Nitrosative stress and potassium channel-mediated neuronal apoptosis: Is zinc the link?

Pflugers Archiv European Journal of Physiology

Volumn 448, Issue 3, 2004, Pages 296-303

  Pal, Sumon ^a   He, Kai ^a   Aizenman, Elias ^a  

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

Author keywords

Apoptosis; Kv2.1; Metallothionein; Nitric oxide; p38; Peroxynitrite; Potassium channel; Zinc

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL; IONOPHORE; LINOPIRDINE; OXIDIZING AGENT; PEROXYNITRITE; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; TETRYLAMMONIUM; THIOL DERIVATIVE; THYMIDINE DIPHOSPHATE; VALINOMYCIN; VOLTAGE GATED POTASSIUM CHANNEL; ZINC; 3 NITROTYROSINE; 3-NITROTYROSINE; DRUG DERIVATIVE; PEROXYNITROUS ACID; TYROSINE;

APOPTOSIS; BRAIN MITOCHONDRION; BRAIN NERVE CELL; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CHELATION; HUMAN; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; POTASSIUM CURRENT; PRIORITY JOURNAL; REVIEW; ANIMAL; DRUG EFFECT; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; HUMANS; NEURONS; OXIDATIVE STRESS; PEROXYNITROUS ACID; POTASSIUM CHANNELS, VOLTAGE-GATED; TYROSINE; ZINC;

EID: 9344254033     PISSN: 00316768     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00424-004-1256-7     Document Type: Review

References (106)

1. Adler M, Shafer H, Hamilton T, Petrali JP (1999) Cytotoxic actions of the heavy metal chelator TPEN on NG108-15 neuroblastoma-glioma cells. Neurotoxicology 20:571-582
2. Ahn YH, Kim YH, Hong SH, Koh JY (1998) Depletion of intracellular zinc induces protein synthesis-dependent neuronal apoptosis in mouse cortical culture. Exp Neurol 154:47-56
3. Aizenman E, Brimecombe JC, Potthoff WK, Rosenberg PA (1998) Why is the role of nitric oxide in NMDA receptor function and dysfunction so controversial? Prog Brain Res 118:53-71
4. Aizenman E, Stout AK, Hartnett KA, Dineley KE, McLaughlin B, Reynolds IJ (2000) Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release. J Neurochem 75:1878-1888
5. Aniksztejn L, Charton G, Ben-Ari Y (1987) Selective release of endogenous zinc from the hippocampal mossy fibers in situ. Brain Res 404:58-64
6. 2+ release from metallothionein by destroying zinc-sulphur clusters without concomitant formation of S-nitrosothiol. Biochem J 344:253-258
7. Aschner M (1996) The functional significance of brain metallothioneins. FASEB J 10:1129-1136
8. 2+ from brain tissue during activity. Nature 308:734-736
9. Atar D, Backx PH, Appel MM, Gao WD, Marban E (1995) Excitation- transcription coupling mediated by zinc influx through voltage-dependent calcium channels. J Biol Chem 270:2473-2477
10. Berendji D, Kolb-Bachofen V, Meyer KL, Grapenthin O, Weber H, Wahn V, Kroncke KD (1997) Nitric oxide mediates intracytoplasmic and intranuclear zinc release. FEBS Lett 405:37-41
11. Berg JM, Shi Y (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271:1081-1085
12. Bortner CD, Cidlowski JA (1996) Absence of volume regulatory mechanisms contributes to the rapid activation of apoptosis in thymocytes. Am J Physiol 271:C950-C961
13. +, cell shrinkage, and mitochondrial membrane potential during lymphocyte apoptosis. J Biol Chem 274:21953-21962
14. + channels. Neuron 41:351-365
15. Brito C, Naviliat M, Tiscornia AC, Vuillier F, Gualco G, Dighiero G, Radi R, Cayota AM (1999) Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death. J Immunol 162:3356-3366
16. 2+ inhibits alpha-ketoglutarate- stimulated mitochondrial respiration and the isolated alpha-ketoglutarate dehydrogenase complex. J Biol Chem 275:13441-13447
17. Brugg B, Michel PP, Agid Y, Ruberg M (1996) Ceramide induces apoptosis in cultured mesencephalic neurons. J Neurochem 66:733-739
18. Chai F, Truong-Tran AQ, Ho LH, Zalewski PD (1999) Regulation of caspase activation and apoptosis by cellular zinc fluxes and zinc deprivation: a review. Immunol Cell Biol 77:272-278
19. Chi XX, Xu ZC (2000) Differential changes of potassium currents in CA1 pyramidal neurons after transient forebrain ischemia. J Neurophysiol 84:2834-2843
20. Choi DW (1992) Excitotoxic cell death. J Neurobiol 23:1261-1276
21. Choi DW, Yokoyama M, Koh J (1988) Zinc neurotoxicity in cortical cell culture. Neuroscience 24:67-79
22. Cohen JJ, Duke RC (1984) Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J Immunol 132:38-42
23. Colom LV, Diaz ME, Beers DR, Neely A, Xie WJ, Appel SH (1998) Role of potassium channels in amyloid-induced cell death. Neurochemistry 70:1925-1934
24. 2+ homeostasis in neurons. Eur J Pharmacol 479:171-185
25. Csermely P, Szamel M, Resch K, Somogyi J (1988) Zinc can increase the activity of protein kinase C and contributes to its binding to plasma membranes in T lymphocytes. J Biol Chem 263:6487-6490
26. Cuajungco MP, Lees GJ (1998) Nitric oxide generators produce accumulation of chelatable zinc in hippocampal neuronal perikarya. Brain Res 799:118-129
27. Dawson VL, Dawson TM (1995) Physiological and toxicological actions of nitric oxide in the central nervous system. Adv Pharmacol 34:323-342
28. Dineley KE, Votyakova TV, Reynolds IJ (2003) Zinc inhibition of cellular energy production: implication for mitochondria and neurodegeneration. J Neurochem 85:563-570
29. Estevez AG, Jordan J (2002) Nitric oxide and superoxide, a deadly cocktail. Ann NY Acad Sci 962:207-211
30. Fliss H, Menard M (1991) Hypochlorous acid-induced mobilization of zinc from metalloproteins. Arch Biochem Biophys 287:175-179
31. Fraker PJ, Telford WG (1997) A reappraisal of the role of zinc in life and death decisions of cells. Exp Biol Med 215:229-236
32. Frederickson CJ (1989) Neurobiology of zinc and zinc-containing neurons. Int Rev Neurobiol 31:145-238
33. Frederickson CJ, Hernandez MD, Goik SA, Morton JD, McGinty JF (1988) Loss of zinc staining from hippocampal mossy fibers during kainic acid induced seizures: a histofluorescence study. Brain Res 446:383-386
34. Galli C, Meucci O, Scorziello A, Werge TM, Calissano P, Schettini G (1995) Apoptosis in cerebellar granule cells is blocked by high KCl, forskolin, and IGF-1 through distinct mechanisms of action: the involvement of intracellular calcium and RNA synthesis. J Neurosci 15:1172-1179
35. Garthwaite J, Boulton CL (1995) Nitric oxide signalling in the central nervous system. Annu Rev Physiol 57:683-706
36. Garthwaite J, Charles SL, Chess-Williams R (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336:385-388
37. Groves JT (1999) Peroxynitrite: reactive, invasive and enigmatic. Curr Opin Chem Biol 3:226-235
38. Hannun YA (1994) The sphingomyelin cycle and the second messenger function of ceramide. J Biol Chem 269:3125-3128
39. Hara H, Aizenman E (2004) A molecular technique for detecting the liberation of intracellular zinc in cultured neurons. J Neurosci Methods (In press)
40. Ho LH, Ratnaike RN, Zalewski PD (2000) Involvement of intracellular labile zinc in suppression of DEVD-caspase activity in human neuroblastoma cells. Biochem Biophys Res Commun 268:148-154
41. Holm P, Kankaanranta H, Metsa-Ketela T, Moilanen E (1998) Radical releasing properties of nitric oxide donors GEA 3162, SIN-1 and S-nitroso-N-acetylpenicillamine. Eur J Pharmacol 346:97-102
42. Howell GA, Welch MG, Frederickson CJ (1984) Stimulation-induced uptake and release of zinc in hippocampal slices. Nature 308:736-738
43. Jiang LJ, Maret W, Vallee BL (1998) The glutathione redox couple modulates zinc transfer from metallothionein to zinc-depleted sorbitol dehydrogenase. Proc Natl Acad Sci USA 95:3483-348
44. Kägi JHR (1993) Evolution, structure and chemical activity of class I metallothioneins: an overview. In: Suzuki KT, Imura N, Kimura M (eds) Metallothionein III: biological roles and medical implications. Birkhäuser, Basel, pp 29-55
45. Katakai K, Liu J, Nakajima K, Keefer LK, Waalkes MP (2001) Nitric oxide induces metallothionein (MT) gene expression apparently by displacing zinc bound to MT. Toxicol Lett 119:103-108
46. Kay AR (2003) Evidence for chelatable zinc in the extracellular space of the hippocampus, but little evidence for synaptic release of Zn. J Neurosci 23:6847-6855
47. Kim YH, Koh JY (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
48. 2+ entry produces oxidative neuronal necrosis in cortical cell cultures. Eur J Neurosci 11:327-334
49. Kim YH, Kim EY, Gwag BJ, Sohn S, Koh JY (1999b) Zinc-induced cortical neuronal death with features of apoptosis and necrosis: mediation by free radicals. Neuroscience 89:175-182
50. Kissner R, Nauser T, Bugnon P, Lye PG, Koppenol WH (1998) Formation and properties of peroxynitrite as studied by laser flash photolysis, high-pressure stopped-flow technique, and pulse radiolysis. Chem Res Toxicol 10:1285-1292
51. 2+ ions on mitochondrial electron transport. Arch Biochem Biophys 165:121-125
52. Koh JY (2001) Zinc and diseases of the brain. Mol Neurobiol 24:99-106
53. Koh JY, Choi DW (1994) Zinc toxicity on cultured cortical neurons: involvement of N-methyl-D-aspartate receptors. Neuroscience 60:1049-1057
54. Koh JY, Suh SW, Gwag BJ, He YY, Hsu CY, Choi DW (1996) The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 272:1013-1016
55. Kroncke KD, Fehsel K, Schmidt T, Zenke FT, Dasting I, Wesener JR, Bettermann H, Breunig KD, Kolb-Bachofen V (1994) Nitric oxide destroys zinc-sulfur clusters inducing zinc release from metallothionein and inhibition of the zinc finger-type yeast transcription activator LAC9. Biochem Biophys Res Commun 200:1105-1110
56. Lee JY, Park J, Kim YH, Kim DH, Kim CG, Koh JY (2000) Induction by synaptic zinc of heat shock protein-70 in hippocampus after kainate seizures. Exp Neurol 161:433-441
57. Lee JY, Kim JH, Palmiter RD, Koh JY (2003) Zinc released from metallothionein-III may contribute to hippocampal CA1 and thalamic neuronal death following acute brain injury. Exp Neurol 184:337-347
58. Legos JJ, McLaughlin B, Skaper SD, Strijbos PJ, Parsons AA, Aizenman E, Herin GA, Barone FC, Erhardt JA (2002) The selective p38 inhibitor SB-239063 protects primary neurons from mild to moderate excitotoxic cell death. Eur J Pharmacol 447:37-42
59. Link TA, Jagow G von (1995) Zinc ions inhibit the QP center of bovine heart mitochondrial bcl complex by blocking a protonatable group. J Biol Chem 270:25001-25006
60. Lipton SA, Kater SB (1989) Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci 12:265-270
61. Manev H, Kharlamov E, Uz T, Mason RP, Cagnoli CM (1997) Characterization of zinc-induced neuronal death in primary cultures of rat cerebellar granule cells. Exp Neurol 146:171-178
62. Maret W (1994) Oxidative metal release from metallothionein via zinc-thiol/disulfide interchange. Proc Natl Acad Sci USA 91:237-241
63. Maret W (1995) Metallothionein/disulfide interactions, oxidative stress, and the mobilization of cellular zinc. Neurochem Int 27:111-117
64. Maret W, Vallee BL (1998) Thiolate ligands in metallothionein confer redox activity on zinc clusters. Proc Natl Acad Sci USA 95:3478-3482
65. McLaughlin B, Pal S, Tran MP, Parsons AA, Barone FC, Erhardt JA, Aizenman E (2001) p38 activation is required upstream of potassium current enhancement and caspase cleavage in thiol oxidant-induced neuronal apoptosis. J Neurosci 21:3303-3311
66. McMahon RJ, Cousins RJ (1998) Regulation of the zinc transporter ZnT-1 by dietary zinc. Proc Natl Acad Sci USA 95:4841-486
67. Misko TP, Highkin MK, Veenhuizen AW, Manning PT, Stern MK, Currie MG, Salvemini D (1998) Characterization of the cytoprotective action of peroxynitrite decomposition catalysts. J Biol Chem 273:15646-15653
68. Noh KM, Kim YH, Koh JY (1999) Mediation by membrane protein kinase C of zinc-induced oxidative neuronal injury in mouse cortical cultures. J Neurochem 72:1609-1616
69. Pal S, Hartnett KA, Nerbonne JM, Levitan ES, Aizenman E (2003) Mediation of neuronal apoptosis by Kv2.1-encoded potassium channels. J Neurosci 23:4798-4802
70. Paoletti P, Ascher P, Neyton J (1997) High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J Neurosci 17:5711-5725
71. Park JA, Koh JY (1999) Induction of an immediate early gene egr-1 by zinc through extracellular signal-regulated kinase activation in cortical culture: its role in zinc-induced neuronal death. J Neurochem 73:450-456
72. Park JA, Lee JY, Sato TA, Koh JY (2000) Co-induction of p75NTR and p75NTR-associated death executor in neurons after zinc exposure in cortical culture or transient ischemia in the rat. J Neurosci 20:9096-9103
73. Pearce LL, Gandley RE, Han W, Wasserloos K, Stitt M, Kanai AJ, McLaughlin MK, Pitt BR, Levitan ES (2000) Role of metallothionein in nitric oxide signaling as revealed by a green fluorescent fusion protein. Proc Natl Acad Sci USA 97:477-482
74. Perry DK, Smyth MJ, Stennicke HR, Salvesen GS, Duriez P, Poirier GG, Hannun YA (1997) Zinc is a potent inhibitor of the apoptotic protease, caspase-3. A novel target for zinc in the inhibition of apoptosis. J Biol Chem 272:18530-18533
75. Radi R, Beckman JS, Bush KM, Freeman BA (1991) Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 288:481-487
76. Radi R, Rodriguez M, Castro L, Telleri R (1994) Inhibition of mitochondrial electron transport by peroxynitrite. Arch Biochem Biophys 308:89-95
77. 2+-stimulated sphingomyelinase is secreted by many cell types and is a product of the acid sphingomyelinase gene. J Biol Chem 271:18431-18436
78. Schrantz N, Auffredou M-T, Bourgeade MF, Besnault L, Leca G, Vazquez A (2001) Zinc-mediated regulation of caspases activity: dose-dependent inhibition or activation of caspase-3 in the human Burkitt lymphoma B cells (Ramos). Cell Death Diff 8:152-161
79. Sensi SL, Canzoniero LM, Yu SP, Ying HS, Koh JY, Kerchner GA, Choi DW (1997) Measurement of intracellular free zinc in living cortical neurons: routes of entry. J Neurosci 17:9554-9564
80. 2+-permeable AMPA/kainate channels triggers prolonged mitochondrial superoxide production. Proc Natl Acad Sci USA 96:2414-2419
81. 2+ uptake and persistent mitochondrial dysfunction. Eur J Neurosci 12:3813-3818
82. 2+ pools. Proc Natl Acad Sci USA 100:6157-6162
83. + and inhibition of glycolysis. J Neurosci 20:3139-3146
84. Sloviter RS (1985) A selective loss of hippocampal mossy fiber Timm stain accompanies granule cell seizure activity induced by perforant path stimulation. Brain Res 330:150-153
85. 2+-stimulated sphingomyelinase in fetal bovine serum. J Biol Chem 264:5358-5363
86. St. Croix CM, Wasserloos KJ, Dineley KE, Reynolds IJ, Levitan ES, Pitt BR (2002) Nitric oxide-induced changes in intracellular zinc homeostasis are mediated by metallothionein/thionein. Am J Physiol 282:L185-L192
87. Takeda A (2000) Movement of zinc and its functional significance in the brain. Brain Res Rev 34:137-148
88. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, Minowa O, Miyazono K, Noda T, Ichijo H (2001) ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2:222-228
89. 2+ fit in? Cell Calcium 24:387-403
90. Tonder N, Johansen FF, Frederickson CJ, Zimmer J, Diemer NH (1990) Possible role of zinc in the selective degeneration of dentate hilar neurons after cerebral ischemia in the adult rat. Neurosci Lett 109:247-252
91. Underwood DC, Osborn RR, Kotzer CJ, Adams JL, Lee JC, Webb EF, Carpenter DC, Bochnowicz S, Thomas HC, Hay DW, Griswold DE (2000) SB 239063, a potent p38 MAP kinase inhibitor, reduces inflammatory cytokine production, airways eosinophil infiltration, and persistence. J Pharmacol Exp Ther 293:281-288
92. Virag L, Szabo C (1999) Inhibition of poly(ADP-ribose) synthetase (PARS) and protection against peroxynitrite-induced cytotoxicity by zinc chelation. Br J Pharmacol 126:769-777
93. Vogt K, Mellor J, Tong G, Nicoll R (2000) The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 26:187-196
94. Walev I, Reske K, Palmer M, Valeva A, Bhakdi S (1995) Potassium-inhibited processing of IL-1 beta in human monocytes. EMBO J 14:1607-1614
95. Weiss JH, Hartley DM, Koh JY, Choi DW (1993) AMPA receptor activation potentiates zinc neurotoxicity. Neuron 10:43-49
96. 2+: a novel ionic mediator of neural injury in brain disease. Trends Pharmacol Sci 21:395-401
97. Wudarczyk J, Debska G, Lenartowicz E (1999) Zinc as an inducer of the membrane permeability transition in rat liver mitochondria. Arch Biochem Biophys 363:1-8
98. Xia S, Lampe PA, Deshmukh M, Yang A, Brown BS, Rothman SM, Johnson EM Jr, Yu SP (2002) Multiple channel interactions explain the protection of sympathetic neurons from apoptosis induced by nerve growth factor deprivation. J Neurosci 22:114-122
99. Yokoyama M, Koh J, Choi DW (1986) Brief exposure to zinc is toxic to cortical neurons. Neurosci Lett 71:351-355
100. Yu SP (2003) Regulation and critical role of potassium homeostasis in apoptosis. Prog Neurobiol 70:363-86
101. Yu SP, Yeh CH, Sensi SL, Gwag BJ, Canzoniero LM, Farhangrazi ZS, Ying HS, Tian M, Dugan LL, Choi DW (1997) Mediation of neuronal apoptosis by enhancement of outward potassium current. Science 278:114-117
102. Yu SP, Farhangrazi ZS, Ying HS, Yeh CH, Choi DW (1998) Enhancement of outward potassium current may participate in beta-amyloid peptide-induced cortical neuronal death. Neurobiol Dis 5:81-88
103. Yu SP, Yeh CH, Gottron F, Wang X, Grabb MC, Choi DW (1999) Role of the outward delayed rectifier K+ current in ceramide-induced caspase activation and apoptosis in cultured cortical neurons. J Neurochem 73:933-941
104. + channel inhibitor identified by high-throughput screening in yeast. Mol Pharmacol 65:214-219
105. Zalewski PD, Forbes IJ, Betts WH (1993) Correlation of apoptosis with change in intracellular labile Zn(II) using zinquin [(2-methyl-8-p- toluenesulphonamido-6-quinolyloxy)acetic acid], a new specific fluorescent probe for Zn(II). Biochem J 296:403-408
106. 2 in vitro is modulated by metallothionein. Mol Cell Biol 23:8471-8485