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Biophys J. 1998 Nov; 75(5): 2577–2586.
PMCID: PMC1299933

Membrane capacitance changes associated with particle uptake during phagocytosis in macrophages.


We report the use of capacitance measurements to monitor particle uptake after cellular exposure to phagocytic stimuli. In these studies, human monocyte-derived macrophages (HMDMs) and cells from the murine macrophage-like cell line J774.1 were exposed to immune complexes or sized latex particles (0.8 or 3.2 micron in diameter). An average decrease in cell capacitance of 8 pF was seen after exposure of the cells to immune complexes. Cells in which particle uptake was inhibited by cytochalasin B treatment before exposure to immune complexes showed an average increase of 0.5 pF. The decrease in membrane capacitance after exposure of cells to particulate stimuli was absent with the soluble stimulus, platelet-activating factor, further confirming that decreases in membrane capacitance were due to particle uptake. Exposure of cells to sized latex particles resulted in a graded, stepwise decrease in membrane capacitance. The average step size for 0.8-micron particles was 250 fF, and the average step change for the larger 3.2-micron particles was 480 fF, as calculated from Gaussian fits to the step size amplitude histograms. The predicted step size for the individual particles based upon the minimum amount of membrane required to enclose a particle and a specific capacitance of 10 fF/micron2 was 20 and 320 fF, respectively. The step size for the smaller particles deviates significantly from the predicted size distribution, indicating either a possible lower limit to the size of the phagocytic vacuole or multiple particles taken up within a single phagosome. Dynamic interaction between phagocytosis and exocytosis was observed in a number of cells as a biphasic response consisting of an initial rapid increase in capacitance, consistent with cellular exocytosis, followed by stepwise decreases in capacitance.

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  • Artalejo CR, Adams ME, Fox AP. Three types of Ca2+ channel trigger secretion with different efficacies in chromaffin cells. Nature. 1994 Jan 6;367(6458):72–76. [PubMed]
  • Artalejo CR, Elhamdani A, Palfrey HC. Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells. Neuron. 1996 Jan;16(1):195–205. [PubMed]
  • Artalejo CR, Henley JR, McNiven MA, Palfrey HC. Rapid endocytosis coupled to exocytosis in adrenal chromaffin cells involves Ca2+, GTP, and dynamin but not clathrin. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8328–8332. [PMC free article] [PubMed]
  • Bokoch GM. Regulation of the phagocyte respiratory burst by small GTP-binding proteins. Trends Cell Biol. 1995 Mar;5(3):109–113. [PubMed]
  • Breckenridge LJ, Almers W. Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature. 328(6133):814–817. [PubMed]
  • Breckenridge LJ, Almers W. Final steps in exocytosis observed in a cell with giant secretory granules. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1945–1949. [PMC free article] [PubMed]
  • Fernandez JM, Neher E, Gomperts BD. Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature. 312(5993):453–455. [PubMed]
  • Fidler N, Fernandez JM. Phase tracking: an improved phase detection technique for cell membrane capacitance measurements. Biophys J. 1989 Dec;56(6):1153–1162. [PMC free article] [PubMed]
  • Lim NF, Nowycky MC, Bookman RJ. Direct measurement of exocytosis and calcium currents in single vertebrate nerve terminals. Nature. 1990 Mar 29;344(6265):449–451. [PubMed]
  • Griffin FM, Jr, Griffin JA, Leider JE, Silverstein SC. Studies on the mechanism of phagocytosis. I. Requirements for circumferential attachment of particle-bound ligands to specific receptors on the macrophage plasma membrane. J Exp Med. 1975 Nov 1;142(5):1263–1282. [PMC free article] [PubMed]
  • Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. [PubMed]
  • Holevinsky KO, Nelson DJ. Simultaneous detection of free radical release and membrane current during phagocytosis. J Biol Chem. 1995 Apr 7;270(14):8328–8336. [PubMed]
  • Horrigan FT, Bookman RJ. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron. 1994 Nov;13(5):1119–1129. [PubMed]
  • Ince C, Coremans JM, Ypey DL, Leijh PC, Verveen AA, van Furth R. Phagocytosis by human macrophages is accompanied by changes in ionic channel currents. J Cell Biol. 1988 Jun;106(6):1873–1878. [PMC free article] [PubMed]
  • Joshi C, Fernandez JM. Capacitance measurements. An analysis of the phase detector technique used to study exocytosis and endocytosis. Biophys J. 1988 Jun;53(6):885–892. [PMC free article] [PubMed]
  • Kaplan G, Mørland B. Properties of a murine monocytic tumor cell line J-774 in vitro. I. Morphology and endocytosis. Exp Cell Res. 1978 Aug;115(1):53–61. [PubMed]
  • KARRER HE. Electron microscopic study of the phagocytosis process in lung. J Biophys Biochem Cytol. 1960 Apr;7:357–366. [PMC free article] [PubMed]
  • Katnik C, Nelson DJ. Platelet activating factor-induced increase in cytosolic calcium and transmembrane current in human macrophages. J Membr Biol. 1993 Jun;134(3):213–224. [PubMed]
  • Knaus UG, Heyworth PG, Evans T, Curnutte JT, Bokoch GM. Regulation of phagocyte oxygen radical production by the GTP-binding protein Rac 2. Science. 1991 Dec 6;254(5037):1512–1515. [PubMed]
  • Kubo Y, Baldwin TJ, Jan YN, Jan LY. Primary structure and functional expression of a mouse inward rectifier potassium channel. Nature. 1993 Mar 11;362(6416):127–133. [PubMed]
  • Lindau M, Fernandez JM. IgE-mediated degranulation of mast cells does not require opening of ion channels. Nature. 1986 Jan 9;319(6049):150–153. [PubMed]
  • Lindau M, Neher E. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch. 1988 Feb;411(2):137–146. [PubMed]
  • Matthews G, Neher E, Penner R. Second messenger-activated calcium influx in rat peritoneal mast cells. J Physiol. 1989 Nov;418:105–130. [PMC free article] [PubMed]
  • Mørland B, Kaplan G. Properties of a murine monocytic tumor cell line J-774 in vitro. II. Enzyme activities. Exp Cell Res. 1978 Aug;115(1):63–72. [PubMed]
  • Neher E. The influence of intracellular calcium concentration on degranulation of dialysed mast cells from rat peritoneum. J Physiol. 1988 Jan;395:193–214. [PMC free article] [PubMed]
  • Neher E. Ion influx as a transduction signal in mast cells. Int Arch Allergy Appl Immunol. 1991;94(1-4):47–50. [PubMed]
  • Neher E, Marty A. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6712–6716. [PMC free article] [PubMed]
  • Nelson DJ, Jacobs ER, Tang JM, Zeller JM, Bone RC. Immunoglobulin G-induced single ionic channels in human alveolar macrophage membranes. J Clin Invest. 1985 Aug;76(2):500–507. [PMC free article] [PubMed]
  • Nelson DJ, Jow B, Jow F. Whole-cell currents in macrophages: I. Human monocyte-derived macrophages. J Membr Biol. 1990 Jul;117(1):29–44. [PubMed]
  • Nüsse O, Lindau M. The dynamics of exocytosis in human neutrophils. J Cell Biol. 1988 Dec;107(6 Pt 1):2117–2123. [PMC free article] [PubMed]
  • Odin JA, Edberg JC, Painter CJ, Kimberly RP, Unkeless JC. Regulation of phagocytosis and [Ca2+]i flux by distinct regions of an Fc receptor. Science. 1991 Dec 20;254(5039):1785–1788. [PubMed]
  • Parsons TD, Lenzi D, Almers W, Roberts WM. Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells. Neuron. 1994 Oct;13(4):875–883. [PubMed]
  • Ryan TC, Weil GJ, Newburger PE, Haugland R, Simons ER. Measurement of superoxide release in the phagovacuoles of immune complex-stimulated human neutrophils. J Immunol Methods. 1990 Jul 3;130(2):223–233. [PubMed]
  • Schweizer FE, Schäfer T, Tapparelli C, Grob M, Karli UO, Heumann R, Thoenen H, Bookman RJ, Burger MM. Inhibition of exocytosis by intracellularly applied antibodies against a chromaffin granule-binding protein. Nature. 1989 Jun 29;339(6227):709–712. [PubMed]
  • Smith CB, Betz WJ. Simultaneous independent measurement of endocytosis and exocytosis. Nature. 1996 Apr 11;380(6574):531–534. [PubMed]
  • Snyderman R, Pike MC, Fischer DG, Koren HS. Biologic and biochemical activities of continuous macrophage cell lines P388D1 and J774.1. J Immunol. 1977 Dec;119(6):2060–2066. [PubMed]
  • Solsona C, Innocenti B, Fernández JM. Regulation of exocytotic fusion by cell inflation. Biophys J. 1998 Feb;74(2 Pt 1):1061–1073. [PMC free article] [PubMed]
  • Suzuki T. Signal transduction mechanisms through Fc gamma receptors on the mouse macrophage surface. FASEB J. 1991 Feb;5(2):187–193. [PubMed]
  • Swanson JA, Baer SC. Phagocytosis by zippers and triggers. Trends Cell Biol. 1995 Mar;5(3):89–93. [PubMed]
  • Thomas P, Surprenant A, Almers W. Cytosolic Ca2+, exocytosis, and endocytosis in single melanotrophs of the rat pituitary. Neuron. 1990 Nov;5(5):723–733. [PubMed]
  • von Gersdorff H, Matthews G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature. 1994 Feb 24;367(6465):735–739. [PubMed]
  • Voronov I, Santerre JP, Hinek A, Callahan JW, Sandhu J, Boynton EL. Macrophage phagocytosis of polyethylene particulate in vitro. J Biomed Mater Res. 1998 Jan;39(1):40–51. [PubMed]
  • Wright SD, Silverstein SC. Tumor-promoting phorbol esters stimulate C3b and C3b' receptor-mediated phagocytosis in cultured human monocytes. J Exp Med. 1982 Oct 1;156(4):1149–1164. [PMC free article] [PubMed]
  • 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 U S A. 1987 Mar;84(6):1585–1589. [PMC free article] [PubMed]

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