Chemical blocking of zinc ions in CNS increases neuronal damage following traumatic brain injury (TBI) in mice

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Doering, Peter ^a   Stoltenberg, Meredin ^a   Penkowa, Milena ^b   Rungby, Jørgen ^a   Larsen, Agnete ^a   Danscher, Gorm ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; GLIAL FIBRILLARY ACIDIC PROTEIN; SELENITE; SELENIUM; ZINC ION; CHELATING AGENT; DIETHYLDITHIOCARBAMIC ACID; DIHYDROXYETHYLDITHIOCARBAMATE; DRUG DERIVATIVE; GLUTAMIC ACID; SODIUM SELENITE; ZINC;

ANALYTIC METHOD; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN DAMAGE; BRAIN SLICE; CELL COUNT; CENTRAL NERVOUS SYSTEM; CHELATION; CONTROLLED STUDY; GLIOSIS; HISTOPATHOLOGY; MOUSE; NICK END LABELING; NONHUMAN; TRAUMATIC BRAIN INJURY; WILD TYPE; ANIMAL; BRAIN INJURY; CELL DEATH; DRUG EFFECT; METABOLISM; MOUSE MUTANT; NERVE CELL; PATHOLOGY;

MUS;

ANIMALS; BRAIN INJURIES; CELL DEATH; CENTRAL NERVOUS SYSTEM; CHELATING AGENTS; DITIOCARB; GLUTAMIC ACID; MICE; MICE, KNOCKOUT; NEURONS; SODIUM SELENITE; ZINC;

EID: 77955619761     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010131     Document Type: Article

References (57)

1. Takeda A (2000) Movement of zinc and its functional significance in the brain. Brain Res Rev 34(3): 137-148.
2. Dineley KE, Votyakova TV, Reynolds IJ (2003) Zinc inhibition of cellular energy production: implications for mitochondria and neurodegeneration. J Neurochem 85(3): 563-570.
3. Pérez-Clausell J, Danscher G (1985) Intravesicular localization of zinc in rat telencephalic boutons. A histochemical study. Brain Res 337(1): 91-98.
4. Frederickson CJ, Suh SW, Silva D, Frederickson CJ, Thompson RB (2000) Importance of zinc in the central nervous system: the zinc-containing neuron. J Nutr 130(5S Suppl): 1471S-1483S.
5. Takeda A (2001) Zinc homeostasis and functions of zinc in the brain. Biometals 14(3-4): 343-351.
6. 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(4): 867-877.
7. Danscher G, Stoltenberg M (2005) Zinc-specific autometallographic in vivo selenium methods: tracing of zinc-enriched (ZEN) terminals, ZEN pathways, and pools of zinc ions in a multitude of other ZEN cells. J Histochem Cytochem 53(2): 141-153.
8. Danscher G, Jo SM, Varea E, Wang Z, Cole TB, et al. (2001) Inhibitory zincenriched terminals in mouse spinal cord. Neuroscience 105: 941-947.
9. Wang Z, Danscher G, Kim YK, Dahlstrom A, Jo SM (2002) Inhibitory zincenriched terminals in the mouse cerebellum: double-immunohistochemistry for zinc transporter 3 and glutamate decarboxylase. Neurosci Lett 321: 37-40.
10. Paoletti P, Vergnano AM, Barbour B, Casado M (2009) Zinc at glutamatergic synapses. Neuroscience 158(1): 126-136. Epub 2008 Feb 15.
11. Frederickson CJ, Burdette SC, Frederickson CJ, Sensi SL, Weiss JH, et al. (2004) Method for identifying neuronal cells suffering zinc toxicity by use of a novel fluorescent sensor. J Neurosci Methods 139(1): 79-89.
12. Danscher G (1982) Exogenous selenium in the brain. A histochemical technique for light and electron microscopical localization of catalytic selenium bonds. Histochemistry 76(3): 281-293.
13. Danscher G, Stoltenberg M (2006) Silver enhancement of quantum dots resulting from (1) metabolism of toxic metals in animals and humans, (2) in vivo, in vitro and immersion created zinc-sulphur/zinc-selenium nanocrystals, (3) metal ions liberated from metal implants and particles. Prog Histochem Cytochem 41(2): 57-139.
14. Slomianka L, Danscher G, Frederickson CJ (1990) Labeling of the neurons of origin of zinc-containing pathways by intraperitoneal injections of sodium selenite. Neuroscience 38(3): 843-854.
15. Peŕez-Clausell J (1996) Distribution of terminal fields stained for zinc in the neocortex of the rat. J Chem Neuroanat 11(2): 99-111.
16. Brown CE, Dyck RH (2004) Distribution of zincergic neurons in the mouse forebrain. J Comp Neurol 479(2): 156-167.
17. Assaf SY, Chung SH (1984) Release of endogenous Zn2+ from brain tissue during activity. Nature 308(5961): 734-736.
18. Danscher G (1984) Dynamic changes in the stainability of rat hippocampal mossy fiber boutons after local injection of sodium sulphide, sodium selenite, and sodium diethyldithiocarbamate. In: Frederickson CJ, Howell GA, Kasarskis E, eds. The neurobiology of zinc, Part B. New York: Alan R Liss Inc. pp 177-191.
19. Howell GA, Welch MG, Frederickson CJ (1984) Stimulation-induced uptake and release of zinc in hippocampal slices. Nature 308(5961): 736-738.
20. Weiss JH, Sensi SL (2000) Ca2+-Zn2+ permeable AMPA or kainate receptors: possible key factors in selective neurodegeneration. Trends Neurosci 23(8): 365-371.
21. Wang Z, Danscher G, Kim YK, Dahlstrom A, Mook Jo S (2002) Inhibitory zincenriched terminals in the mouse cerebellum: double-immunohistochemistry for zinc transporter 3 and glutamate decarboxylase. Neurosci Lett 321(1-2): 37-40.
22. Palmiter RD, Cole TB, Quaife CJ, Findley SD (1996) ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc Natl Acad Sci U S A 93(25): 14934-14939.
23. Wenzel HJ, Cole TB, Born DE, Schwartzkroin PA, Palmiter RD (1997) Ultrastructural localization of zinc transporter-3 (ZnT-3) to synaptic vesicle membranes within mossy fiber boutons in the hippocampus of mouse and monkey. Proc Natl Acad Sci U S A 94(23): 12676-12681.
24. Linkous DH, Flinn JM, Koh JY, Lanzirotti A, Bertsch PM, et al. (2008) Evidence that the ZNT3 protein controls the total amount of elemental zinc in synaptic vesicles. J Histochem Cytochem 56(1): 3-6, Epub 2007 Aug 21.
25. Cole TB, Wenzel HJ, Kafer KE, 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 U S A 96(4): 1716-1721.
26. Danscher G (1976) Heavy metals in the hippocampal region: Some aspects of localization, function and content with special emphasis on the effect of chelating agents. Thesis, Aarhus University.
27. Danscher G, Shipley MT, Andersen P (1975) Persistent function of mossy fibre synapses after metal chelation with DEDTC (antabuse). Brain Res 85: 522-526.
28. Suh SW, Jo SM, Vajda Z, Danscher G (2001) Adrenalectomy causes loss of zinc ions in zinc-enriched (ZEN) terminals and decreases seizure-induced neuronal death. Brain Res 895(1-2): 25-32.
29. Cole TB, Robbins CA, Wenzel HJ, Schwartzkroin PA, Palmiter RD (2000) Seizures and neuronal damage in mice lacking vesicular zinc. Epilepsy Res 39(2): 153-169.
30. Frederickson CJ, Cuajungco MP, Frederickson CJ (2005) Is zinc the link between compromises of brain perfusion (excitotoxicity) and Alzheimer's disease? J Alzheimer Dis 8(2): 155-160; discussion 209-215.
31. Suh SW, Chen JW, Motamedi M, Bell B, Listiak K, et al. (2000) Evidence that synaptically-released zinc contributes to neuronal injury after traumatic brain injury. Brain Res 852(2): 268-273.
32. Koh JY, Suh SW, Gwag BJ, He YY, Hsu CY, et al. (1996) The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 272(5264): 1013-1016.
33. Sørensen JC, Mattsson B, Andreasen A, Johansson BB (1998) Rapid disappearance of zinc positive terminals in focal brain ischemia. Brain Res 812(1-2): 265-269.
34. Frederickson CJ, Hernandez MD, McGinty JF (1989) Translocation of zinc may contribute to seizure-induced death of neurons. Brain Res 480(1-2): 317-321.
35. Danscher G, Haug FM, Fredens K (1973) Effect of diethyldithiocarbamate (DEDTC) on sulphide silver stained boutons. Reversible blocking of Timm's sulphide silver stain for ''heavy'' metals in DEDTC treated rats (light microscopy). Exp Brain Res 16(5): 521-532.
36. Côté A, Chiasson M, Peralta MR, 3rd, Lafortune K, Pellegrini L, Tóth K (2005) Cell type-specific action of seizure-induced intracellular zinc accumulation in the rat hippocampus. J Physiol 566(Pt 3): 821-837. Epub 2005 May 26.
37. Domínguez MI, Blasco-Ibáñez JM, Crespo C, Nacher J, Marqués-Mari ́ AI, et al. (2006) Neural overexcitation and implication of NMDA and AMPA receptors in a mouse model of temporal lobe epilepsy implying zinc chelation. Epilepsia 47(5): 887-899.
38. Valente T, Auladell C (2002) Developmental expression of ZnT3 in mouse brain: correlation between the vesicular zinc transporter protein and chelatable vesicular zinc (CVZ) cells. Glial and neuronal CVZ cells interact. Mol Cell Neurosci 21(2): 189-204.
39. Slomianka L (1992) Neurons of origin of zinc-containing pathways and the distribution of zinc-containing boutons in the hippocampal region of the rat. Neuroscience 48(2): 325-352.
40. Danscher G, Stoltenberg M (2006) Silver enhancement of quantum dots resulting from (1) metabolism of toxic metals in animals and humans, (2) in vivo, in vitro and immersion created zinc-sulphur/zinc-selenium nanocrystals, (3) metal ions liberated from metal implants and particles. Prog Histochem Cytochem 41(2): 57-139. Epub 2006 Aug 7. Review.
41. Doering P, Danscher G, Larsen A, Bruhn M, Søndergaard C, et al. (2007) Changes in the vesicular zinc pattern following traumatic brain injury. Neuroscience 150(1): 93-103.
42. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874(2): 123-130.
43. Carrasco J, Penkowa M, Hadberg H, Molinero A, Hidalgo J (2000) Enhanced seizures and hippocampal neurodegeneration following kainic acid-induced seizures in metallothionein-I + II-deficient mice. Eur J Neurosci 12(7): 2311-2322.
44. Larsen A, Kolind K, Pedersen DS, Doering P, Pedersen MO, et al. (2008) Gold ions bio-released from metallic gold particles reduce inflammation and apoptosis and increase the regenerative responses in focal brain injury. Histochem Cell Biol 130(4): 681-692. Epub 2008 Jun 10.
45. Wang Z, Li JY, Dahlstrom A, Danscher G (2001) Zinc-enriched GABAergic terminals in mouse spinal cord. Brain Res 921: 165-172.
46. Yeiser EC, Lerant AA, Casto RM, Levenson CW (1999) Free zinc increases at the site of injury after cortical stab wounds in mature but not immature rat brain. Neurosci Lett 277(2): 75-78.
47. Lee JY, Cole TB, Palmiter RD, Koh JY (2000) Accumulation of zinc in degenerating hippocampal neurons of ZnT3-null mice after seizures: evidence against synaptic vesicle origin. J Neurosci 20(11): RC79.
48. 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(1): 337-347.
49. Kitamura Y, Iida Y, Abe J, Ueda M, Mifune M, et al. (2006) Protective effect of zinc against ischemic neuronal injury in a middle cerebral artery occlusion model. J Pharmacol Sci 100(2): 142-148.
50. Hellmich HL, Eidson K, Cowart J, Crookshanks J, Boone DK, et al. (2008) Chelation of neurotoxic zinc levels does not improve neurobehavioral outcome after traumatic brain injury. 1: Neurosci Lett 440(2): 155-159. Epub.May 23.
51. Ismail T, Mauerhofer E, Slomianka L (2008) The hippocampal region of rats and mice after a single i.p. dose of clioquinol: loss of synaptic zinc, cell death and c-Fos induction. Neuroscience 157(3): 697-707. Epub 2008 Sep 11.
52. Stoltenberg M, Bush AI, Bach G, Smidt K, Larsen A, et al. (2007) Amyloid plaques arise from zinc-enriched cortical layers in APP/PS1 transgenic mice and are paradoxically enlarged with dietary zinc deficiency. Neuroscience 150(2): 357-369. Epub 2007 Sep 18.
53. Maret W (2009) Molecular aspects of human cellular zinc homeostasis: redox control of zinc potentials and zinc signals. Biometals 22(1): 149-157. Epub 2009 Jan 7.
54. Bitanihirwe BK, Cunningham MG (2009) Zinc: the brain's dark horse. Synapse 63(11): 1029-1049.
55. Yeiser EC, Vanlandingham JW, Levenson CW (2002) Moderate zinc deficiency increases cell death after brain injury in the rat. Nutr Neurosci 5(5): 345-352.
56. Lee JM, Zipfel GJ, Park KH, He YY, Hsu CY, et al. (2002) Zinc translocation accelerates infarction after mild transient focal ischemia. Neuroscience 115(3): 871-878.
57. Suh SW, Frederickson CJ, Danscher G (2006) Neurotoxic zinc translocation into hippocampal neurons is inhibited by hypothermia and is aggravated by hyperthermia after traumatic brain injury in rats. J Cereb Blood Flow Metab 26(2): 161-169.