Transbilayer Coupling Mechanism for the Formation of Lipid Asymmetry in Biological Membranes. Application to the Photoreceptor Disc Membrane

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 1990 Jan 1

PMID 2297564

Citations 15

Authors

W L Hubbell

Affiliations

Soon will be listed here.

Abstract

An equilibrium transmembrane asymmetry in charged lipids is shown to arise as a result of oriented, bipolar proteins in the membrane. The basic interaction giving rise to the asymmetry is between a lipid molecule and a transbilayer potential generated by the asymmetric charge distribution in the protein. Thus, a protein can generate a lipid asymmetry without a direct binding interaction between lipid and protein. The generation of an asymmetry in charged lipid by this mechanism can also lead to a concomitant asymmetry in neutral lipids if deviations from ideality in the lipid mixture are taken into account. It is shown that regular solution theory applied to the lipid phase predicts an asymmetry in all components of a ternary mixture as long as one component is electrostatically oriented according to the mechanism mentioned above. The resulting asymmetry is not strongly salt dependent. The mechanism quantitatively accounts for the experimentally determined phospholipid asymmetry in the rod outer segment disc membrane of the vertebrate photoreceptor.

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References

McLaughlin S, Harary H . Phospholipid flip-flop and the distribution of surface charges in excitable membranes. Biophys J. 1974; 14(3):200-8. PMC: 1334495. DOI: 10.1016/S0006-3495(74)85907-2. View

Blume A, Ackermann T . A calorimetric study of the lipid phase transitions in aqueous dispersions of phosphorylcholine--phosphorylethanolamine mixtures. FEBS Lett. 1974; 43(1):71-4. DOI: 10.1016/0014-5793(74)81108-7. View

McConnell H . Phase separations in phospholipd membranes. Biochemistry. 1975; 14(4):847-54. DOI: 10.1021/bi00675a032. View

Chabre M, Cavaggioni A . X-ray diffraction studies of retinal rods. II. Light effect on the osmotic properties. Biochim Biophys Acta. 1975; 382(3):336-43. DOI: 10.1016/0005-2736(75)90275-8. View

Castle J, Hubbell W . Estimation of membrane surface potential and charge density from the phase equilibrium of a paramagnetic amphiphile. Biochemistry. 1976; 15(22):4818-31. DOI: 10.1021/bi00667a011. View

McQuarrie D, Mulas P . Asymmetric charge distributions in planar bilayer systems. Biophys J. 1977; 17(2):103-9. PMC: 1473464. DOI: 10.1016/S0006-3495(77)85629-4. View

Smith Jr H, Fager R, Litman R . Light-activated calcium release from sonicated bovine retinal rod outer segment disks. Biochemistry. 1977; 16(7):1399-405. DOI: 10.1021/bi00626a025. View

Luna E, McConnell H . Lateral phase separations in binary mixtures of phospholipids having different charges and different crystalline structures. Biochim Biophys Acta. 1977; 470(2):303-16. DOI: 10.1016/0005-2736(77)90108-0. View

Lee A . Lipid phase transitions and phase diagrams. II. Mictures involving lipids. Biochim Biophys Acta. 1977; 472(3-4):285-344. DOI: 10.1016/0304-4157(77)90001-6. View

10.

van Zoelen E, de Kruijff B, Van Deenen L . Protein-mediated transbilayer movement of lysophosphatidylcholine in glycophorin-containing vesicles. Biochim Biophys Acta. 1978; 508(1):97-108. DOI: 10.1016/0005-2736(78)90191-8. View

11.

Crain R, Marinetti G, OBrien D . Topology of amino phospholipids in bovine retinal rod outer segment disk membranes. Biochemistry. 1978; 17(20):4186-92. DOI: 10.1021/bi00613a012. View

12.

Shimshick E, McConnell H . Lateral phase separation in phospholipid membranes. Biochemistry. 1973; 12(12):2351-60. DOI: 10.1021/bi00736a026. View

13.

Chapman D, Urbina J . Biomembrane phase transitions. Studies of lipid-water systems using differential scanning calorimetry. J Biol Chem. 1974; 249(8):2512-21. View

14.

Sklar L, Miljanich G, Dratz E . Phospholipid lateral phase separation and the partition of cis-parinaric acid and trans-parinaric acid among aqueous, solid lipid, and fluid lipid phases. Biochemistry. 1979; 18(9):1707-16. DOI: 10.1021/bi00576a012. View

15.

Op den Kamp J . Lipid asymmetry in membranes. Annu Rev Biochem. 1979; 48:47-71. DOI: 10.1146/annurev.bi.48.070179.000403. View

16.

Stewart T, Hui S, Portis Jr A, Papahadjopoulos D . Complex phase mixing of phosphatidylcholine and phosphatidylserine in multilamellar membrane vesicles. Biochim Biophys Acta. 1979; 556(1):1-16. DOI: 10.1016/0005-2736(79)90415-2. View

17.

Eisenberg M, Gresalfi T, Riccio T, McLaughlin S . Adsorption of monovalent cations to bilayer membranes containing negative phospholipids. Biochemistry. 1979; 18(23):5213-23. DOI: 10.1021/bi00590a028. View

18.

Watts A, Volotovski I, Marsh D . Rhodopsin-lipid associations in bovine rod outer segment membranes. Identification of immobilized lipid by spin-labels. Biochemistry. 1979; 18(22):5006-13. DOI: 10.1021/bi00589a031. View

19.

Sklar L, Dratz E . Analysis of membrane bilayer asymmetry using parinaric acid fluorescent probes. FEBS Lett. 1980; 118(2):308-10. DOI: 10.1016/0014-5793(80)80245-6. View

20.

Drenthe E, Bonting S, Daemen F . Transbilayer distribution of phospholipids in photoreceptor membrane studied with various phospholipases. Biochim Biophys Acta. 1980; 603(1):117-29. DOI: 10.1016/0005-2736(80)90395-8. View