Control of the Ca2+ Release Induced by myo-Inositol Trisphosphate and the Implication in Signal Transduction

  • Ludwig Missiaen
  • Jan B. Parys
  • Humbert De Smedt
  • Ilse Sienaert
  • Martin D. Bootman
  • Rik Casteels
Part of the Subcellular Biochemistry book series (SCBI, volume 26)


Inositol-1,4,5-trisphosphate (InsP3) is a diffusible messenger formed within the cell in response to external stimuli. It mobilizes Ca2+ from those nonmitochondrial Ca2+ pools that express the InsP3 receptor (InsP3R), a specific Ca2+-release channel (Berridge and Irvine, 1989; Berridge, 1993). The nonmitochondrial pools were originally classified as InsP3-sensitive and InsP3insensitive. Recent evidence suggests that the InsP3-sensitive Ca2+ pool is much larger than hitherto expected (Bird et al., 1992) and that InsP3-insensitive Ca2+ pools can artifactually be formed during the permeabilization procedure (Hajnóczky et al., 1994). Under conditions of very mild permeabilization, 95% of the nonmitochondrial Ca2+ pools can be InsP3-sensitive, e.g., in A7r5 smooth muscle cells (Missiaen et al., 1992b).


Calcium Release Ryanodine Receptor Inositol Phosphate Pancreatic Acinar Cell Inositol Trisphosphate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations used in this Chapter




InsP3 receptor


cyclic- AMP-dependent protein kinase


cyclic-GMP-dependent protein kinase


Ca2+ concentration


cytosolic Ca2+ concentration


polymerase chain reaction


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  1. Benevolensky, D., Moraru, I. I., and Watras, J., 1994, Micromolar calcium decreases affinity of inositol trisphosphate receptor in vascular smooth muscle, Biochem J. 299:631–636.PubMedGoogle Scholar
  2. Berridge, M. J., 1991, Caffeine inhibits inositol-trisphosphate-induced membrane potential oscillations in Xenopus oocytes, Proc. R. Soc. Lond. [Biol.] 244:57–62.Google Scholar
  3. Berridge, M. J., 1993, Inositol trisphosphate and calcium signalling, Nature 361:315–325.PubMedGoogle Scholar
  4. Berridge, M. J., and Irvine, R. F., 1989, Inositol phosphates and cell signalling, Nature 341:197–205.PubMedGoogle Scholar
  5. Bezprozvanny, I., and Ehrlich, B. E., 1993, ATP modulates the function of inositol 1,4,5-trisphosphate-gated channels at two sites, Neuron 10:1175–1184.PubMedGoogle Scholar
  6. Bezprozvanny, I., Watras, J., and Ehrlich, B. E., 1991, Bell-shaped calcium-response curves of InsP3-and calcium-gated channels from endoplasmic reticulum of cerebellum, Nature 351:751–754.PubMedGoogle Scholar
  7. Bezprozvanny, I., Bezprozvannaya, S., and Ehrlich, B. E., 1994, Caffeine-induced inhibition of inositol(l,4,5)-trisphosphate-gated calcium channels from cerebellum, Mol. Biol. Cell 5:97–103.PubMedGoogle Scholar
  8. Bird, G. St. J., Obie, J. F., and Putney, J. W., Jr., 1992, Functional homogeneity of the nonmitochondrial Ca2+ pool in intact mouse lacrimal cells, J. Biol. Chem. 267:18382–18386.PubMedGoogle Scholar
  9. Bird, G. St. J., Rossier, M. F., Obie, J. F., and Putney, J. W., Jr., 1993a, Sinusoidal oscillations in intracellular calcium requiring negative feedback by protein kinase C., J. Biol. Chem. 268:8425–8428.PubMedGoogle Scholar
  10. Bird, G. St. J., Burgess, G. M., and Putney, J. W., Jr., 1993b, Sulfhydryl reagents and cAMP-dependent kinase increase the sensitivity of the inositol 1,4,5-trisphosphate receptor in hepato-cytes, J. Biol. Chem. 268:17917–17923.PubMedGoogle Scholar
  11. Blondel, O., Takeda, J., Janssen, H., Seino, S., and Bell, G. I., 1993, Sequence and functional characterization of a third inositol trisphosphate receptor subtype, IP3R-3, expressed in pancreatic islets, kidney, gastrointestinal tract, and other tissues, J. Biol. Chem. 268:11356–11363.PubMedGoogle Scholar
  12. Blondel, O., Moody, M., Depaoli, M., Sharp, A. H., Ross, C. A., Swift, H., and Bell, E. I., 1994, Localization of inositol trisphosphate receptor subtype 3 to insulin and somatostatin secretory granules and regulation of expression in islets and insulinoma cells, Proc. Natl. Acad. Sci. U.S.A. 91:7777–7781.PubMedGoogle Scholar
  13. Boitano, S., Dirksen, E. R., and Sanderson, M. J., 1992, Intercellular propagation of calcium waves mediated by inositol trisphosphate, Science 258:292–295.PubMedGoogle Scholar
  14. Bond, J. M., and Taylor, C. W., 1991, Solubilization of rat liver inositol 1,4,5-trisphosphate receptor, Cell. Signal. 3:607–612.PubMedGoogle Scholar
  15. Bootman, M. D., Berridge, M. J., and Taylor, C. W., 1992a, All-or-none Ca2+ mobilization from the intracellular stores of single histamine-stimulated HeLa cells, J. Physiol. 450:163–178.PubMedGoogle Scholar
  16. Bootman, M. D., Taylor, C. W., and Berridge, M. J., 1992b, The thiol reagent, thimerosal, evokes Ca2+ spikes in Hela cells by sensitizing the inositol 1,4,5-trisphosphate receptor, J. Biol. Chem. 267:25113–25119.PubMedGoogle Scholar
  17. Bootman, M. D., Missiaen L., Parys, J. B., De Smedt, H., and Casteels, R., 1995, Control of inositol 1,4,5-trisphosphate-induced Ca2+ release by cytosolic Ca2+, Biochem J. 306:445–451.PubMedGoogle Scholar
  18. Bourguignon, L. Y. W., Iida, N., and Jin, H., 1993a, The involvement of the cytoskeleton in regulating IP3 receptor-mediated internal Ca2+ release in human blood platelets, Cell Biol. 17:751–758.Google Scholar
  19. Bourguignon, L. Y. W., Jin, H., Iida, N., Brandt, N. R., and Zhang, S. H., 1993b, The involvement of ankyrin in the regulation of inositol 1,4,5-trisphosphate receptor-mediated internal Ca2+ release from Ca2+ storage vesicles in mouse T-lymphoma cells, J. Biol. Chem. 268:7290–7297.PubMedGoogle Scholar
  20. Brass, L. F., and Joseph, S. K., 1985, A role for inositol triphosphate in intracellular Ca2+ mobilization and granule secretion in platelets, J. Biol. Chem. 260:15172–15179.PubMedGoogle Scholar
  21. Brown, G. R., Sayers, L. G., Kirk, C. J., Michell, R. H., and Michelangeli, F., 1992, The opening of the inositol 1,4,5-trisphosphate-sensitive channel in rat cerebellum is inhibited by caffeine, Biochem. J. 282:309–312.PubMedGoogle Scholar
  22. Burgess, G. M., Bird, G. S. J., Obie, J. F., and Putney, J. W., Jr., 1991, The mechanism for synergism between phospholipase C-and adenylylcyclase-linked hormones in liver. Cyclic AMP-dependent kinase augments inositol trisphosphate-mediated Ca2+ mobilization without increasing the cellular levels of inositol polyphosphates, J. Biol. Chem. 266:4772–4781.PubMedGoogle Scholar
  23. Byron, K. L., and Taylor, C. W., 1993, Spontaneous Ca2+ spiking in avascular smooth muscle cell line is independent of the release of intracellular Ca2+ stores, J. Biol. Chem. 268:6945–6952.PubMedGoogle Scholar
  24. Callamaras, N., and Parker, I., 1994, Inositol 1,4,5-trisphosphate receptors in Xenopus laevis oocytes: Localization and modulation by Ca2+, Cell Calcium 15:66–78.PubMedGoogle Scholar
  25. Carroll, J., and Swann, K., 1992, Spontaneous cytosolic calcium oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes, J. Biol. Chem. 267:11196–11201.PubMedGoogle Scholar
  26. Chadwick, C. C., Saito, A., and Fleischer, S., 1990, Isolation and characterization of the inositol trisphosphate receptor from smooth muscle, Proc. Natl. Acad. Sci. U.S.A. 87:2132–2136.PubMedGoogle Scholar
  27. Champeil, P., Combettes, L., Berthon, B., Doucet, E., Orlowski, S., and Claret, M., 1989, Fast kinetics of calcium release induced by myo-inositol trisphosphate in permeabilized rat hepato-cytes, J. Biol. Chem. 264:17665–17673.PubMedGoogle Scholar
  28. Cheek, T. R., McGuinness, O. M., Vincent, C., Moreton, R. B., Berridge, M. J., and Johnson, M. H., 1993, Fertilisation and thimerosal stimulate similar calcium spiking patterns in mouse oocytes but by separate mechanisms, Development 119:179–189.PubMedGoogle Scholar
  29. Combettes, L., Claret, M., and Champeil, P., 1992, Do submaximal InsP3 concentrations only induce the partial discharge of permeabilized hepatocyte calcium pools because of the concomitant reduction of intraluminal Ca2+ concentration? FEBS Lett. 301:287–290.PubMedGoogle Scholar
  30. Combettes, L., Claret, M., and Champeil, P., 1993, Calcium control on InsP3-induced discharge of calcium from permeabilised hepatocyte pools, Cell Calcium 14:279–292.PubMedGoogle Scholar
  31. Combettes, L., Hannaert-Merah, Z., Coquil, J.-F., Rousseau, C., Claret, M., Swillens, S., and Champeil, P., 1994a, Rapid filtration studies of the effect of cytosolic Ca2+ on InsP3-induced 45Ca2+ release from cerebellar microsomes, J. Biol. Chem. 269:17561–17571.PubMedGoogle Scholar
  32. Combettes, L. Berthon, B., and Claret, M., 1994b, Caffeine inhibits cytosolic calcium oscillations induced by noradrenaline and vasopressin in rat hepatocytes, Biochem. J. 301:737–744.PubMedGoogle Scholar
  33. Danoff, S. K., Ferris, C. D., Donath, C., Fischer, G., Munemitsu, S., Ullrich, A., Snyder, S. H., and Ross, C. A., 1991, Inositol 1,4,5-trisphosphate receptors: distinct neuronal and nonneuro-nal forms derived by alternative splicing differ in phosphorylation, Proc. Natl. Acad. Sci. U.S.A. 88:2951–2955.PubMedGoogle Scholar
  34. De Lisle, S., Radenberg, T., Wintermantel, M. R., Tietz, C., Parys, J. B., Pittet, D., Welsh, M. J., and Mayr, G. W., 1994, Second messenger specificity of the inositol trisphosphate receptor: Reappraisal based on novel inositol phosphates, Am. J. Physiol. 266:C429–C436.Google Scholar
  35. De Smedt, H., Missiaen, L., Parys, J. B., Bootman, M. D., Mertens, L., Van Den Bosch, L., and Casteels, R., 1994, Determination of the relative amounts of inositol trisphosphate receptor mRNA isoforms by ratio polymerase chain reaction, J. Biol. Chem. 269:21691–21698.PubMedGoogle Scholar
  36. Diarra, A., Wang, R., Garneau, L., Gallo-Payet, N., and Sauvé, R., 1994, Histamine-evoked Ca2+ oscillations in HeLa cells are sensitive to methylxanthines but insensitive to ryanodine, Pflugers Arch. 426:129–138.PubMedGoogle Scholar
  37. Ehrlich, B. E., and Watras, J., 1988, Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum, Nature 336:583–586.PubMedGoogle Scholar
  38. Enyedi, P., Szabadkai, G., Horváth, A., Szilágyi, L., Gráf, L., and Spät, A., 1994, Inositol 1,4,5-trisphosphate receptor subtypes in adrenal glomerulosa cells, Endocrinology 134:2354–2359.PubMedGoogle Scholar
  39. Feng, L., and Kraus-Friedman, N., 1993, Association of the hepatic IP3 receptor with the plasma membrane: Relevance to mode of action, Am. J. Physiol. 265:C1588–C1596.PubMedGoogle Scholar
  40. Ferris, C. D., and Snyder, S. H., 1992, Inositol 1,4,5-trisphosphate-activated calcium channels, Annu. Rev. Physiol. 54:469–488.PubMedGoogle Scholar
  41. Ferris, C. D., Huganir, R. L., Supattapone, S., and Snyder, S. H., 1989, Purified inositol 1,4,5-trisphosphate receptor mediates calcium flux in reconstituted lipid vesicles, Nature 342:87–89.PubMedGoogle Scholar
  42. Ferris, C. D., Huganir, R. L., and Snyder, S. H., 1990, Calcium flux mediated by purified inositol 1,4,5-trisphosphate receptor in reconstituted lipid vesicles is allosterically regulated by adenine nucleotides, Proc. Natl. Acad. Sci. U.S.A. 87:2147–2151.PubMedGoogle Scholar
  43. Ferris, C. D., Huganir, R. L., Bredt, D. S., Cameron, A. M., and Snyder, S. H., 1991, Inositol trisphosphate receptor: phosphorylation by protein kinase C and calcium calmodulin-dependent protein kinases in reconstituted lipid vesicles, Proc. Natl. Acad. Sci. U.S.A. 88:2232–2235.PubMedGoogle Scholar
  44. Ferris, C. D., Cameron, A. M., Bredt, D. S., Huganir, R. L., and Snyder, S. H., 1992a, Auto-phosphorylation of inositol 1,4,5-trisphosphate receptors, J. Biol. Chem. 267:7036–7041.PubMedGoogle Scholar
  45. Ferris, C. D., Cameron, A. M., Huganir, R. L., and Snyder, S. H., 1992b, Quantal calcium release by purified reconstituted inositol 1,4,5-trisphosphate receptors, Nature 356:350–352.PubMedGoogle Scholar
  46. Finch, E. A., and Goldin, S. M., 1994, Response to “Calcium and inositol 1,4,5-trisphosphate-induced Ca2+ release,” Science 265:813–815.Google Scholar
  47. Finch, E. A., Turner, T. J., and Goldin, S. M., 1991, Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release, Science 252:443–446.PubMedGoogle Scholar
  48. Fujimoto, T., Nakade, S., Miyawaki, A., Mikoshiba, K., and Ogawa, K., 1992, Localization of inositol 1,4,5-trisphosphate receptor-like protein in plasmalemmal caveolae, J. Cell Biol. 119:1507–1513.PubMedGoogle Scholar
  49. Furuichi, T., Yoshikawa, S., Miyawaki, A., Wada, K., Maeda, N., and Mikoshiba, K., 1989, Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400, Nature 342:32–38.PubMedGoogle Scholar
  50. Furuichi, T., Shiota, C., and Mikoshiba, K., 1990, Distribution of inositol 1,4,5-trisphosphate receptor mRNA in mouse tissues, FEBS Lett. 267:85–88.PubMedGoogle Scholar
  51. Fumichi, T., Simon-Chazottes, D., Fujino, I., Yamada, N., Hasegawa, M., Miyawaki, A., Yoshikawa, S., Guénet, J.-L., and Mikoshiba, K., 1993, Widespread expression of inositol 1,4,5-trisphosphate receptor type 1 gene (Insp3rl) in the mouse central nervous system, Receptors Channels 1:11–24.Google Scholar
  52. Galione, A., McDougall, A., Busa, W. B., Willmott, N., Gillot, I., and Whitaker, M., 1993, Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs, Science 261:348–352.PubMedGoogle Scholar
  53. Gericke, M., Droogmans, G., and Nilius, B., 1993, Thimerosal induced changes of intracellular calcium in human endothelial cells, Cell Calcium 14:201–207.PubMedGoogle Scholar
  54. Ghosh, T. K., Eis, P. S., Mullaney, J. M., Ebert, C. L., and Gill, D. L., 1988, Competitive, reversible, and potent antagonism of inositol 1,4,5-trisphosphate-activated calcium release by heparin, J. Biol. Chem. 263:11075–11079.PubMedGoogle Scholar
  55. Gill, D. L., 1989, Receptor kinships revealed, Nature 342:16–18.PubMedGoogle Scholar
  56. Glennon, M. C., Bird, G. St. J., Kwan, C.-Y., and Putney, J. W., Jr., 1992, Actions of vasopressin and the Ca2+-ATPase inhibitor, thapsigargin, on Ca2+ signaling in hepatocytes, J. Biol. Chem. 267:8230–8233.PubMedGoogle Scholar
  57. Gorza, L., Schiaffino, S., and Volpe, P., 1993, Inositol 1,4-5-trisphosphate receptor in heart: Evidence for its concentration in Purkinje myocytes of the conduction system, J. Cell Biol. 121:345–353.PubMedGoogle Scholar
  58. Guillemette, G., and Segui, J. A., 1988, Effects of pH, reducing and alkylating reagents on the binding and Ca2+ release activities of inositol 1,4,5-trisphosphate in the bovine adrenal cortex, Mol. Endocrinol. 2:1249–1255.PubMedGoogle Scholar
  59. Guillemette, G., Balla, T., Baukal, A. J., and Catt, K. J., 1987, Inositol 1,4,5-trisphosphate binds to a specific receptor and releases microsomal calcium in the anterior pituitary gland, Proc. Natl. Acad. Sci. U.S.A. 84:8195–8199.PubMedGoogle Scholar
  60. Guillemette, G., Favreau, I., Boulay, G., and Potier, M., 1990, Solubilization and partial characterization of inositol 1,4,5-trisphosphate receptor of bovine adrenal cortex reveal similarities with the receptor of rat cerebellum, Mol. Pharmacol. 38:841–847.PubMedGoogle Scholar
  61. Györke, S., and Fill, M., 1993, Ryanodine receptor adaptation: control mechanism of Ca2+-induced Ca2+ release in heart, Science 260:807–809.PubMedGoogle Scholar
  62. Hajnóczky, G., and Thomas, A. P., 1994, The inositol trisphosphate calcium channel is inactivated by inositol trisphosphate, Nature 370:474–477.PubMedGoogle Scholar
  63. Hajnóczky, G., Gao, E., Nomura, T., Hoek, J. B., and Thomas, A. P., 1993, Multiple mechanisms by which protein kinase A potentiates inositol 1,4,5-trisphosphate-induced Ca2+ mobilization in permeabilized hepatocytes, Biochem. J. 293: 413–422.PubMedGoogle Scholar
  64. Hajnóczky, G., Lin, C., and Thomas, A. P., 1994, Luminal communication between intracellular calcium stores modulated by GTP and the cytoskeleton, J. Biol. Chem. 269:10280–10287.PubMedGoogle Scholar
  65. Harootunian, A. T., Kao, J. P. Y., Paranjape, S., and Tsien, R. Y., 1991, Generation of calcium oscillations in fibroblasts by positive feedback between calcium and IP3, Science 251:75–78.PubMedGoogle Scholar
  66. Hilly, M., Piétri-Rouxel, F., Coquil, J. F., Guy, M., and Mauger, J. P., 1993, Thiol reagents increase the affinity of the inositol 1,4,5-trisphosphate receptor, J. Biol. Chem. 268:16488–16494.PubMedGoogle Scholar
  67. Hirata, M., Suematsu, E., Hashimoto, T., Hamachi, T., and Koga, T., 1984, Release of Ca2+ from a non-mitochondrial store site in peritoneal macrophages treated with saponin by inositol 1,4,5-trisphosphate, Biochem. J. 223:229–236.PubMedGoogle Scholar
  68. Hirata, M., Narumoto, N., Watanabe, Y., Kanematsu, T., Koga, T., and Ozaki, S., 1994, DL-myo-inositol 1,2,4,5-tetrakisphosphate, a potent analog of D-myo-inositol 1,4,5-trisphosphate, Mol. Pharmacol. 45:271–276.PubMedGoogle Scholar
  69. Hirose, K., Iino, M., and Endo, M., 1993, Caffeine inhibits Ca2+-mediated potentiation of inositol 1,4,5-trisphosphate-induced Ca2+-release in permeabilized vascular smooth muscle cells, Biochem. Biophys. Res. Commun. 194:726–732.PubMedGoogle Scholar
  70. Iino, M., 1990, Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci, J. Gen. Physiol. 95:1103–1122.PubMedGoogle Scholar
  71. Iino, M., 1991, Effect of adenine nucleotides on inositol 1,4,5-trisphosphate-induced calcium release in vascular smooth muscle cells, J. Gen. Physiol. 98:681–698.PubMedGoogle Scholar
  72. Iino, M., and Endo, M., 1992, Calcium-dependent immediate feedback control of inositol 1,4,5-trisphosphate-induced Ca2+ release, Nature 360:76–78.PubMedGoogle Scholar
  73. Imagawa, T., Smith, J. S., Coronado, R., and Campbell, K. P., 1987, Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum is the Ca2+-permeable pore of the calcium release channel. J. Biol. Chem. 262:16636–16643.PubMedGoogle Scholar
  74. Irvine, R. F., 1990, “Quantal” Ca2+ release and the control of Ca2+ entry by inositol phosphates—a possible mechanism, FEBS Lett. 263:5–9PubMedGoogle Scholar
  75. Irvine, R. F., 1991, Inositol tetrakisphosphate as a second messenger: Confusions, contradictions, and a potential resolution, BioEssays 13:419–427.PubMedGoogle Scholar
  76. Irvine, R. F., Brown, K. D., and Berridge, M. J., 1984, Specificity of inositol trisphosphate-induced calcium release from permeabilized Swiss mouse 3T3 cells, Biochem. J. 222:269–272.PubMedGoogle Scholar
  77. Jacob, R., Merritt, J. E., Hallam, T. J., and Rink, T. J., 1988, Repetitive spikes in cytoplasmic calcium evoked by histamine in human endothelial cells, Nature 335:40–45.PubMedGoogle Scholar
  78. Joseph, S. K., 1994, Biosynthesis of the inositol trisphosphate receptor in WB rat liver epithelial cells, J. Biol. Chem. 269:5673–5679.PubMedGoogle Scholar
  79. Joseph, S. K., and Ryan, S. V., 1993, Phosphorylation of the inositol trisphosphate receptor in isolated rat hepatocytes, J. Biol. Chem. 268:23059–23065.PubMedGoogle Scholar
  80. Joseph, S. K., and Samanta, S., 1993, Detergent solubility of the inositol trisphosphate receptor in rat brain membranes. Evidence for association of the receptor with ankyrin, J. Biol. Chem. 268:6477–6486.PubMedGoogle Scholar
  81. Kasai, H., Li, Y. X., and Miyashita, Y., 1993, Subcellular distribution of Ca2+ release channels underlying Ca2+ waves and oscillations in exocrine pancreas, Cell 74:669–677.PubMedGoogle Scholar
  82. Khan, A. A., Steiner, J. P., and Snyder, S. H., 1992a, Plasma membrane inositol-trisphosphate receptor of lymphocytes: Selective enrichment in sialic acid and unique binding specificity, Proc. Natl. Acad. Sci. U.S.A. 89:2849–2853.PubMedGoogle Scholar
  83. Khan, A. A., Steiner, J. P., Klein, M. G., Schneider, M. F., and Snyder, S. H., 1992b, IP3 receptor: Localization to plasma membrane of T cells and cocapping with the T cell receptor, Science 257:815–818.PubMedGoogle Scholar
  84. Kline, J. T., and Kline, D., 1994, Regulation of intracellular calcium in the mouse egg: Evidence for inositol trisphosphate-induced calcium release, but not calcium-induced calcium release, Biol. Reprod. 50:193–203.PubMedGoogle Scholar
  85. Koga, T., Yoshida, Y., Cai, J.-Q., Islam, M. O., and Imai, S., 1994, Purification and characterization of 240-kDA cGMP-dependent protein kinase substrate of vascular smooth muscle. Close resemblance to inositol 1,4,5-trisphosphate receptor, J. Biol. Chem. 269:11640–11647.PubMedGoogle Scholar
  86. Komalavilas, P., and Lincoln, T. M., 1994, Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic GMP-dependent protein kinase, J. Biol. Chem. 269:8701–8707.PubMedGoogle Scholar
  87. Kume, S., Muto, A., Aruga, J., Nakagawa, T., Michikawa, T., Furuichi, T., Nakade, S., Okano, H., and Mikoshiba, K., 1993, The Xenopus IP3 receptor: structure, function, and localization in oocytes and eggs, Cell 73:555–570.PubMedGoogle Scholar
  88. Lai, F. A., Erickson, H. P., Rousseau, E., Liu, Q. Y., and Meissner, G., 1988, Purification and reconstitution of the calcium release channel from skeletal muscle, Nature 331:315–319.PubMedGoogle Scholar
  89. Lechleiter, J., Girard, S., Clapham, D., and Peralta, E., 1991, Subcellular patterns of calcium release determined by G protein-specific residues of muscarinic receptors, Nature 350:505–508.PubMedGoogle Scholar
  90. Lee, H. C., Aarhus, R., and Walseth, T. F., 1993, Calcium mobilization by dual receptors during fertilization of sea urchin eggs, Science 261:352–355.PubMedGoogle Scholar
  91. Lièvremont, J.-P., Hill, A.-M., Hilly, M., and Mauger, J.-P., 1994, The inositol 1,4,5-trisphosphate receptor is localized on specialized sub-regions of the endoplasmic reticulum in rat liver, Biochem. J. 300:419–427.PubMedGoogle Scholar
  92. Lipscombe, D., Madison, D. V., Poenie, M., Reuter, H., Tsien, R. W., and Tsien, R. Y., 1988, Imaging of cytosolic Ca2+ transients arising from Ca2+ stores and Ca2+ channels in sympathetic neurons, Neuron 1:355–365.PubMedGoogle Scholar
  93. Loomis-Husselbee, J. W., and Dawson, A. P., 1993, A steady-state mechanism can account for the properties of inositol 2,4,5-trisphosphate-stimulated Ca2+ release from permeabilized L1210 cells, Biochem. J. 289:861–866.PubMedGoogle Scholar
  94. Luttrell, B. M., 1993, The biological relevance of the binding of calcium ions by inositol phosphates, J. Biol. Chem. 268:1521–1524.PubMedGoogle Scholar
  95. Lynn, S., Morgan, J. M., Gillespie, J. I., and Greenwell, J. R., 1993. A novel ryanodine sensitive calcium release mechanism in cultured human myometrial smooth-muscle cells, FEBS Lett. 330:227–230.PubMedGoogle Scholar
  96. Maeda, N., Niinobe, M., Nakahira, K., and Mikoshiba, K., 1988, Purification and characterization of P400 protein, a glycoprotein characteristic of Purkinje cell, from mouse cerebellum, J. Neurochem. 51:1724–1730.PubMedGoogle Scholar
  97. Maeda, N., Niinobe, M., Inoue, Y., and Mikoshiba, K., 1989, Developmental expression and intracellular location of P400 protein characteristic of Purkinje cells in mouse cerebellum, Dev. Biol. 133:67–76.PubMedGoogle Scholar
  98. Maeda, N., Niinobe, M., and Mikoshiba, K., 1990, A cerebellar Purkinje cell marker P400 protein is an inositol 1,4,5-trisphosphate (InsP3) receptor protein. Purification and characterization of InsP3 receptor complex, EMBO J. 9:61–67.PubMedGoogle Scholar
  99. Maeda, N., Kawasaki, T., Nakade, S., Yokota, N., Taguchi, T., Kasai, M., and Mikoshiba, K., 1991, Structural and functional characterization of inositol 1,4,5-trisphosphate receptor channel from mouse cerebellum, J. Biol. Chem. 266:1109–1116.PubMedGoogle Scholar
  100. Magnussen, A., Haug, L. S., Walaas, S. I., and Østvold, A. C., 1993, Calcium-induced degradation of the inositol (1,4,5)-trisphosphate receptor/Ca2+-channel, FEBS Lett. 323:229–232.Google Scholar
  101. Maranto, A. R., 1994, Primary structure, ligand binding, and localization of the human type 3 inositol 1,4,5-trisphosphate receptor expressed in intestinal epithelium, J. Biol. Chem. 269:1222–1230.PubMedGoogle Scholar
  102. Marks, A. R., Tempst, P., Chadwick, C. C., Riviere, L., Fleischer, S., and Nadal-Ginard, B., 1990, Smooth muscle and brain inositol 1,4,5-trisphosphate receptors are structurally and functionally similar, J. Biol. Chem. 265:20719–20722.PubMedGoogle Scholar
  103. Marshall, I. C. B., and Taylor, C. W., 1993a, Biphasic effects of cytosolic Ca2+ on InsP3-stimulated Ca2+ mobilization in hepatocytes, J. Biol. Chem. 268:13214–13220.PubMedGoogle Scholar
  104. Marshall, I. C. B., and Taylor, C. W., 1993b, Regulation of inositol 1,4,5-trisphosphate receptors, J. Exp. Biol. 184:161–182.PubMedGoogle Scholar
  105. Marshall, I. C. B., and Taylor, C. W., 1994, Two calcium-binding sites mediate the interconversion of liver inositol 1,4,5-trisphosphate receptors between three conformational states, Biochem. J. 301:591–598.PubMedGoogle Scholar
  106. Matter, N., Ritz, M. F., Freyermuth, S., Rogue, P., and Malviya, A. N., 1993, Stimulation of nuclear protein kinase C leads to phosphorylation of nuclear inositol 1,4,5-trisphosphate receptor and accelerated calcium release by inositol 1,4,5-trisphosphate from isolated rat liver nuclei, J. Biol. Chem. 268:732–736.PubMedGoogle Scholar
  107. Mauger, J.-P., Claret, M., Piétri, F., and Hilly, M., 1989, Hormonal regulation of inositol 1,4,5-trisphosphate receptor in rat liver, J. Biol. Chem. 264:8821–8826.PubMedGoogle Scholar
  108. Mauger, J.-P., Lièvremont, J.-P., Piétri-Rouxel, F., Hilly, M., and Coquil, J.-F., 1994, The inositol 1,4,5-trisphosphate receptor: Kinetic properties and regulation, Mol. Cell. Endocrinol. 98:133–139.PubMedGoogle Scholar
  109. Mayrleitner, M., Chadwick, C. C., Timmerman, A. P., Fleischer, S., and Schindler, H., 1991, Purified IP3 receptor from smooth muscle forms an IP3 gated and heparin sensitive Ca2+ channel in planar bilayers, Cell Calcium 12:505–514.PubMedGoogle Scholar
  110. Menniti, F. S., Bird, G. St. J., Takemura, H., Thastrup, O., Potter, B. V. L., and Putney, J. W., Jr., 1991, Mobilization of calcium by inositol trisphosphates from permeabilized rat parotid acinar cells. Evidence for translocation of calcium from uptake to release sites within the inositol 1,4,5-trisphosphate-and thapsigargin-sensitive calcium pool, J. Biol. Chem. 266:13646–13653.PubMedGoogle Scholar
  111. Meyer, T., and Stryer, L., 1990, Transient calcium release induced by successive increments of inositol 1,4,5-trisphosphate, Proc. Natl. Acad. Sci. U.S.A. 87:3841–3845.PubMedGoogle Scholar
  112. Meyer, T., Wensel, T., and Stryer, L., 1990, Kinetics of calcium channel opening by inositol 1,4,5-trisphosphate, Biochemistry 29:32–37.PubMedGoogle Scholar
  113. Michikawa, T., Hamanaka, H., Otsu, H., Yamamoto, A., Miyawaki, A., Furuichi, T., Tashiro, Y., and Mikoshiba, K., 1994, Transmembrane topology and sites of N-glycosylation of inositol 1,4,5-trisphosphate receptor, J. Biol. Chem. 269:9184–9189.PubMedGoogle Scholar
  114. Mignery, G. A., and Südhof, T. C., 1990, The ligand binding site and transduction mechanism in the inositol-1,4,5-trisphosphate receptor, EMBO J. 9:3893–3898.PubMedGoogle Scholar
  115. Mignery, G. A., Südhof, T. C., Takei, K., and De Camilli, P., 1989, Putative receptor for inositol 1,4,5-trisphosphate similar to the ryanodine receptor, Nature 342:192–195.PubMedGoogle Scholar
  116. Mignery, G. A., Newton, C. L., Archer, B. T. III, and Südhof, T. C., 1990, Structure and expression of the rat inositol 1,4,5-trisphosphate receptor, J. Biol. Chem. 265:12679–12684.PubMedGoogle Scholar
  117. Mignery, G. A., Johnston, P. A., and Südhof, T. C., 1992, Mechanism of Ca2+ inhibition of inositol 1,4,5-trisphosphate (InsP3) binding to the cerebellar InsP3 receptor, J. Biol. Chem. 267:7450–7455.PubMedGoogle Scholar
  118. Mikoshiba, K., 1993, Inositol 1,4,5-trisphosphate receptor, Trends Pharmacol. Sci. 14:86–89.PubMedGoogle Scholar
  119. Missiaen, L., Taylor, C. W., and Berridge, M. J., 1991, Spontaneous calcium release from inositol trisphosphate-sensitive calcium stores, Nature 352:241–244.PubMedGoogle Scholar
  120. Missiaen, L., Taylor, C. W., and Berridge, M. J., 1992a, Luminal Ca2+ promoting spontaneous Ca2+ release from inositol trisphosphate-sensitive stores in rat hepatocytes, J. Physiol. 455:623–640.PubMedGoogle Scholar
  121. Missiaen, L., De Smedt, H., Droogmans, G., and Casteels, R., 1992b, Ca2+ release induced by inositol 1,4,5-trisphosphate is a steady-state phenomenon controlled by luminal Ca2+ in per-meabilized cells, Nature 357:599–602.PubMedGoogle Scholar
  122. Missiaen, L., De Smedt, H., Droogmans, G., and Casteels, R., 1992c, Luminal Ca2+ controls the activation of the InsP3 receptor by cytosolic Ca2+, J. Biol. Chem. 267:22961–22966.PubMedGoogle Scholar
  123. Missiaen, L., De Smedt, H., Parys, J. B., and Casteels, R., 1994a, Co-activation of inositol trisphosphate-induced Ca2+ release by cytosolic Ca2+ is loading-dependent, J. Biol. Chem. 269:7238–7242.PubMedGoogle Scholar
  124. Missiaen, L., Parys, J. B., De Smedt, H., Himpens, B., and Casteels, R., 1994b, Inhibition of inositol trisphosphate-induced calcium release by caffeine is prevented by ATP, Biochem. J. 300:81–84.PubMedGoogle Scholar
  125. Missiaen, L., Parys, J. B., De Smedt, H., Oike, M., and Casteels, R., 1994c, Partial calcium release in response to submaximal inositol 1,4,5-trisphosphate receptor activation, Mol. Cell. Endocrinol. 98:147–156.PubMedGoogle Scholar
  126. Miyawaki, A., Furuichi, T., Maeda, N., and Mikoshiba, K., 1990, Expressed cerebellar-type inositol 1,4,5-trisphosphate receptor, P400, has calcium release activity in a fibroblast L cell line. Neuron 5:11–18.PubMedGoogle Scholar
  127. Miyawaki, A., Furuichi, T., Ryou, Y., Yoshikawa, S., Nakagawa, T., Saitoh, T., and Mikoshiba, K., 1991, Structure-function relationships of the mouse inositol 1,4,5-trisphosphate receptor, Proc. Natl. Acad. Sci. U.S.A. 88:4911–4915.PubMedGoogle Scholar
  128. Miyazaki, S.-I., Shirakawa, H., Nakada, K., Honda, Y., Yuzaki, M., Nakade, S., and Mikoshiba, K., 1992, Antibody to the inositol trisphosphate receptor blocks thimerosal-enhanced Ca2+-induced Ca2+ release and Ca2+ oscillations in hamster eggs, FEBS Lett. 309:180–184.PubMedGoogle Scholar
  129. Mohr, F. C., Hershey, P. E. C., Zimányi, I., and Pessah, I. N., 1993, Regulation of inositol 1,4,5-trisphosphate receptors in rat basophilic leukemia cells. I. Multiple conformational states of the receptor in a microsomal preparation, Biochim. Biophys. Acta 1147:105–114.PubMedGoogle Scholar
  130. Moschella, M. C., and Marks, A. R., 1993, Inositol 1,4,5-trisphosphate receptor expression in cardiac myocytes, J. Cell Biol. 120:1137–1146.PubMedGoogle Scholar
  131. Mourey, R. J., Verma, A., Supattapone, S., and Snyder, S. H., 1990, Purification and characterization of the inositol 1,4,5-trisphosphate receptor protein from vas deferens, Biochem. J. 272:383–389.PubMedGoogle Scholar
  132. Mourey, R. J., Estevez, V. A. Marecek, J. F., Barrow, R. K., Prestwich, G. D., and Snyder, S. H., 1993, Inositol 1,4,5-trisphosphate receptors: Labeling the inositol 1,4,5-trisphosphate binding site with photoaffinity ligands, Biochemistry 32:1719–1726.PubMedGoogle Scholar
  133. Muallem, S., Pandol, S. J., and Beeker, T. G., 1989, Hormone-evoked calcium release from intracellular stores is a quantal process, J. Biol. Chem. 264:205–212.PubMedGoogle Scholar
  134. Nakade, S., Maeda, N., and Mikoshiba, K., 1991, Involvement of the C-terminus of the inositol 1,4,5-trisphosphate receptor in Ca2+ release analysed using region-specific monoclonal antibodies, Biochem. J. 277:125–131.PubMedGoogle Scholar
  135. Nakade, S., Rhee, S. K., Hamanaka, H., and Mikoshiba, K., 1994, Cyclic AMP-dependent phosphorylation of an immunoaffinity-purified homotetrameric inositol 1,4,5-trisphosphate receptor (type I) increases Ca2+ flux in reconstituted lipid vesicles, J. Biol. Chem. 269:6735–6742.PubMedGoogle Scholar
  136. Nakagawa, T., Okano, H., Furuichi, T., Amga, J., and Mikoshiba, K., 1991a, The subtypes of the mouse inositol 1,4,5-trisphosphate receptor are expressed in a tissue-specific and developmen-tally specific manner, Proc. Natl. Acad. Sci. U.S.A. 88:6244–6248.PubMedGoogle Scholar
  137. Nakagawa, T., Shiota, C., Okano, H., and Mikoshiba, K., 1991b, Differential localization of alternative spliced transcripts encoding inositol 1,4,5-trisphosphate receptors in mouse cerebellum and hippocampus: In situ hybridization study, J. Neurochem. 57:1807–1810.PubMedGoogle Scholar
  138. Nathanson, M. H., Fallon, M. B., Padfield, P. J., and Maranto, A. R., 1994, Localization of the type 3 inositol 1,4,5-trisphosphate receptor in the Ca2+ wave trigger zone of pancreatic acinar cells, J. Biol. Chem. 269:4693–4696.PubMedGoogle Scholar
  139. Nunn, D. L., and Taylor, C. W., 1990, Liver inositol 1,4,5-trisphosphate-binding sites are the Ca2+-mobilizing receptors, Biochem J. 270:227–232.PubMedGoogle Scholar
  140. Nunn, D. L., and Taylor, C. W., 1992, Luminal Ca2+ increases the sensitivity of Ca2+ stores to inositol 1,4,5-trisphosphate, Mol. Pharmacol. 41:115–119.PubMedGoogle Scholar
  141. Oldershaw, K. A., and Taylor, C. W., 1993, Luminal Ca2+ increases the affinity of inositol 1,4,5-trisphosphate for its receptor, Biochem. J. 292:631–633.PubMedGoogle Scholar
  142. Oldershaw, K. A., Nunn, D. L., and Taylor, C. W., 1991, Quantal Ca2+ mobilization stimulated by inositol 1,4,5-trisphosphate in permeabilized hepatocytes, Biochem. J. 278:705–708.PubMedGoogle Scholar
  143. Oldershaw, K. A., Richardson, A., and Taylor, C. W., 1992, Prolonged exposure to inositol 1,4,5-trisphosphate does not cause intrinsic desensitization of the intracellular Ca2+-mobilizing receptor, J. Biol. Chem. 267:16312–16316.PubMedGoogle Scholar
  144. Ospichuk, Y. V., Wakui, M., Yule, D. I., Gallacher, D. V., and Petersen, O. H., 1990, Cytoplasmic Ca2+ oscillations evoked by receptor stimulation, G-protein activation, internal application of inositol trisphosphate or Ca24: Simultaneous microfluorimetry and Ca2+ dependent Cl- current recording in single pancreatic acinar cells, EMBO J. 9:697–704.Google Scholar
  145. Ozaki, S., Watanabe, Y., Ogasawara, T., Hirata, M., and Kanamatsu, M., 1992, Synthesis and biological properties of 2-substituted myo-inositol 1,4,5-trisphosphate analogues directing toward affinity chromatography and photoaffinity labeling, Carbohydr. Res. 234: 189–206.PubMedGoogle Scholar
  146. Parker, I., and Ivorra, I., 1990a, Inhibition by Ca2+ of inositol trisphosphate-mediated Ca2+ liberation: A possible mechanism for oscillatory release of Ca2+, Proc. Natl. Acad. Sci. U.S.A. 87:260–264.PubMedGoogle Scholar
  147. Parker, I., and Ivorra, I., 1990b, Localized all-or-none calcium liberation by inositol trisphosphate. Science 250:977–979.PubMedGoogle Scholar
  148. Parker, I., and Ivorra, I., 1991, Caffeine inhibits inositol trisphosphate-mediated liberation of intracellular calcium in Xenopus oocytes, J. Physiol. 433:229–240.PubMedGoogle Scholar
  149. Parker, I., and Yao, Y., 1991, Regenerative release of calcium from functionally discrete subcellular stores by inositol trisphosphate, Proc. R. Soc. Lond. [Biol.] 246:269–274.Google Scholar
  150. Parys, J. B., Sernett, S. W., DeLisle, S., Snyder, P. M., Welsh, M. J., and Campbell, K. P., 1992, Isolation, characterization, and localization of the inositol 1,4,5-trisphosphate receptor protein in Xenopus laevis oocytes, J. Biol. Chem. 267:18776–18782.PubMedGoogle Scholar
  151. Parys, J. B., Missiaen, L., De Smedt, H., and Casteels, R., 1993a, Loading dependence of inositol 1,4,5-trisphosphate-induced Ca2+ release in the clonal cell line A7r5. Implications for the mechanism of quantal Ca2+ release, J. Biol. Chem. 268:25206–25212.PubMedGoogle Scholar
  152. Parys, J. B., Missiaen, L., De Smedt, H., Droogmans, G., and Casteels, R., 1993b, Bell-shaped activation of inositol 1,4,5-trisphosphate-induced Ca2+ release by thimerosal in permeabilized A7r5 smooth-muscle cells, Pflugers Arch. 424:516–522.PubMedGoogle Scholar
  153. Parys, J. B., McPherson, S. M., Mathews, L., Campbell, K. P., and Longo, F., 1994, Presence of inositol 1,4,5-trisphosphate receptor, calreticulin, and calsequestrin in eggs of sea urchins and Xenopus laevis, Dev. Biol. 161:466–476.PubMedGoogle Scholar
  154. Parys, J. B., De Smedt, H., Missiaen, L., Bootman, M. D., Sienaert, I., and Casteels, R., 1995, Rat basophilic leukemia cells as model system for inositol 1,4,5-trisphosphate receptor IV, a receptor of the type II family: functional comparison and immunological detection, Cell Calcium 17:239–249.PubMedGoogle Scholar
  155. Peng, Y.-W., Sharp, A. H., Snyder, S. H., and Yau, K.-W., 1991, Localization of the inositol 1,4,5-trisphosphate receptor in synaptic terminal in the vertebrate retina, Neuron 6:525–531.PubMedGoogle Scholar
  156. Petersen, O. H., 1992, Stimulus-secretion coupling: Cytoplasmic calcium signals and the control of ion channels in exocrine acinar cells, J. Physiol. 448:1–51.PubMedGoogle Scholar
  157. Piétri, F., Hilly, M., and Mauger, J. P., 1990, Calcium mediates the interconversion between two states of the liver inositol 1,4,5-trisphosphate receptor, J. Biol. Chem. 265:17478–17485.PubMedGoogle Scholar
  158. Piétri Rouxel, F., Hilly, M., and Mauger, J. P., 1992 Characterization of a rapidly dissociating inositol 1,4,5-trisphosphate-binding site in liver membranes, J. Biol. Chem. 267:20017–20023.Google Scholar
  159. Poitras, M., Bernier, S., Servant, M., Richard, D. E., Boulay, G., and Guillemette, G., 1993, The high affinity state of inositol 1,4,5-trisphosphate receptor is a functional state, J. Biol. Chem. 268:24078–24082.PubMedGoogle Scholar
  160. Renard, D. C., Seitz, M. B., and Thomas, A. P., 1992, Oxidized glutathione causes sensitization of calcium release to inositol 1,4,5-trisphosphate in permeabilized hepatocytes, Biochem. J. 284:507–512.PubMedGoogle Scholar
  161. Richardson, A., and Taylor, C. W., 1993, Effects of Ca2+ chelators on purified inositol 1,4,5-trisphosphate (InsP3) receptors and InsP3-stimulated Ca2+ mobilization, J. Biol. Chem. 268:11528–11533.PubMedGoogle Scholar
  162. Rooney, T. A., Renard, D. C., Sass, E. J., and Thomas, A. P., 1991, Oscillatory cytosolic calcium waves independent of stimulated inositol 1,4,5-trisphosphate formation in hepatocytes, J. Biol. Chem. 266:12272–12282.PubMedGoogle Scholar
  163. Ross, C. A., Meldolesi, J., Milner, T. A., Satoh, T, Supattapone, S., and Snyder, S. H., 1989. Inositol 1,4,5-trisphosphate receptor localized to endoplasmic reticulum in cerebellar Purkinje neurons, Nature 339:468–470.PubMedGoogle Scholar
  164. Ross, C. A., Danoff, S. K., Schell, M. J., Snyder, S. H., and Ullrich, A., 1992, Three additional inositol 1,4,5-trisphosphate receptors: Molecular cloning and differential localization in brain and peripheral tissues, Proc. Natl. Acad. Sci. U.S.A. 89:4265–4269.PubMedGoogle Scholar
  165. Rossier, M. F., Bird, G. St. J., and Putney, J. W., Jr., 1991, Subcellular distribution of the calcium-storing inositol 1,4,5-trisphosphate-sensitive organelle in rat liver. Possible linkage to the plasma membrane through the actin microfilaments, Biochem. J. 274:643–650.PubMedGoogle Scholar
  166. Sanchez-Bueno, A., Marrero, I., and Cobbold, P. H., 1994, Caffeine inhibits agonist-induced cytoplasmic Ca2+ oscillations in single rat hepatocytes, Biochem. Biophys. Res. Commun. 198:728–733.PubMedGoogle Scholar
  167. Sayers, L. G., Brown, G. R., Michell, R. H., and Michelangeli, F., 1993, The effects of thimerosal on calcium uptake and inositol 1,4,5-triphosphate-induced calcium release in cerebellar microsomes, Biochem. J. 289:883–887.PubMedGoogle Scholar
  168. Schell, M. J., Danoff, S. K., and Ross, C. A., 1993, Inositol (l,4,5)-trisphosphate receptor: Characterization of neuron-specific alternative splicing in rat brain and peripheral tissues, Mol. Brain Res. 17:212–216.PubMedGoogle Scholar
  169. Sharp, A. H., Snyder, S. H., and Nigam, S. K., 1992, Inositol 1,4,5-trisphosphate receptors. Localization in epithelial tissues, J. Biol. Chem. 267:7444–7449.PubMedGoogle Scholar
  170. Sharp, A. H., Dawson, T. M., Ross, C. A., Fotuhi, M., Mourey, R. J., and Snyder, S. H., 1993, Inositol 1,4,5-trisphosphate receptors: Immunohistochemical localization to discrete areas of rat central nervous system, Neuroscience 53:927–942.PubMedGoogle Scholar
  171. Short, A. D., Klein, M. G., Schmeider, M. F., and Gill, D. L., 1993, Inositol 1,4,5-trisphosphate-mediated quantal Ca2+ release measured by high resolution imaging of Ca2+ within organelles, J. Biol. Chem. 268:25887–25893.PubMedGoogle Scholar
  172. Shuttleworth, T. S., 1992, Ca2+ release from inositol trisphosphate-sensitive stores is not modulated by intraluminal [Ca2+], J. Biol. Chem. 267:3573–3576.PubMedGoogle Scholar
  173. Sitsapesan, R., and Williams, A. J., 1994, Regulation of the gating of the sheep cardiac sarcoplasmic reticulum Ca2+-release channel by luminal Ca2+, J. Membr. Biol. 137:215–226.PubMedGoogle Scholar
  174. Spät, A., Bradford, P. G., McKinney, J. S., Rubin, R. P., and Putney, J. W., Jr., 1986, A saturable receptor for 32P-inositol-1,4,5-trisphosphate in hepatocytes and neutrophils, Nature 319:514–516.PubMedGoogle Scholar
  175. Spät, A., Eberhardt, I., and Kiesel, L., 1992, Low concentrations of adenine nucleotides enhance the receptor binding of inositol 1,4,5-trisphosphate, Biochem. J. 287:335–336.PubMedGoogle Scholar
  176. Südhof, T. C., Newton, C. L., Archer, B. T. III, Ushkaryov, Y. A., and Mignery, G. A., 1991, Structure of a novel InsP3 receptor, EMBO J. 10:3199–3206.PubMedGoogle Scholar
  177. Sugiyama, T., Yamamoto-Hino, M., Miyawaki, A., Furuichi, T., Mikoshiba, K., and Hasegawa, M., 1994, Subtypes of inositol 1,4,5-trisphosphate receptor in human hematopoietic cell lines: Dynamic aspects of their cell-type specific expression, FEBS Lett. 349:191–196.PubMedGoogle Scholar
  178. Supattapone, S., Worley, P. F., Baraban, J. M., and Snyder, S. H., 1988, Solubilization, purification, and characterization of an inositol trisphosphate receptor, J. Biol. Chem. 263:1530–1534.PubMedGoogle Scholar
  179. Swann, K., 1991, Thimerosal causes calcium oscillations and sensitizes calcium-induced calcium release in unfertilized hamster eggs, FEBS Lett. 278:175–178.PubMedGoogle Scholar
  180. Takahashi, M., Tanzawa, K., and Takahashi, S., 1994, Adenophostins, newly discovered metabolites of Penicillium brevicompactum, act as potent agonists of the inositol 1,4,5-trisphosphate receptor, J. Biol. Chem. 269:369–372.PubMedGoogle Scholar
  181. Takei, K., Mignery, G. A., Mugnaini, E., Südhof, T. C., and De Camilli, P., 1994, Inositol 1,4,5-trisphosphate receptor causes formation of ER cisternal stacks in transfected fibroblasts and in cerebellar Purkinje cells, Neuron 12:327–342.PubMedGoogle Scholar
  182. Tanaka, Y., and Tashjian, A. H., Jr., 1994, Thimerosal potentiates Ca2+ release mediated by both the inositol 1,4,5-trisphosphate and the ryanodine receptors in sea urchin eggs. Implications for mechanistic studies on Ca2+ signaling, J. Biol. Chem. 269:11247–11253.PubMedGoogle Scholar
  183. Tasaka, K., Mio, M., Akagi, M., Fujisawa, K., and Aoki, I., 1991, Role of the cytoskeleton in Ca2+ release from the intracellular Ca store of rat peritoneal mast cells, Agents Actions 33:44–47.PubMedGoogle Scholar
  184. Taylor, C. W., and Potter, B. V. L., 1990, The size of inositol 1,4,5-trisphosphate-sensitive Ca2+ stores depends on inositol 1,4,5-trisphosphate concentration, Biochem. J. 266:189–194.PubMedGoogle Scholar
  185. Taylor, C. W., and Richardson, A., 1991, Structure and function of inositol trisphosphate receptors, Pharmacol. Ther. 51:97–137.PubMedGoogle Scholar
  186. Thorn, P., Brady, P., Llopis, J., Gallacher, D. V., and Petersen, O. H., 1992, Cytosolic Ca2+ spikes evoked by the thiol reagent thimerosal in both intact and internally perfused single pancreatic acinar cells, Pflugers Arch. 422:173–178.PubMedGoogle Scholar
  187. Thorn, P., Lawrie, A. M., Smith, P. M., Gallacher, D. V., and Petersen, O. H., 1993, Local and global cytosolic Ca2+ oscillations in exocrine cells evoked by agonists and inositol trisphosphate, Cell 74:661–668.PubMedGoogle Scholar
  188. Toescu, E. C., O’Neill, S. C., Petersen, O. H., and Eisner, D. A., 1992, Caffeine inhibits the agonist-evoked cytosolic Ca2+ signal in mouse pancreatic acinar cells by blocking inositol trisphosphate production, J. Biol. Chem. 267:23467–23470.PubMedGoogle Scholar
  189. Tregear, R., Dawson, A. P., and Irvine, R. F., 1991, Quantal release of Ca2+ from intracellular stores by InsP3: Tests of the concept of control of Ca2+ release by intraluminal Ca2+, Proc. R. Soc. Lond. [Biol.] 243:263–268.Google Scholar
  190. Tshipamba, M., De Smedt, H., Missiaen, L., Himpens, B., Van Den Bosch, L., and Borghgraef, R., 1993, Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca2+ release in renal epithelial LLC-PK1 cells, J. Cell. Physiol. 155:96–103.PubMedGoogle Scholar
  191. Tsukioka, M., Iino, M., and Endo, M., 1994, pH dependence of inositol 1,4,5-trisphosphate-induced Ca2+ release in permeabilized smooth muscle cells of the guinea-pig, J. Physiol. 475:369–375.PubMedGoogle Scholar
  192. Tsunada, Y., 1986, An ATP-dependent and inositol trisphosphate-sensitive Ca2+ pool linked with microfilaments of the parietal cell, FEBS Lett. 207:47–52.Google Scholar
  193. Van Delden, C., Foti, M., Lew, D. P., and Krause, K. H., 1993, Ca2+ and Mg2+ regulation of inositol 1,4,5-trisphosphate binding in myeloid cells, J. Biol. Chem. 268:12443–12448.PubMedGoogle Scholar
  194. Varney, M. A., Rivera, J., Lopez Bernal, A., and Watson, S. P., 1990, Are there subtypes of the inositol 1,4,5-trisphosphate receptor? Biochem. J. 269:211–216.PubMedGoogle Scholar
  195. Volpe, P., and Alderson-Lang, B. H., 1990, Regulation of inositol 1,4,5-trisphosphate-induced Ca2+ release II. Effect of cAMP-dependent protein kinase, Am. J. Physiol. 258:C1086–C1091.PubMedGoogle Scholar
  196. Wagenknecht, T., Grassucci, R., Frank, J., Saito, A., Inui, M., and Fleischer, S., 1989, Three-dimensional architecture of the calcium channel/foot structure of sarcoplasmic reticulum, Nature 338:167–170.PubMedGoogle Scholar
  197. Wakui, M., Potter, B. V. L., and Petersen, O. H., 1989, Pulsatile intracellular calcium release does not depend on fluctuations in inositol trisphosphate concentration, Nature 339:317–320.PubMedGoogle Scholar
  198. Wakui, M. Osipchuk, Y. V., and Petersen, O. H., 1990, Receptor-activated cytoplasmic Ca2+ spiking mediated by inositol trisphosphate is due to Ca2+-induced Ca2+ release, Cell 63:1025–1032.PubMedGoogle Scholar
  199. White, A. M., Varney, M. A., Watson, S. P., Rigby, S., Changsheng, L., Ward, J. G., Reese, C. B., Graham, H. C., and Williams, R. J. P., 1991, Influence of Mg2+ and pH on n.m.r. spectra and radioligand binding of inositol 1,4,5-trisphosphate, Biochem. J. 278:759–764.PubMedGoogle Scholar
  200. White, A. M., Varney, M. A., Maeda, M., Mikoshiba, K., and Watson, S. P., 1993, Comparison of Ins(l,4,5)P3 receptors from rat cerebellum and bovine adrenal cortex, Biochim. Biophys. Acta 1175:307–311.PubMedGoogle Scholar
  201. Wilcox, R. A., Whitham, E. M., Liu, C., Potter, B. V. L., and Nahorski, S. R., 1993, Myo-inositol 1,3,4,5-tetrakisphosphate can independently mobilise intracellular calcium, via the inositol 1,4,5-trisphosphate receptor: Studies with myo-inositol l,4,5-trisphosphate-3-phosphorothioate and myo-inositol hexakisphosphate, FEBS Lett. 336:267–271.PubMedGoogle Scholar
  202. Wilcox, R. A., Safrany, S. T., Lampe, D., Mills, S. J., Nahorski, S. R., and Potter, B. V. L., 1994, Modification at C2 of myo-inositol 1,4,5-trisphosphate produces inositol trisphosphates and tetrakisphosphates with potent biological activities, Eur. J. Biochem. 223:115–124.PubMedGoogle Scholar
  203. Wojcikiewicz, R. J. H., Furuichi, T., Nakade, S., Mikoshiba, K., and Nahorski, S. R., 1994, Muscarinic receptor activation down-regulates the type I inositol 1,4,5-trisphosphate receptor by accelerating its degradation, J. Biol. Chem. 269:7963–7969.PubMedGoogle Scholar
  204. Woods, N. M., Cuthbertson, K. S. R., and Cobbold, P. H., 1986, Repetitive transient rises in cytoplasmic free calcium in hormone-stimulated hepatocytes, Nature 319:600–602.PubMedGoogle Scholar
  205. Worley, P. F., Baraban, J. M., Supattapone, S., Wilson, V. S., and Snyder, S. H., 1987, Characterization of inositol trisphosphate receptor binding in brain. Regulation by pH and calcium, J. Biol. Chem. 262:12132–12136.PubMedGoogle Scholar
  206. Yamada, N., Makino, Y., Clark, R. A., Pearson, D. W., Mattel, M.-G., Guénet, J.-L., Ohama, E., Fujino, L, Miyawaki, A., Furuichi, T., and Mikoshiba, K., 1994, Human inositol 1,4,5-trisphosphate type-1 receptor, InsP3Rl: Structure, function, regulation of expression and chromosomal localization, Biochem. J. 302:781–790.PubMedGoogle Scholar
  207. Yamamoto-Hino, M., Sugiyama, T., Hikichi, K., Mattei, M. G., Hasegawa, K., Sekine, S., Sakurada, K., Miyawaki, A., Furuichi, T., Hasegawa, M., and Mikoshiba, K., 1994, Cloning and characterization of human type 2 and type 3 inositol 1,4,5-trisphosphate receptors, Receptors Channels 2:9–22.PubMedGoogle Scholar
  208. Yao, Y., and Parker, I., 1992, Potentiation of inositol trisphosphate-induced Ca2+ mobilization in Xenopus oocytes by cytosolic Ca2+, J. Physiol. 458:319–338.PubMedGoogle Scholar
  209. Yoo, S. H., 1994, pH-dependent interaction of chromogranin A with integral membrane proteins of secretory vesicle including 260-kDa protein reactive to inositol 1,4,5-trisphosphate receptor antibody, J. Biol. Chem. 269:12001–12006.PubMedGoogle Scholar
  210. Yoo, S. H., and Lewis, M. S., 1994, pH-dependent interaction of an intraluminal loop of inositol 1,4,5-trisphosphate receptor with chromogranin A, FEBS Lett. 341:28–32.PubMedGoogle Scholar
  211. Yoshikawa, M., Tanimura, T., Miyawaki, A., Nakamura, M., Yuzaki, M., Furuichi, T., and Mikoshiba, K., 1992, Molecular cloning and characterization of the inositol 1,4,5-trisphosphate receptor in Drosophila melanogaster, J. Biol. Chem. 267:16613–16619.PubMedGoogle Scholar
  212. Zhang, B. X., and Muallem, S., 1992, Feedback inhibition of Ca2+ release by Ca2+ is the underlying mechanism of agonist-evoked intracellular Ca2+ oscillations in pancreatic acinar cells, J. Biol. Chem. 267:24387–24393.PubMedGoogle Scholar
  213. Zhang, B. X., Zhao, H., and Muallem, S., 1993, Ca2+-dependent kinase and phosphatase control inositol 1,4,5-trisphosphate-mediated Ca2+ release. Modification by agonist stimulation, J. Biol. Chem. 268:10997–11001.PubMedGoogle Scholar
  214. Zhao, H., Khademazad, M., and Muallem, S., 1990a, Agonist-mediated Ca2+ release in per-meabilized UMR-106-01 cells. Transport properties and generation of inositol 1,4,5-trisphosphate, J. Biol. Chem. 265:14822–14827.PubMedGoogle Scholar
  215. Zhao, H., Loessberg, P. A., Sachs, G., and Muallem, S., 1990b, Regulation of intracellular Ca2+ oscillations in AR42J cells, J. Biol. Chem. 265:20856–20862.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1996

Authors and Affiliations

  • Ludwig Missiaen
    • 1
  • Jan B. Parys
    • 1
  • Humbert De Smedt
    • 1
  • Ilse Sienaert
    • 1
  • Martin D. Bootman
    • 2
  • Rik Casteels
    • 1
  1. 1.Laboratory for PhysiologyCatholic University of LeuvenLeuvenBelgium
  2. 2.The Babraham Institute Laboratory of Molecular Signaling, Department of ZoologyCambridge UniversityCambridgeUK

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