New Perspectives on Ca2+ Influx in Mast Cells

  • Michael A. McCloskey
Chapter

Abstract

The importance of extracellular calcium for anaphylactic release of histamine was suggested by experiments of Mongar and Schild in 1958, years before the discovery of IgE or its high-affinity receptor, the FcεRI.1 Many subsequent studies using radiotracer flux and fluorescent Ca2+ indicators revealed that multivalent binding of antigen to the IgE-FcεRI complex elicits the release of internal as well as the influx of extracellular Ca2+, and there appears to be a causal relation between these two events. For the RBL-2H3 mast cell line used in many of these studies,2 it is generally agreed that Ca2+ influx is crucial for antigen-induced secretion of preformed inflammatory mediators.3

Keywords

Histamine Cyclosporin Cytosol Acetylcholine Strontium 

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References

  1. 1.
    Mongar JL, Schild HO. The effect of calcium and pH on the anaphylactic reaction. J Physiol (Camb) 1958;140:272–284.Google Scholar
  2. 2.
    Barsumian EL, Isersky C, Petrino MB, et al. IgE-induced histamine release from rat basophilic leukemia cell lines: isolation of releasing and nonreleasing clones. Eur J Immunol 1981;11:317–323.PubMedGoogle Scholar
  3. 3.
    Hide M, Beaven MA. Calcium influx in a rat mast cell (RBL-2H3) line. Use of multivalent metal ions to define its characteristics and role in exocytosis. J Biol Chem 1991 266:15221–15229.PubMedGoogle Scholar
  4. 4.
    Zhang L, McCloskey MA. Immunoglobulin E receptor-activated calcium conductance in rat mast cells. J Physiol (Camb) 1995;483:59–66.Google Scholar
  5. 5.
    Parekh AB, Penner R. Depletion-activated calcium current is inhibited by protein kinase in RBL-2H3 cells. Proc Natl Acad Sci USA 1995;92:7907–7911.PubMedGoogle Scholar
  6. 6.
    Douglas WW, Rubin RP. The role of calcium in the secretory response of the adrenal medulla to acetylcholine. J Physiol (Camb) 1961;159:40–57.Google Scholar
  7. 7.
    Douglas WW. Stimulus-secretion coupling: the concept and clues from chromaffin and other cells. Br J Pharmacol 1968;34:451–474.PubMedGoogle Scholar
  8. 8.
    Putney JW. Capacitative calcium entry revisited. Cell Calcium 1990;11:611–624.PubMedGoogle Scholar
  9. 9.
    Hutchinson LE, McCloskey MA. FcεRI-mediated induction of nuclear factor of activated T cells. J Biol Chem 1995;270:16333–16338.PubMedGoogle Scholar
  10. 10.
    Ozawa K, Szallasi Z, Kazanietz MG, et al. Ca2+- dependent and Ca2+-independent isozymes of protein kinase C mediate exocytosis in antigen-stimulated rat basophilic RBL-2H3 cells. J Biol Chem 1993;268:1749–1756.PubMedGoogle Scholar
  11. 11.
    Foreman JC, Mongar JL, Gomperts BD. Calcium ionophores and movement of calcium ions following the physiological stimulus to a secretory process. Nature (Lond) 1973;245:249–251.Google Scholar
  12. 12.
    Cochrane DE, Douglas WW. Calcium-induced extrusion of secretory granules (exocytosis) in mast cells exposed to 48/80 or the ionophores A-23187 and X-537A. Proc Natl Acad Sci USA 1974;71:408–412.PubMedGoogle Scholar
  13. 13.
    Siraganian RP, Kulczycki A Jr, Mendoza G, et al. Ionophore A-23187 induced histamine release from rat mast cells and rat basophil leukemia (RBL-1) cells. J Immunol 1975;115:1599–1602.PubMedGoogle Scholar
  14. 14.
    Kanno T, Cochrane DE, Douglas WW. Exocytosis (secretory granule extrusion) induced by injection of calcium into mast cells. Can J Physiol Pharmacol 1973;51:1001–1004.PubMedGoogle Scholar
  15. 15.
    Theoharides TC, Douglas WW. Secretion in mast cells induced by calcium entrapped within phospholipid vesicles. Science 1978;201:1143–1145.PubMedGoogle Scholar
  16. 16.
    Douglas WW, Kagayama M. Calcium and stimulus-secretion coupling in the mast cell: stimulant and inhibitory effects of calcium-rich media on exocytosis. J Physiol (Camb) 1977;270:691–703.Google Scholar
  17. 17.
    WoldeMussie E, Moran NC. Histamine release by compound 48/80: evidence for the depletion and repletion of calcium using Chlortetracycline and 45calcium. Agents Actions 1984;15:268–272.Google Scholar
  18. 18.
    Foreman JC, Mongar JL. The role of the alkaline earth ions in anaphylactic histamine secretion. J Physiol (Camb) 1972;224:753–869.Google Scholar
  19. 19.
    Foreman JC, Hallett MB, Mongar JL. The relationship between histamine secretion and 45calcium uptake by mast cells. J Physiol (Camb) 1977;271:193–214.Google Scholar
  20. 20.
    Foreman JC, Hallett MB, Mongar JL. Movement of strontium ions into mast cells and its relationship to the secretory response. J Physiol (Camb) 1977;271:233–251.Google Scholar
  21. 21.
    Taurog JD, Mendoza GR, Hook WA, et al. Noncytotoxic IgE-mediated release of histamine and serotonin from murine mastocytoma cells. J Immunol 1977;119:1757–1761.PubMedGoogle Scholar
  22. 22.
    Crews FT, Morita Y, McGivney A, et al. IgE-mediated histamine release in rat basophilic leukemia cells: receptor activation, phospholipid methylation, Ca2+ flux, and release of arachidonic acid. Arch Biochem Biophys 1981;212:561–571.PubMedGoogle Scholar
  23. 23.
    Kanner BI, Metzger H. Initial characterization of the calcium channel activated by the crosslinking of the receptors for immunoglobulin E. J Biol Chem 1984;259:10188–10193.Google Scholar
  24. 24.
    Tsien RY. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 1980;19:2396–2404.PubMedGoogle Scholar
  25. 25.
    White JR, Ishizaka T, Ishizaka K, et al. Direct demonstration of increased intracellular concentration of free calcium as measured by quin-2 in stimulated rat peritoneal mast cell. Proc Natl Acad Sci USA 1984;81:3978–3982.PubMedGoogle Scholar
  26. 26.
    Neher E, Almers W. Fast calcium transients in rat peritoneal mast cells are not sufficient to trigger exocytosis. EMBO J 1986;5:51–53.PubMedGoogle Scholar
  27. 27.
    Beaven MA, Rogers J, Moore JP, et al. The mechanism of the calcium signal and correlation with histamine release in 2H3 cells. J Biol Chem 1984;259:7129–7136.PubMedGoogle Scholar
  28. 28.
    Pearce FL, Ennis AT, White JR. Role of intra- and extracellular calcium in histamine release from rat peritoneal mast cells. Agents Actions 1981;11:51–54.PubMedGoogle Scholar
  29. 29.
    Mohr FC, Fewtrell C. The relative contributions of extracellular and intracellular calcium to secretion from tumor mast cells. Multiple effects of the proton ionophore carbonyl cyanide m-chlorophenylhydrazone. J Biol Chem 1987;262:10638–10643.PubMedGoogle Scholar
  30. 30.
    Mohr FC, Fewtrell C. Depolarization of rat basophilic leukemia cells inhibits calcium uptake and exocytosis. J Cell Biol 1987;104:783–792.PubMedGoogle Scholar
  31. 31.
    Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985;260:3440–3450.PubMedGoogle Scholar
  32. 32.
    Millard PJ, Ryan TA, Webb WW, et al. Immunoglobulin E receptor cross-linking induces oscillations in intracellular free ionized calcium in individual tumor mast cells. J Biol Chem 1989;264:19730–19739.PubMedGoogle Scholar
  33. 33.
    Pearce FL, White JR. Effect of lanthanide ions on histamine secretion from rat peritoneal mast cells. Br J Pharmacol 1981;72:341–347.PubMedGoogle Scholar
  34. 34.
    Lindau M, Fernandez JM. IgE-mediated degranulation of mast cells does not require opening of ion channels. Nature (Lond) 1986;319:150–153.Google Scholar
  35. 35.
    Lindau M, Fernandez JM. A patch-clamp study of histamine-secreting cells. J Gen Physiol 1986;88:349–368.PubMedGoogle Scholar
  36. 36.
    Neher E. The influence of intracellular calcium concentration on degranulation of dialysed mast cells from rat peritoneum. J Physiol (Camb) 1988;395:193–214.Google Scholar
  37. 37.
    Hoth M, Penner R. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature (Lond) 1992;355:353–356.Google Scholar
  38. 38.
    Lewis RS, Cahalan MD. Mitogen-induced oscillations of cytosolic Ca2+ and transmembrane Ca2+ current in human leukemic T cells. Cell Regul 1989;1:99–112.PubMedGoogle Scholar
  39. 39.
    Zweifach A, Lewis RS. Mitogen-regulated Ca2+ current of T lymphocytes is activated by depletion of intracellular Ca2+ stores. Proc Natl Acad Sci USA 1993;90:6295–6299.PubMedGoogle Scholar
  40. 40.
    Fasolato C, Hoth M, Penner R. A GTP-dependent step in the activation mechanism of capacitative calcium influx. J Biol Chem 1993;268:20737–20740.PubMedGoogle Scholar
  41. 41.
    Berridge MJ. Capacitative calcium entry. Biochem J 1995;312:1–11.PubMedGoogle Scholar
  42. 42.
    Fanger CM, Hoth M, Crabtree GR, et al. Characterization of T cell mutants with defects in capacitative calcium entry: genetic evidence for the physiological roles of CRAC channels. J Cell Biol 1995;131:655–667.PubMedGoogle Scholar
  43. 43.
    Fasolato C, Innocenti B, Pozzan T. Receptor-activated Ca2+ influx: how many mechanisms for how many channels? Trends Pharmacol Sci 1994;15:77–83.PubMedGoogle Scholar
  44. 44.
    Thastrup O, Cullen PJ, Drobak BK, et al. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2+-ATPase. Proc Natl Acad Sci USA 1990;87:2466–2470.PubMedGoogle Scholar
  45. 45.
    Ali H, Maeyama K, Sagi-Eisenberg R, et al. Antigen and thapsigargin promote influx of Ca2+ in rat basophilic RBL-2H3 cells by ostensibly similar mechanisms that allow filling of inositol 1,4,5-trisphosphate-sensitive and mitochondrial Ca2+ stores. Biochem J 1994;304:431–440.PubMedGoogle Scholar
  46. 46.
    Hoth M, Penner R. Calcium release-activated calcium current in rat mast cells. J Physiol (Camb) 1993;465:359–386.Google Scholar
  47. 47.
    Fasolato C, Hoth M, Matthews G, et al. Ca2+ and Mn2+ influx through receptor-mediated activation of nonspecific cation channels in mast cells. Proc Natl Acad Sci USA 1993;90:3068–3072.PubMedGoogle Scholar
  48. 48.
    Wolde Mussie E, Maeyama K, Beaven MA. Loss of secretory response of rat basophilic leukemia (2H3) cells at 40°C is associated with reversible suppression of inositol phospholipid breakdown and calcium signals. J Immunol 1986;137:1674–1680.Google Scholar
  49. 49.
    Pusch M, Neher E. Rates of diffusional exchange between small cells and a measuring patch pipette. Pflügers Arch 1988;411:204–211.PubMedGoogle Scholar
  50. 50.
    Penner R, Pusch M, Neher E. Washout phenomena in dialyzed mast cells allow discrimination of different steps in stimulus-secretion coupling. Biosci Rep 1987;7:313–321.PubMedGoogle Scholar
  51. 51.
    Horn R, Marty A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 1988;92:145–159.PubMedGoogle Scholar
  52. 52.
    Fewtrell C, Kessler A, Metzger H, Weissmann G, eds. Advances in Inflammation Research. New York: Raven Press, 1979.Google Scholar
  53. 53.
    Stump RF, Oliver JM, Cragoe EJ Jr, et al. The control of mediator release from RBL-2H3 cells: roles for Ca2+, Na+, and protein kinase C. J Immunol 1987;139:881–886.PubMedGoogle Scholar
  54. 54.
    Qian Y-X, McCloskey MA. Activation of mast cell K+ channels through multiple G proteinlinked receptors. Proc Natl Acad Sci USA 1993;90:7844–7848.PubMedGoogle Scholar
  55. 55.
    Mazurek N, Schindler H, Schurholz T, et al. The cromolyn binding protein constitutes the Ca2+ channel of basophils opening upon immunological stimulus. Proc Natl Acad Sci USA 1984;81:6841–6845.PubMedGoogle Scholar
  56. 56.
    Fewtrell C, Sherman E. IgE receptor-activated calcium permeability pathway in rat basophilic leukemia cells: measurement of the unidirectional influx of calcium using Quin2-buffered cells. Biochemistry 1987;26:6995–7003.PubMedGoogle Scholar
  57. 57.
    Kanner BI, Metzger H. Crosslinking of the receptors for immunoglobulin E depolarizes the plasma membrane of rat basophilic leukemia cells. Proc Natl Acad Sci USA 1983;80:5744–5748.PubMedGoogle Scholar
  58. 58.
    Sagi-Eisenberg R, Pecht I. Membrane potential changes during IgE-mediated histamine release from rat basophilic leukemia cells. J Membr Biol 1983;75:97–104.PubMedGoogle Scholar
  59. 59.
    Zweifach A, Lewis RS. Calcium-dependent potentiation of store-operated calcium channels in T lymphocytes. J Gen Physiol 1996;107:597–610.PubMedGoogle Scholar
  60. 60.
    Hoth M. Calcium and barium permeation through calcium release-activated calcium (CRAC) channels. Pflügers Arch 1995;430:315–322.PubMedGoogle Scholar
  61. 61.
    Penner R, Neher E. Secretory responses of rat peritoneal mast cells to high intracellular calcium. FEBS Lett 1988;226:307–313.PubMedGoogle Scholar
  62. 62.
    Mohr FC, Fewtrell C. IgE receptor-mediated depolarization of rat basophilic leukemia cells measured with the fluorescent probe bisoxonol. J Immunol 1987;138:1564–1570.PubMedGoogle Scholar
  63. 63.
    McCloskey MA, Cahalan MD. G protein control of potassium channel activity in a mast cell line. J Gen Physiol 1990;95:205–227.PubMedGoogle Scholar
  64. 64.
    Hultsch T, Albers MW, Schreiber SL, et al. Immunophilin ligands demonstrate common features of signal transduction leading to exocytosis or transcription. Proc Natl Acad Sci USA 1991;88:6229–6233.PubMedGoogle Scholar
  65. 65.
    Randriamampita C, Tsien RY. Emptying of intracellular Ca2+ stores releases a novel small messenger that stimulates Ca2+ influx. Nature (Lond) 1993;364:809–814.Google Scholar
  66. 66.
    Choi OH, Kim J-H, Kinet J-P. Calcium mobilization via sphingosine kinase in signalling by the FcεRI antigen receptor. Nature (Lond) 1996;380:634–636.Google Scholar
  67. 67.
    Zweifach A, Lewis RS. Slow calcium-dependent inactivation of depletion-activated calcium current. J Biol Chem 1995;270:14445–14451.PubMedGoogle Scholar
  68. 68.
    Mongar JL, Schild HO. Effect of temperature on the anaphylactic reaction. J Physiol (Camb) 1958;135:320–338.Google Scholar
  69. 69.
    McCloskey MA, Qian Y-X. Selective expression of K+ channels during mast cell differentiation. J Biol Chem 1994;269:14813–14819.PubMedGoogle Scholar
  70. 70.
    Fan Y, McCloskey MA. Dual pathways for GTP-dependent regulation of chemoattractant-activated K+ conductance in murine J774 monocytes. J Biol Chem 1994;269:31533–31543.PubMedGoogle Scholar
  71. 71.
    Innocenti B, Pozzan T, Fasolato C. Intracellular ADP modulates the Ca2+ release-activated Ca2+ current in a temperature- and Ca2+-dependent way. J Biol Chem 1996;271:8582–8587.PubMedGoogle Scholar
  72. 72.
    Birnbaumer L, Zhu X, Jiang M, et al. On the molecular basis and regulation of cellular capacitative calcium entry: roles for Trp proteins. Proc Natl Acad Sci USA 1996;93:15195–15202.PubMedGoogle Scholar
  73. 73.
    Hardie RC. Calcium signaling: setting store by calcium channels. Curr Biol 1996;6:1371–1373.PubMedGoogle Scholar
  74. 74.
    Kindman LA, Kim S, McDonald TV, et al. Characterization of a novel intracellular sphingolipid-gated Ca2+-permeable channel from rat basophilic leukemia cells. J Biol Chem 1994;269:13088–13091.PubMedGoogle Scholar
  75. 75.
    Beaven MA. Calcium signaling: sphingosine kinase versus phospholipase C? Curr Biol 1996;6:798–801.PubMedGoogle Scholar
  76. 76.
    Simon SM, Llinas RR. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys J 1985;48:485–498.PubMedGoogle Scholar
  77. 77.
    Llinas R, Sugimori M, Silver RB. Microdomains of high calcium concentration in a presynaptic terminal. Science 1992;256:677–679.PubMedGoogle Scholar
  78. 78.
    Kim K-T, Westhead EW. Cellular responses to Ca2+ from extracellular and intracellular sources are different as shown by simultaneous measurements of cytosolic Ca2+ and secretion from bovine chromaffin cells. Proc Natl Acad Sei USA 1989;86:9881–9885.Google Scholar
  79. 79.
    Robinson IM, Finnegan JM, Monck JR, et al. Colocalization of calcium entry and exocytotic release sites in adrenal chromaffin cells. Proc Natl Acad Sci USA 1995;92:2474–2478.PubMedGoogle Scholar
  80. 80.
    Zweifach A, Lewis RS. Rapid inactivation of depletion-activated caclium current (ICRAC) due to local calcium feedback. J Gen Physiol 1995;105:209–226.PubMedGoogle Scholar
  81. 81.
    Haydon PG, Marchese-Ragona S, Basarsky TA, et al. Near-field confocal optical spectroscopy (NCOS): subdiffraction optical resolution for biological systems. J Microsc (Oxf) 1996;182:208–216.Google Scholar
  82. 82.
    Baumgartner RA, Yamada K, Deramo VA, et al. Secretion of TNF from a rat mast cell line is a brefeldin A-sensitive and a calcium/protein kinase C-regulated process. J Immunol 1994;153:2609–2617.PubMedGoogle Scholar
  83. 83.
    Goldfeld AE, Tsai E, Kincaid R, et al. Calcineurin mediates tumor necrosis factor-oc gene induction in stimulated T and B cells. J Exp Med 1994;180:763–768.PubMedGoogle Scholar
  84. 84.
    Leal-Berumen I, Conlon P, Marshall JS. IL-6 production by rat peritoneal mast cells is not necessarily preceded by histamine release and can be induced by bacterial lipopolysaccharide. J Immunol 1994;152:5468–5476.PubMedGoogle Scholar
  85. 85.
    Crabtree GR, Clipstone NA. Signal transmission between the plasma membrane and nucleus of T lymphocytes. Annu Rev Biochem 1994;63:1045–1083.PubMedGoogle Scholar
  86. 86.
    Rao A. NF-ATp: a transcription factor required for the co-ordinate induction of several cytokine genes. Immunol Today 1994;15:274–281.PubMedGoogle Scholar
  87. 87.
    Jain J, McCaffrey PG, Valge-Archer VE, et al. Nuclear factor of activated T cells contains Fos and Jun. Nature (Lond) 1992;356:801–804.Google Scholar
  88. 88.
    Northrop JP, Ho SN, Chen L, et al. NF-AT components define a family of transcription factors targeted in T-cell activation. Nature (Lond) 1994;369:497–502.Google Scholar
  89. 89.
    McCaffrey PG, Luo C, Kerppola TK, et al. Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 1993;262:750–754.PubMedGoogle Scholar
  90. 90.
    Li X, Ho SN, Luna J, et al. Cloning and chromosomal localization of the human and murine genes for the T-cell transcription factors NFATc and NFATp. Cytogenet Cell Genet 1995;68:185–191.PubMedGoogle Scholar
  91. 91.
    Goldsmith MA, Weiss A. Early signal transduction by ther antigen receptor without committment to T cell activation. Science 1988;240:1029–1031.PubMedGoogle Scholar
  92. 92.
    Timmerman LA, Clipstone NA, Ho SN, et al. Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature (Lond) 1996;383:837–840.Google Scholar
  93. 93.
    Clipstone NA, Crabtree GR. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature (Lond) 1992;357:695–697.Google Scholar
  94. 94.
    Loh C, Shaw KT-Y, Carew J, et al. Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activity. J Biol Chem 1996;271:10884–10891.PubMedGoogle Scholar
  95. 95.
    Cockerill PN, Shannon MF, Bert AG, et al. The granulocyte-macrophage colony-simulating factor/interleukin 3 locus is regulated by an inducible cyclosporin A-sensitive enhancer. Proc Natl Acad Sci USA 1993;90:2466–2470.PubMedGoogle Scholar
  96. 96.
    Jain J, Miner Z, Rao A. Analysis of the preexisting and nuclear forms of nuclear factor of activated T cells. J Immunol 1993;151:837–848.PubMedGoogle Scholar
  97. 97.
    Baranes D, Razin E. Protein kinase C regulates proliferation of mast cells and the expression of the mRNAs of fos and jun protooncogenes during activation by IgE-Ag or calcium ionophore A23187. Blood 1991;78:2354–2364.PubMedGoogle Scholar
  98. 98.
    Wolfe PC, Chang E-Y, Rivera J, et al. Differential effects of the protein kinase C activator phorbol-12-myristate 13-acetate on calcium responses and secretion in adherent and suspended RBL-2H3 mucosal mast cells. J Biol Chem 1996;271:6658–6665.PubMedGoogle Scholar
  99. 99.
    Ghosh P, Sica A, Cippitelli M, et al. Activation of nuclear factor of activated T cells in a cyclosporin A-resistant pathway. J Biol Chem 1996;271:7700–7704.PubMedGoogle Scholar
  100. 100.
    Woodrow MA, Rayter S, Downward J, et al. p21ras function is important for T cell antigen receptor and protein kinase C regulation of nuclear factor of activated T cells. J Immunol 1993;150:3853–3861.PubMedGoogle Scholar
  101. 101.
    Woodrow M, Clipstone NA, Cantrell D. p21ras and calcineurin synergize to regulate the nuclear factor of activated T cells. J Exp Med 1993;178:1517–1522.PubMedGoogle Scholar
  102. 102.
    Wodnar-Filipowicz A, Moroni C. Regulation of interleukin 3 mRNA expression in mast cells occurs at the posttranscriptional level and is mediated by calcium ions. Proc Natl Acad Sci USA 1990;87:777–781.PubMedGoogle Scholar
  103. 103.
    Nair APK, Hahn S, Banholzer R, et al. Cyclosporin A inhibits growth of autocrine tumor cell lines by destabilizing interleukin-3 mRNA. Nature (Lond) 1994;369:239–242.Google Scholar
  104. 104.
    Prieschl EE, Gouilleux-Gruart V, Walker C, et al. A nuclear factor of activated T cell-like transcription factor in mast cells is involved in IL-5 gene regulation after IgE plus antigen stimulation. J Immunol 1995;154:6112–6119.PubMedGoogle Scholar
  105. 105.
    Razin E, Szallasi Z, Kazanietz MG, et al. Protein kinases C-β and C-ε link the mast cell high-affinity receptor for IgE to the expression of c-fos and c-jun. Proc Natl Acad Sci USA 1994;91:7722–7726.PubMedGoogle Scholar
  106. 106.
    Xanthoudakis S, Viola JPB, Shaw KTY, et al. An enhanced immune response in mice lacking the transcription factor NFAT1. Science 1996;272:892–895.PubMedGoogle Scholar
  107. 107.
    Lepple-Wienhues A, Cahalan MD. Conductance and permeation of monvalent cations through depletion-activated Ca2+ channels (ICRAC) in Jurkat T cells. Biophys J 1996;71:787–794.PubMedGoogle Scholar
  108. 108.
    Premack BA, McDonald TV, Gardner P. Activation of Ca2+ current in Jurkat T cells following the depletion of Ca2+ stores by microsomal Ca2+-ATPase inhibitors. J Immunol 1994;152:5226–5240.PubMedGoogle Scholar

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  • Michael A. McCloskey

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