The versatility and universality of calcium signalling

Nature Reviews Molecular Cell Biology - Tập 1 Số 1 - Trang 11-21 - 2000
Michael J. Berridge1, Peter Lipp1, Martin D. Bootman1
1The Babraham Institute, Laboratory of Molecular Signalling, Babraham Hall, Babraham, UK

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Berridge, M. J. Inositol trisphosphate and calcium signalling. Nature 361, 315?325 (1993).

Clapham, D. E. Calcium signaling. Cell 80, 259? 268 (1995).

Clapper, D. L., Walseth, T. F., Dargei, P. J. & Lee, H. C. Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J. Biol. Chem. 262, 9561?9568 ( 1987).

Genazzini, A. A. & Galione, A. A. Ca2+ release mechanism gated by the novel pyridine nucleotide, NAADP. Trends Pharmacol. Sci. 18, 108?110 (1997).

Mao, C. G. et al. Molecular cloning and characterization of SCaMPER, a sphingolipid Ca2+ release-mediating protein from endoplasmic reticulum. Proc. Natl Acad. Sci. USA 93, 1993? 1996 (1996).

Cancela, J. M. & Petersen, O. H. The cyclic ADP ribose antagonist 8-NH2-cADP-ribose blocks cholecystokinin-evoked cytosolic Ca2+ spiking in pancreatic acinar cells. Pfluger's Arch. 435, 746?748 (1998).

Young, K. W., Challiss, R. A. J., Nahorski, S. R., & Mackrill, J. J. Lysophosphatidic acid-mediated Ca2+ mobilization in human SH-SY5Y neuroblastoma cells is independent of phosphoinositide signalling, but dependent on sphingosine kinase activation. Biochem. J. 343, 45?52 (1999).

Putney, J. W. Jr. A model for receptor-regulated calcium entry. Cell Calcium 7, 1?12 ( 1986).

Hofmann, T. et al. Direct activation of human TRP6 and TRPC3 channels by diacylglycerol . Nature 397, 259?263 (1999).The mammalian homologues of the Drosophila transient receptor potential (TRP) proteins function as Ca2+ channels but their control is still largely unknown. This paper suggests that some may be regulated by diacylglycerol.

Broad, L. M., Cannon, T. R. & Taylor, C. W. A non-capacitative pathway activated by arachidonic acid is the major Ca2+ entry mechanism in rat A7r5 smooth muscle cells stimulated with low concentrations of vasopressin. J. Physiol. 517, 121?134 ( 1999).

Mignen, O. & Shuttleworth, T. J. IARC, a novel arachidonate-regulated, noncapacitative Ca2+ entry channel . J. Biol. Chem. 275, 9114? 9119 (2000).

Kiselyov, K. et al. Functional interaction between InsP3 receptors and store-operated Htrp3 channels. Nature 396, 478?482 (1998).Some of the first evidence to indicate that inositol-1,4,5-trisphosphate receptors might be directly linked to Ca2+ channels in the plasma membrane.

Boulay, G. et al. Modulation of Ca2+ entry by polypeptides of the inositol 1,4,5-trisphosphate receptor (IP3R) that bind transient receptor potential (TRP): Evidence for roles of TRP and IP3R in store depletion-activated Ca2+ entry. Proc. Natl Acad. Sci. USA 96, 14955?14960 (1999).

Berridge, M. J. Capacitative calcium entry. Biochem. J. 312, 1?11 (1995).

Bootman, M. D. & Lipp, P. Calcium signalling: Ringing changes to the ?bell-shaped curve?. Curr. Biol. 9, R876?R878 ( 1999).

Mermelstein, P. G., Bito, H., Deisseroth, K. & Tsien, R. W. Critical dependence of cAMP response element-binding protein phosphorylation on L-type calcium channels support a selective response to EPSPs in preference to action potentials . J. Neurosci. 20, 266? 273 (2000).

Berridge, M. J. Neuronal calcium signaling. Neuron 21, 13?26 (1998).

Nakamura, T., Barbara, J. G., Nakamura, K. & Ross, W. N. Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials. Neuron 24, 727? 737 (1999).Direct evidence that the inositol-1,4,5-trisphosphate receptor may act as a coincident detector, integrating a Ca2+ signal coming from an action potential and inositol-1,4,5-trisphosphate generated by a metabotropic receptor.

Cancela, J. M., Churchill, G. C. & Galione, A. Coordination of agonist-induced Ca2+-signalling patterns by NAADP in pancreatic acinar cells. Nature 398, 74?76 (1999).

Fierro, L. & Llano, I. High endogenous calcium buffering in Purkinje cells from rat cerebellar slices. J. Physiol. 496, 617?625 (1996).

Pozzan, T., Rizzuto, R., Volpe, P. & Meldolesi, J. Molecular and cellular physiology of intracellular calcium stores. Physiol. Rev. 74, 595?636 ( 1994).

Blaustein, M. P. & Lederer, W. J. Sodium/calcium exchange: Its physiological implications. Physiol. Rev. 79, 763?854 (1999).

Budd, S. L. & Nicholls, D. G. A reevaluation of the role of mitochondria in neuronal Ca2+ homeostasis. J. Neurochem. 66, 403?411 ( 1996).

Jouaville, L. S., Ichas, F., Holmuhamedor, E. L., Camacho, P. & Lechleiter, J. D. Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature 377, 438?441 ( 1995).

Collins, T. J., Lipp, P., Berridge, M. J., Li, W. & Bootman, M. D. Inositol 1,4,5-trisphosphate-induced Ca2+ release is inhibited by mitochondrial depolarization. Biochem. J. 347, 593?600 (2000).

Duchen, M. R. Contributions of mitochondria to animal physiology: from homeostatic sensor to calcium signalling and cell death. J. Physiol. 516 , 1?17 (1999).

Rizzuto, R., Brini, M., Murgia, M. & Pozzan, T. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 262, 744?747 (1993).The first demonstration that mitochondria sense the high concentrations of Ca2+ that build up in the vicinity of intracellular channels such as the inositol-1,4,5-trisphosphate receptor.

Csordas, G., Thomas, A. P. & Hajnoczky, G. Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO J. 18, 96?108 (1999).

Leissring, M. A. et al. Capacitative calcium entry deficits and elevated luminal calcium content in mutant presenilin-1 knockin mice. J. Cell Biol. 149, 793?797 (2000).

Bernadi, P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev. 79, 1127? 1155 (1999).

Ichas, F., Jouaville, L. S. & Mazat, J. P. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89, 1145?1153 (1997).

Berridge, M. J. Elementary and global aspects of calcium signalling. J. Physiol. 499, 291?306 ( 1997).

Lipp, P. & Niggli, E. A hierarchical concept of cellular and subcellular Ca2+ signaling. Prog. Biophys. Mol. Biol. 65, 265?296 ( 1996).

Lipp, P. & Niggli, E. Fundamental calcium release events revealed by two-photon excitation photolysis of caged calcium in guinea-pig cardiac myocytes. J. Physiol. 508, 801? 809 (1998)

Bootman, M., Niggli, E., Berridge, M. J. & Lipp, P. Imaging the hierarchical Ca2+ signalling system in HeLa cells. J. Physiol. 499, 307?314 (1997).

Cheng, H., Lederer, W. J. & Cannell, M. B. Calcium sparks ? elementary events underlying excitation-contraction coupling in heart-muscle. Science 262, 740?744 (1993). One of the first visualizations of the localized Ca2+ signal emerging from small groups of ryanodine receptors. Such elementary events are the basic building blocks of Ca2+ signals.

Yao, Y., Coi, J. & Parker, I. Quantal puffs of intracellular Ca2+ evoked by inositol trisphosphate in Xenopus oocytes. J. Physiol. 482, 533?553 (1995).

Sun, X. -P., Callamaras, N., Marchant, J. S. & Parker, I. A continuum of InsP3-mediated elementary Ca2+ signalling events in Xenopus oocytes. J. Physiol. 509, 67?80 (1998).

Thomas, D. Lipp, P., Berridge, M. J. & Bootman, M. D. Hormone-evoked elementary Ca2+ signals are not stereotypic, but reflect activation of different size channel clusters and variable recruitment of channels within a cluster. J. Biol. Chem. 273, 27130?27136 (1998).

Lansley, A. B. & Sanderson, M. J. Regulation of airway ciliary activity by Ca2+: Simultaneous measurement of beat frequency and intracellular Ca2+. Biophys. J. 77, 629?638 ( 1999).

Robb-Gaspers, L. D. & Thomas, A. P. Coordination of Ca2+ signaling by intercellular propogation of Ca2+ waves in the intact liver. J. Biol. Chem. 270, 8102?8107 (1995). The first demonstration of intercellular Ca2+ waves travelling through large numbers of cells in an intact organ.

Zimmermann, B. & Walz, B. The mechanism mediating regenerative intercellular Ca2+ waves in the blowfly salivary gland. EMBO J. 18, 3222? 3231 (1999).

Tse, F. W. & Tse, A. Regulation of exocytosis via release of Ca2+ from intracellular stores. BioEssays 21, 861?865 (1999).

Maturana, A. D. et al. Angiotensin II negatively modulates L-type calcium channels through a pertussis toxin-sensitive G protein in adrenal glomerulosa cells . J. Biol. Chem. 274, 19943? 19948 (1999).

Lipp, P., Thomas, D., Berridge, M. J. & Bootman, M. D. Nuclear calcium signalling by individual cytoplasmic calcium puffs. EMBO J. 16, 7166?7173 ( 1997).A demonstration that Ca2+ puffs are concentrated around the nucleus and are therefore able to feed Ca2+ directly into the nucleoplasm.

DeKoninck, P. & Schulman, H. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279, 227?230 (1998).

Oancea, E. & Meyer, T. Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell 95, 307?318 (1998).

Li, W. H., Llopis, J., Whitney, M., Zlokarnik, G. & Tsien, R. Y. Cell-permeant caged InsP3 ester shows that Ca2+ spike frequency can optimize gene expression. Nature 392, 936?941 ( 1998).

Dolmetsch, R. E., Xu, K. L. & Lewis, R. S. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933? 936 (1998).

Ding, J. M. et al. A neuronal ryanodine receptor mediates light-induced phase delays of the circadian clock. Nature 394, 381?384 (1998).

Hamada, T. et al. The role of inositol trisphosphate-induced Ca2+ release from IP3-receptor in the rat suprachiasmatic nucleus on circadian entrainment mechanism. Neurosci. Lett. 263 , 125?128 (1999).

Miyazaki, S. et al. Essential role of the inositol 1,4,5-trisphosphate receptor/Ca2+ release channel in Ca2+ waves and Ca2+ oscillations at fertilization of mammalian eggs. Dev. Biol. 158, 62?78 (1993).

Jones, K. T., Matsuda, M., Parrington, J., Katan, M. & Swann, K. Different Ca2+-releasing abilities of sperm extracts compared with tissue extracts and phospholipase C isoforms in sea urchin egg homogenate, and mouse eggs. Biochem. J. 346, 743?749 ( 2000).

Swanson, C. A., Arkin, A. P. & Ross, J. An endogenous calcium oscillator may control early embryonic division. Proc. Natl Acad. Sci. USA 94, 1194?119 (1997).

Kono, T., Jones, K. T., BosMikich, A., Whittingham, D. G. & Carroll, J. A cell cycle-associated change in Ca2+ releasing activity leads to the generation of Ca2+ transients in mouse embryos during the first mitotic division . J. Cell Biol. 132, 915? 923(1996).

Chang, D. C. & Meng, C. L A localized elevation of cytosolic-free calcium is associated with cytokinesis in the zebrafish embryo. J. Cell Biol. 131, 1539?1545 (1995).

Keating, T. J., Cork, R. J. & Robinson, K. R. Intracellular free calcium oscillations in normal and cleavage-blocked embryos and artificially activated eggs of Xenopus-laevis . J. Cell Sci. 107, 2229? 2237 (1994).

Kubota, H. Y., Yoshimoto, Y. & Hiramoto, Y. Oscillation of intracellular free calcium in cleaving and cleavage-arrested embryos of Xenopus-laevis. Dev. Biol. 160, 512?518 ( 1993).

Stith, B. J., Goalstone, M., Silva, S. & Jaynes, C. Inositol 1,4,5-trisphosphate mass changes from fertilization through 1st-cleavage in Xenopus laevis . Mol. Biol. Cell 4, 435? 443 (1993).

Han, J. K. Oscillation of inositol polyphosphates in the embryonic cleavage cycle of the Xenopus laevis. Biochem. Biophys. Res. Commun. 206, 775?780 (1995).

Ciapa, B., Pesando, D., Wilding, M. & Whitaker, M. Cell-cycle calcium transients driven by cyclic changes in inositol trisphosphate levels. Nature 368, 875?878 ( 1994).Some of the first evidence that cyclic changes in inositol-1,4,5-trisphosphate and Ca2+ are responsible for controlling certain cell-cycle events, especially those occurring at mitosis.

Gilland, E., Miller, A. L., Karplus, E., Baker, R. & Webb, S. E. Imaging of multicellular large-scale rhythmic calcium waves during zebrafish gastrulation. Proc. Natl Acad. Sci. USA 96, 157?161(1999).

Webb, S. E. & Miller, A. L. Calcium signalling during zebrafish embryonic development. Bioessays 22, 113 ?123 (2000).

Creton, R., Speksnijder, J. E. & Jaffe, L. F. Patterns of free calcium in zebrafish embryos. J. Cell Sci. 111, 1613?1622 (1998).

Maslanski, J. A, Leshko, L. & Busa, W. B. Lithium-sensitive production of inositol phosphates during amphibian embryonic mesoderm induction. Science 256, 243?245(1992).

Kume, S., Muto, A., Okano, H. & Mikoshiba, K. Developmental expression of the inositol 1,4,5-trisphosphate receptor and localization of inositol 1,4,5-trisphosphate during early embryogenesis in Xenopus laevis . Mech. Dev. 66, 157?168 (1997).

Reinhard, E. et al. Localized calcium signals in early zebrafish development. Dev. Biol. 170, 50?71( 1995).

Creton, R., Kreiling, J. A. & Jaffe, L. F. Presence and roles of calcium gradients along the dorsal-ventral axis in Drosophila embryos. Dev. Biol. 217, 375?385 (2000).

K¨hl, M., Sheldahl, L. C., Malbon, C. C. & Moon, R. T. 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?12711 (2000).

Kume, S. et al. Role of inositol 1,4,5-trisphosphate receptor in ventral signaling in Xenopus embryos. Science 278, 1940?1943 (1997). A role for Ca2+ in setting up the dorsoventral axis in Xenopus oocytes was demonstrated by showing that the axis was modified by inhibiting the activity of the inositol-1,4,5-trisphosphate receptor.

Buonanno, A. & Fields, R. D. Gene regulation by patterned electrical activity during neural and skeletal muscle development. Curr. Opin. Neurobiol. 9, 110?120 ( 1999).

Ferrari, M. B., Ribbeck, K., Hagler, D. J. & Spitzer, N. C. A calcium signaling cascade essential for myosin thick filament assembly in Xenopus myocytes. J. Cell Biol. 141, 1349 ?1356 (1998).

Gu, X. N. & Spitzer, N. C. Breaking the code: Regulation of neuronal differentiation by spontaneous calcium transients. Dev. Neurosci. 19, 33?41(1997).

Carey, M. B. & Matsumoto, S. G. Spontaneous calcium transients are required for neuronal differentiation of murine neural crest. Dev. Biol. 215, 298?313 (1999).

Gomez, T. M. & Spitzer, N. C. In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature 397, 350?355( 1999).By studying Ca2+ signals in individual neurons growing in vivo , it was possible to show that brief Ca2+ transients function both in the extension of the axon and in its ability to locate its target.

Wong, R. O. L. Retinal waves and visual system development. Annu. Rev. Neurosci. 22, 29?47 ( 1999).

Lu, K. P. & Means, A. R. Regulation of the cell-cycle by calcium and calmodulin. Endocrine Rev. 14, 40?58 (1993).

Berridge, M. J. Calcium signalling and cell-proliferation. Bioessays 17, 491?500 (1995).

Monks, C. R. F., Freiberg, B. A., Kupfer, H., Sciaky, N. & Kupfer, A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82?86 (1998).

Akagi, K., Nagao, T. & Urushidani, T. Correlation between Ca2+ oscillation and cell proliferation via CCKB/gastrin receptor. Biochim. Biophys. Acta 1452, 243?253 (1999).

Scharenberg, A. M. & Kinet, J. P. Ptdlns-3,4,5-P 3: A regulatory nexus between tyrosine kinases and sustained calcium signals. Cell 94, 5?8 (1998).

Lewis, R. S. & Cahalan, M. D. Potassium and calcium channels in lymphocytes. Annu. Rev. Immunol. 13, 623?653 (1995).

Hoth, M., Fanger, C. M. & Lewis, R. S. Mitochondrial regulation of store-operated calcium signalling in T lymphocytes. J. Cell Biol. 137, 633?648 (1997).

Crabtree, G. R. Generic signals and specific outcomes: Signaling through Ca2+, calcineurin, and NF-AT. Cell 96, 611? 614 (1999).

Timmerman, L. A., Clipstone, N. A., Ho, S. N., Northrop, J. P. & Crabtree, G. R. Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature 383, 837?840 ( 1996).

Chawla, S., Hardingham, G. E., Quinn, D. R. & Bading, H. CBP: A signal-regulated transcriptional coactivator controlled by nuclear calcium and CaM kinase IV. Science 281, 1505?1509 (1998).

Hardingham, G. E., Chawla, S., Cruzalegui, F. H. & Bading, H. Control of recruitment and transcription?activating function of CBP determines gene regulation by NMDA receptors and L-type calcium channels. Neuron 22, 789?798 ( 1999).

Wang, J. H., Moreira, K. M., Campos, B., Kaetzel, M. A. & Dedman, J. R. Targeted neutralization of calmodulin in the nucleus blocks DNA synthesis and cell cycle progression. Biochim. Biophys. Acta 1313, 223?228 (1996).

Yang, H., Shen, F., Herenyiova, M. & Weber, G. Phospholipase C (EC 3. 1. 4. 11): A malignancy linked signal transduction enzyme. Anticancer Res. 18, 1399?1404 (1998).

Smith, M. R. et al. Overexpression of phosphoinositide-specific phospholipase C γ in NIH 3T3 cells promotes transformation and tumorigenicity. Carcinogenesis 19, 177?185 (1998).

Rizzo, M. T. & Weber, G. L. Phosphatidylinositol 4-kinase ? an enzyme linked with proliferation and malignancy. Cancer Res. 54, 2611?2614 ( 1994).

Benzaquen, L. R., Brugnara, C., Byers, H. R., Gattoni-Celli, S. & Halperin, J. A. Clotrimazole inhibits cell proliferation in vitro and in vivo. Nature Med. 1, 534?540 (1995).

Nie, L., Mogami, H., Kanzaki, M., Shibata, H. & Kojima, I. Blockade of DNA synthesis induced by platelet-derived growth factor by tranilast, an inhibitor of Ca2+ entry, in vascular smooth muscle cells. Mol. Pharm. 50, 763?769 (1996).

Haverstick, D. M., Heady, T. N., Macdonald, T. L. & Gray, L. S. Inhibition of human prostate cancer proliferation in vitro and in a mouse model by a compound synthesized to block Ca2+ entry. Cancer Res. 60, 1002?1008 (2000).

Kohn, E. C. et al. Clinical investigation of a cytostatic calcium influx inhibitor in patients with refractory cancers. Cancer Res. 56 , 569?573 (1996).

Gao, B. et al. Functional properties of a new voltage-dependent calcium channel α 2δ auxiliary subunit gene (CACNA2D2). J. Biol. Chem. 275, 12237?12242 ( 2000).One of the first indications that malignancy might be linked to an alteration in Ca2+ signalling.

Kass, G. E. N. & Orrenius, S. Calcium signaling and cytotoxicity. Environ. Health Perspect. 107, 25?35 (1999).

Szalai, G., Krishnamurthy, R. & Hajnoczky, G. Apoptosis driven by IP3-linked mitochondrial calcium signals. EMBO J. 18, 6349? 6361 (1999).

Shimizu, S., Narita, M. & Tsujimoto, Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399, 483?487 (1999).

Barr, P. J. & Tomei, L. D. Apoptosis and its role in human disease. Biotechnology 12, 487? 493 (1994).

Reed, J. C. Bcl-2 and the regulation of programmed cell-death. J. Cell Biol. 124, 1?6 (1994 ).

Murphy, A., Bredesen, D. E., Cortopassi, G., Wang, E. & Fiskum, G. Bcl-2 potentiates the maximal calcium uptake capacity of neural cell mitochondria. Proc. Natl Acad. Sci. USA 93, 9893?9898 ( 1996).

Vander Heiden, M., Chandel, N. S., Williamson, E. K., Schumacker, P. T. & Thompson, C. B. Bcl-x L regulates the membrane potential and volume homeostasis of mitochondria . Cell 91, 627?637 (1997).

Zhu, L. P. et al. Modulation of mitochondrial Ca2+ homeostasis by Bcl-2. J. Biol. Chem. 274, 33267? 33273 (1999).Evidence that mitochondrial metabolism can be modulated by the anti-apoptotic modulator Bcl-2.

Kuo, T. H. et al. Modulation of endoplasmic reticulum calcium pump by Bcl-2 . Oncogene 17, 1903?1910 (1998).

Foyouzi-Youssefi, R. et al. Bcl-2 decreases the free Ca2+ concentration within the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 97, 5723?5728 (2000)

Pinton, P. et al. Reduced loading on intracellular Ca2+ stores and downregulation of capacitative Ca2+ influx in Bcl-2-overexpressing cells. J. Biol. Chem. 275, 857? 862 (2000).

Schlossmann, J. et al. Regulation of intracellular calcium by a signalling complex of IRAG, IP3 receptor and cGMP kinase Iβ. Nature 404, 197?201 ( 2000).

Morimoto, A. M. et al. The MMAC1 tumor suppressor phosphatase inhibits phospholipase C and integrin-linked kinase-activity. Oncogene 19, 200?209 (2000).

Lev, S. et al. Protein-tyrosine kinase PYK2 involved in Ca2+-induced regulation of ion-channel and map kinase functions. Nature 376, 737?745 (1995).

Brinson, A. E. et al. Regulation of a calcium-dependent tyrosine kinase in vascular smooth muscle cells by angiotensin II and platelet-derived growth factor. Dependence on calcium and the actin cytoskeleton. J. Biol. Chem. 273, 1711?1718 ( 1998).

Prenzel, N. et al. EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinases of proHB?EGF. Nature 402, 884?888 (1999).