Regenerative release of calcium from functionally discrete subcellular stores by inositol trisphosphate

Fluorescence imaging was used to determine the spatial and temporal patterns of subcellular calcium (Ca2+) liberation induced in Xenopus oocytes by photorelease of inositol 1,4,5-trisphosphate (InsP3) from a caged precursor. Increasing levels of InsP3 evoked Ca2+ release that began in a graded m anner but, at varying threshold levels of Ins-P3, localized sites then showed transient and asynchronous ‘puffs’ of Ca2+ release. With higher levels of Ins.P3, Ca2+ from adjacent sites formed a focus for initiation of a propagating Ca2+ wave. The results show that Ins.P3-sensitive Ca2+ stores are arranged as distinct and functionally independent units, and that Ca2+ is released in both graded and regenerative fashions.

[1]  Taenia Caeci.  Biphasic Ca 2+ Dependence of Inositol 1,4,5-Trisphosphate-induced Ca Release in Smooth Muscle Cells of the Guinea Pig , 1990 .

[2]  A Goldbeter,et al.  Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[3]  S. Delisle.  The four dimensions of calcium signalling in Xenopus oocytes. , 1991, Cell calcium.

[4]  S. Miyazaki.  Inositol 1,4,5-trisphosphate-induced calcium release and guanine nucleotide-binding protein-mediated periodic calcium rises in golden hamster eggs , 1988, The Journal of cell biology.

[5]  A. Peres.  InsP3‐ and Ca2+‐induced Ca2+ release in single mouse oocytes , 1990, FEBS letters.

[6]  I. Parker,et al.  Caffeine inhibits inositol trisphosphate‐mediated liberation of intracellular calcium in Xenopus oocytes. , 1991, The Journal of physiology.

[7]  R. Miledi,et al.  Nonlinearity and facilitation in phosphoinositide signaling studied by the use of caged inositol trisphosphate in Xenopus oocytes , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  M. Berridge,et al.  Spatial and temporal aspects of cell signalling. , 1988, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  M. Berridge.  Caffeine inhibits inositol-trisphosphate-induced membrane potential oscillations in Xenopus oocytes , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  R Y Tsien,et al.  Generation of calcium oscillations in fibroblasts by positive feedback between calcium and IP3. , 1991, Science.

[11]  James Watras,et al.  Bell-shaped calcium-response curves of lns(l,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum , 1991, Nature.

[12]  T. Meyer.  Cell signalling by second messenger waves , 1991, Cell.

[13]  T. Cheek.  Spatial aspects of calcium signalling. , 1989, Journal of cell science.

[14]  D. Trentham,et al.  Properties and Uses of Photoreactive Caged Compounds , 1989 .

[15]  T. Bolton,et al.  Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. , 1986, The Journal of physiology.

[16]  Y. Hiramoto,et al.  Free calcium wave upon activation in Xenopus eggs. , 1987, Developmental biology.

[17]  M. Berridge,et al.  Localization and heterogeneity of agonist‐induced changes in cytosolic calcium concentration in single bovine adrenal chromaffin cells from video imaging of fura‐2. , 1989, The EMBO journal.

[18]  R. Miledi,et al.  Cholinergic and catecholaminergic receptors in the Xenopus oocyte membrane , 1982, The Journal of physiology.

[19]  R. Tsien,et al.  Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. , 1989, The Journal of biological chemistry.

[20]  C. Wahlestedt,et al.  Calcium wave evoked by activation of endogenous or exogenously expressed receptors in Xenopus oocytes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Clapham,et al.  Spiral calcium wave propagation and annihilation in Xenopus laevis oocytes. , 1991, Science.

[22]  S. Muallem,et al.  Hormone-evoked calcium release from intracellular stores is a quantal process. , 1989, The Journal of biological chemistry.

[23]  L. Stryer,et al.  Kinetics of calcium channel opening by inositol 1,4,5-trisphosphate. , 1990, Biochemistry.

[24]  L. Stryer,et al.  Highly cooperative opening of calcium channels by inositol 1,4,5-trisphosphate. , 1988, Science.

[25]  R. Miledi,et al.  Chloride current induced by injection of calcium into Xenopus oocytes. , 1984, The Journal of physiology.

[26]  M. Berridge.  Inositol trisphosphate‐induced membrane potential oscillations in Xenopus oocytes. , 1988, The Journal of physiology.

[27]  A. Dawson,et al.  Quantal release of Ca2+ from intracellular stores by InsP3: tests of the concept of control of Ca2+ release by intraluminal Ca2+ , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  M. Berridge,et al.  Spontaneous calcium release from inositol trisphosphate-sensitive calcium stores , 1991, Nature.

[29]  R. Nuccitelli,et al.  An elevated free cytosolic Ca2+ wave follows fertilization in eggs of the frog, Xenopus laevis , 1985, The Journal of cell biology.

[30]  R. Irvine.  ‘Quanta’ Ca2+ release and the control of Ca2+ entry by inositol phosphates ‐ a possible mechanism , 1990, FEBS letters.

[31]  C. Taylor,et al.  The size of inositol 1,4,5-trisphosphate-sensitive Ca2+ stores depends on inositol 1,4,5-trisphosphate concentration. , 1990, The Biochemical journal.

[32]  I. Parker,et al.  Localized all-or-none calcium liberation by inositol trisphosphate. , 1990, Science.

[33]  S. M. Goldin,et al.  Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. , 1991, Science.

[34]  Michael J. Berridge,et al.  Inositol phosphates and cell signalling , 1989, Nature.

[35]  L. Stryer,et al.  Transient calcium release induced by successive increments of inositol 1,4,5-trisphosphate. , 1990, Proceedings of the National Academy of Sciences of the United States of America.