) Ultrafast glycerophospholipid-selective transbilayer motion mediated by a protein in the endoplasmic reticulum membrane. J. Biol. Chem. 271, 6651-6657.
21. 21. Smith, G.H., Fager, R.S. & Litman, B.J. (1977) Light-activated calcium release from sonicated bovine retinal rod outer segment disks. Biochemistry 16, 1399-1405.
22. 22. Crain, R.C., Marinetti, G.V. & O'Brien, D.F. (1978) Topology of ammo phospholipids in bovine retinal rod outer segment disk membrane. Biochemistry 17, 4186-4192.
23. 23. Miljanich, G.P., Nemes, P.P., White, D.L. & Dratz, E.A. (1981) The asymmetry transmembrane distribution of phosphatidylethanolamine, phosphatidyl-serine, and fatty acids of the bovine retinal rod outer segment disk membrane. J. Membr. Biol. 60, 249-255.
24. 24. Sklar, L.A., Miljanich, G.P., Bursten, S.L. & Dratz, E.A. (1979) Thermal lateral phase separations in bovine retinal rod outer segment membranes and phospholipids as evidenced by parinaric acid fluorescence polarization and energy transfer. J. Biol. Chem. 254, 9583-9591.
25. 25. Sklar, L.A. & Dratz, E.A. (1980) Analysis of membrane bilayer asymmetry using parinaric acid fluorescent probes. FEBS Lett. 118, 308-310.
26. 26. Drenthe, E.H.S., Klompmakers, A.A., Bonting, S.L. & Daemen, F.J.M. (1980) Transbilayer distribution of phospholipids in photoreceptor membrane studied with various phospholipases. Biochim. Biophys. Acta 603, 117-129.
27. 27. Drenthe, E.H.S., Klompmakers, A.A., Bonting, S.L. & Daemen, F.J.M. (1980) Transbilayer distribution of phospholipids in photoreceptor membrane studied with trinitrobenzensulfonate alone and in combination with phospholipase D. Biochim. Biophys. Acta 603, 130-141.
28. 28. Drenthe, E.H.S., Bonting, S.L. & Daemen, F.J.M. (1981) Transbilayer distribution of phospholipid fatty acyl chains in photoreceptor membrane. Biochim. Biophys. Acta 641, 377-385.
29. 29. Wu, G. & Hubbell, W.L. (1993) Phospholipid asymmetry and transmembrane diffusion in photoreceptor disk membranes. Biochemistry 32, 879-888.
30. 30. Haest, C.W.M., Plasa, G. & Deuticke, B. (1981) Selective removal of lipids from the outer membrane layer of human erythrocytes without hemolysis. Consequences for bilayer stability and cell shape. Biochim. Biophys. Acta 649, 701-708.
31. 31. Seigneuret, M. & Devaux, P.F. (1984) Asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc. Natl Acad. Sci. USA 81, 3751-3755.
32. 32. Morrot, G., Hervé, P., Zachowski, A., Fellmann, P. & Devaux, P.F. (1989) Aminophospholipid translocase of human erythrocytes: phospholipid substrates specifity and effect of cholesterol. Biochemistry 28, 3456-3462.
33. 33. Fellmann, P., Zachowski, A. & Devaux, P.F. (1994) Synthesis and use of spin-labeled lipids for studies of the transmembrane movement of phospholipids. In Methods in Molecular Biology, Vol. 27 (Graham, J.M. & Higgins, J.A., eds), pp. 161-175. Human Press, Totowa, NJ, USA.
34. 34. Schnetkamp, P.P.M. (1986) Sodium-calcium exchange in the outer segments of bovine rod photoreceptors. J. Physiol. 373, 25-45.
35. 35. Smith, G., Stubbs, G.W. & Litman, B.J. (1975) The isolation and purification of osmotically intact discs from retinal rod outer segments. Exp. Eye Res. 20, 211-217.
36. 2+ release from bovine rod outer segment disks. Biochemistry 26, 3249-3253.
37. 37. Daemen, F.J.M. (1973) Vertebrate rod outer segment membranes. Biochim. Biophys. Acta 300, 255-288.
38. 38. Marx, U., Lassmann, G., Wimalasena, K., Müller, P. & Herrmann, A. (1997) Rapid kinetics of insertion and accessibility of spin-labeled phospholipid analogs in lipid membranes: a stopped-flow electron paramagnetic resonance approach. Biophys. J. 73, 1645-1654.
39. 39. Calvez, J., Zachowski, A., Herrmann, A., Morrot, G. & Devaux, P.F. (1988) Asymmetric distribution of phospholipids in spectrin-poor erythrocyte vesicles. Biochemistry 27, 5666-5670.
40. 40. Müller, K., Pomorski, T., Müller, P., Zachowski, A. & Herrmann, A. (1994) Protein-dependent translocation of aminophospholipids and asymmetric transbilayer distribution of phospholipids in the plasma membrane of ram sperm cells. Biochemistry 33, 9968-9974.
41. 41. Lin, S., Yang, E. & Huestis, W.H. (1994) Relationship of phospholipid distribution to shape change in Ca(2+)-crenated and recovered human erythrocytes. Biochemistry 33, 7337-7344.
42. 42. Müller, P., Pomorski, T., Rorwoli, S., Tauber, R. & Herrmann, A. (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.
43. 43. Molday, R.S. & Molday, L.L. (1987) Differences in the protein composition of bovine retinal rod outer segment disk and plasma membranes isolated by a ricin-gold-dextran density perturbation method. J. Cell biol. 105, 2589-2600.
44. 44. Tsui, F.C., Sundberg, S.A. & Hubbell, W.L. (1990) Distribution of charge on photoreceptor disc membranes and implications for charged lipid asymmetry. Biophys. J. 57, 85-97.
45. 45. Hubbell, W.L. (1990) Transbilayer coupling mechanism for the formation of lipid asymmetry in biological membranes. Application to the photoreceptor disc membrane. Biophys. J. 57, 99-108.
46. 46. Reichert, J. & Hofmann, K.P. (1984) Sulfhydryl group modification of photoreceptor G-protein prevents its light-induced binding to rhodopsin. FEBS Lett. 168, 121-124.
47. 47. Hofmann, K.P. & Reichert, J. (1985) Chemical probing of the light-induced interaction between rhodopsin and G-protein. Near-infrared light-scattering and sulfhydryl modifications. J. biol. Chemistry 260, 7990-7995.
48. 48. Illing, M., Molday, L.L. & Molday, R.S. (1997) The 220-kDa rim protein of retinal rod outer segments is a member of the ABC transporter superfamily. J. Biol. Chem. 272, 10303-10310.
49. 49. Kornberg, R.D. & McConell, H.M. (1971) Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry 10, 1111-1120.
50. 50. Kahlert, M., Pepperberg, D.R. & Hofmann, K.P. (1990) Effect of bleached rhodopsin on signal amplification in rod visual receptors. Nature 345, 537-539.
51. 51. Körschen, H.G., Beyermann, M., Müller, F., Heck, M., Vantler, M., Koch, K.-W., Kellner, R., Wolfrum, U., Bode, C., Hofmann, K.P. & Kaupp, U.B. (1999) Interaction of glutamic-acid-rich proteins with the cGMP signalling pathway in rod photoreceptors. Nature 400, 761-766.