Secretion without membrane fusion: Porocytosis

Anatomical Record - Part B New Anatomist

Volumn 282, Issue 1, 2005, Pages 18-37

  Silver, Robert B ^a,b,c,e   Pappas, George D ^d  

^a Wayne State University   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF ILLINOIS   (United States)

^e WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Constitutive secretion; Membrane fusion; Plasma membrane; Porocytosis; Quantal release; SNARE; Vesicular secretion

Indexed keywords

ACETYLCHOLINE; CALCIUM ION; PHOSPHOLIPID; SNARE PROTEIN; SYNAPTOTAGMIN; SYNTAXIN; VOLTAGE GATED CALCIUM CHANNEL;

ATOMIC FORCE MICROSCOPY; CELL SECRETION; CHROMAFFIN CELL; ELECTRIC CAPACITANCE; ENERGY TRANSFER; EXOCYTOSIS; HAGFISH; LIPID BILAYER; MECHANICAL STRESS; MEMBRANE FUSION; MINIATURE ENDPLATE POTENTIAL; NEUROTRANSMITTER RELEASE; NONHUMAN; PARAMECIUM; PHYSICAL CHEMISTRY; POROCYTOSIS; POROSITY; PRIORITY JOURNAL; REVIEW; SECRETORY VESICLE; TETRAHYMENA;

ANIMALS; BODILY SECRETIONS; CALCIUM; CALCIUM SIGNALING; CELL MEMBRANE; EXOCYTOSIS; HUMANS; MEMBRANE FUSION; MEMBRANE LIPIDS; SECRETORY VESICLES;

EID: 13444267333     PISSN: 0003276X     EISSN: None     Source Type: Journal    
DOI: 10.1002/ar.b.20050     Document Type: Review

References (159)

1. Ales E, Tabares L, Poyato JM, Valero V, Lindau M, Alvarez de Toledo G. 1999. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat Cell Biol 1:E3-E4.
2. Amano T, Furuno T, Hirashima N, Ohyama N, Nakanishi M. 2001. Dynamics of intracellular granules with CD63-GFP in rat basophilic leukemia cells. J Biochem (Tokyo) 129:739-744.
3. Atlas D. 2001. Functional and physical coupling of voltage-sensitive calcium channels with exocytotic proteins: ramifications for the secretion mechanism. J Neurochem 77:972-985.
4. Averbakh A, Lobyshev VI. 2000. Adsorption of polyvalent cations to bilayer membranes from negatively charged lipid: estimating the lipid accessibility in the case of complete binding. J Biochem Biophys Meth 45:23-44.
5. Berke G. 1994. The binding and lysis of target cells by cytotoxic lymphocytes: molecular and cellular aspects. Ann Rev Immunol 12:735-773.
6. Beuers U. 1997. A view of exocytotic vesicle fusion in living secretory cells. Hepatology 26:241-243.
7. Binder H, Zschornig O. 2002. The effect of metal cations on the phase behavior and hydration characteristics of phospholipid membranes. Chem Phys Lipids 115:39-61.
8. Birks RI, Huxley HE, Katz B. 1960. The fine structure of the neuromuscular junction of the frog. J Physiol 134:134-144.
9. Blobel G, Dobberstein B. 1975. Transfer of proteins across membranes: I, presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol 67:835-851.
10. Bloc A, Bugnard E, Dunant Y, Falk-Vairant J, Israel M, Loctin F, Roulet E. 1999. Acetylcholine synthesis and quantal release reconstituted by transfection of mediatophore and choline acetyltransferase cDNAs. Eur J Neurosci 11:1523-1534.
11. Brodsky M, Zhitenev NB, Ashoori RC, Pfeiffer LN, West KW. 2000. Localization in artificial disorder: two coupled quantum dots. Phys Rev Lett 85:2356-2359.
12. Cavalli V, Corti M, Gruenberg J. 2001. Endocytosis and signaling cascades: a close encounter. FEBS Lett 498:190-196.
13. Cevc G, Richardson H. 1999. Lipid vesicles and membrane fusion. Adv Drug Deliv Rev 38:207-232.
14. Chanturiya A, Scaria P, Woodle MC. 2000. The role of membrane lateral tension in calcium-induced membrane fusion. J Membr Biol 176:67-75.
15. Chanturiya A, Yang J, Scaria P, Stanek J, Frei J, Mett H, Woodle M. 2003. New cationic lipids form channel-like pores in phospholipid bilayers. Biophys J 84:1750-1755.
16. Cheng Y, Chen B, Lu J, Wang K. 1998. The reaction of lanthanide ions with n-doxyl stearic acids and its utilization for the ESR study on the permeability of lipid-bilayer of erythrocyte membrane to gadolinium ions. J Inorg Biochem 69:1-7.
17. Cheng Y, Liu M, Rongchang L, Wang C, Bai C, Wang K. 1999. Gadolinium induces domain and pore formation of human erythrocyte membrane: an atomic force microscopic study. Biochim Biophys Acta 142:249-260.
18. Cho WJ, Jeremic A, Rognlien KT, Zhvania MG, Lazrishvili I, Tamar B, Jena BP. 2004. Structure, isolation, composition and reconstitution of the neuronal fusion pore. Cell Biol Int Rep 28:699-708.
19. Crivellato E, Belloni A, Nico B, Nussdorfer GC, Ribatti D. 2004. Chromaffin granules in the rat adrenal medulla release their secretory content in a particulate fashion. Anat Rec 227A:204-208.
20. Dan Y, Poo M-M. 1994. Calcium-dependent postsynaptic exocytosis: a possible mechanism for activity-dependent synaptic modulation. J Neurobiol 25:336-341.
21. Del Castillo J, Katz B. 1954. Quantal components of the end-plate potential. J Physiol 124:560-573.
22. Del Castillo J, Katz B. 1957. La base "quantale" de la transmission neuro-musculaire. CNRS Paris 67:245-258.
23. Dodge FA Jr, Rahamimoff R. 1967. Cooperative action of calcium ions in at the neuromuscular junction. J Physiol 193:419-432.
24. Downing SW, Salo WL, Spitzer RH, Koch EA. 1981. The hagfish slime gland: a model system for studying the biology of mucus. Science 214:1143-1145.
25. Duncan RR, Greaves J, Wiegand UK, Matskevich I, Bodammer G, Apps DK, Shipston MJ, Chow RH. 2003. Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422:176-180.
26. Duke TAJ, Bray D. 1999. Heightened sensitivity of a lattice of membrane receptors. Proc Nat Acad Sci USA 96:10104-10108.
27. Dunant Y, Israel M. 1995. Mediatophore and other presynaptic proteins: a cybernetic linking at the active zone. J Physiol Paris 89:147-156.
28. Dunant Y, Israel M. 2000. Neurotransmitter release at rapid synapses. Biochimie 82:289-302.
29. Duzgunes N, Ohki S. 1981. Fusion of small unilamellar liposomes with phospholipid planar bilayer membranes and large single-bilayer vesicles. Biochim Biophys Acta 640:734-747.
30. Duzgunes N, Wilschut J, Fraley R, Papahadjopoulos D. 1981. Studies on the mechanism of membrane fusion: role of head-group composition in calcium- and magnesium-induced fusion of mixed phospholipid vesicles. Biochim Biophys Acta 642:182-195.
31. Dvorak AM. 1991. Basophil and mast cell degranulation and recovery. In: Harris JR, editor. Blood cell biochemistry, vol. 4. New York: Plenum Press. p 340-377.
32. Dvorak AM. 2000. Ultrastructural features of human basophil and mast cell secretory function. In: Marone G, Lichtenstein LM, Galli SJ, editors. Mast cells and basophils. New York: Academic Press. p 63-88.
33. Eder-Colli L, Amato S. 1985. Membrane-bound choline acetyltransferase in Torpedo electric organ: a marker for synaptosomal plasma membranes? Neuroscience 15:577-589.
34. Erxleben C, Kriebel ME. 1988a. Subunit composition of the spontaneous miniature endplate currents at the mouse neuromuscular junction. J Physiol 400:659-676.
35. Erxleben C, Kriebel ME. 1988b. Characteristics of spontaneous miniature and subminiature end-plate currents at the mouse neuromuscularjunction. J Physiol 400:645-658.
36. Evans E, Heinrich V, Ludwig F, Rawicz W. 2003. Dynamic tension spectroscopy and strength of biomembranes. Biophys J 85:2342-2350.
37. Fatt P, Katz B. 1952. Spontaneous subthreshold activity at motor nerve endings. J Physiol 117:109-128.
38. Fesce R, Grohovaz F, Valtorta F, Meldolesi J. 1994. Neurotransmitter release: fusion or "kiss and run." Trends Cell Biol 4:1-4.
39. Fesce R, Meldolesi J. 1999. Peeping at the vesicle kiss. Nat Cell Biol 1:40-44.
40. Florey E, Kriebel ME. 1983. Changes in acetylcholine concentration, miniature end-plate potentials and synaptic vesicles in frog neuromuscular preparations during lanthanum treatment. Comp Biochem Physiol C 75:285-294.
41. Forsman CA, Elfvin LG. 1983. An ultra-structural study of presynaptic membrane specializations in sympathetic ganglia of 4-aminopyridine treated guinea pigs and rats. Brain Res 280:355-360.
42. Forzan M, Wirblich C, Roy P. 2004. A capsid protein of nonenveloped Bluetongue virus exhibits membrane fusion activity. Proc Nat Acad Sci USA 101:21002105.
43. Fox GQ. 1988. A morphometric analysis of synaptic vesicle distributions. Brain Res 475:103-117.
44. Fox GQ, Kriebel ME. 1994. Dynamic responses of presynaptic terminal membrane pools to electrical simulation. Brain Res 660:113-128.
45. Fox GQ. 1996. A morphormetric analysis of exocytosis in KCl-stimulated bovine chromaffin cells. Cell Tissue Res 284:303-316.
46. Galla HJ, Sackmann E. 1975. Chemically induced lipid phase separation in model membranes containing charged lipids: a spin label study. Biochim Biophys Acta 401:509-521.
47. Garofalo RS, Satir BH. 1984. Paramecium secretory granule content: quantitative studies on in vitro expansion and its regulation by calcium and pH. J Cell Biol 99:2193-2199.
48. Gibbons DL, Vaney MC, Roussel A, Vigoroux A, Reilly B, Lepault J, Kiellan M, Rey FA. 2004. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427:320-325.
49. Gilligan DM, Satir BH. 1983. Stimulation and inhibition of secretion in Paramecium: role of divalent cations. J Cell Biol 97:224-234.
50. Gulley RL, Landis DM, Reese TS. 1978. Internal organization of membranes at end bulbs of Held in the anteroventral cochlear nucleus. J Comp Neurol 180:707-741.
51. Haimann C, Torri-Tarelli F, Fesce R, Ceccarelli B. 1985. Measurement of quantal secretion induced by ouabain and its correlation with depletion of synaptic vesicles. J Cell Biol 101:1953-1965.
52. Harlow M, Ress D, Koster A, Marshall RM, Schwarz M, McMahan UJ. 1998. Dissection of active zones at the neuromuscular junction by EM tomography. J Physiol Paris 92:75-78.
53. Harlow ML, Ress D, Stoschek A, Marshall RM, McMahan UJ. 2001. The architecture of active zone material at the frog's neuromuscularjunction. Nature 409:479-484.
54. Heidelberger R, Heinemann C, Neher E, Matthews G. 1994. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371:513-515.
55. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. 1999. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 94:3791-3799.
56. Heinrich V, Ritchie K, Mohandas N, Evans E. 2001. Elastic thickness compressibilty of the red cell membrane. Biophys J 81:1452-1463.
57. Heuser JE, Reese TS, Dennis MJ, Jan Y, Jan L, Evans L. 1979. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol 81:275-300.
58. Heuser JE, Reese TS. 1981. Structural changes after transmitter release at the frog neuromuscular junction. J Cell Biol 88:564-580.
59. Hibino M, Shigemori M, Itoh H, Nagayama K, Kinosita K Jr. 1991. Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential. Biophys J 59:209-220.
60. Hibino M, Itoh H, Kinosita K Jr. 1993. Time courses of cell electroporation as revealed by submicrosecond imaging of transmembrane potential. Biophys J 64:1789-1800.
61. Horrigan FT, Bookman RJ. 1994. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13:1119-1129.
62. Hunt JM, Silinsky EM. 1993. Ionomycin-induced acetylcholine release and its inhibition by adenosine at frog motor nerve endings. Br J Pharmacol 110:828-832.
63. 2+ binding to retinal lipid membranes: consequences for lipid organization. Biophys J 78:3011-3018.
64. Jahn R, Grubmuller H. 2002. Membrane fusion. Curr Opin Cell Biol 14:488-495.
65. Jahn R, Lang T, Sudhof TC. 2003. Membrane fusion. Cell 112:519-533.
66. Jena BP. 2003. Fusion pore or porosome: structure and dynamics. J Endocrinol 176:169-174.
67. Katz B, Miledi R. 1979. Estimates of quantal content during "chemical potentiation" of transmitter release. Proc Royal Soc Lond B 205:369-378.
68. Kita H, Van Der Klotz W. 1976. Effects of the ionophore X-537A on acetylcholine release at the frog neuromuscular junction. J Physiol 259:177-198.
69. Korn H, Faber DS. 1987. Regulation and significance of probabilistic release mechanisms at central synapses. In: Edelman GM, Gall WE, Cowan WM, editors. Synaptic function. New York: John Wiley and Sons. p 57-108.
70. Koval LM, Yavorskaya EN, Lukyanetz EA. 2001. Electron microscopic evidence for multiple types of secretory vesicles in bovine chromaffin cells. Gen Comp Endocrinol 121:261-277.
71. Kriebel ME, Gross CE. 1974. Multimodal distribution of frog miniature endplate potentials in adult denervated and tadpole leg muscles. J Gen Physiol 64:85-103.
72. Kriebel ME, Stopler DR. 1975. Non-Poisson distribution in time of small- and large-mode miniature end-plate potentials. Am J Physiol 229:1321-1329.
73. Kriebel ME, Llados F, Matteson DR. 1976. Spontaneous subminiature end-plate potentials in mouse diaphragm muscle: evidence of synchronous release. J Physiol 262:553-581.
74. Kriebel ME, Keller B, Holsapple J, Fox GQ, Pappas GD. 2000. Porocytosis: fusion pore array secretion of neurotransmitter. Neuroscientist 6:422-427.
75. Kriebel M, Keller B, Silver RB, Fox GQ, Pappas GD. 2001. Porocytosis: quantal synaptic secretion by an array of pores. Brain Res 38:20-32.
76. Kuffler SW, Yoshikami D. 1975. The number of transmitter molecules in a quantum: an estimate from iontophoretic application of acetylcholine at the neuromuscular synapse. J Physiol 251:465-482.
77. Lentz BR, McIntyre GF, Parks DJ, Yates JC, Massenburg D. 1992. Bilayer curvature and certain amphipaths promote poly(ethylene glycol)-induced fusion of dipalmitoylphosphatidylcholine unilamellar vesicles. Biochemistry 31:2643-2653.
78. Leontiadou H, Mark AE, Marrink SJ. 2004. Molecular simulations of hydrophilic pores in lipid bilayers. Biophys J 86:56-64.
79. Llados FT, Kriho V, Pappas GD. 1988. Immunocytochemical localization of alpha-actinin in frog muscle treated with the ionophore A23187. Muscle Nerve 11:953-956.
80. Llinás R, Heuser J. 1977. Depolarization-release coupling systems in neurons. Neurosci Res Prog Bull 15:555-587.
81. Llinás R, Sugimori M, Silver RB. 1991. Imaging preterminal calcium concentration microdomains in the squid giant synapse. Biol Bull 181:316-317.
82. Llinás R, Sugimori M, Silver RB. 1992. Microdomains of high calcium concentration in a presynaptic terminal. Science 256:677-679.
83. Lowen SB, Cash SS, Poo M-M, Teich MC. 1997. Quantal neurotransmitter secretion rate exhibits fractal behavior. J Neurosci 17:5666-5677.
84. Macucci M, Hess K, Iafrate GJ. 1993. Electronic energy spectrum and the concept of capacitance in quantum dots. Phys Rev B Condens Matter 48:17354-17363.
85. Martin GG, Lin HM, Luc C. 1999. Reexamination of hemocytes in brine shrimp (Crustacea, brachipodia). J Morphol 242:283-294.
86. 2+-regulated secretory organelles. Eur J Cell Biol 80:775-783.
87. Melikov KC, Samsonov AV, Pirutin SK, Frolov VA. 1999. Study of conductance changes of bilayer lipid membrane induced by electric field. Membr Cell Biol 13:121-130.
88. Melikov KC, Frolov VA, Shcherbakov A, Samsonov AV, Chizmadzhev YA, Chernomordik LV. 2001. Voltage-induced nonconductive pre-pores and metastable single pores in unmodified planar lipid bilayer. Biophys J 80:1829-1836.
89. Melikyan GB, Barnard RJ, Markosyan RM, Young JA, Cohen FS. 2004. Low pH is required for avian sarcoma and leukosis virus Env-induced hemifusion and fusion pore formation but not for pore growth. J Virol 78:3753-3762.
90. Miledi R. 1967. Spontaneous synaptic potentials and quantal release of transmitter in the stellate ganglion of the squid. J Physiol 192:379-406.
91. Modis Y, Ogata S, Clements D, Harrison SC. 2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313-319.
92. Muniak CG, Kriebel ME, Carlson CG. 1982. Changes in MEPP and EPP amplitude distributions in the mouse diaphragm during synapse formation and degeneration. Dev Brain Res 5:123-138.
93. Nanavati C, Markin VS, Oberhauser AF, Fernandez JM. 1992. The exocytotic fusion pore modeled as a lipidic pore. Biophys J 63:1118-1132.
94. Neher E, Marty A. 1982. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci USA 79:6712-6716.
95. Nyquist H. 1928. Certain topics in telegraph transmission theory. Trans AIEE 47:617-644.
96. Olbrich K, Rawicz W, Needham D, Evans E. 2000. Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys J 79:321-327.
97. Ohki S. 1984. Effects of divalent cations, temperature, osmotic pressure gradient, and vesicle curvature on phosphatidylserine vesicle fusion. J Membr Biol 77:265-275.
98. Ornberg RL, Reese TS. 1981. Beginning of exocytosis captured by rapid-freezing of Limulus amebocytes. J Cell Biol 90:40-54.
99. Ortiz A, Killian JA, Verkleij AJ, Wilschut J. 1999. Membrane fusion and the lamellar-to-inverted-hexagonal phase transition in cardiolipin vesicle systems induced by divalent cations. Biophys J 77:2003-2014.
100. Palay SL, Palade GE. 1954. Electron microscopic observations of interneuronal and neuromuscular synapses. Anat Rec 118:335.
101. Palay SL, Palade GE. 1955. The fine structure of neurons. J Biophys Biochem Cytol 1:69-88.
102. Palay SL. 1956. Synapses in the central nervous system. J Biophys Biochem Cytol 2(Suppl):193-202.
103. ++-ATPase activity at the frog neuromuscular junction. J Neurocytol 17:417-423.
104. Pappas GD, Kriho V, Becker RP. 1988. Fine structural correlates of calcium dynamics in the presynaptic terminal. In: Zimmerman H, editor. Cellular and molecular basis of synaptic transmission. New York: Springer-Verlag. p 121-136.
105. Pawson PA, Grinnell AD, Wolowske B. 1998. Quantitative freeze-fracture analysis of the frog neuromuscular junction synapse: I, naturally occurring variability in active zone structure. J Neurocytol 5:361-377.
106. Peacocke AR. 1983. The physical chemistry of biological organization. New York: Oxford Science Publications. chap 4.
107. Peaker M, Wilde CJ. 1996. Feedback control of milk secretion from milk. J Mamm Gland Biol Neoplas 1:307-315.
108. Plattner H, Artalejo AR, Neher E. 1997. Ultrastructural organization of bovine chromaffin cell cortex-analysis by cryofixation and morphometry of aspects pertinent to exocytosis. J Cell Biol 139:1709-1717.
109. Pumplin DW, Reese TS, Llinás R. 1981. Are the presynaptic membrane particles the calcium channels? Proc Nat Acad Sci USA 78:7210-7213.
110. Ravoo BJ, Weringa WD, Engberts JB. 1999. Membrane fusion in vesicles of oligomerizable lipids. Biophys J 76:374-386.
111. 2+-dependent neurotransmitter release. Cell 104:71-81.
112. Rorsman P, Renstrom E. 2003. Insulin granule dynamics in pancreatic beta cells. Diabetologia 46:1029-1045.
113. Rose SJ, Pappas GD, Kriebel ME. 1978 The fine structure of identified frog neuromuscular junctions in relation to synaptic activity. Brain Res 144:213-239.
114. Rupert LA, van Breemen JF, van Bruggen EF, Engberts JB, Hoekstra D. 1987. Calcium-induced fusion of didodecylphosphate vesicles: the lamellar to hexagonal II (HII) phase transition. J Membr Biol. 95:255-263.
115. Saegusa C, Fukuda M, Mikoshiba K. 2002. Synaptotagmin V is targeted to densecore vesicles that undergo calcium-dependent exocytosis in PC12 cells. J Biol Chem 277:24499-24505.
116. Sagen J, Pappas GD. 1987. Morphological and functional correlates of chromaffin cell transplants in CNS pain modulatory regions. Ann NY Acad Sci 495:306-333.
117. Satir P, Satir B. 1974. Partition coefficient of membrane particles in the fusion rosette. Exp Cell Res 89:404-407.
118. 2+ gates. Science 199:536-538.
119. Schaeffer SF, Raviola E, Heuser JE. 1982. Membrane specializations in the outer plexiform layer of the turtle retina. J Comp Neurol 204:253-267.
120. Schindler H. 1980. Autocatalytic transport of the peptide antibiotics suzukacillin and alamethicin across lipid membranes. FEBS Lett 122:77-79.
121. Schneggenburger R, Meyer AC, Neher E. 1999. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23:399-409.
122. Schneggenburger R, Sakaba T, Neher E. 2002. Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206-212.
123. Schikorski T, Stevens CF. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858-5867.
124. Schnetkamp PP, Kaupp UB. 1985. Calcium-hydrogen exchange in isolated bovine rod outer segments. Biochemistry 24:723-727.
125. Seagar M, Leveque C, Charvin N, Marqueze B, Martin-Moutot N, Boudier JA, Boudier JL, Shoji-Kasai Y, Sato K, Takahashi M. 1999. Interactions between proteins implicated in exocytosis and voltage-gated calcium channels. Philos Trans R Soc Lond B Biol Sci 354:289-297.
126. Segawa A, Loffredo F, Puxeddu R, Yamashina S, Testa Riva F, Riva A. 1998. Exocytosis in human salivary glands visualized by high-resolution scanning electron microscopy. Cell Tissue Res 291:325-336.
127. Shannon CE. 1949. Communicaiton in the presence of noise. Proc Inst Rario Engin 37:10-21.
128. 2+-dependent aequorin luminescence of microdomains and QEDs in pre-synaptic terminals. Biol Bull 187:293-299.
129. Silver RB, Kriebel M, Keller B, Pappas GD. 2001. Porocytosis: quantal synaptic secretion at the neuromuscular junction. Biol Bull 201:263-264.
130. Silver RB, Kriebel M, Keller B, Pappas GD. 2003. Porocytosis: secretion from small and medium diameter vesicles and vesicle arrays without membrane fusion. J Neurocytol 32:277-291.
131. Silvius JR, Gagne J. 1984. Calcium-induced fusion and lateral phase separations in phosphatidylcholine-phosphatidylserine vesicles: correlation by calorimetric and fusion measurements. Biochemistry 23:3241-3247.
132. Skehel JJ, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Ann Rev Biochem 69:531-569.
133. Sugimori M, Lang EJ, Silver RB, Llinás R. 1994. High resolution measurement of the time course of calcium-concentration microdomains at squid presynaptic terminals. Biol Bull 187:300-303.
134. 2+-dependent protein interactions mediated by the C2A domains of synaptotagmins. Biochemistry 39:2940-2949.
135. Sundler R, Papahadjopoulos D. 1981. Control of membrane fusion by phospholipid head groups: I, phosphatidate/phosphatidylinositol specificity. Biochim Biophys Acta 649:743-750.
136. Taraska JW, Perrais D, Ohara-Imaizumi M, Nagamatsu S, Almers W. 2003. Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci USA 100:2070-2075.
137. Taraska JW, Almers W. 2004. Bilayers merge even when exocylosis is transient. Proc Natl Acad Sci USA 101:8780-8785.
138. Tekle E, Astumian RD, Chock PB. 1994. Selective and asymmetric molecular transport across electroporated cell membranes. Proc Nat Acad Sci USA 91:11512-11516.
139. Tekle E, Astumian RD, Friauf WA, Chock PB. 2001. Asymmetric pore distribution and loss of membrane lipid in electroporated DOPC vesicles. Biophys J 81:960-968.
140. Tieleman DP, Leontiadou H, Mark AE, Siewert-Jan Marrink S-J. 2003. Simulation of pore formation in lipid bilayers by mechanical and electric fields. J Am Chem Soc 125:6382-6383.
141. Tokunaga A, Akert K, Sandri C. 1979. Three types of membrane modulations during transmitter release in rat spinal cord synapses. Neurosci Lett 12:147-152.
142. Tomohiro T, Ogawa Y, Okuno H, Kodaka M. 2003. Synthesis and spectroscopic analysis of chromophoric lipids inducing pH-dependent liposome fusion. J Am Chem Soc 125:14733-14740.
143. Torri-Tarelli F, Grohovaz F, Fesce R, Ceccarelli B. 1985. Temporal coincidence between synaptic vesicle fusion and quantal secretion of acetylcholine. J Cell Biol 101:1386-1399.
144. Travis ER, Wightman RM. 1999. Spatiotemporal resolution of exocytosis from individual cells. Ann Rev Biophys Biomol Struct 27:77-103.
145. Triller A, Korn H. 1985. Activity-dependent deformations of presynaptic grids at central synapses. J Neurocytol 14:177-192.
146. Uvnas B, Aborg CH. 1980. Possible role of nerve impulse induced sodium ion flux in a proposed multivesicular fractional release of adrenaline and noradrenaline from the chromaffin cell. Acta Physiol Scand 109:363-368.
147. Vautrin J, Mambrini J. 1981. Characteristics of the unitary end-plate potential of the frog. J Physiol (Paris) 77:999-1010.
148. Vautrin J, Kriebel M. 1991. Focal, extracellular recording of slow miniature junctional potentials at the mouse neuromuscular junction. J Neurosci Res 31:502-506.
149. Vautrin J, Kriebel M. 1992. Characteristics of slow-miniature endplate currents show a subunit composition. Neuroscience 41:71-88.
150. Walter P, Gilmore R, Blobel G. 1984. Protein translocation across the endoplasmic reticulum. Cell 38:5-8.
151. Weikl TR, Lipowsky R. 2001. Adhesion-induced phase behavior of multicomponent membranes. Phys Rev E Stat Nonlin Soft Matter Phys 64:011903.
152. Wiegand H, Papadopoulos R, Csicsaky M, Kramer U. 1984. The action of thallium acetate on spontaneous transmitter release in the rat neuromuscular junction. Arch Toxicol 55:253-257.
153. Wilhelm C, Winterhalter M, Zimmermann U, Benz R. 1993. Kinetics of pore size during irreversible electrical breakdown of lipid bilayer membranes. Biophys J 64:121-128.
154. Wilschut J, Duzgunes N, Papahadjopoulos D. 1981. Calcium/magnesium specificity in membrane fusion: kinetics of aggregation and fusion of phosphatidylserine vesicles and the role of bilayer curvature. Biochemistry 20:3126-3133.
155. Wilschut J, Duzgunes N, Hoekstra D, Papahadjopoulos D. 1985. Modulation of membrane fusion by membrane fluidity: temperature dependence of divalent cation induced fusion of phosphatidylserine vesicles. Biochemistry 24:8-14.
156. Winfree AT. 1977. Spatial and temporal organization in the Zhabotinsky reaction. Adv Biol Med Phys 16:115-136.
157. Zhitenev NB, Brodsky M, Ashoori RC, Pfeiffer LN, West KW. 1999. Localization-delocalization transition in quantum dots. Science 285:715-718.
158. Zimmerman H, Denston CR. 1977. Recycling of synaptic vesicles in the cholinergic synapses of the Torpedo electric organ during induced transmitter release. Neuroscience 2:695-714.
159. Zimmermann H. 1982. Neurotransmitter vesicles. New York: Academic Press. p 241-259.