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Activation of a potassium outward current by zymosan and opsonized zymosan in mouse peritoneal macrophages

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Abstract

The effects of zymosan and human serum opsonized zymosan on membrane currents of adherent mouse peritoneal macrophages which had been cultured for 5 to 20 days were investigated with the whole-cell voltage-clamp technique. Both stimuli activated an outward current. The outward current activation was transient and lasted about 5 min. In solutions with 10 or 50 mmol/l extracellular potassium concentration the activation of an outwardly directed current occurred at test potentials positive to the respective potassium equilibrium potential. This particle-induced current resembled a calciu-mactivated potassium current which could be activated with the calcium ionophore A 23187 and with platelet activating factor. The order of maximal responses (test potential +55 mV, amplitude given as percentage of the respective control) was: 0.1 μmol/l platelet activating factor (222±36%,n=8,P<0.01) > 1 μmol/l A 23187 (190±24%,n=11,P<0.01) >900 μg/ml opsonized zymosan (134±7%,n=22,P<0.01) >900 μg/ml zymosan (116±5%,n = 21,P<0.01) The lower efficiency of zymosan as compared to opsonized zymosan is explained in part by a lower percentage of responding cells which was 48% for zymosan and 73% for opsonized zymosan. Macrophages which were pretreated with particles showed a greater reactivity to calcium as compared to untreated cells. Elevation of extracellular calcium from 0.9 to 4.5 mmol/l activated the outward current to 145±12% (n = 11,P< 0.01) after preincubation with opsonized zymosan and to 144±21% (n = 12,P< 0.01) under the influence of zymosan while in untreated cells current increase by elevation of extracellular calcium was not significant (120±10%,n = 9, n.s.).

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References

  • Aderem AA, Scott WA, Cohn ZA (1984) A selective defect in arachidonic acid release from macrophage membranes in high potassium media. J Cell Biol 99:1235–1241

    Article  PubMed  CAS  Google Scholar 

  • Berger F, Borchard U, Hafner D, Weis T (1993) Activation of membrane outward currents by human low density lipoprotein in mouse peritoneal macrophages. Naunyn Schmiedebergs Arch Pharmacol 348: 207–212

    Article  PubMed  CAS  Google Scholar 

  • Conrad GW Rink TJ (1986) Platelet activating factor raises intracellular calcium ion concentration in macrophages. J Cell Biol 103: 439–450

    Article  PubMed  CAS  Google Scholar 

  • Di Virgilio F, Meyer BC, Greenberg S, Silverstein SC (1988) Fe receptor-mediated phagocytosis occurs in macrophages at exceedingly low cytosolic Ca2+ levels. J Cell Biol 106:657–666

    Article  PubMed  Google Scholar 

  • Gallin EK (1981) Voltage clamp studies in macrophages from mouse spleen cultures. Science 214:458–460, 1981

    Article  PubMed  CAS  Google Scholar 

  • Gallin EK (1984) Calcium- and voltage-activated potassium channels in human macrophages. Biophys J 46:821–825

    Article  PubMed  CAS  Google Scholar 

  • Gallin EK (1989) Evidence for a Ca-activated inwardly rectifying K channel in human macrophages. Am J Physiol 257 (Cell Physiol 26):C77-C85

    PubMed  CAS  Google Scholar 

  • Gallin EK (1991) Ion channels in leukocytes. Physiol Rev 71:775–811

    PubMed  CAS  Google Scholar 

  • Gallin EK, Gallin JI (1977) Interaction of chemotactic factors with human macrophages. Induction of transmembrane potential changes. J Cell Biol 75:277–289

    Article  PubMed  CAS  Google Scholar 

  • Gallin EK, McKinney LC (1988) Patch-clamp studies in human macrophages: single-channel and whole-cell characterization of two K+ conductances. J Membr Biol 103:55–66

    Article  PubMed  CAS  Google Scholar 

  • Gallin EK, Sheehy PA (1985) Differential expression of inward and outward potassium currents in the macrophage-like cell line J774.1. J Physiol (Lond) 369:475–499

    CAS  Google Scholar 

  • Gallin EK, Wiederhold ML, Lipsky PE, Rosenthal AS (1975) Spontaneous and induced membrane hyperpolarizations in macrophages. J Cell Physiol 86:653–662

    Article  PubMed  Google Scholar 

  • Greenberg S, El Khoury J, DiVirgilio F, Kaplan EM, Silverstein SC (1991) Ca2+-independent F-acting assembly and disassembly during Fe receptor-mediated phagocytosis in mouse macrophages. J Cell Biol 113:757–767

    Article  PubMed  CAS  Google Scholar 

  • Hamill OP, Marty A, Netter E, Salmann B, Sigworth F (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85–100

    Article  PubMed  CAS  Google Scholar 

  • Hishikawa T, Cheung JY, Yelamarty RV, Knutson DW (1991) Calcium transients during Fc receptor-mediated and nonspecific phagocytosis by murine peritoneal macrophages. J Cell Biol 115:59–66

    Article  PubMed  CAS  Google Scholar 

  • Ichinose M, Hara N, Sawada M, Maeno T (1992) Activation of K+ current in macrophages by platelet activating factor. Biochem Biophys Res Commun 182:372–378

    Article  PubMed  CAS  Google Scholar 

  • Ince C, Coremans JMCC, Ypey DL, Leijh PCJ, Verveen AA, van Furth R (1988) Phagocytosis by human macrophages is accompanied by changes in ionic channel currents. J Cell Biol 106:1873–1878

    Article  PubMed  CAS  Google Scholar 

  • Kolb HA, Ubl J (1987) Activation of anion channels by zymosan particles in membranes of peritoneal macrophages. Biochim Biophys Acta 899:239–246

    Article  PubMed  CAS  Google Scholar 

  • Kouri J, Noa M, Diaz B, Niubo E (1980) Hyperpolarisation of rat peritoneal macrophages phagocytosing latex particles. Nature 283: 868–869

    Article  PubMed  CAS  Google Scholar 

  • Kruskal BA, Maxfield FR (1987) Cytosolic free calcium increases before and oscillate during frustrated phagocytosis in macrophages. J Cell Biol 105:2685–2693

    Article  PubMed  CAS  Google Scholar 

  • Letari O, Malgaroli A, Morgan DW Welton AF, Nicosia S (1991) Cytosolic calcium ion and arachidonic acid release and metabolism in macrophages. Eur J Pharmacol 206:211–219

    Article  PubMed  CAS  Google Scholar 

  • Lipton SA (1986) Antibody activates cationic channels via second messenger Ca2+. Biochim Biophys Acta 856:59–67

    Article  PubMed  CAS  Google Scholar 

  • McCann FV, Keller TM, Guyre PM (1987) Ion channels in human macrophages compared with the U-937 cell line. J Membr Biol 96:57–64

    Article  PubMed  CAS  Google Scholar 

  • McKinney LC, Gallin EK (1988) Inwardly rectifying whole-cell and single-channel K currents in the murine macrophage cell line J774.1. J Membr Biol 103:41–53

    Article  PubMed  CAS  Google Scholar 

  • McNeil PL, Swanson JA, Wright SD, Silverstein SC, Taylor DL (1986) Fc-receptor-mediated phagocytosis occurs in macrophages without an increase in average [Ca++]i. J Cell Biol 102:1586–1592

    Article  PubMed  CAS  Google Scholar 

  • Michl J, Ohlbaum DJ, Silverstein SC (1976) 2-deoxyglucose selectively inhibits Fc and complement receptor-mediated phagocytosis in mouse peritoneal macrophages. I. Description of the inhibitory effect. J Exp Med 144:1465–1483

    Article  PubMed  CAS  Google Scholar 

  • Miles PR, Bowman L, Castranova V (1981) Transmembrane potential changes during phagocytosis in rat alveolar macrophages. J Cell Physiol 106:109–117

    Article  PubMed  CAS  Google Scholar 

  • Nelson DJ, Jacobs ER, Tang JM, Zeller JM, Bone RC (1985) Immunoglobulin G-induced single ionic channels in human alveolar macrophage membranes. J Clin Invest 76:500–507

    Article  PubMed  CAS  Google Scholar 

  • Nelson DJ, Jow B, Jow F (1990a) Whole-cell currents in macrophages: I. human monocyte-derived macrophages. J Membr Biol 117:29–44

    Article  CAS  Google Scholar 

  • Nelson DJ, Jow B, Popovich KJ (1990b) Whole-cell currents in macrophages: II. alveolar macrophages. J Membr Biol 117:45–55

    Article  CAS  Google Scholar 

  • Randriamampita C, Trautmann A (1987) Ionic channels in murine macrophages. J Cell Biol 105:761–769

    Article  PubMed  CAS  Google Scholar 

  • Silverstein SC, Steinman RM, Cohn ZA (1977) Endocytosis. Ann Rev Biochem 46:669–722

    Article  PubMed  CAS  Google Scholar 

  • Somogyi R, Uhl J, Kolb HA (1987) Zymosan and potassium induced activation of single voltage-dependent ion channels in membranes of peritoneal macrophages. Adv Biosci 66:275–284

    Google Scholar 

  • Suzuki T (1991) Signal transduction mechanisms through Fc receptors on the mouse macrophage surface. FASEB J 5:187–193

    PubMed  CAS  Google Scholar 

  • Young JDE, Unkeless JC, Kaback HR, Cohn ZA (1983a) Macrophage membrane potential changes associated with 2b/1 Fc receptor-ligand binding. Proc Natl Acad Sci 80:1357–1361

    Article  CAS  Google Scholar 

  • Young JDE, Unkeless JC, Kaback HR, Cohn ZA (1983b) Mouse macrophage Fe receptor for IgG 2b/1 in artificial and plasma membrane vesicles functions as a ligand-dependent ionophore. Proc Natl Acad Sci 80:1636–1640

    Article  CAS  Google Scholar 

  • Young JDE, Unkeless JC, Young TM, Mauro A, Cohn ZA (1983c) Role for mouse macrophage IgG Fc receptor as ligand-dependent ion channel. Nature 306:186–189

    Article  CAS  Google Scholar 

  • Young JDE, Ko SS, Cohn ZA (1984) The increase in intracellular free calcium associated with IgG 2b/1 Fc receptor-ligand interactions: role in phagocytosis. Proc Natl Acad Sci 81:5430–5434

    Article  PubMed  CAS  Google Scholar 

  • Ypey DL, Clapham DE (1984) Development of a delayed outward-rectifying K+ conductance in cultured mouse peritoneal macrophages. Proc Natl Acad Sci 81:3083–3087

    Article  PubMed  CAS  Google Scholar 

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Correspondence to: U. Borchard at the above address

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Berger, F., Borchard, U., Hafner, D. et al. Activation of a potassium outward current by zymosan and opsonized zymosan in mouse peritoneal macrophages. Naunyn-Schmiedeberg's Arch. Pharmacol. 349, 594–601 (1994). https://doi.org/10.1007/BF01258465

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  • DOI: https://doi.org/10.1007/BF01258465

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