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. 1977 Aug 15;166(2):255–263. doi: 10.1042/bj1660255

Membrane cholesterol and cell fusion of hen and guinea-pig erythrocytes.

M J Hope, K R Bruckdorfer, C A Hart, J A Lucy
PMCID: PMC1165002  PMID: 199160

Abstract

1. The cholesterol content of hen erythrocytes was modified by treating the cells with phospholipid liposomes. 2. Depletion of cellular cholesterol, by using liposomes of dipalmitoylglycerophosphocholine or phosphatidylcholine from hen erythrocytes, had no effect on the susceptibility of the cells to fusion induced by oleoylglycerol, but markedly decreased fusion induced by Sendai virus. 3. By contrast, enrichment of cellular cholesterol by using liposomes of dipalmitoylglycerophosphocholine and cholesterol increased cell fusion induced by oleoylglycerol, poly(ethylene glycol) and Sendai virus. 4. Virus-induced cell fusion of guinea-pig erythrocytes, which were enriched in cholesterol by feeding a cholesterol-rich diet to the animals, was also enhanced. 5. Hen erythrocytes that were treated with liposomes prepared from egg phosphatidylcholine contained increased quantities of phospholipid phosphorus and fused readily on incubation with retinol, independently of their cholesterol content. 6. It is suggested that cholesterol may enhance cell fusion by acting to facilitate a phase separation of protein-free areas of lipid bilayer, which subsequently provide the sites for cell fusion.

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Selected References

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  1. Ahkong Q. F., Fisher D., Tampion W., Lucy J. A. Mechanisms of cell fusion. Nature. 1975 Jan 17;253(5488):194–195. doi: 10.1038/253194a0. [DOI] [PubMed] [Google Scholar]
  2. Ahkong Q. F., Fisher D., Tampion W., Lucy J. A. The fusion of erythrocytes by fatty acids, esters, retinol and alpha-tocopherol. Biochem J. 1973 Sep;136(1):147–155. doi: 10.1042/bj1360147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Breisblatt W., Ohki S. Fusion in phospholipid spherical membranes. II. Effect of cholesterol, divalent ions and pH. J Membr Biol. 1976 Oct 20;29(1-2):127–146. doi: 10.1007/BF01868956. [DOI] [PubMed] [Google Scholar]
  4. Bruckdorfer K. R., Demel R. A., De Gier J., van Deenen L. L. The effect of partial replacements of membrane cholesterol by other steroids on the osmotic fragility and glycerol permeability of erythrocytes. Biochim Biophys Acta. 1969 Jul 15;183(2):334–345. doi: 10.1016/0005-2736(69)90089-3. [DOI] [PubMed] [Google Scholar]
  5. Bruckdorfer K. R., Edwards P. A., Green C. Properties of aqueous dispersions of phospholipid and cholesterol. Eur J Biochem. 1968 May;4(4):506–511. doi: 10.1111/j.1432-1033.1968.tb00241.x. [DOI] [PubMed] [Google Scholar]
  6. Brûlet P., McConnell H. M. Lateral hapten mobility and immunochemistry of model membranes. Proc Natl Acad Sci U S A. 1976 Sep;73(9):2977–2981. doi: 10.1073/pnas.73.9.2977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cooper R. A., Arner E. C., Wiley J. S., Shattil S. J. Modification of red cell membrane structure by cholesterol-rich lipid dispersions. A model for the primary spur cell defect. J Clin Invest. 1975 Jan;55(1):115–126. doi: 10.1172/JCI107901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. DINGLE J. T., LUCY J. A. Studies on the mode of action of excess of vitamin A. 5. The effect of vitamin A on the stability of the erythrocyte membrane. Biochem J. 1962 Sep;84:611–621. doi: 10.1042/bj0840611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deuticke B., Ruska C. Changes of nonelectrolyte permeability in cholesterol-loaded erythrocytes. Biochim Biophys Acta. 1976 May 21;433(3):638–653. doi: 10.1016/0005-2736(76)90287-x. [DOI] [PubMed] [Google Scholar]
  10. FOLCH J., LEES M., SLOANE STANLEY G. H. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957 May;226(1):497–509. [PubMed] [Google Scholar]
  11. Finean J. B. Cholesterol: lecithin association at molecular ratios of up to 2 : 1. Chem Phys Lipids. 1975 Aug;14(4):313–320. doi: 10.1016/0009-3084(75)90067-5. [DOI] [PubMed] [Google Scholar]
  12. Fisher K. A. Analysis of membrane halves: cholesterol. Proc Natl Acad Sci U S A. 1976 Jan;73(1):173–177. doi: 10.1073/pnas.73.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grunze M., Deuticke B. Changes of membrane permeability due to extensive cholesterol depletion in mammalian erythrocytes. Biochim Biophys Acta. 1974 Jul 12;356(1):125–130. doi: 10.1016/0005-2736(74)90300-9. [DOI] [PubMed] [Google Scholar]
  14. Hart C. A., Fisher D., Hallinan T., Lucy J. A. Effects of calcium ions and the bivalent cation ionophore A23187 on the agglutination and fusion of chicken erythrocytes by Sendai virus. Biochem J. 1976 Jul 15;158(1):141–145. doi: 10.1042/bj1580141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Heiniger H. J., Kandutsch A. A., Chen H. W. Depletion of L-cell sterol depresses endocytosis. Nature. 1976 Oct 7;263(5577):515–517. doi: 10.1038/263515a0. [DOI] [PubMed] [Google Scholar]
  16. Kleemann W., McConnell H. M. Interactions of proteins and cholesterol with lipids in bilayer membranes. Biochim Biophys Acta. 1976 Jan 21;419(2):206–222. doi: 10.1016/0005-2736(76)90347-3. [DOI] [PubMed] [Google Scholar]
  17. Kosower N. S., Kosower E. M., Wegman P. Membrane mobility agents. II. Active promoters of cell fusion. Biochim Biophys Acta. 1975 Sep 2;401(3):530–534. doi: 10.1016/0005-2736(75)90250-3. [DOI] [PubMed] [Google Scholar]
  18. Kroes J., Ostwald R. Erythrocyte membranes--effect of increased cholesterol content on permeability. Biochim Biophys Acta. 1971 Dec 3;249(2):647–650. doi: 10.1016/0005-2736(71)90147-7. [DOI] [PubMed] [Google Scholar]
  19. Kroes J., Ostwald R., Keith A. Erythrocyte membranes--compression of lipid phases by increased cholesterol content. Biochim Biophys Acta. 1972 Jul 3;274(1):71–74. doi: 10.1016/0005-2736(72)90281-7. [DOI] [PubMed] [Google Scholar]
  20. Lucy J. A. Lipids and membranes. FEBS Lett. 1974 Mar 23;40(0):suppl–suppl:S111. doi: 10.1016/0014-5793(74)80692-7. [DOI] [PubMed] [Google Scholar]
  21. Lyman G. H., Preisler H. D., Papahadjopoulos D. Membrane action of DMSO and other chemical inducers of Friend leukaemic cell differentiation. Nature. 1976 Jul 29;262(5567):361–363. doi: 10.1038/262360a0. [DOI] [PubMed] [Google Scholar]
  22. Maggio B., Ahkong Q. F., Lucy J. A. Poly(ethylene glycol), surface potential and cell fusion. Biochem J. 1976 Sep 15;158(3):647–650. doi: 10.1042/bj1580647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maggio B., Lucy J. A. Studies on mixed monolayers of phospholipids and fusogenic lipids. Biochem J. 1975 Sep;149(3):597–608. doi: 10.1042/bj1490597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McIntyre J. A., Gilula N. B., Karnovsky M. J. Cryoprotectant-induced redistribution of intramembranous particles in mouse lymphocytes. J Cell Biol. 1974 Jan;60(1):192–203. doi: 10.1083/jcb.60.1.192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Papahadjopoulos D., Hui S., Vail W. J., Poste G. Studies on membrane fusion. I. Interactions of pure phospholipid membranes and the effect of myristic acid, lysolecithin, proteins and dimethylsulfoxide. Biochim Biophys Acta. 1976 Oct 5;448(2):254–264. [PubMed] [Google Scholar]
  26. Papahadjopoulos D., Poste G., Schaeffer B. E. Fusion of mammalian cells by unilamellar lipid vesicles: inflluence of lipid surface charge, fluidity and cholesterol. Biochim Biophys Acta. 1973 Sep 27;323(1):23–42. doi: 10.1016/0005-2736(73)90429-x. [DOI] [PubMed] [Google Scholar]
  27. Papahadjopoulos D., Poste G., Schaeffer B. E., Vail W. J. Membrane fusion and molecular segregation in phospholipid vesicles. Biochim Biophys Acta. 1974 May 30;352(1):10–28. doi: 10.1016/0005-2736(74)90175-8. [DOI] [PubMed] [Google Scholar]
  28. Papahadjopoulos D., Vail W. J., Pangborn W. A., Poste G. Studies on membrane fusion. II. Induction of fusion in pure phospholipid membranes by calcium ions and other divalent metals. Biochim Biophys Acta. 1976 Oct 5;448(2):265–283. doi: 10.1016/0005-2736(76)90241-8. [DOI] [PubMed] [Google Scholar]
  29. Poste G., Reeve P., Alexander D. J., Terry G. Effect of plasma membrane lipid composition on cellular susceptibility to virus-induced cell fusion. J Gen Virol. 1972 Oct;17(1):133–136. doi: 10.1099/0022-1317-17-1-133. [DOI] [PubMed] [Google Scholar]
  30. ROSE H. G., OKLANDER M. IMPROVED PROCEDURE FOR THE EXTRACTION OF LIPIDS FROM HUMAN ERYTHROCYTES. J Lipid Res. 1965 Jul;6:428–431. [PubMed] [Google Scholar]
  31. Raheja R. K., Kaur C., Singh A., Bhatia I. S. New colorimetric method for the quantitative estimation of phospholipids without acid digestion. J Lipid Res. 1973 Nov;14(6):695–697. [PubMed] [Google Scholar]
  32. Rudel L. L., Morris M. D. Determination of cholesterol using o-phthalaldehyde. J Lipid Res. 1973 May;14(3):364–366. [PubMed] [Google Scholar]
  33. Tanaka K. I., Ohnishi S. Heterogeneity in the fluidity of intact erythrocyte membrane and its homogenization upon hemolysis. Biochim Biophys Acta. 1976 Mar 5;426(2):218–231. doi: 10.1016/0005-2736(76)90333-3. [DOI] [PubMed] [Google Scholar]
  34. Vanderkooi J., Fischkoff S., Chance B., Cooper R. A. Fluorescent probe analysis of the lipid architecture of natural and experimental cholesterol-rich membranes. Biochemistry. 1974 Apr 9;13(8):1589–1595. doi: 10.1021/bi00705a006. [DOI] [PubMed] [Google Scholar]
  35. Verkleij A. J., Nauta I. L., Werre J. M., Mandersloot J. G., Reinders B., Ververgaert P. H., de Gier J. The fusion of abnormal plasma lipoprotein (LP-X) and the erythrocyte membrane in patients with cholestasis studied by electronmicroscopy. Biochim Biophys Acta. 1976 Jun 17;436(2):366–376. doi: 10.1016/0005-2736(76)90200-5. [DOI] [PubMed] [Google Scholar]
  36. WARREN L. The thiobarbituric acid assay of sialic acids. J Biol Chem. 1959 Aug;234(8):1971–1975. [PubMed] [Google Scholar]
  37. Zentgraf H., Deumling B., Jarasch E. D., Franke W. W. Nuclear membranes and plasma membranes from hen erythrocytes. I. Isolation, characterization, and comparison. J Biol Chem. 1971 May 10;246(9):2986–2995. [PubMed] [Google Scholar]
  38. van der Bosch J., Schudt C., Pette D. Influence of temperature, cholesterol, dipalmitoyllecithin and Ca2+ on the rate of muscle cell fusion. Exp Cell Res. 1973 Dec;82(2):433–438. doi: 10.1016/0014-4827(73)90362-5. [DOI] [PubMed] [Google Scholar]

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