Evidence for the extended phospholipid conformation in membrane fusion and hemifusion

Biophysical Journal

Volumn 76, Issue 4, 1999, Pages 2111-2120

  Holopainen, Juha M ^a   Lehtonen, Jukka Y A ^a   Kinnunen, Paavo K J ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

1,6 DIPHENYL 1,3,5 HEXATRIENE; CALCIUM; DIOLEOYLPHOSPHATIDIC ACID; LIPOSOME; MAGNESIUM; PHOSPHOLIPID; PHOSPHORYLCHOLINE;

ARTICLE; CONFORMATION; FLUORESCENCE SPECTROSCOPY; HYDROPHOBICITY; LIPID BILAYER; MEMBRANE FUSION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PHOSPHOLIPID VESICLE; POLARIZATION; STOICHIOMETRY;

EID: 0033024295     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77367-4     Document Type: Article

References (88)

1. Abrams, F. S., and E. London. 1993. Extension of parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescent quenching by a spin-label attached to the phospholipid polar headgroup. Biochemistry. 32:10826-10831.
2. Arnold, K. 1995. Cation-induced vesicle fusion modulated by polymers and proteins. In Handbook of Biological Physics, Vol. 1. R. Lipowsky and E. Sackmann, editors. Elsevier Science, Amsterdam. 903-957.
3. Bartlett, D., M. Glaser, and R. Welti. 1997. Membrane penetration depth and lipid phase preference of acyl-labeled dansyl phosphatidylcholines in phosphatidylcholine vesicles. Biochim. Biophys. Acta. 1328:48-54.
4. Ben-Shaul, A., I. Szleifer, and W. M. Gelbart. 1984. Statistical thermodynamics of amphiphile chains in micelles. Proc. Natl Acad. Sci. U.S.A. 81:4601-4605.
5. Bondi, A. 1954. Free volumes and free rotation in simple liquids and liquid saturated hydrocarbons. J. Phys. Chem. 58:929-939.
6. Cantor, R. S. 1997. Lateral pressure profile in cell membranes: a mechanism for modulation of protein function. J. Phys. Chem. 101:1723-1725.
7. Chattopadya, A., and E. London. 1987. Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry. 26:39-45.
8. Chernomordik, L. 1996. Non-bilayer lipids and biological fusion intermediates. Chem. Phys. Lipids. 81:203-213
9. Chernomordik, L., A. Chanturiya, J. Green, and J. Zimmerberg. 1995. The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition. Biophys. J. 69:922-929.
10. Chernomordik, L., E. Leikina, V. Frolov, P. Bronk, and J. Zimmerberg. 1997. An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids. J. Cell Biol. 136:81-93.
11. Chernomordik, L. V., G. B. Melikyan, and Y. A. Chizmadzhev. 1987. Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim. Biophys. Acta. 906: 309-352.
12. Creutz, C. E. 1992. The annexins and exocytosis. Science. 258:924-931
13. Dimitrov, D. S. 1995. Electroporation and electrofusion of membranes. In Handbook of Biological Physics, Vol. 1. R. Lipowsky and E. Sackmann, editors. Elsevier Science, Amsterdam. 851-901
14. Duportail, G., and P. Lianos. 1996. Fluorescence probing of vesicles using pyrene and pyrene derivatives. In Vesicles. M. Rosoff, editor. Marcel Dekker, New York. 295-372.
15. Duzgünes, N., K. Hong, P. A. Baldwin, J. Bentz, S. Nir, and D. Papahadjopoulos. 1987. Fusion of phospholipid vesicles induced by divalent cations and protons. In Cell Fusion. A. E. Sowers, editor. Plenum Press, New York. 241-267.
16. Eklund, K., J. A. Virtanen, P. K. J. Kinnunen, J. Kasurinen, and P. J. Somerharju. 1992. Conformation of phosphatidylcholine in neat and cholesterol-containing liquid-crystalline bilayers: application of a novel method. Biochemistry. 31:8560-8565.
17. 2+-induced lateral phase separation in phosphatidic acid/phosphatidylcholine monolayers as revealed by fluorescence microscopy. Biochemistry. 27:3433-3437.
18. II phase transition. Biochemistry. 25:4141-4147.
19. Ellens, H., D. P. Siegel, D. Alford, P. L. Yeagle, L. Boni, L. J. Lis, P. J. Quinn, and J. Bentz. 1989. Membrane fusion and inverted phases. Biochemistry. 28:3692-3703.
20. Epand, R. F., R. Kraayenhof, G. J. Sterk, H. W. Wong Fong Sang, and R. M. Epand. 1996. Fluorescent probes of membrane surface properties. Biochim. Biophys. Acta. 1284:191-195.
21. 2H-NMR study. Biochem. Biophys. Res. Commun. 111:675-682.
22. Förster, T. 1969. Excimers. Angew. Chem. Int. Ed. 8:333-343.
23. Galla, H.-J., and W. Hartmann. 1980. Excimer-forming lipids in membrane research. Chem. Phys. Lipids. 27:199-219.
24. Galla, H.-J., W. Hartmann, U. Theilen, and E. Sackmann. 1979. On two dimensional passive random walk in lipid bilayers and fluid pathways in biomembranes. J. Membr. Biol 48:215-236.
25. Galla, H.-J., and E. Sackmann. 1974. Lateral diffusion in the hydrophobic region of membranes: use of pyrene excimers as optical probes. Biochim. Biophys. Acta. 339:103-115.
26. Gruner, S. M. 1985. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. Proc. Natl. Acad. Sci. U.S.A. 82:3665-3669.
27. Gruner, S. M. 1989. Stability of lyotropic phases with curved interphases. J. Phys. Chem. 93:7562-7570.
28. Hauser, H., W. Guyer, I. Pascher, P. Skrabal, and S. Sundell. 1980. Polar group conformation of phosphatidylcholine: effects of solvent and aggregation. Biochemistry. 19:366-373.
29. Hauser, H., I. Pascher, and S. Sundell. 1988. Preferred conformation and dynamics of the glycerol backbone in phospholipids: an NMR and x-ray single-crystal analysis. Biochemistry. 27:9166-9174.
30. Helm, C. A., J. N. Israelachvili, and P. M. McGuiggan. 1992. Role of hydrophobic forces in bilayer adhesion and fusion. Biochemistry. 31: 1794-1805.
31. Hoekstra, D. 1990. Membrane fusion of enveloped viruses: especially a matter of proteins. J. Bioenerg. Biomembr. 22:121-155
32. Hong, K., N. Düzgunes, R. Ekerdt, and D. Papahadjopoulos. 1982. Synexin facilitates fusion of specific phospholipid membranes at divalent cation concentrations found intracellularly. Proc. Natl. Acad. Sci. U.S.A. 79: 4642-4644.
33. Hresko, R. C., I. P. Sugár, Y. Barenholz, and T. E. Thompson. 1986. Lateral distribution of a pyrene-labeled phosphatidylcholine in phosphatidylcholine bilayers: fluorescence phase and modulation study. Biochemistry. 25:3813-3823.
34. Hybl, A., and D. Dorset. 1971. The crystal structure of the 1,3-diglyceride of 11-bromoundecanoic acid. Acta Crystallogr. B27:977-986.
35. Israelachvili, J. N., S. Marcelja, and R. G. Horn. 1980. Physical principles of membrane organization. Q. Rev. Biophys. 13:121-200.
36. Jensen, L. H., and A. J. Mabis. 1966. Refinement of the structure of beta-tricaprin. Acta Crystallogr. 21:770-781.
37. II phase forming lipids. Chem. Phys. Lipids. 63:251-258.
38. Kinnunen, P. K. J. 1996a. On the molecular-level mechanism of peripheral protein-membrane interactions induced by lipids forming inverted non-lamellar phases. Chem. Phys. Lipids. 81:151-166.
39. II propensity. In Handbook of Nonmedical Applications of Liposomes. D. D. Lasic and Y. Barenholz, editors. CRC Press, Boca Raton, FL. 153-171.
40. Kinnunen, P. K. J., A. Kōiv, and P. Mustonen. 1993. Pyrene-labelled lipids as fluorescent probes in studies on biomembranes and membrane models. In Fluorescence Spectroscopy. O. S. Wolfbeis, editor. Springer-Verlag, Berlin. 159-169.
41. Kinnunen, P. K. J., A-P. Tulkki, H. Lemmetyinen, J. Paakkola, and J. A. Virtanen. 1987. Characteristics of excimer formation in Langmuir-Blodgett assemblies of 1-palmitoyl-2-pyrenedecanoylphosphatidylcholine and dipalmitoylphosphatidylcholine. Chem. Phys. Lett. 136: 539-545.
42. Kouaouci, R., J. R. Silvius, I. Graham, and M. Pezolet. 1985. Calcium induced lateral phase separations in phosphatidylcholine-phosphatidic acid mixtures: a raman spectroscopic study. Biochemistry. 24: 7132-7140.
43. Lakowicz, J. R., F. G. Prendergast, and D. Hogen. 1979a. Differential polarized phase fluorometric investigations of diphenylhexatriene in lipid bilayers: quantitation of hindered depolarizing rotations. Biochemistry. 18:508-519.
44. Lakowicz, J. R., F. G. Prendergast, and D. Hogen. 1979b. Fluorescence anisotropy measurements under oxygen quenching conditions as a method to quantify the depolarizing rotations of fluorophores: application to diphenylhexatriene in isotropic solvents and in lipid bilayers. Biochemists. 18:520-527.
45. Larsson, K. 1963. The crystal structure of the 1,3-diglyceride of 3-thiadodecanoic acid. Acta Crystallogr. 16:741-751.
46. Larsson, K. 1986. Physical properties: structural and physical characteristics. In The Lipid Handbook. F. D. Gunstone, J. L. Harwood, and F. B. Padley, editors. Chapman and Hall, London. 321-381.
47. Lehtonen, J. Y. A., and P. K. J. Kinnunen. 1994. Changes in the lipid dynamics of liposomal membranes induced by poly(ethylene glycol): free volume alterations revealed by inter- and intramolecular excimer-forming phospholipid analogs. Biophys. J. 66:1981-1990.
48. Leikin, S. L., M. M. Kozlov, L. V. Chemomordik, V. S. Markin, and Y. A. Chizmadzhev. 1987. Membrane fusion: overcoming of the hydration barrier and local restructuring. J. Theor. Biol. 129:411-425.
49. Leventis, R., J. Gagne, N. Fuller, R. P. Rand, and J. R. Silvius. 1986. Divalent cation induced fusion and lipid lateral segregation in phosphatidylcholine-phosphatidic acid vesicles. Biochemistry. 25:6978-6987.
50. Liao, M. J. and J. H. Prestegard. 1979. Fusion of phosphatidic acid-phosphatidylcholine mixed lipid vesicles. Biochim. Biophys. Acta. 550: 157-173.
51. MacDonald, R. C., R. I. MacDonald, B. M. Menco, K. Takeshita, N. K. Subbarao, and L. R. Hu. 1991. Small-volume extrusion apparatus for preparation of large, unilamellar vesicles. Biochim. Biophys. Acta. 1061: 297-303.
52. Markin, V. S., M. M. Kozlov, and V. L. Borovjagin. 1984. On the theory of membrane fusion: the stalk mechanism. Gen. Physiol. Biophys. 3:361-377.
53. Marra, J. 1986a. Direct measurement of the interaction between phosphati-dylglycerol bilayers in aqueous electrolyte solutions. Biophys. J. 50: 815-825.
54. Marra, J. 1986b. Effects of counterion specificity on the interactions between quaternary ammonium surfactants in monolayers and bilayers. J. Phys. Chem. 90:2145-2150.
55. 31P-NMR. Biochim. Biophys. Acta. 774:227-236.
56. Ohki, S., and K. Arnold. 1990. Surface dielectric constant, surface hydro-phobicity and membrane fusion. J. Membr. Biol. 114:195-203.
57. Ohki, S. and N. Düzgünes. 1979. Divalent cation-induced interaction of phospholipid vesicle and monolayer membranes. Biochim. Biophys. Acta. 552:438-449.
58. Ohki, S., and O. Zschörnig. 1993. Ion-induced fusion of phosphatidic acid vesicles and correlation between surface hydrophobicity and membrane fusion. Chem. Phys. Lipids. 65:193-204.
59. Olson, F., C. A. Hunt, F. C. Szoka, W. J. Vail, and D. Papahadjopoulos. 1979. Preparation of liposomes of defined size distribution by extrusion through polycarbonate membranes. Biochim. Biophys. Acta. 557:9-23.
60. Papahadjopoulos, D., S. Nir, and N. Düzgünes. 1990. Molecular mechanism of calcium-induced membrane fusion. J. Bioenerg. Biomembr. 22:157-179.
61. Papahadjopoulos, D., W. J. Vail, C. Newton, S. Nir, K. Jacobson, G. Poste, and R. Lazo. 1977. Studies on membrane fusion. III. The role of calcium-induced phase changes. Biochim. Biophys. Acta. 465:579-598.
62. Park, J. B., T. H. Lee, and H. Kim. 1992. Fusion of phospholipid vesicles induced by phospholipase D in the presence of calcium ion. Biochem. Int. 27:417-422.
63. 2+, and inhibition by spectrin. Biochemistry. 18:780-790.
64. Prendergast, F. G., R. P. Haugland, and P. J. Callahan. 1981. 1-[4-(Trimethylamino)phenyl]-6-phenylhexa-1,3,5-triene: synthesis, fluorescence properties, and use as a fluorescent probe of lipid bilayers. Biochemistry. 20:7333-7338.
65. Rand, R. P., and V. A. Parsegian. 1986. Mimicry and mechanism in phospholipid models of membrane fusion. Annu. Rev. Physiol. 48: 201-212.
66. Rand, R. P., and V. A. Parsegian. 1989. Hydration forces between phospholipid bilayers Biochim. Biophys. Acta. 988:351-376.
67. Relini, A., D. Cassinadri, Q. Fan, A. Gulik, Z. Mirghani, M. De Rosa, and A. Gliozzi, 1996. Effect of physical constraints on the mechanism of membrane fusion: bolaform lipid vesicles as model systems. Biophys. J. 71:1789-1795.
68. Relini, A., D. Cassinadri, Z. Mirghani, O. Brandt, A. Gambacorta, A. Trincone, M. De Rosa, and A. Gliozzi. 1994. Calcium-induced interaction and fusion of archaeobacterial lipid vesicles: a fluorescence study. Biochim. Biophys. Acta. 1194:17-24.
69. Siegel, D. P. 1984. Inverted micellar structures in bilayer membranes: formation rates and half-lifes. Biophys. J. 45:399-420.
70. Siegel, D. P. 1993. Energetics of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate mechanism. Biophys. J. 65:2124-2140.
71. Siegel, D. P., and R. M. Epand. 1997. The mechanisms of lamellar-to-inverted hexagonal phase transitions in phosphatidylethanolamine: implications for membrane fusion mechanism. Biophys. J. 73:3089-3111.
72. Silvius, J. R. 1990. Calcium-induced lipid phase separations and interactions of phosphatidylcholine/anionic phospholipid vesicles: fluorescence studies using carbazole-labeled and brominated phospholipids. Biochemistry. 29:2930-2938.
73. Simmonds, A. C., and M. J. Halsey, 1985. General and local anesthetics perturb the fusion ot phospholipid membranes. Biochim. Biophys. Acta. 813:331-337.
74. Smaal, E. B., J. G. Mandersloot, R. A. Demel, B. de Kruijff, and J. de Gier. 1987. Consequences of the interaction of calcium with dioleoylphosphatidate-containing model membranes: calcium-membrane and membrane-membrane interactions. Biochim. Biophys. Acta. 897:180-190.
75. Somerharju, P. J., J. A. Virtanen, K. K. Eklund, P. Vainio, and P. K. J. Kinnunen. 1985. 1-Palmitoyl-2-pyrenedecanoyl glycerophospholipids as membrane probes: evidence for regular distribution in liquid-crystalline phosphatidylcholine bilayers. Biochemistry. 24:2773-2781.
76. Sunamoto, J., H. Kondo, T. Nomura, and H. Okamoto. 1980. Liposomal membranes. II. Synthesis of a novel pyrene-labeled lecithin and structural studies on liposomal bilayers. J. Am. Chem. Soc. 102:1146-1152.
77. Tate, M. W., E. F. Eikenberry, D. C. Turner, E. Shyamsunder, and S. M. Gruner. 1991. Nonbilayer phases of membrane lipids. Chem. Phys. Lipids. 57:147-164.
78. Thurén, T., P. Vainio, J. A. Virtanen, P. Somerharju, K. Blomqvist, and P. K. J. Kinnunen. 1984. Evidence for the control of the action of phospholipases A by the physical state of the substrate. Biochemistry. 23:5129-5134.
79. Turnbull, D., and M. H. Cohen. 1970. On the free volume model of the liquid-glass transition. J. Chem. Phys. 52:3038-3041.
80. Verkleij, A. J., R. De Maagd, J. Leunissen-Bijvelt, and B. De Kruijff. 1982. Divalent cations and chlorpromazine can induce nonbilayer structures. Biochim. Biophys. Acta. 684:255-262.
81. Verkleij, A. J., C. Members, W. J. Gerritsen, J. Leunissen-Bijvelt, and P. R. Cullis. 1979. Fusion of phospholipid vesicles in association with the appearance of lipidic panicles as visualized by freeze fracturing. Biochim. Biophys. Acta. 555:358-361.
82. White, J. M. 1992. Membrane fusion. Science. 258:917-924.
83. Wilschut, J., J. Corver, J. L. Nieva, R. Bron, L. Moesby, R. Chandraprakash, and R. Bittman. 1995. Fusion of Semliki Forest virus with cholesterol-containing liposomes at low pH: a specific requirement for sphingolipids. Mol. Membr. Biol. 12:143-149.
84. Xiang, T.-X. 1993. A computer simulation of free-volume distributions and related structural properties in a model lipid bilayer. Biophys. J. 65: 1108-1120.
85. 1H nuclear magnetic resonance cross-relaxation spectroscopy. Biophys. J. 49:779-783.
86. Yang, Q., Y. Guo, L. Li, and S. W. Hui. 1997. Effects of lipid headgroup and packing stress on poly(ethylene glycol)-induced phospholipid vesicle aggregation and fusion. Biophys. J. 73:277-282.
87. Zaks, W. J., and C. E. Creutz. 1990. Evaluation of the annexins as potential mediators of membrane fusion in exocytosis. J. Bioenerg. Biomembr. 22:97-120
88. Zimmerberg, J., S. S. Vogel, and L. V. Chernomordik. 1993. Mechanism of membrane fusion. Annu. Rev. Biomol. Struct. 22:433-466.