Mitochondrial Dysfunction and NAD+ Metabolism Alterations in the Pathophysiology of Acute Brain Injury

Translational Stroke Research

Volumn 4, Issue 6, 2013, Pages 618-634

  Owens, Katrina ^a   Park, Ji H ^a   Schuh, Rosemary ^a,b   Kristian, Tibor ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Brain; Ischemia; Mitochondria; Nicotinamide adenine dinucleotide

Indexed keywords

CD38 ANTIGEN; CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; GLYCOSIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; SILENT INFORMATION REGULATOR PROTEIN; SIRTUIN;

BIOSYNTHESIS; BRAIN DAMAGE; BRAIN INJURY; CATABOLISM; CYTOSOL; DEGRADATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME SYNTHESIS; GENOTOXICITY; MITOCHONDRIAL PERMEABILITY; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE METABOLISM; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; STRESS;

AGOUTI-RELATED PROTEIN; ANIMALS; ANTIGENS, CD38; BRAIN INJURIES; HUMANS; MICE; MITOCHONDRIA; NAD; POLY(ADP-RIBOSE) POLYMERASES;

EID: 84888299579     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-013-0278-x     Document Type: Review

References (251)

1. Kristian T. Metabolic stages, mitochondria and calcium in hypoxic/ischemic brain damage. Cell Calcium. 2004;36(3-4): 221-33.
2. Beal MF. Mitochondria take center stage in aging and neurodegeneration. Ann Neurol. 2005;58(4): 495-505.
3. Sullivan PG, Rabchevsky AG, Waldmeier PC, Springer JE. Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death? J Neurosci Res. 2005;79(1-2): 231-9.
4. Stavrovskaya IG, Kristal BS. The powerhouse takes control of the cell: is the mitochondrial permeability transition a viable therapeutic target against neuronal dysfunction and death? Free Radic Biol Med. 2005;38(6): 687-97.
5. Swerdlow RH. Brain aging, Alzheimer's disease, and mitochondria. Biochim Biophys Acta. 2011;1812(12): 1630-9.
6. Perez-Pinzon MA, Stetler RA, Fiskum G. Novel mitochondrial targets for neuroprotection. J Cereb Blood Flow Metab. 2012;32(7): 1362-76.
7. Chaturvedi RK, Flint Beal M. Mitochondrial diseases of the brain. Free Radic Biol Med. 2013;63: 1-29.
8. Kristian T, Gido G, Kuroda S, Schutz A, Siesjo BK. Calcium metabolism of focal and penumbral tissues in rats subjected to transient middle cerebral artery occlusion. Exp Brain Res. 1998;120(4): 503-9.
9. +] in the hippocampus during recovery from short-term, transient ischemia. J Cereb Blood Flow Metab. 1992;12(5): 759-72.
10. Dux E, Mies G, Hossmann KA, Siklos L. Calcium in the mitochondria following brief ischemia of gerbil brain. Neurosci Lett. 1987;78(3): 295-300.
11. Zaidan E, Sims NR. The calcium content of mitochondria from brain subregions following short-term forebrain ischemia and recirculation in the rat. J Neurochem. 1994;63(5): 1812-9.
12. Sims NR, Pulsinelli WA. Altered mitochondrial respiration in selectively vulnerable brain subregions following transient forebrain ischemia in the rat. J Neurochem. 1987;49(5): 1367-74.
13. Fujimura M, Morita-Fujimura Y, Murakami K, Kawase M, Chan PH. Cytosolic redistribution of cytochrome c after transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 1998;18(11): 1239-47.
14. Perez-Pinzon MA, Xu GP, Born J, Lorenzo J, Busto R, Rosenthal M, et al. Cytochrome C is released from mitochondria into the cytosol after cerebral anoxia or ischemia. J Cereb Blood Flow Metab. 1999;19(1): 39-43.
15. Sugawara T, Fujimura M, Morita-Fujimura Y, Kawase M, Chan PH. Mitochondrial release of cytochrome c corresponds to the selective vulnerability of hippocampal CA1 neurons in rats after transient global cerebral ischemia. J Neurosci. 1999;19(22): RC39.
16. Ouyang YB, Tan Y, Comb M, Liu CL, Martone ME, Siesjo BK, et al. Survival- and death-promoting events after transient cerebral ischemia: phosphorylation of Akt, release of cytochrome C and activation of caspase-like proteases. J Cereb Blood Flow Metab. 1999;19(10): 1126-35.
17. Nakahara I, Kikuchi H, Taki W, Nishi S, Kito M, Yonekawa Y, et al. Changes in major phospholipids of mitochondria during postischemic reperfusion in rat brain. J Neurosurg. 1992;76(2): 244-50.
18. Gilboe DD, Kintner D, Fitzpatrick JH, Emoto SE, Esanu A, Braquet PG, et al. Recovery of postischemic brain metabolism and function following treatment with a free radical scavenger and platelet-activating factor antagonists. J Neurochem. 1991;56(1): 311-9.
19. Wagner KR, Kleinholz M, Myers RE. Delayed decreases in specific brain mitochondrial electron transfer complex activities and cytochrome concentrations following anoxia/ischemia. J Neurol Sci. 1990;100(1-2): 142-51.
20. Allen KL, Almeida A, Bates TE, Clark JB. Changes of respiratory chain activity in mitochondrial and synaptosomal fractions isolated from the gerbil brain after graded ischaemia. J Neurochem. 1995;64(5): 2222-9.
21. Bernardi P. The permeability transition pore. Control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death. Biochim Biophys Acta. 1996;1275(1-2): 5-9.
22. Siesjo BK, Elmer E, Janelidze S, Keep M, Kristian T, Ouyang YB, et al. Role and mechanisms of secondary mitochondrial failure. Acta neurochirurgica Supplement. 1999;73: 7-13.
23. Knott AB, Bossy-Wetzel E. Impairing the mitochondrial fission and fusion balance: a new mechanism of neurodegeneration. Ann N Y Acad Sci. 2008;1147: 283-92.
24. Knott AB, Perkins G, Schwarzenbacher R, Bossy-Wetzel E. Mitochondrial fragmentation in neurodegeneration. Nat Rev Neurosci. 2008;9(7): 505-18.
25. Berman SB, Pineda FJ, Hardwick JM. Mitochondrial fission and fusion dynamics: the long and short of it. Cell Death Differ. 2008;15(7): 1147-52.
26. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337(6098): 1062-5.
27. Perkins G, Bossy-Wetzel E, Ellisman MH. New insights into mitochondrial structure during cell death. Exp Neurol. 2009;218(2): 183-92.
28. Anne Stetler R, Leak RK, Gao Y, Chen J. The dynamics of the mitochondrial organelle as a potential therapeutic target. J Cereb Blood Flow Metab. 2013;33(1): 22-32.
29. Reddy PH, Reddy TP, Manczak M, Calkins MJ, Shirendeb U, Mao P. Dynamin-related protein 1 and mitochondrial fragmentation in neurodegenerative diseases. Brain Res Rev. 2011;67(1-2): 103-18.
30. Johri A, Beal MF. Mitochondrial dysfunction in neurodegenerative diseases. J Pharmacol Exp Ther. 2012;342(3): 619-30.
31. Skaper SD. Poly(ADP-ribose) polymerase-1 in acute neuronal death and inflammation: a strategy for neuroprotection. Ann N Y Acad Sci. 2003;993: 217-28. discussion 87-8.
32. Kauppinen TM, Swanson RA. The role of poly(ADP-ribose) polymerase-1 in CNS disease. Neuroscience. 2007;145(4): 1267-72.
33. Ma Y, Chen H, He X, Nie H, Hong Y, Sheng C, et al. NAD+ metabolism and NAD(+)-dependent enzymes: promising therapeutic targets for neurological diseases. Current drug targets. 2012;13(2): 222-9.
34. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta. 1995;1241(2): 139-76.
35. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev. 1999;79(4): 1127-55.
36. Bernardi P, Petronilli V, Di Lisa F, Forte M. A mitochondrial perspective on cell death. Trends Biochem Sci. 2001;26(2): 112-7.
37. Crompton M, Barksby E, Johnson N, Capano M. Mitochondrial intermembrane junctional complexes and their involvement in cell death. Biochimie. 2002;84(2-3): 143-52.
38. Halestrap AP, McStay GP, Clarke SJ. The permeability transition pore complex: another view. Biochimie. 2002;84(2-3): 153-66.
39. Kristian T, Weatherby TM, Bates TE, Fiskum G. Heterogeneity of the calcium-induced permeability transition in isolated non-synaptic brain mitochondria. J Neurochem. 2002;83(6): 1297-308.
40. Chalmers S, Nicholls DG. The relationship between free and total calcium concentrations in the matrix of liver and brain mitochondria. J Biol Chem. 2003;278(21): 19062-70.
41. Kristian T, Gertsch J, Bates TE, Siesjo BK. Characteristics of the calcium-triggered mitochondrial permeability transition in nonsynaptic brain mitochondria: effect of cyclosporin A and ubiquinone O. J Neurochem. 2000;74(5): 1999-2009.
42. Brustovetsky N, Brustovetsky T, Purl KJ, Capano M, Crompton M, Dubinsky JM. Increased susceptibility of striatal mitochondria to calcium-induced permeability transition. J Neurosci. 2003;23(12): 4858-67.
43. 2+ overload than nonsynaptic mitochondria. J Biol Chem. 2006;281(17): 11658-68.
44. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem. 2001;276(4): 2571-5.
45. Kristian T, Fiskum G. A fluorescence-based technique for screening compounds that protect against damage to brain mitochondria. Brain Res Brain Res Protoc. 2004;13(3): 176-82.
46. Kristian T, Bernardi P, Siesjo BK. Acidosis promotes the permeability transition in energized mitochondria: implications for reperfusion injury. J Neurotrauma. 2001;18(10): 1059-74.
47. Garcia JH, Cox JV, Hudgins WR. Ultrastructure of the microvasculature in experimental cerebral infarction. Acta neuropathologica. 1971;18(4): 273-85.
48. Garcia JH, Kalimo H, Kamijyo Y, Trump BF. Cellular events during partial cerebral ischemia. Virchows Archiv B: Cell pathology. 1977;25(3): 191-206.
49. Petito CK. Transformation of postischemic perineuronal glial cells. I. Electron microscopic studies. J Cereb Blood Flow Metab. 1986;6(5): 616-24.
50. Pantoni L, Garcia JH, Gutierrez JA. Cerebral white matter is highly vulnerable to ischemia. Stroke. 1996;27(9): 1641-6. discussion 7.
51. Solenski NJ, diPierro CG, Trimmer PA, Kwan AL, Helm GA. Ultrastructural changes of neuronal mitochondria after transient and permanent cerebral ischemia. Stroke. 2002;33(3): 816-24.
52. Uchino H, Minamikawa-Tachino R, Kristian T, Perkins G, Narazaki M, Siesjo BK, et al. Differential neuroprotection by cyclosporin A and FK506 following ischemia corresponds with differing abilities to inhibit calcineurin and the mitochondrial permeability transition. Neurobiol Dis. 2002;10(3): 219-33.
53. Petito CK, Babiak T. Early proliferative changes in astrocytes in postischemic noninfarcted rat brain. Ann Neurol. 1982;11(5): 510-8.
54. Uchino H, Elmer E, Uchino K, Lindvall O, Siesjo BK. Cyclosporin A dramatically ameliorates CA1 hippocampal damage following transient forebrain ischaemia in the rat. Acta Physiol Scand. 1995;155(4): 469-71.
55. Uchino H, Elmer E, Uchino K, Li PA, He QP, Smith ML, et al. Amelioration by cyclosporin A of brain damage in transient forebrain ischemia in the rat. Brain Res. 1998;812(1-2): 216-26.
56. Friberg H, Ferrand-Drake M, Bengtsson F, Halestrap AP, Wieloch T. Cyclosporin A, but not FK 506, protects mitochondria and neurons against hypoglycemic damage and implicates the mitochondrial permeability transition in cell death. J Neurosci. 1998;18(14): 5151-9.
57. Yoshimoto T, Siesjo BK. Posttreatment with the immunosuppressant cyclosporin A in transient focal ischemia. Brain Res. 1999;839(2): 283-91.
58. Basso E, Fante L, Fowlkes J, Petronilli V, Forte MA, Bernardi P. Properties of the permeability transition pore in mitochondria devoid of cyclophilin D. J Biol Chem. 2005;280(19): 18558-61.
59. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature. 2005;434(7033): 658-62.
60. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature. 2005;434(7033): 652-8.
61. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, et al. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci U S A. 2005;102(34): 12005-10.
62. Alano CC, Tran A, Tao R, Ying W, Karliner JS, Swanson RA. Differences among cell types in NAD(+) compartmentalization: a comparison of neurons, astrocytes, and cardiac myocytes. J Neurosci Res. 2007;85(15): 3378-85.
63. Petronilli V, Nicolli A, Costantini P, Colonna R, Bernardi P. Regulation of the permeability transition pore, a voltage-dependent mitochondrial channel inhibited by cyclosporin A. Biochim Biophys Acta. 1994;1187(2): 255-9.
64. Shalbuyeva N, Brustovetsky T, Bolshakov A, Brustovetsky N. Calcium-dependent spontaneously reversible remodeling of brain mitochondria. J Biol Chem. 2006;281(49): 37547-58.
65. 2+ responses to physiological stimuli in adult neurons. Eur J Neurosci. 2011;33(5): 831-42.
66. Fiskum G, Danilov CA, Mehrabian Z, Bambrick LL, Kristian T, McKenna MC, et al. Postischemic oxidative stress promotes mitochondrial metabolic failure in neurons and astrocytes. Ann N Y Acad Sci. 2008;1147: 129-38.
67. +/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxidants & redox signaling. 2008;10(2): 179-206.
68. + depletion and mitochondrial permeability transition. J Biol Chem. 2004;279(18): 18895-902.
69. + depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci. 2010;30(8): 2967-78.
70. Chance B, Thorell B. Localization and kinetics of reduced pyridine nucleotide in living cells by microfluorometry. J Biol Chem. 1959;234: 3044-50.
71. Pittelli M, Formentini L, Faraco G, Lapucci A, Rapizzi E, Cialdai F, et al. Inhibition of nicotinamide phosphoribosyltransferase: cellular bioenergetics reveals a mitochondrial insensitive NAD pool. J Biol Chem. 2010;285(44): 34106-14.
72. + levels dictate cell survival. Cell. 2007;130(6): 1095-107.
73. + and vitamin B3: from metabolism to therapies. J Pharmacol Exp Ther. 2008;324(3): 883-93.
74. Silver I, Erecinska M. Oxygen and ion concentrations in normoxic and hypoxic brain cells. Adv Exp Med Biol. 1998;454: 7-16.
75. Pysh JJ, Khan T. Variations in mitochondrial structure and content of neurons and neuroglia in rat brain: an electron microscopic study. Brain Res. 1972;36(1): 1-18.
76. Deutsch C, Erecinska M, Werrlein R, Silver IA. Cellular energy metabolism, trans-plasma and trans-mitochondrial membrane potentials, and pH gradients in mouse neuroblastoma. Proc Natl Acad Sci U S A. 1979;76(5): 2175-9.
77. + transporter in Saccharomyces cerevisiae. J Biol Chem. 2006;281(3): 1524-31.
78. + between intact isolated plant mitochondria and suspending medium. Biochem J. 1983;216(2): 443-50.
79. Di Martino C, Pallota ML. Mitochondria-localized biosynthesis by nicotinamide mononucleotide adenylyltransferase in Jerusalem artichoke (Helianthus tuberosus L.) heterotrophic tissues. Planta. 2011;234(4): 657-70.
80. + carrier proteins. J Biol Chem. 2009;284(45): 31249-59.
81. Rustin P, Parfait B, Chretien D, Bourgeron T, Djouadi F, Bastin J, et al. Fluxes of nicotinamide adenine dinucleotides through mitochondrial membranes in human cultured cells. J Biol Chem. 1996;271(25): 14785-90.
82. Barile M, Passarella S, Danese G, Quagliariello E. Rat liver mitochondria can synthesize nicotinamide adenine dinucleotide from nicotinamide mononucleotide and ATP via a putative matrix nicotinamide mononucleotide adenylyltransferase. Biochem Mol Biol Int. 1996;38(2): 297-306.
83. +-dependent signalling. FEBS Lett. 2011;585(11): 1651-6.
84. +: an old metabolite controlling new metabolic signaling pathways. Endocr Rev. 2010;31(2): 194-223.
85. Sauve AA, Wolberger C, Schramm VL, Boeke JD. The biochemistry of sirtuins. Annu Rev Biochem. 2006;75: 435-65.
86. Michan S, Sinclair D. Sirtuins in mammals: insights into their biological function. Biochem J. 2007;404(1): 1-13.
87. Araki T, Sasaki Y, Milbrandt J. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science. 2004;305(5686): 1010-3.
88. Michishita E, Park JY, Burneskis JM, Barrett JC, Horikawa I. Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Molecular biology of the cell. 2005;16(10): 4623-35.
89. Jing E, Gesta S, Kahn CR. SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell metabolism. 2007;6(2): 105-14.
90. +-dependent tubulin deacetylase. Mol Cell. 2003;11(2): 437-44.
91. Vaziri H, Dessain SK, Ng Eaton E, Imai SI, Frye RA, Pandita TK, et al. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell. 2001;107(2): 149-59.
92. Haigis MC, Mostoslavsky R, Haigis KM, Fahie K, Christodoulou DC, Murphy AJ, et al. SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell. 2006;126(5): 941-54.
93. Liszt G, Ford E, Kurtev M, Guarente L. Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J Biol Chem. 2005;280(22): 21313-20.
94. Shi T, Wang F, Stieren E, Tong Q. SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J Biol Chem. 2005;280(14): 13560-7.
95. Feng R, Li S, Li F. Toll-like receptor 4 is involved in ischemic tolerance of postconditioning in hippocampus of tree shrews to thrombotic cerebral ischemia. Brain Res. 2011;1384: 118-27.
96. Morris KC, Lin HW, Thompson JW, Perez-Pinzon MA. Pathways for ischemic cytoprotection: role of sirtuins in caloric restriction, resveratrol, and ischemic preconditioning. J Cereb Blood Flow Metab. 2011;31(4): 1003-19.
97. Raghavan A, Shah ZA. Sirtuins in neurodegenerative diseases: a biological-chemical perspective. Neuro-degenerative diseases. 2012;9(1): 1-10.
98. Raval AP, Dave KR, Perez-Pinzon MA. Resveratrol mimics ischemic preconditioning in the brain. J Cereb Blood Flow Metab. 2006;26(9): 1141-7.
99. Raval AP, Lin HW, Dave KR, Defazio RA, Della Morte D, Kim EJ, et al. Resveratrol and ischemic preconditioning in the brain. Curr Med Chem. 2008;15(15): 1545-51.
100. Della-Morte D, Dave KR, DeFazio RA, Bao YC, Raval AP, Perez-Pinzon MA. Resveratrol pretreatment protects rat brain from cerebral ischemic damage via a sirtuin 1-uncoupling protein 2 pathway. Neuroscience. 2009;159(3): 993-1002.
101. + consumption by SIRT1 may endanger energetically compromised neurons. Neuromolecular medicine. 2009;11(1): 28-42.
102. Kakefuda K, Fujita Y, Oyagi A, Hyakkoku K, Kojima T, Umemura K, et al. Sirtuin 1 overexpression mice show a reference memory deficit, but not neuroprotection. Biochem Biophys Res Commun. 2009;387(4): 8.
103. Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, et al. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell. 2006;23(4): 607-18.
104. Ramponi G, Manao G, Camici G. Nonenzymatic acetylation of histones with acetyl phosphate and acetyl adenylate. Biochemistry. 1975;14(12): 2681-5.
105. Paik WK, Pearson D, Lee HW, Kim S. Nonenzymatic acetylation of histones with acetyl-CoA. Biochim Biophys Acta. 1970;213(2): 513-22.
106. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R, et al. Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol. 2007;27(24): 8807-14.
107. Fujino T, Kondo J, Ishikawa M, Morikawa K, Yamamoto TT. Acetyl-CoA synthetase 2, a mitochondrial matrix enzyme involved in the oxidation of acetate. J Biol Chem. 2001;276(14): 11420-6.
108. Ahn BH, Kim HS, Song S, Lee IH, Liu J, Vassilopoulos A, et al. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci U S A. 2008;105(38): 14447-52.
109. Hafner AV, Dai J, Gomes AP, Xiao CY, Palmeira CM, Rosenzweig A, et al. Regulation of the mPTP by SIRT3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy. Aging. 2010;2(12): 914-23.
110. Verdin E, Dequiedt F, Fischle W, Frye R, Marshall B, North B. Measurement of mammalian histone deacetylase activity. Methods Enzymol. 2004;377: 180-96.
111. +-dependent deacetylase SIRT5 by suramin. Structure. 2007;15(3): 377-89.
112. Schlicker C, Gertz M, Papatheodorou P, Kachholz B, Becker CF, Steegborn C. Substrates and regulation mechanisms for the human mitochondrial sirtuins Sirt3 and Sirt5. J Mol Biol. 2008;382(3): 790-801.
113. Kim SH, Lu HF, Alano CC. Neuronal Sirt3 protects against excitotoxic injury in mouse cortical neuron culture. PLoS One. 2011;6(3): e14731.
114. Yamada M, Mizuguchi M, Otsuka N, Ikeda K, Takahashi H. Ultrastructural localization of CD38 immunoreactivity in rat brain. Brain Res. 1997;756(1-2): 52-60.
115. Mizuguchi M, Otsuka N, Sato M, Ishii Y, Kon S, Yamada M, et al. Neuronal localization of CD38 antigen in the human brain. Brain Res. 1995;697(1-2): 235-40.
116. Ceni C, Pochon N, Brun V, Muller-Steffner H, Andrieux A, Grunwald D, et al. CD38-dependent ADP-ribosyl cyclase activity in developing and adult mouse brain. Biochem J. 2003;370(Pt 1): 175-83.
117. Verderio C, Bruzzone S, Zocchi E, Fedele E, Schenk U, De Flora A, et al. Evidence of a role for cyclic ADP-ribose in calcium signalling and neurotransmitter release in cultured astrocytes. J Neurochem. 2001;78(3): 646-57.
118. Mayo L, Jacob-Hirsch J, Amariglio N, Rechavi G, Moutin MJ, Lund FE, et al. Dual role of CD38 in microglial activation and activation-induced cell death. J Immunol. 2008;181(1): 92-103.
119. + glycohydrolase in cyclic ADP-ribose metabolism. Biochem Biophys Res Commun. 1998;253(2): 246-52.
120. Brailoiu E, Miyamoto MD. Inositol trisphosphate and cyclic adenosine diphosphate-ribose increase quantal transmitter release at frog motor nerve terminals: possible involvement of smooth endoplasmic reticulum. Neuroscience. 2000;95(4): 927-31.
121. Lee HC. Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol Rev. 1997;77(4): 1133-64.
122. Higashida H, Salmina AB, Olovyannikova RY, Hashii M, Yokoyama S, Koizumi K, et al. Cyclic ADP-ribose as a universal calcium signal molecule in the nervous system. Neurochem Int. 2007;51(2-4): 192-9.
123. Partida-Sanchez S, Cockayne DA, Monard S, Jacobson EL, Oppenheimer N, Garvy B, et al. 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. 2001;7(11): 1209-16.
124. Choe CU, Lardong K, Gelderblom M, Ludewig P, Leypoldt F, Koch-Nolte F, et al. CD38 exacerbates focal cytokine production, postischemic inflammation and brain injury after focal cerebral ischemia. PLoS One. 2011;6(5): e19046.
125. Kristian T, Balan I, Schuh R, Onken M. Mitochondrial dysfunction and nicotinamide dinucleotide catabolism as mechanisms of cell death and promising targets for neuroprotection. J Neurosci Res. 2011;89(12): 1946-55.
126. Ame JC, Spenlehauer C, de Murcia G. The PARP superfamily. BioEssays. 2004;26(8): 882-93.
127. Ha HC, Snyder SH. Poly(ADP-ribose) polymerase-1 in the nervous system. Neurobiol Dis. 2000;7(4): 225-39.
128. + depletion and cell death induced by oxidative stress. J Biol Chem. 2003;278(20): 18426-33.
129. Dawson VL, Dawson TM. Deadly conversations: nuclear-mitochondrial cross-talk. J Bioenerg Biomembr. 2004;36(4): 287-94.
130. Pieper AA, Blackshaw S, Clements EE, Brat DJ, Krug DK, White AJ, et al. Poly(ADP-ribosyl)ation basally activated by DNA strand breaks reflects glutamate-nitric oxide neurotransmission. Proc Natl Acad Sci U S A. 2000;97(4): 1845-50.
131. Davidovic L, Vodenicharov M, Affar EB, Poirier GG. Importance of poly(ADP-ribose) glycohydrolase in the control of poly(ADP-ribose) metabolism. Exp Cell Res. 2001;268(1): 7-13.
132. Herceg Z, Wang ZQ. Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat Res. 2001;477(1-2): 97-110.
133. Kraus WL, Lis JT. PARP goes transcription. Cell. 2003;113(6): 677-83.
134. Ullrich O, Diestel A, Bechmann I, Homberg M, Grune T, Hass R, et al. Turnover of oxidatively damaged nuclear proteins in BV-2 microglial cells is linked to their activation state by poly-ADP-ribose polymerase. FASEB J. 2001;15(8): 1460-2.
135. Andrabi SA, Kim NS, Yu SW, Wang H, Koh DW, Sasaki M, et al. Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci U S A. 2006;103(48): 18308-13.
136. Endres M, Wang ZQ, Namura S, Waeber C, Moskowitz MA. Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase. J Cereb Blood Flow Metab. 1997;17(11): 1143-51.
137. Szabo C, Dawson VL. Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion. Trends Pharmacol Sci. 1998;19(7): 287-98.
138. Whalen MJ, Clark RS, Dixon CE, Robichaud P, Marion DW, Vagni V, et al. Reduction of cognitive and motor deficits after traumatic brain injury in mice deficient in poly(ADP-ribose) polymerase. J Cereb Blood Flow Metab. 1999;19(8): 835-42.
139. Chiarugi A, Moskowitz MA. Poly(ADP-ribose) polymerase-1 activity promotes NF-kappaB-driven transcription and microglial activation: implication for neurodegenerative disorders. J Neurochem. 2003;85(2): 306-17.
140. Chiarugi A. Intrinsic mechanisms of poly(ADP-ribose) neurotoxicity: three hypotheses. Neurotoxicology. 2005;26(5): 847-55.
141. Berger F, Ramirez-Hernandez MH, Ziegler M. The new life of a centenarian: signalling functions of NAD(P). Trends Biochem Sci. 2004;29(3): 111-8.
142. Yang J, Klaidman LK, Nalbandian A, Oliver J, Chang ML, Chan PH, et al. The effects of nicotinamide on energy metabolism following transient focal cerebral ischemia in Wistar rats. Neurosci Lett. 2002;333(2): 91-4.
143. Ying W, Chen Y, Alano CC, Swanson RA. Tricarboxylic acid cycle substrates prevent PARP-mediated death of neurons and astrocytes. J Cereb Blood Flow Metab. 2002;22(7): 774-9.
144. Nagayama T, Simon RP, Chen D, Henshall DC, Pei W, Stetler RA, et al. Activation of poly(ADP-ribose) polymerase in the rat hippocampus may contribute to cellular recovery following sublethal transient global ischemia. J Neurochem. 2000;74(4): 1636-45.
145. Paschen W, Olah L, Mies G. Effect of transient focal ischemia of mouse brain on energy state and NAD levels: no evidence that NAD depletion plays a major role in secondary disturbances of energy metabolism. J Neurochem. 2000;75(4): 1675-80.
146. Goto S, Xue R, Sugo N, Sawada M, Blizzard KK, Poitras MF, et al. Poly(ADP-ribose) polymerase impairs early and long-term experimental stroke recovery. Stroke. 2002;33(4): 1101-6.
147. + and nicotinamide: sex differences in cerebral ischemia. Neuroscience. 2013;237: 223-31.
148. Chiarugi A. Poly(ADP-ribose) polymerase: killer or conspirator? The 'suicide hypothesis' revisited. Trends Pharmacol Sci. 2002;23(3): 122-9.
149. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, et al. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science. 2002;297(5579): 259-63.
150. Hong SJ, Dawson TM, Dawson VL. Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling. Trends Pharmacol Sci. 2004;25(5): 259-64.
151. Komjati K, Mabley JG, Virag L, Southan GJ, Salzman AL, Szabo C. Poly(ADP-ribose) polymerase inhibition protect neurons and the white matter and regulates the translocation of apoptosis-inducing factor in stroke. Int J Mol Med. 2004;13(3): 373-82.
152. Dumitriu IE, Voll RE, Kolowos W, Gaipl US, Heyder P, Kalden JR, et al. UV irradiation inhibits ABC transporters via generation of ADP-ribose by concerted action of poly(ADP-ribose) polymerase-1 and glycohydrolase. Cell Death Differ. 2004;11(3): 314-20.
153. Moss J, Stanley SJ, Levine RL. Inactivation of bacterial glutamine synthetase by ADP-ribosylation. J Biol Chem. 1990;265(34): 21056-60.
154. Seman M, Adriouch S, Haag F, Koch-Nolte F. Ecto-ADP-ribosyltransferases (ARTs): emerging actors in cell communication and signaling. Curr Med Chem. 2004;11(7): 857-72.
155. Huang HY, Graves DJ, Robson RM, Huiatt TW. ADP-ribosylation of the intermediate filament protein desmin and inhibition of desmin assembly in vitro by muscle ADP-ribosyltransferase. Biochem Biophys Res Commun. 1993;197(2): 570-7.
156. Zolkiewska A, Nightingale MS, Moss J. Molecular characterization of NAD: arginine ADP-ribosyltransferase from rabbit skeletal muscle. Proc Natl Acad Sci U S A. 1992;89(23): 11352-6.
157. Glowacki G, Braren R, Firner K, Nissen M, Kuhl M, Reche P, et al. The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse. Protein Sci. 2002;11(7): 1657-70.
158. Okazaki IJ, Moss J. Characterization of glycosylphosphatidylinositiol-anchored, secreted, and intracellular vertebrate mono-ADP-ribosyltransferases. Annu Rev Nutr. 1999;19: 485-509.
159. Moss J, Zolkiewska A, Okazaki I. ADP-ribosylarginine hydrolases and ADP-ribosyltransferases. Partners in ADP-ribosylation cycles. Adv Exp Med Biol. 1997;419: 25-33.
160. Shi W, Gong P, Fan J, Yan YH, Ni L, Wu X, et al. The expression pattern of ADP-ribosyltransferase 3 in rat traumatic brain injury. J Mol Histol. 2012;43(1): 37-47.
161. Matsuyama S, Tsuyama S. Mono-ADP-ribosylation in brain: purification and characterization of ADP-ribosyltransferases affecting actin from rat brain. J Neurochem. 1991;57(4): 1380-7.
162. Coggins PJ, McLean K, Nagy A, Zwiers H. ADP-ribosylation of the neuronal phosphoprotein B-50/GAP-43. J Neurochem. 1993;60(1): 368-71.
163. Benowitz LI, Perrone-Bizzozero NI. The expression of GAP-43 in relation to neuronal growth and plasticity: when, where, how, and why? Prog Brain Res. 1991;89: 69-87.
164. Koch-Nolte F, Adriouch S, Bannas P, Krebs C, Scheuplein F, Seman M, et al. ADP-ribosylation of membrane proteins: unveiling the secrets of a crucial regulatory mechanism in mammalian cells. Annals Med. 2006;38(3): 188-99.
165. Rankin PW, Jacobson EL, Benjamin RC, Moss J, Jacobson MK. Quantitative studies of inhibitors of ADP-ribosylation in vitro and in vivo. J Biol Chem. 1989;264(8): 4312-7.
166. Banasik M, Komura H, Shimoyama M, Ueda K. Specific inhibitors of poly(ADP-ribose) synthetase and mono(ADP-ribosyl)transferase. J Biol Chem. 1992;267(3): 1569-75.
167. Allport JR, Donnelly LE, Hayes BP, Murray S, Rendell NB, Ray KP, et al. Reduction by inhibitors of mono(ADP-ribosyl)transferase of chemotaxis in human neutrophil leucocytes by inhibition of the assembly of filamentous actin. Br J Pharmacol. 1996;118(5): 1111-8.
168. Kim JH, Yenari MA, Giffard RG, Cho SW, Park KA, Lee JE. Agmatine reduces infarct area in a mouse model of transient focal cerebral ischemia and protects cultured neurons from ischemia-like injury. Exp Neurol. 2004;189(1): 122-30.
169. Schuman EM, Meffert MK, Schulman H, Madison DV. An ADP-ribosyltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation. Proc Natl Acad Sci U S A. 1994;91(25): 11958-62.
170. Masmoudi A, Islam F, Mandel P. ADP-ribosylation of highly purified rat brain mitochondria. J Neurochem. 1988;51(1): 188-93.
171. Cervantes-Laurean D, Loflin PT, Minter DE, Jacobson EL, Jacobson MK. Protein modification by ADP-ribose via acid-labile linkages. J Biol Chem. 1995;270(14): 7929-36.
172. McDonald LJ, Moss J. Enzymatic and nonenzymatic ADP-ribosylation of cysteine. Mol Cell Biochem. 1994;138(1-2): 221-6.
173. Ayoub IA, Lee EJ, Ogilvy CS, Beal MF, Maynard KI. Nicotinamide reduces infarction up to two hours after the onset of permanent focal cerebral ischemia in Wistar rats. Neurosci Lett. 1999;259(1): 21-4.
174. Ayoub IA, Maynard KI. Therapeutic window for nicotinamide following transient focal cerebral ischemia. Neuroreport. 2002;13(2): 213-6.
175. Mokudai T, Ayoub IA, Sakakibara Y, Lee EJ, Ogilvy CS, Maynard KI. Delayed treatment with nicotinamide (vitamin B(3)) improves neurological outcome and reduces infarct volume after transient focal cerebral ischemia in Wistar rats. Stroke. 2000;31(7): 1679-85.
176. Spector R. Niacin and niacinamide transport in the central nervous system In vivo studies. J Neurochem. 1979;33(4): 895-904.
177. + prevents apoptosis in the mouse brain induced by tertiary-butylhydroperoxide. Neurosci Lett. 1996;206(1): 5-8.
178. +, as a PARP inhibitor and by partial restoration of mitochondrial function. Pharmacology. 2003;69(3): 150-7.
179. Klaidman LK, Mukherjee SK, Adams Jr JD. Oxidative changes in brain pyridine nucleotides and neuroprotection using nicotinamide. Biochim Biophys Acta. 2001;1525(1-2): 136-48.
180. Balan IS, Fiskum G, Kristian T. Visualization and quantification of NAD(H) in brain sections by a novel histo-enzymatic nitrotetrazolium blue staining technique. Brain Res. 2010;1316: 112-9.
181. Chong ZZ, Lin SH, Maiese K. Nicotinamide modulates mitochondrial membrane potential and cysteine protease activity during cerebral vascular endothelial cell injury. J Vasc Res. 2002;39(2): 131-47.
182. Mukherjee SK, Klaidman LK, Yasharel R, Adams Jr JD. Increased brain NAD prevents neuronal apoptosis in vivo. Eur J Pharmacol. 1997;330(1): 27-34.
183. Ungerstedt JS, Blomback M, Soderstrom T. Nicotinamide is a potent inhibitor of proinflammatory cytokines. Clin Exp Immunol. 2003;131(1): 48-52.
184. Althaus FR, Kleczkowska HE, Malanga M, Muntener CR, Pleschke JM, Ebner M, et al. Poly ADP-ribosylation: a DNA break signal mechanism. Mol Cell Biochem. 1999;193(1-2): 5-11.
185. Alvarez-Gonzalez R, Althaus FR. Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents. Mutat Res. 1989;218(2): 67-74.
186. Jacobson MK, Smith JY, Mingmuang M, Payne DM, Jacobson EL. Mono- and poly(ADP-ribose) metabolism following DNA damage. Princess Takamatsu Symposia. 1983;13: 165-74.
187. Jagtap P, Szabo C. Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov. 2005;4(5): 421-40.
188. Cervantes-Laurean D, Jacobson EL, Jacobson MK. Glycation and glycoxidation of histones by ADP-ribose. J Biol Chem. 1996;271(18): 10461-9.
189. Jacobson EL, Cervantes-Laurean D, Jacobson MK. ADP-ribose in glycation and glycoxidation reactions. Adv Exp Med Biol. 1997;419: 371-9.
190. + channels in rat ventricular myocytes. Am J Physiol. 1996;271(2 Pt 1): C464-8.
191. Li PL, Zhang DX, Ge ZD, Campbell WB. Role of ADP-ribose in 11, 12-EET-induced activation of K(Ca) channels in coronary arterial smooth muscle cells. Am J Physiol Heart Circ Physiol. 2002;282(4): H1229-36.
192. Kuhn FJ, Heiner I, Luckhoff A. TRPM2: a calcium influx pathway regulated by oxidative stress and the novel second messenger ADP-ribose. Pflugers Archiv. 2005;451(1): 212-9.
193. Fernandez A, Ribeiro JM, Costas MJ, Pinto RM, Canales J, Cameselle JC. Specific ADP-ribose pyrophosphatase from Artemia cysts and rat liver: effects of nitroprusside, fluoride and ionic strength. Biochim Biophys Acta. 1996;1290(1): 121-7.
194. Ribeiro JM, Cameselle JC, Fernandez A, Canales J, Pinto RM, Costas MJ. Inhibition and ADP-ribose pyrophosphatase-I by nitric-oxide-generating systems: a mechanism linking nitric oxide to processes dependent on free ADP-ribose. Biochem Biophys Res Commun. 1995;213(3): 1075-81.
195. Mildvan AS, Xia Z, Azurmendi HF, Saraswat V, Legler PM, Massiah MA, et al. Structures and mechanisms of Nudix hydrolases. Arch Biochem Biophys. 2005;433(1): 129-43.
196. McLennan AG. The Nudix hydrolase superfamily. Cell Mol Life Sci. 2006;63(2): 123-43.
197. Gasmi L, Cartwright JL, McLennan AG. Cloning, expression and characterization of YSA1H, a human adenosine 5′-diphosphosugar pyrophosphatase possessing a MutT motif. Biochem J. 1999;344(Pt 2): 331-7.
198. Yang H, Slupska MM, Wei YF, Tai JH, Luther WM, Xia YR, et al. Cloning and characterization of a new member of the Nudix hydrolases from human and mouse. J Biol Chem. 2000;275(12): 8844-53.
199. Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, Schmitz C, et al. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature. 2001;411(6837): 595-9.
200. Perraud AL, Shen B, Dunn CA, Rippe K, Smith MK, Bessman MJ, et al. NUDT9, a member of the Nudix hydrolase family, is an evolutionarily conserved mitochondrial ADP-ribose pyrophosphatase. J Biol Chem. 2003;278(3): 1794-801.
201. Lin S, Gasmi L, Xie Y, Ying K, Gu S, Wang Z, et al. Cloning, expression and characterisation of a human Nudix hydrolase specific for adenosine 5′-diphosphoribose (ADP-ribose). Biochim Biophys Acta. 2002;1594(1): 127-35.
202. Knowles H, Li Y, Perraud AL. The TRPM2 ion channel, an oxidative stress and metabolic sensor regulating innate immunity and inflammation. Immunol Res. 2013;55(1-3): 241-8.
203. Jia J, Verma S, Nakayama S, Quillinan N, Grafe MR, Hurn PD, et al. Sex differences in neuroprotection provided by inhibition of TRPM2 channels following experimental stroke. J Cereb Blood Flow Metab. 2011;31(11): 2160-8.
204. Perraud AL, Takanishi CL, Shen B, Kang S, Smith MK, Schmitz C, et al. Accumulation of free ADP-ribose from mitochondria mediates oxidative stress-induced gating of TRPM2 cation channels. J Biol Chem. 2005;280(7): 6138-48.
205. + as a metabolic link between DNA damage and cell death. J Neurosci Res. 2005;79(1-2): 216-23.
206. Zhu K, Swanson RA, Ying W. NADH can enter into astrocytes and block poly(ADP-ribose) polymerase-1-mediated astrocyte death. Neuroreport. 2005;16(11): 1209-12.
207. Wang S, Xing Z, Vosler PS, Yin H, Li W, Zhang F, et al. Cellular NAD replenishment confers marked neuroprotection against ischemic cell death: role of enhanced DNA repair. Stroke. 2008;39(9): 2587-95.
208. Lu H, Burns D, Garnier P, Wei G, Zhu K, Ying W. P2X7 receptors mediate NADH transport across the plasma membranes of astrocytes. Biochem Biophys Res Commun. 2007;362(4): 946-50.
209. + fluxes in intact cells. FASEB J. 2001;15(1): 10-2.
210. Anderson CM, Bergher JP, Swanson RA. ATP-induced ATP release from astrocytes. J Neurochem. 2004;88(1): 246-56.
211. 2+ signaling. J Neurosci. 2006;26(5): 1378-85.
212. Nagasawa K, Escartin C, Swanson RA. Astrocyte cultures exhibit P2X7 receptor channel opening in the absence of exogenous ligands. Glia. 2009;57(6): 622-33.
213. Robson SC, Sevigny J, Zimmermann H. The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance. Purinergic Signal. 2006;2(2): 409-30.
214. Wink MR, Braganhol E, Tamajusuku AS, Lenz G, Zerbini LF, Libermann TA, et al. Nucleoside triphosphate diphosphohydrolase-2 (NTPDase2/CD39L1) is the dominant ectonucleotidase expressed by rat astrocytes. Neuroscience. 2006;138(2): 421-32.
215. Nagai K, Nagasawa K, Fujimoto S. Transport mechanisms for adenosine and uridine in primary-cultured rat cortical neurons and astrocytes. Biochem Biophys Res Commun. 2005;334(4): 1343-50.
216. Nagasawa K, Kawasaki F, Tanaka A, Nagai K, Fujimoto S. Characterization of guanine and guanosine transport in primary cultured rat cortical astrocytes and neurons. Glia. 2007;55(14): 1397-404.
217. Okuda H, Higashi Y, Nishida K, Fujimoto S, Nagasawa K. Contribution of P2X7 receptors to adenosine uptake by cultured mouse astrocytes. Glia. 2010;58(14): 1757-65.
218. Won SJ, Choi BY, Yoo BH, Sohn M, Ying W, Swanson RA, et al. Prevention of traumatic brain injury-induced neuron death by intranasal delivery of nicotinamide adenine dinucleotide. J Neurotrauma. 2012;29(7): 1401-9.
219. + synthesis. Adv Enzymol Relat Areas Mol Biol. 1999;73: 135-82, xi.
220. + metabolism in health and disease. Trends Biochem Sci. 2007;32(1): 12-9.
221. Jacobson EL, Dame AJ, Pyrek JS, Jacobson MK. Evaluating the role of niacin in human carcinogenesis. Biochimie. 1995;77(5): 394-8.
222. Collins PB, Chaykin S. The management of nicotinamide and nicotinic acid in the mouse. J Biol Chem. 1972;247(3): 778-83.
223. Garten A, Petzold S, Korner A, Imai S, Kiess W. Nampt: linking NAD biology, metabolism and cancer. Trends in endocrinology and metabolism. TEM. 2009;20(3): 130-8.
224. Tatibana M, Kita K, Taira M, Ishijima S, Sonoda T, Ishizuka T, et al. Mammalian phosphoribosyl-pyrophosphate synthetase. Adv Enzym Regul. 1995;35: 229-49.
225. Fukuhara A, Matsuda M, Nishizawa M, Segawa K, Tanaka M, Kishimoto K, et al. Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science. 2005;307(5708): 426-30.
226. Revollo JR, Grimm AA, Imai S. The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. J Biol Chem. 2004;279(49): 50754-63.
227. Sasaki Y, Araki T, Milbrandt J. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J Neurosci. 2006;26(33): 8484-91.
228. Kitani T, Okuno S, Fujisawa H. Growth phase-dependent changes in the subcellular localization of pre-B-cell colony-enhancing factor. FEBS Lett. 2003;544(1-3): 74-8.
229. Zhang W, Xie Y, Wang T, Bi J, Li H, Zhang LQ, et al. Neuronal protective role of PBEF in a mouse model of cerebral ischemia. J Cereb Blood Flow Metab. 2010;30(12): 1962-71.
230. Wang P, Xu TY, Guan YF, Tian WW, Viollet B, Rui YC, et al. Nicotinamide phosphoribosyltransferase protects against ischemic stroke through SIRT1-dependent adenosine monophosphate-activated kinase pathway. Ann Neurol. 2011;69(2): 360-74.
231. Wang P, Guan YF, Du H, Zhai QW, Su DF, Miao CY. Induction of autophagy contributes to the neuroprotection of nicotinamide phosphoribosyltransferase in cerebral ischemia. Autophagy. 2012;8(1): 77-87.
232. Manwani B, McCullough LD. Function of the master energy regulator adenosine monophosphate-activated protein kinase in stroke. J Neurosci Res. 2013;91: 1018-29.
233. Coleman MP, Freeman MR. Wallerian degeneration, wld(s), and nmnat. Annu Rev Neurosci. 2010;33: 245-67.
234. Raffaelli N, Sorci L, Amici A, Emanuelli M, Mazzola F, Magni G. Identification of a novel human nicotinamide mononucleotide adenylyltransferase. Biochem Biophys Res Commun. 2002;297(4): 835-40.
235. Emanuelli M, Carnevali F, Saccucci F, Pierella F, Amici A, Raffaelli N, et al. Molecular cloning, chromosomal localization, tissue mRNA levels, bacterial expression, and enzymatic properties of human NMN adenylyltransferase. J Biol Chem. 2001;276(1): 406-12.
236. Zhang X, Kurnasov OV, Karthikeyan S, Grishin NV, Osterman AL, Zhang H. Structural characterization of a human cytosolic NMN/NaMN adenylyltransferase and implication in human NAD biosynthesis. J Biol Chem. 2003;278(15): 13503-11.
237. Berger F, Lau C, Dahlmann M, Ziegler M. Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J Biol Chem. 2005;280(43): 36334-41.
238. Yahata N, Yuasa S, Araki T. Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J Neurosci. 2009;29(19): 6276-84.
239. Babetto E, Beirowski B, Russler EV, Milbrandt J, Diantonio A. The phr1 ubiquitin ligase promotes injury-induced axon self-destruction. Cell reports. 2013;3(5): 1422-9.
240. Ljungberg MC, Ali YO, Zhu J, Wu CS, Oka K, Zhai RG, et al. CREB-activity and nmnat2 transcription are down-regulated prior to neurodegeneration, while NMNAT2 over-expression is neuroprotective, in a mouse model of human tauopathy. Hum Mol Genet. 2012;21(2): 251-67.
241. Zhai RG, Zhang F, Hiesinger PR, Cao Y, Haueter CM, Bellen HJ. NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration. Nature. 2008;452(7189): 887-91.
242. Jayaram HN, Kusumanchi P, Yalowitz JA. NMNAT expression and its relation to NAD metabolism. Curr Med Chem. 2011;18(13): 1962-72.
243. Lai Y, Chen Y, Watkins SC, Nathaniel PD, Guo F, Kochanek PM, et al. Identification of poly-ADP-ribosylated mitochondrial proteins after traumatic brain injury. J Neurochem. 2008;104(6): 1700-11.
244. Meyer RG, Meyer-Ficca ML, Jacobson EL, Jacobson MK. Human poly(ADP-ribose) glycohydrolase (PARG) gene and the common promoter sequence it shares with inner mitochondrial membrane translocase 23 (TIM23). Gene. 2003;314: 181-90.
245. Meyer-Ficca ML, Meyer RG, Coyle DL, Jacobson EL, Jacobson MK. Human poly(ADP-ribose) glycohydrolase is expressed in alternative splice variants yielding isoforms that localize to different cell compartments. Exp Cell Res. 2004;297(2): 521-32.
246. Whatcott CJ, Meyer-Ficca ML, Meyer RG, Jacobson MK. A specific isoform of poly(ADP-ribose) glycohydrolase is targeted to the mitochondrial matrix by a N-terminal mitochondrial targeting sequence. Exp Cell Res. 2009;315(20): 3477-85.
247. Oka S, Kato J, Moss J. Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J Biol Chem. 2006;281(2): 705-13.
248. Ono T, Kasamatsu A, Oka S, Moss J. The 39-kDa poly(ADP-ribose) glycohydrolase ARH3 hydrolyzes O-acetyl-ADP-ribose, a product of the Sir2 family of acetyl-histone deacetylases. Proc Natl Acad Sci U S A. 2006;103(45): 16687-91.
249. Mueller-Dieckmann C, Kernstock S, Lisurek M, von Kries JP, Haag F, Weiss MS, et al. The structure of human ADP-ribosylhydrolase 3 (ARH3) provides insights into the reversibility of protein ADP-ribosylation. Proc Natl Acad Sci U S A. 2006;103(41): 15026-31.
250. Nakagawa T, Lomb DJ, Haigis MC, Guarente L. SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell. 2009;137(3): 560-70.
251. Stein LR, Imai S. The dynamic regulation of NAD metabolism in mitochondria. Trends in endocrinology and metabolism. TEM. 2012;23(9): 420-8.