Zinc in stroke: Time for a new approach?

Metal Ion in Stroke

Volumn , Issue , 2012, Pages 209-226

  Thompson, Richard B ^a  

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

Author keywords

Apoptosis; Excitotoxicity; Oxidative stress; Reactive oxygen species; Stroke; TPEN; Zinc

Indexed keywords

EID: 85017132545     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4419-9663-3_9     Document Type: Chapter

References (111)

1. Acworth IN (2003) Handbook of redox biochemistry. ESA, Inc., Chelmsford, MA
2. Ahn Y-H, Kim Y-H, Hong S-H, Koh J-Y (1998) Depletion of intracellular zinc induces protein synthesis-dependent neuronal apoptosis in mouse cortical culture. Exp Neurol 154:47-56
3. Aiuchi T, Mihara S, Nakaya M, Masuda Y, Nakajo S, Nakaya K (1998) Zinc ions prevent processing of caspase-3 during apoptosis induced by geranylgeraniol in HL-60 cells. J Biochem 124:300-303
4. Aizenman E, Stout AK, Hartnett KA, Dinely KE, McLaughlin B, Reynolds IJ (2000) Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release. J Neurochem 75:1878-1889
5. Aras MA, Aizenman E (2011) Redox regulation of intracellular zinc: molecular signaling in the life and death of neurons. Antioxidants Redox Signal 15:2249-2263
6. Arslan P, Di Virgilio F, Beltrame M, Tsien RY, Pozzan T (1985) Cytosolic Ca2+ homeostasis in Ehrlich and Yoshida carcinomas. A new, membrane-permeant chelator of heavy metals reveals that these ascites tumor cell lines have normal cytosolic free Ca2+. J Biol Chem 260:2719-2727
7. Beers MH, Berkow R (eds) (1999) The Merck manual of diagnosis and therapy, 17th edn. Merck Research Laboratories, Whitehouse Station, NJ
8. Bhatt A, Farooq MU, Enduri S, Pillainayagam C, Naravetla B, Razak A, Safdar A, Hussain S, Kassab M, Majid A (2010) Clinical significance of serum zinc levels in cerebral ischemia. Stroke Res Treat 2010:245-715.
9. Bogaert YE, Rosenthal RE, Fiskum G (1994) Postischemic inhibition of cerebral cortex pyruvate dehydrogenase. Free Radical Biol Med 16:811-820
10. Bonnani L, Chachar M, Jover-Mengual T, Li H, Jones A, Yokota H, Ofengeim D, Flannery RJ, Miyawaki T, C-h C, Polster BM, Pypaert M, Hardwick JM, Seni SL, Zukin RS, Jonas EA (2006) Zinc-dependent multi-conductance channel activity in mitochondria isolated from ischemic brain. J Neurosci 26:6851-6862
11. Boveris A, Chance B (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134:707-716
12. Bozym R, Hurst TK, Westerberg N, Stoddard A, Fierke CA, Frederickson CJ, Thompson RB (2008) Determination of zinc using carbonic anhydrase-based fluorescence biosensors. In: Brand L, Johnson M (eds) Fluorescence spectroscopy. Academic, San Diego, pp 287-309
13. Bozym RA, Thompson RB, Stoddard AK, Fierke CA (2006) Measuring picomolar intracellular exchangeable zinc in PC-12 cells using a ratiometric fluorescence biosensor. ACS Chem Biol 1:103-111
14. Bozym RA, Chimienti F, Giblin LJ, Gross GW, Korichneva I, Li Y, Libert S, Maret W, Parviz M, Frederickson CJ, Thompson RB (2010) Free zinc outside a narrow concentration range is toxic to a variety of ceils in vitro. Exp Biol Med 235:741-750
15. Bush AI, Pettingell WH, Multhaup G, Md P, Vonsattel J-P, Gusella JF, Beyreuther K, Masters CL, Tanzi RE (1994) Rapid induction of Alzheimer AB amyloid formation by zinc. Science 265:1464-1467
16. Calderone A, Jover T, Mashiko T, K-m N, Tanaka H, Bennett MVL, Zukin RS (2004) Late calcium EDTA rescues hippocampal CA1 neurons from global ischemia-induced death. J Neurosci 24:9903-9913
17. Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA (1992) 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G--T and A--C substitutions. J Biol Chem 267:166-172
18. Cherny RA, Atwood CS, Xilinas ME, Gray DN, Jones WD, McLean CA, Barnham KJ, Volitakis I, Fraser FW, Kim YS, Huang X, Goldstein LE, Moir RD, Lim JT, Beyreuther K, Zheng H, Tanzi RE, Masters C, Bush AI (2001) Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 30:665-676
19. Chimienti F, Seve M, Richard S, Mathieu J, Favier A (2001) Role of cellular zinc in programmed cell death: temporal relationship between zinc depletion, activation of caspases, and cleavage of Sp family transcription factors. Biochem Pharmacol 62:51-62
20. Choi DW, Koh JY (1998) Zinc and brain injury. Ann Rev Neurosci 21:347-375
21. Christianson DW (1991) Structural biology of zinc. Adv Protein Chem 42:281-355
22. Cole TB, Wenzel HJ, Kafer KA, Schwartzkroin PA, Palmiter RD (1999) Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc Natl Acad Sci 96:1716-1721
23. Costello LC, Liu Y, Franklin RB, Kennedy MC (1997) Zinc inhibition of mitochondrial aconitase and its importance in citrate metabolism of prostate epithelial cells. J Biol Chem 272:28875-28881
24. Coulter DA (2000) Mossy fiber zinc and temporal lobe epilepsy: Pathological association with altered "epileptic" GABAa receptors in dentate granule cells. Epilepsia 41(Suppl 6):S96-S99
25. Diener H-C, Schneider D, Lampl Y, Bornstein NM, Kozak A, Rosenberg G, on Behalf of the Study G (2008) DP-b99, a membrane-activated metal ion chelator, as neuroprotective therapy in ischemic stroke. Stroke 39:1774-1778
26. Dinely KE, Richards LL, Votyakova TV, Reynolds IJ (2005) Zinc causes loss of membrane potential and elevates reactive oxygen species in rat brain mitochondria. Mitochondrion 5:55-65
27. Dittmer PJ, Miranda JG, Gorski JA, Palmer AE (2009) Genetically encoded sensors to elucidate spatial distribution of cellular zinc. J Biol Chem 284:16289-16297
28. Dongen EMWMV, Evers TH, Dekkers LM, Meijer EW, Klomp LWJ, Merkx M (2007) Variation of linker length in ratiometric fluorescent sensor proteins allows rational tuning of Zn(II) affinity in the picomolar to femtomolar range. J Am Chem Soc 129:3494-3495
29. Elsas S-M, Hazany S, Gregory WL, Mody I (2008) Hippocampal zinc infusion delays the development of after discharges and seizures in a kindling model of epilepsy. Epilepsy 49:1-10
30. Feng P, Li T-L, Guan Z-X, Franklin RB, Costello LC (2002) Direct effect of zinc on mitochondrial apoptogenesis in prostate cells. Prostate 52:311-318
31. Fenton HJH (1894) Oxidation of tartaric acid in the presence of iron. J Chem Soc 65:899-910
32. Fiskum G, Murphy AN, Beal MF (1999) Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases. J Cerebral Blood Flow Metab 19:351-369
33. Fiskum G, Rosenthal RE, Vereczki V, Martin E, Hoffman GE, Chinopoulos C, Kowaltowski A (2004) Protection against ischemic brain injury by inhibition of mitochondrial oxidative stress. J Bioenerg Biomembr 36:347-352
34. Frazzini V, Rockabrand E, Mocchegiani E, Sensi S (2006) Oxidative stress and brain aging: is zinc the link? Biogerontology 7:307-314
35. Frederickson CJ, Maret W, Cuajungco MP (2004) Zinc and excitotoxic brain injury: a new model. Neuroscientist 10:18-25
36. Frederickson CJ, Koh J-Y, Bush AI (2005) The neurobiology of zinc in health and disease. Nat Rev Neurosci 6:449-462
37. Frederickson CJ, Klitenick MA, Manton WI, Kirkpatrick JB (1983) Cytoarchitectonic distribution of zinc in the hippocampus of man and the rat. Brain Res 273:335-339
38. Frederickson CJ, Kasarskis EJ, Ringo D, Frederickson RE (1987) A quinoline fluorescence method for visualizing and assaying histochemically reactive zinc (bouton zinc) in the brain. J Neurosci Methods 20:91-103
39. Frederickson CJ, Suh SW, Koh J-Y, Cha YK, Thompson RB, LaBuda CJ, Balaji RV, Cuajungco MP (2002) Depletion of intracellular zinc from neurons by use of an extracellular chelator in vivo and in vitro. J Histochem Cytochem 50:1659-1662
40. Frederickson CJ, Giblin LJ, Krezel A, McAdoo DJ, Muelle RN, Zeng Y, Balaji RV, Masalha R, Thompson RB, Fierke CA, Sarvey JM, Md V, Prough DS, Zornow MH (2006) Concentrations of extracellular free zinc (pZn)e in the central nervous system during simple anesthetization, ischemia, and reperfusion. Exp Neurol 198:285-293
41. GaberBP, FluhartyAL (1972) Cadmium and arsenitebinding by N-dihydrolipoylaminoethoxydextran: a model study of enzyme dithiol criteria. Bioinorg Chem 2:135-148
42. Galasso SL, Dyck RH (2007) The role of zinc in cerebral ischemia. Mol Med 13:380-387
43. Gazaryan I, Krasnikov BF, Ashby GA, Thorneley RNF, Kristal BS, Brown AM (2002) Zinc is a potent inhibitor of thiol oxidoreductase activity and stimulates reactive oxygen species production by lipoamide dehydrogenase. J Biol Chem 277:10064-10072
44. Gazaryan IG, Krasinskaya IP, Kristal BS, Brown AM (2007) Zinc irreversibly damages major enzymes of energy production and antioxidant defense prior to mitochondrial permeability transition. J Biol Chem 282:24373-24380
45. Ginsberg MD (2009) Current status of neuroprotection for cerebral ischemia. Stroke 40:S111-S114
46. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of calcium indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450
47. Halliwell B, Gutteridge JMC (1992) Biologically relevant metal ion-dependent hydroxyl radical generation. FEBS Lett 307:108-112
48. Haugland RP (2005) The handbook: a guide to fluorescent probes and labeling technologies, 10th edn. Invitrogen Corp, Carlsbad, CA
49. Jiang D, Sullivan PG, Sensi SL, Steward O, Weiss JH (2001) Zn2+ induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria. J Biol Chem 276:47524-47529
50. Kitamura Y, Iida Y, Abe J, Mifune M, Kasuya F, Ohta M, Igarashi K, Saito Y, Saji H (2006a) Release of vesicular Zn2+ in a rat transient middle cerebral artery occlusion model. Brain Res Bull 69:622
51. Kitamura Y, Iida Y, Abe J, Ueda M, Mifune M, Kasuya F, Ohta M, Igarashi K, Saito Y, Saji H (2006b) Protective effect of zinc against ischemic neuronal injury in a middle cerebral artery occlusion model. J Pharmacol Sci 100:142-148
52. Krezel A, Maret W (2006) Zinc-buffering capacity of a eukaryotic cell at physiological pZn. J Biol Inorg Chem 11:1049-1062
53. Krezel A, Maret W (2008) Thionein/metallothionein control Zn(II) availability and the activity of enzymes. J Biol Inorg Chem 13:401-409
54. Kroncke K-D, Klotz L-O (2009) Zinc fingers as biological redox switches. Antioxidants Redox Signal 11:1015-1027
55. Kumar S (ed) (1998) Apoptosis: mechanisms and role in disease. Springer-Verlag, Berlin
56. Kumar S (ed) (1999) Apoptosis: biology and mechanisms. Springer-Verlag, Berlin
57. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787-795
58. Lindskog S, Henderson LE, Kannan KK, Liljas A, Nyman PO, Strandberg B (1971) Carbonic anhydrase. In: Boyer PD (ed) The enzymes. Academic, New York, pp 587-665
59. Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80:780-787
60. Liu Y, Rosenthal RE, Haywood Y, Miljkovic-Lolic M, Vanderhoek JY, Fiskum G (1998) Normoxic ventilation after cardiac arrest reduces oxidation of brain lipids and improves neurological outcome. Stroke 29:1679-1686
61. Lo EH, Dalkara T, Moskowitz MW (2003) Mechanisms, challenges, and opportunities in stroke. Nat Rev Neurosci 4:399-414
62. Loh SN (2010) The missing zinc: p53 misfolding and cancer. Metallomics 2:442-449
63. 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
64. Maret W (1994) Oxidative metal release from metallothionein via zinc-thiol/disulfide interchange. Proc Natl Acad Sci 91:237-241
65. Maret W (2008) Metallothionein redox biology in the cytoprotective and cytotoxic functions of zinc. Exp Gerontol 43:363-369
66. Maret W, Jacob C, Vallee BL, Fischer EH (1999) Inhibitory sites in enzymes: zinc removal and reactivation by thionein. Proc Natl Acad Sci 96:1936-1940
67. Martin JL, Stork CJ, Li YV (2006) Determining zinc with commonly used calcium and zinc fluorescent indicators, a question on calcium signals. Cell Calcium 40:393-402
68. Maske H (1955) Uber den topochemischen Nachweir von Zink im Ammonshorn verschiedener Säugetiere. Die Naturwissenschaften 42:424
69. McCabe MJ, Jiang SA, Orrenius S (1993) Chelation of Intracellular zinc triggers apoptosis in mature thymocytes. Lab Investig 69:101-110
70. McCranor BM, Bozym RA, Vitolo MI, Fierke CA, Bambrick L, Polster BM, Fiskum G, Thompson RB (2012) Quantitative imaging of mitochondrial and cytosolic free zinc levels in an in vitro model of ischemia/reperfusion. J Bioenerg Biomembr in the press
71. Medvedeva YV, Lin B, Shuttleworth CW, Weiss JH (2009) Intracellular Zn2+ accumulation contributes to synaptic failure, mitochondrial depolarization, and cell death in an acute slice oxygen glucose deprivation model of ischemia. J Neurosci 29:1105-1114
72. Mik EG, Johannes T, Zuurbier CJ, Heinen A, Houben-Weerts JHPM, Balestra GM, Stap J, Beek JF, Ince C (2008) In vivo mitochondrial oxygen tension measured by a delayed fluorescence lifetime technique. Biophys J 95:3977
73. Mohr JP, Choi DW, Grotta JC, Weir B, Wolf PA (eds) (2004) Stroke: pathophysiology, diagnosis and management, 4th edn. Churchill Livingstone, Philadelphia
74. Mott DD, Benveniste M, Dingledine RJ (2008) pH-dependent inhibition of kainate receptors by zinc. J Neurosci 28:1659-1671
75. Paoletti P, Ascher P, Neyton J (1997) High-affinity zinc inhibition of NMDA NR1 -NR2A receptors. J Neurosci 17:5711-5725
76. 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. J Biol Chem 272:18530-18533
77. Qin Y, Dittmer PJ, Park JG, Jansen KB, Palmer AE (2011) Measuring steady-state and dynamic endoplasmic reticulum and Golgi Zn2+ with genetically encoded sensors. Proc Natl Acad Sci U S A 109:2012
78. Richards EM, Rosenthal RE, Kristian T, Fiskum G (2006) Postischemic hyperoxia reduces hippocampal pyruvate dehydrogenase activity. Free Radical Biol Med 40:1960
79. Ritchie CW, Bush AI, MacKinnon A, MacFarlane S, Mastwyk M, MacGregor L, Kiers L, Cherny R, Q-x L, Tammer A, Carrington D, Mavros C, Volitakis I, Xilinas M, Ames D, Davis S, Beyreuther K, Tanzi RE, Masters CL (2003) Metal-protein attenuation with Iodochlorhy droxyquin (Clioquinol) targeting A-beta amyloid deposition and toxicity in Alzheimer disease. Arch Neuorol 60:1685-1691
80. Rosenberg G, Bornstein N, Diener H-C, Gorelick PB, Shuaib A, Lees K (2011) The Membrne-Activated Chelator Stroke Intervention (MACSI) trial of DP-b99 in acute ischemic stroke: a randomized, double-blind, placebo-controlled, multinational pivotal Phase III study. Int J Stroke 6:362-367
81. Rudolf E, Rudolf K, Cervinka M (2005) Zinc induced apoptosis in HEP-2 cancer cells: the role of oxidative stress and mitochondria. BioFactors 23:107-120
82. Sensi SL, Paoletti P, Bush AI, Sekler I (2009) Zinc in the physiology and pathology of the CNS. Nat Rev Neurosci 10:780
83. Sensi SL, Ton-That D, Weiss JH, Rothe A, Gee KR (2003) A new mitochondrial fluorescent zinc sensor. Cell Calcium 34:281-284
84. Shabanzadeh AP, Shuaib A, Yang T, Salam A, Wang CX (2004) Effect of zinc in ischemic brain injury in an embolic model of stroke in rats. Neurosci Lett 356:369
85. Sheline CT, Behrens MM, Choi DW (2000) Zinc-induced cortical neuronal death: Contribution of energy failure attributable to loss of NAD and inhibition of glycolysis. J Neuorsci 20:3139-3146
86. Shuttleworth CW, Weiss JH (2011) Zinc: new clues to diverse roles in brain ischemia. Trends Pharmacol Sci 32:480
87. Sindreu C, Palmiter RD, Storm DR (2011) Zinc transporter ZnT-3 regulates presynaptic Erk1/2 signaling and hippocampus-dependent memory. Proc Natl Acad Sci 108:3366-3370
88. Soane L, Polster BM, Fiskum G (2010) Mitochondrial mechanisms of neural cell death in cerebral ischemia. In: Reed JC, Green D (eds) Apoptosis: physiology and pathology of cell death. Cambridge University Press, Cambridge
89. Solenski NJ, Rosenthal RE, Fiskum G (2006) Ischemic brain injury. In: Hemmings HC, Hopkins PM (eds) Foundations of anesthesia, 2nd edn. Elsevier, New York
90. Sorensen J, Mattson B, Andreasen A, Johansson B (1998) Rapid disappearance of zinc positive terminals in focal brain ischemia. Brain Res 812:265-269
91. Starkov AA, Fiskum G, Chinopoulos C, Lorenzo BJ, Browne SE, Patel MS, Beal MF (2004) Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J Neurosci 24:7779-7788
92. Stork CJ, Li YV (2006) Intracellular zinc elevation measured with a "calcium-specific" indicator during ischemia and reperfusion in rat hippocampus: a question on calcium overload. J Neurosci 26:10430-10437
93. Stork CJ, Li YV (2009) Rising zinc: a significant cause of ischemic neuronal death in the CA1 region of rat hippocampus. J Cerebral Blood Flow Metab 29:1399-1408
94. Suh SW, Thompson RB, Frederickson CJ (2001) Loss of vesicular zinc and appearance of per- ikaryal zinc after seizures induced by pilocarpine. Neuroreport 12:1523-1525
95. Suh SW, Chen JW, Motamedi M, Bell B, Listiak K, Pons NF, Danscher G, Frederickson CJ (1999) Evidence that synaptically-released zinc contributes to neuronal injury after traumatic brain injury. Brain Res 852:268-273
96. Telford W, Fraker PJ (1995) Preferential induction of apoptosis in mouse CD4 + CD8+ alpha betaTCR10CD3e thymocytes by zinc. J Cell Physiol 164:259-270
97. Thompson RB, Peterson D, Mahoney W, Cramer M, Maliwal BP, Suh SW, Frederickson CJ (2002) Fluorescent zinc indicators for neurobiology. J Neurosci Methods 118:63-75
98. 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
99. Turan B, Fliss H, Desilets M (1997) Oxidants increase intracellular free Zn2+ concentration in rabbit ventricular myocytes. Am J Physiol Heart Circul Physiol 272:H2095-H2106
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 Cerebral Blood Flow Metab 26:821-835
101. Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: A dawn for evolutionary medicine. Annu Rev Genet 39:359-407
102. Wei G, Hough CJ, Li Y, Sarvey JM (2004) Characterization of extracellular accumulation of Zn2+ during ischemia and reperfusion of hippocampus slices in rat. Neuroscience 125:867-877
103. Weiss JH, Sensi SL, Koh J-Y (2000) Zn(II): a novel ionic mediator of neural injury in brain disease. Trends Pharmacol Sci 21:395-401
104. Whibley C, Pharoah PDP, Hollstein M (2009) p53 polymorphisms: cancer implications. Nat Rev Cancer 9:95-107
105. Wilson DF, Rumsey WL, Green TJ, Vanderkooi JM (1988) The oxygen dependence of mitochondrial oxidative phosphorylation measured by a new optical method for measuring oxygen concentration. J Biol Chem 263:2712-2718
106. Winterbourn CC (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 4:278
107. Yin HZ, Sensi SL, Ogoshi F, Weiss JH (2002) Blockade of Ca2 + -permeable AMPA/kainate channels decreases oxygen-glucose deprivation-induced Zn2+ accumulation and neuronal loss in hippocampal pyramidal neurons. J Neurosci 22:1273-1279
108. Yokoyama M, Koh J, Choi DW (1986) Brief exposure to zinc is toxic to cortical neurons. Neurosci Lett 71:351-355
109. Zalewski P, Forbes IJ, Giannakis C (1991) Physiological role for zinc in prevention of apoptosis (gene-directed death). Biochem Int 24:1093-1101
110. 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
111. Zeng H-H, Bozym RA, Rosenthal RE, Fiskum G, Cotto-Cumba C, Westerberg N, Fierke CA, Stoddard A, Cramer ML, Frederickson CJ, Thompson RB (2005) In situ measurement of free zinc in an ischemia model and cell culture using a ratiometric fluorescence-based biosensor. In: Vo-Dinh T, Grundfest WS, Benaron DA, Cohn GE (eds) SPIE conference on advanced biomedical and clinical diagnostic systems III. SPIE, San Jose, CA, pp 51-59