Mitochondrial dysfunction and nicotinamide dinucleotide catabolism as mechanisms of cell death and promising targets for neuroprotection

Journal of Neuroscience Research

Volumn 89, Issue 12, 2011, Pages 1946-1955

  Kristian, Tibor ^a   Balan, Irina ^a   Schuh, Rosemary ^a,b   Onken, Mitch ^a  

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

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Acute neurodegenerative disease; CD38; Cell death; Mitochondria; NAD catabolism

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD38 ANTIGEN; GLYCOSIDASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ALZHEIMER DISEASE; BRAIN DAMAGE; BRAIN INFARCTION; BRAIN MITOCHONDRION; CATABOLISM; CELL DEATH; CELL SPECIFICITY; CITRIC ACID CYCLE; DEGENERATIVE DISEASE; DNA DAMAGE; ENZYME ACTIVITY; GLIA; GLYCOLYSIS; HUMAN; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MULTIPLE SCLEROSIS; NERVE CELL; NERVE CELL NECROSIS; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNTHESIS;

ANIMALS; ANTIGENS, CD38; CELL DEATH; HUMANS; METABOLISM; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NAD; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS;

EID: 80053642559     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22626     Document Type: Review

References (108)

1. Aksoy P, White TA, Thompson M, Chini EN. 2006. Regulation of intracellular levels of NAD: a novel role for CD38. Biochem Biophys Res Commun 345: 1386-1392.
2. + depletion and mitochondrial permeability transition. J Biol Chem 279: 18895-18902.
3. + depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 30: 2967-2978.
4. Almeida A, Allen KL, Bates TE, Clark JB. 1995. Effect of reperfusion following cerebral ischaemia on the activity of the mitochondrial respiratory chain in the gerbil brain. J Neurochem 65: 1698-1703.
5. Anderson RE, Tan WK, Meyer FB. 1999. Brain acidosis, cerebral blood flow, capillary bed density, and mitochondrial function in the ischemic penumbra. J Stroke Cerebrovasc Dis 8: 368-379.
6. Araki T, Sasaki Y, Milbrandt J. 2004. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305: 1010-1013.
7. Ayoub IA, Maynard KI. 2002. Therapeutic window for nicotinamide following transient focal cerebral ischemia. Neuroreport 13: 213-216.
8. Ayoub IA, Lee EJ, Ogilvy CS, Beal MF, Maynard KI. 1999. Nicotinamide reduces infarction up to two hours after the onset of permanent focal cerebral ischemia in Wistar rats. Neurosci Lett 259: 21-24.
9. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD. 2005. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434: 658-662.
10. + glycohydrolase activity in rat brain sub-regions. Soc Neurosci Abstr 148.1.
11. Balan IS, Fiskum G, Kristian T. 2010. Visualization and quantification of NAD(H) in brain sections by a novel histo-enzymatic nitrotetrazolium blue staining technique. Brain Res 1316C: 112-119.
12. Basso E, Fante L, Fowlkes J, Petronilli V, Forte MA, Bernardi P. 2005. Properties of the permeability transition pore in mitochondria devoid of cyclophilin D. J Biol Chem 280: 18558-18561.
13. Beal MF. 2005. Mitochondria take center stage in aging and neurodegeneration. Ann Neurol 58: 495-505.
14. + metabolism in health and disease. Trends Biochem Sci 32: 12-19.
15. + metabolism. J Biol Chem 284: 158-164.
16. Berger F, Lau C, Dahlmann M, Ziegler M. 2005. Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J Biol Chem 280: 36334-36341.
17. Bernardi P. 1992. Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J Biol Chem 267: 8834-8839.
18. Bernardi P. 1999. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79: 1127-1155.
19. Bernardi P, Petronilli V, Di Lisa F, Forte M. 2001. A mitochondrial perspective on cell death. Trends Biochem Sci 26: 112-117.
20. + in fungi and humans. Cell 117: 495-502.
21. + precursor vitamins in human nutrition. Annu Rev Nutr 28: 115-130.
22. + glycohydrolase. Implications for the role of pyridine nucleotide hydrolysis in mitochondrial calcium fluxes. J Biol Chem 268: 4016-4020.
23. Brennan AM, Connor JA, Shuttleworth CW. 2006. NAD(P)H fluorescence transients after synaptic activity in brain slices: predominant role of mitochondrial function. J Cereb Blood Flow Metab 26: 1389-1406.
24. + and cyclic ADP-ribose metabolism and regulates intracellular calcium in 3T3 fibroblasts. J Biol Chem 276: 48300-48308.
25. Canevari L, Kuroda S, Bates TE, Clark JB, Siesjo BK. 1997. Activity of mitochondrial respiratory chain enzymes after transient focal ischemia in the rat. J Cereb Blood Flow Metab 17: 1166-1169.
26. Chiarugi A, Moskowitz MA. 2002. Cell biology. PARP-1-a perpetrator of apoptotic cell death? Science 297: 200-201.
27. Chong ZZ, Lin SH, Maiese K. 2002. Nicotinamide modulates mitochondrial membrane potential and cysteine protease activity during cerebral vascular endothelial cell injury. J Vasc Res 39: 131-147.
28. Clementi E, Riccio M, Sciorati C, Nistico G, Meldolesi J. 1996. The type 2 ryanodine receptor of neurosecretory PC12 cells is activated by cyclic ADP-ribose. Role of the nitric oxide/cGMP pathway. J Biol Chem 271: 17739-17745.
29. Crompton M. 2003. On the involvement of mitochondrial intermembrane junctional complexes in apoptosis. Curr Med Chem 10: 1473-1484.
30. 2+-dependent pore activated by oxidative stress in heart mitochondria. Biochem J 245: 915-918.
31. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 255: 357-360.
32. Crompton M, Barksby E, Johnson N, Capano M. 2002. Mitochondrial intermembrane junctional complexes and their involvement in cell death. Biochimie 84: 143-152.
33. + metabolism. FEBS Lett 492: 4-8.
34. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem 276: 2571-2575.
35. Du H, Guo L, Zhang W, Rydzewska M, Yan S. 2009. Cyclophilin D deficiency improves mitochondrial function and learning/memory in aging Alzheimer disease mouse model. Neurobiol Aging 10.1016/j.neurobiolaging.2009.03.003.
36. Dumont M, Lin MT, Beal MF. 2010. Mitochondria and antioxidant targeted therapeutic strategies for Alzheimer's disease. J Alzheimers Dis 20( Suppl 2): S633-S643.
37. Endres M, Wang ZQ, Namura S, Waeber C, Moskowitz MA. 1997. Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase. J Cereb Blood Flow Metab 17: 1143-1151.
38. Fiskum G. 2000. Mitochondrial participation in ischemic and traumatic neural cell death. J Neurotrauma 17: 843-855.
39. Fiskum G. 2004. Mechanisms of neuronal death and neuroprotection. J Neurosurg Anesthesiol 16: 108-110.
40. Formentini L, Moroni F, Chiarugi A. 2009. Detection and pharmacological modulation of nicotinamide mononucleotide (NMN) in vitro and in vivo. Biochem Pharmacol 77: 1612-1620.
41. Forte M, Gold BG, Marracci G, Chaudhary P, Basso E, Johnsen D, Yu X, Fowlkes J, Rahder M, Stem K, Bernardi P, Bourdette D. 2007. Cyclophilin D inactivation protects axons in experimental autoimmune encephalomyelitis, an animal model of multiple sclerosis. Proc Natl Acad Sci U S A 104: 7558-7563.
42. Franco L, Guida L, Bruzzone S, Zocchi E, Usai C, De Flora A. 1998. The transmembrane glycoprotein CD38 is a catalytically active transporter responsible for generation and influx of the second messenger cyclic ADP-ribose across membranes. FASEB J 12: 1507-1520.
43. Franco L, Bodrato N, Moreschi I, Usai C, Bruzzone S, Scarf i S, Zocchi E, De Flora A. 2006. Cyclic ADP-ribose is a second messenger in the lipopolysaccharide-stimulated activation of murine N9 microglial cell line. J Neurochem 99: 165-176.
44. Galione A. 1993. Cyclic ADP-ribose: a new way to control calcium. Science 259: 325-326.
45. Glass JD, Brushart TM, George EB, Griffin JW. 1993. Prolonged survival of transected nerve fibres in C57BL/Ola mice is an intrinsic characteristic of the axon. J Neurocytol 22: 311-321.
46. Greene JG, Greenamyre JT. 1996. Bioenergetics and glutamate excitotoxicity. Prog Neurobiol 48: 613-634.
47. 2+-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem J 268: 153-160.
48. Halestrap AP, McStay GP, Clarke SJ. 2002. The permeability transition pore complex: another view. Biochimie 84: 153-166.
49. Hazelton JL, Petrasheuskaya M, Fiskum G, Kristian T. 2009. Cyclophilin D is expressed predominantly in mitochondria of gamma-aminobutyric acidergic interneurons. J Neurosci Res 87: 1250-1259.
50. Heneka MT, Rodriguez JJ, Verkhratsky A. 2010. Neuroglia in neurodegeneration. Brain Res Rev 63: 189-211.
51. Hoffmann A, Kann O, Ohlemeyer C, Hanisch UK, Kettenmann H. 2003. Elevation of basal intracellular calcium as a central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. J Neurosci 23: 4410-4419.
52. Hotta T, Asai K, Fujita K, Kato T, Higashida H. 2000. Membrane-bound form of ADP-ribosyl cyclase in rat cortical astrocytes in culture. J Neurochem 74: 669-675.
53. Iqbal J, Kumar K, Sun L, Zaidi M. 2006. Selective up-regulation of the ADP-ribosyl cyclases CD38 and CD157 by TNF but not by RANK-L reveals differences in downstream signaling. Am J Physiol Renal Physiol 291: F557-566.
54. Kershman J. 1939. Genesis of microglia in the human brain. Arch Neurol Psychiatr 41: 24-50.
55. Kim SY, Gul R, Rah SY, Kim SH, Park SK, Im MJ, Kwon HJ, Kim UH. 2008. Molecular mechanism of ADP-ribosyl cyclase activation in angiotensin II signaling in murine mesangial cells. Am J Physiol Renal Physiol 294: F982-F989.
56. + prevents apoptosis in the mouse brain induced by tertiary-butylhydroperoxide. Neurosci Lett 206: 5-8.
57. Klaidman LK, Mukherjee SK, Adams JDJr. 2001. Oxidative changes in brain pyridine nucleotides and neuroprotection using nicotinamide. Biochim Biophys Acta 1525: 136-148.
58. +, as a PARP inhibitor and by partial restoration of mitochondrial function. Pharmacology 69: 150-157.
59. Kohler C, Peterson A, Eriksson LG, Okuno E, Schwarcz R. 1988. Immunohistochemical identification of quinolinic acid phosphoribosyltransferase in glial cultures from rat brain. Neurosci Lett 84: 115-119.
60. Kou W, Banerjee S, Eudy J, Smith LM, Persidsky R, Borgmann K, Wu L, Sakhuja N, Deshpande MS, Walseth TF, Ghorpade A. 2009. CD38 regulation in activated astrocytes: implications for neuroinflammation and HIV-1 brain infection. J Neurosci Res 87: 2326-2339.
61. Kristal BS, Stavrovskaya IG, Narayanan MV, Krasnikov BF, Brown AM, Beal MF, Friedlander RM. 2004. The mitochondrial permeability transition as a target for neuroprotection. J Bioenerg Biomembr 36: 309-312.
62. Kristian T. 2004. Metabolic stages, mitochondria and calcium in hypoxic/ischemic brain damage. Cell Calcium 36: 221-233.
63. Kristian T, Fiskum G. 2004. A fluorescence-based technique for screening compounds that protect against damage to brain mitochondria. Brain Res Brain Res Protoc 13: 176-182.
64. Kristian T, Gido G, Kuroda S, Schutz A, Siesjo BK. 1998. Calcium metabolism of focal and penumbral tissues in rats subjected to transient middle cerebral artery occlusion. Exp Brain Res 120: 503-509.
65. Kuroda S, Katsura K, Hillered L, Bates TE, Siesjo BK. 1996. Delayed treatment with alpha-phenyl-N-tert-butyl nitrone (PBN) attenuates secondary mitochondrial dysfunction after transient focal cerebral ischemia in the rat. Neurobiol Dis 3: 149-157.
66. Lai Y, Chen Y, Watkins SC, Nathaniel PD, Guo F, Kochanek PM, Jenkins LW, Szabo C, Clark RS. 2008. Identification of poly-ADP-ribosylated mitochondrial proteins after traumatic brain injury. J Neurochem 104: 1700-1711.
67. Lee HC. 1997. Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol Rev 77: 1133-1164.
68. + depletion protects neurons against excitotoxicity: bioenergetic effects of mild mitochondrial uncoupling and caloric restriction. Ann N Y Acad Sci 1147: 275-282.
69. + consumption by SIRT1 may endanger energetically compromised neurons. Neuromol Med 11: 28-42.
70. Luk T, Malam Z, Marshall JC. 2008. Pre-B cell colony-enhancing factor (PBEF)/visfatin: a novel mediator of innate immunity. J Leukoc Biol 83: 804-816.
71. Malavasi F, Deaglio S, Funaro A, Ferrero E, Horenstein AL, Ortolan E, Vaisitti T, Aydin S. 2008. Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol Rev 88: 841-886.
72. Martin E, Rosenthal RE, Fiskum G. 2005. Pyruvate dehydrogenase complex: metabolic link to ischemic brain injury and target of oxidative stress. J Neurosci Res 79: 240-247.
73. Masmoudi A, Islam F, Mandel P. 1988. ADP-ribosylation of highly purified rat brain mitochondria. J Neurochem 51: 188-193.
74. Mattson MP. 2004. Pathways towards and away from Alzheimer's disease. Nature 430: 631-639.
75. Mayo L, Jacob-Hirsch J, Amariglio N, Rechavi G, Moutin MJ, Lund FE, Stein R. 2008. Dual role of CD38 in microglial activation and activation-induced cell death. J Immunol 181: 92-103.
76. Mokudai T, Ayoub IA, Sakakibara Y, Lee EJ, Ogilvy CS, Maynard KI. 2000. Delayed treatment with nicotinamide (vitamin B3) improves neurological outcome and reduces infarct volume after transient focal cerebral ischemia in Wistar rats. Stroke 31: 1679-1685.
77. Morais VA, De Strooper B. 2010. Mitochondria dysfunction and neurodegenerative disorders: cause or consequence. J Alzheimers Dis 20( Suppl 2): S255-S263.
78. Mukherjee SK, Klaidman LK, Yasharel R, Adams JDJr. 1997. Increased brain NAD prevents neuronal apoptosis in vivo. Eur J Pharmacol 330: 27-34.
79. Naga KS, Geddes JW. 2007. High cyclophilin D content of synaptic mitochondria results in increased vulnerability to permeability transition. J Neurosci 27: 7469-7475.
80. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T, Tsujimoto Y. 2005. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434: 652-658.
81. Perry GM, Tallaksen-Greene S, Kumar A, Heng MY, Kneynsberg A, van Groen T, Detloff PJ, Albin RL, Lesort M. 2010. Mitochondrial calcium uptake capacity as a therapeutic target in the R6/2 mouse model of Huntington's disease. Hum Mol Genet 19: 3354-3371.
82. Petronilli V, Nicolli A, Costantini P, Colonna R, Bernardi P. 1994. Regulation of the permeability transition pore, a voltage-dependent mitochondrial channel inhibited by cyclosporin A. Biochim Biophys Acta 1187: 255-259.
83. Pieper AA, Verma A, Zhang J, Snyder SH. 1999. Poly (ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol Sci 20: 171-181.
84. Reinherz EL, Kung PC, Goldstein G, Levey RH, Schlossman SF. 1980. Discrete stages of human intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of T-cell lineage. Proc Natl Acad Sci U S A 77: 1588-1592.
85. Richards EM, Rosenthal RE, Kristian T, Fiskum G. 2006. Postischemic hyperoxia reduces hippocampal pyruvate dehydrogenase activity. Free Radic Biol Med 40: 1960-1970.
86. Ruddick JP, Evans AK, Nutt DJ, Lightman SL, Rook GA, Lowry CA. 2006. Tryptophan metabolism in the central nervous system: medical implications. Expert Rev Mol Med 8: 1-27.
87. + levels in ischemic core and penumbra. Neurochem Res 28: 1227-1234.
88. Sakakibara Y, Mitha AP, Ayoub IA, Ogilvy CS, Maynard KI. 2002. Delayed treatment with nicotinamide (vitamin B3) reduces the infarct volume following focal cerebral ischemia in spontaneously hypertensive rats, diabetic and non-diabetic Fischer 344 rats. Brain Res 931: 68-73.
89. Salmina AB, Malinovskaya NA, Okuneva OS, Taranushenko TE, Fursov AA, Mikhutkina SV, Morgun AV, Prokopenko SV, Zykova LD. 2008. Perinatal hypoxic and ischemic damage to the central nervous system causes changes in the expression of connexin 43 and CD38 and ADP-ribosyl cyclase activity in brain cells. Bull Exp Biol Med 146: 733-736.
90. Sasaki Y, Araki T, Milbrandt J. 2006. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J Neurosci 26: 8484-8491.
91. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA, Korsmeyer SJ. 2005. 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 102: 12005-12010.
92. Shalbuyeva N, Brustovetsky T, Bolshakov A, Brustovetsky N. 2006. Calcium-dependent spontaneously reversible remodeling of brain mitochondria. J Biol Chem 281: 37547-37558.
93. Snell CR, Snell PH, Richards CD. 1984. Degradation of NAD by synaptosomes and its inhibition by nicotinamide mononucleotide: implications for the role of NAD as a synaptic modulator. J Neurochem 43: 1610-1615.
94. Spector R, Johanson CE. 2007. Vitamin transport and homeostasis in mammalian brain: focus on vitamins B and E. J Neurochem 103: 425-438.
95. Spector R, Kelley P. 1979. Niacin and niacinamide accumulation by rabbit brain slices and choroid plexus in vitro. J Neurochem 33: 291-298.
96. Stavrovskaya IG, Kristal BS. 2005. 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 38: 687-697.
97. Sullivan PG, Rabchevsky AG, Waldmeier PC, Springer JE. 2005. Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death? J Neurosci Res 79: 231-239.
98. Szabo C, Dawson VL. 1998. Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion. Trends Pharmacol Sci 19: 287-298.
99. Ungerstedt JS, Blomback M, Soderstrom T. 2003. Nicotinamide is a potent inhibitor of proinflammatory cytokines. Clin Exp Immunol 131: 48-52.
100. Vereczki V, Martin E, Rosenthal RE, Hof PR, Hoffman GE, Fiskum G. 2006. Normoxic resuscitation after cardiac arrest protects against hippocampal oxidative stress, metabolic dysfunction, and neuronal death. J Cereb Blood Flow Metab 26: 821-835.
101. Willmott NJ, Asselin J, Galione A. 1996. Calcium store depletion potentiates a phosphodiesterase inhibitor- and dibutyryl cGMP-evoked calcium influx in rat pituitary GH3 cells. FEBS Lett 386: 39-42.
102. Yamada M, Mizuguchi M, Otsuka N, Ikeda K, Takahashi H. 1997. Ultrastructural localization of CD38 immunoreactivity in rat brain. Brain Res 756: 52-60.
103. Yang J, Klaidman LK, Chang ML, Kem S, Sugawara T, Chan P, Adams JD. 2002. Nicotinamide therapy protects against both necrosis and apoptosis in a stroke model. Pharmacol Biochem Behav 73: 901-910.
104. Yang JL, Weissman L, Bohr VA, Mattson MP. 2008. Mitochondrial DNA damage and repair in neurodegenerative disorders. DNA Repair 7: 1110-1120.
105. -/- mouse. Biochem Biophys Res Commun 346: 188-192.
106. Zhang W, Xie Y, Wang T, Bi J, Li H, Zhang LQ, Ye SQ, Ding S. 2010. Neuronal protective role of PBEF in a mouse model of cerebral ischemia. J Cereb Blood Flow Metab 30: 1962-71.
107. Ziegler M. 2000. New functions of a long-known molecule. Emerging roles of NAD in cellular signaling. Eur J Biochem 267: 1550-1564.
108. Zoratti M, Szabo I. 1995. The mitochondrial permeability transition. Biochim Biophys Acta 1241: 139-176.