High Dose Zinc Supplementation Induces Hippocampal Zinc Deficiency and Memory Impairment with Inhibition of BDNF Signaling

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Yang, Yang ^a   Jing, Xiao Peng ^a   Zhang, Shou Peng ^a   Gu, Run Xia ^a   Tang, Fang Xu ^a   Wang, Xiu Lian ^a   Xiong, Yan ^a   Qiu, Mei ^a   Sun, Xu Ying ^a   Ke, Dan ^a   Wang, Jian Zhi ^a   Liu, Rong ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; BRAIN PROTEIN; DRINKING WATER; GLUTAMATE RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; POSTSYNAPTIC DENSITY PROTEIN 93; POSTSYNAPTIC DENSITY PROTEIN 95; UNCLASSIFIED DRUG; ZINC;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN LEVEL; BRAIN METABOLISM; CHELATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DENDRITIC SPINE; DIET SUPPLEMENTATION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL MOSSY FIBER; HIPPOCAMPUS; IN VIVO STUDY; INSTITUTE FOR CANCER RESEARCH MOUSE; INTOXICATION; MALE; MEMORY DISORDER; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; SYNAPSE; WEANING; ZINC DEFICIENCY; ZINC METABOLISM; ZINC OVERLOAD;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DIETARY SUPPLEMENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; GUANYLATE KINASE; HIPPOCAMPUS; HISTOLOGICAL TECHNIQUES; MALE; MEMBRANE PROTEINS; MEMORY DISORDERS; MICE; MICE, INBRED ICR; RECEPTOR, TRKB; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; ZINC;

EID: 84873179877     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055384     Document Type: Article

References (54)

1. Maret W, Sandstead HH, (2006) Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Biol 20: 3-18.
2. Prasad AS, (2009) Impact of the discovery of human zinc deficiency on health. J Am Coll Nutr 28: 257-265.
3. Yu SM, Kogan MD, Gergen P, (1997) Vitamin-mineral supplement use among preschool children in the United States. Pediatrics 100: E4.
4. Brown KH, Peerson JM, Baker SK, Hess SY, (2009) Preventive zinc supplementation among infants, preschoolers, and older prepubertal children. Food Nutr Bull 30: S12-S40.
5. Lassi ZS, Haider BA, Bhutta ZA (2010) Zinc supplementation for the prevention of pneumonia in children aged 2 months to 59 months. Cochrane Database Syst Rev: D5978.
6. Wang W, MacDonald VM, Paudel M, Banke KK, (2011) National scale-up of zinc promotion in Nepal: results from a post-project population-based survey. J Health Popul Nutr 29: 207-217.
7. Briefel R, Ziegler P, Novak T, Ponza M, (2006) Feeding Infants and Toddlers Study: characteristics and usual nutrient intake of Hispanic and non-Hispanic infants and toddlers. J Am Diet Assoc 106: S84-S95.
8. Huybrechts I, Maes L, Vereecken C, De Keyzer W, De Bacquer D, et al. (2010) High dietary supplement intakes among Flemish preschoolers. Appetite 54: 340-345.
9. Frederickson CJ, Koh JY, Bush AI, (2005) The neurobiology of zinc in health and disease. Nat Rev Neurosci 6: 449-462.
10. Qian J, Noebels JL, (2005) Visualization of transmitter release with zinc fluorescence detection at the mouse hippocampal mossy fibre synapse. J Physiol 566: 747-758.
11. Vogt K, Mellor J, Tong G, Nicoll R, (2000) The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 26: 187-196.
12. Li Y, Hough CJ, Frederickson CJ, Sarvey JM, (2001) Induction of mossy fiber -> Ca3 long-term potentiation requires translocation of synaptically released Zn2+. J Neurosci 21: 8015-8025.
13. Lu YM, Taverna FA, Tu R, Ackerley CA, Wang YT, et al. (2000) Endogenous Zn(2+) is required for the induction of long-term potentiation at rat hippocampal mossy fiber-CA3 synapses. Synapse 38: 187-197.
14. Guidolin D, Polato P, Venturin G, Zanotti A, Mocchegiani E, et al. (1992) Correlation between zinc level in hippocampal mossy fibers and spatial memory in aged rats. Ann N Y Acad Sci 673: 187-193.
15. Frederickson RE, Frederickson CJ, Danscher G, (1990) In situ binding of bouton zinc reversibly disrupts performance on a spatial memory task. Behav Brain Res 38: 25-33.
16. Bhatnagar S, Taneja S, (2001) Zinc and cognitive development. Br J Nutr 85Suppl 2: S139-S145.
17. Gao HL, Xu H, Xin N, Zheng W, Chi ZH, et al. (2011) Disruption of the CaMKII/CREB signaling is associated with zinc deficiency-induced learning and memory impairments. Neurotox Res 19: 584-591.
18. Halas ES, Hunt CD, Eberhardt MJ, (1986) Learning and memory disabilities in young adult rats from mildly zinc deficient dams. Physiol Behav 37: 451-458.
19. Flinn JM, Hunter D, Linkous DH, Lanzirotti A, Smith LN, et al. (2005) Enhanced zinc consumption causes memory deficits and increased brain levels of zinc. Physiol Behav 83: 793-803.
20. Turner TY, Soliman MR, (2000) Effects of zinc on spatial reference memory and brain dopamine (D1) receptor binding kinetics in rats. Prog Neuropsychopharmacol Biol Psychiatry 24: 1203-1217.
21. Chauhan AK, Moretti FA, Iaconcig A, Baralle FE, Muro AF, (2005) Impaired motor coordination in mice lacking the EDA exon of the fibronectin gene. Behav Brain Res 161: 31-38.
22. Cui Y, Jin J, Zhang X, Xu H, Yang L, et al. (2011) Forebrain NR2B overexpression facilitating the prefrontal cortex long-term potentiation and enhancing working memory function in mice. PLoS One 6: e20312.
23. Kellendonk C, Simpson EH, Polan HJ, Malleret G, Vronskaya S, et al. (2006) Transient and selective overexpression of dopamine D2 receptors in the striatum causes persistent abnormalities in prefrontal cortex functioning. Neuron 49: 603-615.
24. Kaitsuka T, Li ST, Nakamura K, Takao K, Miyakawa T, et al. (2011) Forebrain-specific constitutively active CaMKKalpha transgenic mice show deficits in hippocampus-dependent long-term memory. Neurobiol Learn Mem 96: 238-247.
25. Sindreu C, Palmiter RD, Storm DR, (2011) Zinc transporter ZnT-3 regulates presynaptic Erk1/2 signaling and hippocampus-dependent memory. Proc Natl Acad Sci U S A 108: 3366-3370.
26. Tronel S, Belnoue L, Grosjean N, Revest JM, Piazza PV, et al. (2012) Adult-born neurons are necessary for extended contextual discrimination. Hippocampus 22: 292-298.
27. 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.
28. Deacon RM, Bannerman DM, Kirby BP, Croucher A, Rawlins JN, (2002) Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behav Brain Res 133: 57-68.
29. Frankland PW, Cestari V, Filipkowski RK, McDonald RJ, Silva AJ, (1998) The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 112: 863-874.
30. Plonka PM, Handjiski B, Popik M, Michalczyk D, Paus R, (2005) Zinc as an ambivalent but potent modulator of murine hair growth in vivo- preliminary observations. Exp Dermatol 14: 844-853.
31. Wang CY, Wang T, Zheng W, Zhao BL, Danscher G, et al. (2010) Zinc overload enhances APP cleavage and Abeta deposition in the Alzheimer mouse brain. PLoS One 5: e15349.
32. Railey AM, Micheli TL, Wanschura PB, Flinn JM, (2010) Alterations in fear response and spatial memory in pre- and post-natal zinc supplemented rats: remediation by copper. Physiol Behav 100: 95-100.
33. Linkous DH, Adlard PA, Wanschura PB, Conko KM, Flinn JM, (2009) The effects of enhanced zinc on spatial memory and plaque formation in transgenic mice. J Alzheimers Dis 18: 565-579.
34. Railey AM, Groeber CM, Flinn JM, (2011) The effect of metals on spatial memory in a transgenic mouse model of Alzheimer's disease. J Alzheimers Dis 24: 375-381.
35. Piechal A, Blecharz-Klin K, Pyrzanowska J, Widy-Tyszkiewicz E, (2012) Maternal zinc supplementation improves spatial memory in rat pups. Biol Trace Elem Res 147: 299-308.
36. Corona C, Masciopinto F, Silvestri E, Viscovo AD, Lattanzio R, et al. (2010) Dietary zinc supplementation of 3xTg-AD mice increases BDNF levels and prevents cognitive deficits as well as mitochondrial dysfunction. Cell Death Dis 1: e91.
37. 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: 1471S-1483S.
38. Maynard CJ, Cappai R, Volitakis I, Laughton KM, Masters CL, et al. (2009) Chronic exposure to high levels of zinc or copper has little effect on brain metal homeostasis or Abeta accumulation in transgenic APP-C100 mice. Cell Mol Neurobiol 29: 757-767.
39. Chowanadisai W, Kelleher SL, Lonnerdal B, (2005) Maternal zinc deficiency reduces NMDA receptor expression in neonatal rat brain, which persists into early adulthood. J Neurochem 94: 510-519.
40. Takeda A, Takefuta S, Okada S, Oku N, (2000) Relationship between brain zinc and transient learning impairment of adult rats fed zinc-deficient diet. Brain Res 859: 352-357.
41. Danscher G, (1981) Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electronmicroscopy. Histochemistry 71: 1-16.
42. Leutgeb S, (2008) Neuroscience. Detailed differences. Science 319: 1623-1624.
43. Riedel G, Platt B, Micheau J, (2003) Glutamate receptor function in learning and memory. Behav Brain Res 140: 1-47.
44. Vessey JP, Karra D, (2007) More than just synaptic building blocks: scaffolding proteins of the post-synaptic density regulate dendritic patterning. J Neurochem 102: 324-332.
45. Adlard PA, Parncutt JM, Finkelstein DI, Bush AI, (2010) Cognitive loss in zinc transporter-3 knock-out mice: a phenocopy for the synaptic and memory deficits of Alzheimer's disease? J Neurosci 30: 1631-1636.
46. Caldeira MV, Melo CV, Pereira DB, Carvalho RF, Carvalho AL, et al. (2007) BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons. Mol Cell Neurosci 35: 208-219.
47. Hu X, Ballo L, Pietila L, Viesselmann C, Ballweg J, et al. (2011) BDNF-induced increase of PSD-95 in dendritic spines requires dynamic microtubule invasions. J Neurosci 31: 15597-15603.
48. Kim JH, Roberts DS, Hu Y, Lau GC, Brooks-Kayal AR, et al. (2012) Brain-derived neurotrophic factor uses CREB and Egr3 to regulate NMDA receptor levels in cortical neurons. J Neurochem 120: 210-219.
49. Egan MF, Kojima M, Callicott JH, Goldberg TE, Kolachana BS, et al. (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112: 257-269.
50. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, et al. (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 92: 8856-8860.
51. Patterson SL, Abel T, Deuel TA, Martin KC, Rose JC, et al. (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16: 1137-1145.
52. Hwang IY, Sun ES, An JH, Im H, Lee SH, et al. (2011) Zinc-triggered induction of tissue plasminogen activator by brain-derived neurotrophic factor and metalloproteinases. J Neurochem 118: 855-863.
53. Nowak G, Legutko B, Szewczyk B, Papp M, Sanak M, et al. (2004) Zinc treatment induces cortical brain-derived neurotrophic factor gene expression. Eur J Pharmacol 492: 57-59.
54. Hwang JJ, Park MH, Choi SY, Koh JY, (2005) Activation of the Trk signaling pathway by extracellular zinc. Role of metalloproteinases. J Biol Chem 280: 11995-12001.