Advertisement

Separate but Interacting Calcium Stores

Chapter

Abstract

Mobilization of intracellular Ca2+ stores is a principal signaling mechanism employed by cells to respond to a wide variety of stimuli, both external and internal. One of the most dramatic examples occurs during fertilization. Immediately after sperm-egg fusion, a highly localized Ca2+ elevation is initiated right at the fusion site. This spark of Ca2+ then grows into a wave propagating across the entire egg. Intriguingly, the initiation of apoptotic cell death also involves Ca2+ mobilization. How cells can differentiate between Ca2+ signals as disparate as those governing life and death is a question of fundamental importance.

Keywords

Ryanodine Receptor Pancreatic Acinar Cell Calcium Store Basolateral Side 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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Streb H, Irvine RF, Berridge MJ and 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.PubMedCrossRefGoogle Scholar
  2. 2.
    Berridge MJ. 1983. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem. J. 212: 849–858.PubMedGoogle Scholar
  3. 3.
    Clapper DL, Walseth TF, Dargie PJ and Lee HC. 1987. Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J. Biol. Chem. 262: 9561–9568.PubMedGoogle Scholar
  4. 4.
    Lee HC, Walseth TF, Bratt GT, Hayes RN and Clapper DL. 1989. Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2+-mobilizing activity. J. Biol. Chem. 264: 1608–1615.PubMedGoogle Scholar
  5. 5.
    Lee HC and Aarhus R. 1995. A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP-ribose. J. Biol. Chem. 270: 2152–2157.PubMedCrossRefGoogle Scholar
  6. 6.
    Lee HC. 1997. Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol. Rev. 11: 1133–1164.Google Scholar
  7. 7.
    Lee HC. 2001. Physiological functions of cyclic ADP-ribose and NAADP as calcium messengers. Ann. Rev. Pharmacol. Toxicol. 41: 317–345.CrossRefGoogle Scholar
  8. 8.
    Zocchi E, Carpaneto A, Cerrano C, Bavestrello G, Giovine M, Bruzzone S, Guida L, Franco L and Usai C. 2002. The temperature-signaling cascade in sponges involves a heat-gated cation channel, abscisic acid, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 98: 14859–14864.CrossRefGoogle Scholar
  9. 9.
    Masuda W, Takenaka S, Inageda K, Nishina H, Takahashi K, Katada T, Tsuyama S, Inui H, Miyatake K and Nakano Y. 1997. Oscillation of ADP-ribosyl cyclase activity during the cell cycle and function of cyclic ADP-ribose in a unicellular organism, Euglena Gracilis. FEBS Lett. 405: 104–106.PubMedCrossRefGoogle Scholar
  10. 10.
    Zocchi E, Daga A, Usai C, Franco L, Guida L, Bruzzone S, Costa A, Marchetti C and Deflora A. 1998. Expression of CD38 increases intracellular calcium concentration and reduces doubling time in HeLa and 3T3 cells. J. Biol. Chem. 273: 8017–8024.PubMedCrossRefGoogle Scholar
  11. 11.
    Franco L, Zocchi E, Usai C, Guida L, Bruzzone S, Costa A and De Flora A. 2001. Paracrine roles of NAD+ and cyclic ADP-ribose in increasing intracellular calcium and enhancing cell proliferation of 3T3 fibroblasts. J. Biol. Chem. 276: 21642–21648.PubMedGoogle Scholar
  12. 12.
    Dargie PJ, Agre MC and Lee HC. 1990. Comparison of Ca2+ mobilizing activities of cyclic ADP-ribose and inositol trisphosphate. Cell Regul. 1: 279–290.PubMedGoogle Scholar
  13. 13.
    Kuroda R, Kontani K, Kanda Y, Katada T, Nakano T, Satoh Y-I, Suzuki N and Kuroda H. 2001. Increase of cGMP, cADP-ribose and inositol 1,4,5-trisphosphate preceding Ca2+ transients in fertilization of sea urchin eggs. Development 128: 4405–4414.PubMedGoogle Scholar
  14. 14.
    Lee HC. 1996. Cyclic ADP-ribose and calcium signaling in eggs. Biol. Signals 5: 101–110.PubMedCrossRefGoogle Scholar
  15. 15.
    Okamoto H. 1999. The CD38-cyclic ADP-ribose signaling system in insulin secretion. Mol. Cell. Biochem. 193: 115–118.PubMedCrossRefGoogle Scholar
  16. 16.
    Lino S, Cui Y, Galione A and Terrar DA. 1997. Actions of cADP-ribose and its antagonists on contraction in guinea pig isolated ventricular myocytes - Influence of temperature. Circ. Res. 81: 879–884.PubMedCrossRefGoogle Scholar
  17. 17.
    Partida-Sanchez S, Cockayne D, Monard S, Jacobson EL, Oppenheimer N, Garvy B, Kusser K, Goodricj S, Howard M, Harmsen A, Randall T and Lund FE. 2001. Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nature Med. 7: 1209–1216.PubMedCrossRefGoogle Scholar
  18. 18.
    Reyes-Harde M, Empson R, Potter BVL, Galione A and Stanton PK. 1999. Evidence of a role for cyclic ADP-ribose in long-term synaptic depression in hippocampus. Proc. Natl. Acad. Sci. USA 96: 4061–4066.PubMedCrossRefGoogle Scholar
  19. 19.
    Reyes-Harde M, Potter BVL, Galione A and Stanton PK. 1999. Induction of hippocampal LTD requires nitric-oxide-stimulated PKG activity and Ca2+ release from cyclic ADP-ribose-sensitive stores. J. Neurophysioi 82: 1569–1576.Google Scholar
  20. 20.
    Podesta M, Zocchi E, Pitto A, Usai C, Franco L, Bruzzone S, Guida L, Bacigalupo A, Scadden DT, Walseth TF, De Flora A and Daga A. 2000. Extracellular cyclic ADP-ribose increases intracellular free calcium concentration and stimulates proliferation of human hemopoietic progenitors. FASEB J. 14: 680–690.PubMedGoogle Scholar
  21. 21.
    Zocchi E, Podesta M, Pitto A, Usai C, Bruzzone S, Franco L, Guida L, Bacigalupo A and De Flora A. 2001. Paracrinally stimulated expansion of early human hemopoietic progenitors by stroma-generated cyclic ADP-ribose. FASEB J. 15: 1610–1612.PubMedGoogle Scholar
  22. 22.
    Walseth TF and Lee HC. 1993. Synthesis and characterization of antagonists of cyclic-ADP-ribose-induced Ca2+ release. Biochim. Biophys. Acta 1178: 235–242.PubMedCrossRefGoogle Scholar
  23. 23.
    Sethi JK, Empson RM, Bailey VC, Potter BVL and Galione A. 1997. 7-Deaza-8-bromo-cyclic ADP-ribose, the first membrane-permeant, hydrolysis-resistant cyclic ADP-ribose antagonist. J. Biol. Chem. 272: 16358–16363.PubMedCrossRefGoogle Scholar
  24. 24.
    Deflora A, Guida L, Franco L, Zocchi E, Pestarino M, Usai C, Marchetti C, Fedele E, Fontana G and Raiteri M. 1996. Ectocellular in vitro and in vivo metabolism of cADP-ribose in cerebellum. Biochem. J. 320: 665–671.Google Scholar
  25. 25.
    Franco L, Bruzzone S, Song P, Guida L, Zocchi E, Walseth TF, Crimi E, Usai C, De Flora A and Brusasco V. 2001. Extracellular cyclic ADP-ribose potentiates ACh-induced contraction in bovine tracheal smooth muscle. Am. J. Physiol. 280: L98–L106.Google Scholar
  26. 26.
    Fukushi Y, Kato I, Takasawa S, Sasaki T, Ong BH, Sato M, Ohsaga A, Sato K, Shirato K, Okamoto H and Maruyama Y. 2001. Identification of cyclic ADP-ribose-dependent mechanisms in pancreatic muscarinic Ca2+ signaling using CD38 knockout mice. J. Biol. Chem. 276: 649–655.PubMedCrossRefGoogle Scholar
  27. 27.
    Wu Y, Kuzma J, Marechal E, Graeff R, Lee HC, Foster R and Chua NH. 1997. Abscisic acid signaling through cyclic ADP-ribose in plants. Science 278: 2126–2130.PubMedCrossRefGoogle Scholar
  28. 28.
    Guse AH, da Silva CP, Berg I, Skapenko AL, Weber K, Heyer P, Hohenegger M, Ashamu GA, Schulze-Koops H, Potter BVL and Mayr GW. 1999. Regulation of calcium signalling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature 398: 70–73.PubMedCrossRefGoogle Scholar
  29. 29.
    Kato I, Yamamoto Y, Fujimura M, Noguchi N, Takasawa S and Okamoto H. 1998. CD38 disruption impairs glucose-induced increases in cyclic ADP-ribose, [Ca2+]i and insulin secretion. J. Biol. Chem. 274: 1869–1872.CrossRefGoogle Scholar
  30. 30.
    Takahashi K, Kukimoto I, Tokita K, Inageda K, Inoue S, Kontani K, Hoshino S, Nishina H, Kanaho Y and Katada T. 1995. Accumulation of cyclic ADP-ribose measured by a specific radioimmunoassay in differentiated human leukemic HL-60 cells with all-trans-retinoic acid. FEBS Lett. 371: 204–208.PubMedCrossRefGoogle Scholar
  31. 31.
    Polzonetti V, Cardinali M, Mosconi G, Natalini P, Meiri I and Carnevali O. 2002. Cyclic ADPR and calcium signaling in sea bream (Sparus aurata) egg fertilization. Mol. Reprod. Dev. 61:213–217.PubMedCrossRefGoogle Scholar
  32. 32.
    Masuda W, Takenaka S, Tsuyama S, Tokunaga M, Yamaji R, Inui H, Miyatake K and Nakano Y. 1997. Inositol 1,4,5-trisphosphate and cyclic ADP-ribose mobilize Ca2+ in a protist, Euglena Gracilis. Comp. Biochem. Physiol. 118: 279–283.Google Scholar
  33. 33.
    Allen GJ, Muir SR and Sanders D. 1995. Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose. Science 268: 735–737.PubMedCrossRefGoogle Scholar
  34. 34.
    Leckie CP, McAinsh MR, Allen GJ, Sanders D and Hetherington AM. 1998. Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 95: 15837–15842.PubMedCrossRefGoogle Scholar
  35. 35.
    Navazio L, Mariani P and Sanders D. 2001. Mobilization of Ca2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol. 125: 2129–2138.PubMedCrossRefGoogle Scholar
  36. 36.
    Durner J, Wendehenne D and Klessig DF. 1998. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 95: 10328–10333.PubMedCrossRefGoogle Scholar
  37. 37.
    Rusinko N and Lee HC. 1989. Widespread occurrence in animal tissues of an enzyme catalyzing the conversion of NAD+ into a cyclic metabolite with intracellular Ca2+-mobilizing activity. J. Biol. Chem. 264: 11725–11731.PubMedGoogle Scholar
  38. 38.
    Galione A. Lee HC and Busa WB. 1991. Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253: 1143–1146.PubMedCrossRefGoogle Scholar
  39. 39.
    Santella L and Kyozuka K. 1997. Effects of 1-methyladenine on nuclear Ca2+ transients and meiosis resumption in starfish oocytes are mimicked by the nuclear injection of inositol 1,4,5-trisphosphate and cADP-ribose. Cell Calium 22: 11–20.CrossRefGoogle Scholar
  40. 40.
    Mothet JP, Fossier P, Meunier FM, Stinnakre J, Tauc L and Baux G. 1998. Cyclic ADP-ribose and calcium-induced calcium release regulate neurotransmitter release at a cholinergic synapse of Aplysia. J. Physiol. 507.2: 405–414.Google Scholar
  41. 41.
    Albrieux M, Lee HC and Villaz M. 1998. Calcium signaling by cyclic ADP-ribose, NAADP, and inositol trisphosphate are involved in distinct functions in Ascidian oocytes. J. Biol. Chem. 273: 14566–14574.PubMedCrossRefGoogle Scholar
  42. 42.
    Messutat S, Heine M and Wicher D. 2001. Calcium-induced calcium release in neurosecretory insect neurons:fast and slow responses. Cell Calcium 30: 199–211.PubMedCrossRefGoogle Scholar
  43. 43.
    Fluck R, Abraham V, Miller A and Galione A. 1999. Microinjection of cyclic ADP-ribose triggers a regenerative wave of Ca2+ release and exocytosis of cortical alveoli in medaka eggs. Zygote 7: 285–292.PubMedCrossRefGoogle Scholar
  44. 44.
    Hua SY, Tokimasa T, Takasawa S, Furuya Y, Nohmi M, Okamoto H and Kuba K. 1994. Cyclic ADP-ribose modulates Ca2+ release channels for activation by physiological Ca2+ entry in bullfrog sympathetic neurons. Neuron 12: 1073–1079.PubMedCrossRefGoogle Scholar
  45. 45.
    Brailoiu E and Miyamoto D. 2000. Inositol trisphosphate and cyclic adenosine diphosphate-ribose increase quantal transmitter release at frog motor nerve terminals: Possible involvement of smooth endoplasmic reticulum. Neuroscience 95: 927–931.PubMedCrossRefGoogle Scholar
  46. 46.
    Graeff R and Lee HC. 2002. A novel cycling assay for cellular cyclic ADP-ribose with nanomolar sensitivity.Biochem. J. 361: 379–384.PubMedGoogle Scholar
  47. 47.
    Khoo KM, Han M-K, Park JB, Chae SW, Kim U-H, Lee HC, Bay BH and Chang CF. 2000. Localization of the cyclic ADP-ribose-dependent calcium signaling pathway in hepatocyte nucleus. J. Biol. Chem. 275: 24807–24817.PubMedCrossRefGoogle Scholar
  48. 48.
    Yusufi ANK, Cheng J, Thompson MA, Dousa TP, Warner GM, Walker HJ and Grande JP. 2001. cADP-ribose/ryanodine channel/Ca2+-release signal transduction pathway in mesangial cells. Am. J. Physiol. 281: F91–F102.Google Scholar
  49. 49.
    Takasawa S, Akiyama T, Nata K, Kuroki M, Tohgo A, Noguchi N, Kobayashi S, Kato I, Katada T, Okamoto H, Takasawa S, Akiyama T, Nata K, Kuroki M, Tohgo A, Noguchi N, Kobayashi S, Kato I, Katada T, et al. 1998. Cyclic ADP-ribose and inositol 1,4,5-trisphosphate as alternate second messengers for intracellular Ca2+ mobilization in normal and diabetic beta-cells. J. Biol. Chem. 273: 2497–2500.PubMedCrossRefGoogle Scholar
  50. 50.
    Li P-L, Tang W-X, Valdivia HH, Zou A-P and Campbell WB. 2001. cADP-ribose activates reconstituted ryanodine receptors from coronary arterial smooth muscle. Am. J. Physiol. 280:H208–H215.Google Scholar
  51. 51.
    Prakash YS, Kannan MS, Walseth TF and Sieck GC. 1998. Role of cyclic ADP-ribose in the regulation of [Ca2+ in porcine tracheal smooth muscle. Am. J. Physiol. 43: C1653–C1660.Google Scholar
  52. 52.
    Cancela JM and Petersen OH. 1998. The cyclic ADP ribose antagonist 8-NH2-cADP-ribose blocks cholecystokinin-evoked cytosolic Ca2+ spiking in pancreatic acinar cells. Pflug. Arch. 435: 746–748.CrossRefGoogle Scholar
  53. 53.
    Guse AH, Dasilva CP, Emmrich F, Ashamu GA, Potter BVL and Mayr GW. 1995. Characterization of cyclic adenosine diphosphate-ribose-induced Ca2+ release in T lymphocyte cell lines. J. Immunol. 155: 3353–3359.PubMedGoogle Scholar
  54. 54.
    Guse AH, Berg I, Dasilva CP, Potter BVL and Mayr GW. 1997. Ca2+ entry induced by cyclic ADP-ribose in intact T-lymphocytes. J. Biol. Chem. 272: 8546–8550.PubMedCrossRefGoogle Scholar
  55. 55.
    Galione A, White A, Willmott N, Turner M, Potter BV and Watson SP. 1993. cGMP mobilizes intracellular Ca2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature 365: 456–459.PubMedCrossRefGoogle Scholar
  56. 56.
    Drum CL, Yan SZ, Bard J, Shen YQ, Lu D, Soelaiman S, Grabarek Z, Bohm A and Tang WJ. 2002. Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415: 396–402.PubMedCrossRefGoogle Scholar
  57. 57.
    Madden JC, Ruiz N and Caparon M. 2001. Cytolysin-mediated translocation (CMT): A functional equivalent of type III secretion in Gram-positive bacteria. Cell 104: 143–152.PubMedCrossRefGoogle Scholar
  58. 58.
    Karasawa T, Takasawa S, Yamakawa K, Yonekura H, Okamoto H and Nakamura S. 1995. NAD+-glycohydrolase from Streptococcus pyogenes shows cyclic ADP-ribose forming activity. FEMS Microbiol. Lett. 130: 201–204.PubMedCrossRefGoogle Scholar
  59. 59.
    Howard M, Grimaldi JC, Bazan JF, Lund FE, Santos-Argumedo L, Parkhouse RM, Walseth TF and Lee HC. 1993. Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262: 1056–1059.PubMedCrossRefGoogle Scholar
  60. 60.
    Navazio L, Bewell MA, Siddiqua A, Dickinson GD, Galione A and Sanders D. 2000. Calcium release from the endoplasmic reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate. Proc. Natl. Acad. Sci. USA 97: 8693–8698.PubMedCrossRefGoogle Scholar
  61. 61.
    Churchill GC and Galione A. 2001. NAADP induces Ca2+ oscillations via a two-pool mechanism by priming IP3- and cADPR-sensitive Ca2+ stores. EMBO J. 20: 2666–2671.PubMedCrossRefGoogle Scholar
  62. 62.
    Santella L, Kyozuka K, Genazzani AA, De Riso L and Carafoli E. 2000. Nicotinic acid adenine dinucleotide phosphate-induced Ca2+ release. Interactions among distinct Ca2+ mobilizing mechanisms in starfish oocytes. J. Biol. Chem. 275: 8301–8306.PubMedCrossRefGoogle Scholar
  63. 63.
    Chameau P, Van De Vrede Y, Fossier P and Baux G. 2001. Ryanodine-, IP3- and NAADP-dependent calcium stores control acetylcholine release. Pflugers Arch. 443: 289–296.PubMedCrossRefGoogle Scholar
  64. 64.
    Brailoiu E, Miyamoto MD and Dun NJ. 2001. Nicotinic acid adenine dinucleotide phosphate enhances quantal neurosecretion at the frog neuromuscular junction: possible action on synaptic vesicles in the releasable pool. Mol. Pharmacol. 60: 718–724.PubMedGoogle Scholar
  65. 65.
    Cancela JM, Churchill GC and Galione A. 1999. Coordination of agonist-induced Ca2+-signalling patterns by NAADP in pancreatic acinar cells. Nature 398: 74–76.PubMedCrossRefGoogle Scholar
  66. 66.
    Bak J, White P, Timár G, Missiaen L, Genazzani AA and Galione A. 1999. Nicotinic acid adenine dinucleotide phosphate triggers Ca2+ release from brain microsomes. Curr. Biol. 9: 751–754.PubMedCrossRefGoogle Scholar
  67. 67.
    Patel S, Churchill GC, Sharp T and Galione A. 2000. Widespread distribution of binding sites for the novel Ca2+-mobilizing messenger, nicotinic acid adenine dinucleotide phosphate, in the brain. J. Biol. Chem. 275: 36495–36497.PubMedCrossRefGoogle Scholar
  68. 68.
    Berg I, Potter BVL, Mayr GW and Guse AH. 2000. Nicotinic acid adenine dinucleotide phosphate (NAADP+) is an essential regulator of T-lymphocyte Ca2+-signaling. J. Cell Biol. 150:581–588.PubMedCrossRefGoogle Scholar
  69. 69.
    Bak J, Billington RA, Timar G, Dutton AC and Genazzani AA. 2001. NAADP receptors are present and functional in the heart. Curr. Biol. 11: 987–990.PubMedCrossRefGoogle Scholar
  70. 70.
    Mojzisova A, Krizanova O, Zacikova L, Kominkova V and Ondrias K. 2001. Effect of nicotinic acid adenine dinucleotide phosphate on ryanodine calcium release channel in heart. Eur. J. Physiol. 441: 674–677.CrossRefGoogle Scholar
  71. 71.
    Cheng J, Yusufi AN, Thompson MA, Chini EN and Grande JP. 2001. Nicotinic acid adenine dinucleotide phosphate: A new Ca2+ releasing agent in kidney. J. Am. Soc. Nephrol. 12: 54–60.PubMedGoogle Scholar
  72. 72.
    Yusufi AN, Cheng J, Thompson MA, Burnett JC and Grande JP. 2002. Differential mechanisms of Ca2+ release from vascular smooth muscle cell microsomes. Exp.Biol.Md. 227: 36–44.Google Scholar
  73. 73.
    Yusufi AN, Cheng J, Thompson MA, Chini EN and Grande JP. 2001. Nicotinic acid-adenine dinucleotide phosphate (NAADP) elicits specific microsomal Ca2+ release from mammalian cells. Biochem. J. 353: 531–536.PubMedCrossRefGoogle Scholar
  74. 74.
    Graeff R  and Lee HC. 2002. A novel cycling assay for NAADP with nanomolar sensitivity. Biochem. J. (in press).Google Scholar
  75. 75.
    Graeff RM, Podein RJ, Aarhus R and Lee HC. 1995. Magnesium ions but not ATP inhibit cyclic ADP-ribose-induced calcium release. Biochem. Biophys. Res. Commun. 206:786–791.PubMedCrossRefGoogle Scholar
  76. 76.
    Lee HC. 1993. Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J. Biol. Chem. 268: 293–299.PubMedGoogle Scholar
  77. 77.
    Lee HC, Aarhus R, Graeff R, Gurnack ME and Walseth TF. 1994. Cyclic ADP ribose activation of the ryanodine receptor is mediated by calmodulin. Nature 370: 307–309.PubMedCrossRefGoogle Scholar
  78. 78.
    Lee HC Aarhus R and Graeff RM. 1995. Sensitization of calcium-induced calcium release by cyclic ADP-ribose and calmodulin. J. Biol. Chem. 270: 9060–9066.PubMedCrossRefGoogle Scholar
  79. 79.
    Tanaka Y and Tashjian AH, Jr. 1995. Calmodulin is a selective mediator of Ca2+-induced Ca2+ release via the ryanodine receptor-like Ca2+ channel triggered by cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 92: 3244–3248.PubMedCrossRefGoogle Scholar
  80. 80.
    Perez CF, Marengo JJ, Bull R and Hidalgo C. 1998. Cyclic ADP-ribose activates caffeine-sensitive calcium channels from sea urchin egg microsomes. Am. J. Physiol. 274: C430–C439.PubMedGoogle Scholar
  81. 81.
    Lokuta AJ, Darszon A, Beltran C and Valdivia HH. 1998. Detection and functional characterization of ryanodine receptors from sea urchin eggs. J. Physiol. 510.1: 155–164.Google Scholar
  82. 82.
    Meszaros LG, Bak J and Chu A. 1993. Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel. Nature 364: 76–79.PubMedCrossRefGoogle Scholar
  83. 83.
    Sitsapesan R and Williams AJ. 1995. Cyclic ADP-ribose and related compounds activate sheep skeletal sarcoplasmic reticulum Ca2+ release channel. Am. J. Physiol. 268: CI 235–C1240.Google Scholar
  84. 84.
    Sonnleitner A, Conti A, Bertocchini F, Schindler H and Sorrentino V. 1998. Functional properties of the ryanodine receptor type 3 (Ryr3) Ca2+ release channel. EMBO J. 17: 2790–2798.PubMedCrossRefGoogle Scholar
  85. 85.
    Zhang X, Wen J, Bidasee KR, Besch Jr HR, Wojcikiewicz RJ, Lee B and Rubin RP. 1999. Ryanodine and inositol trisphosphate receptors are differentially distributed and expressed in rat parotid gland. Biochem. J. 340: 519–527.PubMedCrossRefGoogle Scholar
  86. 86.
    Empson RM and Galione A. 1997. Cyclic ADP-ribose enhances coupling between voltage-gated Ca2+ entry and intracellular Ca2+ release. J. Biol. Chem. 272: 20967–20970.PubMedCrossRefGoogle Scholar
  87. 87.
    Hashii M, Minabe Y and Higashida H. 2000. cADP-ribose potentiates cytosolic Ca2+ elevation and Ca2+ entry via L-type voltage-activated Ca2+ channels in NG108-15 neuronal cells. Biochem. J. 345: 207–215.PubMedCrossRefGoogle Scholar
  88. 88.
    Lee HC. 1996. Modulator and messenger functions of cyclic ADP-ribose in calcium signaling. Re. Prog. Horm. Res. 51: 355–388.Google Scholar
  89. 89.
    Lee HC. 2000. NAADP: An emerging calcium signaling molecule. J. Memb. Biol. 173: 1–8.CrossRefGoogle Scholar
  90. 90.
    Genazzani AA, Mezna M, Dickey DM, Michelangeli F, Walseth TF and Galione A. 1997. Pharmacological properties of the Ca2Velease mechanism sensitive to NAADP in the sea urchin egg. Brit. J. Pharm. 121: 1489–1495.CrossRefGoogle Scholar
  91. 91.
    Lee HC and Aarhus R. 1997. Structural determinants of nicotinic acid adenine dinucleotide phosphate important for its calcium-mobilizing activity. J. Biol. Chem. 272: 20378–20383.PubMedCrossRefGoogle Scholar
  92. 92.
    Aarhus R, Dickey DM, Graeff RM, Gee KR, Walseth TF and Lee HC. 1996. Activation and inactivation of Ca2+ release by NAADP+. J. Biol. Chem. 271: 8513–8516.PubMedCrossRefGoogle Scholar
  93. 93.
    Aarhus R, Graeff RM, Dickey DM, Walseth TF and Lee HC. 1995. ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. J. Biol. Chem. 270: 30327–30333.PubMedCrossRefGoogle Scholar
  94. 94.
    Lee HC. 1991. Specific binding of cyclic ADP-ribose to calcium-storing microsomes from sea urchin eggs. J. Biol. Chem. 266: 2276–2281.PubMedGoogle Scholar
  95. 95.
    Lee HC and Aarhus R. 2000. Functional visualization of the separate but interacting calcium stores sensitive to NAADP and cyclic ADP-ribose. J. Cell Sci. 113: 4413–4420.PubMedGoogle Scholar
  96. 96.
    Churchill GC and Louis CF. 1999. Imaging of intracellular calcium stores in single permeabilized lens cells. Am. J. Physiol. 276: C426–C434.PubMedGoogle Scholar
  97. 97.
    Mitchell KJ, Pinton P, Varadi A, Tacchetti C, Ainscow EK, Pozzan T, Rizzuto R and Rutter GA. 2001. Dense core secretory vesicles revealed as a dynamic Ca2+ store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J. Cell Biol. 155:41–51.PubMedCrossRefGoogle Scholar
  98. 98.
    Gerasimenko OV, Gerasimenko JV, Belan PV and Petersen OH. 1996. Inositol trisphosphate and cyclic ADP-ribose-mediated release of Ca2+ from single isolated pancreatic zymogen granules. Cell 84: 473–480.PubMedCrossRefGoogle Scholar
  99. 99.
    Gerasimenko OV, Gerasimenko JV, Tepikin AV and Petersen OH. 1995. ATP-dependent accumulation and inositol trisphosphate- or cyclic ADP-ribose-mediated release of Ca2+ from the nuclear envelope. Cell 80: 439–444.PubMedCrossRefGoogle Scholar
  100. 100.
    Adebanjo OA, Anandatheerthavarada HK, Koval AP, Moonga BS, Biswas G, Sun L, Sodam BR, Bevis PJR, Huang CLH, Epstein S, Lai FA, Avadhani NG and Zaidi M. 1999. A new function for CD38/ADP-ribosyl cyclase in nuclear Ca2+ homeostasis. Nature Cell Biol. 1: 409–414.PubMedCrossRefGoogle Scholar
  101. 101.
    Santella L, Deriso L, Gragnaniello G and Kyozuka E. 1998. Separate activation of the cytoplasmic and nuclear calcium pools in maturing starfish oocytes. Biochem. Biophys. Res. Commun. 252: 1–4.PubMedCrossRefGoogle Scholar
  102. 102.
    Genazzani AA and Galione A. 1996. Nicotinic acid-adenine dinucleotide phosphate mobilizes Ca2+ from a thapsigargin-insensitive pool. Biochem. J. 315: 721–725.PubMedGoogle Scholar
  103. 103.
    Lim D, Kyozuka K, Gragnaniello G, Carafoli E and Santella L. 2001. NAADP+ initiates the Ca2+ response during fertilization of starfish oocytes. FASEB J. 15: 2257–2267.PubMedCrossRefGoogle Scholar
  104. 104.
    Aarhus R, Gee K and Lee HC. 1995. Caged cyclic ADP-ribose - synthesis and use. J. Biol. Chem. 270: 7745–7749.PubMedCrossRefGoogle Scholar
  105. 105.
    Lee HC, Aarhus R, Gee KR and Kestner T. 1997. Caged nicotinic acid adenine dinucleotide phosphate — Synthesis and use. J. Biol. Chem. 272: 4172–4178.PubMedCrossRefGoogle Scholar
  106. 106.
    Nusco GA, Lim D, Sabala P and Santella L. 2002. Ca2+ response to cADPr during maturation and fertilization of starfish oocytes. Biochem. Biophys. Res. Commun. 290: 1015–1021.PubMedCrossRefGoogle Scholar
  107. 107.
    Leite MF, Burgstahler AD and Nathanson MH. 2002. Ca2+ waves require sequential activation of inositol trisphosphate receptors and ryanodine receptors in pancreatic acini. Gastroenterology 122: 415–427.PubMedCrossRefGoogle Scholar
  108. 108.
    Leite MF, Dranofff JA, Gao L and Nathanson MH. 1999. Expression and subcellular localization of the ryanodine receptor in rat pancreatic acinar cells. Biochem. J. 337: 305–309.PubMedCrossRefGoogle Scholar
  109. 109.
    Krause E, Gobel A and Schulz I. 2002. Cell side-specific sensitivities of intracellular Ca2+ stores for inositol l,4,5-trisphosphate,cyclic ADP-ribose and Nicotinic adenine dinucleotide phosphate in permeabilized pancreatic acinar cells from mouse. J. Biol. Chem. 11696–11702Google Scholar
  110. 110.
    Zhang XJ, Wen JY, Bidasee KR, Besch HR and Rubin RP. 1997. Ryanodine receptor expression is associated with intracellular Ca2+ release in rat parotid acinar cells. Am. J. Physiol. 42:C1306–C1314.Google Scholar
  111. 111.
    Putney JW, Jr. 1986. A model for receptor-regulated calcium entry. Cell Calcium 7: 1–12.PubMedCrossRefGoogle Scholar
  112. 112.
    Parekh AB and Penner R. 1997. Store depletion and calcium influx. Physiol. Rev. 11: 901–930.Google Scholar
  113. 113.
    Kiselyov K, Shin DM, Shcheynikov N, Kurosaki T and Muallem S. 2001. Regulation of Ca2+-release-activated Ca2+ current (ICRAC) by ryanodine receptors in inositol 1,4,5-trisphosphate-receptor-deficient DT40 cells. Biochem. J. 360: 17–22.PubMedCrossRefGoogle Scholar
  114. 114.
    Sugawara H, Kurosaki M, Takata M and Kurosaki T. 1997. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J. 16: 3078–3088.PubMedCrossRefGoogle Scholar
  115. 115.
    Guse AH, Dasilva CP, Weber K, Ashamu GA, Potter BVL and Mayr GW. 1996. Regulation of cADP-ribose-induced Ca2+ release by Mg2+ and inorganic phosphate. J. Biol. Chem. 271: 23946–23953.PubMedCrossRefGoogle Scholar
  116. 116.
    De Flora A, Franco L, Guida L, Bruzzone S, Usai C and Zocchi E. 2000. Topology of CD38. Chem. Immunol. 75: 79–98.PubMedCrossRefGoogle Scholar
  117. 117.
    Kuemmerle JF and Makhlouf GM. 1995. Agonist-stimulated cyclic ADP ribose. Endogenous modulator of Ca2+-induced Ca2+ release in intestinal longitudinal muscle. J. Biol. Chem. 270: 25488–25494.PubMedCrossRefGoogle Scholar
  118. 118.
    Takasawa S, Nata K, Yonekura H and Okamoto H. 1993. Cyclic ADP-ribose in insulin secretion from pancreatic beta cells. Science 259: 370–373.PubMedCrossRefGoogle Scholar
  119. 119.
    Islam MS, Larsson O and Berggren PO. 1993. Cyclic ADP-ribose in beta cells. Science 262: 584–586.PubMedCrossRefGoogle Scholar
  120. 120.
    Varadi A and Rutter GA. 2002. Dynamic imaging of endoplasmic reticulum Ca2+ concentration in insulin-secreting MIN6 cells using recombinant targeted cameleons: Roles of sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA)-2 and ryanodine receptors. Diabetes 51, Suppl 1: S190–S201.Google Scholar
  121. 121.
    Huang MS, Adebanjo O, Moonga BS, Goldstein S, Lai FA, Lipschitz DA and Zaidi M. 1998. Upregulation of functional ryanodine receptors during in vitro aging of human diploid fibroblasts. Biochem. Biophys. Res. Commun.  245: 50–52.PubMedCrossRefGoogle Scholar
  122. 122.
    Burdakov D, Cancela JM and Petersen OH. 2001. Bombesin-induced cytosolic Ca2+ spiking in pancreatic acinar cells depends on cyclic ADP-ribose and ryanodine receptors. Cell Calcium 29: 211–216.PubMedCrossRefGoogle Scholar
  123. 123.
    Burdakov D and Galione A. 2000. Two neuropeptides recruit different messenger pathways to evoke Ca2+ signals in the same cell. Curr. Biol. 10: 993–996.PubMedCrossRefGoogle Scholar
  124. 124.
    Gromada J, Jorgensen TD and Dissing S. 1995. The release of intracellular Ca2+ in lacrimal acinar cells by alpha-, beta-adrenergic and muscarinic cholinergic stimulation: the roles of inositol triphosphate and cyclic ADP-ribose. Pflug. Arch. 429: 751–761.CrossRefGoogle Scholar
  125. 125.
    Lee HC, Aarhus R and Walseth TF. 1993. Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science 261: 352–355.PubMedCrossRefGoogle Scholar
  126. 126.
    Galione A, McDougall A, Busa WB, Willmott N, Gillot I and M. W. 1993. Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science 261: 348–352.PubMedCrossRefGoogle Scholar
  127. 127.
    Matsumoto M, Nakagawa T, Inoue T, Nagata E, Tanaka K, Takano H, Minowa O, Kuno J, Sakakibara S, Yamada M, Yoneshima H, Miyawaki A, Fukuuchi Y, Furuichi T, Okano H, Mikoshiba K and Noda T. 1996. Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor. Nature 379: 168–171.PubMedCrossRefGoogle Scholar
  128. 128.
    Churchill GC and Galione A. 2000. Spatial control of Ca2+ signaling by nicotinic acid adenine dinucleotide phosphate diffusion and gradients. J. Biol. Chem. 275: 38687–38692.PubMedCrossRefGoogle Scholar
  129. 129.
    Churchill GC and Galione A. 2001. Prolonged inactivation of nicotinic acid adenine dinucleotide phosphate-induced Ca2+ Release mediates a spatiotemporal Ca2+ memory. J. Biol. Chem. 276: 11223–11225.PubMedCrossRefGoogle Scholar
  130. 130.
    Genazzani AA, Empson RM and Galione A. 1996. Unique inactivation properties of NAADP-sensitive Ca2+ release. J. Biol. Chem. 271: 11599–11602.PubMedCrossRefGoogle Scholar
  131. 131.
    Churchill GC and Louis CF. 1998. Roles of Ca2+, inositol trisphosphate and cyclic ADP-ribose in mediating intercellular Ca2+ signaling in sheep lens cells. J. Cell Sci. 111: 1217–1225.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  1. 1.Department of PharmacologyUniversity of MinnesotaMinneapolisUSA

Personalised recommendations