NAD+ and NADH in cellular functions and cell death

Frontiers in Bioscience

Volumn 11, Issue SUPPL. 3, 2006, Pages 3129-3148

  Ying, Weihai ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aging; Calcium; Cell death; Mitochondria; NAD+; NADH; Review

Indexed keywords

EID: 33744480316     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/2038     Document Type: Review

References (187)

1. Stryer, L. Biochemistry. W.H. Freeman and Company, New York (1995)
2. Veech, R. L., L. V. Eggleston & H. A. Krebs: The redox state of free nicotinamide-adenine dinucleotide phosphate in the cytoplasm of rat liver. Biochem J, 115, 609-19 (1969)
3. Stubbs, M., R. L. Veech & H. A. Krebs: Control of the redox state of the nicotinamide-adenine dinucleotide couple in rat liver cytoplasm. Biochem J, 126, 59-65 (1972)
4. Zhang, Q., D. W. Piston & R. H. Goodman: Regulation of corepressor function by nuclear NADH. Science, 295, 1895-7 (2002)
5. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem, 276, 2571-5 (2001)
6. Livingston, B. E., R. A. Altschuld & C. M. Hohl: Metabolic compartmentalization in neonatal swine myocytes. Pediatr Res, 40, 59-65 (1996)
7. Tischler, M. E., D. Friedrichs, K. Coll & J. R. Williamson: Pyridine nucleotide distributions and enzyme mass action ratios in hepatocytes from fed and starved rats. Arch Biochem Biophys, 184, 222-36 (1977)
8. + synthesis. Adv Enzymol Relat Areas Mol Biol, 73, 135-82, xi (1999)
9. + homeostasis in man. Cell Mol Life Sci, 61, 19-34 (2004)
10. Berger, F., C. Lau, M. Dahlmann & M. Ziegler: Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J Biol Chem, 280, 36334-41 (2005)
11. Raffaelli, N., L. Sorci, A. Amid, M. Emanuelli, F. Mazzola & G. Magni: Identification of a novel human nicotinamide mononucleotide adenylyltransferase. Biochem Biophys Res Commun, 297, 835-40 (2002)
12. Chi, N. W. & H. F. Lodish: Tankyrase is a golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles. J Biol Chem, 275, 38437-44 (2000)
13. Du, L., X. Zhang, Y. Y. Han, N. A. Burke, P. M. Kochanek, S. C. Watkins, S. H. Graham, J. A. Carcillo, C. Szabo & R. S. Clark: Intra-mitochondrial poly(ADP-ribosylation) contributes to NAD+ depletion and cell death induced by oxidative stress. J Biol Chem, 278, 18426-33 (2003)
14. Schweiger, M., K. Hennig, F. Lerner, M. Niere, M. Hirsch-Kauffmann, T. Specht, C. Weise, S. L. Oei & M. Ziegler: Characterization of recombinant human nicotinamide mononucleotide adenylyl transferase (NMNAT), a nuclear enzyme essential for NAD synthesis. FEBS Lett, 492, 95-100 (2001)
15. D'Amours, D., S. Desnoyers, I. D'Silva & G. G. Poirier: Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J, 342, 249-68 (1999)
16. Araki, T., Y. Sasaki & J. Milbrandt: Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science, 305, 1010-3 (2004)
17. Virag, L. & C. Szabo: The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev, 54, 375-429 (2002)
18. + as a metabolic link between DNA damage and cell death. J Neurosci Res, 79, 216-23 (2005)
19. Corda, D. & M. Di Girolamo: Functional aspects of protein mono-ADP-ribosylation. Embo J, 22, 1953-8 (2003)
20. Di Girolamo, M., N. Dani, A. Stilla & D. Corda: Physiological relevance of the endogenous mono(ADP-ribosyl)ation of cellular proteins. FEBS J, 272, 4565-75 (2005)
21. Blander, G. & L. Guarente: The Sir2 family of protein deacetylases. Annu Rev Biochem, 73, 417-35 (2004)
22. Ziegler, M.: New functions of a long-known molecule. Emerging roles of NAD in cellular signaling. Eur J Biochem, 267, 1550-64 (2000)
23. + Depletion Mediates PARP-1-induced astrocyte Death. 33th Annual Meeting of Amercan Society for Neurosciences Abstract (2003)
24. + depletion and mitochondrial permeability transition. J Biol Chem, 279, 18895-902 (2004)
25. McKenna, M. C., H. S. Waagepetersen, A. Schousboe & U. Sonnewald: Neuronal and astrocytic shuttle mechanisms for cytosolic-mitochondrial transfer of reducing equivalents: Current evidence and pharmacological tools. Biochem Pharmacol, 71, 399-407 (2006)
26. Waagepetersen, H. S., H. Qu, A. Schousboe & U. Sonnewald: Elucidation of the quantitative significance of pyruvate carboxylation in cultured cerebellar neurons and astrocytes. J Neurosci Res, 66, 763-70 (2001)
27. + fluxes in intact cells. FASEB J, 15, 10-2 (2001)
28. Verderio, C., S. Bruzzone, E. Zocchi, E. Fedele, U. Schenk, A. De Flora & M. Matteoli: Evidence of a role for cyclic ADP-ribose in calcium signalling and neurotransmitter release in cultured astrocytes. J Neurochem, 78, 646-57 (2001)
29. + repletion prevents PARP-1-induced glycolytic blockade and cell death in cultured mouse astrocytes. Biochem Biophys Res Commun, 308, 809-13 (2003)
30. Zhu, K., R. A. Swanson & W. Ying: NADH can enter into astrocytes and block poly(ADP-ribose) polymerase-1-mediated astrocyte death. Neuroreport, 16, 1209-12 (2005)
31. th American Society for Neurosciences Annual Meeting Abstracts (2005)
32. Berger, F., M. H. Ramirez-Hernandez & M. Ziegler: The new life of a centenarian: signalling functions of NAD(P). Trends Biochem Sci, 29, 111-8 (2004)
33. Rutter, J., M. Reick, L. C. Wu & S. L. McKnight: Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science, 293, 510-4 (2001)
34. Starai, V. J., I. Celic, R. N. Cole, J. D. Boeke & J. C. Escalante-Semerena: Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science, 298, 2390-2 (2002)
35. Rodgers, J. T., C. Lerin, W. Haas, S. P. Gygi, B. M. Spiegelman & P. Puigserver: Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature, 434, 113-8 (2005)
36. Zoratti, M. & I. Szabo: The mitochondrial permeability transition. Biochim Biophys Acta, 1241, 139-76 (1995)
37. Green, D. R. & J. C. Reed: Mitochondria and apoptosis. Science, 281, 1309-12 (1998)
38. La Piana, G., D. Marzulli, V. Gorgoglione & N. E. Lofrumento: Porin and cytochrome oxidase containing contact sites involved in the oxidation of cytosolic NADH. Arch Biochem Biophys, 436, 91-100 (2005)
39. Nicholls, D. G., S. L. Budd, M. W. Ward & R. F. Castilho: Excitotoxicity and mitochondria. Biochem Soc Symp, 66, 55-67 (1999)
40. Luo, J., A. Y. Nikolaev, S. Imai, D. Chen, F. Su, A. Shiloh, L. Guarente & W. Gu: Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell, 107, 137-48 (2001)
41. Langley, E., M. Pearson, M. Faretta, U. M. Bauer, R. A. Frye, S. Minucci, P. G. Pelicci & T. Kouzarides: Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. Embo J, 21, 2383-96 (2002)
42. Guse, A. H.: Second messenger function and the structure-activity relationship of cyclic adenosine diphosphoribose (cADPR). Febs J, 272, 4590-7 (2005)
43. Kuhn, F. J., I. Heiner & A. Luckhoff: TRPM2: a calcium influx pathway regulated by oxidative stress and the novel second messenger ADP-ribose. Pflugers Arch, 451, 212-9 (2005)
44. Gasser, A., G. Glassmeier, R. Fliegert, M. F. Langhorst, S. Meinke, D. Kein, S. Kruger, K. Weber, I. Heiner, N. Oppenheimer, J. R. Schwarz & A. H. Guse: Activation of T cell calcium influx by the second messenger ADP-ribose. J Biol Chem, 281, 2489-96 (2006)
45. Grubisha, O., L. A. Rafty, C. L. Takanishi, X. Xu, L. Tong, A. L. Perraud, A. M. Scharenberg & J. M. Denu: Metabolite of SIR2 reaction modulates TRPM2 ion channel. J Biol Chem, (In press; 2006)
46. Aswad, F., H. Kawamura & G. Dennert: High sensitivity of CD4+CD25+ regulatory T cells to extracellular metabolites nicotinamide adenine dinucleotide and ATP: a role for P2X7 receptors. J Immunol, 175, 3075-83 (2005)
47. North, R. A. & E. A. Barnard: Nucleotide receptors. Curr Opin Neurobiol, 7, 346-57 (1997)
48. Lee, J. M., G. J. Zipfel & D. W. Choi: The changing landscape of ischaemic brain injury mechanisms. Nature, 399, A7-14 (1999)
49. Lee, H. C.: Multiplicity of Ca2+ messengers and Ca2+ stores: a perspective from cyclic ADP-ribose and NAADP. Curr Mol Med, 4, 227-37 (2004)
50. Kolisek, M., A. Beck, A. Fleig & R. Penner: Cyclic ADP-ribose and hydrogen peroxide synergize with ADP-ribose in the activation of TRPM2 channels. Mol Cell, 18, 61-9 (2005)
51. Nilius, B. & T. Voets: TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Arch, 451, 1-10 (2005)
52. Ramsey, I. S., M. Delling & D. E. Clapham: An introduction to trp channels. Annu Rev Physiol, 68, 619-47 (2006)
53. Aarts, M. M. & M. Tymianski: TRPM7 and ischemic CNS injury. Neuroscientist, 11, 116-23 (2005)
54. MacDonald, J. F., Z. G. Xiong & M. F. Jackson: Paradox of Ca2+ signaling, cell death and stroke. Trends Neurosci, 29, 75-81 (2006)
55. Fonfria, E., I. C. Marshall, C. D. Benham, I. Boyfield, J. D. Brown, K. Hill, J. P. Hughes, S. D. Skaper & S. McNulty: TRPM2 channel opening in response to oxidative stress is dependent on activation of poly(ADP-ribose) polymerase. Br J Pharmacol, 143, 186-92 (2004)
56. Yang, K. T., W. L. Chang, P. C. Yang, C. L. Chien, M. S. Lai, M. J. Su & M. L. Wu: Activation of the transient receptor potential M2 channel and poly(ADP-ribose) polymerase is involved in oxidative stress-induced cardiomyocyte death. Cell Death Differ, (In press; 2006)
57. Fonfria, E., I. C. Marshall, I. Boyfield, S. D. Skaper, J. P. Hughes, D. E. Owen, W. Zhang, B. A. Miller, C. D. Benham & S. McNulty: Amyloid beta-peptide(1-42) and hydrogen peroxide-induced toxicity are mediated by TRPM2 in rat primary striatal cultures. J Neurochem, 95, 715-23 (2005)
58. Kaplin, A. I., S. H. Snyder & D. J. Linden: Reduced nicotinamide adenine dinucleotide-selective stimulation of inositol 1,4,5-trisphosphate receptors mediates hypoxic mobilization of calcium. J Neurosci, 16, 2002-11 (1996)
59. 2+ release via locally derived NADH. Proc Natl Acad Sci U S A, 102, 1357-9 (2005)
60. Zima, A. V., J. A. Copello & L. A. Blatter: Differential modulation of cardiac and skeletal muscle ryanodine receptors by NADH. FEBS Lett, 547, 32-6 (2003)
61. 2+ release in permeabilized rat ventricular myocytes. J Physiol, 555, 727-41 (2004)
62. Cherednichenko, G., A. V. Zima, W. Feng, S. Schaefer, L. A. Blatter & I. N. Pessah: NADH oxidase activity of rat cardiac sarcoplasmic reticulum regulates calcium-induced calcium release. Circ Res, 94, 478-86 (2004)
63. Wang, Z. Q., L. Stingl, C. Morrison, M. Jantsch, M. Los, K. Schulze-Osthoff & E. F. Wagner: PARP is important for genomic stability but dispensable in apoptosis. Genes Dev, 11, 2347-58 (1997)
64. Seimiya, H.: The telomeric PARP, tankyrases, as targets for cancer therapy. Br J Cancer, 94, 341-5 (2006)
65. Imai, S., C. M. Armstrong, M. Kaeberlein & L. Guarente: Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature, 403, 795-800 (2000)
66. Hisahara, S., S. Chiba, H. Matsumoto & Y. Horio: Transcriptional regulation of neuronal genes and its effect on neural functions: NAD-dependent histone deacetylase SIRT1 (Sir2alpha). J Pharmacol Sci, 98, 200-4 (2005)
67. Ford, E., R. Voit, G. Liszt, C. Magin, I. Grummt & L. Guarente: Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription. Genes Dev, (2006)
68. Jaeschke, H., C. Kleinwaechter & A. Wendel: NADH-dependent reductive stress and ferritin-bound iron in allyl alcohol-induced lipid peroxidation in vivo: the protective effect of vitamin E. Chem Biol Interact, 81, 57-68 (1992)
69. Zhang, Z., D. R. Blake, C. R. Stevens, J. M. Kanczler, P. G. Winyard, M. C. Symons, M. Benboubetra & R. Harrison: A reappraisal of xanthine dehydrogenase and oxidase in hypoxic reperfusion injury: the role of NADH as an electron donor. Free Radic Res, 28, 151-64 (1998)
70. Kaeberlein, M., M. McVey & L. Guarente: The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev, 13, 2570-80 (1999)
71. Tissenbaum, H. A. & L. Guarente: Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature, 410, 227-30 (2001)
72. Lin, S. J., E. Ford, M. Haigis, G. Liszt & L. Guarente: Calorie restriction extends yeast life span by lowering the level of NADH. Genes Dev, 18, 12-6 (2004)
73. Mostoslavsky, R., K. F. Chua, D. B. Lombard, W. W. Pang, M. R. Fischer, L. Gellon, P. Liu, G. Mostoslavsky, S. Franco, M. M. Murphy, K. D. Mills, P. Patel, J. T. Hsu, A. L. Hong, E. Ford, H. L. Cheng, C. Kennedy, N. Nunez, R. Bronson, D. Frendewey, W. Auerbach, D. Valenzuela, M. Karow, M. O. Hottiger, S. Bursting, J. C. Barrett, L. Guarente, R. Mulligan, B. Demple, G. D. Yancopoulos & F. W. Alt: Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell, 124, 315-29 (2006)
74. Kennedy, B. K., E. D. Smith & M. Kaeberlein: The enigmatic role of Sir2 in aging. Cell, 123, 548-50 (2005)
75. Fabrizio, P., C. Gattazzo, L. Battistella, M. Wei, C. Cheng, K. McGrew & V. D. Longo: Sir2 blocks extreme life-span extension. Cell, 123, 655-67 (2005)
76. Blasco, M. A.: Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet, 6, 611-22 (2005)
77. Smogorzewska, A. & T. de Lange: Regulation of telomerase by telomeric proteins. Annu Rev Biochem, 73, 177-208 (2004)
78. Grube, K. & A. Burkle: Poly(ADP-ribose) polymerase activity in mononuclear leukocytes of 13 mammalian species correlates with species-specific life span. Proc Natl Acad Sci U S A, 89, 11759-63 (1992)
79. Burkle, A., J. Diefenbach, C. Brabeck & S. Beneke: Ageing and PARP. Pharmacol Res, 52, 93-9 (2005)
80. von Kobbe, C., J. A. Harrigan, A. May, P. L. Opresko, L. Dawut, W. H. Cheng & V. A. Bohr: Central role for the Werner syndrome protein/poly(ADP-ribose) polymerase 1 complex in the poly(ADP-ribosyl)ation pathway after DNA damage. Mol Cell Biol, 23, 8601-13 (2003)
81. von Kobbe, C., J. A. Harrigan, V. Schreiber, P. Stiegler, J. Piotrowski, L. Dawut & V. A. Bohr: Poly(ADP-ribose) polymerase 1 regulates both the exonuclease and helicase activities of the Werner syndrome protein. Nucleic Acids Res, 32, 4003-14 (2004)
82. Sohal, R. S. & R. Weindruch: Oxidative stress, caloric restriction, and aging. Science, 273, 59-63 (1996)
83. Ying, W.: Deleterious network hypothesis of aging. Med Hypotheses, 48, 143-8 (1997)
84. Hasmann, M. & I. Schemainda: FK866, a highly specific noncompetitive inhibitor of nicotinamide phosphoribosyltransferase, represents a novel mechanism for induction of tumor cell apoptosis. Cancer Res, 63, 7436-42 (2003)
85. Graziani, G., F. Battaini & J. Zhang: PARP-1 inhibition to treat cancer, ischemia, inflammation. Pharmacol Res, 52, 1-4 (2005)
86. Hahn, W. C.: Role of telomeres and telomerase in the pathogenesis of human cancer. J Clin Oncol, 21, 2034-43 (2003)
87. Seimiya, H., Y. Muramatsu, T. Ohishi & T. Tsuruo: Tankyrase 1 as a target for telomere-directed molecular cancer therapeutics. Cancer Cell, 7, 25-37 (2005)
88. Ford, J., M. Jiang & J. Milner: Cancer-specific functions of SIRT1 enable human epithelial cancer cell growth and survival. Cancer Res, 65, 10457-63 (2005)
89. Chen, W. Y., D. H. Wang, R. C. Yen, J. Luo, W. Gu & S. B. Baylin: Tumor suppressor HIC1 directly regulates SIRT1 to modulate p53-dependent DNA-damage responses. Cell, 123, 437-48 (2005)
90. Bruzzone, S., A. De Flora, C. Usai, R. Graeff & H. C. Lee: Cyclic ADP-ribose is a second messenger in the lipopolysaccharide-stimulated proliferation of human peripheral blood mononuclear cells. Biochem J, 375, 395-403 (2003)
91. Seman, M., S. Adriouch, F. Scheuplein, C. Krebs, D. Freese, G. Glowacki, P. Deterre, F. Haag & F. Koch-Nolte: NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity, 19, 571-82 (2003)
92. Chan, P. H.: Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab, 21, 2-14 (2001)
93. Nagayama, T., J. Lan, D. C. Henshall, D. Chen, C. O'Horo, R. P. Simon & J. Chen: Induction of oxidative DNA damage in the peri-infarct region after permanent focal cerebral ischemia. J Neurochem, 75, 1716-28 (2000)
94. Lan, J., W. Li, F. Zhang, F. Y. Sun, T. Nagayama, C. O'Horo & J. Chen: Inducible repair of oxidative DNA lesions in the rat brain after transient focal ischemia and reperfusion. J Cereb Blood Flow Metab, 23, 1324-39 (2003)
95. Chan, P. H.: Role of oxidants in ischemic brain damage. Stroke, 27, 1124-9 (1996)
96. Zhang, J., V. L. Dawson, T. M. Dawson & S. H. Snyder: Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science, 263, 687-9 (1994)
97. Eliasson, M. J., K. Sampei, A. S. Mandir, P. D. Hum, R. J. Traystman, J. Bao, A. Pieper, Z. Q. Wang, T. M. Dawson, S. H. Snyder & V. L. Dawson: Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat Med, 3, 1089-95 (1997)
98. Narasimhan, P., M. Fujimura, N. Noshita & P. H. Chan: Role of superoxide in poly(ADP-ribose) polymerase upregulation after transient cerebral ischemia. Brain Res Mol Brain Res, 113, 28-36 (2003)
99. Tokime, T., K. Nozaki, T. Sugino, H. Kikuchi, N. Hashimoto & K. Ueda: Enhanced poly(ADP-ribosyl)ation after focal ischemia in rat brain. J Cereb Blood Flow Metab, 18, 991-7 (1998)
100. Endres, M., Z. Q. Wang, S. Namura, C. Waeber & M. A. Moskowitz: Ischemic brain injury is mediated by the activation of poly(ADP- ribose)polymerase. J Cereb Blood Flow Metab, 17, 1143-51 (1997)
101. Love, S., R. Barber & G. K. Wilcock: Neuronal accumulation of poly(ADP-ribose) after brain ischaemia. Neuropathol Appl Neurobiol, 25, 98-103 (1999)
102. Goto, S., R. Xue, N. Sugo, M. Sawada, K. K. Blizzard, M. F. Poitras, D. C. Johns, T. M. Dawson, V. L. Dawson, B. J. Grain, R. J. Traystman, S. Mori & P. D. Hum: Poly(ADP-ribose) polymerase impairs early and long-term experimental stroke recovery. Stroke, 33, 1101-6 (2002)
103. Szabo, C. & V. L. Dawson: Role of poly(ADP-ribose) synthetase in inflammation and ischaemia- reperfusion. Trends Pharmacol Sci, 19, 287-98 (1998)
104. Wolozin, B. & N. Golts: Iron and Parkinson's disease. Neuroscientist, 8, 22-32 (2002)
105. Beal, M. F.: Mitochondrial dysfunction and oxidative damage in Alzheimer's and Parkinson's diseases and coenzyme Q10 as a potential treatment. J Bioenerg Biomembr, 36, 381-6 (2004)
106. Ying, W.: A new hypothesis of neurodegenerative diseases: the deleterious network hypothesis. Med Hypotheses, 47, 307-13 (1996)
107. Moreira, P. I., K. Honda, Q. Liu, M. S. Santos, C. R. Oliveira, G. Aliev, A. Nunomura, X. Zhu, M. A. Smith & G. Perry: Oxidative stress: the old enemy in Alzheimer's disease pathophysiology. Curr Alzheimer Res, 2, 403-8 (2005)
108. Zhu, X., A. K. Raina, H. G. Lee, G. Casadesus, M. A. Smith & G. Perry: Oxidative stress signalling in Alzheimer's disease. Brain Res, 1000, 32-9 (2004)
109. Mhatre, M., R. A. Floyd & K. Hensley: Oxidative stress and neuroinflammation in Alzheimer's disease and amyotrophic lateral sclerosis: common links and potential therapeutic targets. J Alzheimers Dis, 6, 147-57 (2004)
110. Keller, J. N., Q. Guo, F. W. Holtsberg, A. J. Bruce-Keller & M. P. Mattson: Increased sensitivity to mitochondrial toxin-induced apoptosis in neural cells expressing mutant presenilin-1 is linked to perturbed calcium homeostasis and enhanced oxyradical production. J Neurosci, 18, 4439-50 (1998)
111. Cosi, C., F. Colpaert, W. Koek, A. Degryse & M. Marien: Poly(ADP-ribose) polymerase inhibitors protect against MPTP-induced depletions of striatal dopamine and cortical noradrenaline in C57B1/6 mice. Brain Res, 729, 264-9 (1996)
112. Mandir, A. S., C. M. Simbulan-Rosenthal, M. F. Poitras, J. R. Lumpkin, V. L. Dawson, M. E. Smulson & T. M. Dawson: A novel in vivo post-translational modification of p53 by PARP-1 in MPTP-induced parkinsonism. J Neurochem, 83, 186-92 (2002)
113. Mandir, A. S., S. Przedborski, V. Jackson-Lewis, Z. Q. Wang, C. M. Simbulan-Rosenthal, M. E. Smulson, B. E. Hoffman, D. B. Guastella, V. L. Dawson & T. M. Dawson: Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1, 2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism. Proc Natl Acad Sci U S A, 96, 5774-9 (1999)
114. Iwashita, A., S. Yamazaki, K. Mihara, K. Hattori, H. Yamamoto, J. Ishida, N. Matsuoka & S. Mutoh: Neuroprotective effects of a novel poly(ADP-ribose) polymerase-1 inhibitor, 2-[3-[4-(4-chlorophenyl)-1-piperazinyl] propyl]-4(3H)-quinazolinone (FR255595), in an in vitro model of cell death and in mouse 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J Pharmacol Exp Ther, 309, 1067-78 (2004)
115. Przedborski, S., V. Jackson-Lewis, R. Djaldetti, G. Liberatore, M. Vila, S. Vukosavic & G. Almer: The parkinsonian toxin MPTP: action and mechanism. Restor Neurol Neurosci, 16, 135-42 (2000)
116. Cecchi, C., C. Fiorillo, S. Sorbi, S. Latorraca, B. Nacmias, S. Bagnoli, P. Nassi & G. Liguri: Oxidative stress and reduced antioxidant defenses in peripheral cells from familial Alzheimer's patients. Free Radic Biol Med, 33, 1372-9 (2002)
117. Hensley, K., D. A. Butterfield, N. Hall, P. Cole, R. Subramaniam, R. Mark, M. P. Mattson, W. R. Markesbery, M. E. Harris, M. Aksenov & et al.: Reactive oxygen species as causal agents in the neurotoxicity of the Alzheimer's disease-associated amyloid beta peptide. Ann N Y Acad Sci, 786, 120-34 (1996)
118. LaPlaca, M. C., J. Zhang, R. Raghupathi, J. H. Li, F. Smith, F. M. Bareyre, S. H. Snyder, D. I. Graham & T. K. McIntosh: Pharmacologic inhibition of poly(ADP-ribose) polymerase is neuroprotective following traumatic brain injury in rats. J Neurotrauma, 18, 369-76 (2001)
119. Pieper, A. A., D. J. Brat, D. K. Krug, C. C. Watkins, A. Gupta, S. Blackshaw, A. Verma, Z. Q. Wang & S. H. Snyder: Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocin-induced diabetes. Proc Natl Acad Sci U S A, 96, 3059-64 (1999)
120. Suh, S. W., K. Aoyama, Y. Chen, P. Garnier, Y. Matsumori, E. Gum, J. Liu & R. A. Swanson: Hypoglycemic neuronal death and cognitive impairment are prevented by poly(ADP-ribose) polymerase inhibitors administered after hypoglycemia. J Neurosci, 23, 10681-90 (2003)
121. Pieper, A. A., A. Verma, J. Zhang & S. H. Snyder: Poly (ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol Sci, 20, 171-81 (1999)
122. Berger, N. A.: Poly(ADP-ribose) in the cellular response to DNA damage. Radiat Res, 101, 4-15 (1985)
123. Yu, S. W., H. Wang, M. F. Poitras, C. Coombs, W. J. Bowers, H. J. Federoff, G. G. Poirier, T. M. Dawson & V. L. Dawson: Mediation of poly (ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science, 297, 259-63 (2002)
124. Ying, W., Y. Chen, C. C. Alano & R. A. Swanson: Tricarboxylic acid cycle substrates prevent PARP-mediated death of neurons and astrocytes. J Cereb Blood Flow Metab, 22, 774-9 (2002)
125. Pillai, J. B., A. Isbatan, S. Imai & M. P. Gupta: Poly (ADP-ribose) polymerase-1-dependent cardiac myocyte cell death during heart failure is mediated by NAD+ depletion and reduced Sir2alpha deacetylase activity. J Biol Chem, 280, 43121-30 (2005)
126. Kolthur-Seetharam, U., F. Dantzer, M. W. McBurney, G. de Murcia & P. Sassone-Corsi: Control of AIF-mediated Cell Death by the Functional Interplay of SIRT1 and PARP-1 in Response to DNA Damage. Cell Cycle, 5 (2006)
127. Hum, P. D., S. J. Vannucci & H. Hagberg: Adult or perinatal brain injury: does sex matter? Stroke, 36, 193-5 (2005)
128. McCullough, L. D., Z. Zeng, K. K. Blizzard, I. Debchoudhury & P. D. Hum: Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. J Cereb Blood Flow Metab, 25, 502-12 (2005)
129. Hagberg, H., M. A. Wilson, H. Matsushita, C. Zhu, M. Lange, M. Gustavsson, M. F. Poitras, T. M. Dawson, V. L. Dawson, F. Northington & M. V. Johnston: PARP-1 gene disruption in mice preferentially protects males from perinatal brain injury. J Neurochem, 90, 1068-75 (2004)
130. Davidovic, L., M. Vodenicharov, E. B. Affar & G. G. Poirier: Importance of poly(ADP-ribose) glycohydrolase in the control of poly(ADP-ribose) metabolism. Exp Cell Res, 268, 7-13 (2001)
131. Rossi, L., M. Denegri, M. Torti, G. G. Poirier & A. Ivana Scovassi: Poly(ADP-ribose) degradation by post-nuclear extracts from human cells. Biochimie, 84, 1229-35 (2002)
132. Ohashi, S., M. Kanai, S. Hanai, F. Uchiumi, H. Maruta, S. Tanuma & M. Miwa: Subcellular localization of poly(ADP-ribose) glycohydrolase in mammalian cells. Biochem Biophys Res Commun, 307, 915-21 (2003)
133. Uchiumi, F., D. Ikeda & S. Tanuma: Changes in the activities and gene expressions of poly(ADP-ribose) glycohydrolases during the differentiation of human promyelocytic leukemia cell line HL-60. Biochim Biophys Acta, 1676, 1-11 (2004)
134. Di Meglio, S., M. Denegri, S. Vallefuoco, F. Tramontano, A. I. Scovassi & P. Quesada: Poly(ADPR) polymerase-1 and poly(ADPR) glycohydrolase level and distribution in differentiating rat germinal cells. Mol Cell Biochem, 248, 85-91 (2003)
135. Ying, W. & R. A. Swanson: The poly(ADP-ribose) glycohydrolase inhibitor gallotannin blocks oxidative astrocyte death. Neuroreport, 11, 1385-8 (2000)
136. Ying, W., M. B. Sevigny, Y. Chen & R. A. Swanson: Poly(ADP-ribose) glycohydrolase mediates oxidative and excitotoxic neuronal death. Proc Natl Acad Sci U S A, 98, 12227-32 (2001)
137. Boulares, A. H., A. J. Zoltoski, Z. A. Sherif, A. G. Yakovlev & M. E. Smulson: The Poly(ADP-ribose) polymerase-1-regulated endonuclease DNAS1L3 is required for etoposide-induced internucleosomal DNA fragmentation and increases etoposide cytotoxicity in transfected osteosarcoma cells. Cancer Res, 62, 4439-44 (2002)
138. 2+-dependent endonuclease in apoptosis and its inhibition by Poly(ADP-ribose) polymerase. J Biol Chem, 275, 21302-8 (2000)
139. Cuzzocrea, S. & Z. Q. Wang: Role of poly(ADP-ribose) glycohydrolase (PARG) in shock, ischemia and reperfusion. Pharmacol Res, 52, 100-8 (2005)
140. Cuzzocrea, S., R. Di Paola, E. Mazzon, U. Cortes, T. Genovese, C. Muia, W. Li, W. Xu, J. H. Li, J. Zhang & Z. Q. Wang: PARG activity mediates intestinal injury induced by splanchnic artery occlusion and reperfusion. Faseb J, 19, 558-66 (2005)
141. Patel, N. S., U. Cortes, R. Di Poala, E. Mazzon, H. Mota-Filipe, S. Cuzzocrea, Z. Q. Wang & C. Thiemermann: Mice lacking the 110-kD isoform of poly(ADP-ribose) glycohydrolase are protected against renal ischemia/reperfusion injury. J Am Soc Nephrol, 16, 712-9 (2005)
142. Lu, X. C., E. Massuda, Q. Lin, W. Li, J. H. Li & J. Zhang: Post-treatment with a novel PARG inhibitor reduces infarct in cerebral ischemia in the rat. Brain Res, 978, 99-103 (2003)
143. Genovese, T., R. Di Paola, P. Catalano, J. H. Li, W. Xu, E. Massuda, A. P. Caputi, J. Zhang & S. Cuzzocrea: Treatment with a novel poly(ADP-ribose) glycohydrolase inhibitor reduces development of septic shock-like syndrome induced by zymosan in mice. Crit Care Med, 32, 1365-74 (2004)
144. Hwang, J. J., S. Y. Choi & J. Y. Koh: The role of NADPH oxidase, neuronal nitric oxide synthase and poly(ADP ribose) polymerase in oxidative neuronal death induced in cortical cultures by brain-derived neurotrophic factor and neurotrophin-4/5. J Neurochem, 82, 894-902 (2002)
145. Kim, Y. H. & J. Y. Koh: The role of NADPH oxidase and neuronal nitric oxide synthase in zinc- induced poly(ADP-ribose) polymerase activation and cell death in cortical culture. Exp Neurol, 177, 407-18 (2002)
146. Bakondi, E., P. Bai, K. Erdelyi, C. Szabo, P. Gergely & L. Virag: Cytoprotective effect of gallotannin in oxidatively stressed HaCaT keratinocytes: the role of poly(ADP-ribose) metabolism. Exp Dermatol, 13, 170-8 (2004)
147. Burns, D., W. Ying, P. Garnier & R. A. Swanson: Decreased expression of the full-length poly(ADP-ribose) glycohydrolase by antisensense oligonucletide treatment prevents PARP-1-mediated astrocyte death. 34th American Society for Neurosciences Annual Meeting Abstracts (2004)
148. Blenn, C., F. R. Althaus & M. Malanga: Poly(ADP-ribose) glycohydrolase silencing protects against H 2O 2-induced cell death. Biochem J, (2006)
149. Koh, D. W., A. M. Lawler, M. F. Poitras, M. Sasaki, S. Wattler, M. C. Nehls, T. Stoger, G. G. Poirier, V. L. Dawson & T. M. Dawson: Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc Natl Acad Sci U S A, 101, 17699-704 (2004)
150. Meyer, R. G., M. L. Meyer-Ficca, E. L. Jacobson & M. K. Jacobson: Human poly(ADP-ribose) glycohydrolase (PARG) gene and the common promoter sequence it shares with inner mitochondrial membrane translocase 23 (TIM23). Gene, 314, 181-90 (2003)
151. Kaminker, P. G., S. H. Kim, R. D. Taylor, Y. Zebarjadian, W. D. Funk, G. B. Morin, P. Yaswen & J. Campisi: TANK2, a new TRF1-associated poly(ADP-ribose) polymerase, causes rapid induction of cell death upon overexpression. J Biol Chem, 276, 35891-9 (2001)
152. Kofler, J., T. Otsuka, Z. Zhang, R. Noppens, M. R. Grafe, D. W. Koh, V. L. Dawson, J. M. de Murcia, P. D. Hurn & R. J. Traystman: Differential effect of PARP-2 deletion on brain injury after focal and global cerebral ischemia. J Cereb Blood Flow Metab, 26, 135-41 (2006)
153. Porter, A. G. & R. U. Janicke: Emerging roles of caspase-3 in apoptosis. Cell Death Differ, 6, 99-104 (1999)
154. Chen, J., T. Nagayama, K. Jin, R. A. Stetler, R. L. Zhu, S. H. Graham & R. P. Simon: Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci, 18, 4914-28 (1998)
155. Graham, S. H. & J. Chen: Programmed cell death in cerebral ischemia. J Cereb Blood Flow Metab, 21, 99-109 (2001)
156. Wang, K. K.: Calpain and caspase: can you tell the difference? Trends Neurosci, 23, 20-6 (2000)
157. Zong, W. X., D. Ditsworth, D. E. Bauer, Z. Q. Wang & C. B. Thompson: Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev, 18, 1272-82 (2004)
158. Zong, W. X. & C. B. Thompson: Necrotic death as a cell fate. Genes Dev, 20, 1-15 (2006)
159. Boulares, A. H., A. J. Zoltoski, Z. A. Sherif, A. Yakovlev & M. E. Smulson: Roles of DNA fragmentation factor and poly(ADP-ribose) polymerase-1 in sensitization of fibroblasts to tumor necrosis factor-induced apoptosis. Biochem Biophys Res Commun, 290, 796-801 (2002)
160. Nargi-Aizenman, J. L., C. M. Simbulan-Rosenthal, T. A. Kelly, M. E. Smulson & D. E. Griffin: Rapid activation of poly(ADP-ribose) polymerase contributes to Sindbis virus and staurosporine-induced apoptotic cell death. Virology, 293, 164-71 (2002)
161. West, J. D., C. Ji & L. J. Marnett: Modulation of DNA fragmentation factor 40 nuclease activity by poly(ADP-ribose) polymerase-1. J Biol Chem, 280, 15141-7 (2005)
162. Kim, J. W., J. Won, S. Sohn & C. O. Joe: DNA-binding activity of the N-terminal cleavage product of poly(ADP- ribose) polymerase is required for UV mediated apoptosis. J Cell Sci, 113, 955-61 (2000)
163. Garnier, P., W. Ying & R. A. Swanson: Ischemic preconditioning by caspase cleavage of poly(ADP-ribose) polymerase-1. J Neurosci, 23, 7967-73 (2003)
164. Affar, E. B., M. Germain, E. Winstall, M. Vodenicharov, R. G. Shah, G. S. Salvesen & G. G. Poirier: Caspase-3-mediated processing of poly(ADP-ribose) glycohydrolase during apoptosis. J Biol Chem, 276, 2935-42 (2001)
165. McGinnis, K. M., M. E. Gnegy, Y. H. Park, N. Mukerjee & K. K. Wang: Procaspase-3 and poly(ADP)ribose polymerase (PARP) are calpain substrates. Biochem Biophys Res Commun, 263, 94-9 (1999)
166. Neumar, R. W., Y. A. Xu, H. Gada, R. P. Guttmann & R. Siman: Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis. J Biol Chem, 278, 14162-7 (2003)
167. Gendron, M. C., N. Schrantz, D. Metivier, G. Kroemer, Z. Maciorowska, F. Sureau, S. Koester & P. X. Petit: Oxidation of pyridine nucleotides during Fas- and ceramide-induced apoptosis in Jurkat cells: correlation with changes in mitochondria, glutathione depletion, intracellular acidification and caspase 3 activation. Biochem J, 353, 357-67 (2001)
168. Yeung, F., J. E. Hoberg, C. S. Ramsey, M. D. Keller, D. R. Jones, R. A. Frye & M. W. Mayo: Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. Embo J, 23, 2369-80 (2004)
169. Wang, J., Q. Zhai, Y. Chen, E. Lin, W. Gu, M. W. McBurney & Z. He: A local mechanism mediates NAD-dependent protection of axon degeneration. J Cell Biol, 170, 349-55 (2005)
170. Plaschke, K., J. Kopitz, M. A. Weigand, E. Martin & H. J. Bardenheuer: The neuroprotective effect of cerebral poly(ADP-ribose)polymerase inhibition in a rat model of global ischemia. Neurosci Lett, 284, 109-12 (2000)
171. Kannurpatti, S. S. & N. B. Joshi: Energy metabolism and NAD-NADH redox state in brain slices in response to glutamate exposure and ischemia. Metab Brain Dis, 14, 33-43 (1999)
172. Nagayama, T., R. P. Simon, D. Chen, D. C. Henshall, W. Pei, R. A. Stetler & J. Chen: Activation of poly(ADP-ribose) polymerase in the rat hippocampus may contribute to cellular recovery following sublethal transient global ischemia. J Neurochem, 74, 1636-45 (2000)
173. Gobbel, G. T., M. Bellinzona, A. R. Vogt, N. Gupta, J. R. Fike & P. H. Chan: Response of postmitotic neurons to X-irradiation: implications for the role of DNA damage in neuronal apoptosis. J Neurosci, 18, 147-55 (1998)
174. 2+-endonuclease inhibitor aurintricarboxylic acid prevents peroxynitrite-induced DNA damage and death of murine astrocytes. Biochem Biophys Res Commun, 344, 881-86 (2006)
175. Visochek, L., R. A. Steingart, I. Vulih-Shultzman, R. Klein, E. Priel, I. Gozes & M. Cohen-Armon: PolyADP-ribosylation is involved in neurotrophic activity. J Neurosci, 25, 7420-8 (2005)
176. + depletion and ribosylation of 14-3-3gamma. J Neurochem, 85, 697-708 (2003)
177. Cohen-Armon, M., L. Visochek, A. Katzoff, D. Levitan, A. J. Susswein, R. Klein, M. Valbrun & J. H. Schwartz: Long-term memory requires polyADP-ribosylation. Science, 304, 1820-2 (2004)
178. Zlokovic, B. V., J. G. McComb, M. N. Lipovac, T. C. Chen, J. B. Mackic, J. Schneider, S. L. Gianotta & M. H. Weiss: Differential brain penetration of cerebroprotective drugs. Adv Exp Med Biol, 331, 117-20 (1993)
179. Ross, T. M., P. M. Martinez, J. C. Renner, R. G. Thorne, L. R. Hanson & W. H. Frey, 2nd: Intranasal administration of interferon beta bypasses the blood-brain barrier to target the central nervous system and cervical lymph nodes: a non-invasive treatment strategy for multiple sclerosis. J Neuroimmunol, 151, 66-77 (2004)
180. Wang, D., H. Lu & W. Ying: Intranasal delivery of gallotannin decreases ischemic brain damage in a rat model of transient focal ischemia with extended window of opportunity. 36th American Society for Neurosciences Annual Meeting Abstracts (In press; 2006)
181. + delivery decreases ischemic brain damage in a rat model of transient focal ischemia. 36th American Society for Neurosciences Annual Meeting Abstracts (In press; 2006)
182. Ying, W.: Deleterious network hypothesis of Alzheimer's disease. Med Hypotheses, 46, 421-8 (1996)
183. Ying, W.: Deleterious network: a testable pathogenetic concept of Alzheimer's disease. Gerontology, 43, 242-53 (1997)
184. Ying, W.: Deleterious network hypothesis of apoptosis. Med Hypotheses, 50, 393-8 (1998)
185. Mattson, M. P.: Calcium as sculptor and destroyer of neural circuitry. Exp Gerontol, 27, 29-49 (1992)
186. Kristian, T. & B. K. Siesjo: Calcium in ischemic cell death. Stroke, 29, 705-18 (1998)
187. Protein kinase functions. Eds: Woodgett J, Oxford University Press, USA (2000)