Advertisement

The CD38-Cyclic ADP-Ribose Signal System in Pancreatic ß-Cells

The Discovery and Biological Significance of a Novel Signal System in Mammalian Cells
Chapter

Abstract

In the early 1980’s, we showed that maintenance of the cellular NAD+ level in β-cells of the islets of Langerhans is essential for the synthesis and secretion of insulin, and proposed a unifying model for the action of the diabetogenic agents alloxan and streptozotocin on pancreatic β-cells (Figure 1) [1–10]. Central to the model are breaks in the nuclear DNA of β-cells, resulting from either an accumulation of free radicals or from the alkylation of DNA. These breaks induce DNA repair involving the activation of poly(ADP-ribose) synthetase/polymerase (PARP), which uses cellular NAD+ as a substrate. As a result, the intracellular levels of NAD+ fall dramatically, which leads to energy depletion and the inhibition of cellular functions including insulin synthesis and secretion, and thus the β-cell ultimately dies.

Keywords

Insulin Secretion Pancreatic Islet Ryanodine Receptor PARP Inhibitor Glucose Stimulation 
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.
    Okamoto H. 1981. Regulation of proinsulin synthesis in pancreatic islets and a new aspect to insulin-dependent diabetes. Mol. Cell. Biochem. 37: 43–61.PubMedCrossRefGoogle Scholar
  2. 2.
    Okamoto H. 1985. Molecular basis of experimental diabetes: degeneration, oncogenesis, and regeneration of pancreatic B-cells of islets of Langerhans. BioEssays 2: 15–21.CrossRefGoogle Scholar
  3. 3.
    Okamoto H, Yamamoto H, Takasawa S, Inoue C, Terazono K, Shiga K and Kitagawa M. 1988. Molecular mechanism of degeneration, oncogenesis and regeneration of pancreatic B-cells of islets of Langerhans. In Lessons from Animal Diabetes II, ed. E Shafrir, AE Renold, pp. 149–157. London: John Libbey & Company Ltd.Google Scholar
  4. 4.
    Okamoto H. 1990. The molecular basis of experimental diabetes. In Molecular biology of the islets of Langerhans, ed. H Okamoto, pp.209–231. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  5. 5.
    Okamoto H, Takasawa S and Tohgo A. 1995. New aspects of the physiological significance of NAD, poly ADP-ribose and cyclic ADP-ribose. Biochimie 11: 356–363.CrossRefGoogle Scholar
  6. 6.
    Okamoto H. 1996. Okamoto model for B-cell damage: Recent advances. In Lessons from animal diabetes VI, ed. E Shafrir, pp. 97–111. Boston: Birkhäuser.CrossRefGoogle Scholar
  7. 7.
    Okamoto H, Takasawa S and Nata K. 1997. The CD38-cyclic ADP-ribose signalling system in insulin secretion: Molecular basis and clinical implications. Diabetologia 40: 1485–1491.PubMedCrossRefGoogle Scholar
  8. 8.
    Okamoto H, Takasawa S, Nata K, Kato I, Tohgo A and Noguchi N. 2000. Physiological and pathological significance of the CD38-cyclic ADP-ribose signaling system. Chem. Immunol. 75: 121–45.PubMedCrossRefGoogle Scholar
  9. 9.
    Takasawa S and Okamoto H. 2002. Pancreatic ß-Cell death, regeneration and insulin secretion: Roles of poly(ADP-ribose) polymerase and cyclic ADP-ribose. Int. J. Exp. Diabet. Res. (in press).Google Scholar
  10. 10.
    Okamoto H and Takasawa S. 2002. Recent advances in the OKAMOTO model: The CD38-cyclic ADP-ribose signal system and the Reg-Reg receptor system in ß-cells. Diabetes (in press).Google Scholar
  11. 11.
    Yamamoto H and Okamoto H. 1980. Protection by picolinamide, a novel inhibitor of poly(ADP-ribose) synthetase, against both streptozotocin-induced depression of proinsulin synthesis and reduction of NAD content in pancreatic islets. Biochem. Biophys. Res. Commun. 95: 474–481.PubMedCrossRefGoogle Scholar
  12. 12.
    Yamamoto H, Uchigata Y and Okamoto H. 1981. Streptozotocin and alloxan induce DNA strand breaks and poly(ADP-ribose) synthetase in pancreatic islets. Nature 294: 284–286.PubMedCrossRefGoogle Scholar
  13. 13.
    Uchigata Y, Yamamoto H, Kawamura A and Okamoto H. 1982. Protection by superoxide dismutase, catalase, and poly(ADP-ribose) synthetase inhibitors against alloxan- and streptozotocin-induced islet DNA strand breaks and against the inhibition of proinsulin synthesis. J. Biol. Chem. 257: 6084–6088.PubMedGoogle Scholar
  14. 14.
    Uchigata Y, Yamamoto H, Nagai H and Okamoto H. 1983. Effect of poly(ADP-ribose) synthetase inhibitor administration to rats before and after injection of alloxan and streptozotocin on islet proinsulin synthesis. Diabetes 32: 316–318.PubMedCrossRefGoogle Scholar
  15. 15.
    Shima K, Hirota M, Sato M, Numoto S and Oshima I. 1987. Effect of poly(ADP-ribose) synthetase inhibitor administration to treptozotocin-induced diabetic rats on insulin and glucagon contents in their pancreas. Diabetes Res. Clin. Practice 3: 135–142.CrossRefGoogle Scholar
  16. 16.
    Takamura T, Kato I, Kimura N, Nakazawa T, Yonekura H, Takasawa S and Okamoto H. 1998. Transgenic mice overexpressing type 2 nitric oxide synthase in pancreatic ß cells develop insulin-dependent diabetes without insulitis. J. Biol. Chem. 273: 2493–2496.PubMedCrossRefGoogle Scholar
  17. 17.
    Charron MJ and Bonner-Weir S. 1999. Implicating PARP and NADV depletion in type I diabetes. Nature Med. 5: 269–270PubMedCrossRefGoogle Scholar
  18. 18.
    Burkart V, Wang ZQ, Radons J, Heller B, Herceg Z, Stingl L, Wagner EF and Kolb H. 1999. Mice lacking the poly(ADP-ribose) polymerase gene are resistant to pancreatic beta-cell destruction and diabetes development induced by streptozocin. Nature Med. 5: 314–319.PubMedCrossRefGoogle Scholar
  19. 19.
    Masutani M, Suzuki H, Kamada N, Watanabe M, Ueda O, Nozaki T, Jishage K, Watanabe T, Sugimoto T, Nakagama H, Ochiya T and Sugimura T. 1999. Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. USA 96: 2301–2304.PubMedCrossRefGoogle Scholar
  20. 20.
    Pieper AA, Brat DJ, Krug DK, Watkins CC, Gupta A, Blackshaw S, Verma A, Wang ZQ and Snyder SH. 1999. Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. USA 96: 3059–3064.PubMedCrossRefGoogle Scholar
  21. 21.
    Eliasson MJ, Sampei K, Mandir AS, Hum PD, Traystman RJ, Bao J, Pieper A, Wang ZQ, Dawson TM, Snyder SH and Dawson VL. 1997. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nature Med. 3: 1089–1095.PubMedCrossRefGoogle Scholar
  22. 22.
    Szabó C, Cuzzocrea S, Zingarelli B, O'Connor M and Salzman AL. 1997. Endothelial dysfunction in a rat model of endotoxic shock: Importance of the activation of poly(ADP-ribose) synthetase by peroxynitrite. J. Clin. Invest. 100: 723–735.PubMedCrossRefGoogle Scholar
  23. 23.
    Zingarelli B, Salzman AL and Szabo C. 1998. Genetic disruption of poly (ADP-ribose) synthetase inhibits the expression of P-selectin and intercellular adhesion molecule-1 in myocardial ischemia/reperfusion injury. Circ. Res. 83: 85–94.PubMedCrossRefGoogle Scholar
  24. 24.
    Szabó C, Virág L, Cuzzocrea S, Scott GS, Hake P, O'Connor MP, Zingarelli B, Salzman A and Kun E. 1998. Protection against peroxynitrite-induced fibroblast injury and arthritis development by inhibition of poly(ADP-ribose) synthetase. Proc. Natl. Acad. Sci. USA 95: 3867–3872.PubMedCrossRefGoogle Scholar
  25. 25.
    Mandir AS, Przedborski S, Jackson-Lewis V, Wang ZQ, Simbulan-Rosenthal CM, Smulson ME, Hoffman BE, Guastella DB, Dawson VL and Dawson TM. 1999. Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism. Proc. Natl. Acad. Sci. USA 96: 5774–5779.PubMedCrossRefGoogle Scholar
  26. 26.
    Stern Y, Salzman A, Cotton RT and Zingarelli B. 1999. Protective effect of 3-aminobenzamide, an inhibitor of poly(ADP-ribose) synthetase, against laryngeal injury in rats. Am. J. Resir. Crit. Care Med. 160: 1743–1749.Google Scholar
  27. 27.
    Bowes J, McDonald MC, Piper J and Thiemermann C. 1999. Inhibitors of poly(ADP-ribose) synthetase protect rat cardiomyocytes against oxidant stress. Cardiovasc. Res. 41: 126–134.PubMedCrossRefGoogle Scholar
  28. 28.
    Filipovic DM, Meng X and Reeves WB. 1999. Inhibition of PARP prevents oxidant-induced necrosis but not apoptosis in LLC-PK1 cells. Am. J. Physiol. 277: F428–F436.PubMedGoogle Scholar
  29. 29.
    Oliver FJ, Menissier-de Murcia J, Nacci C, Decker P, Andriantsitohaina R, Muller S, de la Rubia Gr, Stoclet JC and de Murcia G. 1999. Resistance to endotoxic shock as a consequence of defective NF-kB activation in poly(ADP-ribose) polymerase-1 deficient mice. EMBO J. 18: 4446–4454.PubMedCrossRefGoogle Scholar
  30. 30.
    Zingarelli B, Szabo C and Salzman AL. 1999. Blockade of poly(ADP-ribose) synthetase inhibits neutrophil recruitment, oxidant generation, and mucosal injury in murine colitis. Gastroenterology 116: 335–345.PubMedCrossRefGoogle Scholar
  31. 31.
    Tsao BP, Cantor RM, Grossman JM, Shen N, Teophilov NT, Wallace DJ, Arnett FC, Hartung K, Goldstein R, Kalunian KC, Hahn BH and Rotter JI. 1999. PARP alleles within the linked chromosomal region are associated with systemic lupus erythematosus. J. Clin. Invest. 103:1135–1140.PubMedCrossRefGoogle Scholar
  32. 32.
    Plaschke K, Kopitz J, Weigand MA, Martin E and Bardenheuer HJ. 2000. The neuroprotective effect of cerebral poly(ADP-ribose) polymerase inhibition in a rat model of global ischemia. Neurosi. Lett. 284: 109–112.CrossRefGoogle Scholar
  33. 33.
    Ducrocq S, Benjelloun N, Plotkine M, Ben-Ari Y and Charriaut-Marlangue C. 2000. Poly(ADP-ribose) synthase inhibition reduces ischemic injury and inflammation in neonatal rat brain. J. Neurochem. 74: 2504–2511.PubMedCrossRefGoogle Scholar
  34. 34.
    Mandir AS, Poitras MF, Berliner AR, Herring WJ, Guastella DB, Feldman A, Poirier GG, Wang ZQ, Dawson TM and Dawson VL. 2000. NMDA but not non-NMDA excitotoxicity is mediated by Poly(ADP-ribose) polymerase. J. Neurosci. 20: 8005–8011.PubMedGoogle Scholar
  35. 35.
    Pieper AA, Walles T, Wei G, Clements EE, Verma A, Snyder SH and Zweier JL. 2000. Myocardial postischemic injury is reduced by polyADPribose polymerase-1 gene disruption. Mol. Med. 6: 271–282.PubMedGoogle Scholar
  36. 36.
    Liaudet L, Soriano FG, Szabó E, Virag L, Mabley JG, Salzman AL and Szabó C. 2000. Protection against hemorrhagic shock in mice genetically deficient in poly(ADP-ribose)polymerase. Proc. Natl. Acad. Sci. USA 97: 10203–10208.PubMedCrossRefGoogle Scholar
  37. 37.
    McDonald MC, Mota-Filipe H, Wright JA, Abdelrahman M, Threadgill MD, Thompson AS and Thiemermann C. 2000. Effects of 5-aminoisoquinolinone, a water-soluble, potent inhibitor of the activity of poly(ADP-ribose) polymerase on the organ injury and dysfunction caused by haemorrhagic shock. Br. J. Pharmacol. 130: 843–850.PubMedCrossRefGoogle Scholar
  38. 38.
    Jijon HB, Churchill T, Malfair D, Wessler A, Jewell LD, Parsons HG and Madsen KL. 2000. Inhibition of poly(ADP-ribose) polymerase attenuates inflammation in a model of chronic colitis. Am. J. Physiol. 279: G641–G651.Google Scholar
  39. 39.
    Martin DR, Levvington AJ, Hammerman MR and Padanilam BJ. 2000. Inhibition of poly(ADP-ribose) polymerase attenuates ischemic renal injury in rats. Am. J. Physiol. 279: R1834–R1840.Google Scholar
  40. 40.
    Soriano FG, Virag L, Jagtap P, Szabó E, Mabley JG, Liaudet L, Marton A, Hoyt DG, Murthy KGK, Salzman AL, Southan GJ and Szabo C. 2001. Diabetic endothelial dysfunction: the role of poly(ADP-ribose) polymerase activation. Nature Med. 7: 108–113.CrossRefGoogle Scholar
  41. 41.
    Pacher P, Liaudet L, Soriano FG, Mabley JG, Szabó É and Szabó C. 2002. The role of poly(ADP-ribose) polymerase activation in the development of myocardial and endothelial dysfunction in diabetes. Diabetes 51: 514–521.PubMedCrossRefGoogle Scholar
  42. 42.
    Germain M, Scovassi I and Poirier GG. 2000. Role of poly(ADP-ribose) polymerase in apoptosis. In Cell Death—The Role of Poly (ADP-ribose) polymerase, ed. C. Szabó, pp. 209–225. Boca Raton: CRC Press.Google Scholar
  43. 43.
    Sauter B, Albert ML, Francisco L, Larsson M, Somersan S and Bhardwaj N. 2000. Consequences of cell death: Exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med. 191:423–433.PubMedCrossRefGoogle Scholar
  44. 44.
    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
  45. 45.
    Okamoto H, Takasawa S, Nata K and Yonekura H. 1992. Cyclic ADP-ribose, a novel second messenger for intracellular Ca++ mobilization in pancreatic islets. In First IUBMB Conference: Biochemistry of Diseases, ed. I Yamashina, pp. 218. Nagoya: Bridge Ltd.Google Scholar
  46. 46.
    Takasawa S, Nata K, Yonekura H and Okamoto H. 1993. Cyclic ADP-ribose in insulin secretion from pancreatic ß cells. Science 259: 370–373.PubMedCrossRefGoogle Scholar
  47. 47.
    Ashcroft FM, Harrison DE and Ashcroft SJH. 1984. Glucose induced closure of single potassium channels in isolated rat pancreatic ß-cells. Nature 312: 446–448.PubMedCrossRefGoogle Scholar
  48. 48.
    Takasawa S, Tohgo A, Noguchi N, Koguma T, Nata K, Sugimoto T, Yonekura H and Okamoto H. 1993. Synthesis and hydrolysis of cyclic ADP-ribose by human leukocyte antigen CD38 and inhibition of the hydrolysis by ATP. J. Biol. Chem. 268: 26052–26054.PubMedGoogle Scholar
  49. 49.
    Koguma T, Takasawa S, Tohgo A, Karasawa T, Furuya Y, Yonekura H and Okamoto H. 1994. Cloning and characterization of cDNA encoding rat ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase (homologue to human CD38) from islets of Langerhans. Biochim. Biophys. Acta 1223: 160–162.PubMedCrossRefGoogle Scholar
  50. 50.
    Tohgo A, Takasawa S, Noguchi N, Koguma T, Nata K, Sugimoto T, Furuya Y, Yonekura H and Okamoto H. 1994. Essential cysteine residues for cyclic ADP-ribose synthesis and hydrolysis by CD38. J. Biol. Chem. 269: 28555–28557.PubMedGoogle Scholar
  51. 51.
    Nakagawara K, Mori M, Takasawa S, Nata K, Takamura T, Berlova A, Tohgo A, Karasawa T, Yonekura H, Takeuchi T and Okamoto H. 1995. Assignment of CD38, the gene encoding human leukocyte antigen CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase), to chromosome 4pl5. Cytogenet. Cell Genet. 69: 38–39.PubMedCrossRefGoogle Scholar
  52. 52.
    Nata K, Sugimoto T, Tohgo A, Takamura T, Noguchi N, Matsuoka A, Numakunai T, Shikama K, Yonekura H, Takasawa S and Okamoto H. 1995. The structure of the Aplysia kurodai gene encoding ADP-ribosyl cyclase, a second-messenger enzyme. Gene 158:213–218.PubMedCrossRefGoogle Scholar
  53. 53.
    Kato I, Takasawa S, Akabane A, Tanaka O, Abe H, Takamura T, Suzuki Y, Nata K, Yonekura H, Yoshimoto T and Okamoto H. 1995. Regulatory role of CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase) in insulin secretion by glucose in pancreatic ß cells: Enhanced insulin secretion in CD38 transgenic mice. J. Biol. Chem. 270: 30045–30050.PubMedCrossRefGoogle Scholar
  54. 54.
    Takasawa S, Ishida A, Nata K, Nakagawa K, Noguchi N, Tohgo A, Kato I, Yonekura H, Fujisawa H and Okamoto H. 1995. Requirement of calmodulin-dependent protein kinase II in cyclic ADP-ribose-mediated intracellular Ca2+ mobilization. J. Biol. Chem. 270: 30257–30259.PubMedCrossRefGoogle Scholar
  55. 55.
    Kato I, Suzuki Y, Akabane A, Yonekura H, Tanaka O, Kondo H, Takasawa S, Yoshimoto T and Okamoto H. 1996. Enhancement of glucose-induced insulin secretion in transgenic mice overexpressing human VIP gene in pancreatic ß cells. Ann. NY Acad. Sci. 805: 232–243.PubMedCrossRefGoogle Scholar
  56. 56.
    Noguchi N, Takasawa S, Nata K, Tohgo A, Kato I, Ikehata F, Yonekura H and Okamoto H. 1997. Cyclic ADP-ribose binds to FK506-binding protein 12.6 to release Ca2+ from islet microsomes. J. Biol. Chem. 272: 3133–3136.PubMedCrossRefGoogle Scholar
  57. 57.
    Tohgo A, Munakata H, Takasawa S, Nata K, Akiyama T, Hayashi, N and Okamoto H. 1997. Lysine 129 of CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase) participates in the binding of ATP to inhibit the cyclic ADP-ribose hydrolase. J. Biol. Chem. 272: 3879–3882.PubMedCrossRefGoogle Scholar
  58. 58.
    Nata K, Takamura T, Karasawa T, Kumagai T, Hashioka W, Tohgo A, Yonekura H, Takasawa S, Nakamura S and Okamoto H. 1997. Human gene encoding CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase): organization, nucleotide sequence and alternative splicing. Gene 186: 285–292.PubMedCrossRefGoogle Scholar
  59. 59.
    Takasawa S, Akiyama T, Nata K, Kuroki M, Tohgo A, Noguchi N, Kobayashi K, Kato I, Katada T and Okamoto H. 1998. Cyclic ADP-ribose and inositol 1,4,5-trisphosphate as alternate second messengers for intracellular Ca2+ mobilization in normal and diabetic ß-cells. J. Biol. Chem. 273: 2497–2500.PubMedCrossRefGoogle Scholar
  60. 60.
    Yagui K, Shimada F, Miura M, Hashimoto N, Suzuki Y, Tokuyama Y, Nata K, Tohgo A, Ikehata F, Takasawa S, Okamoto H, Makino H, Saito Y and Kanatsuka A. 1998. A missense mutation in the CD38 gene, a novel factor for insulin secretion: Association with Type II diabetes mellitus in Japanese subjects and evidence of abnormal function when expressed in vitro. Diabetologia 41: 1024–1028.PubMedCrossRefGoogle Scholar
  61. 61.
    Ikehata F, Satoh J, Nata K, Tohgo A, Nakazawa T, Kato I, Kobayashi S, Akiyama T, Takasawa S, Toyota T and Okamoto H. 1998. Autoantibodies against CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase) which impair glucose-induced insulin secretion in non-insulin dependent diabetes patients. J. Clin. Invest. 102: 395–401.PubMedCrossRefGoogle Scholar
  62. 62.
    Kato I, Yamamoto Y, Fujimura M, Noguchi N, Takasawa S and Okamoto H. 1999. CD38 disruption impairs glucose-induced increases in cyclic ADP-ribose, [Ca2+]i and insulin secretion. J. Biol. Chem. 274: 1869–1872.PubMedCrossRefGoogle Scholar
  63. 63.
    Okamoto H and Takasawa S. 2002. CD38. In Encyclopedia of Molecular Medicine, ed. TE Creighton, pp. 601–604. New York: John Wiley & Sons, Inc.Google Scholar
  64. 64.
    Islam MS, Larsson O, Berggren PO, Takasawa S, Nata K, Yonekura H and Okamoto H, Galione A. 1993. Cyclic ADP-ribose in ß cells. Science 262: 584–586.PubMedCrossRefGoogle Scholar
  65. 65.
    Rutter GA, Theler J-M and Wollheim CB. 1994. Ca2+ stores in insulin-secreting cells: lack of effect of cADP ribose. Cell Calcium 16: 71–80.PubMedCrossRefGoogle Scholar
  66. 66.
    Webb D-L, Islam MS, Efanov AM, Brown G, Kohler M, Larsson O and Berggren P-O. 1996. Insulin exocytosis and glucose-mediated increase in cytoplasmic free Ca2+ concentration in the pancreatic ß-cell are independent of cyclic ADP-ribose. J. Biol. Chem. 271: 19074–19079.PubMedCrossRefGoogle Scholar
  67. 67.
    Islam MS and Berggren PO. 1997. Cyclic ADP-ribose and the pancreatic beta cell: where do we stand? Diabetologia 40: 1480–1484.PubMedCrossRefGoogle Scholar
  68. 68.
    Malaisse WJ, Kanda Y, Inageda K, Scruel O, Sener A and Katada T. 1997. Cyclic ADP-ribose measurements in rat pancreatic islets. Biochem. Biophys. Res. Commun. 231: 546–548.PubMedCrossRefGoogle Scholar
  69. 69.
    Scruel O, Wada T, Kontani K, Sener A, Katada T and Malaisse WJ. 1998. Effects of D-glucose and starvation upon the cyclic ADP-ribose content of rat pancreatic islets. Biochem. Mol. Biol. Int. 45: 783–790.PubMedGoogle Scholar
  70. 70.
    An NH, Han MK, Urn C, Park BR Park BJ, Kim HK and Kim UH. 2001. Significance of ecto-cyclase activity of CD38 in insulin secretion of mouse pancreatic islet cells. Biochem. Biophys. Res. Commun. 282: 781–786.PubMedCrossRefGoogle Scholar
  71. 71.
    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
  72. 72.
    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
  73. 73.
    Howard M, Grimaldi JC, Bazan JF, 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
  74. 74.
    Zocchi E, Franco L, Guida L, Benatti U, Bargellesi A, Malavasi F, Lee HC and De Flora A. 1993. A single protein immunologically identified as CD38 displays NAD+ glycohydrolase, ADP-ribosyl cyclase and cyclic ADP-ribose hydrolase activities at the outer surface of human erythrocytes. Biochem. Biophys. Res. Commun. 196: 1459–1465.PubMedCrossRefGoogle Scholar
  75. 75.
    Kaisho T, Ishikawa J, Oritani K, Inazawa J, Tomizawa H, Muraoka O, Ochi T and Hirano T. 1994. BST-1, a surface molecule of bone marrow stromal cell lines that facilitates pre-B-cell growth. Proc. Natl. Acad. Sci. USA 91: 5325–5329.PubMedCrossRefGoogle Scholar
  76. 76.
    Muraoka O, Tanaka H, Itoh M, Ishihara K and Hirano T. 1996. Genomic structure of human BST-1. Immunology Lett. 54: 1–4.CrossRefGoogle Scholar
  77. 77.
    Dong C, Willerford D, Alt FW and Cooper MD. 1996. Genomic organization and chromosomal localization of the mouse Bp3 gene, a member of the CD38/ADP-ribosyl cyclase family. Immunogenetics 45: 35–43.PubMedCrossRefGoogle Scholar
  78. 78.
    Furuya Y, Takasawa S, Yonekura H, Tanaka T, Takahara J and Okamoto, H. 1995. Cloning of a cDNA encoding rat bone marrow stromal cell antigen 1 (BST-1) from the islets of Langerhans. Gene 165: 329–330.PubMedCrossRefGoogle Scholar
  79. 79.
    Kajimoto Y, Miyagawa J, Ishihara K, Okuyama Y, Fujitani Y, Itoh M, Yoshida H, Kaisho T, Matsuoka T, Watada H, Hanafusa T, Yamasaki Y, Kamada T, Matsuzawa Y and Hirano T. 1996. Pancreatic islet cells express BST-1, a CD38-like surface molecule having ADP-Ribosyl cyclase activity. Biochem. Biophys. Res. Commun. 219: 941–946.PubMedCrossRefGoogle Scholar
  80. 80.
    Itoh M, Ishihara K, Hiroi T, Lee BO, Maeda H, Iijima H, Yanagita M, Kiyono H and Hirano T. 1998. Deletion of bone marrow stromal cell antigen-1 (CD 157) gene impaired systemic thymus independent-2 antigen-induced IgG3 and mucosal TD antigen-elicited IgA responses. J. Immunol. 161: 3974–3983.PubMedGoogle Scholar
  81. 81.
    Hirata Y, Kimura N, Sato K, Ohsugi Y, Takasawa S, Okamoto H, Ishikawa J, Kaisho T, Ishihara K and Hirano T. 1994. ADP ribosyl cyclase activity of a novel bone marrow stromal cell surface molecule, BST-1. FEBS Lett. 356: 244–248.PubMedCrossRefGoogle Scholar
  82. 82.
    Rojas E, Carroll PB, Ricordi C, Boschero AC, Stojilkovic SS and Atwater I. 1994. Control of cytosolic free calcium in cultured human pancreatic ß-cells occurs by external calcium-dependent and independent mechanisms. Endocrinology 134: 1771–1781.PubMedCrossRefGoogle Scholar
  83. 83.
    Mészáros 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
  84. Holz GG, Leech GA, Heller RS, Castonguay M and Habener JF. 1999. cAMP-dependent mobilization of intracellular Ca2+ stores by activation of ryanodine receptors in pancreatic beta-cells: A Ca2+ signaling system stimulated by insulinotropic hormone glucagon-likepeptide-l-(7-37). J. Biol. Chem. 274: 14147–14156.PubMedCrossRefGoogle Scholar
  85. 85.
    Fukao K, Ochiai T, Takahashi K, Endo T, Yokoyama I, Uchida K, Oshima S, Ishibashi M, Takahara S, Iwasaki Y, Ota K, Takagi H and Sonoda T. 1994. A late phase II study of FK506 (Tacrolimus) on kidney transplantation. Jps. J. Transplantation 29: 614–631.Google Scholar
  86. 86.
    Pirsch JD, Miller J, Deierhoi MH, Vincenti F and Filo RS. 1997. A comparison of tacrolimus (FK506) and cyclosporine for immunosuppression after cadaveric renal transplantation: FK506 Kidney Transplant Study Group. Transplantation 63: 977–983.PubMedCrossRefGoogle Scholar
  87. Ashcroft FM and Ashcroft SJH. 1992. Mechanism of insulin secretion. In Insulin: Molecular biology to pathology, ed. FM Ashcroft, SJH Ashcroft, pp. 97–150. Oxford: IRL Press.Google Scholar
  88. 88.
    Pupilli C, Giannini S, Marchetti P, Lupi R, Antonelli A, Malavasi F, Takasawa S, Okamoto H and Ferrannini E. 1999. Autoanitibodies to CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase) in Caucasian patients with diabetes: Effects on insulin release from human islets. Diabetes 48: 2309–2315.PubMedCrossRefGoogle Scholar
  89. 89.
    Mallone R, Ortolan E, Baj G, Funaro A, Giunti S, Lillaz E, Saccucci F, Cassader M, Cavallo-Perin P and Malavasi F. 2001. Autoantibody response to CD38 in Caucasian patients with type 1 and type 2 diabetes: immunological and genetic characterization. Diabetes 50: 752–762.PubMedCrossRefGoogle Scholar
  90. 90.
    Antonelli A, Baj G, Marchetti P, Fallahi P, Surico N, Pupilli C, Malavasi F and Ferrannini E. 2001. Human anti-CD38 autoantibodies raise intracellular calcium and stimulate insulin release in human pancreatic islets. Diabetes 50: 985–991PubMedCrossRefGoogle Scholar
  91. 91.
    Berridge MJ and Irvine RF. 1984. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312, 315–321.PubMedCrossRefGoogle Scholar
  92. 92.
    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
  93. 93.
    Matsuoka T, Kajimoto Y, Watada H, Umayahara Y, Kubota M, Kawamori R, Yamasaki Y and Kamada T. 1995. Expression of CD38 gene, but not of mitochondrial glycerol-3-phosphate dehydrogenase gene, is impaired in pancreatic islets of GK rats. Biochem. Biophys. Res. Commun. 214: 239–246.PubMedCrossRefGoogle Scholar
  94. 94.
    Galione A. 1993. Cyclic ADP-ribose: A new way to control calcium. Science 259: 325–326.PubMedCrossRefGoogle Scholar
  95. 95.
    Sasaki T, Shimura S, Takasawa S, Nagaki M, Satoh M, Okamoto H and Shirato K. 1993. Cyclic ADP-ribose, a candidate for a novel Ca2+-mobilizing second messenger, induced Ca2+-dependent current responses in airway submucosal gland cells. Am. Rev. Resp. Dis. 147: A936.Google Scholar
  96. 96.
    Hua S-Y, 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
  97. 97.
    Thorn P, Gerashimenko O and Petersen OH. 1994. Cyclic ADP-ribose regulation of ryanodine receptors involved in agonist evoked cytosolic Ca2+ oscillations in pancreatic acinar cells. EMBO J. 13:2038–2043.PubMedGoogle Scholar
  98. 98.
    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
  99. 99.
    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
  100. 100.
    Higashida H, Robbins J, Egorova A, Noda M, Taketo M, Ishizaka N, Takasawa S, Okamoto H and Brown DA. 1995. Nicotinamide-adenine dinucleotide regulates muscarinic receptor-coupled KV(M) channels in rodent NG108-15 cells. J. Physiol. 482: 317–323.PubMedGoogle Scholar
  101. 101.
    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
  102. 102.
    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
  103. 103.
    Gromada J, Jorgensen TD and Dissing S. 1995. Cyclic ADP-ribose and inositol 1,4,5-trisphosphate mobilizes Ca2+ from distinct intracellular pools in permeabilized lacrimal acinar cells. FEBS Lett. 360: 303–306.PubMedCrossRefGoogle Scholar
  104. 104.
    Rakovic S, Galione A, Ashamu GA, Potter BVL and Terrar DA. 1996. A specific cyclic ADP-ribose antagonist inhibits cardiac excitation-contraction coupling. Curr. Biol. 6: 989–996.PubMedCrossRefGoogle Scholar
  105. 105.
    Ebihara S, Sasaki T, Hida W, Kikuchi Y, Oshiro T, Shimura S, Takasawa S, Okamoto H, Nishiyama A, Akaike N and Shirato K. 1997. Role of cyclic ADP-ribose in ATP-activated potassium currents in alveolar macrophages. J. Biol. Chem. 272:16023–16029.PubMedCrossRefGoogle Scholar
  106. 106.
    Yamaki H, Morita K, Kitayama S. Imai Y, Itadani K, Akagawa Y and Doi T. 1998. Cyclic ADP-ribose induces Ca2+ release from caffeine-insensitive Ca2+ pools in canine salivary gland cells. J. Dental Res. 11: 1807–1816.CrossRefGoogle Scholar
  107. 107.
    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
  108. 108.
    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: 405–414.PubMedCrossRefGoogle Scholar
  109. Li PL, Zou AP and Campbell WB. 1998. Regulation of K-Ca-channel activity by cyclic ADP-ribose and ADP-ribose in coronary arterial smooth muscle. Am. J. Physiol. 44: H1002–HI010.Google Scholar
  110. 110.
    Sun L, Adebanjo OA, Moonga BS, Corisdeo S, Anandatheerthavarada HK, Biswas G, Arakawa T, Hakeda Y, Koval A, Sodam B, Bevis PJ, Moser AJ, Lai FA, Epstein S, Troen BR, Kumegawa M and Zaidi M. 1999. CD38/ADP-ribosyl cyclase: A new role in the regulation of osteoclastic bone resorption. J. Cell Biol. 146: 1161–1172.PubMedCrossRefGoogle Scholar
  111. 111.
    Reyes-Harde M, Potter BV, 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. Neurophysiol. 82: 1569–1576.PubMedGoogle Scholar
  112. 112.
    Rakovic S, Cui Y, Iino S, Galione A, Ashamu GA, Potter BV and Terrar DA. 1999. An antagonist of cADP-ribose inhibits arrhythmogenic oscillations of intracellular Ca2+ in heart cells. J. Biol. Chem. 274: 17820–17827.PubMedCrossRefGoogle Scholar
  113. 113.
    Inngjerdingen M, Al-Aoukaty A, Damaj B and Maghazachi AA. 1999. Differential utilization of cyclic ADP-ribose pathway by chemokines to induce the mobilization of intracellular calcium in NK cells. Biochem. Biophys. Res. Commun. 262: 467–472.PubMedCrossRefGoogle Scholar
  114. 114.
    Guse AH, da Silva CP, Berg I, Skapenko AL, Weber K, Heyer P, Hohenegger M, Ashamu GA, Schulze-Koops H, Potter BV and Mayr GW. 1999. Regulation of calcium signalling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature 398: 70–73.PubMedCrossRefGoogle Scholar
  115. 115.
    Khoo KM, Han MK, Park JB, Chae SW, Kim UH, 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
  116. 116.
    Han MK, Cho YS, Kim YS, Yim CY and Kim UH. 2000. Interaction of two classes of ADP-ribose transfer reactions in immune signalling. J. Biol. Chem. 275: 20799–20805.PubMedCrossRefGoogle Scholar
  117. 117.
    Fukushi Y, Kato I, Takasawa S, Sasaki T, Ong BH, 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
  118. 118.
    Partida-Sanchez S, Coockayne DA, Monard S, Jacobson EL, Oppenheimer N, Garvy B, Kusser K, Goodrich S, Howard M, Harmsen A, Randall TD 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
  119. 119.
    Higashida H, Yokoyama S, Hashii M, Taketo M, Higashida M, Takayasu T, Ohshima T, Takasawa S, Okamoto H and Noda M 1997. Muscarinic receptor-mediated dual regulation of ADP-ribosyl cyclase in NG108-15 neuronal cell membranes analyzed by thin layer chromatography. J. Biol. Chem. 272: 31272–31277.PubMedCrossRefGoogle Scholar
  120. 120.
    Terazono K, Yamamoto H, Takasawa S, Shiga K, Yonemura Y, Tochino Y and Okamoto H. 1988. A novel gene activated in regenerating islets. J. Biol. Chem. 263: 2111–2114.PubMedGoogle Scholar
  121. 121.
    Watanabe T, Yonekura H, Terazono K, Yamamoto H and Okamoto H. 1990. Complete nucleotide sequence of human reg gene and its expression in normal and tumoral tissues: The reg protein, pancreatic stone protein, and pancreatic thread protein are one and the same product of the gene. J. Biol. Chem. 265: 7432–7439.PubMedGoogle Scholar
  122. 122.
    Watanabe T, Yonemura Y, Yonekura H, Suzuki Y, Miyashita H, Sugiyama K, Moriizumi S, Unno M, Tanaka O, Kondo H, Bone AJ, Takasawa S and Okamoto H. 1994. Pancreatic beta-cell replication and amelioration of surgical diabetes by Reg protein. Proc. Natl. Acad. Sci. USA 91: 3589–3592.PubMedCrossRefGoogle Scholar
  123. 123.
    Okamoto H. 1999. The Reg gene family and Reg proteins: With special attention to the regeneration of pancreatic ß-cells. J. Hepatobiliary Pancreat. Surg. 6: 254–262.PubMedCrossRefGoogle Scholar
  124. 124.
    Kobayashi S, Akiyama T, Nata K, Abe M, Tajima M, Shervani NJ, Unno M, Matsuno S, Sasaki H, Takasawa S and Okamoto H. 2000. Identification of a receptor for Reg (Regenerating Gene) protein, a pancreatic ß-cell regeneration factor. J. Biol. Chem. 275: 10723–10726.PubMedCrossRefGoogle Scholar
  125. 125.
    Unno M, Nata K, Noguchi N, Narushima Y, Akiyama T, Ikeda T, Nakagawa K, Takasawa S and Okamoto H. 2002. Production and characterization of Reg knockout mice: Reduced proliferation of pancreatic ß-cells in Reg knockout mice. Diabetes (in press).Google Scholar
  126. Akiyama T, Takasawa S, Nata K, Kobayashi S, Abe M, Shervani NJ, Ikeda T, Nakagawa K, Unno M, Matsuno S and Okamoto H. 2001. Activation of Reg gene, a gene for insulin-producing ß-cell regeneration: Poly(ADP-ribose) polymerase binds Reg promoter and regulates the transcription by autopoly(ADP-ribosyl)ation. Proc. Natl. Acad. Sci. USA 98: 48–53.PubMedGoogle Scholar
  127. 127.
    Livesey JF, O'Brien AJ, Li M, Smith GA, Murphy JL and Hunt PS. 1997. A Schwann cell mitogen accompanying regeneration of motor neurons. Nature 390: 614–618.PubMedCrossRefGoogle Scholar
  128. 128.
    Nishimune H, Vasseur S, Wiese S, Biding MC, Holtmann B, Sendtner M, Iovanna JL and Henderson CE. 2000. Reg-2 is a motoneuron neurotrophic factor and a signalling intermediate in the CNTF survival pathway. Nature Cell Biol. 2: 906–914.PubMedCrossRefGoogle Scholar
  129. 129.
    Asahara M, Mushiake S, Shimada S, Fukui H, Kinoshita Y, Kawakami C, Watanabe T, Tanaka T, Ichikawa A, Uchiyama Y, Narushima Y, Takasawa S, Okamoto H, Tohyama M and Chiba T. 1996. Reg gene expression is increased in rat gastric enterochromaffin-like cells following water immersion stress. Gastroenterology 111: 45–55.PubMedCrossRefGoogle Scholar
  130. 130.
    Fukui H, Kinoshita Y, Maekawa T, Okada A, Waki S, Hassan S, Okamoto H and Chiba T. 1998. Regenerating gene protein may mediate gastric mucosal proliferation induced by hypergastrinemia in rats. Gastroenterology 115: 1483–1493.PubMedCrossRefGoogle Scholar
  131. 131.
    Kazumori H, Ishirara S, Hoshino E, Kawashima K, Moriyama N, Suetsugu H, Sato H, Adachi K, Fukuda R, Watanabe M, Takasawa S, Okamoto H, Fukui H, Chiba T and Kinoshita Y. 2000. Neutrophil chemoattractant-2ß regulates the expression of the Reg gene in injured gastric mucosa in rats. Gastroenterology 119: 1610–1622.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  1. 1.Department of BiochemistryTohoku University Graduate School of MedicineMiyagiJapan

Personalised recommendations