Pharmacology of Cyclic ADP-Ribose and NAADP

Synthesis and Properties of Analogs


Multiple Ca2+ stores are generally present in cells. Principal among them are the mitochondria and the endoplasmic reticulum. It is generally accepted that inositol trisphosphate mobilizes Ca2+ stores in the endoplasmic reticulum [1]. Also present in the organelle is another Ca2+ release channel, the ryanodine receptor. The discovery of two other Ca2+ signaling molecules, cyclic ADP-ribose (cADPR) and nicotinic acid adenine dinucleotide phosphate (NAADP) [2–4] further highlights the complexity of Ca2+ mobilization as a fundamental signaling mechanism [1].


Ryanodine Receptor Pancreatic Acinar Cell Nicotinamide Adenine Dinucleotide Phosphate Inositol Trisphosphate Nicotinic Acid Adenine Dinucleotide Phosphate 
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  1. 1.
    Berridge MJ. 1993. Inositol trisphosphate and calcium signaling. Nature 361: 315–325PubMedCrossRefGoogle Scholar
  2. 2.
    Clapper DL, Walseth TF, Dargie PJ and Lee HC. 1987. Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositiol trisphosphate. J. Biol. Chem. 262: 9561–9568.PubMedGoogle Scholar
  3. 3.
    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
  4. 4.
    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
  5. 5.
    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
  6. 6.
    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
  7. 7.
    Lee HC. 1993. Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J. Biol. Chem. 268: 293–299.PubMedGoogle Scholar
  8. 8.
    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
  9. 9.
    Cancela JM, Gerasimenko OV, Gerasimenko JV, Tepikin AV and Petersen OH. 2000. Two different but converging messenger pathways to intracellular Ca2+ release: the roles of nicotinic acid adenine dinucleotide phosphate, cyclic ADP-ribose and inositol trisphosphate. EMBO J. 19: 2549–2557.PubMedCrossRefGoogle Scholar
  10. 10.
    Lee HC and Aarhus R. 1991. ADP-ribosyl cyclase: an enzyme that cyclizes NAD+ into a calcium-mobilizing metabolite. Cell Regul. 2: 203–209.PubMedGoogle Scholar
  11. 11.
    Walseth TF, Aarhus R, Gurnack ME, Wong L, Breitinger HG, et al. 1997. Preparation of cyclic ADP-ribose antagonists and caged cyclic ADP-ribose. Meth. Enzymol. 280: 294–305.PubMedCrossRefGoogle Scholar
  12. 12.
    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
  13. 13.
    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
  14. 14.
    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
  15. 15.
    Lee HC and Aarhus R. 1998. Fluorescent analogs of NAADP with calcium mobilizing activity. Biochim. Biophys. Acta 1425: 263–271.PubMedCrossRefGoogle Scholar
  16. 16.
    Lee HC, Aarhus R, Levitt D. 1994. The crystal structure of cyclic ADP-ribose. Nature Struct. Biol 1: 143–144.PubMedCrossRefGoogle Scholar
  17. 17.
    Munshi C and Lee HC. 1997. High-level expression of recombinant Aplysia ADP-ribosyl cyclase in Pichia pastor is by fermentation. Prot. Expres. Purif. 11: 104–110.CrossRefGoogle Scholar
  18. 18.
    Ashamu GA, Sethi JK, Galione A and Potter BVL. 1997. Roles for adenosine ribose hydroxyl groups in cyclic adenosine 5’-diphosphate ribose-mediated Ca2+ release. Biochemistry 36: 9509–9517.PubMedCrossRefGoogle Scholar
  19. 19.
    Bailey VC, Fortt SM, Summerhill RJ, Galione A and Potter BVL. 1996. Cyclic aristeromycin diphosphate ribose: a potent and poorly hydrolysable Ca2+-mobilizing mimic of cyclic adenosine diphosphate ribose. FEBS Lett. 379: 227–230.PubMedCrossRefGoogle Scholar
  20. 20.
    Bailey VC, Sethi JK, Fortt SM, Galione A and Potter B. 1997. 7-deaza cyclic adenosine 5’-diphosphate ribose - First example of a Ca2+-mobilizing partial agonist related to cyclic adenosine 5’-diphosphate ribose. Chem. Biol 4: 51–61.PubMedCrossRefGoogle Scholar
  21. 21.
    Bailey VC, Sethi JK, Galione A and Potter B. 1997. Synthesis of 7-deaza-8-bromo cyclic adenosine 5’-diphosphate ribose - the first hydrolysis resistant antagonist at the cADPR receptor. Chem. Commun. 7: 695–696.CrossRefGoogle Scholar
  22. 22.
    Wong L, Aarhus R, Lee HC and Walseth TF. 1999. Cyclic 3-deaza-adenosine diphosphoribose: a potent and stable analog of cyclic ADP-ribose. Biochim. Biophys. Acta 1472:555–564.Google Scholar
  23. 23.
    Shuto S, Fukuoka M, Manikowsky A, Ueno Y, Nakano T, et al 2001. Total synthesis of cyclic ADP-carbocyclic-ribose, a stable mimic of Ca2+-mobilizing second messenger cyclic ADP-ribose. J. Am. Chem. Soc. 123: 8750–8759.PubMedCrossRefGoogle Scholar
  24. 24.
    Shuto S, Fukuoka M, Abe H and Matsuda A. 2001. Intracellular Ca2+-mobilizing adenine nucleotides. Synthesis and biological activity of cyclic ADP-carbocyclic-ribose and C-glycosidic analog of adenophostin A. Nucleosides, Nucleotides Nucleic Acids 20: 461–470.PubMedCrossRefGoogle Scholar
  25. 25.
    Fukuoka M, Shuto S, Minakawa N, Ueno Y and Matsuda A. 2001. Synthesis and biological activities of cyclic ADP-carbocyclic-ribose and its analogs. Nucleosides, Nucleotides Nucleic Acids 20: 1355–1358.PubMedCrossRefGoogle Scholar
  26. 26.
    Fukuoka M, Shuto S, Minakawa N, Ueno Y and Matsuda A. 2000. An efficient synthesis of cyclic I DP- and cyclic 8-bromo-IDP-carbocyclic-riboses using a modified hata condensation method to form an intramolecular pyrophosphate linkage as a key step. An entry to a general method for the chemical synthesis of cyclic ADP-ribose analogues. J. Org. Chem. 65: 5238–5248.PubMedCrossRefGoogle Scholar
  27. 27.
    Galeone A, Mayol L, Oliviero G, Piccialli G and Varra M. 2002. Synthesis of a novel N-1 carbocyclic, N-9 butyl analogue of cyclic ADP ribose (cADPR). Tetrahedron 58: 363–368.CrossRefGoogle Scholar
  28. 28.
    Huang L-J, Zhoa Y-Y, Yuan L, Min J-M and Zhang L-H. 2002. Chemical Synthesis and Calcium Release Activity of Nl-Ether Strand substituted cADPR Mimic. Bioorg. Med. Chem. Lett. 12:887–889.PubMedCrossRefGoogle Scholar
  29. 29.
    Walseth TF, Aarhus R, Kerr JA and Lee HC. 1993. Identification of cyclic ADP-ribose-binding proteins by photoaffinity labeling. J. Biol. Chem. 268: 26686–26691.PubMedGoogle Scholar
  30. 30.
    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
  31. 31.
    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
  32. 32.
    Prakash YS, Kannan MS, Walseth TF and Sieck GC. 1998. Role of cyclic ADP-ribose in the regulation of [Ca2+]i in porcine tracheal smooth muscle. Am. J. Physiol. 43: CI 653–C1660.Google Scholar
  33. 33.
    Rakovic S, Galione A, Ashamu GA, Potter B and Terrar DA. 1996. A specific cyclic ADP-ribose antagonist inhibits cardiac excitation-contraction coupling. Cur. Biol. 6: 989–996.CrossRefGoogle Scholar
  34. 34.
    Rakovic S, Cui Y, Iino S, Galione A, Ashamu GA, et al. 1999. An antagonist of cADP-ribose inhibits arrhythmogenic oscillations of intracellular Ca2+ in heart cells. J. Biol. Chem. 274: 17820–17827.PubMedCrossRefGoogle Scholar
  35. 35.
    Prakash YS, Kannan MS, Walseth TF and Sieck GC. 2000. cADP ribose and [Ca2+]i regulation in rat cardiac myocytes. Am. J. Physiol. 279: H1482–H1489.Google Scholar
  36. 36.
    Guse AH, Berg I, Dasilva CP, Potter B and Mayr GW. 1997. Ca2+ entry induced by cyclic ADP-ribose in intact T-lymphocytes. J. Biol. Chem. 272: 8546–8550.PubMedCrossRefGoogle Scholar
  37. 37.
    Verderio C, Bruzzone S, Zocchi E, Fedele E, Schenk U, et al. 2001. Evidence of a role for cyclic ADP-ribose in calcium signalling and neurotransmitter release in cultured astrocytes. J. Neurochem. 78: 646–657.PubMedCrossRefGoogle Scholar
  38. 38.
    Linden DJ, Dawson TM and Dawson VL. 1995. An evaluation of the nitric oxide/cGMP/cGMP-dependent protein kinase cascade in the induction of cerebellar long-term depression in culture. J. Neurosci. 15: 5098–5105.PubMedGoogle Scholar
  39. 39.
    Ebihara S, Sasaki T, Hida W, Kikuchi Y, Oshiro T, et al. 1997. Role of cyclic ADP-ribose in ATP-activated potassium currents in alveolar macrophages. J. Biol. Chem. 272: 16023–16029.PubMedCrossRefGoogle Scholar
  40. 40.
    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. Pfluegers Archiv 435: 746–748.PubMedCrossRefGoogle Scholar
  41. 41.
    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
  42. 42.
    Leckie CP, McAinsh MR, Allen GJ, Sanders D and Hetherington AM. 1998. Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Pro. Nat.I Acad. Sci. USA. 95: 15837–15842.CrossRefGoogle Scholar
  43. 43.
    De Flora A, Guida L, Franco L, Zocchi E, Pestarino M, et al. 1996. Ectocellular in vitro and in vivo metabolism of cADP-ribose in cerebellum. Biochem. J. 320: 665–672.PubMedGoogle Scholar
  44. 44.
    Podesta M, Zocchi E, Pitto A, Usai C, Franco L, et al. 2000. Extracellular cyclic ADP-ribose increases intracellular free calcium concentration and stimulates proliferation of human hemopoietic progenitors. FASEB J. 14: 680–690.PubMedGoogle Scholar
  45. 45.
    Franco L, Bruzzone S, Song PF, Guida L, Zocchi E, et al. 2001. Extracellular cyclic ADP-ribose potentiates ACh-induced contraction in bovine tracheal smooth muscle. Am. J. Physiol. 280:L98–L106.Google Scholar
  46. 46.
    Franco L, Zocchi E, Usai C, Guida L, Bruzzone S, et al. 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
  47. 47.
    Zocchi E, Podesta M, Pitto A, Usai C, Bruzzone S, et al. 2001. Stroma-generated cyclic ADP-ribose stimulates the expansion of early human hemopoietic progenitors by a paracrine interaction. FASEB J. 15: 29.Google Scholar
  48. 48.
    Sethi JK, Empson RM, Bailey VC, Potter B 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
  49. 49.
    Dipp M and Evans AM. 2001. Cyclic ADP-ribose is the primary trigger for hypoxic pulmonary vasoconstriction in the rat lung in situ. Cir. Res. 89: 77–83.CrossRefGoogle Scholar
  50. 50.
    Wilson HL, Dipp M, Thomas JM, Lad C, Galione A and Evans AM. 2001. ADP-ribosyl cyclase and cyclic ADP-ribose hydrolase act as a redox sensor - A primary role for cyclic ADP-ribose in hypoxic pulmonary vasoconstriction. J. Biol. Chem. 276: 11180–11188.PubMedCrossRefGoogle Scholar
  51. 51.
    Partida-Sanchez S, Cockayne DA, Monard S, Jacobson EL, Oppenheimer N, et al. 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
  52. 52.
    Yu JZ, Zhang DX, Zou AP, Campbell WB and Li PL. 2000. Nitric oxide inhibits Ca2+ mobilization through cADP-ribose signaling in coronary arterial smooth muscle cells. Am. J. Physiol. 279: H873–H881.Google Scholar
  53. 53.
    Guse AH, da Silva CP, Berg I, Skapenko AL, Weber K, et al. 1999. Regulation of calcium signalling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature 398: 70–73.PubMedCrossRefGoogle Scholar
  54. 54.
    Guse AH, Dasilva CP, Weber K, Armah CN, Ashamu GA, et al. 1997. l-(5-phospho-beta-D-ribosyl)2’-phosphoadenosine 5’-phosphate cyclic anhydride induced Ca2+ release in human T-cell lines. Eur. J. Biochem. 245: 411–417.CrossRefGoogle Scholar
  55. 55.
    Lee HC. 1997. Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol. Rev. 77: 1133–1164.PubMedGoogle Scholar
  56. 56.
    Lee HC. 2001. Physiological functions of cyclic ADP-ribose and NAADP as calcium messengers. Annu. Rev. Pharmacol. Toxicol. 41: 317–345.PubMedCrossRefGoogle Scholar
  57. 57.
    Shiwa M, Murayama T and Ogawa Y. 2002. Molecular cloning and characterization of ryanodine receptor from unfertilized sea urchin eggs. Am. J. Physiol. 282: R727–R737.Google Scholar
  58. 58.
    Shuto S, Shirato M, Sumita Y, Ueno Y and Matsuda A. 1998. Synthetic studies of carbocyclic analogs of cyclic ADP-ribose - formation of a cyclic dimer, a 36-membered-ring product, in the condensation reaction of an 8-brorno-n-l-[5-(phenylthiophosphoryl)-Google Scholar
  59. carbocyclic-ribosyl] inosine 5’-phosphate derivative mediated by AgN03. Tetrahedron Lett. 39:7341–7344.Google Scholar
  60. 59.
    Sumita Y, Shirato M, Ueno Y, Matsuda A and Shuto S. 2000. Nucleosides and nucleotides. 192. Toward the total synthesis of cyclic ADP-carbocyclic-ribose. Formation of the intramolecular pyrophosphate linkage by a conformation-restriction strategy in a syn-form using a halogen substitution at the 8-position of the adenine ring. Nucleosides Nucleotides Nucleic Acids 19: 175–187.PubMedCrossRefGoogle Scholar
  61. 60.
    Wall KA, Klis M, Kornet J, Coyle D, Ame JC, et al. 1998. Inhibition of the intrinsic NAD+ glycohydrolase activity of CD38 by carbocyclic NAD analogues. Biochem. J. 335:631–636.PubMedGoogle Scholar
  62. 61.
    Howard M, Grimaldi JC, Bazan JF, Lund FE, Santos AL, et al. 1993. Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262: 1056–1059.PubMedCrossRefGoogle Scholar
  63. 62.
    Zhang FJ, Yamada S, Gu QM and Sih CJ. 1996. Synthesis and characterization of cyclic ATP-ribose - a potent mediator of calcium release. Bioorg. Med. Chem. Lett. 6: 1203–1208.CrossRefGoogle Scholar
  64. 63.
    Zhang FJ, Gu QM, Jing P and Sih CJ. 1995. Enyzmatic cyclization of nicotinamide adenine dinucleotide phosphate (NADP). Bioorg. Med. Chem. Lett. 5: 2267–2272.CrossRefGoogle Scholar
  65. 64.
    Vu CQ, Lu PJ, Chen CS and Jacobson MK. 1996. 2’-Phospho-cyclic ADP-ribose, a calcium-mobilizing agent derived from NADP. J. Biol. Chem. 271: 4747–4754.PubMedCrossRefGoogle Scholar
  66. 65.
    Vu CQ, Coyle DL and Jacobson MK. 1997. Natural occurrence of 2’-phospho-cyclic ADP ribose in mammalian tissues. Biochem. Biophys. Res. Commun. 236: 723–726.PubMedCrossRefGoogle Scholar
  67. 66.
    Walseth TF, Aarhus R. Zeleznikar RJ and Lee HC. 1991. Determination of endogenous levels of cyclic ADP-ribose in rat tissues. Biochim. Biophys. Acta 1094: 113–120.Google Scholar
  68. 67.
    Wong L. 1999. Measurement of intracellular cyclic ADP-ribose and characterization of its analogs. PH.D. thesis. University of Minnesota, Minneapolis. 176 pp.Google Scholar
  69. 68.
    Zhang FJ and Sih CJ. 1995. Novel enzymatic cyclizations of pyridine nucleotide analogs - cyclic-GDP-ribose and cyclic-HDP-ribose. Tetrahedron Lett. 36: 9289–9292.CrossRefGoogle Scholar
  70. 69.
    Graeff RM, Walseth TF, Fryxell K, Branton WD and Lee HC. 1994. Enzymatic synthesis and characterizations of cyclic GDP-ribose. A procedure for distinguishing enzymes with ADP-ribosyl cyclase activity. J. Biol. Chem. 269: 30260–30267.PubMedGoogle Scholar
  71. 70.
    Graeff RM, Walseth TF, Hill HK and Lee HC. 1996. Fluorescent analogs of cyclic ADP-ribose: synthesis, spectral characterization, and use. Biochemistry 35: 379–386.PubMedCrossRefGoogle Scholar
  72. 71.
    Zhang FJ and Sih CJ. 1995. Enzymatic cyclization of l,n-6-etheno-nicotinamide adenine dinucleotide. Bioorg. Med. Chem. Lett. 5: 1701–1706CrossRefGoogle Scholar
  73. 72.
    Zhang FJ and Sih CJ. 1996. Novel analogs of cyclic-ADP-ribose - 9-cyclic etheno-ADP-ribose and cyclic etheno-CDP-ribose. Bioorg. Med. Chem. Lett. 6: 2311–2316.CrossRefGoogle Scholar
  74. 73.
    Graeff RM, Mehta K and Lee HC. 1994. GDP-ribosyl cyclase activity as a measure of CD38 induction by retinoic acid in HL-60 cells. Biochem. Biophys. Res. Commun. 205: 722–727.PubMedCrossRefGoogle Scholar
  75. 74.
    Graeff RM, Franco L, Deflora A and Lee HC. 1998. Cyclic GMP-dependent and -independent effects on the synthesis of the calcium messengers cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate. J. Biol. Chem. 273: 118–125.PubMedCrossRefGoogle Scholar
  76. 75.
    Li NJ, Teggatz EG, Li PL, Allaire R and Zou AP. 2000. Formation and actions of cyclic ADP-ribose in renal microvessels. Microvasc. Res. 60: 149–159.PubMedCrossRefGoogle Scholar
  77. 76.
    Liang M, Chini EN, Cheng JF and Dousa TP. 1999. Synthesis of NAADP and cADPR in mitochondria. Arch. Biochem. Biophys. 371: 317–325.PubMedCrossRefGoogle Scholar
  78. 77.
    Looms D, Nauntofte B and Dissing S. 1998. ADP-ribosyl cyclase activity in rat parotid acinar cells. Eur. J. Morphol. 36: 181–185.PubMedGoogle Scholar
  79. 78.
    Masuda W and Noguchi T. 2000. ADP-ribosyl cyclase in rat salivary glands. Biochem. Biophys. Res. Commun. 270: 469–472.PubMedCrossRefGoogle Scholar
  80. 79.
    Matsumura N and Tanuma S. 1998. Involvement of cytosolic NAD+ glycohydrolase in cyclic ADP-ribose metabolism. Biochem.Biophys. Res. Commun. 253: 246–252.PubMedCrossRefGoogle Scholar
  81. 80.
    Ziegler M, Jorcke D and Schweiger M. 1997. Identification of bovine liver mitochondrial NADV glycohydrolase as ADP-ribosyl cyclase. Biochem. J. 326: 401–405.PubMedGoogle Scholar
  82. 81.
    Meszaros LG, Wrenn RW and Varadi G. 1997. Sarcoplasmic reticulum-associated and protein kinase C-regulated ADP-ribosyl cyclase in cardiac muscle. Biochem. Biophys. Res. Commun. 234: 252–256.PubMedCrossRefGoogle Scholar
  83. 82.
    Aarhus R, Gee K and Lee HC. 1995. Caged cyclic ADP-ribose. Synthesis and use. J. Biol. Chem. 270: 7745–7749.PubMedCrossRefGoogle Scholar
  84. 83.
    Guo XQ and Becker PL. 1997. Cyclic ADP-ribose-gated Ca2+ release in sea urchin eggs requires an elevated [Ca2+]. J. Biol. Chem. 272: 16984–16989.PubMedCrossRefGoogle Scholar
  85. 84.
    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
  86. 85.
    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
  87. 86.
    Lokuta AJ, Darszon A, Beltran C and Valdivia HH. 1998. Defection and functional characterization of ryanodine receptors from sea urchin eggs. J. Physiol. London 510: 155–164.PubMedCrossRefGoogle Scholar
  88. 87.
    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 Calcium 22: 11–20.PubMedCrossRefGoogle Scholar
  89. 88.
    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: S190–S201.PubMedCrossRefGoogle Scholar
  90. 89.
    Chini EN, Beers KW and Dousa TP. 1995. Nicotinate adenine dinucleotide phosphate (NAADP) triggers a specific calcium release system in sea urchin eggs. J. Biol. Chem. 270:3216–3223.PubMedCrossRefGoogle Scholar
  91. 90.
    Dickey DM. 1999. Characterization of the nicotinic acid adenine dinucleotide phosphate binding protein. Ph.D. thesis. University of Minnesota, Minneapolis. 228 pp.Google Scholar
  92. 91.
    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. 92.
    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
  94. 93.
    Dickey DM, Aarhus R, Walseth TF and Lee HC. 1997. Thio-NADP is not an antagonist of NAADP. Cell Biochem. Biophys. 28: 63–73.CrossRefGoogle Scholar
  95. 94.
    Genazzani AA, Empson R and Galione A. 1996. Unique activation properties of NAADP-induced Ca2+ release. J. Biol. Chem. 271: 11599–11602.PubMedCrossRefGoogle Scholar
  96. 95.
    Churchill GC and Galione A. 2000. Spatial control of Ca 2+ signaling by nicotinic acid adenine dinucleotide phosphate diffusion and gradients. J. Biol. Chem. 275: 38687–38692.PubMedCrossRefGoogle Scholar
  97. 96.
    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
  98. 97.
    Lee HC. 2000. NAADP: An emerging calcium signaling molecule. J. Membr. Biol. 173: 1–8.PubMedCrossRefGoogle Scholar
  99. 98.
    Low A, Faulhammer HG and Sprinzl M. 1992. Affinity labeling of GTP-binding proteins in cellular extracts. FEBS Lett. 303: 64–68.PubMedCrossRefGoogle Scholar
  100. 99.
    Low A, Sprinzl M and Faulhammer HG. 1993. Affinity labeling of c-H-ras p21 consensus elements with periodate-oxidized GDP and GTP. Eur. J. Biochem. 215: 473–479.PubMedCrossRefGoogle Scholar
  101. 100.
    Peter ME, She J, Huber LA and Terhorst C. 1993. Labeling of adenine and guanine nucleotide-binding proteins in permeabilized cells with in situ periodate-oxidized nucleotides. Anal. Biochem. 210: 77–85.PubMedCrossRefGoogle Scholar
  102. 101.
    Hohenegger M, Herrmann-Frank A, Richter M and Lehmann-Horn F. 1995. Activation and labelling of the purified skeletal muscle ryanodine receptor by an oxidized ATP analogue. J. Biol. Chem. 268: 293–299.Google Scholar
  103. 102.
    Yee L. 2002. Characterization of Nicotinic Acid Adenine Dinucleotide Phosphate Signaling System. Masters thesis. University of Minnesota, Minneapolis. 113 pp.Google Scholar

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© Springer Science+Business Media New York 2002

Authors and Affiliations

  1. 1.Department of PharmacologyUniversity of MinnesotaMinneapolisUSA

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