The modified stalk mechanism of lamellar/inverted phase transitions and its implications for membrane fusion

Biophysical Journal

Volumn 76, Issue 1 I, 1999, Pages 291-313

  Siegel, David P ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ELECTRON MICROSCOPY; ENERGY BALANCE; LIPID BILAYER; MATHEMATICAL ANALYSIS; MEMBRANE FUSION; MEMBRANE MODEL; PHASE TRANSITION; PREDICTION;

EID: 0032926928     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77197-3     Document Type: Article

References (92)

1. Andersen, D. M., S. M. Gruner, and S. Leibler. 1988. Geometrical aspects of the frustration in the cubic phases of lyotropic liquid crystals. Proc. Natl. Acad. Sci. USA. 85:5364-5368.
2. Andersson, S., S. T. Hyde, K. Larsson, and S. Lidin. 1988. Minimal surfaces and structures: from inorganic and metal crystals to cell membranes and biopolymers. Chem. Rev. 88:221-242.
3. Basáñez, G., F. M. Goñi, and A. Alonso. 1998. Effect of single chain lipids on phospholipase C-promoted vesicle fusion. A test for the stalk hypothesis of membrane fusion. Biochemistry. 37:3901-3908.
4. Benedicto, A., and D. F. O'Brien. 1997. Bicontinuous cubic morphologies in block copolymers and amphiphile/water systems. Mathematical description through the minimal surfaces. Macromolecules. 30:3395-3402.
5. Briggs, J., and M. Caffrey. 1994. The temperature-composition phase diagram of monomyristolein in water: equilibrium and metastability aspects. Biophys. J. 66:573-587.
6. Caffrey, M. 1985. Kinetics and mechanism of the lamellar gel/lamellar liquid crystal and lamellar/inverted hexagonal phase transition in phosphatidylethanolamine: a real-time x-ray diffraction study using synchrotron radiation. Biochemistry. 24:4826-4844.
7. Caffrey, M. 1987. Kinetics and mechanism of transitions involving the lamellar, cubic, inverted hexagonal, and fluid isotropic phases of hydrated monoacylglycerides monitored by time-resolved x-ray diffraction. Biochemistry. 26:6349-6363.
8. Caffrey, M., R. L. Magin, B. Hummel, and J. Zhang. 1990. Kinetics of the lamellar and hexagonal phase transitions in phosphatidylethanolamine. Time-resolved x-ray diffraction study using a microwave-induced temperature jump. Biophys. J. 58:21-29.
9. Chen, Z., and R. P. Rand. 1997. The influence of cholesterol on phospholipid membrane curvature and bending elasticity. Biophys. J. 73: 267-276.
10. Chernomordik, L., A. Chanturiya, J. Green, and J. Zimmerberg. 1995a. The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition. Biophys. J. (in press).
11. Chernomordik, L. V., M. M. Kozlov, G. B. Melikyan, I. G. Abidor, V. S. Markin, and Yu. A. Chizmadzhev. 1985. The shape of lipid molecules and monolayer membrane fusion. Biochim. Biophys. Acta. 812: 643-655.
12. Chernomordik, L., M. M. Kozlov, and J. Zimmerberg. 1995b. Lipids in biological membrane fusion. J. Membr. Biol. 146:1-14.
13. Chernomordik, L. V., G. B. Melikyan, and Yu. A. Chizmadzhev. 1987. Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim. Biophys. Acta. 906: 309-352.
14. Chernomordik, L., and J. Zimmerberg. 1995. Bending membranes to the task: structural intermediates in bilayer fusion. Curr. Opin. Struct. Biol. 5:541-547.
15. Chizmadzhev, Y. A., F. S. Cohen, A. Shcherbakov, and J. Zimmerberg. 1995. Membrane mechanics can account for fusion pore dilation in stages. Biophys. J. (in press).
16. Chung, H., and M. Caffrey. 1994a. The curvature elastic energy function of the lipid-water cubic mesophase. Nature. 368:224-226.
17. Chung, H., and M. Caffrey. 1994b. The neutral area surface of the cubic mesophase: location and properties. Biophys. J. 66:377-381.
18. Colotto, A., and R. M. Epand. 1997. Structural study of the relationship between the rate of membrane fusion and the ability of the fusion peptide of influenza virus to perturb bilayers. Biochemistry. 36:7644-7651.
19. Colotto, A., I. Martin, J.-M. Ruysschaert, A. Sen, S. W. Hui, and R. M. Epand. 1996. Structural study of the interaction between the SIV fusion peptide and model membranes. Biochemistry. 35:980-989.
20. Cullis, P. R., P. W. M. van Dijck, B. de Kruijff, and J. de Gier. 1978. Effects of cholesterol on the properties of equimolar mixtures of synthetic phosphatidylethanolamine and phosphatidylcholine. Biochim. Biophys. Acta. 513:21-30.
21. II phase transition. Biochemistry. 25:4141-4147.
22. 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.
23. Epand, R. M. 1985. High sensitivity differential scanning calorimetry of the bilayer to hexagonal phase transitions of diacylphosphatidylethanolamines. Chem. Phys. Lipids. 36:387-393.
24. Epand, R. M. 1990. Hydrogen bonding and the thermotropic transitions of phosphatidylethanolamines. Chem. Phys. Lipids. 52:227-230.
25. Epand, R. M., and C. T. Lemay. 1993. Lipid concentration affects the kinetic stability of dielaidoylphosphatidylethanolamine bilayers. Chem. Phys. Lipids. 66:181-187.
26. Erramilli, S., F. Osterberg, S. M. Gruner, M. W. Tate, and M. Kriechbaum. 1995. Time-resolved x-ray studies on pressure-jump induced topological transitions in biological membranes. SPIE Proc. 2521:188-196.
27. Evans. E., and D. Needham. 1986. Giant vesicle bilayers composed of lipids, cholesterol and peptides. Faraday Discuss. Chem. Soc. 81: 267-280.
28. Evans, E., and D. Needham. 1987. Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion, and colloidal interactions. J. Phys. Chem. 91:4219-4228.
29. Fournier, J. B. 1996. Nontopological saddle-splay and curvature instabilities from anisotropic membrane inclusions. Phys. Rev. Lett. 76: 4436-4439.
30. Frederik, P. M., K. N. J. Burger, M. C. A. Stuart, and A. J. Verkelij. 1991. Lipid polymorphism as observed by cryo-electron microscopy. Biochim. Biophys. Acta. 1062:133-141.
31. Gagné, J., L. Stamatatos, T. Diacovo, S. W. Hui, P. Yeagle, and J. Silvius. 1985. Physical properties and surface interactions of bilayer membranes containing N-methylated phosphatidylethanolamines. Biochemistry. 24: 4400-4408.
32. Gruner, S. M. 1990. Stability of lyotropic phases with curved interfaces. J. Phys. Chem. 93:7562-7570.
33. Gruner, S. M., M. W. Tate, G. L. Kirk, P. T. C. So, D. C. Turner, D. T. Keane, C. P. S. Tilcock, and P. R. Cullis. 1988. X-ray diffraction study of the polymorphic behavior of N-methylated dioleoylphosphatidylethanolamine. Biochemistry. 27:2853-2866.
34. Helfrich, W. 1973. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. Sect. C Biosci. 280:693-703.
35. Hui, S. W., and T. P. Stewart. 1981. "Lipidic particles" are intermembrane attachment sites. Nature. 287:166-167.
36. Hui, S. W., T. P. Stewart, and L. T. Boni. 1982. Membrane fusion through point defects in bilayers. Science. 212:921-923.
37. Hui, S. W., T. P. Stewart, and L. T. Boni. 1983. The nature of lipidic particles and their roles in polymorphic transitions. Chem. Phys. Lipids. 33:113-116.
38. Keller, S. L., S. M. Bezrukov, S. M. Gruner, M. W. Tate, I. Vodyanov, and V. A. Parsegian. 1993. Probability of alamethicin conductance states varies with nonlamellar tendency of bilayer phospholipids. Biophys. J. 65:23-27.
39. Keller, S. L., S. M. Gruner, and K. Gawrisch. 1996. Small concentrations of alamethicin induce a cubic phase in bulk phosphatidylethanolamine mixtures. Biochim. Biophys. Acta. 1278:241-246.
40. II lipid liquid crystalline phase transition: hydrocarbon packing vs. intrinsic curvature. J. Physiol. (Paris). 46:761-769.
41. Kozlov, M. M., S. L. Leikin, L. V. Chernomordik, V. S. Markin, and Yu. A. Chizmadzhev. 1989. Stalk mechanism of membrane fusion. Intermixing of aqueous contents. Eur. Biophys. J. 17:121-129.
42. Kozlov, M. M., S. Leikin, and R. P. Rand. 1994. Bending, hydration and interstitial energies quantitatively account for the hexagonal-lamellar-hexagonal reentrant phase transition in dioleoylphosphatidylethanolamine. Biophys. J. 67:1603-1611.
43. Kozlov, M. M., and M. Winterhalter. 1991a. Elastic moduli for strongly curved monolayers. Position of the neutral surface. J. Phys. II (France). 1:1077-1084.
44. Kozlov, M. M., and M. Winterhalter. 1991b. Elastic moduli and neutral surface for strongly curved monolayers. Analysis of experimental results. J. Phys. II (France). 1:1085-1100.
45. Kriechbaum, M., G. Rapp, J. Hendrix, and P. Laggner. 1989. Millisecond time-resolved x-ray diffraction on liquid-crystalline phase transitions using infrared laser T-jump technique and synchrotron radiation. Rev. Sci. Instrum. 60:2541-2544.
46. Laggner, P., and M. Kriechbaum. 1991. Phospholipid phase transitions: kinetics and structural mechanisms. Chem. Phys. Lipids. 57:121-145.
47. Laggner, P., M. Kriechbaum, and G. Rapp. 1991. Structural intermediates in phospholipid phase transitions. J. Appl. Crystallogr. 24:836-842.
48. Leikin, S. L., M. M. Kozlov, L. V. Chernomordik, V. S. Markin, and Yu. A. Chizmadzhev. 1987. Membrane fusion: overcoming of the hydration barrier and local restructuring. J. Theor. Biol. 129:411-425.
49. Leikin, S., M. M. Kozlov, N. L. Fuller, and R. P. Rand. 1996. Measured effects of diacylglycerol on structural and elastic properties of phospholipid membranes. Biophys. J. 71:2623-2632.
50. Leventis, R., N. Fuller, R. P. Rand, P. L. Yeagle, A. Sen, M. J. Zuckermann, and J. R. Silvius. 1991. Molecular organization and stability of hydrated dispersions of headgroup-modified phosphatidylethanolamine analogs. Biochemistry. 30:7212-7219.
51. Lewis, R. A. H., D. A. Mannock, R. N. McElhaney, D. C. Turner, and S. M. Gruner. 1989. Effect of fatty acid chain length and structure on the lamellar gel to liquid crystalline and lamellar to reversed hexagonal phase transitions of aqueous phosphatidylethanolamine dispersions. Biochemistry. 28:541-548.
52. Lewis, R. N. A. H., R. N. McElhaney, P. E. Harper, D. C. Turner, and S. M. Gruner. 1994. Studies of the thermotropic phase behavior of phosphatidylcholines containing 2-alkyl substituted fatty acyl chains: a new class of phosphatidylcholines forming inverted nonlamellar phases. Biophys. J. 66:1088-1103.
53. Lindblom, G., and L. Rilfors. 1989. Cubic phases and isotropic structures formed by lipids - possible biological relevance. Biochim. Biophys. Acta. 988:221-256.
54. Longo, M. L., A. J. Waring, and D. A. Hammer. 1997. Interaction of influenza hemagglutinin fusion peptide with lipid bilayers: area expansion and permeation. Biophys. J. 73:1430-1439.
55. Mannock, D. A., R. N. A. H. Lewis, R. N. McElhaney, M. Akiyama, H. Yamada, D. C. Turner, and S. M. Gruner. 1992. Effect of chirality of the glycerol backbone on the bilayer and nonbilayer phase transitions in the diastereomers of di-dodecyl-β-D-glucopyranosyl glycerol. Biophys. J. 63:1355-1368.
56. Mannock, D. A., R. N. McElhaney, P. E. Harper, and S. M. Gruner. 1994. Differential scanning calorimetry and x-ray diffraction studies of the thermotropic phase behavior of the diastereomeric di-tetradecyl-β-D-galactosyl glycerols and their mixture. Biophys. J. 66:734-740.
57. Markin, V. S., M. M. Kozlov, and V. L. Borovjagin. 1984. On the theory of membrane fusion. The stalk mechanism. Gen. Physiol. Biophys. 5:361-377.
58. Marsh, D. 1990. Handbook of Lipid Bilayers. CRC Press, Boca Raton, FL. 151.
59. McIntosh, T. J., S. Advani, R. E. Burton, D. V. Zhelev, D. Needham, and S.A. Simon. 1995. Experimental tests for protrusion and undulation pressures in phospholipid bilayers. Biochemistry. 34:8520-8532.
60. McIntosh, T. J., and S. A. Simon. 1986. Area per molecule and distribution of water in fully hydrated dilauroylphosphatidylethanolamine bilayers. Biochemistry. 25:4948-4952.
61. McIntosh, T. J., and S. A. Simon. 1996. Adhesion between phosphatidylethanolamine bilayers. Langmuir. 12:1622-1630.
62. Morein, S., E. Strandberg, J. A. Killian, S. Persson, G. Arvidson, R. E. Koeppe II, and G. Lindblom. 1997. Influence of membrane-spanning α-helical peptides on the phase behavior of the dioleoylphosphatidylcholine/water system. Biophys. J. 73:3078-3088.
63. Nanavati, C., V. S. Markin, A. F. Oberhauser, and J. M. Fernandez. 1992. The exocytotic pore modeled as a lipidic pore. Biophys. J. 63: 1118-1132.
64. Rand, R. P., N. L. Fuller, S. M. Gruner, and V. A. Parsegian. 1990. Membrane curvature, lipid segregation, and structural transitions for phospholipids under dual-solvent stress. Biochemistry. 29:76-87.
65. Rand, R. P., N. Fuller, V. A. Parsegian, and D. C. Rau. 1988. Variation in hydration forces between neutral phospholipid bilayers: evidence for hydration attraction. Biochemistry. 27:7711-7722.
66. Rand, R. P., T. S. Reese, and R. G. Miller. 1981. Phospholipid bilayer deformations associated with interbilayer contact and fusion. Nature. 293:237-238.
67. II) phase, and non-lamellar phase transitions in lipids. Biochim. Biophys. Acta. 1031: 1-69.
68. Shyamsunder, E., S. M. Gruner, M. W. Tate, D. C. Turner, P. T. C. So, and C. P. S. Tilcock. 1988. Observation of inverted cubic phase in hydrated dioleoylphosphatidylethanolamine membranes. Biochemistry. 27: 2332-2336.
69. II phase transition. Biophys. J. 49:1155-1170.
70. Siegel, D. P. 1986b. Inverted micellar intermediates and the transitions between lamellar, inverted hexagonal, and cubic lipid phases. II. Implications for membrane-membrane interactions and membrane fusion. Biophys. J. 49:1171-1183.
71. II phases. Chem. Phys. Lipids. 42:279-301.
72. Siegel, D. P. 1993. Energetics of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate structures. Biophys. J. 65:2124-2140.
73. II) phase transition in N-methylated dioleoylphosphatidylethanolamine. Biochemistry. 29:5975-5981.
74. Siegel, D. P., J. L. Banschbach, D. Alford, H. Ellens, L. J. Lis, P. J. Quinn, P. L. Yeagle, and J. Bentz. 1989a. Physiological levels of diacylglycerols in phospholipid membranes induce membrane fusion and stabilize inverted phases. Biochemistry. 28:3703-3709.
75. II phases by low levels of diglycerides and alkanes: an NMR, calorimetric, and X-ray diffraction study. Biochemistry. 29:5975-5981.
76. Siegel, D. P., J. L. Burns, M. H. Chestnut, and Y. Talmon. 1989c. Intermediates in membrane fusion and bilayer/non-bilayer phase transitions imaged by time-resolved cryo-transmission electron microscopy. Biophys. J. 56:161-169.
77. Siegel, D. P., and R. M. Epand. 1997. The mechanism of lamellar-to-inverted hexagonal phase transitions in phosphatidylethanolamine: implications for membrane fusion mechanisms. Biophys. J. 73:3089-3111.
78. Siegel, D. P., W. J. Green, and Y. Talmon. 1994. The mechanism of lamellar-to-inverted hexagonal phase transitions: a study using temperature-jump cryo-electron microscopy. Biophys. J. 66:402-414.
79. Sjölund, M., G. Lindblom, L. Rilfors, and G. Avidson. 1987. Hydrophobic molecules in lecithin-water systems. I. Formation of reversed hexagonal phase at high and low water contents. Biophys. J. 52:145-153.
80. Small, D. M. 1986. The physical chemistry of lipids. In The Handbook of Lipid Research, Vol. 4. D. J. Hanahan, series editor. Plenum Press, New York.
81. 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.
82. Tate, M. W., and S. M. Gruner. 1987. Lipid polymorphism of dioleoylphosphatidylethanolamine and saturated and monounsaturated phosphatidylcholines of various chain lengths. Biochemistry. 26: 231-236.
83. II) phase of phosphatidylethanolamine-containing membranes. Biochemistry. 28:4245-4253.
84. Tate, M. W., E. Shyamsunder, S. M. Gruner, and K. L. D'Amico. 1992. Kinetics of the lamellar-to-inverted hexagonal phase transition determined by time-resolved x-ray diffraction. Biochemistry. 31:1081-1092.
85. Templer, R. H. 1995. On the area neutral surface of inverse bicontinuous cubic phases of lyotropic liquid crystals. Langmuir. 11:334-340.
86. Templer. R. H., J. M. Seddon, and N. A. Warrender. 1994. Measuring the elastic parameters for inverse bicontinuous cubic phases. Biophys. Chem. 49:1-12.
87. Tenchov, B., R. Koynova, and G. Rapp. 1998. Accelerated formation of cubic phases in phosphatidylethanolamine dispersions. Biophys. J. 75: 853-866.
88. Thomas, E. L., D. M. Anderson, C. S. Henkee, and D. Huffman. 1988. Periodic area-minimizing surfaces in block copolymers. Nature. 334: 598-601.
89. 31P nuclear magnetic resonance studies of the appearance of an isotropic component in dielaidoylphosphatidylethanolamine. Biophys. J. 57:637-641.
90. Verkleij, A. L 1984. Lipidic intramembranous particles. Biochim. Biophys. Acta. 779:43-63.
91. Verkleij, A. J., C. Mombers, W. J. Gerritsen, L. Leunissen-Bijvelt, and P. R. Cullis. 1978. Fusion of phospholipid vesicles in association with the appearance of lipidic particles as visualized by freeze-fracturing. Biochim. Biophys. Acta. 555:358-361.
92. Verkleij, A. J., C. Mombers, J. Lenissen-Bijvelt, and P. H. J. Th. Ververgaert. 1979. Lipidic intramembranous particles. Nature. 279:162-163.