Dr. Silver is in the Departments of Pharmacology, Physiology, and Radiology, School of Medicine, Department of Biomedical Engineering, and College of Engineering at Wayne State University, Detroit, MI. He also holds appointments at the John D. Dingell VA Medical Center, Detroit, MI, and the Decision and Information Sciences Division, Argonne National Laboratory, Argonne, IL.
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Secretion without membrane fusion: Porocytosis
Article first published online: 25 JAN 2005
DOI: 10.1002/ar.b.20050
Copyright © 2005 Wiley-Liss, Inc.
Issue
The Anatomical Record Part B: The New Anatomist
Volume 282B, Issue 1, pages 18–37, January 2005
Additional Information
How to Cite
Silver, R. B. and Pappas, G. D. (2005), Secretion without membrane fusion: Porocytosis. Anat. Rec., 282B: 18–37. doi: 10.1002/ar.b.20050
Publication History
- Issue published online: 25 JAN 2005
- Article first published online: 25 JAN 2005
Funded by
- NSF MCB. Grant Number: 9602056
- U.S. Department of Veterans Affairs
- National Institutes of Health. Grant Number: DA 01551
LITERATURE CITED
- , , , , , . 1999. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat Cell Biol 1: E3–E4.
- , , , , . 2001. Dynamics of intracellular granules with CD63-GFP in rat basophilic leukemia cells. J Biochem (Tokyo) 129: 739–744.
- . 2001. Functional and physical coupling of voltage-sensitive calcium channels with exocytotic proteins: ramifications for the secretion mechanism. J Neurochem 77: 972–985.Direct Link:
- , . 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.
- . 1994. The binding and lysis of target cells by cytotoxic lymphocytes: molecular and cellular aspects. Ann Rev Immunol 12: 735–773.
- . 1997. A view of exocytotic vesicle fusion in living secretory cells. Hepatology 26: 241–243.Direct Link:
- , . 2002. The effect of metal cations on the phase behavior and hydration characteristics of phospholipid membranes. Chem Phys Lipids 115: 39–61.
- , , . 1960. The fine structure of the neuromuscular junction of the frog. J Physiol 134: 134–144.
- , . 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.
- , , , , , , . 1999. Acetylcholine synthesis and quantal release reconstituted by transfection of mediatophore and choline acetyltransferase cDNAs. Eur J Neurosci 11: 1523–1534.Direct Link:
- , , , , . 2000. Localization in artificial disorder: two coupled quantum dots. Phys Rev Lett 85: 2356–2359.
- , , . 2001. Endocytosis and signaling cascades: a close encounter. FEBS Lett 498: 190–196.
- , . 1999. Lipid vesicles and membrane fusion. Adv Drug Deliv Rev 38: 207–232.
- , , . 2000. The role of membrane lateral tension in calcium-induced membrane fusion. J Membr Biol 176: 67–75.
- , , , , , , . 2003. New cationic lipids form channel-like pores in phospholipid bilayers. Biophys J 84: 1750–1755.
- , , , . 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.
- , , , , , . 1999. Gadolinium induces domain and pore formation of human erythrocyte membrane: an atomic force microscopic study. Biochim Biophys Acta 142: 249–260.
- , , , , , , . 2004. Structure, isolation, composition and reconstitution of the neuronal fusion pore. Cell Biol Int Rep 28: 699–708.
- , , , , . 2004. Chromaffin granules in the rat adrenal medulla release their secretory content in a particulate fashion. Anat Rec 227A: 204–208.Direct Link:
- , . 1994. Calcium-dependent postsynaptic exocytosis: a possible mechanism for activity-dependent synaptic modulation. J Neurobiol 25: 336–341.Direct Link:
- , . 1954. Quantal components of the end-plate potential. J Physiol 124: 560–573.
- , . 1957. La base “quantale” de la transmission neuro-musculaire. CNRS Paris 67: 245–258.
- , . 1967. Co-operative action of calcium ions in at the neuromuscular junction. J Physiol 193: 419–432.
- , , , . 1981. The hagfish slime gland: a model system for studying the biology of mucus. Science 214: 1143–1145.
- , , , , , , , . 2003. Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422: 176–180.
- , . 1999. Heightened sensitivity of a lattice of membrane receptors. Proc Nat Acad Sci USA 96: 10104–10108.
- , . 1995. Mediatophore and other presynaptic proteins: a cybernetic linking at the active zone. J Physiol Paris 89: 147–156.
- , . 2000. Neurotransmitter release at rapid synapses. Biochimie 82: 289–302.
- , . 1981. Fusion of small unilamellar liposomes with phospholipid planar bilayer membranes and large single-bilayer vesicles. Biochim Biophys Acta 640: 734–747.
- , , , . 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.
- . 1991. Basophil and mast cell degranulation and recovery. In: HarrisJR, editor. Blood cell biochemistry, vol. 4. New York: Plenum Press. p 340–377.
- . 2000. Ultrastructural features of human basophil and mast cell secretory function. In: MaroneG, LichtensteinLM, GalliSJ, editors. Mast cells and basophils. New York: Academic Press. p 63–88.
- , . 1985. Membrane-bound choline acetyltransferase in Torpedo electric organ: a marker for synaptosomal plasma membranes? Neuroscience 15: 577–589.
- , . 1988a. Subunit composition of the spontaneous miniature endplate currents at the mouse neuromuscular junction. J Physiol 400: 659–676.
- , . 1988b. Characteristics of spontaneous miniature and subminiature end-plate currents at the mouse neuromuscular junction. J Physiol 400: 645–658.
- , , , . 2003. Dynamic tension spectroscopy and strength of biomembranes. Biophys J 85: 2342–2350.
- , . 1952. Spontaneous subthreshold activity at motor nerve endings. J Physiol 117: 109–128.
- , , , . 1994. Neurotransmitter release: fusion or “kiss and run.” Trends Cell Biol 4: 1–4.
- , . 1999. Peeping at the vesicle kiss. Nat Cell Biol 1: 40–44.
- , . 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.
- , . 1983. An ultrastructural study of presynaptic membrane specializations in sympathetic ganglia of 4-aminopyridine treated guinea pigs and rats. Brain Res 280: 355–360.
- , , . 2004. A capsid protein of nonenveloped Bluetongue virus exhibits membrane fusion activity. Proc Nat Acad Sci USA 101: 21002105.
- . 1988. A morphometric analysis of synaptic vesicle distributions. Brain Res 475: 103–117.
- , . 1994. Dynamic responses of presynaptic terminal membrane pools to electrical simulation. Brain Res 660: 113–128.
- . 1996. A morphometric analysis of exocytosis in KCl-stimulated bovine chromaffin cells. Cell Tissue Res 284: 303–316.
- , . 1975. Chemically induced lipid phase separation in model membranes containing charged lipids: a spin label study. Biochim Biophys Acta 401: 509–521.
- , . 1984. Paramecium secretory granule content: quantitative studies on in vitro expansion and its regulation by calcium and pH. J Cell Biol 99: 2193–2199.
- , , , , , , , . 2004. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427: 320–325.
- , . 1983. Stimulation and inhibition of secretion in Paramecium: role of divalent cations. J Cell Biol 97: 224–234.
- , , . 1978. Internal organization of membranes at end bulbs of Held in the anteroventral cochlear nucleus. J Comp Neurol 180: 707–741.Direct Link:
- , , , . 1985. Measurement of quantal secretion induced by ouabain and its correlation with depletion of synaptic vesicles. J Cell Biol 101: 1953–1965.
- , , , , , . 1998. Dissection of active zones at the neuromuscular junction by EM tomography. J Physiol Paris 92: 75–78.
- , , , , . 2001. The architecture of active zone material at the frog's neuromuscular junction. Nature 409: 479–484.
- , , , . 1994. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371: 513–515.
- , , , , . 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.
- , , , . 2001. Elastic thickness compressibilty of the red cell membrane. Biophys J 81: 1452–1463.
- , , , , , . 1979. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol 81: 275–300.
- , . 1981. Structural changes after transmitter release at the frog neuromuscular junction. J Cell Biol 88: 564–580.
- , , , , 1991. Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential. Biophys J 59: 209–220.
- , , 1993. Time courses of cell electroporation as revealed by submicrosecond imaging of transmembrane potential. Biophys J 64: 1789–1800.
- , . 1994. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13: 1119–1129.
- , . 1993. Ionomycin-induced acetylcholine release and its inhibition by adenosine at frog motor nerve endings. Br J Pharmacol 110: 828–832.
- , , . 2000. Strength of Ca2+ binding to retinal lipid membranes: consequences for lipid organization. Biophys J 78: 3011–3018.
- , . 2002. Membrane fusion. Curr Opin Cell Biol 14: 488–495.
- , , . 2003. Membrane fusion. Cell 112: 519–533.
- . 2003. Fusion pore or porosome: structure and dynamics. J Endocrinol 176: 169–174.
- , . 1979. Estimates of quantal content during “chemical potentiation” of transmitter release. Proc Royal Soc Lond B 205: 369–378.
- , . 1976. Effects of the ionophore X-537A on acetylcholine release at the frog neuromuscular junction. J Physiol 259: 177–198.
- , . 1987. Regulation and significance of probabilistic release mechanisms at central synapses. In: EdelmanGM, GallWE, CowanWM, editors. Synaptic function. New York: John Wiley and Sons. p 57–108.
- , , . 2001. Electron microscopic evidence for multiple types of secretory vesicles in bovine chromaffin cells. Gen Comp Endocrinol 121: 261–277.
- , . 1974. Multimodal distribution of frog miniature endplate potentials in adult denervated and tadpole leg muscles. J Gen Physiol 64: 85–103.
- , . 1975. Non-Poisson distribution in time of small- and large-mode miniature end-plate potentials. Am J Physiol 229: 1321–1329.
- , , . 1976. Spontaneous subminiature end-plate potentials in mouse diaphragm muscle: evidence of synchronous release. J Physiol 262: 553–581.
- , , , , . 2000. Porocytosis: fusion pore array secretion of neurotransmitter. Neuroscientist 6: 422–427.
- , , , , . 2001. Porocytosis: quantal synaptic secretion by an array of pores. Brain Res 38: 20–32.
- , . 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.
- , , , , . 1992. Bilayer curvature and certain amphipaths promote poly(ethylene glycol)-induced fusion of dipalmitoylphosphatidylcholine unilamellar vesicles. Biochemistry 31: 2643–2653.
- , , . 2004. Molecular simulations of hydrophilic pores in lipid bilayers. Biophys J 86: 56–64.
- , , . 1988. Immunocytochemical localization of alpha-actinin in frog muscle treated with the ionophore A23187. Muscle Nerve 11: 953–956.Direct Link:
- , . 1977. Depolarization-release coupling systems in neurons. Neurosci Res Prog Bull 15: 555–587.
- , , . 1991. Imaging preterminal calcium concentration microdomains in the squid giant synapse. Biol Bull 181: 316–317.
- , , . 1992. Microdomains of high calcium concentration in a presynaptic terminal. Science 256: 677–679.
- , , , . 1997. Quantal neurotransmitter secretion rate exhibits fractal behavior. J Neurosci 17: 5666–5677.
- , , . 1993. Electronic energy spectrum and the concept of capacitance in quantum dots. Phys Rev B Condens Matter 48: 17354–17363.
- , , . 1999. Reexamination of hemocytes in brine shrimp (Crustacea, brachipodia). J Morphol 242: 283–294.Direct Link:
- , , , , . 2001. A parafusin-related Toxoplasma protein in Ca2+-regulated secretory organelles. Eur J Cell Biol 80: 775–783.
- , , , . 1999. Study of conductance changes of bilayer lipid membrane induced by electric field. Membr Cell Biol 13: 121–130.
- , , , , , . 2001. Voltage-induced nonconductive pre-pores and metastable single pores in unmodified planar lipid bilayer. Biophys J 80: 1829–1836.
- , , , , . 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.
- . 1967. Spontaneous synaptic potentials and quantal release of transmitter in the stellate ganglion of the squid. J Physiol 192: 379–406.
- , , , . 2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427: 313–319.
- , , . 1982. Changes in MEPP and EPP amplitude distributions in the mouse diaphragm during synapse formation and degeneration. Dev Brain Res 5: 123–138.
- , , , . 1992. The exocytotic fusion pore modeled as a lipidic pore. Biophys J 63: 1118–1132.
- , . 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.
- . 1928. Certain topics in telegraph transmission theory. Trans AIEE 47: 617–644.
- , , , . 2000. Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys J 79: 321–327.
- . 1984. Effects of divalent cations, temperature, osmotic pressure gradient, and vesicle curvature on phosphatidylserine vesicle fusion. J Membr Biol 77: 265–275.
- , . 1981. Beginning of exocytosis captured by rapid-freezing of Limulus amebocytes. J Cell Biol 90: 40–54.
- , , , . 1999. Membrane fusion and the lamellar-to-inverted-hexagonal phase transition in cardiolipin vesicle systems induced by divalent cations. Biophys J 77: 2003–2014.
- , . 1954. Electron microscopic observations of interneuronal and neuromuscular synapses. Anat Rec 118: 335.
- , . 1955. The fine structure of neurons. J Biophys Biochem Cytol 1: 69–88.
- . 1956. Synapses in the central nervous system. J Biophys Biochem Cytol 2( Suppl): 193–202.
- , . 1988. Fine structural localization of Ca++-ATPase activity at the frog neuromuscular junction. J Neurocytol 17: 417–423.
- , , . 1988. Fine structural correlates of calcium dynamics in the presynaptic terminal. In: ZimmermanH, editor. Cellular and molecular basis of synaptic transmission. New York: Springer-Verlag. p 121–136.
- , , . 1998. Quantitative freeze-fracture analysis of the frog neuromuscular junction synapse: I, naturally occurring variability in active zone structure. J Neurocytol 5: 361–377.
- . 1983. The physical chemistry of biological organization. New York: Oxford Science Publications. chap 4.
- , . 1996. Feedback control of milk secretion from milk. J Mamm Gland Biol Neoplas 1: 307–315.
- , , . 1997. Ultrastructural organization of bovine chromaffin cell cortex-analysis by cryofixation and morphometry of aspects pertinent to exocytosis. J Cell Biol 139: 1709–1717.
- , , . 1981. Are the presynaptic membrane particles the calcium channels? Proc Nat Acad Sci USA 78: 7210–7213.
- , , . 1999. Membrane fusion in vesicles of oligomerizable lipids. Biophys J 76: 374–386.
- , , , , , , . 2001. Complexins regulate a late step in Ca2+-dependent neurotransmitter release. Cell 104: 71–81.
- , . 2003. Insulin granule dynamics in pancreatic beta cells. Diabetologia 46: 1029–1045.
- , , . 1978. The fine structure of identified frog neuromuscular junctions in relation to synaptic activity. Brain Res 144: 213–239.
- , , , , . 1987. Calcium-induced fusion of didodecylphosphate vesicles: the lamellar to hexagonal II (HII) phase transition. J Membr Biol 95: 255–263.
- , , . 2002. Synaptotagmin V is targeted to dense-core vesicles that undergo calcium-dependent exocytosis in PC12 cells. J Biol Chem 277: 24499–24505.
- , . 1987. Morphological and functional correlates of chromaffin cell transplants in CNS pain modulatory regions. Ann NY Acad Sci 495: 306–333.Direct Link:
- , . 1974. Partition coefficient of membrane particles in the fusion rosette. Exp Cell Res 89: 404–407.
- , . 1978. Paramecium fusion rosettes: possible function as Ca2+ gates. Science 199: 536–538.
- , , . 1982. Membrane specializations in the outer plexiform layer of the turtle retina. J Comp Neurol 204: 253–267.Direct Link:
- . 1980. Autocatalytic transport of the peptide antibiotics suzukacillin and alamethicin across lipid membranes. FEBS Lett 122: 77–79.
- , , . 1999. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23: 399–409.
- , , . 2002. Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25: 206–212.
- , . 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17: 5858–5867.
- , . 1985. Calcium-hydrogen exchange in isolated bovine rod outer segments. Biochemistry 24: 723–727.
- , , , , , , , , , . 1999. Interactions between proteins implicated in exocytosis and voltage-gated calcium channels. Philos Trans R Soc Lond B Biol Sci 354: 289–297.
- , , , , , . 1998. Exocytosis in human salivary glands visualized by high-resolution scanning electron microscopy. Cell Tissue Res 291: 325–336.
- . 1949. Communicaiton in the presence of noise. Proc Inst Rario Engin 37: 10–21.
- , , , . 1994. Time resolved imaging of Ca2+-dependent aequorin luminescence of microdomains and QEDs in pre-synaptic terminals. Biol Bull 187: 293–299.
- , , , . 2001. Porocytosis: quantal synaptic secretion at the neuromuscular junction. Biol Bull 201: 263–264.
- , , , . 2003. Porocytosis: secretion from small and medium diameter vesicles and vesicle arrays without membrane fusion. J Neurocytol 32: 277–291.
- , . 1984. Calcium-induced fusion and lateral phase separations in phosphatidylcholine-phosphatidylserine vesicles: correlation by calorimetric and fusion measurements. Biochemistry 23: 3241–3247.
- , . 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Ann Rev Biochem 69: 531–569.
- , , , . 1994. High resolution measurement of the time course of calcium-concentration microdomains at squid presynaptic terminals. Biol Bull 187: 300–303.
- , . 2000. Specificity of Ca2+-dependent protein interactions mediated by the C2A domains of synaptotagmins. Biochemistry 39: 2940–2949.
- , . 1981. Control of membrane fusion by phospholipid head groups: I, phosphatidate/phosphatidylinositol specificity. Biochim Biophys Acta 649: 743–750.
- , , , , . 2003. Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci USA 100: 2070–2075.
- , . 2004. Bilayers merge even when exocytosis is transient. Proc Natl Acad Sci USA 101: 8780–8785.
- , , . 1994. Selective and asymmetric molecular transport across electroporated cell membranes. Proc Nat Acad Sci USA 91: 11512–11516.
- , , , . 2001. Asymmetric pore distribution and loss of membrane lipid in electroporated DOPC vesicles. Biophys J 81: 960–968.
- , , , . 2003. Simulation of pore formation in lipid bilayers by mechanical and electric fields. J Am Chem Soc 125: 6382–6383.
- , , . 1979. Three types of membrane modulations during transmitter release in rat spinal cord synapses. Neurosci Lett 12: 147–152.
- , , , . 2003. Synthesis and spectroscopic analysis of chromophoric lipids inducing pH-dependent liposome fusion. J Am Chem Soc 125: 14733–14740.
- , , , . 1985. Temporal coincidence between synaptic vesicle fusion and quantal secretion of acetylcholine. J Cell Biol 101: 1386–1399.
- , . 1999. Spatio-temporal resolution of exocytosis from individual cells. Ann Rev Biophys Biomol Struct 27: 77–103.
- , . 1985. Activity-dependent deformations of presynaptic grids at central synapses. J Neurocytol 14: 177–192.
- , . 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.Direct Link:
- , . 1981. Characteristics of the unitary end-plate potential of the frog. J Physiol (Paris) 77: 999–1010.
- , . 1991. Focal, extracellular recording of slow miniature junctional potentials at the mouse neuromuscular junction. J Neurosci Res 31: 502–506.Direct Link:
- , . 1992. Characteristics of slow-miniature endplate currents show a subunit composition. Neuroscience 41: 71–88.
- , , . 1984. Protein translocation across the endoplasmic reticulum. Cell 38: 5–8.
- , . 2001. Adhesion-induced phase behavior of multicomponent membranes. Phys Rev E Stat Nonlin Soft Matter Phys 64: 011903.
- , , , . 1984. The action of thallium acetate on spontaneous transmitter release in the rat neuromuscular junction. Arch Toxicol 55: 253–257.
- , , , . 1993. Kinetics of pore size during irreversible electrical breakdown of lipid bilayer membranes. Biophys J 64: 121–128.
- , , . 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.
- , , , . 1985. Modulation of membrane fusion by membrane fluidity: temperature dependence of divalent cation induced fusion of phosphatidylserine vesicles. Biochemistry 24: 8–14.
- . 1977. Spatial and temporal organization in the Zhabotinsky reaction. Adv Biol Med Phys 16: 115–136.
- , , , , . 1999. Localization-delocalization transition in quantum dots. Science 285: 715–718.
- , . 1977. Recycling of synaptic vesicles in the cholinergic synapses of the Torpedo electric organ during induced transmitter release. Neuroscience 2: 695–714.
- . 1982. Neurotransmitter vesicles. New York: Academic Press. p 241–259.