Summary
Some electrophysiological characteristics of macrophages and macrophage polykaryons of foreign body granuloma have been investigated. Cells were obtained from implants of small coverslips in the subcutaneous tissue or in the peritoneal cavity of rats and mice. Transmembrane potentials ranged from −5 to −40 mV. Input resistances ranged from 5 to 120 MΩ, being significantly higher in mice polykaryons. Approximately 10% of the cells exhibited spontaneous slow membrane hyperpolarizations (SH) indistinguishable from those observed in macrophages. SH responses were invariably evoked by iontophoretic injection of calcium ions into the cytoplasm of mice macrophages or macrophage polykaryons. The amplitude of these responses increased with the amount of current carried by calcium ions into the cells. The maximum amplitude of the calcium-induced SH responses is a linear function of the logarithm of [K+] 0 (from 3 to 40mm). The slope of the regression line is 43 mV for a 10-fold increase in [K+] 0 . Substituting sodium chloride by sodium isethionate or by choline chloride does not interfere with the occurrence of SH. The assumption that the SH is solely a consequence of an increase in the membrane conductance to K+ was used to calculate the potassium equilibrium potential (E K). TheE K value is also a linear function of the logarithm of [K+] 0 (from 3 to 40mm). The slope of the regression line is 46 mV for a 10-fold increase in [K+] 0 . These results constitute evidence of the calcium dependence of K+ permeability during SH both in macrophages and macrophage polykaryons. Macrophage polykaryons are a more convenient model than macrophages for the study of the mechanisms underlying the SH responses and their possible physiological implications.
Similar content being viewed by others
References
Anchieta, O., Kouri, J. 1971. Ultra-estrutura de la inflamación aséptica.Rev. CENIC (Cuba) 3:111–126
Atwater, I., Dawson, C.M., Ribalet, B., Rojas, E. 1979. Potassium permeability activated by intracellular calcium ion concentration in the pancreatic β-cell.J. Physiol. 288:575–588
Castranova, V., Bowman, L., Miles, P.R. 1979. Transmembrane potential and ionic content of rat alveolar macrophages.J. Cell. Physiol. 101:471–480
Chambers, T.J. 1977. Studies on the phagocytic capacity of macrophage polykaryons.J. Pathol. 123:65–77
Dos Reis, G.A., Oliveira-Castro, G.M. 1977. Electrophysiology of phagocytic membranes: I. Potassium dependent slow membrane hyperpolarizations in mice macrophages.Biochim. Biophys. Acta 469:257–263
Dos Reis, G.A., Persechini, P.M., Ribeiro, J.M.C., Oliveira-Castro, G.M. 1979. Electrophysiology of phagocytic membranes: II. Membrane potential and induction of slow hyperpolarizations in activated macrophages.Biochim. Biophys. Acta 552:331–340
Gallin, E.K., Gallin, J.I. 1977. Interaction of chemotactic factors with human macrophages. Induction of transmembrane potential changes.J. Cell. Biol. 75:277–289
Gallin, E.K., Wiederhold, M.L., Lipsky, P.E., Rosenthal, A.S. 1976. Spontaneous and induced membrane hyperpolarizations in macrophages.J. Cell. Physiol. 86:653–661
Gallin, J.I., Gallin, E.K., Malech, H.L., Cramer, E.B. 1978. Structural and ionic events during leucocyte chemotaxisIn: “Leukocyte Chemotaxis”. J.I. Gallin and P.G. Quie, editors, pp. 123–141. Raven Press, New York
Henkart, M.P., Nelson, P.G. 1979. Evidence for an intracellular calcium store releasable by surface stimuli in fibroblasts (L cells).J. Gen. Physiol. 73:655–673
Hodgkin, A.L., Huxley, A.F. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve.J. Physiol. 117:500–544
Iwatsuki, N., Petersen, O.H. 1978. Intracellular Ca2+ injection causes membrane hyperpolarization and conductance increase in lacrimal acinar cells.Pfluegers Arch. 377:185–187
Krnjevic, K., Lisiewicz, A. 1972. Injections of calcium ions into spinal motoneurones.J. Physiol. 225:363–390
Lew, V., Ferreira, H.G. 1978. Calcium transport and the properties of a calcium-activated potassium channel in red cell membranes.In: Current Topics in Membranes and Transport. Vol. 10, pp. 217–277. Academic Press, New York
Mariano, M., Nikitin, T., Malucelli, B.E. 1976. Immunological and non-immunological phagocytosis by inflammatory macrophages, epithelioid cells and macrophage polykaryons from foreign body granulomata.J. Pathol. 120:151–159
Mariano, M., Spector, W.G. 1974. The formation and properties of macrophage polykaryons (inflammatory giant cells).J. Pathol. 133:1–19
Meech, R.W. 1976. Intracellular calcium and the control of membrane permeability.In: Calcium in Biological Systems. C.J. Duncan, editor, pp. 161–191. Cambridge University Press, Cambridge
Nelson, P.G., Peacock, J., Minna, J. 1972. An active electrical response in fibroblasts.J. Gen. Physiol. 60:58–71
Okada, Y., Doida, Y., Roy, G., Tsuchiya, W., Inouye, K., Inouye, A. 1977. Oscillations of membrane potential in L cells: I. Basic characteristics.J. Membrane Biol. 35:319–335
Okada, Y., Tsuchiya, W., Inouye, A. 1979. Oscillations of membrane potential in L cells. IV. Role of intracellular Ca2+ in hyperpolarizing excitability.J. Membrane Biol. 47:357–376
Oliveira-Castro, G.M., Dos Reis, G.A. 1980. Electrophysiology of phagocytic membranes: III. Evidences for a calcium dependent potassium permeability change during slow membrane hyperpolarizations of activated macrophages.Biochim. Biophys. Acta 640:500–511
Oliveira-Castro, G.M., Machado, R.D. 1969. Control of glass microelectrodes for intracellular recordings.Experientia 25:556–558
Papadimitriou, J.M. 1979. The role of resident and exudate macrophages in multinucleate giant cell formation.J. Pathol. 128:93–97
Papadimitriou, J.M., Kingston, K.J. 1977. The locomotory behaviour of the multinucleate giant cells of foreign body reactions.J. Pathol. 121:27–36
Papadimitriou, J.M., Rigby, P.J. 1979. The detection of a contractile apparatus in murine multinucleate giant cells.J. Pathol. 129:91–97
Papadimitriou, J.M., Robertson, T.A. 1980. Exocytosis by macrophage polykarya: An ultrastructural study.J. Pathol. 130:75–81
Papadimitriou, J.M., Robertson, T.A., Walters, M.N. 1975. An analysis of the phagocytic potential of multinucleate foreign body giant cells.Am. J. Pathol. 78:343–358
Papadimitriou, J.M., Spector, W.G. 1971. The origin, properties and fate of epithelioid cells.J. Pathol. 105:187–203
Papadimitriou, J.M., Wee, S.H. 1976. Selective release of lysosomal enzymes from cell populations containing multinucleate giant cells.J. Pathol. 120:193–199
Parod, R.J., Putney, J.W., Jr. 1978. The role of calcium in the receptor mediated control of potassium permeability in the rat lacrimal gland.J. Physiol. 281:371–381
Putney, J.W., Jr. 1978. Role of calcium in the fade of the potassium release response in the rat parotid gland.J. Physiol. 281:383–394
Putney, J.W., Jr., Leslie, B.A., Marier, S.H. 1978. Calcium and the control of potassium efflux in the sublingual gland.Am. J. Physiol. 235:C128-C135
Romero, P.J., Whittam, R. 1971. The control by internal calcium of membrane permeability to sodium and potassium.J. Physiol. 214:481–507
Schneider, C., Gennaro, R., Nicola, G. de, Romeo, D. 1978. Secretion of granule enzymes from alveolar macrophages.Exp. Cell. Res. 112:249–256
Trautwein, W., Dudel, J. 1958. Zum Mechanismus der Membranwirkung des Acetylcholin an der Herzmuskelfaser.Pfluegers Arch. 266:324–334
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Persechini, P.M., Araujo, E.G. & Oliveira-Castro, G.M. Electrophysiology of phagocytic membranes: Induction of slow membrane hyperpolarizations in macrophages and macrophage polykaryons by intracellular calcium injection. J. Membrain Biol. 61, 81–90 (1981). https://doi.org/10.1007/BF02007634
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02007634