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Pyridine Nucleotide Metabolites and Calcium Release from Intracellular Stores

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Calcium Signaling

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1131))

Abstract

Ca2+ signals are probably the most common intracellular signaling cellular events, controlling an extensive range of responses in virtually all cells. Many cellular stimuli, often acting at cell surface receptors, evoke Ca2+ signals by mobilizing Ca2+ from intracellular stores. Inositol trisphosphate (IP3) was the first messenger shown to link events at the plasma membrane to release Ca2+ from the endoplasmic reticulum (ER), through the activation of IP3-gated Ca2+ release channels (IP3 receptors). Subsequently, two additional Ca2+ mobilizing messengers were discovered, cADPR and NAADP. Both are metabolites of pyridine nucleotides, and may be produced by the same class of enzymes, ADP-ribosyl cyclases, such as CD38. Whilst cADPR mobilizes Ca2+ from the ER by activation of ryanodine receptors (RyRs), NAADP releases Ca2+ from acidic stores by a mechanism involving the activation of two pore channels (TPCs). In addition, other pyridine nucleotides have emerged as intracellular messengers. ADP-ribose and 2′-deoxy-ADPR both activate TRPM2 channels which are expressed at the plasma membrane and in lysosomes.

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References

  1. Ringer S (1882) Concerning the influence exerted by each of the constituents of the blood on the contraction of the ventricle. J Physiol 3:380–393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ashley CC, Ridgway EB (1968) Simultaneous recording of membrane potential, calcium transient and tension in single muscle fibers. Nature 219:1168–1169

    Article  CAS  PubMed  Google Scholar 

  3. Douglas WW, Poisner AM (1964) Stimulus-secretion coupling in a neurosecretory organ: the role of calcium in the release of vasopressin from the neurohypophysis. J Physiol 172:1–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Nielsen SP, Petersen OH (1972) Transport of calcium in the perfused submandibular gland of the cat. J Physiol 223:685–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Michell RH (1975) Inositol phospholipids and cell surface receptor function. Biochim Biophys Acta 415:81–47

    Article  CAS  PubMed  Google Scholar 

  6. Berridge MJ (1983) Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem J 212:849–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. Supattapone S, Worley PF, Baraban JM, Snyder SH (1988) Solubilization, purification, and characterization of an inositol trisphosphate receptor. J Biol Chem 263:1530–1534

    CAS  PubMed  Google Scholar 

  9. Maeda N, Niinobe M, Mikoshiba K (1990) A cerebellar Purkinje cell marker P400 protein is an inositol 1,4,5-trisphosphate (InsP3) receptor protein. Purification and characterization of InsP3 receptor complex. Embo J 9:61–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Furuichi T, Yoshikawa S, Miyawaki A, Wada K, Maeda N, Mikoshiba K (1989) Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400. Nature 342:32–38

    Article  CAS  PubMed  Google Scholar 

  11. Mignery GA, Sudhof TC, Takei K, De Camilli P (1989) Putative receptor for inositol 1,4,5-trisphosphate similar to ryanodine receptor. Nature 342:192–195

    Article  CAS  PubMed  Google Scholar 

  12. Serysheva II, Baker MR, Fan G (2017) Structural Insights into IP3R Function. Adv Exp Med Biol 981:121–147

    Article  CAS  PubMed  Google Scholar 

  13. Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361: 315–325

    Article  CAS  PubMed  Google Scholar 

  14. Whitaker M, Irvine RF (1984) Inositol 1,4,5 trisphosphate microinjection activates sea urchin eggs. Nature 312:636–639

    Article  CAS  Google Scholar 

  15. Clapper DL, Lee HC (1985) Inositol trisphosphate induces calcium release from nonmitochondrial stores i sea urchin egg homogenates. J Biol Chem 260:13947–13954

    CAS  PubMed  Google Scholar 

  16. Clapper DL, Walseth TF, Dargie PJ, Lee HC (1987) Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J Biol Chem 262:9561–9568

    CAS  PubMed  Google Scholar 

  17. Lee HC, Walseth TF, Bratt GT, Hayes RN, Clapper DL (1989) Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2+-mobilizing activity. J Biol Chem 264:1608–1615

    CAS  PubMed  Google Scholar 

  18. Lee HC, Aarhus R (1995) A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP-ribose. J Biol Chem 270:2152–2157

    Article  CAS  PubMed  Google Scholar 

  19. Rusinko N, 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

    CAS  PubMed  Google Scholar 

  20. Hellmich MR, Strumwasser F (1991) Purification and characterization of a molluscan egg-specific NADase, a second-messenger enzyme. Cell Regul 2:193–202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Glick DL, Hellmich MR, Beushausen S, Tempst P, Bayley H, Strumwasser F (1991) Primary structure of a molluscan egg-specific NADase, a second-messenger enzyme. Cell Regul 2:211–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lee HC, Aarhus R (1991) ADP-ribosyl cyclase: an enzyme that cyclizes NAD+ into a calcium-mobilizing metabolite. Cell Regul 2:203–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Malavasi F, Deaglio S, Funaro A, Ferrero E, Horenstein AL, Ortolan E et al (2008) Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol Rev 88:841–886

    Article  CAS  PubMed  Google Scholar 

  24. Chini EN, Chini CCS, Espindola Netto JM, de Oliveira GC, van Schooten W (2018) The pharmacology of CD38/NADase: an emerging target in cancer and diseases of aging. Trends Pharmacol Sci 39:424–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Howard M, Grimaldi JC, Bazan JF, Lund FE, Santos-Argumedo L, Parkhouse RM et al (1993) Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38. Science 262:1056–1059

    Article  CAS  PubMed  Google Scholar 

  26. Aarhus R, Graeff RM, Dickey DM, Walseth TF, Lee HC (1995) ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. J Biol Chem 270:30327–30333

    Article  CAS  PubMed  Google Scholar 

  27. Graeff R, Liu Q, Kriksunov IA, Hao Q, Lee HC (2006) Acidic residues at the active sites of CD38 and ADP-ribosyl cyclase determine nicotinic acid adenine dinucleotide phosphate (NAADP) synthesis and hydrolysis activities. J Biol Chem 281:28951–28957

    Article  CAS  PubMed  Google Scholar 

  28. Berridge G, Cramer R, Galione A, Patel S (2002) Metabolism of the novel Ca2+-mobilizing messenger nicotinic acid-adenine dinucleotide phosphate via a 2′-specific Ca22+-dependent phosphatase. Biochem J 365:295–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lee HC (2000) Enzymatic functions and structures of CD38 and homologs. Chem Immunol 75:39–59

    Article  CAS  PubMed  Google Scholar 

  30. Churamani D, Boulware MJ, Geach TJ, Martin AC, Moy GW, Su YH et al (2007) Molecular characterization of a novel intracellular ADP-ribosyl cyclase. PLoS One 2:e797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Davis LC, Morgan AJ, Ruas M, Wong JL, Graeff RM, Poustka AJ et al (2008) Ca2+ signaling occurs via second messenger release from intraorganelle synthesis sites. Curr Biol 18:1612–1618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Churamani D, Boulware MJ, Ramakrishnan L, Geach TJ, Martin AC, Vacquier VD et al (2008) Molecular characterization of a novel cell surface ADP-ribosyl cyclase from the sea urchin. Cell Signal 20:2347–2355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ramakrishnan L, Muller-Steffner H, Bosc C, Vacquier VD, Schuber F, Moutin MJ et al (2010) A single residue in a novel ADP-ribosyl cyclase controls production of the calcium-mobilizing messengers cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate. J Biol Chem 285:19900–19909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Galione A, Lee HC, Busa WB (1991) Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253:1143–1146

    Article  CAS  PubMed  Google Scholar 

  35. Galione A, Churchill GC (2000) Cyclic ADP ribose as a calcium-mobilizing messenger. Sci STKE 2000:pe1

    CAS  PubMed  Google Scholar 

  36. Fill M, Copello JA (2002) Ryanodine receptor calcium release channels. Physiol Rev 82:893–922

    Article  CAS  PubMed  Google Scholar 

  37. McPherson SM, McPherson PS, Mathews L, Campbell KP, Longo FJ (1992) Cortical localization of a calcium release channel in sea urchin eggs. J Cell Biol 116:1111–1121

    Article  CAS  PubMed  Google Scholar 

  38. Lokuta AJ, Darszon A, Beltran C, Valdivia HH (1998) Detection and functional characterization of ryanodine receptors from sea urchin eggs. J Physiol 510:155–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Shiwa M, Murayama T, Ogawa Y (2002) Molecular cloning and characterization of ryanodine receptor from unfertilized sea urchin eggs. Am J Physiol Regul Integr Comp Physiol 282:R727–R737

    Article  CAS  PubMed  Google Scholar 

  40. Taylor CW (1998) Inositol trisphosphate receptors: Ca2+-modulated intracellular Ca2+ channels. Biochim Biophys Acta 1436:19–33

    Article  CAS  PubMed  Google Scholar 

  41. Roderick HL, Berridge MJ, Bootman MD (2003) Calcium-induced calcium release. Curr Biol 13:R425

    Article  CAS  PubMed  Google Scholar 

  42. Lee HC (1993) Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J Biol Chem 268:293–299

    CAS  PubMed  Google Scholar 

  43. Parys JB, De Smedt H (2012) Inositol 1,4,5-trisphosphate and its receptors. Adv Exp Med Biol 740:255–279

    Article  CAS  PubMed  Google Scholar 

  44. Lee HC, Aarhus R, Graeff RM (1995) Sensitization of calcium-induced calcium release by cyclic ADP-ribose and calmodulin. J Biol Chem 270:9060–9066

    Article  CAS  PubMed  Google Scholar 

  45. Zhu X, Ghanta J, Walker JW, Allen PD, Valdivia HH (2004) The calmodulin binding region of the skeletal ryanodine receptor acts as a self-modulatory domain. Cell Calcium 35: 165–177

    Article  CAS  PubMed  Google Scholar 

  46. Thomas JM, Summerhill RJ, Fruen BR, Churchill GC, Galione A (2002) Calmodulin dissociation mediates desensitization of the cADPR-induced Ca2+ release mechanism. Curr Biol 12:2018–2022

    Article  CAS  PubMed  Google Scholar 

  47. Morita K, Kitayama T, Kitayama S, Dohi T (2006) Cyclic ADP-ribose requires FK506-binding protein to regulate intracellular Ca2+ dynamics and catecholamine release in acetylcholine-stimulated bovine adrenal chromaffin cells. J Pharmacol Sci 101:40–51

    Article  CAS  PubMed  Google Scholar 

  48. Noguchi N, Takasawa S, Nata K, Tohgo A, Kato I, Ikehata F et al (1997) Cyclic ADP-ribose binds to FK506-binding protein 12.6 to release Ca2+ from islet microsomes. J Biol Chem 272:3133–3136

    Article  CAS  PubMed  Google Scholar 

  49. Tang WX, Chen YF, Zou AP, Campbell WB, Li PL (2002) Role of FKBP12.6 in cADPR-induced activation of reconstituted ryanodine receptors from arterial smooth muscle. Am J Physiol Heart Circ Physiol 282:H1304–H1310

    Article  CAS  PubMed  Google Scholar 

  50. Wang YX, Zheng YM, Mei QB, Wang QS, Collier ML, Fleischer S et al (2004) FKBP12.6 and cADPR regulation of Ca2+ release in smooth muscle cells. Am J Physiol Cell Physiol 286:C538–C546

    Article  CAS  PubMed  Google Scholar 

  51. Zhang X, Tallini YN, Chen Z, Gan L, Wei B, Doran R et al (2009) Dissociation of FKBP12.6 from ryanodine receptor type 2 is regulated by cyclic ADP-ribose but not beta-adrenergic stimulation in mouse cardiomyocytes. Cardiovasc Res 84:253–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Zheng J, Wenzhi B, Miao L, Hao Y, Zhang X, Yin W et al (2010) Ca2+ release induced by cADP-ribose is mediated by FKBP12.6 proteins in mouse bladder smooth muscle. Cell Calcium 47:449–457

    Article  CAS  PubMed  Google Scholar 

  53. Copello JA, Qi Y, Jeyakumar LH, Ogunbunmi E, Fleischer S (2001) Lack of effect of cADP-ribose and NAADP on the activity of skeletal muscle and heart ryanodine receptors. Cell Calcium 30:269–284

    Article  CAS  PubMed  Google Scholar 

  54. Zhang K, Sun W, Huang L, Zhu K, Pei F, Zhu L et al (2017) Identifying glyceraldehyde 3-phosphate dehydrogenase as a cyclic adenosine diphosphoribose binding protein by photoaffinity protein-ligand labeling approach. J Am Chem Soc 139:156–170

    Article  CAS  PubMed  Google Scholar 

  55. Walseth TF, Lee HC (1993) Synthesis and characterization of antagonists of cyclic-ADP-ribose-induced Ca2+ release. Biochim Biophys Acta 1178:235–242

    Article  CAS  PubMed  Google Scholar 

  56. Sethi JK, Empson RM, Bailey VC, Potter BV, 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

    Article  CAS  PubMed  Google Scholar 

  57. Lukyanenko V, Gyorke I, Wiesner TF, Gyorke S (2001) Potentiation of Ca2+ release by cADP-ribose in the heart is mediated by enhanced SR Ca2+ uptake into the sarcoplasmic reticulum. Circ Res 89:614–622

    Article  CAS  PubMed  Google Scholar 

  58. Yamasaki-Mann M, Demuro A, Parker I (2009) cADPR stimulates SERCA activity in Xenopus oocytes. Cell Calcium 45:293–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Guse AH, Lee HC (2008) NAADP: a universal Ca2+ trigger. Sci Signal 1:re10

    Article  CAS  PubMed  Google Scholar 

  60. Galione A (2015) A primer of NAADP-mediated Ca2+ signalling: from sea urchin eggs to mammalian cells. Cell Calcium 58:27–47

    Article  CAS  PubMed  Google Scholar 

  61. Genazzani AA, Mezna M, Summerhill RJ, Galione A, Michelangeli F (1997) Kinetic properties of nicotinic acid adenine dinucleotide phosphate-induced Ca2+ release. J Biol Chem 272:7669–7675

    Article  CAS  PubMed  Google Scholar 

  62. Genazzani AA, Mezna M, Dickey DM, Michelangeli F, Walseth TF, Galione A (1997) Pharmacological properties of the Ca2+-release mechanism sensitive to NAADP in the sea urchin egg. Br J Pharmacol 121:1489–1495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Chini EN, Dousa TP (1996) Nicotinate-adenine dinucleotide phosphate-induced Ca2+-release does not behave as a Ca2+-induced Ca2+-release system. Biochem J 316:709–711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Genazzani AA, Galione A (1996) Nicotinic acid-adenine dinucleotide phosphate mobilizes Ca2+ from a thapsigargin-insensitive pool. Biochem J 315:721–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Lee HC, 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

    CAS  PubMed  Google Scholar 

  66. Aarhus R, Dickey DM, Graeff RM, Gee KR, Walseth TF, Lee HC (1996) Activation and inactivation of Ca2+ release by NAADP+. J Biol Chem 271:8513–8516

    Article  CAS  PubMed  Google Scholar 

  67. Churchill GC, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Churchill GC, Okada Y, Thomas JM, Genazzani AA, Patel S, Galione A (2002) NAADP mobilizes Ca2+ from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 111:703–708

    Article  CAS  PubMed  Google Scholar 

  69. Morgan AJ, Platt FM, Lloyd-Evans E, Galione A (2011) Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease. Biochem J 439:349–374

    Article  CAS  PubMed  Google Scholar 

  70. Lee HC (2012) Cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate (NAADP) as messengers for calcium mobilization. J Biol Chem 287:31633–31640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Cancela JM, Churchill GC, Galione A (1999) Coordination of agonist-induced Ca2+-signalling patterns by NAADP in pancreatic acinar cells. Nature 398:74–76

    Article  CAS  PubMed  Google Scholar 

  72. Naylor E, Arredouani A, Vasudevan SR, Lewis AM, Parkesh R, Mizote A et al (2009) Identification of a chemical probe for NAADP by virtual screening. Nat Chem Biol 5:220–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Patel S, Churchill GC, Galione A (2001) Coordination of Ca2+ signalling by NAADP. Trends Biochem Sci 26:482–489

    Article  CAS  PubMed  Google Scholar 

  74. Kilpatrick BS, Yates E, Grimm C, Schapira AH, Patel S (2016) Endo-lysosomal TRP mucolipin-1 channels trigger global ER Ca2+ release and Ca2+ influx. J Cell Sci 129:3859–3867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Galione A, Morgan AJ, Arredouani A, Davis LC, Rietdorf K, Ruas M et al (2010) NAADP as an intracellular messenger regulating lysosomal calcium-release channels. Biochem Soc Trans 38:1424–1431

    Article  CAS  PubMed  Google Scholar 

  76. Menteyne A, Burdakov A, Charpentier G, Petersen OH, Cancela JM (2006) Generation of specific Ca2+ signals from Ca2+ stores and endocytosis by differential coupling to messengers. Curr Biol 16:1931–1937

    Article  CAS  PubMed  Google Scholar 

  77. Melchionda M, Pittman JK, Mayor R, Patel S (2016) Ca2+/H+ exchange by acidic organelles regulates cell migration in vivo. J Cell Biol 212:803–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Jardin I, Lopez JJ, Pariente JA, Salido GM, Rosado JA (2008) Intracellular calcium release from human platelets: different messengers for multiple stores. Trends Cardiovasc Med 18:57–61

    Article  CAS  PubMed  Google Scholar 

  79. Garrity AG, Wang W, Collier CM, Levey SA, Gao Q, Xu H (2016) The endoplasmic reticulum, not the pH gradient, drives calcium refilling of lysosomes. Elife 5

    Google Scholar 

  80. Lloyd-Evans E, Morgan AJ, He X, Smith DA, Elliot-Smith E, Sillence DJ et al (2008) Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat Med 14:1247–1255

    Article  CAS  PubMed  Google Scholar 

  81. Hoglinger D, Haberkant P, Aguilera-Romero A, Riezman H, Porter FD, Platt FM et al (2015) Intracellular sphingosine releases calcium from lysosomes. Elife 4

    Google Scholar 

  82. Billington RA, Genazzani AA (2000) Characterization of NAADP+ binding in sea urchin eggs. Biochem Biophys Res Commun 276:112–116

    Article  CAS  PubMed  Google Scholar 

  83. Patel S, Churchill GC, Galione A (2000) Unique kinetics of nicotinic acid-adenine dinucleotide phosphate (NAADP) binding enhance the sensitivity of NAADP receptors for their ligand. Biochem J 352:725–729

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Dickinson GD, Patel S (2003) Modulation of NAADP (nicotinic acid-adenine dinucleotide phosphate) receptors by K2+ ions: evidence for multiple NAADP receptor conformations. Biochem J 375:805–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Churamani D, Dickinson GD, Patel S (2005) NAADP binding to its target protein in sea urchin eggs requires phospholipids. Biochem J 386:497–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Berridge G, Dickinson G, Parrington J, Galione A, Patel S (2002) Solubilization of receptors for the novel Ca2+-mobilizing messenger, nicotinic acid adenine dinucleotide phosphate. J Biol Chem 277:43717–43723

    Article  CAS  PubMed  Google Scholar 

  87. Churamani D, Dickinson GD, Ziegler M, Patel S (2006) Time sensing by NAADP receptors. Biochem J 397:313–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Genazzani AA, Empson RM, Galione A (1996) Unique inactivation properties of NAADP-sensitive Ca2+ release. J Biol Chem 271:11599–11602

    Article  CAS  PubMed  Google Scholar 

  89. Churchill GC, 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

    Article  CAS  PubMed  Google Scholar 

  90. Bargal R, Avidan N, Ben-Asher E, Olender Z, Zeigler M, Frumkin A et al (2000) Identification of the gene causing mucolipidosis type IV. Nat Genet 26:118–123

    Article  CAS  PubMed  Google Scholar 

  91. Sun M, Goldin E, Stahl S, Falardeau JL, Kennedy JC, Acierno JS Jr et al (2000) Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum Mol Genet 9:2471–2478

    Article  CAS  PubMed  Google Scholar 

  92. Bach G (2001) Mucolipidosis type IV. Mol Genet Metab 73:197–203

    Article  CAS  PubMed  Google Scholar 

  93. Galione A, Evans AM, Ma J, Parrington J, Arredouani A, Cheng X et al (2009) The acid test: the discovery of two-pore channels (TPCs) as NAADP-gated endolysosomal Ca2+ release channels. Pflugers Arch 458:869–876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Zhu MX, Ma J, Parrington J, Calcraft PJ, Galione A, Evans AM (2010) Calcium signaling via two-pore channels: local or global, that is the question. Am J Physiol Cell Physiol 298:C430–C441

    Article  CAS  PubMed  Google Scholar 

  95. Cai X, Patel S (2010) Degeneration of an intracellular ion channel in the primate lineage by relaxation of selective constraints. Mol Biol Evol 27:2352–2359

    Article  CAS  PubMed  Google Scholar 

  96. Rahman T, Cai X, Brailoiu GC, Abood ME, Brailoiu E, Patel S (2014) Two-pore channels provide insight into the evolution of voltage-gated Ca2+ and Na+ channels. Sci Signal 7:ra109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Ishibashi K, Suzuki M, Imai M (2000) Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochem Biophys Res Commun 270:370–376

    Article  CAS  PubMed  Google Scholar 

  98. Furuichi T, Cunningham KW, Muto S (2001) A putative two pore channel AtTPC1 mediates Ca2+ flux in Arabidopsis leaf cells. Plant Cell Physiol 42:900–905

    Article  CAS  PubMed  Google Scholar 

  99. Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM et al (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408

    Article  CAS  PubMed  Google Scholar 

  100. Hedrich R, Marten I (2011) TPC1-SV channels gain shape. Mol Plant 4:428–441

    Article  CAS  PubMed  Google Scholar 

  101. Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X et al (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459:596–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Zhang F, Li PL (2007) Reconstitution and characterization of a nicotinic acid adenine dinucleotide phosphate (NAADP)-sensitive Ca2+ release channel from liver lysosomes of rats. J Biol Chem 282:25259–25269

    Article  CAS  PubMed  Google Scholar 

  103. Pryor PR, Reimann F, Gribble FM, Luzio JP (2006) Mucolipin-1 is a lysosomal membrane protein required for intracellular lactosylceramide traffic. Traffic 7:1388–1398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Yamaguchi S, Jha A, Li Q, Soyombo AA, Dickinson GD, Churamani D et al (2011) Transient receptor potential mucolipin 1 (TRPML1) and two-pore channels are functionally independent organellar ion channels. J Biol Chem 286:22934–22942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Zong X, Schieder M, Cuny H, Fenske S, Gruner C, Rotzer K et al (2009) The two-pore channel TPCN2 mediates NAADP-dependent Ca2+-release from lysosomal stores. Pflugers Arch 458:891–899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Brailoiu E, Churamani D, Cai X, Schrlau MG, Brailoiu GC, Gao X et al (2009) Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J Cell Biol 186:201–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Kinnear NP, Boittin FX, Thomas JM, Galione A, Evans AM (2004) Lysosome-sarcoplasmic reticulum junctions. A trigger zone for calcium signaling by nicotinic acid adenine dinucleotide phosphate and endothelin-1. J Biol Chem 279:54319–54326

    Article  CAS  PubMed  Google Scholar 

  108. Kinnear NP, Wyatt CN, Clark JH, Calcraft PJ, Fleischer S, Jeyakumar LH et al (2008) Lysosomes co-localize with ryanodine receptor subtype 3 to form a trigger zone for calcium signalling by NAADP in rat pulmonary arterial smooth muscle. Cell Calcium 44:190–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Ogunbayo OA, Zhu Y, Rossi D, Sorrentino V, Ma J, Zhu MX et al (2011) Cyclic adenosine diphosphate ribose activates ryanodine receptors, whereas NAADP activates two-pore domain channels. J Biol Chem 286:9136–9140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Ruas M, Rietdorf K, Arredouani A, Davis LC, Lloyd-Evans E, Koegel H et al (2010) Purified TPC isoforms form NAADP receptors with distinct roles for Ca2+ signaling and endolysosomal trafficking. Curr Biol 20:703–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Brailoiu E, Hooper R, Cai X, Brailoiu GC, Keebler MV, Dun NJ et al (2010) An ancestral deuterostome family of two-pore channels mediates nicotinic acid adenine dinucleotide phosphate-dependent calcium release from acidic organelles. J Biol Chem 285:2897–2901

    Article  CAS  PubMed  Google Scholar 

  112. Schieder M, Rotzer K, Bruggemann A, Biel M, Wahl-Schott CA (2010) Characterization of two-pore channel 2 (TPCN2)-mediated Ca2+ currents in isolated lysosomes. J Biol Chem 285:21219–21222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Jha A, Ahuja M, Patel S, Brailoiu E, Muallem S (2014) Convergent regulation of the lysosomal two-pore channel-2 by Mg2+, NAADP, PI(3,5)P2 and multiple protein kinases. Embo J 33:501–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Pitt SJ, Funnell TM, Sitsapesan M, Venturi E, Rietdorf K, Ruas M et al (2010) TPC2 is a novel NAADP-sensitive Ca2+ release channel, operating as a dual sensor of luminal pH and Ca2+. J Biol Chem 285:35039–35046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Brailoiu E, Rahman T, Churamani D, Prole DL, Brailoiu GC, Hooper R et al (2010) An NAADP-gated two-pore channel targeted to the plasma membrane uncouples triggering from amplifying Ca2+ signals. J Biol Chem 285:38511–38516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Arredouani A, Ruas M, Collins SC, Parkesh R, Clough F, Pillinger T et al (2015) Nicotinic Acid Adenine Dinucleotide Phosphate (NAADP) and endolysosomal two-pore channels modulate membrane excitability and stimulus-secretion coupling in mouse pancreatic beta cells. J Biol Chem 290:21376–21392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Park KH, Kim BJ, Shawl AI, Han MK, Lee HC, Kim UH (2013) Autocrine/paracrine function of nicotinic acid adenine dinucleotide phosphate (NAADP) for glucose homeostasis in pancreatic beta-cells and adipocytes. J Biol Chem 288:35548–35558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Tugba Durlu-Kandilci N, Ruas M, Chuang KT, Brading A, Parrington J, Galione A (2010) TPC2 proteins mediate nicotinic acid adenine dinucleotide phosphate (NAADP)- and agonist-evoked contractions of smooth muscle. J Biol Chem 285:24925–24932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Aley PK, Mikolajczyk AM, Munz B, Churchill GC, Galione A, Berger F (2010) Nicotinic acid adenine dinucleotide phosphate regulates skeletal muscle differentiation via action at two-pore channels. Proc Natl Acad Sci USA 107:19927–19932

    Article  PubMed  PubMed Central  Google Scholar 

  120. Ruas M, Davis LC, Chen CC, Morgan AJ, Chuang KT, Walseth TF et al (2015) Expression of Ca2+-permeable two-pore channels rescues NAADP signalling in TPC-deficient cells. Embo J 34:1743–1758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Wang X, Zhang X, Dong XP, Samie M, Li X, Cheng X et al (2012) TPC proteins are phosphoinositide- activated sodium-selective ion channels in endosomes and lysosomes. Cell 151:372–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Guo J, Zeng W, Chen Q, Lee C, Chen L, Yang Y et al (2016) Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. Nature 531:196–201

    Article  CAS  PubMed  Google Scholar 

  123. Hedrich R, Mueller TD, Becker D, Marten I (2018) Structure and function of TPC1 vacuole SV channel gains shape. Mol Plant 11:764–775

    Article  CAS  PubMed  Google Scholar 

  124. Kintzer AF, Stroud RM (2016) Structure, inhibition and regulation of two-pore channel TPC1 from Arabidopsis thaliana. Nature 531:258–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Kintzer AF, Stroud RM (2018) On the structure and mechanism of two-pore channels. Febs J 285:233–243

    Article  CAS  PubMed  Google Scholar 

  126. Patel S, Penny CJ, Rahman T (2016) Two-pore channels enter the atomic era: structure of plant TPC revealed. Trends Biochem Sci 41:475–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Grimm C, Butz E, Chen CC, Wahl-Schott C, Biel M (2017) From mucolipidosis type IV to Ebola: TRPML and two-pore channels at the crossroads of endo-lysosomal trafficking and disease. Cell Calcium 67:148–155

    Article  CAS  PubMed  Google Scholar 

  128. Patel S, Kilpatrick BS (2018) Two-pore channels and disease. Biochim Biophys Acta Mol Cell Res 1865:1678–1686

    Article  CAS  PubMed  Google Scholar 

  129. Gerasimenko JV, Maruyama Y, Yano K, Dolman NJ, Tepikin AV, Petersen OH et al (2003) NAADP mobilizes Ca2+ from a thapsigargin-sensitive store in the nuclear envelope by activating ryanodine receptors. J Cell Biol 163:271–282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Dammermann W, Guse AH (2005) Functional ryanodine receptor expression is required for NAADP-mediated local Ca2+ signaling in T-lymphocytes. J Biol Chem 280:21394–21399

    Article  CAS  PubMed  Google Scholar 

  131. Lin-Moshier Y, Walseth TF, Churamani D, Davidson SM, Slama JT, Hooper R et al (2012) Photoaffinity labeling of nicotinic acid adenine dinucleotide phosphate (NAADP) targets in mammalian cells. J Biol Chem 287:2296–2307

    Article  CAS  PubMed  Google Scholar 

  132. Walseth TF, Lin-Moshier Y, Jain P, Ruas M, Parrington J, Galione A et al (2012) Photoaffinity labeling of high affinity nicotinic acid adenine dinucleotide phosphate (NAADP)-binding proteins in sea urchin egg. J Biol Chem 287:2308–2315

    Article  CAS  PubMed  Google Scholar 

  133. Galione A, Petersen OH (2005) The NAADP receptor: new receptors or new regulation? Mol Interv 5:73–79

    Article  CAS  PubMed  Google Scholar 

  134. Guse AH, Diercks BP (2018) Integration of nicotinic acid adenine dinucleotide phosphate (NAADP)-dependent calcium signalling. J Physiol 596:2735–2743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Galione A (2011) NAADP receptors. Cold Spring Harb Perspect Biol 3:a004036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Morgan AJ, Davis LC, Wagner SK, Lewis AM, Parrington J, Churchill GC et al (2013) Bidirectional Ca2+ signaling occurs between the endoplasmic reticulum and acidic organelles. J Cell Biol 200:789–805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Kilpatrick BS, Eden ER, Schapira AH, Futter CE, Patel S (2013) Direct mobilisation of lysosomal Ca2+ triggers complex Ca2+ signals. J Cell Sci 126:60–66

    Article  CAS  PubMed  Google Scholar 

  138. Kilpatrick BS, Eden ER, Hockey LN, Yates E, Futter CE, Patel S (2017) An endosomal NAADP-sensitive two-pore Ca2+ channel regulates ER-endosome membrane contact sites to control growth factor signaling. Cell Rep 18:1636–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Churchill GC, O’Neill JS, Masgrau R, Patel S, Thomas JM, Genazzani AA et al (2003) Sperm deliver a new second messenger: NAADP. Curr Biol 13:125–128

    Article  CAS  PubMed  Google Scholar 

  140. Moccia F, Lim D, Kyozuka K, Santella L (2004) NAADP triggers the fertilization potential in starfish oocytes. Cell Calcium 36:515–524

    Article  CAS  PubMed  Google Scholar 

  141. Brailoiu GC, Brailoiu E, Parkesh R, Galione A, Churchill GC, Patel S et al (2009) NAADP-mediated channel ‘chatter’ in neurons of the rat medulla oblongata. Biochem J 419:91–97.

    Article  CAS  PubMed  Google Scholar 

  142. Hockey LN, Kilpatrick BS, Eden ER, Lin-Moshier Y, Brailoiu GC, Brailoiu E et al (2015) Dysregulation of lysosomal morphology by pathogenic LRRK2 is corrected by TPC2 inhibition. J Cell Sci 128:232–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Lin-Moshier Y, Keebler MV, Hooper R, Boulware MJ, Liu X, Churamani D et al (2014) The Two-Pore Channel (TPC) interactome unmasks isoform-specific roles for TPCs in endolysosomal morphology and cell pigmentation. Proc Natl Acad Sci USA 111:13087–13092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Wilding M, Russo GL, Galione A, Marino M, Dale B (1998) ADP-ribose gates the fertilization channel in ascidian oocytes. Am J Physiol 275:C1277–C1283

    Article  CAS  PubMed  Google Scholar 

  145. Sumoza-Toledo A, Penner R (2011) TRPM2: a multifunctional ion channel for calcium signalling. J Physiol 589:1515–1525

    Article  CAS  PubMed  Google Scholar 

  146. Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, Schmitz C et al (2001) ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 411:595–599

    Article  CAS  PubMed  Google Scholar 

  147. Iordanov I, Mihalyi C, Toth B, Csanady L (2016) The proposed channel-enzyme transient receptor potential melastatin 2 does not possess ADP ribose hydrolase activity. Elife 5: e17600

    Google Scholar 

  148. Beck A, Kolisek M, Bagley LA, Fleig A, Penner R (2006) Nicotinic acid adenine dinucleotide phosphate and cyclic ADP-ribose regulate TRPM2 channels in T lymphocytes. FASEB J 20:962–964

    Article  CAS  PubMed  Google Scholar 

  149. Toth B, Iordanov I, Csanady L (2015) Ruling out pyridine dinucleotides as true TRPM2 channel activators reveals novel direct agonist ADP-ribose-2′-phosphate. J Gen Physiol 145:419–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Gasser A, Glassmeier G, Fliegert R, Langhorst MF, Meinke S, Hein D et al (2006) Activation of T cell calcium influx by the second messenger ADP-ribose. J Biol Chem 281:2489–2496

    Article  CAS  PubMed  Google Scholar 

  151. Lange I, Yamamoto S, Partida-Sanchez S, Mori Y, Fleig A, Penner R (2009) TRPM2 functions as a lysosomal Ca2+-release channel in beta cells. Sci Signal 2:ra23

    Article  PubMed  PubMed Central  Google Scholar 

  152. Basile G, Taglialatela-Scafati O, Damonte G, Armirotti A, Bruzzone S, Guida L et al (2005) ADP-ribosyl cyclases generate two unusual adenine homodinucleotides with cytotoxic activity on mammalian cells. Proc Natl Acad Sci USA 102:14509–14514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Fliegert R, Bauche A, Wolf Perez AM, Watt JM, Rozewitz MD, Winzer R et al (2017) 2′-Deoxyadenosine 5′-diphosphoribose is an endogenous TRPM2 superagonist. Nat Chem Biol 13:1036–1044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Huang Y, Winkler PA, Sun W, Lu W, Du J (2018) Architecture of the TRPM2 channel and its activation mechanism by ADP-ribose and calcium. Nature 562:145–149

    Article  CAS  PubMed  Google Scholar 

  155. Sutherland EW (1972) Studies on the mechanism of hormone action. Science 177:401–408

    Article  CAS  PubMed  Google Scholar 

  156. Morgan AJ, Galione A (2008) Investigating cADPR and NAADP in intact and broken cell preparations. Methods 46:194–203

    Article  CAS  PubMed  Google Scholar 

  157. Churamani D, Carrey EA, Dickinson GD, Patel S (2004) Determination of cellular nicotinic acid-adenine dinucleotide phosphate (NAADP) levels. Biochem J 380:449–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Lewis AM, Masgrau R, Vasudevan SR, Yamasaki M, O'Neill JS, Garnham C et al (2007) Refinement of a radioreceptor binding assay for nicotinic acid adenine dinucleotide phosphate. Anal Biochem 371:26–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Graeff R, Lee HC (2002) A novel cycling assay for cellular cADP-ribose with nanomolar sensitivity. Biochem J 361:379–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Graeff R, Lee HC (2002) A novel cycling assay for nicotinic acid-adenine dinucleotide phosphate with nanomolar sensitivity. Biochem J 367:163–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Graeff RM, Walseth TF, Fryxell K, Branton WD, 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

    CAS  PubMed  Google Scholar 

  162. Galione A, White A, Willmott N, Turner M, Potter BV, Watson SP (1993) cGMP mobilizes intracellular Ca2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature 365:456–459

    Article  CAS  PubMed  Google Scholar 

  163. Graeff RM, Franco L, De Flora A, 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

    Article  CAS  PubMed  Google Scholar 

  164. Kim BJ, Park KH, Yim CY, Takasawa S, Okamoto H, Im MJ et al (2008) Generation of nicotinic acid adenine dinucleotide phosphate and cyclic ADP-ribose by glucagon-like peptide-1 evokes Ca2+ signal that is essential for insulin secretion in mouse pancreatic islets. Diabetes 57:868–878

    Article  CAS  PubMed  Google Scholar 

  165. Wilson HL, Galione A (1998) Differential regulation of nicotinic acid-adenine dinucleotide phosphate and cADP-ribose production by cAMP and cGMP. Biochem J 331(Pt 3):837–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Yamasaki M, Thomas JM, Churchill GC, Garnham C, Lewis AM, Cancela JM et al (2005) Role of NAADP and cADPR in the induction and maintenance of agonist-evoked Ca2+ spiking in mouse pancreatic acinar cells. Curr Biol 15:874–878

    Article  CAS  PubMed  Google Scholar 

  167. Gasser A, Bruhn S, Guse AH (2006) Second messenger function of nicotinic acid adenine dinucleotide phosphate revealed by an improved enzymatic cycling assay. J Biol Chem 281:16906–16913

    Article  CAS  PubMed  Google Scholar 

  168. Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, Love J et al (2007) The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318:1789–1792

    Article  CAS  PubMed  Google Scholar 

  169. Kato I, Yamamoto Y, Fujimura M, Noguchi N, Takasawa S, Okamoto H (1999) CD38 disruption impairs glucose-induced increases in cyclic ADP-ribose, [Ca2+]i, and insulin secretion. J Biol Chem 274:1869–1872

    Article  CAS  PubMed  Google Scholar 

  170. Fukushi Y, Kato I, Takasawa S, Sasaki T, Ong BH, Sato M et al (2001) Identification of cyclic ADP-ribose-dependent mechanisms in pancreatic muscarinic Ca2+ signaling using CD38 knockout mice. J Biol Chem 276:649–655

    Article  CAS  PubMed  Google Scholar 

  171. Cosker F, Cheviron N, Yamasaki M, Menteyne A, Lund FE, Moutin MJ et al (2010) The ecto-enzyme CD38 is a nicotinic acid adenine dinucleotide phosphate (NAADP) synthase that couples receptor activation to Ca2+ mobilization from lysosomes in pancreatic acinar cells. J Biol Chem 285:38251–38259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Takahashi J, Kagaya Y, Kato I, Ohta J, Isoyama S, Miura M et al (2003) Deficit of CD38/cyclic ADP-ribose is differentially compensated in hearts by gender. Biochem Biophys Res Commun 312:434–440

    Article  CAS  PubMed  Google Scholar 

  173. Deshpande DA, White TA, Guedes AG, Milla C, Walseth TF, Lund FE et al (2005) Altered airway responsiveness in CD38-deficient mice. Am J Respir Cell Mol Biol 32:149–156

    Article  CAS  PubMed  Google Scholar 

  174. Mitsui-Saito M, Kato I, Takasawa S, Okamoto H, Yanagisawa T (2003) CD38 gene disruption inhibits the contraction induced by alpha-adrenoceptor stimulation in mouse aorta. J Vet Med Sci 65:1325–1330

    Article  CAS  PubMed  Google Scholar 

  175. Partida-Sanchez S, Cockayne DA, Monard S, Jacobson EL, Oppenheimer N, Garvy B 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. Nat Med 7:1209–1216

    Article  CAS  PubMed  Google Scholar 

  176. Jin D, Liu HX, Hirai H, Torashima T, Nagai T, Lopatina O et al (2007) CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446:41–45

    Article  CAS  PubMed  Google Scholar 

  177. Park KH, Kim BJ, Kang J, Nam TS, Lim JM, Kim HT et al (2011) Ca2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal 4:ra31

    Article  CAS  PubMed  Google Scholar 

  178. Kim SY, Cho BH, Kim UH (2010) CD38-mediated Ca2+ signaling contributes to angiotensin II-induced activation of hepatic stellate cells: attenuation of hepatic fibrosis by CD38 ablation. J Biol Chem 285:576–582

    Article  CAS  PubMed  Google Scholar 

  179. Rah SY, Mushtaq M, Nam TS, Kim SH, Kim UH (2010) Generation of cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate by CD38 for Ca2+ signaling in interleukin-8-treated lymphokine-activated killer cells. J Biol Chem 285:21877–21887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Lin WK, Bolton EL, Cortopassi WA, Wang Y, O'Brien F, Maciejewska M et al (2017) Synthesis of the Ca2+-mobilizing messengers NAADP and cADPR by intracellular CD38 enzyme in the mouse heart: role in beta-adrenoceptor signaling. J Biol Chem 292: 13243–13257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Soares S, Thompson M, White T, Isbell A, Yamasaki M, Prakash Y et al (2007) NAADP as a second messenger: neither CD38 nor base-exchange reaction are necessary for in vivo generation of NAADP in myometrial cells. Am J Physiol Cell Physiol 292:C227–C239

    Article  CAS  PubMed  Google Scholar 

  182. Higashida H, Liang M, Yoshihara T, Akther S, Fakhrul A, Stanislav C et al (2017) An immunohistochemical, enzymatic, and behavioral study of CD157/BST-1 as a neuroregulator. BMC Neurosci 18:35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. De Flora A, Guida L, Franco L, Zocchi E (1997) The CD38/cyclic ADP-ribose system: a topological paradox. Int J Biochem Cell Biol 29:1149–1166

    Article  PubMed  Google Scholar 

  184. Lee HC (2011) Cyclic ADP-ribose and NAADP: fraternal twin messengers for calcium signaling. Sci China Life Sci 54(8):699–711

    Article  CAS  PubMed  Google Scholar 

  185. Zhao YJ, Lam CM, Lee HC (2012) The membrane-bound enzyme CD38 exists in two opposing orientations. Sci Signal 5:ra67

    Article  CAS  PubMed  Google Scholar 

  186. Liu J, Zhao YJ, Li WH, Hou YN, Li T, Zhao ZY et al (2017) Cytosolic interaction of type III human CD38 with CIB1 modulates cellular cyclic ADP-ribose levels. Proc Natl Acad Sci USA

    Google Scholar 

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Galione, A., Chuang, KT. (2020). Pyridine Nucleotide Metabolites and Calcium Release from Intracellular Stores. In: Islam, M. (eds) Calcium Signaling. Advances in Experimental Medicine and Biology, vol 1131. Springer, Cham. https://doi.org/10.1007/978-3-030-12457-1_15

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