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Recent advances in physiological and pathological significance of NAD+ metabolites: roles of poly(ADP-ribose) and cyclic ADP-ribose in insulin secretion and diabetogenesis

Published online by Cambridge University Press:  14 December 2007

Hiroshi Okamoto  and
Shin Takasawa
Hiroshi Okamoto*
Affiliation:
Department of Biochemistry and Advanced Biological Sciences for Regeneration (Kotobiken Medical Laboratories)Tohoku University Graduate School of Medicine, Sendai 980-8575, Japan
Shin Takasawa
Affiliation:
Department of Biochemistry and Advanced Biological Sciences for Regeneration (Kotobiken Medical Laboratories)Tohoku University Graduate School of Medicine, Sendai 980-8575, Japan
*
*Corresponding author: Dr Hiroshi Okamoto, fax +81 227178083, email okamotoh@mail.tains.tohoku.ac.jp
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Abstract

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Poly(ADP-ribose) synthetase/polymerase (PARP) activation causes NAD+ depletion in pancreatic β-cells, which results in necrotic cell death. On the other hand, ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase (CD38) synthesizes cyclic ADP-ribose from NAD+, which acts as a second messenger, mobilizing intracellular Ca2+ for insulin secretion in response to glucose in β-cells. PARP also acts as a regenerating gene (Reg) transcription factor to induce β-cell regeneration. This provides the new concept that NAD+ metabolism can control the cellular function through gene expression. Clinically, PARP could be one of the most important therapeutic targets; PARP inhibitors prevent cell death, maintain the formation of a second messenger, cyclic ADP-ribose, to achieve cell function, and keep PARP functional as a transcription factor for cell regeneration.

Keywords

Poly(ADP-ribose) synthetase/polymeraseOkamoto model for β-cell damageNecrosisApoptosisRegenerating gene
Type
Research Article
Information
Nutrition Research Reviews , Volume 16 , Issue 2 , December 2003 , pp. 253 - 266
Copyright
Copyright © The Authors 2003

References

Abe, M, Nata, K, Akiyama, T, Shervani, NJ, Kobayashi, S, Tomioka-Kumagai, T, Ito, S, Takasawa, S & Okamoto, H (2000) Identification of a novel Reg family gene, Reg IIIδ, and mapping of all three types of Reg family genes in a 75 kilobase mouse genomic region. Gene 246, 111–122.CrossRefGoogle Scholar
Akiyama, T, Takasawa, S, Nata, K, Kobayashi, S, Abe, M, Shervani, NJ, Ikeda, T, Nakagawa, K, Unno, M, Matsuno, S & Okamoto, H (2001) Activation of Reg gene, a gene for insulin-producing β-cell regeneration: Poly(ADP-ribose) polymerase binds Reg promoter and regulates the transcription by autopoly(ADP-ribosyl)ation. Proceedings of the National Academy of Sciences USA 98, 48–53.Google ScholarPubMed
Alderman, BM, Ulaganathan, M, Judd, LM, Howlett, M, Parker, LM, Yeomans, ND & Giraud, AS (2003) Insights into the mechanisms of gastric adaptation to aspirin injury: A role for regenerating protein but not trefoil peptides. Laboratory Investigation 83, 1415–1425.CrossRefGoogle Scholar
Allen, GJ, Muir, SR & Sanders, D (1995) Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose. Science 268, 735–737.CrossRefGoogle ScholarPubMed
An, NH, Han, MK, Um, C, Park, BH, Park, BJ, Kim, HK & Kim, UH (2001) Significance of ecto-cyclase activity of CD38 in insulin secretion of mouse pancreatic islet cells. Biochemical and Biophysical Research Communications 282, 781–786.CrossRefGoogle ScholarPubMed
Antonelli, A, Baj, G, Marchetti, P, Fallahi, P, Surico, N, Pupilli, C, Malavasi, F & Ferrannini, E (2001) Human anti-CD38 autoantibodies raise intracellular calcium and stimulate insulin release in human pancreatic islets. Diabetes 50, 985–991.CrossRefGoogle ScholarPubMed
Antonelli, A, Tuomi, T, Nannipieri, M, Fallahi, P, Nesti, C, Okamoto, H, Groop, L & Ferrannini, E (2002) Autoimmunity to CD38 and GAD in Type I and Type II diabetes: CD38 and HLA genotypes and clinical phenotypes. Diabetologia 45, 1298–1306.CrossRefGoogle ScholarPubMed
Asahara, M, Mushiake, S, Shimada, S, Fukui, H, Kinoshita, Y, Kawanami, C, Watanabe, T, Tanaka, S, Ichikawa, A, Uchiyama, Y, Narushima, Y, Takasawa, S, Okamoto, H, Tohyama, M & Chiba, T (1996) Reg gene expression is increased in rat gastric enterochromaffin-like cells following water immersion stress. Gastroenterology 111, 45–55.CrossRefGoogle ScholarPubMed
Ashcroft, FM, Harrison, DE & Ashcroft, SJH (1984) Glucose induced closure of single potassium channels in isolated rat pancreatic β-cells. Nature 312, 446–448.CrossRefGoogle ScholarPubMed
Berridge, MJ & Irvine, RF (1984) Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312, 315–321.CrossRefGoogle ScholarPubMed
Bowes, J, McDonald, MC, Piper, J & Thiemermann, C (1999) Inhibitors of poly (ADP-ribose) synthetase protect rat cardiomyocytes against oxidant stress. Cardiovascular Research 41, 126–134.CrossRefGoogle ScholarPubMed
Burkart, V, Wang, ZQ, Radons, J, Heller, B, Herceg, Z, Stingl, L, Wagner, EF & 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 Medicine 5, 314–319.CrossRefGoogle ScholarPubMed
Cardinal, JW, Margison, GP, Mynett, KJ, Yates, AP, Cameron, DP & Elder, RH (2001) Increased susceptibility to streptozotocin-induced β-cell apoptosis and delayed autoimmune diabetes in alkylpurine-DNA-N-glycosylase-deficient mice. Molecular and Cellular Biology 21, 5605–5613.CrossRefGoogle ScholarPubMed
Chambon, P, Weill, JD, Doly, J, Strosser, MT & Mandel, P (1966) ON formation of a novel adenylic compound by enzymatic extracts of liver nuclei. Biochemical and Biophysical Research Communications 25, 638–643.CrossRefGoogle Scholar
Charron, MJ & Bonner-Weir, S (1999) Implicating PARP and NAD+ depletion in type I diabetes. Nature Medicine 5, 269–270.CrossRefGoogle ScholarPubMed
Chini, EN, Chini, CC, Barata da Silva, H & Zielinska, W (2002) The cyclic-ADP-ribose signaling pathway in human myometrium. Archives of Biochemistry and Biophysics 407, 152–159.CrossRefGoogle ScholarPubMed
Clapper, DL, Walseth, TF, Dargie, PJ & Lee, HC (1987) Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. Journal of Biological Chemistry 262, 9561–9568.CrossRefGoogle ScholarPubMed
Cocco, RE & Ucker, DS (2001) Distinct modes of macrophage recognition for apoptotic and necrotic cells are not specified exclusively by phosphatidylserine exposure. Molecular Biology of the Cell 12, 919–930.CrossRefGoogle Scholar
Ducrocq, S, Benjelloun, N, Plotkine, M, Ben-Ari, Y & Charriaut-Marlangue, C (2000) Poly(ADP-ribose) synthase inhibition reduces ischemic injury and inflammation in neonatal rat brain. Journal of Neurochemistry 74, 2504–2511.CrossRefGoogle ScholarPubMed
Dunn, JS, Sheehan, HL & McLetchie, NGB (1943) Necrosis of islets of Langerhans. Lancet i, 484–487.Google Scholar
Ebihara, S, Sasaki, T, Hida, W, Kikuchi, Y, Oshiro, T, Shimura, S, Takasawa, S, Okamoto, H, Nishiyama, A, Akaike, N & Shirato, K (1997) Role of cyclic ADP-ribose in ATP-activated potassium currents in alveolar macrophages. Journal of Biological Chemistry 272, 16023–16029.CrossRefGoogle ScholarPubMed
Eliasson, MJ, Sampei, K, Mandir, AS, Hurn, PD, Traystman, RJ, Bao, J, Pieper, A, Wang, ZQ, Dawson, TM, Snyder, SH & Dawson, VL (1997) Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nature Medicine 3, 1089–1095.CrossRefGoogle ScholarPubMed
Fukui, H, Kinoshita, Y, Maekawa, T, Okada, A, Waki, S, Hassan, S, Okamoto, H & Chiba, T (1998) Regenerating gene protein may mediate gastric mucosal proliferation induced by hypergastrinemia in rats. Gastroenterology 115, 1483–1493.CrossRefGoogle ScholarPubMed
Fukushi, Y, Kato, I, Takasawa, S, Sasaki, T, Ong, BH, Ohsaga, A, Sato, K, Shirato, K, Okamoto, H & Maruyama, Y (2001) Identification of cyclic ADP-ribose-dependent mechanisms in pancreatic muscarinic Ca2+ signaling using CD38 knockout mice. Journal of Biological Chemistry 276, 649–655.CrossRefGoogle ScholarPubMed
Galione, A (1993) Cyclic ADP-ribose: A new way to control calcium. Science 259, 325–326.CrossRefGoogle ScholarPubMed
Germain, M, Scovassi, I & Poirier, GG (2000) Role of poly(ADP-ribose) polymerase in apoptosis. In. In Cell Death – The Role of Poly(ADP-ribose) Polymerase, pp 209–225. [Szabó, C editor]. Boca Raton, FL: CRC Press.Google Scholar
Gromada, J, Jørgensen, TD & Dissing, S (1995) Cyclic ADP-ribose and inositol 1,4,5-trisphosphate mobilizes Ca2+ from distinct intracellular pools in permeabilized lacrimal acinar cells. FEBS Letters 360, 303–306.Google ScholarPubMed
Gross, DJ, Weiss, L, Reibstein, I, van den Brand, J, Okamoto, H, Clark, A & Slavin, S (1998) Amelioration of diabetes in nonobese diabetic mice with advanced disease by Linomide-induced immunoregulation combined with Reg protein treatment. Endocrinology 139, 2369–2374.CrossRefGoogle ScholarPubMed
Guse, AH, da Silva, CP, Berg, I, Skapenko, AL, Weber, K, Heyer, P, Hohenegger, M, Ashamu, GA, Schulze-Koops, H, Potter, BV & Mayr, GW (1999) Regulation of calcium signalling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature 398, 70–73.CrossRefGoogle Scholar
Han, MK, Cho, YS, Kim, YS, Yim, CY & Kim, UH (2000) Interaction of two classes of ADP-ribose transfer reactions in immune signalling. Journal of Biological Chemistry 275, 20799–20805.CrossRefGoogle Scholar
Hartupee, JC, Zhang, H, Bonaldo, MF, Soares, MB & Dieckgraefe, BK (2001) Isolation and characterization of a cDNA encoding a novel member of the human regenerating protein family: Reg IV. Biochimica et Biophysica Acta 1518, 287–293.CrossRefGoogle ScholarPubMed
Higashida, H, Robbins, J, Egorova, A, Noda, M, Taketo, M, Ishizaka, N, Takasawa, S, Okamoto, H & Brown, DA (1995) Nicotinamide-adenine dinucleotide regulates muscarinic receptor-coupled K+(M) channels in rodent NG108–15 cells. Journal of Physiology 482, 317–323.CrossRefGoogle ScholarPubMed
Higashida, H, Yokoyama, S, Hashii, M, Taketo, M, Higashida, M, Takayasu, T, Ohshima, T, Takasawa, S, Okamoto, H & Noda, M (1997) Muscarinic receptor-mediated dual regulation of ADP-ribosyl cyclase in NG108–15 neuronal cell membranes analyzed by thin layer chromatography. Journal of Biological Chemistry 272, 31272–31277.CrossRefGoogle Scholar
Hua, S-Y, Tokimasa, T, Takasawa, S, Furuya, Y, Nohmi, M, Okamoto, H & Kuba, K (1994) Cyclic ADP-ribose modulates Ca2+ release channels for activation by physiological Ca2+ entry in bullfrog sympathetic neurons. Neuron 12, 1073–1079.CrossRefGoogle ScholarPubMed
Ikehata, F, Satoh, J, Nata, K, Tohgo, A, Nakazawa, T, Kato, I, Kobayashi, S, Akiyama, T, Takasawa, S, Toyota, T & 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. Journal of Clinical Investigation 102, 395–401.CrossRefGoogle Scholar
Inngjerdingen, M, Al-Aoukaty, A, Damaj, B & Maghazachi, AA (1999) Differential utilization of cyclic ADP-ribose pathway by chemokines to induce the mobilization of intracellular calcium in NK cells. Biochemical and Biophysical Research Communications 262, 467–472.CrossRefGoogle ScholarPubMed
Islam, MS & Berggren, PO (1997) Cyclic ADP-ribose and the pancreatic beta cell: where do we stand?. Diabetologia 40, 1480–1484.CrossRefGoogle ScholarPubMed
Islam, MS, Larsson, O, Berggren, PO, Takasawa, S, Nata, K, Yonekura, H, Okamoto, H & Galione, A (1993) Cyclic ADP-ribose in β cells. Science 262, 584–586.CrossRefGoogle ScholarPubMed
Jijon, HB, Churchill, T, Malfair, D, Wessler, A, Jewell, LD, Parsons, HG & Madsen, KL (2000) Inhibition of poly(ADP-ribose) polymerase attenuates inflammation in a model of chronic colitis. American Journal of Physiology 279, G641–G651.Google Scholar
Kämäräinen, M, Heiskala, K, Knuutila, S, Heiskal, M, Winqvist, O & Andersson, LC (2003) RELP, a novel human Reg-like protein with up-regulated expression in inflammatory and metaplastic gastrointestinal mucosa. American Journal of Pathology 163, 11–20.CrossRefGoogle ScholarPubMed
Kato, I, Takasawa, S, Akabane, A, Tanaka, O, Abe, H, Takamura, T, Suzuki, Y, Nata, K, Yonekura, H, Yoshimoto, T & Okamoto, H (1995) Regulatory role of CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase) in insulin secretion by glucose in pancreatic β cells: Enhanced insulin secretion in CD38 transgenic mice. Journal of Biological Chemistry 270, 30045–30050.CrossRefGoogle ScholarPubMed
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. Journal of Biological Chemistry 274, 1869–1872.CrossRefGoogle ScholarPubMed
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 & Kinoshita, Y (2000) Neutrophil chemoattractant-2β regulates the expression of the Reg gene in injured gastric mucosa in rats. Gastroenterology 119, 1610–1622.CrossRefGoogle Scholar
Khoo, KM, Han, MK, Park, JB, Chae, SW, Kim, UH, Lee, HC, Bay, BH & Chang, CF (2000) Localization of the cyclic ADP-ribose dependent calcium signaling pathway in hepatocyte nucleus. Journal of Biological Chemistry 275, 24807–24817.CrossRefGoogle ScholarPubMed
Kiji, T, Dohi, Y, Nishizaki, K, Takasawa, S, Okamoto, H, Nagasaka, S, Naito, H, Yonemasu, K & Taniguchi, S (2003) Enhancement of cell viability in cryopreserved rat vascular grafts by administration of regenerating gene (Reg) inducers. Journal of Vascular Research 40, 132–139.CrossRefGoogle ScholarPubMed
Kobayashi, S, Akiyama, T, Nata, K, Abe, M, Tajima, M, Shervani, NJ, Unno, M, Matsuno, S, Sasaki, H, Takasawa, S & Okamoto, H (2000) Identification of a receptor for Reg (Regenerating Gene) protein, a pancreatic β-cell regeneration factor. Journal of Biological Chemistry 275, 10723–10726.CrossRefGoogle ScholarPubMed
Koguma, T, Takasawa, S, Tohgo, A, Karasawa, T, Furuya, Y, Yonekura, H & 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. Biochimica et Biophysica Acta 1223, 160–162.CrossRefGoogle ScholarPubMed
Kuemmerle, JF & Makhlouf, GM (1995) Agonist-stimulated cyclic ADP ribose: Endogenous modulator of Ca2+-induced Ca2+ release in intestinal longitudinal muscle. Journal of Biological Chemistry 270, 25488–25494.CrossRefGoogle Scholar
Lee, HC, Aarhus, R, Graeff, R, Gurnack, ME & Walseth, TF (1994) Cyclic ADP ribose activation of the ryanodine receptor is mediated by calmodulin. Nature 370, 307–309.CrossRefGoogle ScholarPubMed
Li, PL, Zou, AP & Campbell, WB (1998) Regulation of K-Ca-channel activity by cyclic ADP-ribose and ADP-ribose in coronary arterial smooth muscle. American Journal of Physiology 44, H1002–H1010.Google Scholar
Liaudet, L, Soriano, FG, Szabo, E, Virag, L, Mabley, JG, Salzman, AL & Szabó, C (2000) Protection against hemorrhagic shock in mice genetically deficient in poly(ADP-ribose)polymerase. Proceedings of the National Academy of Sciences USA 97, 10203–10208.CrossRefGoogle ScholarPubMed
Livesey, JF, O'Brien, AJ, Li, M, Smith, GA, Murphy, JL & Hunt, PS (1997) A Schwann cell mitogen accompanying regeneration of motor neurons. Nature 390, 614–618.CrossRefGoogle ScholarPubMed
Love, S, Barber, R & Wilcock, GK (1999) Increased poly(ADP-ribosyl)ation of nuclear proteins in Alzheimer's disease. Brain 122, 247–253.CrossRefGoogle ScholarPubMed
Mabley, JG, Suarez-Pinzon, WL, Hasko, G, Salzman, AL, Rabinovitch, A, Kun, E & Szabó, C (2001) Inhibition of poly (ADP-ribose) synthetase by gene disruption or inhibition with 5-iodo-6-amino-1,2-benzopyrone protects mice from multiple-low-dose-streptozotocin-induced diabetes. British Journal of Pharmacology 133, 909–919.CrossRefGoogle ScholarPubMed
Mallone, R, Ortolan, E, Baj, G, Funaro, A, Giunti, S, Lillaz, E, Saccucci, F, Cassader, M, Cavallo-Perin, P & 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.CrossRefGoogle ScholarPubMed
Mandir, AS, Przedborski, S, Jackson-Lewis, V, Wang, ZQ, Simbulan-Rosenthal, CM, Smulson, ME, Hoffman, BE, Guastella, DB, Dawson, VL & Dawson, TM (1999) Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism. Proceedings of the National Academy of Sciences USA 96, 5774–5779.CrossRefGoogle ScholarPubMed
Martin, DR, Lewington, AJ, Hammerman, MR & Padanilam, BJ (2000) Inhibition of poly(ADP-ribose) polymerase attenuates ischemic renal injury in rats. American Journal of Physiology 279, R1834–R1840.Google ScholarPubMed
Masutani, M, Suzuki, H, Kamada, N, Watanabe, M, Ueda, O, Nozaki, T, Jishage, K, Watanabe, T, Sugimoto, T, Nakagama, H, Ochiya, T & Sugimura, T (1999) Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. Proceedings of the National Academy of Sciences USA 96, 2301–2304.CrossRefGoogle ScholarPubMed
Matsuoka, T, Kajimoto, Y, Watada, H, Umayahara, Y, Kubota, M, Kawamori, R, Yamasaki, Y & Kamada, T (1995) Expression of CD38 gene, but not of mitochondrial glycerol-3-phosphate dehydrogenase gene, is impaired in pancreatic islets of GK rats. Biochemical and Biophysical Research Communications 214, 239–246.CrossRefGoogle Scholar
Mitchell, KJ, Pinton, P, Varadi, A, Tacchetti, C, Ainscow, EK, Pozzan, T, Rizzuto, R & Rutter, GA (2001) Dense core secretory vesicles revealed as a dynamic Ca2+ store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. Journal of Cell Biology 155, 41–51.CrossRefGoogle ScholarPubMed
Miyashita, H, Nakagawara, K, Mori, M, Narushima, Y, Noguchi, N, Moriizumi, S, Takasawa, S, Yonekura, H, Takeuchi, T & Okamoto, H (1995) Human REG family genes are tandemly ordered in a 95-kilobase region of chromosome 2p12. FEBS Letters 377, 429–433.Google Scholar
Moriizumi, S, Watanabe, T, Unno, M, Nakagawara, K, Suzuki, Y, Miyashita, H, Yonekura, H & Okamoto, H (1994) Isolation, structural determination and expression of a novel reg gene, human reg Iβ. Biochimica et Biophysica Acta 1217, 199–202.CrossRefGoogle Scholar
Mothet, JP, Fossier, P, Meunier, FM, Stinnakre, J, Tauc, L & Baux, G (1998) Cyclic ADP-ribose and calcium-induced calcium release regulate neurotransmitter release at a cholinergic synapse of Aplysia. Journal of Physiology 507, 405–414.CrossRefGoogle Scholar
Nishimune, H, Vasseur, S, Wiese, S, Birling, MC, Holtmann, B, Sendtner, M, Iovanna, JL & Henderson, CE (2000) Reg-2 is a motoneuron neurotrophic factor and a signalling intermediate in the CNTF survival pathway. Nature Cell Biology 2, 906–914.CrossRefGoogle Scholar
Nishizuka, Y, Ueda, K, Nakazawa, K & Hayaishi, O (1967) Studies on the polymer of adenosine diphosphate ribose. I. Enzymic formation from nicotinamide adenine dinuclotide in mammalian nuclei. Journal of Biological Chemistry 242, 3164–3171.CrossRefGoogle ScholarPubMed
Noguchi, N, Takasawa, S, Nata, K, Tohgo, A, Kato, I, Ikehata, F, Yonekura, H & Okamoto, H (1997) Cyclic ADP-ribose binds to FK506-binding protein 12·6 to release Ca2+ from islet microsomes. Journal of Biological Chemistry 272, 3133–3136.CrossRefGoogle ScholarPubMed
Okamoto, H (1981) Regulation of proinsulin synthesis in pancreatic islets and a new aspect to insulin-dependent diabetes. Molecular and Cellular Biochemistry 37, 43–61.CrossRefGoogle Scholar
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
Okamoto, H (1990) The molecular basis of experimental diabetes. In. In Molecular Biology of the Islets of Langerhans [H Okamoto editor]. pp 209–231. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Okamoto, H (1999) The Reg gene family and Reg proteins: With special attention to the regeneration of pancreatic β-cells. Journal of Hepatobiliary Pancreatic Surgery 6, 254–262.CrossRefGoogle Scholar
Okamoto, H & Takasawa, S (2001) CD38. In. In Encyclopedia of Molecular Medicine [TE Creighton editor]. pp 601–604. New York, NY: Wiley & Sons: Inc.Google Scholar
Okamoto, H & Takasawa, S (2002) Recent advances in the Okamoto model: The CD38-cyclic ADP-ribose signal system and the regenerating gene protein (Reg)-Reg receptor system in β-cells. Diabetes 51, Suppl. 3, S462–S473.CrossRefGoogle ScholarPubMed
Okamoto, H, Takasawa, S & Nata, K (1997) The CD38–cyclic ADP-ribose signalling system in insulin secretion: Molecular basis and clinical implications. Diabetologia 40, 1485–1491.CrossRefGoogle ScholarPubMed
Okamoto, H, Takasawa, S, Nata, K, Kato, I, Tohgo, A & Noguchi, N (2000) Physiological and pathological significance of the CD38-cyclic ADP-ribose signaling system. Chemical Immunology 75, 121–145.Google ScholarPubMed
Okamoto, H, Takasawa, S & Tohgo, A (1995) New aspects of the physiological significance of NAD, poly ADP-ribose and cyclic ADP-ribose. Biochimie 77, 356–363.CrossRefGoogle ScholarPubMed
Okamoto, H, Yamamoto, H, Takasawa, S, Inoue, C, Terazono, K, Shiga, K & Kitagawa, M (1988) Molecular mechanism of degeneration, oncogenesis and regeneration of pancreatic B-cells of islets of Langerhans. In. In Lessons from Animal Diabetes II, [Shafrir, E and Renold, AE editors]. pp 149–157. London: John Libbey & Company Ltd.Google Scholar
Oliver, FJ, Menissier-de Murcia, J, Nacci, C, Decker, P, Andriantsitohaina, R, Muller, S, de la Rubia, G, Stoclet, JC & de Murcia, G (1999) Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO Journal 18, 4446–4454.CrossRefGoogle ScholarPubMed
Pacher, P, Liaudet, L, Soriano, FG, Mabley, JG, Szabó, E & 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.CrossRefGoogle ScholarPubMed
Partida-Sanchez, S, Coockayne, DA, Monard, S, Jacobson, EL, Oppenheimer, N, Garvy, B, Kusser, K, Goodrich, S, Howard, M, Harmsen, A, Randall, TD & 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 Medicine 7, 1209–1216.CrossRefGoogle ScholarPubMed
Pieper, AA, Brat, DJ, Krug, DK, Watkins, CC, Gupta, A, Blackshaw, S, Verma, A, Wang, ZQ & Snyder, SH (1999) Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocin-induced diabetes. Proceedings of the National Academy of Sciences USA 96, 3059–3064.CrossRefGoogle ScholarPubMed
Pieper, AA, Walles, T, Wei, G, Clements, EE, Verma, A, Snyder, SH & Zweier, JL (2000) Myocardial postischemic injury is reduced by polyADPribose polymerase-1 gene disruption. Molecular Medicine 6, 271–282.CrossRefGoogle ScholarPubMed
Plaschke, K, Kopitz, J, Weigand, MA, Martin, E & Bardenheuer, HJ (2000) The neuroprotective effect of cerebral poly(ADP-ribose)polymerase inhibition in a rat model of global ischemia. Neuroscience Letters 284, 109–112.CrossRefGoogle Scholar
Prakash, YS, Kannan, MS, Walseth, TF & Sieck, GC (1998) Role of cyclic ADP-ribose in the regulation of [Ca2+](i) in porcine tracheal smooth muscle. American Journal of Physiology 43, C1653–C1660.CrossRefGoogle Scholar
Pupilli, C, Giannini, S, Marchetti, P, Lupi, R, Antonelli, A, Malavasi, F, Takasawa, S, Okamoto, H & 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.CrossRefGoogle Scholar
Rakieten, N, Rakieten, ML & Nadkarni, MV (1963) Studies on the diabetogenic action of streptozotocin. Cancer Chemotherapy Reports 29, 91–98.Google ScholarPubMed
Rakovic, S, Cui, Y, Iino, S, Galione, A, Ashamu, GA, Potter, BV & Terrar, DA (1999) An antagonist of cADP-ribose inhibits arrhythmogenic oscillations of intracellular Ca2+ in heart cells. Journal of Biological Chemistry 274, 17820–17827.CrossRefGoogle ScholarPubMed
Rakovic, S, Galione, A, Ashamu, GA, Potter, BVL & Terrar, DA (1996) A specific cyclic ADP-ribose antagonist inhibits cardiac excitation-contraction coupling. Current Biology 6, 989–996.CrossRefGoogle ScholarPubMed
Reyes-Harde, M, Potter, BV, Galione, A & Stanton, PK (1999) Induction of hippocampal LTD requires nitric-oxide-stimulated PKG activity and Ca(2+) release from cyclic ADP-ribose-sensitive stores. Journal of Neurophysiology 82, 1569–1576.CrossRefGoogle Scholar
Rutter, GA, Theler, J-M & Wollheim, CB (1994) Ca2+ stores in insulin-secreting cells: lack of effect of cADP ribose. Cell Calcium 16, 71–80.CrossRefGoogle ScholarPubMed
Sasaki, T, Shimura, S, Takasawa, S, Nagaki, M, Satoh, M, Okamoto, H & 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. American Review of Respiratory Diseases 147, A936.Google Scholar
Sauter, B, Albert, ML, Francisco, L, Larsson, M, Somersan, S & 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. Journal of Experimental Medicine 191, 423–433.CrossRefGoogle ScholarPubMed
Shall, S (2002) Poly(ADP-ribosylation) – a common control process?. BioEssays 24, 197–201.CrossRefGoogle ScholarPubMed
Soriano, FG, Virag, L, Jagtap, P, Szabó, E, Mabley, JG, Liaudet, L, Marton, A, Hoyt, DG, Murthy, KGK, Salzman, AL, Southan, GJ & Szabó, C (2001) Diabetic endothelial dysfunction: the role of poly(ADP-ribose) polymerase activation. Nature Medicine 7, 108–113.CrossRefGoogle Scholar
Stern, Y, Salzman, A, Cotton, RT & Zingarelli, B (1999) Protective effect of 3-aminobenzamide, an inhibitor of poly (ADP-ribose) synthetase, against laryngeal injury in rats. American Journal of Respiratory and Critical Care Medicine 160, 1743–1749.CrossRefGoogle ScholarPubMed
Sugimura, T, Fujimura, S, Hasegawa, S & Kawamura, Y (1967) Polymerization of the adenosine 5′-diphosphate ribose moiety of NAD by rat liver nuclear enzyme. Biochimica et Biophysica Acta 138, 438–441.CrossRefGoogle Scholar
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 & Zaidi, M (1999) CD38/ADP-ribosyl cyclase: A new role in the regulation of osteoclastic bone resorption. Journal of Cell Biology 146, 1161–1172.CrossRefGoogle ScholarPubMed
Szabó, C, Cuzzocrea, S, Zingarelli, B, O'Connor, M & Salzman, AL (1997) Endothelial dysfunction in a rat model of endotoxic shock. Importance of the activation of poly (ADP-ribose) synthetase by peroxynitrite. Journal of Clinical Investigation 100, 723–735.CrossRefGoogle Scholar
Szabó, C, Virag, L, Cuzzocrea, S, Scott, GS, Hake, P, O'Connor, MP, Zingarelli, B, Salzman, A & Kun, E (1998) Protection against peroxynitrite-induced fibroblast injury and arthritis development by inhibition of poly(ADP-ribose) synthase. Proceedings of the National Academy of Sciences USA 95, 3867–3872.CrossRefGoogle ScholarPubMed
Takamura, T, Kato, I, Kimura, N, Nakazawa, T, Yonekura, H, Takasawa, S & Okamoto, H (1998) Transgenic mice overexpressing type 2 nitric oxide synthase in pancreatic β cells develop insulin-dependent diabetes without insulitis. Journal of Biological Chemistry 273, 2493–2496.CrossRefGoogle ScholarPubMed
Takasawa, S, Akiyama, T, Nata, K, Kuroki, M, Tohgo, A, Noguchi, N, Kobayashi, K, Kato, I, Katada, T & Okamoto, H (1998) Cyclic ADP-ribose and inositol 1,4,5-trisphosphate as alternate second messengers for intracellular Ca2+ mobilization in normal and diabetic β-cells. Journal of Biological Chemistry 273, 2497–2500.CrossRefGoogle ScholarPubMed
Takasawa, S, Ishida, A, Nata, K, Nakagawa, K, Noguchi, N, Tohgo, A, Kato, I, Yonekura, H, Fujisawa, H & Okamoto, H (1995) Requirement of calmodulin-dependent protein kinase II in cyclic ADP-ribose-mediated intracellular Ca2+ mobilization. Journal of Biological Chemistry 270, 30257–30259.CrossRefGoogle ScholarPubMed
Takasawa, S, Nata, K, Yonekura, H & Okamoto, H (1993) Cyclic ADP-ribose in insulin secretion from pancreatic β-cells. Science 259, 370–373.CrossRefGoogle ScholarPubMed
Takasawa, S, Nata, K, Yonekura, H, Tohgo, A & Okamoto, H (1994) A role of cyclic ADP-ribose, a NAD+ metabolite, in stimulus-secretion coupling in pancreatic B-cells. In. In Frontiers of Insulin Secretion and Pancreatic B-Cell Research [P Flatt and S Lenzen editors]. pp 123–128. London: Smith-Gordon.Google Scholar
Takasawa, S & Okamoto, H (2002) Pancreatic β-Cell death, regeneration and insulin secretion: Roles of poly(ADP-ribose) polymerase and cyclic ADP-ribose. International Journal of Experimental Diabetes Research 3, 79–96.CrossRefGoogle ScholarPubMed
Takasawa, S & Okamoto, H (2002) The CD38-cyclic ADP-ribose signal system in pancreatic β-cells. The discovery and biological significance of a novel signal system in mammalian cells. In Cyclic ADP-Ribose and NAADP: Structure, Metabolism and Functions [HC Lee editor]. pp 269–299. Dordrecht, the Netherlands: Kluwer.CrossRefGoogle Scholar
Takasawa, S, Tohgo, A, Noguchi, N, Koguma, T, Nata, K, Sugimoto, T, Yonekura, H & Okamoto, H (1993) Synthesis and hydrolysis of cyclic ADP-ribose by human leukocyte antigen CD38 and inhibition of the hydrolysis by ATP. Journal of Biological Chemistry 268, 26052–26054.CrossRefGoogle ScholarPubMed
Tanaka, Y & 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. Proceedings of the National Academy of Sciences USA 92, 3244–3248.CrossRefGoogle Scholar
Tang, W-X, Chen, Y-F, Zou, A-P, Campbell, WB & Li, P-L (2002) Role of FKBP12·6 in cADPR-induced activation of reconstituted ryanodine receptors from arterial smooth muscle. American Journal of Physiology 282, H1304–H1310.Google ScholarPubMed
Terazono, K, Yamamoto, H, Takasawa, S, Shiga, K, Yonemura, Y, Tochino, Y & Okamoto, H (1988) A novel gene activated in regenerating islets. Journal of Biological Chemistry 263, 2111–2114.CrossRefGoogle ScholarPubMed
Thorn, P, Gerashimenko, O & Petersen, OH (1994) Cyclic ADP-ribose regulation of ryanodine receptors involved in agonist evoked cytosolic Ca2+ oscillations in pancreatic acinar cells. EMBO Journal 13, 2038–2043.CrossRefGoogle ScholarPubMed
Tohgo, A, Munakata, H, Takasawa, S, Nata, K, Akiyama, T, Hayashi, N & 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. Journal of Biological Chemistry 272, 3879–3882.CrossRefGoogle ScholarPubMed
Tohgo, A, Takasawa, S, Noguchi, N, Koguma, T, Nata, K, Sugimoto, T, Furuya, Y, Yonekura, H & Okamoto, H (1994) Essential cysteine residues for cyclic ADP-ribose synthesis and hydrolysis by CD38. Journal of Biological Chemistry 269, 28555–28557.CrossRefGoogle ScholarPubMed
Tsao, BP, Cantor, RM, Grossman, JM, Shen, N, Teophilov, NT, Wallace, DJ, Arnett, FC, Hartung, K, Goldstein, R, Kalunian, KC, Hahn, BH & Rotter, JI (1999) PARP alleles within the linked chromosomal region are associated with systemic lupus erythematosus. Journal of Clinical Investigation 103, 1135–1140.CrossRefGoogle ScholarPubMed
Uchigata, Y, Yamamoto, H, Kawamura, A & 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. Journal of Biological Chemistry 257, 6084–6088.CrossRefGoogle ScholarPubMed
Uchigata, Y, Yamamoto, H, Nagai, H & 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.CrossRefGoogle ScholarPubMed
Ueda, K & Hayaishi, O (1985) ADP-ribosylation. Annual Review of Biochemistry 54, 73–100.CrossRefGoogle ScholarPubMed
Unno, M, Nata, K, Noguchi, N, Narushima, Y, Akiyama, T, Ikeda, T, Nakagawa, K, Takasawa, S & Okamoto, H (2002) Production and characterization of Reg knockout mice: Reduced proliferation of pancreatic β-cells in Reg knockout mice. Diabetes 51, Suppl. 3, S478–S483.CrossRefGoogle ScholarPubMed
Unno, M, Yonekura, H, Nakagawara, K, Watanabe, T, Miyashita, H, Moriizumi, S, Okamoto, H, Itoh, T & Teraoka, H (1993) Structure, chromosomal localization, and expression of mouse reg genes, reg I and reg II. A novel type of reg gene, reg II, exists in the mouse genome. Journal of Biological Chemistry 268, 15974–15982.CrossRefGoogle Scholar
Varadi, A & Rutter, GA (2002) Dynamic imaging of endoplasmic reticulum Ca2+ concentration in insulin-secreting MIN6 Cells using recombinant targeted cameleons: roles of sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA)-2 and ryanodine receptors. Diabetes 51, Suppl. 1, S190–S201.CrossRefGoogle ScholarPubMed
Von Mering, J & Minkowski, O (1890) Diabetes mellitus nach Pankreasexstirpation (Diabetes mellitus following pancreas removal). Archiv für Experimentelle Pathologie und Pharmakologie 26, 371–387.CrossRefGoogle Scholar
Watanabe, T, Yonekura, H, Terazono, K, Yamamoto, H & 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. Journal of Biological Chemistry 265, 7432–7439.CrossRefGoogle ScholarPubMed
Watanabe, T, Yonemura, Y, Yonekura, H, Suzuki, Y, Miyashita, H, Sugiyama, K, Moriizumi, S, Unno, M, Tanaka, O, Kondo, H, Bone, AJ, Takasawa, S & Okamoto, H (1994) Pancreatic beta-cell replication and amelioration of surgical diabetes by Reg protein. Proceedings of the National Academy of Sciences USA 91, 3589–3592.CrossRefGoogle ScholarPubMed
Webb, D-L, Islam, MS, Efanov, AM, Brown, G, Kohler, M, Larsson, O & Berggren, P-O (1996) Insulin exocytosis and glucose-mediated increase in cytoplasmic free Ca2+ concentration in the pancreatic β-cell are independent of cyclic ADP-ribose. Journal of Biological Chemistry 271, 19074–19079.CrossRefGoogle ScholarPubMed
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 & 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.CrossRefGoogle ScholarPubMed
Yamaki, H, Morita, K, Kitayama, S, Imai, Y, Itadani, K, Akagawa, Y & Doi, T (1998) Cyclic ADP-ribose induces Ca2+ release from caffeine-insensitive Ca2+ pools in canine salivary gland cells. Journal of Dental Research 77, 1807–1816.CrossRefGoogle ScholarPubMed
Yamamoto, H & 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. Biochemical and Biophysical Research Communications 95, 474–481.CrossRefGoogle ScholarPubMed
Yamamoto, H, Uchigata, Y & Okamoto, H (1981) Streptozotocin and alloxan induce DNA strand breaks and poly(ADP-ribose) synthetase in pancreatic islets. Nature 294, 284–286.CrossRefGoogle ScholarPubMed
Yamamoto, H, Uchigata, Y & Okamoto, H (1981) DNA strand breaks in pancreatic islets by in vivo administration of alloxan or streptozotocin. Biochemical and Biophysical Research Communications 103, 1014–1020.CrossRefGoogle ScholarPubMed
Yonemura, Y, Takashima, T, Miwa, K, Miyazaki, I, Yamamoto, H & Okamoto, H (1984) Amelioration of Diabetes mellitus in partially depancreatized rats by poly(ADP-ribose) synthetase inhibitors: Evidence of islet B-cell regeneration. Diabetes 33, 401–404.CrossRefGoogle ScholarPubMed
Zingarelli, B, Salzman, AL & Szabó, 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. Circulation Research 83, 85–94.CrossRefGoogle ScholarPubMed
Zingarelli, B, Szabó, C & Salzman, AL (1999) Blockade of poly(ADP-ribose) synthetase inhibits neutrophil recruitment, oxidant generation, and mucosal injury in murine colitis. Gastroenterology 116, 335–345.CrossRefGoogle ScholarPubMed