Zinc Chelation Reduces Hippocampal Neurogenesis after Pilocarpine-Induced Seizure

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Kim, Jin Hee ^a   Jang, Bong Geom ^a   Choi, Bo Young ^a   Kwon, Lyo Min ^a   Sohn, Min ^b   Song, Hong Ki ^a   Suh, Sang Won ^a  

^a Hallym University   (South Korea)

^b Inha University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CLIOQUINOL; DOUBLECORTIN; KI 67 ANTIGEN; LITHIUM; N,N,N',N' TETRAKIS(2 PYRIDYLMETHYL)ETHYLENEDIAMINE; PILOCARPINE; ZINC;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHELATION; CONTROLLED STUDY; DRUG ACTIVITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HORMONAL REGULATION; HYPOGLYCEMIA; IMMUNOHISTOCHEMISTRY; MALE; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROPROTECTION; NONHUMAN; RAT; SEIZURE; STEM CELL; SUBICULUM;

ANIMALS; CELL DEATH; CELL PROLIFERATION; CHELATING AGENTS; CLIOQUINOL; DENTATE GYRUS; ETHYLENEDIAMINES; HIPPOCAMPUS; MALE; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; NEUROPROTECTIVE AGENTS; PILOCARPINE; RATS; SEIZURES; ZINC;

RATTUS;

EID: 84868272893     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048543     Document Type: Article

References (50)

1. Bengzon J, Kokaia Z, Elmer E, Nanobashvili A, Kokaia M, et al. (1997) Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci U S A 94: 10432-10437.
2. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, et al. (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17: 3727-3738.
3. Parent JM, Valentin VV, Lowenstein DH, (2002) Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J Neurosci 22: 3174-3188.
4. Suh SW, Fan Y, Hong SM, Liu Z, Matsumori Y, et al. (2005) Hypoglycemia induces transient neurogenesis and subsequent progenitor cell loss in the rat hippocampus. Diabetes 54: 500-509.
5. Suh SW, Won SJ, Hamby AM, Yoo BH, Fan Y, et al. (2009) Decreased brain zinc availability reduces hippocampal neurogenesis in mice and rats. J Cereb Blood Flow Metab 29: 1579-1588.
6. Perez-Clausell J, Danscher G, (1985) Intravesicular localization of zinc in rat telencephalic boutons. A histochemical study. Brain Res 337: 91-98.
7. 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.
8. Ming GL, Song H, (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28: 223-250.
9. Prasad AS, Schulert AR, Miale A Jr, Farid Z, Sandstead HH, (1963) Zinc and iron deficiencies in male subjects with dwarfism and hypogonadism but without ancylostomiasis, schistosomiasis or severe anemia. Am J Clin Nutr 12: 437-444.
10. 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.
11. Maret W, Sandstead HH, (2006) Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Biol 20: 3-18.
12. MacDonald RS, (2000) The role of zinc in growth and cell proliferation. J Nutr 130: 1500S-1508S.
13. Stewart GR, Frederickson CJ, Howell GA, Gage FH, (1984) Cholinergic denervation-induced increase of chelatable zinc in mossy-fiber region of the hippocampal formation. Brain Res 290: 43-51.
14. Dvergsten CL, Fosmire GJ, Ollerich DA, Sandstead HH, (1983) Alterations in the postnatal development of the cerebellar cortex due to zinc deficiency. I. Impaired acquisition of granule cells. Brain Res 271: 217-226.
15. Sandstead HH, Frederickson CJ, Penland JG, (2000) History of zinc as related to brain function. J Nutr 130: 496S-502S.
16. Golub MS, Takeuchi PT, Keen CL, Gershwin ME, Hendrickx AG, et al. (1994) Modulation of behavioral performance of prepubertal monkeys by moderate dietary zinc deprivation. Am J Clin Nutr 60: 238-243.
17. Persinger MA, Makarec K, Bradley JC, (1988) Characteristics of limbic seizures evoked by peripheral injections of lithium and pilocarpine. Physiol Behav 44: 27-37.
18. Suh SW, Aoyama K, Chen Y, Garnier P, Matsumori Y, et al. (2003) Hypoglycemic neuronal death and cognitive impairment are prevented by poly(ADP-ribose) polymerase inhibitors administered after hypoglycemia. J Neurosci 23: 10681-10690.
19. Schmued LC, Hopkins KJ, (2000) Fluoro-Jade: novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicol Pathol 28: 91-99.
20. 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.
21. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM, (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115: 97-105.
22. Nacher J, Crespo C, McEwen BS, (2001) Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14: 629-644.
23. Nitzan YB, Sekler I, Frederickson CJ, Coulter DA, Balaji RV, et al. (2003) Clioquinol effects on tissue chelatable zinc in mice. J Mol Med (Berl) 81: 637-644.
24. Danscher G, Rytter Norgaard JO, (1985) Ultrastructural autometallography: a method for silver amplification of catalytic metals. J Histochem Cytochem 33: 706-710.
25. Frederickson CJ, (1989) Neurobiology of zinc and zinc-containing neurons. Int Rev Neurobiol 31: 145-238.
26. Frederickson CJ, Hernandez MD, McGinty JF, (1989) Translocation of zinc may contribute to seizure-induced death of neurons. Brain Res 480: 317-321.
27. Suh SW, Thompson RB, Frederickson CJ, (2001) Loss of vesicular zinc and appearance of perikaryal zinc after seizures induced by pilocarpine. Neuroreport 12: 1523-1525.
28. 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.
29. 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: 1013-1016.
30. 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: 268-273.
31. 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: 161-169.
32. Suh SW, Garnier P, Aoyama K, Chen Y, Swanson RA, (2004) Zinc release contributes to hypoglycemia-induced neuronal death. Neurobiol Dis 16: 538-545.
33. Suh SW, Hamby AM, Swanson RA, (2007) Hypoglycemia, brain energetics, and hypoglycemic neuronal death. Glia 55: 1280-1286.
34. Halas ES, Eberhardt MJ, Diers MA, Sandstead HH, (1983) Learning and memory impairment in adult rats due to severe zinc deficiency during lactation. Physiol Behav 30: 371-381.
35. Altman J, Das GD, (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319-335.
36. Gueneau G, Privat A, Drouet J, Court L, (1982) Subgranular zone of the dentate gyrus of young rabbits as a secondary matrix. A high-resolution autoradiographic study. Dev Neurosci 5: 345-358.
37. Eckenhoff MF, Rakic P, (1988) Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci 8: 2729-2747.
38. Kaplan MS, Hinds JW, (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197: 1092-1094.
39. Bayer SA, Yackel JW, Puri PS, (1982) Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216: 890-892.
40. Kaplan MS, Bell DH, (1984) Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J Neurosci 4: 1429-1441.
41. Cameron HA, Woolley CS, McEwen BS, Gould E, (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56: 337-344.
42. Seki T, Arai Y, (1993) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13: 2351-2358.
43. Kuhn HG, Dickinson-Anson H, Gage FH, (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16: 2027-2033.
44. Okano HJ, Pfaff DW, Gibbs RB, (1993) RB and Cdc2 expression in brain: correlations with 3H-thymidine incorporation and neurogenesis. J Neurosci 13: 2930-2938.
45. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, et al. (1990) Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 10: 267-282.
46. Manford M, Hart YM, Sander JW, Shorvon SD, (1992) National General Practice Study of Epilepsy (NGPSE): partial seizure patterns in a general population. Neurology 42: 1911-1917.
47. Engel J Jr, (1996) Surgery for seizures. N Engl J Med 334: 647-652.
48. Mello LE, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, et al. (1993) Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34: 985-995.
49. Park MH, Lee SJ, Byun HR, Kim Y, Oh YJ, et al. (2011) Clioquinol induces autophagy in cultured astrocytes and neurons by acting as a zinc ionophore. Neurobiol Dis.
50. Corniola RS, Tassabehji NM, Hare J, Sharma G, Levenson CW, (2008) Zinc deficiency impairs neuronal precursor cell proliferation and induces apoptosis via p53-mediated mechanisms. Brain Res 1237: 52-61.