Hostname: page-component-848d4c4894-r5zm4 Total loading time: 0 Render date: 2024-06-25T02:04:01.423Z Has data issue: false hasContentIssue false
  • English
  • Français

Time–resolved capacitance measurements: monitoring exocytosis in single cells

Published online by Cambridge University Press:  17 March 2009

Manfred Lindau
Manfred Lindau
Affiliation:
Biophysics Group, Freie Universität Berlin, Arnimallee 14, D–1000 Berlin 33, Germany
Get access Rights & Permissions [Opens in a new window]

Extract

Many cells release preformed material contained in secretory granules by exocytosis. Exocytosis is a specialized means of secretion in which the granules fuse with the plasma membrane and thereby discharge their contents through the fusion pores. This mechanism mediates, for example, the formation of the fertilization envelope in eggs, the release of neurotransmitters and neuropeptides by neurons, the release of a variety of enzymes and mediators by mast cells and granulocytes or the secretion of hormones by endocrine cells. Classical methods for investigating exocytosis usually measure release of secreted material.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 24 , Issue 1 , February 1991 , pp. 75 - 101
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adrian, R. H. & Almers, W. (1974). Membrane capacity measurements on frog skeletal muscle in media of low ion content. Journal of Physiology 273, 573–605.CrossRefGoogle Scholar
Afzelius, B. A. (1956). The ultrastructure of the cortical granules and their products in the sea urchin egg as studied with the electron microscope. Experimental Cell Research 10, 257–285.CrossRefGoogle ScholarPubMed
Almers, W. (1990). Exocytosis. Annual Reviews of Physiology 52, 607–624.CrossRefGoogle ScholarPubMed
Almers, W. & Neher, E. (1987). Gradual and stepwise changes in the membrane capacitance of rat peritoneal mast cells. Journal of Physiology 386, 205–218.CrossRefGoogle ScholarPubMed
Alvarez De Toledo, G. & Fernandez, J. M. (1988). The events leading to secretory granule fusion. In Cell Physiology of Blood (ed. Gunn, R. B. and Parker, J. C.). Society of General Physiologists series, vol. 43. pp. 333–344. New York: Rockefeller University Press.Google Scholar
Alvarez De Toledo, G. & Fernandez, J. M. (1990 a). Patch-clamp measurements reveal multimodal distribution of granule sizes in rat mast cells. Journal of Cell Biology 110, 1033–1039.CrossRefGoogle ScholarPubMed
Alvarez De Toledo, G. & Fernandez, J. M. (1990 b). The effect of GTPγS and Ca++ on the kinetics of exocytosis of single secretory granules in peritoneal mast cells. Biophysical Journal 57, 495a.Google Scholar
Alvarez De Toledo, G. & Fernandez, J. M. (1990 c). Compound versus multigranular exocytosis in peritoneal mast cells. Journal of General Physiology 95, 397–409.CrossRefGoogle ScholarPubMed
Breckenridge, L. J. & Almers, W. (1987 a). Final steps in exocytosis observed in a cell with giant secretory granules.Proceedings of the National Academy of Sciences, USA 84, 1945–1949.CrossRefGoogle Scholar
Breckenridge, L. J. & Almers, W. (1987 b). Currents through the fusion pore that forms during exocytosis of a secretory vesicle, Nature 328, 814–817.CrossRefGoogle ScholarPubMed
Chandler, D. E. & Kazilek, C. J. (1987). Calcium signals in neutrophils can be divided into three distinct phases. Biochimica et Biophysica Acta 931, 175–179.CrossRefGoogle ScholarPubMed
Chandler, D. E., Whitaker, M. & Zimmerberg, J. (1989). High molecular weight polymers block cortical granule exocytosis in sea urchin eggs at the level of granule matrix disassembly. Journal of Cell Biology 109, 1269–1278.CrossRefGoogle ScholarPubMed
Clapham, D. E. & Neher, E. (1984). Trifluoperazine reduces inward ionic currents and secretion by separate mechanisms in bovine chromaffin cells. Journal of Physiology 353, 541–564.CrossRefGoogle ScholarPubMed
Clausen, C. & Dixon, T. E. (1986). Membrane electrical parameters in turtle pseudemys-scripta-elegans bladder measured using impedance–analysis techniques. Journal of Membrane Biology 92, 9–20.CrossRefGoogle Scholar
Clausen, C. & Fernandez, J. M. (1981). A low-cost method for rapid transfer function measurements with direct application to biological impedance analysis. Pflügers Archiv 390, 290–295.CrossRefGoogle ScholarPubMed
Clausen, C., Machen, T. E. & Diamond, J. M. (1983). Use of alternating current impedance analysis to study membrane changes related to acid secretion in amphibian gastric mucosa. Biophysical Journal 41, 167–178.CrossRefGoogle Scholar
Cole, K. S. (1935). Electric impedance of Hipponoe eggs. Journal of General Physiology 18, 877–887.CrossRefGoogle ScholarPubMed
Cole, K. S. (1968). Membranes, Ions and Impulses. Berkeley: University of California Press.CrossRefGoogle Scholar
Curran, M. & Brodwick, M. (1985). Mast cell exocytosis and the gel-well of granules. Biophysical Journal 47, 172a.Google Scholar
Dixon, T. E., Clausen, C. & Coachman, D. (1988). Constitutive and transport-related endocytotic pathways in turtle bladder epithelium. Journal of Membrane Biology 102, 49–58.CrossRefGoogle ScholarPubMed
Fernandez, J. M. & Alvarez De Toledo, G. (1988). Defective secretory granule formation in Chediak-Hegashi mice. Biophysical Journal 53, 362a.Google Scholar
Fernandez, J. M., Lindau, M. & Eckstein, F. (1987). Intracellular stimulation of mast cells with guanine nucleotides mimic antigenic stimulation. FEBS Letters 216, 89–93.CrossRefGoogle ScholarPubMed
Fernandez, J. M., Neher, E. & Gomperts, B. D. (1984). Capacitance measurements reveal stepwise fusion events in degranulating mast cells, Nature 312, 453–455.CrossRefGoogle ScholarPubMed
Fidler, N. & Fernandez, J. M. (1989). Phase tracking: an improved phase detection technique for cell membrane capacitance measurements. Biophysical Journal 56, 1153–1162.CrossRefGoogle ScholarPubMed
Fidler Lim, N., Nowycky, M. C. & Bookman, R. J. (1990). Direct measurement of exocytosis and calcium currents in single vertebrate nerve terminals. Nature 344, 449–451.CrossRefGoogle Scholar
Gillespie, J. I. 1979. The effect of repetitive stimulation on the passive electrical properties of the prosynaptic terminal of the squid giant synapse.Proceedings of the Royal Society London Ser. B 206, 293–306.Google Scholar
Gillis, K., Pun, R. & Misler, S. (1990). Long-term monitoring of membrane capacitance changes (ΔCM) using perforated patch recording. Biophysical Journal 57, 491a.Google Scholar
Gomperts, B. D. (1983). Involvement of guanine nucleotide-binding protein in the gating of Ca2+ by receptors. Nature 306, 64–66.CrossRefGoogle ScholarPubMed
Grynkiewicz, G., Poenie, M. & Tsien, R. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. Journal of Biological Chemistry 260, 3440–3450.CrossRefGoogle ScholarPubMed
Hamill, O. P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F. J. (1981). Improved patch-clamp techniques for high-resolution recording from cells and cell-free membrane patches. Pflügers Archiv 391, 85–100.CrossRefGoogle ScholarPubMed
Heinemann, S. H., Conti, F., Stuehmer, W. & Neher, E. (1987). Effects of hydrostatic pressure on membrane processes; sodium channels, calcium channels, and exocytosis. Journal of General Physiology 90, 765–778.CrossRefGoogle ScholarPubMed
Horn, R. & Marty, A. (1988). Muscarinic activation of ionic currents measured by a new whole-cell recording method. Journal of General Physiology 92, 145–159.CrossRefGoogle ScholarPubMed
Jaffe, L. A., Hagiwara, S. & Kado, R. T. (1978). The time course of cortical vesicle fusion in sea urchin eggs observed as membrane capacitance changes. Developmental Biology 67, 243–248.CrossRefGoogle ScholarPubMed
Jaffe, L. A. & Schlichter, L. C. (1985). Fertilization-induced ionic conductances in eggs of the frog Rana pipiens. Journal of Physiology 358, 299–320.CrossRefGoogle ScholarPubMed
Jakobs, K. H., Aktories, K. & Schulz, G. (1984). Mechanism of pertussis toxin action on the adenylate cyclase system. European Journal of Biochemistry 140, 177–181.CrossRefGoogle ScholarPubMed
Jakobs, K. H., Gehring, U., Gaugler, B., Pfeuffer, T. & Schulz, G. (1983). Occurrence of an inhibitory guanine nucleotide-binding regulatory component of the adenylate cyclase system in eye variants of 849 lymphoma cells. European Journal of Biochemistry 130, 605–611.CrossRefGoogle Scholar
Joshi, C. & Fernandez, J. M. (1988). Capacitance measurements: an analysis of the phase detector technique used to study exocytosis and endocytosis. Biophysical Journal 53, 885–892.CrossRefGoogle ScholarPubMed
Kim, Y. I. & Neher, E. (1988). IgG from patients with Lambert-Eaton syndrome blocks voltage-dependent calcium channels. Science 239, 405–408.CrossRefGoogle ScholarPubMed
Lindau, M. & Fernandez, J. M. (1986 a). IgE-mediated degranulation of mast cells does not require opening of ion channels. Nature 319, 150–153.CrossRefGoogle Scholar
Lindau, M. & Fernandez, J. M. (1986 b). A patch-clamp study of histamine secreting cells. Journal of General Physiology 88, 349–368.CrossRefGoogle ScholarPubMed
Lindau, M. & Neher, E. (1988). Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflügers Archiv 411, 137–146.CrossRefGoogle ScholarPubMed
Lindau, M. & Nüße, O. (1987). Pertussis toxin does not affect the time course of exocytosis in mast cells stimulated by intracellular application of GTP-γ-S. FEBS Letters 222, 317–321.CrossRefGoogle Scholar
Lindau, M., Nüße, O., Cromwell, O., Bennett, J., Kay, A. B. & Gomperts, B. D. (1990 a). The fine structure of the capacitance changes in degranulating guinea-pig eosinophils. In preparation.Google Scholar
Lindau, M., Stuenkel, E. L. & Nordmann, J. J. (1990 b). Depolarisation, intracellular calcium and exocytosis in single vertebrate nerve endings. Neuron, submitted.Google Scholar
Maruyama, Y. (1986). Ca2+-induced excess capacitance fluctuation studied by phasesensitive detection method in exocrine pancreatic acinar cells. Pflügers Archiv 407, 561–563.CrossRefGoogle ScholarPubMed
Maruyama, Y. (1988). Agonist-induced changes in cell membrane capacitance and conductance in dialysed pancreatic acinar cells of rats. Journal of Physiology 406, 299–313.CrossRefGoogle ScholarPubMed
Maruyama, Y. (1989). Effects of external calcium on acetyl-choline-evoked increases in membrane capacitance in rat pancreatic acinar cells. Pflügers Archiv 413, 438–440.CrossRefGoogle Scholar
Mason, W. T., Sikdar, S. K. & Zorec, R. (1988). Calcium-induced cell membrane capacitance increase in bovine lactotrophs in-vitro. Journal of Physiology 407, 88 p.Google Scholar
Monck, J. R., Oberhauser, A., Alvarez De Toledo, G. & Fernandez, J. M. (1990 a). Is swelling of the secretory matrix the force that dilates the exocytotic fusion pore? Biophysical Journal, submitted.CrossRefGoogle Scholar
Monck, J. R., Alvarez De Toledo, G. & Fernandez, J. M. (1990 b). Tension in secretory granule membranes causes extensive membrane transfer through the exocytotic fusion pore.Proceedings of the National Academy of Sciences, USA. 87, in press.CrossRefGoogle Scholar
Nakamura, T. & Ui, M. (1983). Suppression of passive cutaneous anaphylaxis by pertussis toxin, an islet activating protein, as a result of inhibition of histamine release from mast cells. Biochemical Pharmacology 32, 3435–3441.CrossRefGoogle ScholarPubMed
Neher, E. (1988 a). The use of the patch-clamp technique to study second messenger-mediated cellular events. Neuroscience 26, 727–737.CrossRefGoogle ScholarPubMed
Neher, E. (1988 b). The influence of intracellular calcium concentration on degranulation of dialysed mast cells from rat peritoneum. Journal of Physiology 395, 193–214.CrossRefGoogle ScholarPubMed
Neher, E. & Marty, A. (1982). Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells.Proceedings of the National Academy of Sciences USA 79, 6712–6716.CrossRefGoogle Scholar
Nuccitelli, R. (1980). The electrical changes accompanying fertilization and cortical vesicle secretion in the medaka oryzias-latipes egg. Developmental Biology 7, 483–498.CrossRefGoogle Scholar
Nüße, O. & Lindau, M. (1988). The dynamics of exocytosis in human neutrophils. Journal of Cell Biology 107, 2117–2124.CrossRefGoogle ScholarPubMed
Nüße, O. & Lindau, M. (1990). GTP-γS induced calcium transients and exocytosis in human neutrophils. Bioscience Reports 10, 93–103.CrossRefGoogle Scholar
Nüße, O., Lindau, M., Cromwell, O., Kay, A. B. & Gomperts, B. D. (1990). Intracellular application of GTP-γ-S induces exocytotic granule fusion in guinea-pig eosinophils. Journal of Experimental Medicine 171, 775–786.CrossRefGoogle ScholarPubMed
Penner, R. (1988). Multiple signalling pathways control stimulus-secretion coupling in rat peritoneal mast cells.Proceedings of the National Academy of Sciences USA 85, 9856–9860.CrossRefGoogle Scholar
Penner, R., Matthews, G. & Neher, E. (1988). Regulation of calcium influx by second messengers in rat mast cells. Nature 334, 499–504.CrossRefGoogle ScholarPubMed
Penner, R. & Neher, E. (1988). Secretory responses of rat peritoneal mast cells to high intracellular calcium. FEBS Letters 226, 307–313.CrossRefGoogle ScholarPubMed
Penner, R., Neher, E. & Dreyer, F. (1986). Intracellularly injected tetanus toxin inhibits exocytosis in bovine adrenal chromaffin cells. Nature 324, 76–78.CrossRefGoogle ScholarPubMed
Penner, R., Pusch, M. & Neher, E. (1987). Washout phenomena in dialysed mast cells allow discrimination of different steps in stimulus-secretion coupling. Bioscience Reports 7, 313–321.CrossRefGoogle ScholarPubMed
Peres, A. & Bernardini, G. (1985). The effective membrane capacity of Xenopus eggs: its relations with membrane conductance and cortical granule exocytosis. Pflügers Archiv 404, 266–272.CrossRefGoogle ScholarPubMed
Rich, A., Dixon, T. E. & Clausen, C. (1989). Changes in membrane conductances and areas associated with bicarbonate secretion in turtle bladder. Journal of Membrane Biology 113, 211–219.CrossRefGoogle Scholar
Rothschild, L. (1957). The membrane capacitance of the sea urchin egg. Journal of Biophysical and Biochemical Cytology 3, 103–110.CrossRefGoogle ScholarPubMed
Saito, H., Okajima, F., Molski, T. F. P., Sh'afi, R. I., Ui, M. & Ishizaka, T. (1987). Effects of ADP-ribosylation of GTP-binding protein by pertussis toxin on immunoglobulin E-dependent and independent histamine release from mast cells and basophils. Journal of Immunology 138, 3927–3934.CrossRefGoogle ScholarPubMed
Schäfer, T., Karli, O. U., Schweizer, F. E. & Burger, M. M. (1987). Docking of chromaffin granules – a necessary step in exocytosis? Bioscience Reports 7, 269–279.CrossRefGoogle ScholarPubMed
Schweizer, F. E., Schaefer, T., Tapparelli, C., Grob, M., Karli, O. U., Heumann, R., Thoenen, H., Bookman, R. J. & Burger, M. M. (1989). Inhibition of exocytosis by intracellularly applied antibodies against a chromaffin granule-binding protein. Nature 339, 709–712.CrossRefGoogle ScholarPubMed
Sigworth, F. J. (1983). Electronic design of the patch clamp. In: Single Channel Recording (eds. Sakmann, B. and Neher, E.), pp. 3–35. New York: Plenum Press.CrossRefGoogle Scholar
Sikdar, S. K., Zorec, R., Brown, D. & Mason, W. T. (1989). Dual effects of G-protein activation on Ca-dependent exocytosis in bovine lactotrophs. FEBS Letters 253, 88–92.CrossRefGoogle ScholarPubMed
Spruce, A. E., Breckenridge, L. J., Lee, A. K. & Almers, W. (1990). Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron. 4, 643–654.CrossRefGoogle ScholarPubMed
Spruce, A. E., Iwata, A., White, J. M. & Almers, W. (1989). Patch-clamp studies of single cell-fusion events mediated by a viral fusion protein. Nature 342, 555–558.CrossRefGoogle ScholarPubMed
Tasaka, K., Endo, K. & Yamasaki, H. (1978). Effects of n-decylamine and toluidine blue on the electric capacitance of isolated rat mast cells. Japanese Journal of Pharmacology 28, 21–32.CrossRefGoogle ScholarPubMed
Tatham, P. E. R. & Lindau, M. (1990). ATP-induced pore formation in the plasma membrane of rat peritoneal mast cells. Journal of General Physiology 95, 459–476.CrossRefGoogle ScholarPubMed
Thomas, P., Surprenant, A. & Almers, W. (1990 a). Ca currents, Ca, changes and exocytosis in endorphin/αMSH-secreting rat pituitary cells. Biophysical Journal 57, 245a.Google Scholar
Thomas, P., Surprenant, A. & Almers, W. (1990 b). Cytosotic Ca2+, exocytosis and endocytosis in single melanotrophs of the rat pituitary. Neuron, in press.CrossRefGoogle Scholar
Whitaker, M. & Zimmerberg, J. (1987). Inhibition of secretory granule discharge during exocytosis in sea urchin eggs by polymer solutions. Journal of Physiology 389, 527–540.CrossRefGoogle ScholarPubMed
Zimmerberg, J. & Whitaker, M. J. (1985). Irreversible swelling of secretory granules during exocytosis caused by calcium. Nature 315, 581–584.CrossRefGoogle ScholarPubMed
Zimmerberg, J., Curran, M., Cohen, F. S. & Broadwick, M. (1987). Simultaneous electrical and optical measurements show that membrane fusion precedes secretory granule swelling during exocytosis of beige mouse mast cells. Proceedings of the National Academy of sciences USA 84, 1585–1589.CrossRefGoogle ScholarPubMed
Zorec, R., Mason, W. T. & Sikdar, S. K. (1988). Capacitance measurements on bovine lactotrophs in-vitro. Journal of General Physiology 92, 11a–12a.Google Scholar