The fusion pore and mechanisms of biological membrane fusion

Current Opinion in Cell Biology

Volumn 8, Issue 4, 1996, Pages 524-533

  Monck, Jonathan R ^a   Fernandez, Julio M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEROTONIN;

BILAYER MEMBRANE; CELL FUSION; EXOCYTOSIS; MEMBRANE FUSION; PRIORITY JOURNAL; REVIEW; VIRUS CELL INTERACTION;

INFLUENZA VIRUS;

EID: 0030222281     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(96)80031-7     Document Type: Article

References (79)

1. 1. Sudhof TC, De Camilli P, Niemann H, Jahn R: Membrane fusion machinery: insights from synaptic proteins. Cell 1993, 75:1-4.
2. 2. Sudhof TC: The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 1995, 375:645-653.
3. 3. White JM: Membrane fusion. Science 1992, 258:917-924.
4. 4. White JM: Membrane fusion: the influenza paradigm. Cold Spring Harb Symp Quant Biol 1996, in press. Up-to-date review of viral fusion.
5. 5. Almers W, Tse FW: Transmitter release from synapses: does a preassembled fusion pore initiate exocytosis? Neuron 1990, 4:813-818.
6. 6. Monck JR, Fernandez JM: The exocytotic fusion pore. J Cell Biol 1992, 119:1395-1404.
7. 7. Monck JR, Fernandez JM: The exocytotic fusion pore and neurotransmitter release. Neuron 1994, 12:707-716.
8. 8. Zimmerberg J, Vogel SS, Chernomordik LV: Mechanisms of membrane fusion. Annu Rev Biophys Biomol Struct 1993, 22:433-466.
9. 9. Lindau M, Almers W: Structure and function of fusion pores in exocytosis and ectoplasmic membrane fusion. Curr Opin Cell Biol 1995, 7:509-517.
10. 10. Blumenthal R, Pak CG, Raviv Y, Krumbiegel M, Bergelson LD, Morris SJ, Lowy RJ: Transient domains induced by influenza haemagglutinin during membrane fusion. Mol Membr Biol 1995, 12:135-142. Describes the scaffold model of viral fusion-pore formation. Interesting because of the parallels drawn with the exocytotic fusion pore.
11. 11. Breckenridge LJ, Almers W: Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature 1987, 328:814-817.
12. 12. Zimmerberg J, Curran M, Cohen FS, Brodwick M: Simultaneous electrical and optical measurements show that membrane fusion precedes secretory granule swelling during exocytosis of beige mouse mast cells. Proc Natl Acad Sci USA 1987, 84:1585-1589.
13. 13. Alvarez de Toledo G, Fernandez JM: The events leading to secretory granule fusion. In Cell Physiology of Blood. Edited by Gumm RB, Parker JC. New York: Rockefeller University Press: 1988:334-344. [Society of General Physiologists, vol 43.]
14. 14. Spruce AE, Breckenridge LJ, Lee AK, Almers W: Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron 1990, 4:643-654.
15. 15. Monck JR, Alvarez de Toledo G, Fernandez JM: Tension in secretory granule membranes causes extensive membrane transfer through the exocytotic fusion pore. Proc Natl Acad Sci USA 1990, 87:7004-7808.
16. 16. Oberhauser AF, Monck JR, Fernandez JM: Events leading to the opening and closing of the exocytotic fusion pore have markedly different temperature dependencies. Kinetic analysis of single fusion events in patch-clamped mouse mast cells. Biophys J 1992, 61:800-809.
17. 17. Lindau M, Nusse O, Bennett J, Cromwell O: Membrane fusion events in degranulating guinea pig eosinophils. J Cell Sci 1993, 104:203-209.
18. 18. Lollike K, Borregaard N, Lindau M: The exocytotic fusion pore of small granules has a conductance similar to an ion channel. J Cell Biol 1995, 129:99-104. By making electrical measurements of the fusion pore using a cell-attached patch-clamp, exocytotic fusion pores from small secretory granules were detected. The pores behaved in a similar manner to those seen on fusion of larger granules.
19. 19. Nanavati C, Markin VS, Oberhauser A, Fernandez JM: The exocytotic fusion pore modeled as a lipidic pore. Biophys J 1992, 63:1118-1132.
20. 20. Oberhauser AF, Fernandez JM: Patch-clamp studies of intact secretory granules. Biophys J 1993, 65:1844-1852.
21. 21. Chandler DE, Heuser JE: Arrest of membrane fusion events in mast cells by quick-freezing. J Cell Biol 1980, 86:666-674.
22. 22. Ornberg RL, Reese TS: Beginning of exocytosis captured by rapid-freezing of Limulus amebocytes. J Cell Biol 1981, 90:40-54.
23. 23. Knoll G, Braun C, Plattner H: Quenched flow analysis of exocytosis in Paramecium cells: time course, changes in membrane structure, and calcium requirements revealed after rapid mixing and rapid freezing of intact cells. J Cell Biol 1991, 113:1295-1304.
24. 24. Schmidt W, Patzak A, Lingg G, Winkler H: Membrane events in adrenal chromaffin cells during exocytosis: a freeze-etching analysis after rapid cryofixation. Eur J Cell Biol 1983, 32:31-37.
25. 25. Heuser JE, Reese TS: Structural changes after transmitter release at the frog neuromuscular junction. J Cell Biol 1981, 88:564-580.
26. 26. Plattner H, Miller F, Bachmann L: Membrane specializations in the form of regular membrane-to-membrane attachment sites in Paramecium. A correlated freeze-etching and ultrathin-sectioning analysis. J Cell Sci 1973, 13:687-719.
27. 27. Beisson J, Lefort-Tran M, Pouphile M, Rossignol M, Stir B: Genetic analysis of membrane differentiation in Paramecium. Freeze-fracture study of the trichocyst cycle in wild-type and mutant strains. J Cell Biol 1976, 69:126-143.
28. 28. Olbricht K, Plattner H, Matt H: Synchronous exocytosis in Paramecium cells. II. Intramembranous changes analyzed by freeze-fracturing. Exp Cell Res 1984, 151:14-20.
29. 29. Nakata T, Hirokawa N: Organization of cortical cytoskeleton of cultured chromaffin cells and involvement in secretion as revealed by quick-freeze, deep-etching and double-label and immunoelectron microscopy. J Neurosci 1991, 12:2186-2197.
30. 30. Pollard HB, Rojas E, Pastor RW, Rojas EM, Guy HR, Burns AL: Synexin: molecular mechanism of calcium-dependent membrane fusion and voltage-dependent calcium-channel activity. Ann NY Acad Sci 1992, 635:328-351.
31. 31. Chernomordik L, Kozlov MM, Zimmerberg J: Lipids in biological membrane fusion. J Membr Biol 1995, 146:1-14.
32. 32. Knoll G, Burger KNJ, Bron R, Van Meer G, Verkleij AJ: Fusion of liposomes with the plasma membrane of epithelial cells: fate of incorporated lipids as followed by freeze fracture and autoradiography of plastic sections. J Cell Biol 1988, 107:2511-2521.
33. 33. Spruce AE, Iwata A, White JM, Almers W: Patch clamp studies of single cell-fusion events mediated by a viral fusion protein. Nature 1989, 342:555-558.
34. 34. Spruce AE, Iwata A, Almers W: The first milliseconds of the pore formed by a fusogenic viral envelope protein during membrane fusion. Proc Natl Acad Sci USA 1991, 88:3623-3627
35. 35. Melikyan GB, Miles WD, Cohen FS: Influenza virus hemagglutinin-induced cell-planar bilayer fusion: quantitative dissection of fusion pore kinetics into stages. J Gen Physiol 1993, 102:1151-1170.
36. 36. Melikyan GB, Niles WD, Peeples ME, Cohen FS: Influenza hemagglutinin-mediated fusion pores connecting cells to planar membranes: flickering to final expansion. J Gen Physiol 1993, 102:1131-1149.
37. 37. Hoekstra D: Membrane fusion of enveloped viruses: especially a matter of proteins. J Bioenerg Biomembr 1990, 22:121-155.
38. 38. Bentz J, Ellens H, Alford D: An architecture for the fusion site of influenza hemagglutinin. FEBS Lett 1990, 276:1-5.
39. +-induced insertion of influenza hemagglutinin HA2 N-terminal into the viral membrane. J Biol Chem 1994, 269:18353-18358.
40. 40. Danieli T, Pelletier SL, Henis YI, White JM: Membrane fusion mediated by influenza hemagglutinin requires the concerted action of at least three hemagglutinin. J Cell Biol 1996, in press. Demonstration that at least three or four hemagglutinin trimers (i.e. 9-12 individual protein molecules) are required to form a viral scaffold.
41. 41. Kemble GW, Danieli T, White JM: Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 1994, 76:383-339.
42. 42. Blobel CP, Wolfsberg TG, Turck CW, Myles DG, Primakoff P, White JM: A potential fusion peptide and an integrin ligand domain in a protein active in sperm-egg fusion. Nature 1992, 356:248-252.
43. 43. Wolfsberg TG, Straight PD, Gerena RL, Huovila AP, Primakoff P, Myles DG, White JM: ADAM, a widely distributed and developmentally regulated gene family encoding membrane proteins with a disintegrin and metalloprotease domain. Dev Biol 1995, 169:378-383
44. 44. Neher E: Asymmetric membranes resulting from the fusion of two black lipid bilayers. Biochim Biophys Acta 1974, 373:327-336.
45. 45. Ohki S: Surface tension, hydration energy and membrane fusion. In Molecular Mechanisms of Membrane Fusion. Edited by Ohki S, Doyle D, Flanagan TD, Withers S, Mayhew E. New York: Plenum Press; 1987:123-137.
46. 46. Helm CA, Israelachvili JN: Forces between phospholipid bilayers and relationship to membrane fusion. Methods Enzymol 1993, 220:130-143.
47. 47. Helm GA, Israelachvili JN, McGuiggan PM: Molecular mechanisms and forces involved in the adhesion and fusion of amphiphilic bilayers. Science 1989, 246:919-922.
48. 48. Leckband DE, Helm CA, Israelachvili JN: Role of calcium in the adhesion and fusion of bilayers. Biochemistry 1993, 32:1127-1140.
49. 49. Helfrich W: Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch [C] 1973, 28:693-703.
50. 50. Chernomordik LV, Melikyan GB, Chizmadzhev YA: Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim Biophys Acta 1987, 906:309-352.
51. 51. Chernomordik L, Chanturiya A, Green J, Zimmerberg J: The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition. Biophys J 1995, 69:922-929. Detailed discussion of the hemifusion intermediate and of how membrane curvature is important for membrane fusion.
52. (2+)-, GTP-and pH-dependent fusion of biological membranes. FEBS Lett 1993, 318:71-76.
53. 53. Melikyan GB, White JM, Cohen FS: GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. J Cell Biol 1995, 131:679-691. Demonstration that a mutant hemagglutinin protein, with a GPI anchor replacing the transmembrane domain, could induce hemifusion without fusion-pore formation. Together with [41], this paper provided direct evidence for hemifusion in biological membrane fusion.
54. 54. Markin VS, Kozlov MM, Borovjagin VL: On the theory of membrane fusion. The stalk mechanism. Gen Physiol Biophys 1984, 5:361-377.
55. 55. Kozlov MM, Leikin SL, Chernomordik LV, Markin VS, Chizmadzhev YA: Stalk mechanism of vesicle fusion. Intermixing of aqueous contents. Eur Biophys J 1989, 17:121-129.
56. 56. Chizmadzhev YA, Cohen FS, Shcherbackov A, Zimmerberg J: Membrane mechanics can account for pore dilation instages. Biophys J 1995, 69:2489-2500.
57. 57. Tse FW, Iwata A, Almers W: Membrane flux through the pore formed by a fusogenic viral envelope protein during cell fusion. J Cell Biol 1993, 121:543-552.
58. 58. Zimmerberg J, Blumenthal R, Sarkar DP, Curran M, Morris SJ: Restricted movement of lipid and aqueous dyes through pores formed by influenza hemagglutinin during cell fusion. J Cell Biol 1994, 127:1885-1894.
59. 59. Blumenthal R, Sarkar DP, Durrel S, Howard DE, Morris SJ: Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. Cell 1996, in press.
60. 60. Fernandez-Chacon R, Alvarez de Toledo G: Cytosolic calcium facilitates release of secretory products after exocytotic vesicle fusion. FEBS Lett 1995, 363:221-225.
61. 61. Hartmann J, Lindau M: A novel Ca(2+)-dependent step in exocytosis subsequent to vesicle fusion. FEBS Lett 1995, 363:217-220.
62. 62. Leszczyszyn D, Jankowski JA, Viveros HO, Diliberto EJ Jr, Near JA, Wightman RM: Nicotinic receptor-mediated catecholamine secretion from individual chromaffin cells: chemical evidence for exocytosis. J Biol Chem 1990, 265:14736-14737.
63. 63. Tatham PER, Duchen MR, Millar J: Monitoring exocytosis from single mast cells by fast voltammetry. Pflugers Arch 1991, 419:409-414.
64. 64. Schroeder TJ, Jankowski JA, Kawagoe KT, Wightman RM: Analysis of diffusional broadening of vesicular packets of catecholamines released from biological cells during exocytosis. Anal Chem 1992, 64:3077-3083.
65. 65. Jankowski JA, Schroeder TJ, Ciolkowski EL, Wightman RM: Temporal characteristics of quantal secretion of catecholamines from adrenal medullary cells. J Biol Chem 1993, 268:14694-14700.
66. 66. Wightman RM, Schroeder TJ, Finnegan JM, Ciolkowski EL, Pihel K: Time-course of release of catecholamines from individual vesicles during exocytosis at adrenal medullary cells. Biophys J 1995, 68:383-390.
67. 67. Chow RH, Von Ruden L, Neher E: Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 1992, 356:60-63.
68. 68. Neher E: Secretion without full fusion. Nature 1993, 363:497-498.
69. 69. Alvarez de Toledo G, Fernandez-Chacon R, Fernandez JM: Release of secretory products during transient vesicle fusion. Nature 1993, 363:554-557.
70. 70. Uvnäs, B, Åborg CH: Role of ion exchange in release of biogenic amines. News Physiol Sci 1989, 4:68-71.
71. 71. Uvnäs, B, Åborg CH: Cation exchange - a common mechanism in the storage and release of biogenic amines stored in granules (vesicles)? Acta Physiol Scand 1983, 119:225-234.
72. 72. Marszalek P, Farrell B, Fernandez JM: Kinetics of the release of serotonin from isolated secretory granules. Biophys J 1996, in press.
73. 73. Marszalek P, Farrell B, Fernandez JM: Ion exchange gel regulates neurotransmitter release through the exocytotic fusion pore. J Gen Physiol 1996, in press.
74. 2+ entry and quantal dopamine secretion in carotid body glomus cells. Proc Natl Acad Sci USA 1994, 91:10208-10211.
75. 75. Bruns D, Jahn R: Real-time measurement of transmitter release from single synaptic vesicles. Nature 1995, 376:62-65. Describes the measurement of neurotransmitter release from single synaptic vesicles. Confirms the scaling law for release ([69,73]; see text), suggesting that a common mechanism regulates transmitter release from synaptic vesicles and from large dense core granules.
76. 76. Parpura V, Fernandez JM: Atomic force microscopy study of the secretory granule lumen. Biophys J 1996, in press.
77. 77. Fernandez JM, Neher E, Gomperts BD: Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature 1984, 312:453-455.
78. 78. Robinson IM, Yamada M, Carrion-Vazquez M, Lennon V, Fernandez JM: Specialized release zones in chromaffin cells examined with pulsed laser imaging. Cell Calcium 1996, in press.
79. 79. Valtorta F, Fesce R, Grohovaz F, Haimann C, Hurlbut WP, Iezzi N, Torri Tarelli F, Villa A, Ceccarelli B: Neurotransmitter release and synaptic vesicle recyling. Neuroscience 1990, 35:477-489.