Depletion of vesicular zinc in dorsal horn of spinal cord causes increased neuropathic pain in mice

BioMetals

Volumn 21, Issue 2, 2008, Pages 151-158

  Jo, Seung Mook ^a   Danscher, Gorm ^b   Schrøder, Henrik D ^c   Suh, Sang Won ^d  

^a Gachon University College of Medicine   (South Korea)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autometallography; Pain; Spinal cord; Zinc; Zinc transporter

Indexed keywords

INORGANIC SALT; UNCLASSIFIED DRUG; ZINC; ZINC SELENITE; ZINC TRANSPORTER;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOMETALLOGRAPHY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GRAY MATTER; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LUMBAR SPINE; MALE; MOUSE; NERVE CELL; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; PAIN ASSESSMENT; PAIN THRESHOLD; PRECIPITATION; SPINAL CORD DORSAL HORN; SPINAL GANGLION; SPINAL NERVE;

ANIMALS; CARRIER PROTEINS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; NEURALGIA; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; POSTERIOR HORN CELLS; SELENIUM COMPOUNDS; SPINAL CORD; SPINAL NERVES; ZINC; ZINC COMPOUNDS;

ANIMALIA; MUS; RODENTIA;

EID: 41049101009     PISSN: 09660844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10534-007-9103-x     Document Type: Article

References (55)

1. 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
2. Assaf SY, Chung SH (1984) Release of endogenous Zn2+ from brain tissue during activity. Nature 308:734-736
3. Beaulieu C, Dyck R, Cynader M (1992) Enrichment of glutamate in zinc-containing terminals of the cat visual cortex. Neuroreport 3:861-864
4. Busselberg D, Michael D, Evans ML, Carpenter DO, Haas HL (1992) Zinc (Zn2+) blocks voltage gated calcium channels in cultured rat dorsal root ganglion cells. Brain Res 593:77-81
5. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63
6. Choi YB, Lipton SA (1999) Identification and mechanism of action of two histidine residues underlying high-affinity Zn2+ inhibition of the NMDA receptor. Neuron 23:171-180
7. Christensen MK, Frederickson CJ (1998) Zinc-containing afferent projections to the rat corticomedial amygdaloid complex: a retrograde tracing study. J Comp Neurol 400:375-390
8. 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 USA 96:1716-1721
9. Danscher G (1982) Exogenous selenium in the brain. A histochemical technique for light and electron microscopical localization of catalytic selenium bonds. Histochemistry 76:281-293
10. Danscher G (1996) The autometallographic zinc-sulphide method. A new approach involving in vivo creation of nanometer-sized zinc sulphide crystal lattices in zinc-enriched synaptic and secretory vesicles. Histochem J 28:361-373
11. 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 53:141-153
12. Danscher G, Howell G, Perez-Clausell J, Hertel N (1985) The dithizone, Timm's sulphide silver and the selenium methods demonstrate a chelatable pool of zinc in CNS. A proton activation (PIXE) analysis of carbon tetrachloride extracts from rat brains and spinal cords intravitally treated with dithizone. Histochemistry 83:419-422
13. Danscher G, Stoltenberg M, Bruhn M, Sondergaard C, Jensen D (2004) Immersion autometallography: histochemical in situ capturing of zinc ions in catalytic zinc-sulfur nanocrystals. J Histochem Cytochem 52:1619-1625
14. Danscher G, Jo SM, Varea E, Wang Z, Cole TB, Schroder HD (2001) Inhibitory zinc-enriched terminals in mouse spinal cord. Neuroscience 105:941-947
15. Frederickson CJ, Danscher G (1990) Zinc-containing neurons in hippocampus and related CNS structures. Prog Brain Res 83:71-84
16. Frederickson CJ, Kasarskis EJ, Ringo D, Frederickson RE (1987) A quinoline fluorescence method for visualizing and assaying the histochemically reactive zinc (bouton zinc) in the brain. J Neurosci Methods 20:91-103
17. Frederickson CJ, Suh SW, Silva D, Thompson RB (2000) Importance of zinc in the central nervous system: the zinc-containing neuron. J Nutr 130:1471S-1483S
18. Gingrich KJ, Burkat PM (1998) Zn2+ inhibition of recombinant GABAA receptors: an allosteric, state-dependent mechanism determined by the gamma-subunit. J Physiol 506(Pt 3):609-625
19. Holm IE, Andreasen A, Danscher G, Perez-Clausell J, Nielsen H (1988) Quantification of vesicular zinc in the rat brain. Histochemistry 89:289-293
20. Howell GA, Frederickson CJ (1990) A retrograde transport method for mapping zinc-containing fiber systems in the brain. Brain Res 515:277-286
21. Howell GA, Welch MG, Frederickson CJ (1984) Stimulation-induced uptake and release of zinc in hippocampal slices. Nature 308:736-738
22. Jo SM, Danscher G, Daa Schroder H, Won MH, Cole TB (2000) Zinc-enriched (ZEN) terminals in mouse spinal cord: immunohistochemistry and autometallography. Brain Res 870:163-169
23. Kim SH, Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363
24. Kozma M, Szerdahelyi P, Kasa P (1981) Histochemical detection of zinc and copper in various neurons of the central nervous system. Acta Histochem 69:12-17
25. Larson AA, Kitto KF (1997) Manipulations of zinc in the spinal cord, by intrathecal injection of zinc chloride, disodium-calcium-EDTA, or dipicolinic acid, alter nociceptive activity in mice. J Pharmacol Exp Ther 282:1319-1325
26. Larson AA, Kitto KF (1999) Chelation of zinc in the extracellular area of the spinal cord, using ethylenediaminetetraacetic acid disodium-calcium salt or dipicolinic acid, inhibits the antinociceptive effect of capsaicin in adult mice. J Pharmacol Exp Ther 288:759-765
27. Larson AA, Giovengo SL, Shi Q, Velazquez RA, Kovacs KJ (2000) Zinc in the extracellular area of the central nervous system is necessary for the development of kainic acid-induced persistent hyperalgesia in mice. Pain 86:177-184
28. Li C, Peoples RW, Weight FF (1997) Inhibition of ATP-activated current by zinc in dorsal root ganglion neurones of bullfrog. J Physiol 505(Pt 3):641-653
29. Liu T, Walker JS, Tracey DJ (1999) Zinc alleviates thermal hyperalgesia due to partial nerve injury. Neuroreport 10:1619-1623
30. Ma JY, Zhao ZQ (2001) The effects of Zn2+ on long-term potentiation of C fiber-evoked potentials in the rat spinal dorsal horn. Brain Res Bull 56:575-579
31. Mancini M, Ricci A, Amenta F (1992) Age-related changes in sulfide-silver staining in the rat neostriatum: a quantitative histochemical study. Neurobiol Aging 13:501-504
32. Martinez-Guijarro FJ, Soriano E, Del Rio JA, Lopez-Garcia C (1991) Zinc-positive boutons in the cerebral cortex of lizards show glutamate immunoreactivity. J Neurocytol 20:834-843
33. Mook Jo S, Kuk Kim Y, Wang Z, Danscher G (2002) Retrograde tracing of zinc-enriched (ZEN) neuronal somata projecting to the olfactory bulb. Brain Res 956:230-235
34. Palmiter RD, Cole TB, Quaife CJ, Findley SD (1996) ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc Natl Acad Sci USA 93:14934-14939
35. Paoletti P, Ascher P, Neyton J (1997) High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J Neurosci 17:5711-5725
36. Perez-Clausell J, Danscher G (1985) Intravesicular localization of zinc in rat telencephalic boutons. A histochemical study. Brain Res 337:91-98
37. Perez-Clausell J, Danscher G (1986) Release of zinc sulphide accumulations into synaptic clefts after in vivo injection of sodium sulphide. Brain Res 362:358-361
38. Peters S, Koh J, Choi DW (1987) Zinc selectively blocks the action of N-methyl-D-aspartate on cortical neurons. Science 236:589-593
39. Quinta-Ferreira ME, Matias CM (2005) Tetanically released zinc inhibits hippocampal mossy fiber calcium, zinc and synaptic responses. Brain Res 1047:1-9
40. Rubio ME, Juiz JM (1998) Chemical anatomy of excitatory endings in the dorsal cochlear nucleus of the rat: differential synaptic distribution of aspartate aminotransferase, glutamate, and vesicular zinc. J Comp Neurol 399:341-358
41. Safieh-Garabedian B, Poole S, Allchorne A, Kanaan S, Saade N, Woolf CJ (1996) Zinc reduces the hyperalgesia and upregulation of NGF and IL-1 beta produced by peripheral inflammation in the rat. Neuropharmacology 35:599-603
42. Schroder HD (1977) Sulfide silver architectonics of rat, cat, and guinea pig spinal cord. A light microscopic study with Timm's method for demonstration of heavy metals. Anat Embryol (Berl) 150:251-267
43. Schroder HD (1979) Sulfide silver stainability of a type of bouton in spinal cord motoneuron neuropil: an electron microscopic study with Timm's method for demonstration of heavy metals. J Comp Neurol 186:439-450
44. Schroder HD, Danscher G, Jo SM, Su H (2000) Zinc-enriched boutons in rat spinal cord. Brain Res 868:119-122
45. Smeets WJ, Perez-Clausell J, Geneser FA (1989) The distribution of zinc in the forebrain and midbrain of the lizard Gekko gecko. A histochemical study. Anat Embryol (Berl) 180:45-56
46. Sorensen JC, Slomianka L, Christensen J, Zimmer J (1995) Zinc-containing telencephalic connections to the rat striatum: a combined Fluoro-Gold tracing and histochemical study. Exp Brain Res 105:370-382
47. Takeda A, Hirate M, Tamano H, Oku N (2003) Release of glutamate and GABA in the hippocampus under zinc deficiency. J Neurosci Res 72:537-542
48. Takeda A, Minami A, Seki Y, Oku N (2004) Differential effects of zinc on glutamatergic and GABAergic neurotransmitter systems in the hippocampus. J Neurosci Res 75:225-229
49. Vogt K, Mellor J, Tong G, Nicoll R (2000) The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 26:187-196
50. Wang Z, Li JY, Dahlstrom A, Danscher G (2001a) Zinc-enriched GABAergic terminals in mouse spinal cord. Brain Res 921:165-172
51. Wang Z, Danscher G, Mook Jo S, Shi Y, Daa Schroder H (2001b) Retrograde tracing of zinc-enriched (ZEN) neuronal somata in rat spinal cord. Brain Res 900:80-87
52. Wang ZY, Stoltenberg M, Huang L, Danscher G, Dahlstrom A, Shi Y, Li JY (2005) Abundant expression of zinc transporters in Bergman glia of mouse cerebellum. Brain Res Bull 64:441-448
53. 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 USA 94:12676-12681
54. Westbrook GL, Mayer ML (1987) Micromolar concentrations of Zn2+ antagonize NMDA and GABA responses of hippocampal neurons. Nature 328:640-643
55. Xie X, Smart TG (1994) Modulation of long-term potentiation in rat hippocampal pyramidal neurons by zinc. Pflugers Arch 427:481-486