1932

Abstract

▪ Abstract 

My scientific life has been spent trying to understand how cells communicate with each other. This interest in cell signaling began with studies on the control of fluid secretion by an insect salivary gland, and the subsequent quest led to the discovery of inositol trisphosphate (IP) and its role in calcium signaling, which effectively divided my scientific career into two distinct parts. The first part was primarily experimental and culminated in the discovery of IP, which set the agenda for the second half during which I have enjoyed exploring the many functions of this remarkably versatile signaling system. It has been particularly exciting to find out how this IP/Ca2+ signaling pathway has been adapted to control processes as diverse as fertilization, proliferation, cell contraction, secretion, and information processing in neuronal cells.

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2005-03-17
2024-05-16
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Literature Cited

  1. Berridge MJ. 1965. The physiology of excretion in the cotton stainer Dysdercus fasciatus Signoret. III. Nitrogen excretion and ionic regulation J. Exp. Biol. 43:535–52 [Google Scholar]
  2. Ramsay JA. 1954. Active transport of water by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. Exp. Biol. 31:104–13 [Google Scholar]
  3. Berridge MJ, Patel NG. 1968. Insect salivary glands: stimulation of fluid secretion by 5-hydroxytryptamine and cyclic AMP. Science 162:462–63 [Google Scholar]
  4. Sutherland EW, Rall TW. 1958. Fractionation and characterization of a cyclic adenine ribonucleotide formed by tissue particles. J. Biol. Chem. 232:1077–91 [Google Scholar]
  5. Berridge MJ. 1970. The role of 5-hydro-xytryptamine and cyclic 3′,5′-adenosine monophosphate in the control of fluid secretion by isolated salivary glands. J. Exp. Biol. 53:171–86 [Google Scholar]
  6. Berridge MJ, Prince WT. 1972. Transepithelial potential changes during stimulation of isolated salivary glands with 5-hydroxytryptamine and cyclic AMP. J. Exp. Biol. 56:139–53 [Google Scholar]
  7. Berridge MJ, Lindley BD, Prince WT. 1976. Studies on the mechanism of fluid secretion by isolated salivary glands of Calliphora. J. Exp. Biol. 64:311–22 [Google Scholar]
  8. Douglas WW, Poisner AM. 1963. The influence of calcium on the secretory response of the submaxillary gland to acetylcholine or to noradrenaline. J. Physiol. 165:528–41 [Google Scholar]
  9. Rasmussen H. 1970. Cell communication, calcium ion and adenosine monophosphate. Science 170:404–12 [Google Scholar]
  10. Prince WT, Berridge MJ, Rasmussen H. 1972. Role of calcium and adenosine-3′5′-cyclic monophosphate in controlling fly salivary gland secretion. Proc. Natl. Acad. Sci. USA 69:553–57 [Google Scholar]
  11. Prince WT, Berridge MJ. 1973. The role of calcium in the action of 5-hydroxy-tryptamine and cyclic AMP on salivary glands. J. Exp. Biol. 58:367–84 [Google Scholar]
  12. Berridge MJ. 1981. Electrophysiological evidence for the existence of separate receptor mechanisms mediating the action of 5-hydroxytryptamine. Mol. Cell Endocrin. 23:91–104 [Google Scholar]
  13. Berridge MJ, Heslop JP. 1981. Separate 5-hydroxytryptamine receptors on the salivary gland of the blowfly are linked to the generation of either cyclic adenosine 3′,5′-mono-phosphate or calcium signals. Br. J. Pharmacol. 7:729–38 [Google Scholar]
  14. Hokin MR, Hokin LE. 1953. Enzyme secretion and the incorporation of 32P into phospholipids of pancreas slices. J. Biol. Chem. 203:967–77 [Google Scholar]
  15. Michell RH. 1975. Inositol phospholipids and cell surface receptor function. Biochim. Biophys. Acta 415:81–147 [Google Scholar]
  16. Fain JN, Berridge MJ. 1979. Relationship between hormonal activation of phosphatidylinositol hydrolysis, fluid secretion and calcium flux in the blowfly salivary gland. Biochem. J. 178:45–58 [Google Scholar]
  17. Berridge MJ. 1980. Preliminary measurements of intracellular calcium in an insect salivary gland using a calcium-sensitive microelectrode. Cell Calcium 1:217–27 [Google Scholar]
  18. Berridge MJ, Lipke H. 1979. Changes in calcium transport across Calliphora salivary glands induced by 5-hydroxytryptamine and cyclic nucleotides. J. Exp. Biol. 78:137–48 [Google Scholar]
  19. Berridge MJ, Fain JN. 1979. Inhibition of phosphatidylinositol synthesis and the inactivation of calcium entry after prolonged exposure of the blowfly salivary gland to 5-hydroxytryptamine. Biochem. J. 178:56–68 [Google Scholar]
  20. Fain JN, Berridge MJ. 1979. Relationship between phosphatidylinositol synthesis and recovery of 5-hydroxytryptamine responsive Ca2+ flux in blowfly salivary gland. Biochem. J. 180:655–61 [Google Scholar]
  21. Allison JH, Stewart MA. 1971. Reduced brain inositol in lithium-treated rats. Nature 233:267–68 [Google Scholar]
  22. Allison JH, Blisner ME, Holland WH, Hipps PP, Sherman WR. 1976. Increased brain myo-inositol in lithium-treated rats. Biochem. Biophys. Res. Commun. 71:664–70 [Google Scholar]
  23. Berridge MJ, Downes CP, Hanley MR. 1989. Neural and developmental actions of lithium: a unifying hypothesis. Cell 59:411–19 [Google Scholar]
  24. Berridge MJ, Downes CP, Hanley MR. 1982. Lithium amplifies agonist-dependent phosphatidylinositol responses in brain and salivary glands. Biochem. J. 206:587–95 [Google Scholar]
  25. Berridge MJ, Dawson RMC, Downes CP, Heslop JP, Irvine RF. 1983. Changes in the levels of inositol phosphates after agonist-dependent hydrolysis of membrane phosphoinositides. Biochem. J. 212:473–82 [Google Scholar]
  26. Akhtar RA, Abdel-Latif AA. 1980. Requirement for calcium ions in acetylcholine-stimulated phosphodiesteratic cleavage of phosphatidyl-myo-inositol 4,5-bisphosphate in rabbit iris smooth muscle. Biochem. J. 192:783–91 [Google Scholar]
  27. Michell RH, Kirk CJ, Jones LM, Downes CP, Creba JA. 1981. The stimulation of inositol lipid metabolism that accompanies calcium mobilization in stimulated cells: defined characteristics and unanswered questions. Philos. Trans. R. Soc. London Ser. B 296:123–37 [Google Scholar]
  28. Berridge MJ, Buchan PB, Heslop JP. 1984. Relationship of polyphosphoinositide metabolism to the hormonal activation of the insect salivary gland to 5-hydroxytryptamine. Mol. Cell Endocrinol. 36:37–42 [Google Scholar]
  29. Berridge MJ. 1983. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem. J. 212:849–58 [Google Scholar]
  30. Streb H, Irvine RF, Berridge MJ, Schulz I. 1983. Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol 1,4,5-trisphosphate. Nature 306:67–69 [Google Scholar]
  31. Burgess GM, Godfrey PP, McKinney JS, Berridge MJ, Irvine RF, Putney JW Jr.. 1984. The second messenger linking receptor activation to internal calcium release in liver. Nature 309:63–66 [Google Scholar]
  32. Berridge MJ, Heslop JP, Irvine RF, Brown KD. 1984. Inositol trisphosphate formation and calcium mobilization in Swiss 3T3 cells in response to platelet-derived growth factor. Biochem. J. 222:195–201 [Google Scholar]
  33. Prentki M, Biden TJ, Janjic D, Irvine RF, Berridge MJ, Wollheim CB. 1984. Rapid mobilization of Ca2+ from rat insulinoma microsomes by inositol 1,4,5-trisphosphate. Nature 309:562–64 [Google Scholar]
  34. Biden TJ, Prentki M, Irvine RF, Berridge MJ, Wollheim CB. 1984. Inositol 1,4,5-trisphosphate mobilizes intracellular Ca2+ from permeabilized insulin-secreting cells. Biochem. J. 223:467–73 [Google Scholar]
  35. Fein A, Payne R, Corson DW, Berridge MJ, Irvine RF. 1984. Photoreceptor excitation and adaption by inositol 1,4,5-trisphosphate. Nature 311:157–60 [Google Scholar]
  36. Brown JE, Rubin LJ, Ghalayini AJ, Tarver AP, Irvine RF. et al. 1984. A biochemical and electrophysiological examination of myo-inositol polyphosphate as a putative messenger for excitation in Limulus ventral photoreceptor cells. Nature 311:160–63 [Google Scholar]
  37. Burgess GM, McKinney JS, Irvine RF, Berridge MJ, Hoyle PC, Puntey JW Jr.. 1984. Inositol 1,4,5-trisphosphate may be a signal for f-Met-leu-Phe-induced intracellular calcium mobilization in human leukocytes (HL-60 cells). FEBS Lett. 176:193–96 [Google Scholar]
  38. Takai Y, Kishimoto A, Kikkawa U, Mori T, Nishizuka Y. 1979. Unsaturated diacylglycerol as a possible messenger for the activation of a calcium-activated, phospholipid-dependent protein kinase system. Biochem. Biophys. Res. Commun. 91:1218–24 [Google Scholar]
  39. Nishizuka Y. 1984. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308:693–98 [Google Scholar]
  40. Berridge MJ. 1984. Inositol trisphosphate and diacylglycerol as second messengers. Biochem. J. 220:345–60 [Google Scholar]
  41. Berridge MJ, Irvine RF. 1984. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312:315–21 [Google Scholar]
  42. Berridge MJ. 1993. Inositol trisphosphate and calcium signalling. Nature 361:315–25 [Google Scholar]
  43. Bootman MD, Berridge MJ. 1995. The elemental principles of calcium signalling. Cell 83:675–78 [Google Scholar]
  44. Berridge MJ. 1997. Elementary and global aspects of calcium signalling. J. Physiol. 499:291–306 [Google Scholar]
  45. Berridge MJ, Lipp P, Bootman MD. 2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1:11–21 [Google Scholar]
  46. Galione AG, Berridge MJ. 1988. Pharmacological modulation of oscillations in the blowfly salivary gland. Biochem. Soc. Trans. 16:988–90 [Google Scholar]
  47. Rapp PE, Berridge MJ. 1981. The control of transepithelial potential oscillations in the salivary gland of Calliphora erythrocephala. J. Exp. Biol. 93:119–32 [Google Scholar]
  48. Rapp PE, Berridge MJ. 1977. Oscillations in calcium-cyclic AMP control loops from the basis of pacemaker activity and other high frequency biological rhythms. J. Theor. Biol. 66:497–525 [Google Scholar]
  49. Woods NM, Cuthbertson KSR, Cobbold PH. 1986. Repetitive transient rises in cytoplasmic free calcium in hormone-stimulated hepatocytes. Nature 319:6002 [Google Scholar]
  50. Cuthbertson KSR, Cobbold PH. 1985. Phorbol ester and sperm activate mouse oocytes by inducing sustained oscillations in cell Ca2+. Nature 316:541–42 [Google Scholar]
  51. Miyazaki S-I, Hashimoto N, Yoshimoto Y, Kishimoto T. et al. 1986. Temporal and spatial dynamics of the periodic increase in intracellular free calcium at fertilization of golden hamster eggs. Dev. Biol. 118:259–67 [Google Scholar]
  52. Cheek TR, McGuinness OM, Vincent C, Moreton RB, Berridge MJ, Johnson MH. 1993. Fertilisation and thimerosal stimulate similar calcium spiking patterns in mouse oocytes but by separate mechanisms. Development 119:179–89 [Google Scholar]
  53. Goldbeter A, Dupont G, Berridge MJ. 1990. Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation. Proc. Natl. Acad. Sci. USA 87:1461–65 [Google Scholar]
  54. Dupont G, Berridge MJ, Goldbeter A. 1991. Signal-induced Ca2+ oscillations: properties of a model based on Ca2+-induced Ca2+ release. Cell Calcium 12:73–85 [Google Scholar]
  55. Endo M, Tanaka M, Ogawa Y. 1970. Calcium induced calcium release of calcium from the endoplasmic reticulum of skinned skeletal muscle fibres. Nature 228:34–36 [Google Scholar]
  56. Iino M. 1990. Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate Ca release in smooth muscle cells of the guinea pig Taenia caeci. J. Gen. Physiol. 95:1103–22 [Google Scholar]
  57. Bezprozvanny I, Watras J, Ehrlich BE. 1991. Bell-shaped calcium response curves of Ins(1,4,5)P3- and calcium gated channels from endoplasmic reticulum of cerebellum. Nature 351:751–54 [Google Scholar]
  58. Finch EA, Turner TJ, Goldin SM. 1991. Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 252:443–46 [Google Scholar]
  59. Missiaen L, Taylor CW, Berridge MJ. 1991. Spontaneous calcium release from inositol trisphosphate-sensitive calcium stores. Nature 352:241–44 [Google Scholar]
  60. Berridge MJ, Dupont G. 1994. Spatial and temporal signalling by calcium. Curr. Opin. Cell Biol. 6:267–74 [Google Scholar]
  61. Cheek TR, O'Sullivan AJ, Moreton RB, Berridge MJ, Burgoyne RD. 1989. Spatial localization of the stimulus-induced rise in cytosolic Ca2+ in bovine adrenal chromaffin cells: distinct nicotinic and muscarinic patterns. FEBS Lett. 247:429–34 [Google Scholar]
  62. Cheng H, Lederer WJ, Cannell MB. 1993. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262:740–44 [Google Scholar]
  63. Lipp P, Niggli E. 1994. Modulation of Ca2+ release in cultured neonatal rat cardiac myocytes—insight from subcellular release patterns revealed by confocal microscopy. Circ. Res. 74:979–90 [Google Scholar]
  64. Bootman MD, Berridge MJ. 1996. Sub-cellular Ca2+ signals underlying waves and graded responses in HeLa cells. Curr. Biol. 6:855–65 [Google Scholar]
  65. Yao Y, Choi J, Parker I. 1995. Quantal puffs of intracellular Ca2+ evoked by inositol trisphosphate in Xenopus oocytes. J. Physiol. 482:533–53 [Google Scholar]
  66. Bootman MD, Niggli E, Berridge MJ, Lipp P. 1997. Imaging the hierarchical Ca2+ signalling system in HeLa cells. J. Physiol. 499:307–14 [Google Scholar]
  67. Bootman MD, Berridge MJ, Lipp P. 1997. Cooking with calcium: the recipes for composing global signals from elementary events. Cell 91:367–73 [Google Scholar]
  68. Lechleiter JD, Clapham DE. 1992. Molecular mechanisms of intracellular calcium excitability in X. laevis oocytes. Cell 68:283–94 [Google Scholar]
  69. Williams RSB, Cheng L, Mudge AW, Harwood AJ. 2002. A common mechanism of action for three mood-stabilizing drugs. Nature 417:292–95 [Google Scholar]
  70. Kume S, Muto A, Inoue T, Suga K, Okano H. et al. 1997. Role of inositol 1,4,5-trisphosphate receptor in ventral signalling in Xenopus embryos. Science 278:194043 [Google Scholar]
  71. Kühl M, Sheldahl LC, Malbon CC, Moon RT. 2000. Ca2+/calmodulin-dependent protein kinase II is stimulated by Wnt and frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 275:12701–11 [Google Scholar]
  72. Sharp AH, McPherson PJ, Dawson TM, Aoki C, Campbell KP, Synder SH. 1993. Differential immunohistochemical localization of inositol 1,4,5-trisphosphate- and ryanodine-sensitive Ca2+ release channels in rat brain. J. Neurosci. 13:3051–63 [Google Scholar]
  73. Berridge MJ. 1998. Neural calcium signalling. Neuron 21:13–26 [Google Scholar]
  74. Berridge MJ. 1993. A tale of two messengers. Nature 365:388–89 [Google Scholar]
  75. Wang SSH, Denk W, Häusser M. 2000. Coincident detection in single dendritic spines mediated by calcium release. Nat. Neurosci. 3:1266–73 [Google Scholar]
  76. Nishiyama M, Hong K, Mikoshiba K, Poo M-M. 2000. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 408:584–88 [Google Scholar]
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