Seizures and neuronal damage in mice lacking vesicular zinc

Epilepsy Research

Volumn 39, Issue 2, 2000, Pages 153-169

  Cole, Toby B ^a   Robbins, Carol A ^a   Wenzel, H Jürgen ^a   Schwartzkroin, Philip A ^a,b   Palmiter, Richard D ^a,b  

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

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Bicuculline; Kainic acid; Mouse; MT III; Zinc; ZnT3

Indexed keywords

BICUCULLINE; FLUROTHYL; KAINIC ACID; METALLOTHIONEIN; PENTETRAZOLE; ZINC;

ARTICLE; COMPLEX PARTIAL SEIZURE; CONTROLLED STUDY; DISEASE SEVERITY; ELECTROENCEPHALOGRAM; GENE DISRUPTION; GENE TARGETING; MOUSE; MYOCLONUS SEIZURE; NERVE CELL EXCITABILITY; NERVE CELL LESION; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SEIZURE; SEIZURE SUSCEPTIBILITY; SEIZURE THRESHOLD; SYNAPSE VESICLE; TONIC CLONIC SEIZURE;

EID: 0033977114     PISSN: 09201211     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0920-1211(99)00121-7     Document Type: Article

References (77)

1. L. Aniksztejn G. Charton Y. Ben-Ari Selective release of endogenous zinc from the hippocampal mossy fibers in situ Brain Res. 404 1987 58 64
2. 2+ from brain tissue during activity Nature 308 1984 734 736
3. Y. Ben-Ari E. Cherubini Zinc and GABA in developing brain Nature 353 1991 220
4. E.H. Buhl T.S. Otis I. Mody Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model Science 271 1996 369 373
5. J.J. Celentano M. Gyenes T.T. Gibbs D.H. Farb Negative modulation of the gamma-aminobutyric acid response by extracellular zinc Mol. Pharmacol. 40 1991 766 773
6. 2+ in the hippocampal mossy fiber zone of the rat in situ Exp. Brain Res. 58 1985 202 205
7. D.W. Choi J.Y. Koh Zinc and brain injury Annu. Rev. Neurosci. 21 1998 347 375
8. D.W. Choi M. Yokoyama J. Koh Zinc neurotoxicity in cortical cell culture Neuroscience 24 1988 67 79
9. C.W. Christine D.W. Choi Effect of zinc on NMDA receptor-mediated channel currents in cortical neurons J. Neurosci. 10 1990 108 116
10. 2+) in the brains of epileptogenic and normal mice Brain Res. 280 1983 323 334
11. T.B. Cole H.J. Wenzel K.E. Kafer P.A. Schwartzkroin R.D. Palmiter 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 1999 1716 1721
12. J.T. Coyle P. Puttfarcken Oxidative stress, glutamate, and neurodegenerative disorders Science 262 1993 689 695
13. I.L. Crawford J.D. Connor Zinc in maturing rat brain: hippocampal concentration and localization J. Neurochem. 19 1972 1451 1458
14. G. Danscher Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electron microscopy Histochemistry 71 1981 1 16
15. G. Danscher Dynamic changes in the stainability of rat hippocampal mossy fiber boutons after local injection of sodium sulphide, sodium selenite, and sodium diethyldithiocarbamate C.J. Frederickson E.J. Kasarskis G.A. Howell The Neurobiology of Zinc B 1984 A.R. Liss New York 177 191
16. 2+ Neuron 5 1990 781 788
17. B.H. Eng M.L. Guerinot D. Eide M.H. Saier Jr Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins J. Membrane Biol. 166 1998 1 7
18. R.M. Epand A.R. Stafford M. Tyers E. Nieboer Mechanism of action of diabetogenic zinc-chelating agents Mol. Pharmacol. 27 1985 366 374
19. J.C. Erickson G. Hollopeter S.A. Thomas G.J. Froelick R.D. Palmiter Disruption of the metallothionein-III gene in mice: analysis of brain zinc, behavior, and neuron vulnerability to metals, aging, and seizures J. Neurosci. 17 1997 1271 1281
20. D.J. Feller D.Y. Tso-Olivas D.D. Savage Hippocampal mossy fiber zinc deficit in mice genetically selected for ethanol withdrawal seizure susceptibility Brain Res. 545 1991 73 79
21. D.J. Finney Probit Analysis 1971 Cambridge University Press London
22. C.J. Frederickson D.W. Moncrieff Zinc-containing neurons Biol. Signals 3 1994 127 139
23. C.J. Frederickson E.J. Kasarskis D. Ringo R.E. Frederickson A quinoline fluorescence method for visualizing and assaying the histochemically reactive zinc (bouton zinc) in the brain J. Neurosci. Methods 20 1987 91 103
24. C.J. Frederickson M.D. Hernandez J.F. McGinty Translocation of zinc may contribute to seizure-induced death of neurons Brain Res. 480 1989 317 321
25. C.J. Frederickson Neurobiology of zinc and zinc-containing neurons Int. Rev. Neurobiol. 31 1989 145 238
26. 2+-induced neurotoxicity in rat primary cortical cultures: involvement of L-type calcium channels Brain Res. 654 1994 257 264
27. M. Fukahori M. Itoh Effects of dietary zinc status on seizure susceptibility and hippocampal zinc content in the El (epilepsy) mouse Brain Res. 529 1990 16 22
28. M. Fukahori M. Itoh K. Oomagari H. Kawasaki Zinc content in discrete hippocampal and amygdaloid areas of the epilepsy (El) mouse and normal mice Brain Res. 455 1988 381 384
29. 2+: an endogenous modulator of ligand- and voltage-gated ion channels Neuropharmacology 33 1994 935 952
30. F.M. Haug Electron microscopical localization of the zinc in hippocampal mossy fibre synapses by a modified sulphide silver procedure Histochemie 8 1967 355 368
31. G.E. Homanics T.M. DeLorey L.L. Firestone J.J. Quinlan A. Handforth N.L. Harrison M.D. Krasowski C.E.M. Rick E.R. Korpi R. Mäkela M.H. Brilliant N. Hagiwara C. Ferguson K. Snyder R.W. Olsen Mice devoid of γ-aminobutyrate type A receptor β3 subunit have epilepsy, cleft palate, and hypersensitive behavior Proc. Natl. Acad. Sci. U.S.A. 94 1997 4143 4148
32. G.A. Howell M.G. Welch C.J. Frederickson Stimulation-induced uptake and release of zinc in hippocampal slices Nature 308 1984 736 738
33. L. Huang J. Gitschier A novel gene involved in zinc transport is deficient in the lethal milk mouse Nat. Genet. 17 1997 292 297
34. M. Itoh M. Ebadi The selective inhibition of hippocampal glutamic acid decarboxylase in zinc-induced epileptic seizures Neurochem. Res. 7 1982 1287 1298
35. P. Kantheti X. Qiao M.E. Diaz A.A. Peden G.E. Meyer S.L. Carskadon D. Kapfhamer D. Sufalko M.S. Robinson J.L. Noebels M. Burmeister Mutation of the AP-3 delta subunit in the mocha mouse links endosomal cargo transport to storage deficiency in platelets, melanosomes, and neurotransmitter vesicles Neuron 21 1998 111 122
36. E.J. Kasarskis T.M. Forrester J.T. Slevin Amygdalar kindling is associated with elevated zinc concentration in the cortex and hippocampus of rats Epilepsy Res. 1 1987 227 233
37. S.F. Kash R.S. Johnson L.H. Tecott J.L. Noebels R.D. Mayfield D. Hanahan S. Baekkeskov Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase Proc. Natl. Acad. Sci. U.S.A. 9 1997 14060 14065
38. J.Y. Koh D.W. Choi Zinc toxicity on cultured cortical neurons: involvement of N -methyl- d -aspartate receptors Neuroscience 60 1994 1049 1057
39. J.Y. Koh S.W. Suh B.J. Gwag Y.Y. He C.Y. Hsu D.W. Choi The role of zinc in selective neuronal death after transient global cerebral ischemia Science 272 1996 1013 1016
40. B receptors Neurosci. Lett. 135 1992 215 218
41. G.J. Lees A. Lehmann M. Sandberg A. Hamberger The neurotoxicity of zinc in the rat hippocampus Neurosci. Lett. 120 1990 155 158
42. A channels by Zn Mol. Pharmacol. 39 1991 267 274
43. J. Lerma Kainate reveals its targets Neuron 19 1997 1155 1158
44. M.L. Mayer L. Vyklicky Jr The action of zinc on synaptic transmission and neuronal excitability in cultures of mouse hippocampus J. Physiol. (London) 415 1989 351 365
45. C.L. Mitchell M.I. Barnes Proconvulsant action of diethyldithiocarbamate in stimulation of the perforant path Neurotoxicol. Teratol. 15 1993 165 171
46. J.L. Noebels R.-L. Sidman Persistent hypersynchronization of neocortical neurons in the mocha mutant of mouse J. Neurogenet. 6 1989 53 56
47. R.D. Palmiter S. Findley Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc EMBO J. 14 1995 639 649
48. R.D. Palmiter T.B. Cole S.D. Findley ZnT-2, a mammalian protein that confers resistance to zinc by facilitating vesicular sequestration EMBO J. 15 1996 1784 1791
49. R.D. Palmiter T.B. Cole C.J. Quaife S.D. Findley ZnT-3, a putative transporter of zinc into synaptic vesicles Proc. Natl. Acad. Sci. U.S.A. 93 1996 14934 14939
50. S.E. Pattison M.F. Dunn On the relationship of zinc ion to the structure and function of the 7S nerve growth factor protein Biochemistry 14 1975 2733 2739
51. Y.Q. Pei I. Koyama Features of seizures and behavioral changes induced by intrahippocampal injection of zinc sulfate in the rabbit: a new experimental model of epilepsy Epilepsia 27 1986 183 188
52. J. Pérez-Clausell G. Danscher Intravesicular location of zinc in rat telencephalic boutons. A histochemical study Brain Res. 337 1985 91 98
53. S. Peters J. Koh D.W. Choi Zinc selectively blocks the action of N -methyl- d -aspartate on cortical neurons Science 236 1987 589 593
54. J.W. Prichard B.B. Gallagher G.H. Glaser Experimental seizure-threshold testing with flurothyl J. Pharmacol. Exp. Ther. 166 1969 170 178
55. R.J. Racine Modification of seizure activity by electrical stimulation. II. Motor seizure Electroencephalogr. Clin. Neurophysiol. 32 1972 281 294
56. F.A. Rassendren P. Lory J.P. Pin J. Nargeot Zinc has opposite effects on NMDA and non-NMDA receptors expressed in Xenopus oocytes Neuron 4 1990 733 740
57. S.L. Sensi L.M. Canzoniero S.P. Yu H.S. Ying J.Y. Koh G.A. Kerchner D.W. Choi Measurement of intracellular free zinc in living cortical neurons: routes of entry J. Neurosci. 17 1997 9554 9564
58. L. Slomianka Neurons of origin of zinc-containing pathways and the distribution of zinc-containing boutons in the hippocampal region of the rat Neuroscience 48 1992 325 352
59. R.S. Sloviter A selective loss of hippocampal mossy fiber Timm stain accompanies granule cell seizure activity induced by perforant path stimulation Brain Res. 330 1985 150 153
60. T.G. Smart S.J. Moss X. Xie R.L. Huganir GABAA receptors are differentially sensitive to zinc: dependence on subunit composition Br. J. Pharmacol. 103 1991 1837 1839
61. T.G. Smart X. Xie B.J. Krishek Modulation of inhibitory and excitatory amino acid receptor ion channels by zinc Prog. Neurobiol. 42 1994 393 441
62. S.L. Smart V. Lopantsev C.L. Zhang C.A. Robbins H. Wang S.Y. Chiu P.A. Schwartzkroin A. Messing B.L. Tempel Deletion of the K(V)1.1 potassium channel causes epilepsy in mice Neuron 4 1998 809 819
63. E.F. Sperber S.L. Moshe Age-related differences in seizure susceptibility to flurothyl Brain Res. 467 1988 295 297
64. M. Spiridon D. Kamm B. Billups P. Mobbs D. Atwell Modulation by zinc of the glutamate transporters in glial cells and cones isolated from the tiger salamander retina J. Physiol. 506 1998 363 376
65. N. Tonder F.F. Johansen C.J. Frederickson J. Zimmer N.H. Diemer Possible role of zinc in the selective degeneration of dentate hilar neurons after cerebral ischemia in the adult rat Neurosci. Lett. 109 1990 247 252
66. D.M. Treiman N.Y. Walton C. Kendrick A progressive sequence of electroencephalographic changes during generalized convulsive status epilepticus Epilepsy Res. 5 1990 49 60
67. M. Tsuda K. Imaizumi T. Katayama K. Kitagawa A. Wanaka M. Tohyama T. Takagi Expression of zinc transporter gene, ZnT-1, is induced after transient forebrain ischemia in the gerbil J. Neurosci. 17 1997 6678 6684
68. R.J. Vandenberg A.D. Mitrovic G.A.R. Johnston Molecular basis for differential inhibition of glutamate transporter subtypes by zinc ions Mol. Pharmacol. 54 1998 189 196
69. J.H. Weiss D.M. Hartley J.Y. Koh D.W. Choi AMPA receptor activation potentiates zinc neurotoxicity Neuron 10 1993 43 49
70. H.J. Wenzel T.B. Cole D.E. Born P.A. Schwartzkroin R.D. Palmiter 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 1997 12676 12681
71. 2+ antagonize NMDA and GABA responses of hippocampal neurons Nature 328 1987 640 643
72. B.D. Winegar J.B. Lansman Voltage dependent block by zinc of single calcium channels in mouse myotubes J. Physiol. (London) 425 1990 563 578
73. X.M. Xie T.G. Smart A physiological role for endogenous zinc in rat hippocampal synaptic neurotransmission Nature 349 1991 521 524
74. 2+ permeable AMPA/kainate channels and triggers selective neural injury Neuroreport 6 1995 2553 2556
75. 2+-permeable AMPA/kainate channels Brain Res. 781 1998 45 55
76. M. Yokoyama J. Koh D.W. Choi Brief exposure to zinc is toxic to cortical neurons Neurosci. Lett. 71 1986 351 355
77. J. Zimmer F.M. Haug Laminar differentiation of the hippocampus, fascia dentata and subiculum in developing rats, observed with the Timm sulphide silver method J. Comp. Neurol. 179 1978 581 617