Serum or target deprivation-induced neuronal death causes oxidative neuronal accumulation of Zn2+ and loss of NAD+

European Journal of Neuroscience

Volumn 32, Issue 6, 2010, Pages 894-904

  Sheline, Christian T ^a   Cai, Ai Li ^a,b   Zhu, Julia ^a,b   Shi, Chunxiao ^a,b  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

dorsal lateral geniculate nucleus; mouse; pyruvate; sirtuin; visual cortex ablation

Indexed keywords

ADENOSINE TRIPHOSPHATE; METALLOTHIONEIN III; NICOTINAMIDE ADENINE DINUCLEOTIDE; SIRTUIN; ZINC ION;

ANIMAL CELL; ARTICLE; CATABOLISM; CELL DEATH; CELL METABOLISM; EMBRYO; GLYCOLYSIS; LATERAL GENICULATE BODY; MALE; MITOCHONDRION; MOUSE; MOUSE STRAIN; NERVE CELL; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MALNUTRITION; PROTEIN SYNTHESIS; STAINING; VISUAL CORTEX;

ANIMALS; CATIONS, DIVALENT; CELL DEATH; CELLS, CULTURED; GENICULATE BODIES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NAD; NEURONS; OXIDATIVE STRESS; SERUM ALBUMIN; SIRTUIN 1; ZINC;

EID: 77956796536     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07372.x     Document Type: Article

References (86)

1. Agarwala, S. Kalil, R.E. (1998) Axotomy-induced neuronal death and reactive astrogliosis in the lateral geniculate nucleus following a lesion of the visual cortex in the rat. J. Comp. Neurol., 392, 252 263.
2. Aizenman, E., Stout, A.K., Hartnett, K.A., Dineley, K.E., McLaughlin, B. Reynolds, I.J. (2000) Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release. J. Neurochem., 75, 1878 1888.
3. Al-Abdulla, N.A., Portera-Cailliau, C. Martin, L.J. (1998) Occipital cortex ablation in adult rat causes retrograde neuronal death in the lateral geniculate nucleus that resembles apoptosis. Neuroscience, 86, 191 209.
4. Alano, C.C., Ying, W. Swanson, R.A. (2004) Poly(ADP-ribose) polymerase-1-mediated cell death in astrocytes requires NAD+ depletion and mitochondrial permeability transition. J. Biol. Chem., 279, 18895 18902.
5. Araki, T., Sasaki, Y. Milbrandt, J. (2004) Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science, 305, 1010 1013.
6. 2+ release from metallothionein by destroying zinc-sulphur clusters without concomitant formation of S-nitrosothiol. Biochem. J., 344 (Pt 1 253 258.
7. Bedalov, A. Simon, J.A. (2004) Neuroscience. NAD to the rescue. Science, 305, 954 955.
8. Berardi, N. Maffei, L. (1999) From visual experience to visual function: roles of neurotrophins. J. Neurobiol., 41, 119 126.
9. Blander, G. Guarente, L. (2004) The sir2 family of protein deacetylases. Annu. Rev. Biochem., 73, 417 435.
10. Brunet, A., Sweeney, L.B., Sturgill, J.F., Chua, K.F., Greer, P.L., Lin, Y., Tran, H., Ross, S.E., Mostoslavsky, R., Cohen, H.Y., Hu, L.S., Cheng, H.L., Jedrychowski, M.P., Gygi, S.P., Sinclair, D.A., Alt, F.W. Greenberg, M.E. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science, 303, 2011 2015.
11. Cai, A.L., Zipfel, G.J. Sheline, C.T. (2006) Zinc neurotoxicity is dependent on intracellular NAD levels and the sirtuin pathway. Eur. J. Neurosci., 24, 2169 2176.
12. Caleo, M., Medini, P., von Bartheld, C.S. Maffei, L. (2003) Provision of brain-derived neurotrophic factor via anterograde transport from the eye preserves the physiological responses of axotomized geniculate neurons. J. Neurosci., 23, 287 296.
13. Cesur, S., Kocaturk, P.A., Kavas, G.O., Aksaray, S., Tezeren, D. Ciftci, U. (2005) Serum copper and zinc concentrations in patients with brucellosis. J. Infect., 50, 31 33. (Pubitemid 40028695)
14. Chang, L.K., Putcha, G.V., Deshmukh, M. Johnson, E.M. Jr. (2002) Mitochondrial involvement in the point of no return in neuronal apoptosis. Biochimie, 84, 223 231.
15. Chang, I., Cho, N., Koh, J.Y. Lee, M.S. (2003) Pyruvate inhibits zinc-mediated pancreatic islet cell death and diabetes. Diabetologia, 46, 1220 1227.
16. Cho, E., Hwang, J.J., Han, S.H., Chung, S.J., Koh, J.Y. Lee, J.Y. (2010) Endogenous zinc mediates apoptotic programmed cell death in the developing brain. Neurotox. Res., 17, 156 166.
17. Chong, Z.Z., Lin, S.H. Maiese, K. (2004) The NAD+ precursor nicotinamide governs neuronal survival during oxidative stress through protein kinase B coupled to FOXO3a and mitochondrial membrane potential. J. Cereb. Blood Flow Metab., 24, 728 743.
18. Davis, S.R., McMahon, R.J. Cousins, R.J. (1998) Metallothionein knockout and transgenic mice exhibit altered intestinal processing of zinc with uniform zinc-dependent zinc transporter-1 expression. J. Nutr., 128, 825 831.
19. Desagher, S., Glowinski, J. Premont, J. (1997) Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J. Neurosci., 17, 9060 9067.
20. Deshmukh, M. Johnson, E.M. Jr. (1997) Programmed cell death in neurons: focus on the pathway of nerve growth factor deprivation-induced death of sympathetic neurons. Mol. Pharmacol., 51, 897 906.
21. Dong, H., Fazzaro, A., Xiang, C., Korsmeyer, S.J., Jacquin, M.F. McDonald, J.W. (2003) Enhanced oligodendrocyte survival after spinal cord injury in Bax-deficient mice and mice with delayed Wallerian degeneration. J. Neurosci., 23, 8682 8691.
22. Ellis, R.E., Yuan, J.Y. Horvitz, H.R. (1991) Mechanisms and functions of cell death. Annu. Rev. Cell Biol., 7, 663 698.
23. Endres, M., Wang, Z.Q., Namura, S., Waeber, C. Moskowitz, M.A. (1997) Ischemic brain injury is mediated by the activation of poly(ADP- ribose)polymerase. J. Cereb. Blood Flow Metab., 17, 1143 1151.
24. Erickson, J.C., Hollopeter, G., Thomas, S.A., Froelick, G.J. Palmiter, R.D. (1997) Disruption of the metallothionein-III gene in mice: analysis of brain zinc, behavior, and neuron vulnerability to metals, aging, and seizures. J. Neurosci., 17, 1271 1281.
25. Fjeld, C.C., Birdsong, W.T. Goodman, R.H. (2003) Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor. Proc. Natl. Acad. Sci. USA, 100, 9202 9207.
26. Gillingwater, T.H., Haley, J.E., Ribchester, R.R. Horsburgh, K. (2004) Neuroprotection after transient global cerebral ischemia in Wld(s) mutant mice. J. Cereb. Blood Flow Metab., 24, 62 66.
27. Gillingwater, T.H., Wishart, T.M., Chen, P.E., Haley, J.E., Robertson, K., Macdonald, S.H., Middleton, S., Wawrowski, K., Shipston, M.J., Melmed, S., Wyllie, D.J., Skehel, P.A., Coleman, M.P. Ribchester, R.R. (2006) The neuroprotective Wlds gene regulates expression of PTTG1 and erythroid differentiation regulator 1-like gene in mice and human cells. Hum. Mol. Genet., 15, 625 635.
28. Gottron, F.J., Ying, H.S. Choi, D.W. (1997) Caspase inhibition selectively reduces the apoptotic component of oxygen-glucose deprivation-induced cortical neuronal cell death. Mol. Cell. Neurosci., 9, 159 169.
29. Grozinger, C.M., Chao, E.D., Blackwell, H.E., Moazed, D. Schreiber, S.L. (2001) Identification of a class of small molecule inhibitors of the sirtuin family of NAD-dependent deacetylases by phenotypic screening. J. Biol. Chem., 276, 38837 38843.
30. Hassan, N. Janjua, M.Z. (2001) The optimum dose of nicotinamide for protection of pancreatic beta- cells against the cytotoxic effect of streptozotocin in albino rat. J. Ayub. Med. Coll. Abbottabad, 13, 26 30.
31. Ho, Y., Samarasinghe, R., Knoch, M.E., Lewis, M., Aizenman, E. DeFranco, D.B. (2008) Selective inhibition of mitogen-activated protein kinase phosphatases by zinc accounts for extracellular signal-regulated kinase 1/2-dependent oxidative neuronal cell death. Mol. Pharmacol., 74, 1141 1151.
32. Holleman, M.A.F. (1904) Notice sur l'action de l'eau oxygé née sur les acides a-cétoniques et sur les dicétones 1.2. Recl. Trav. Chim. Pays Bas. Belg, 23, 169 171.
33. Hwang, J.J., Lee, S.J., Kim, T.Y., Cho, J.H. Koh, J.Y. (2008) Zinc and 4-hydroxy-2-nonenal mediate lysosomal membrane permeabilization induced by H2O2 in cultured hippocampal neurons. J. Neurosci., 28, 3114 3122.
34. Kauppinen, R.A. Nicholls, D.G. (1986) Synaptosomal bioenergetics. The role of glycolysis, pyruvate oxidation and responses to hypoglycaemia. Eur. J. Biochem., 158, 159 165.
35. Kim, Y.H. Koh, J.Y. (2002) 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, 407 418.
36. Kim, Y.H., Kim, E.Y., Gwag, B.J., Sohn, S. Koh, J.Y. (1999) Zinc-induced cortical neuronal death with features of apoptosis and necrosis: mediation by free radicals. Neuroscience, 89, 175 182.
37. Klaidman, L., Morales, M., Kem, S., Yang, J., Chang, M.L. Adams, J.D. Jr. (2003) Nicotinamide offers multiple protective mechanisms in stroke as a precursor for NAD+, as a PARP inhibitor and by partial restoration of mitochondrial function. Pharmacology, 69, 150 157.
38. Koh, J.Y., Suh, S.W., Gwag, B.J., He, Y.Y., Hsu, C.Y. Choi, D.W. (1996) The role of zinc in selective neuronal death after transient global cerebral ischemia. Science, 272, 1013 1016.
39. Kojima, S., Wu, S.T., Wikman-Coffelt, J. Parmley, W.W. (1993) Eighteen-hour preservation of rat hearts with hexanol and pyruvate cardioplegia. J. Am. Coll. Cardiol., 21, 1238 1244. (Pubitemid 23106203)
40. Land, P.W. Aizenman, E. (2005) Zinc accumulation after target loss: an early event in retrograde degeneration of thalamic neurons. Eur. J. Neurosci., 21, 647 657.
41. Lantz, K.A. Kaestner, K.H. (2005) Winged-helix transcription factors and pancreatic development. Clin. Sci. (Lond), 108, 195 204.
42. Lee, J.Y., Kim, Y.H. Koh, J.Y. (2001) Protection by pyruvate against transient forebrain ischemia in rats. J. Neurosci., 21, RC171.
43. Lee, J.M., Zipfel, G.J., Park, K.H., He, Y.Y., Hsu, C.Y. Choi, D.W. (2002) Zinc translocation accelerates infarction after mild transient focal ischemia. Neuroscience, 115, 871 878.
44. Lee, J.Y., Kim, J.H., Palmiter, R.D. Koh, J.Y. (2003) Zinc released from metallothionein-iii may contribute to hippocampal CA1 and thalamic neuronal death following acute brain injury. Exp. Neurol., 184, 337 347.
45. Lee, J.Y., Hwang, J.J., Park, M.H. Koh, J.Y. (2006) Cytosolic labile zinc: a marker for apoptosis in the developing rat brain. Eur. J. Neurosci., 23, 435 442.
46. Lin, S.S., Manchester, J.K. Gordon, J.I. (2001) Enhanced gluconeogenesis and increased energy storage as hallmarks of aging in Saccharomyces cerevisiae. J. Biol. Chem., 276, 36000 36007.
47. Malaiyandi, L.M., Dineley, K.E. Reynolds, I.J. (2004) Divergent consequences arise from metallothionein overexpression in astrocytes: zinc buffering and oxidant-induced zinc release. Glia, 45, 346 353.
48. Martell, A.M. Smith, R.M. (1995). Critically Selected Stability Constants of Metal Complexes. N.I.S.T., Gaithersburg, MD.
49. Martin, L.J., Al-Abdulla, N.A., Brambrink, A.M., Kirsch, J.R., Sieber, F.E. Portera-Cailliau, C. (1998) Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res. Bull., 46, 281 309.
50. Martin, L.J., Price, A.C., McClendon, K.B., Al-Abdulla, N.A., Subramaniam, J.R., Wong, P.C. Liu, Z. (2003) Early events of target deprivation/axotomy-induced neuronal apoptosis in vivo: oxidative stress, DNA damage, p53 phosphorylation and subcellular redistribution of death proteins. J. Neurochem., 85, 234 247.
51. Maus, M., Marin, P., Israel, M., Glowinski, J. Premont, J. (1999) Pyruvate and lactate protect striatal neurons against N-methyl-D-aspartate- induced neurotoxicity. Eur. J. Neurosci., 11, 3215 3224.
52. Mengual, E., Casanovas-Aguilar, C., Perez-Clausell, J. Gimenez-Amaya, J.M. (2001) Thalamic distribution of zinc-rich terminal fields and neurons of origin in the rat. Neuroscience, 102, 863 884.
53. Muessel, M.J., Berman, N.E. Klein, R.M. (2000) Early and specific expression of monocyte chemoattractant protein-1 in the thalamus induced by cortical injury. Brain Res., 870, 211 221.
54. Noh, K.M., Kim, Y.H. Koh, J.Y. (1999) Mediation by membrane protein kinase C of zinc-induced oxidative neuronal injury in mouse cortical cultures. J. Neurochem., 72, 1609 1616.
55. Oppenheim, R.W. (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci., 14, 453 501.
56. Pal, S., He, K. Aizenman, E. (2004) Nitrosative stress and potassium channel-mediated neuronal apoptosis: is zinc the link? Pflugers Arch., 448, 296 303.
57. Passonneau, J.V. Lowry, O.H. (1993) Enzymatic Analysis A Practical Guide. Humana Press, Totowa, NJ.
58. Plaschke, K., Kopitz, J., Weigand, M.A., Martin, E. Bardenheuer, H.J. (2000) The neuroprotective effect of cerebral poly(ADP-ribose)polymerase inhibition in a rat model of global ischemia. Neurosci. Lett., 284, 109 112.
59. Purves, D., Snider, W.D. Voyvodic, J.T. (1988) Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature, 336, 123 128.
60. Redman, P.T., Hartnett, K.A., Aras, M.A., Levitan, E.S. Aizenman, E. (2009) Regulation of apoptotic potassium currents by coordinated zinc-dependent signalling. J. Physiol., 587, 4393 4404.
61. Rizzardini, M., Lupi, M., Bernasconi, S., Mangolini, A. Cantoni, L. (2003) Mitochondrial dysfunction and death in motor neurons exposed to the glutathione-depleting agent ethacrynic acid. J. Neurol. Sci., 207, 51 58.
62. Ryu, J.K., Kim, S.U. McLarnon, J.G. (2003) Neuroprotective effects of pyruvate in the quinolinic acid rat model of Huntington's disease. Exp. Neurol., 183, 700 704.
63. Sasaki, Y., Vohra, B.P., Baloh, R.H. Milbrandt, J. (2009a) Transgenic mice expressing the Nmnat1 protein manifest robust delay in axonal degeneration in vivo. J. Neurosci., 29, 6526 6534.
64. Sasaki, Y., Vohra, B.P., Lund, F.E. Milbrandt, J. (2009b) Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. J. Neurosci., 29, 5525 5535.
65. 2+ uptake and persistent mitochondrial dysfunction. Eur. J. Neurosci., 12, 3813 3818.
66. Sensi, S.L., Ton-That, D., Sullivan, P.G., Jonas, E.A., Gee, K.R., Kaczmarek, L.K. Weiss, J.H. (2003) Modulation of mitochondrial function by endogenous Zn2+ pools. Proc. Natl. Acad. Sci. U S A, 100, 6157 6162.
67. Sheline, C.T. Choi, D.W. (1998) Neuronal death in cultured murine cortical cells is induced by inhibition of GAPDH and triosephosphate isomerase. Neurobiol. Dis., 5, 47 54.
68. Sheline, C.T., Behrens, M.M. Choi, D.W. (2000) Zinc-induced cortical neuronal death: contribution of energy failure attributable to loss of NAD(+) and inhibition of glycolysis. J. Neurosci., 20, 3139 3146.
69. Sheline, C.T., Wang, H., Cai, A.L., Dawson, V.L. Choi, D.W. (2003) Involvement of poly ADP ribosyl polymerase-1 in acute but not chronic zinc toxicity. Eur. J. Neurosci., 18, 1402 1409.
70. Sheline, C.T., Takata, T., Ying, H., Canzoniero, L.M., Yang, A., Yu, S.P. Choi, D.W. (2004) Potassium attenuates zinc-induced death of cultured cortical astrocytes. Glia, 46, 18 27.
71. Sheline, C.T., Shi, C. Cai, A. (2006). Oxidative Neuronal Injuries and Target Deprivation: Role of Zn2+, NAD+, and the Sirtuin Pathway Society for Neurosciences Online Itinerary Planner. SFN, Washington, DC, Atlanta, GA, pp. 186.10.
72. Sheline, C.T., Wei, L., Shi, C. Cai, A.L. (2008) Trophic Factor Deprivation: Roles of Oxidation, Zinc, and NAD+. Society for Neurosciences Online Itinerary Planner. SFN, Washington, DC, Washington, DC, pp. 555.15.
73. Suh, S.W., Aoyama, K., Chen, Y., Garnier, P., Matsumori, Y., Gum, E., Liu, J. Swanson, R.A. (2003) Hypoglycemic neuronal death and cognitive impairment are prevented by poly(ADP-ribose) polymerase inhibitors administered after hypoglycemia. J. Neurosci., 23, 10681 10690.
74. Suh, S.W., Aoyama, K., Matsumori, Y., Liu, J. Swanson, R.A. (2005) Pyruvate administered after severe hypoglycemia reduces neuronal death and cognitive impairment. Diabetes, 54, 1452 1458.
75. Suh, S.W., Aoyama, K., Alano, C.C., Anderson, C.M., Hamby, A.M. Swanson, R.A. (2007a) Zinc inhibits astrocyte glutamate uptake by activation of poly(ADP-ribose) polymerase-1. Mol. Med., 13, 344 349.
76. Suh, S.W., Gum, E.T., Hamby, A.M., Chan, P.H. Swanson, R.A. (2007b) Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase. J. Clin. Invest., 117, 910 918.
77. Suh, S.W., Hamby, A.M., Gum, E.T., Shin, B.S., Won, S.J., Sheline, C.T., Chan, P.H. Swanson, R.A. (2008) Sequential release of nitric oxide, zinc, and superoxide in hypoglycemic neuronal death. J. Cereb. Blood Flow Metab., 28, 1697 1706.
78. Szabo, C. Dawson, V.L. (1998) Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion. Trends Pharmacol. Sci., 19, 287 298.
79. Virag, L., Szabo, E., Gergely, P. Szabo, C. (2003) Peroxynitrite-induced cytotoxicity: mechanism and opportunities for intervention. Toxicol. Lett., 140-141, 113 124.
80. Visalli, N., Costa, C. Natoli, A. (1986) [Hypoprolactinemia in subjects with various pathologies of the reproductive system]. Clin. Ter., 116, 421 423.
81. +-ATPase activity as a mechanism of neuronal death mediated by concurrent ATP deficiency and oxidant stress. J. Cell Sci., 116, 2099 2110.
82. Yamada, K., Nonaka, K., Hanafusa, T., Miyazaki, A., Toyoshima, H. Tarui, S. (1982) Preventive and therapeutic effects of large-dose nicotinamide injections on diabetes associated with insulitis. An observation in nonobese diabetic (NOD) mice. Diabetes, 31, 749 753.
83. Ying, W., Sevigny, M.B., Chen, Y. Swanson, R.A. (2001) Poly(ADP-ribose) glycohydrolase mediates oxidative and excitotoxic neuronal death. Proc. Natl. Acad. Sci. USA, 98, 12227 12232.
84. Yoo, M.H., Lee, J.Y., Lee, S.E., Koh, J.Y. Yoon, Y.H. (2004) Protection by pyruvate of rat retinal cells against zinc toxicity in vitro, and pressure-induced ischemia in vivo. Invest. Ophthalmol. Vis. Sci., 45, 1523 1530.
85. Zhang, Y., Wang, H., Li, J., Jimenez, D.A., Levitan, E.S., Aizenman, E. Rosenberg, P.A. (2004) Peroxynitrite-induced neuronal apoptosis is mediated by intracellular zinc release and 12-lipoxygenase activation. J. Neurosci., 24, 10616 10627.
86. Zhang, Y., Aizenman, E., DeFranco, D.B. Rosenberg, P.A. (2007) Intracellular zinc release, 12-lipoxygenase activation and MAPK dependent neuronal and oligodendroglial death. Mol. Med., 13, 350 355.