Advertisement

Role of Phospholipid Head Group Structure and Polarity in the Control of Membrane Fusion

  • Roger Sundler
Part of the Biomembranes book series (B, volume 12)

Abstract

Mammalian cell membranes fulfill a multiplicity of functions, some of which appear quite contrasting. For example, plasma membranes need to constitute a stable and reliable permeability barrier but they also engage in membrane fusion events, known as endo- and exocytosis. Several intracellular membrane structures, such as parts of the endoplasmic reticulum, the Golgi apparatus, lysosomes, and small transport vesicles, take part in similar fusion processes. Membrane fusion can only be understood as a destabilization of the membrane structure at restricted sites of in-termembrane contact, followed by creation and stabilization of new membrane continuities. The molecular details of these events are not yet understood, nor the role of individual membrane components (lipids or proteins).

Keywords

Head Group Membrane Fusion Phospholipid Vesicle Anionic Lipid Bilayer Vesicle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Akhtar, R. A., and Abdel-Latif, A. A., 1978, Studies on the properties of triphosphoinositide phosphomonoesterase and phosphodiesterase of rabbit iris smooth muscle, Biochim. Biophys. Acta 527:159.PubMedGoogle Scholar
  2. Allan, D., and Mitchell, R. H., 1978, A calcium-activated polyphosphoinositide phosphodiesterase in the plasma membrane of human and rabbit erythrocytes, Biochim. Biophys. Acta 508:277.PubMedCrossRefGoogle Scholar
  3. Bell, R. L., and Majerus, P. W., 1980, Thrombin-induced hydrolysis of phosphatidylinositol in human platelets. J. Biol. Chem. 255:1790.PubMedGoogle Scholar
  4. Bretscher, M. S., 1972, Phosphatidylethanolamine: Differential labelling in intact cells and cell ghosts of human erythrocytes by a membrane-impermeable reagent, J. Mol. Biol. 71:523.PubMedCrossRefGoogle Scholar
  5. Browning, J. L., and Seelig, J., 1980, Bilayers of phosphatidylserine: A deuterium and phosphorus nuclear magnetic resonance study, Biochemistry 19:1262.PubMedCrossRefGoogle Scholar
  6. Cevc, G., Watts, A., and Marsh, D., 1980, Non-electrostatic contribution to the titration of the ordered-fluid phase transition of phosphatidylglycerol bilayers, FEBS Lett. 120:267.PubMedCrossRefGoogle Scholar
  7. Cevc, G., Watts, A., and Marsh, D., 1981, Titration of the phase transition of phosphatidylserine bilayer membranes: Effects of pH, surface electrostatics, ion binding and head-group hydration, Biochemistry 20:4955.PubMedCrossRefGoogle Scholar
  8. Cockcroft, S., Bennet, J. P., and Gomperts, B. D., 1980, Stimulus-secretion coupling in rabbit neutrophils is not mediated by phosphatidylinositol breakdown, Nature (London) 288:275.CrossRefGoogle Scholar
  9. Cockcroft, S., Bennet, J. P., and Gomperts, B. D., 1981, The dependence on Ca2+ of phosphatidylinositol breakdown and enzyme secretion in rabbit neutrophils stimulated by formyl-methionyl-leucyl-phenylalanine or ionomycin, Biochem. J. 200:501.PubMedGoogle Scholar
  10. Colodzin, M., and Kennedy, E. P., 1965, Biosynthesis of diphosphoinositide in brain, J. Biol. Chem. 240:3771.PubMedGoogle Scholar
  11. Cooper, P. H., and Hawthorne, J. N., 1976, Phosphatidylinositol kinase and diphosphoinositide kinase in rat kidney cortex. Properties and subcellular localization, Biochem. J. 160:97.PubMedGoogle Scholar
  12. Cowley, A. C., Fuller, N. L., Rand, R. P., and Parsegian, V. A., 1978, Measurement of repulsive forces between charged phospholipid bilayers, Biochemistry 17:3163.PubMedCrossRefGoogle Scholar
  13. Cullis, P. R., and de Kruijff, B., 1979, Lipid polymorphism and the functional roles of lipids in biological membranes, Biochim. Biophys. Acta 559:399.PubMedGoogle Scholar
  14. Cullis, P. R., Verkleij, A. J., and Ververgaert, P. H. J. T., 1978, Polymorphic phase behaviour of cardiolipin as detected by 31P-NMR and freeze-fracture techniques: Effects of calcium dibucain and chlorpromazine, Biochim. Biophys. Acta 513:11.PubMedCrossRefGoogle Scholar
  15. Dawson, R. M. C, and Thompson, W., 1964, The triphosphoinositide phosphomonoesterase of brain tissue, Biochem. J. 91:244.PubMedGoogle Scholar
  16. Day, E. P., Kwok, A. Y. N., Hark, S. K., Ho, J. T., Vail, W. J., Bentz, J., and Nir, S., 1980, Reversibility of sodium-induced aggregation of sonicated phosphatidylserine vesicles, Proc. Natl. Acad. Sci. USA 77:4026.PubMedCrossRefGoogle Scholar
  17. Düzgünes, N., and Papahadjopoulos, D., Ionotropic effects on phospholipid membranes: Calcium/magnesium specificity in binding, fluidity and fusion, in: Membrane Fluidity in Biology, Vol. 1 (R. C. Aloia, ed.), Academic Press, New York.Google Scholar
  18. Düzgünes, N., Wilschut, J., Fraley, R., and Papahadjopoulos, D., 1981, Fusion of phospholipid vesicles by calcium and magnesium: Effect of membrane composition, Biochem. Biophys. Acta 642:182.PubMedCrossRefGoogle Scholar
  19. Eibl, H., 1977, Phospholipid bilayers: Influence of structure and charge, in: Polyunsaturated Fatty Acids (W. H. Kunau and R. T. Holman, eds.), pp. 229–244, American Oil Chemists Society, Champaign, Ill.Google Scholar
  20. Eibl, H., and Blume A., 1979, The influence of charge on phosphatidic acid bilayer membranes, Biochim. Biophys. Acta 553:476.PubMedCrossRefGoogle Scholar
  21. Eisenberg, M., Gresalf T., Riccio, T., and McLaughlin, S., 1979, Adsorption of monovalent cations to bilayer membranes containing negative phospholipids, Biochemistry 18:5213.PubMedCrossRefGoogle Scholar
  22. Emilsson, A., and Sundler, R., 1984, Differential activation of phosphatidylinositol deacylation and a pathway via diphosphoinositide in macrophages responding to zymosan and ionophore A23187, J. Biol. Chem. (in press).Google Scholar
  23. Farese, R. V., Larson, R. E., and Sabir, M. A., 1982, Ca2+-dependent and Ca2+-independent effects of pancreatic secretagogues on phosphatidylinositol metabolism, Biochem. Biophys. Acta 710:391.PubMedGoogle Scholar
  24. Finer, E. G., and Darke, A., 1974, Phospholipid hydration studied by deuteron magnetic resonance spectroscopy, Chem. Phys. Lipids 12:1.PubMedCrossRefGoogle Scholar
  25. Glaser, M., Ferguson, K. A., and Vagelos, P. R., 1974, Manipulation of the phospholipid composition of tissue culture cells, Proc. Natl. Acad. Sci. USA 71:4072.PubMedCrossRefGoogle Scholar
  26. Griffin, H. D., and Hawthorne, J. N., 1978, Calcium-activated hydrolysis of phosphatidyl-myo-inositol-4-phosphate and phosphatidyl-myo-inositol-4,5-biphosphate in guinea-pig synaptosomes, Biochem. J. 176:541.PubMedGoogle Scholar
  27. Hauser, H., 1975, in: Water: A Comprehensive Treatise, Vol. 4 (F. Franks, ed.), pp. 209–297, Plenum Press, New York.Google Scholar
  28. Hauser, H., Finer, E. G., and Darke, A., 1977, Crystalline anhydrous Ca-phosphatidylserine bilayers, Biochem. Biophys. Res. Commun. 76:267.CrossRefGoogle Scholar
  29. Hauser, H., Pascher, I., Pearson, R. H., and Sundell, S., 1981, Preferred conformation and molecular packing of phosphatidylethanolamine and phosphatidylcholine, Biochim. Biophys. Acta 650:21.PubMedGoogle Scholar
  30. Hendrickson, H. S., 1969, Physical properties and interactions of phosphoinositides, Ann. N. Y. Acad. Sci. 165:668.PubMedGoogle Scholar
  31. Hitchcock, P. B., Mason, R., Thomas, K. M., and Shipley, G. G., 1974, Structural chemistry of 1,2-dilauroyl-DL-phosphatidylethanolamine: Molecular conformation and intermolecular packing of phospholipids, Proc. Natl. Acad. Sci. USA 71:3036.PubMedCrossRefGoogle Scholar
  32. Hokin-Neaverson, M., 1974, Acetylcholine causes a net decrease in phosphatidylinositol and a net increase in phosphatidic acid in mouse pancreas, Biochem. Biophys. Res. Commun. 58:763.PubMedCrossRefGoogle Scholar
  33. Irvine, R. F., 1982, How is the level of free arachidonic acid controlled in mammalian cells?, Biochem. J. 204:3.PubMedGoogle Scholar
  34. Israelachvili, J. N., Marcelja, S., and Horn, R. G., 1980, Physical principles of membrane organization, Q. Rev. Biophys. 13:121.PubMedCrossRefGoogle Scholar
  35. Jacobson, K., and Papahadjopoulos, D., 1975, Phase transition and phase separations in phos-pholipid membranes induced by changes in temperature, pH and concentration of bivalent cations, Biochemistry 14:152.PubMedCrossRefGoogle Scholar
  36. Jendrasiak, G. L., and Hasty, J. H., 1974, The hydration of phospholipids, Biochim. Biophys. Acta 337:79.PubMedGoogle Scholar
  37. Jergil, B., and Sundler, R., 1983, Phosphorylation of phosphatidylinositol in rat liver Golgi, J. Biol. Chem. 258:7968.PubMedGoogle Scholar
  38. Jolies, J., Zwiers, H., van Dongen, C. J., Schotman, P., Wirtz, K. W. A., and Gispen, W. H., 1980, Modulation of brain polyphosphoinositide metabolism by ACTH-sensitive protein phosphorylation, Nature (London) 286:623.CrossRefGoogle Scholar
  39. Kai, M., Salway, J. G., and Hawthorne, J. N., 1968, The diphosphoinositide kinase of rat brain, Biochem. J. 106:791.PubMedGoogle Scholar
  40. Kurland, R. J., Hammoudah, M., Nir, S., and Papahadjopoulos, D., 1979, Binding of Ca2+ and Mg2+ to phosphatidylserine vesicles: Different effects on 31P-NMR shifts and relaxation times, Biochem. Biophys. Res. Commun. 88:927.PubMedCrossRefGoogle Scholar
  41. Ladbrooke, B. D., and Chapman, D., 1969, Thermal analysis of lipids, proteins and biological membranes: A review and summary of some recent studies, Chem. Phys. Lipids 3:304.PubMedCrossRefGoogle Scholar
  42. Lapetina, E. G., and Cuatrecasas, P., 1979, Stimulation of phosphatidic acid production in platelets precedes the formation of arachidonate and parallels the release of serotonin, Biochim. Biophys. Acta 573:394.PubMedGoogle Scholar
  43. Lau, A., and McLaughlin, S., 1981, The adsorption of divalent cations to phosphatidylglycerol bilayer membranes, Biochim. Biophys. Acta 645:279.PubMedCrossRefGoogle Scholar
  44. Lis, L. J., Lis, W. T., Parsegian, V. A., and Rand, R. P., 1981, Adsorption of divalent cations to a variety of phosphatidylcholine bilayers, Biochemistry 20:1771.PubMedCrossRefGoogle Scholar
  45. MacDonald, R. C., Simon, S. A., and Baer, E., 1976, Ionic influences on the phase transition of dipalmitoyl phosphatidylserine, Biochemistry 15:885.PubMedCrossRefGoogle Scholar
  46. McGill, K. A., Bennet, J. P., Smith, G. A., Plumb, R. W., and Warren, G. B., 1981, Transbilayer distribution of lipids in a population of sarcoplasmic-reticulum vesicles sealed with their cytoplasmic side outwards, Biochem. J. 195:287.PubMedGoogle Scholar
  47. McLaughlin, A., Grathwohl, C., and McLaughlin, S., 1978, The adsorption of divalent cations to phosphatidylcholine bilayer membranes, Biochim. Biophys. Acta 513:338.PubMedCrossRefGoogle Scholar
  48. Miller, C., and Racker, E., 1976, Fusion of phospholipid vesicles reconstituted with cytochrome oxidase and mitochondrial hydrophobic protein, J. Membr. Biol. 26:319.PubMedCrossRefGoogle Scholar
  49. Mitchell, R. H., 1975, Inositol phospholipids and cell surface receptor function, Biochim. Biophys. Acta 415:81.Google Scholar
  50. Mitchell, R. H., 1982, Is phosphatidylinositol really out of the calcium gate?, Nature (London) 296:492.CrossRefGoogle Scholar
  51. Mitchell, R. H., Harwood, J. L., Coleman, R., and Hawthorne, J. N., 1967, Characteristics of rat liver phosphatidylinositol kinase and its presence in the plasma membrane, Biochim. Biophys. Acta 144:649.Google Scholar
  52. Niijar, M. S., and Hawthorne, J. N., 1977, Purification and properties of polyphosphoinositide phosphomonoesterase from rat brain, Biochim. Biophys. Acta 480:390.Google Scholar
  53. Op den Kamp, J. A. F., 1979, Lipid asymmetry in membranes, Annu. Rev. Biochem. 48:47.PubMedCrossRefGoogle Scholar
  54. Papahadjopoulos, D., 1968, Surface properties of acidic phospholipids: Interaction of mono-layers and hydrated liquid crystals with uni-and bi-valent metal ions, Biochim. Biophys. Acta 163:240.PubMedCrossRefGoogle Scholar
  55. Papahadjopoulos, D., Vail, W. J., Jacobson, K., and Poste, G., 1975, Cochleate lipid cylinders: Formation by fusion of unilamellar vesicles, Biochim. Biophys. Acta 394:483.PubMedCrossRefGoogle Scholar
  56. Papahadjopoulos, D., Vail, W. J., Pangborn, W. A., and Poste, G., 1976, Studies on membrane fusion. II. Induction of fusion in pure phospholipid membranes by calcium ions and other divalent metals, Biochim. Biophys. Acta 448:265.PubMedCrossRefGoogle Scholar
  57. Pearson, R. H., and Pascher, I., 1979, The molecular structure of lecithin dihydrate, Nature (London) 281:499.CrossRefGoogle Scholar
  58. Phillips, J. H., 1973, Phosphatidylinositol kinase: A component of the chromaffin-granule membrane, Biochem. J. 136:579.PubMedGoogle Scholar
  59. Portis, A., Newton, C., Pangborn, W., and Papahadjopoulos, D., 1979, Studies on the mechanism of membrane fusion: Evidence for an inter-membrane Ca2+-phospholipid complex, synergism with Mg2+ and inhibition by spectrin, Biochemistry 18:780.PubMedCrossRefGoogle Scholar
  60. Rand, R. P., 1981, Interacting phospholipid bilayers: Measured forces and induced structural changes, Annu. Rev. Biophys. Bioeng. 10:277.PubMedCrossRefGoogle Scholar
  61. Rand, R. P., and Sengupta, S., 1972, Cardiolipid forms hexagonal structures with divalent cations, Biochim. Biophys. Acta 255:484.PubMedCrossRefGoogle Scholar
  62. Schroeder, F., Perlmutter, J. F., Glaser, M., and Vagelos, P. R., 1976, Isolation and characterization of subcellular membranes with altered phospholipid composition from cultured fibroblasts, J. Biol. Chem. 251:5015.PubMedGoogle Scholar
  63. Seelig, J., 1978, 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes, Biochim. Biophys. Acta 515:105.PubMedGoogle Scholar
  64. Small, D. M., 1967, Phase equilibria and structure of dry and hydrated egg lecithin, J. Lipid Res. 8:551.PubMedGoogle Scholar
  65. Sugiura, Y., 1981, Structure of molecular aggregates of 1-(3-sn-phosphatidyl)-l-myo-inositol-3,4-bis(phosphate) in water, Biochim. Biophys. Acta 641:148.PubMedCrossRefGoogle Scholar
  66. Sundler, R., 1982, Agglutination of glycolipid-phospholipid vesicles by concanavalin A: Evidence for steric modulation of lectin binding by phospholipid head groups, FEBS Lett. 141:11.CrossRefGoogle Scholar
  67. Sundler, R., 1984, Studies on the effective size of phospholipid head groups in bilayer vesicles using lectin-glycolipid interaction as a steric probe, Biochim. Biophys. Acta. (in press).Google Scholar
  68. Sundler, R., Sarcione, S. L., Alberts, A. W., and Vagelos, P. R., 1977, Evidence against phospholipid asymmetry in intracellular membranes from liver, Proc. Natl. Acad. Sci. USA 74:3350.PubMedCrossRefGoogle Scholar
  69. Sundler, R., and Papahadjopoulos, D., 1981, Control of membrane fusion by phospholipid head groups. I. Phophatidate/phosphatidylinositol specificity, Biochim. Biophys. Acta 649:743.PubMedCrossRefGoogle Scholar
  70. Sundler, R., Düzgünes, N., and Papahadjopoulos, D., 1981, Control of membrane fusion by phospholipid head groups. II. The role of phophatidylethanolamine in mixtures with phos-phatidate and phosphatidylinositol, Biochim. Biophys. Acta 649:751.PubMedCrossRefGoogle Scholar
  71. Sundler, R., and Wijkander, J., 1983, Protein-mediated intermembrane contact specifically enhances Ca2+-induced fusion of phosphatidate-containing membranes, Biochem. Biophys. Acta 730:391.PubMedCrossRefGoogle Scholar
  72. Thompson, W., and Dawson, R. M. C, 1964, The triphosphoinositide phosphodiesterase of brain tissue, Biochem. J. 91:237.PubMedGoogle Scholar
  73. Tocanne, J. F., Ververgaert, P. H. J. T., Verkleij, A. J., and van Deenen, L. L. M., 1974, A monolayer and freeze-etching study of charged phospholipids. I. Effects of ions and pH on the ionic properties of phosphatidylglycerol and lysylphosphatidylglycerol, Chem. Phys. Lipids 12:201.PubMedCrossRefGoogle Scholar
  74. Träuble, H., and Eibl, H., 1975, Molecular interactions in lipid bilayers: Cooperative structural changes in lipid bilayers, in: Functional Linkage in Biomolecular Systems (F. O. Schmitt, D. M. Schneider, and D. M. Crothers, eds.), pp. 59–101, Raven Press, New York.Google Scholar
  75. van Dijck, P. W. M., de Kruijff, B., Verkleij, A. J., van Deenen, L. L. M., and de Gier, J., 1978, Comparative studies on the effects of pH and Ca2+ on bilayers of various negatively charged phospholipids and their mixtures with phosphatidylcholine, Biochim. Biophys. Acta 512:84.PubMedCrossRefGoogle Scholar
  76. Verkleij, A. J., Zwaal, R. F. A., Roelofsen, B., Comfurius, P., Kastelijn, D., and van Deenen, L. L. M., 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.PubMedCrossRefGoogle Scholar
  77. Verkleij, A. J., Mombers, C., Gerritsen, W. J., Leunissen-Bijvelt, L., and Cullis, P. R., 1979, Fusion of phospholipid vesicles in association with the appearance of lipidic particles as visualized by freeze fracturing, Biochim. Biophys. Acta 555:358.PubMedCrossRefGoogle Scholar
  78. Verkleij, A. J., van Echteld, C. J. A., Gerritsen, W. J., Cullis, P. R., and de Kruijff, B., 1980, The lipidic particle as an intermediate in membrane fusion processes and bilayer to hexagonal HII transitions, Biochim. Biophys. Acta 600:620.PubMedCrossRefGoogle Scholar
  79. Wilschut, J., Düzgünes, N., Fraley, R., and Papahadjopoulos, D., 1980, Studies on the mechanism of membrane fusion: Kinetics of Ca2+-induced fusion of phosphatidylserine vesicles studied by a fluorescence assay for the intermixing of vesicle contents, Biochemistry 19:6011.PubMedCrossRefGoogle Scholar
  80. Wilschut, J., Düzgünes, N., and Papahadjopoulos, D., 1981, Calcium/magnesium specificity in membrane fusion: Kinetics of aggregation and fusion of phosphatidylserine vesicles and the role of bilayer curvature, Biochemistry 20:3126.PubMedCrossRefGoogle Scholar
  81. Wohlgemuth, R., Waespe-Šarǐevic, N., and Seelig, J., 1980, Bilayers of phosphatidylglycerol: A deuterium and phosphorous nuclear magnetic resonance study of the head group region, Biochemistry 19:3315.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Roger Sundler
    • 1
  1. 1.Department of Physiological ChemistryUniversity of LundLundSweden

Personalised recommendations