Disruption of the CaMKII/CREB signaling is associated with zinc deficiency-induced learning and memory impairments

Neurotoxicity Research

Volumn 19, Issue 4, 2011, Pages 584-591

  Gao, Hui Ling ^a   Xu, He ^a   Xin, Na ^a   Zheng, Wei ^a   Chi, Zhi Hong ^a   Wang, Zhan You ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Calmodulin dependent protein kinase II; cAMP responsive element binding protein; Long term potentiation; Morris water maze; Neurogranin

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DISEASE ASSOCIATION; HIPPOCAMPUS; IMMUNOBLOTTING; LEARNING DISORDER; LONG TERM POTENTIATION; MAZE TEST; MEMORY DISORDER; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPATIAL MEMORY; ZINC DEFICIENCY;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CREB-BINDING PROTEIN; HIPPOCAMPUS; LEARNING; MEMORY DISORDERS; MICE; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; ZINC;

MUS;

EID: 79958098076     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-010-9206-y     Document Type: Article

References (56)

1. Barco A, Alarcon JM, Kandel ER (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689-703 (Pubitemid 34245387)
2. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39 (Pubitemid 23020772)
3. Chin D, Means AR (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10:322-328 (Pubitemid 30445239)
4. Cole TB, Martyanova A, Palmiter RD (2001) Removing zinc from synaptic vesicles does not impair spatial learning, memory, or sensorimotor functions in the mouse. Brain Res 891:253-265 (Pubitemid 32115515)
5. Costa-Mattioli M, Gobert D, Harding H, Herdy B, Azzi M, Bruno M, Bidinosti M, Ben Mamou C, Marcinkiewicz E, Yoshida M, Imataka H, Cuello AC, Seidah N, Sossin W, Lacaille JC, Ron D, Nader K, Sonenberg N (2005) Translational control of hippocampal synaptic plasticity and memory by the eIF2alpha kinase GCN2. Nature 436:1166-1173
6. De Roo M, Klauser P, Muller D (2008) LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol 6:e219
7. Fang L, Wu J, Lin Q, Willis WD (2002) Calcium-calmodulin-dependent protein kinase II contributes to spinal cord central sensitization. J Neurosci 22:4196-4204 (Pubitemid 37465726)
8. Fink CC, Meyer T (2002) Molecular mechanisms of CaMKII activation in neuronal plasticity. Curr Opin Neurobiol 12:293-299 (Pubitemid 34615755)
9. Frederickson CJ, Koh JY, Bush AI (2005) The neurobiology of zinc in health and disease. Nat Rev Neurosci 6:449-462 (Pubitemid 40774861)
10. Fukunaga K, Miyamoto E (2000) A working model of CaM kinase II activity in hippocampal long-term potentiation and memory. Neurosci Res 38:3-17
11. Gao HL, Zheng W, Xin N, Chi ZH, Wang ZY, Chen J (2009) Zinc deficiency reduces neurogenesis accompanied by neuronal apoptosis through caspase-dependent and -independent signaling pathways. Neurotox Res 16:416-425
12. Garry EM, Moss A, Delaney A, O'Neill F, Blakemore J, Bowen J, Husi H, Mitchell R, Grant SG, Fleetwood-Walker SM (2003) Neuropathic sensitization of behavioral reflexes and spinal NMDA receptor/CaM kinase II interactions are disrupted in PSD-95 mutant mice. Curr Biol 13:321-328 (Pubitemid 36230023)
13. Golub MS, Keen CL, Gershwin ME, Hendrickx AG (1995) Developmental zinc deficiency and behavior. J Nutr 125:2263S-2271S
14. Gubellini P, Ben-Ari Y, Gaiarsa JL (2005) Endogenous neurotrophins are required for the induction of GABAergic long-term potentiation in the neonatal rat hippocampus. J Neurosci 25:5796-5802 (Pubitemid 40847892)
15. 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 (Pubitemid 13057257)
16. 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 (Pubitemid 16065580)
17. Hardingham N, Glazewski S, Pakhotin P, Mizuno K, Chapman PF, Giese KP, Fox K (2003) Neocortical long-term potentiation and experience-dependent synaptic plasticity require alpha-calcium/calmodulin-dependent protein kinase II autophosphorylation. J Neurosci 23:4428-4436 (Pubitemid 36706173)
18. Hudmon A, Schulman H (2002a) Neuronal CA2 +/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu Rev Biochem 71:473-510 (Pubitemid 34800228)
19. Hudmon A, Schulman H (2002b) Structure-function of the multi-functional Ca2 +/calmodulin-dependent protein kinase II. Biochem J 364:593-611 (Pubitemid 34680833)
20. Impey S, Mark M, Villacres EC, Poser S, Chavkin C, Storm DR (1996) Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16:973-982
21. Keller KA, Chu Y, Grider A, Coffield JA (2000) Supplementation with L-histidine during dietary zinc repletion improves short-term memory in zinc-restricted young adult male rats. J Nutr 130:1633-1640 (Pubitemid 30340715)
22. Kida S, Josselyn SA, de Ortiz SP, Kogan JH, Chevere I, Masushige S, Silva AJ (2002) CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348-355 (Pubitemid 34279815)
23. Lengyel I, Fieuw-Makaroff S, Hall AL, Sim AT, Rostas JA, Dunkley PR (2000) Modulation of the phosphorylation and activity of calcium/calmodulin- dependent protein kinase II by zinc. J Neurochem 75:594-605 (Pubitemid 30485440)
24. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190 (Pubitemid 135706588)
25. Liu J, Jiang YG, Huang CY, Fang HY, Fang HT, Pang W (2008) Depletion of intracellular zinc down-regulates expression of Uch-L1 mRNA and protein, and CREB mRNA in cultured hippocampal neurons. Nutr Neurosci 11:96-102
26. Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605-623 (Pubitemid 35229980)
27. Lu YM, Taverna FA, Tu R, Ackerley CA, Wang YT, Roder J (2000) Endogenous Zn(2+) is required for the induction of long-term potentiation at rat hippocampal mossy fiber-CA3 synapses. Synapse 38:187-197
28. Marie H, Morishita W, Yu X, Calakos N, Malenka RC (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741-752 (Pubitemid 40320708)
29. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER (1997) Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927-938 (Pubitemid 28028772)
30. Matynia A, Kushner SA, Silva AJ (2002) Genetic approaches to molecular and cellular cognition: a focus on LTP and learning and memory. Annu Rev Genet 36:687-720 (Pubitemid 36109202)
31. Mayford M, Bach ME, Kandel E (1996) CaMKII function in the nervous system explored from a genetic perspective. Cold Spring Harb Symp Quant Biol 61:219-224 (Pubitemid 27257970)
32. Meyer TE, Habener JF (1993) Cyclic adenosine 3′,5′- monophosphate response element binding protein (CREB) and related transcription-activating deoxyribonucleic acid-binding proteins. Endocr Rev 14:269-290 (Pubitemid 23168051)
33. Miller S, Yasuda M, Coats JK, Jones Y, Martone ME, Mayford M (2002) Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36:507-519 (Pubitemid 35291097)
34. Miyamoto E (2006) Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J Pharmacol Sci 100:433-442
35. Miyamoto E, Fukunaga K (1996) A role of Ca2+/calmodulin-dependent protein kinase II in the induction of long-term potentiation in hippocampal CA1 area. Neurosci Res 24:117-122
36. Mizuno M, Yamada K, Maekawa N, Saito K, Seishima M, Nabeshima T (2002) CREB phosphorylation as a molecular marker of memory processing in the hippocampus for spatial learning. Behav Brain Res 133:135-141 (Pubitemid 34754389)
37. Montminy MR, Gonzalez GA, Yamamoto KK (1990) Regulation of cAMP-inducible genes by CREB. Trends Neurosci 13:184-188 (Pubitemid 20145139)
38. 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 (Pubitemid 26419073)
39. Qing H, He G, Ly PT, Fox CJ, Staufenbiel M, Cai F, Zhang Z, Wei S, Sun X, Chen CH, Zhou W, Wang K, Song W (2008) Valproic acid inhibits Abeta production, neuritic plaque formation, and behavioral deficits in Alzheimer's disease mouse models. J Exp Med 205:2781-2789
40. Sensi SL, Canzoniero LM, Yu SP, Ying HS, Koh JY, Kerchner GA, Choi DW (1997) Measurement of intracellular free zinc in living cortical neurons: routes of entry. J Neurosci 17:9554-9564 (Pubitemid 28006399)
41. Shaywitz AJ, Greenberg ME (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68:821-861 (Pubitemid 29449210)
42. Sheng M, Thompson MA, Greenberg ME (1991) CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252:1427-1430 (Pubitemid 21917061)
43. Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127-148 (Pubitemid 28150661)
44. Smart TG, Hosie AM, Miller PS (2004) Zn2+ ions: modulators of excitatory and inhibitory synaptic activity. Neuroscientist 10:432-442 (Pubitemid 39244580)
45. Takeda A (2000) Movement of zinc and its functional significance in the brain. Brain Res Brain Res Rev 34:137-148
46. 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 (Pubitemid 30136108)
47. 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 (Pubitemid 38049393)
48. Takeda A, Fuke S, Minami A, Oku N (2007) Role of zinc influx via AMPA/kainate receptor activation in metabotropic glutamate receptor-mediated calcium release. J Neurosci Res 85:1310-1317 (Pubitemid 46724374)
49. Takeda A, Kanno S, Sakurada N, Ando M, Oku N (2008a) Attenuation of hippocampal mossy fiber long-term potentiation by low micromolar concentrations of zinc. J Neurosci Res 86:2906-2911
50. Takeda A, YamadaK, Tamano H, Fuke S, Kawamura M, Oku N (2008b) Hippocampal calcium dyshomeostasis and long-term potentiation in 2-week zinc deficiency. Neurochem Int 52:241-246 (Pubitemid 350235696)
51. Tropea TF, Kosofsky BE, Rajadhyaksha AM (2008) Enhanced CREB and DARPP-32 phosphorylation in the nucleus accumbens and CREB, ERK, and GluR1 phosphorylation in the dorsal hippocampus is associated with cocaine-conditioned place preference behavior. J Neurochem 106:1780-1790
52. Vallee BL, Falchuk KH (1993) The biochemical basis of zinc physiology. Physiol Rev 73:79-118 (Pubitemid 23065434)
53. Wayman GA, Lee YS, Tokumitsu H, Silva A, Soderling TR (2008) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59:914-931
54. Weiss JH, Koh JY, Christine CW, Choi DW (1989) Zinc and LTP. Nature 338:212
55. Worgotter F, Porr B (2005) Temporal sequence learning, prediction, and control: a review of different models and their relation to biological mechanisms. Neural Comput 17:245-319 (Pubitemid 40190477)
56. Xu H, Gao HL, Zheng W, Xin N, Chi ZH, Bai SL, Wang ZY (2010) Lactational zinc deficiency-induced hippocampal neuronal apoptosis by a BDNF-independent TrkB signaling pathway. Hippocampus. doi: 10.1002/hipo.20767