Zinc transporter ZnT3 is involved in memory dependent on the hippocampus and perirhinal cortex

Behavioural Brain Research

Volumn 223, Issue 1, 2011, Pages 233-238

  Martel, Guillaume ^a   Hevi, Charles ^a   Kane Goldsmith, Noriko ^b   Shumyatsky, Gleb P ^a  

^a RUTGERS UNIVERSITY   (United States)

^b WM Keck Center for Collaborative Neuroscience   (United States)

Author keywords

Hippocampus; Object recognition; Perirhinal cortex; Social recognition; Spatial memory

Indexed keywords

ZINC TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING; MAZE TEST; MOUSE; MOUSE MUTANT; NONHUMAN; PERIRHINAL CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION; RECOGNITION; SOCIAL INTERACTION; SPATIAL MEMORY;

ANIMALS; CARRIER PROTEINS; HIPPOCAMPUS; INTERPERSONAL RELATIONS; MALE; MAZE LEARNING; MEMBRANE PROTEINS; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; TEMPORAL LOBE;

EID: 79958005264     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.04.020     Document Type: Article

References (41)

1. Squire L.R., Zola-Morgan S. Memory: brain systems and behavior. Trends Neurosci 1988, 11:170-175.
2. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 1957, 20:11-21.
3. Squire L.R. The legacy of patient H.M. for neuroscience. Neuron 2009, 61:6-9.
4. Yasuda M., Mayford M.R. CaMKII activation in the entorhinal cortex disrupts previously encoded spatial memory. Neuron 2006, 50:309-318.
5. Palmiter R.D., Cole T.B., Quaife C.J., Findley S.D. ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc Natl Acad Sci USA 1996, 93:14934-14939.
6. Qian J., Noebels J.L. Visualization of transmitter release with zinc fluorescence detection at the mouse hippocampal mossy fibre synapse. J Physiol 2005, 566:747-758.
7. Martel G., Hevi C., Friebely O., Baybutt T., Shumyatsky G.P. Zinc transporter 3 is involved in learned fear and extinction, but not in innate fear. Learn Mem 2010, 17:582-590.
8. Cole T.B., Wenzel H.J., Kafer K.E., Schwartzkroin P.A., Palmiter R.D. Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc Natl Acad Sci USA 1999, 96:1716-1721.
9. Kodirov S.A., Takizawa S., Joseph J., Kandel E.R., Shumyatsky G.P., Bolshakov V.Y. Synaptically released zinc gates long-term potentiation in fear conditioning pathways. Proc Natl Acad Sci USA 2006, 103:15218-15223.
10. Vogt K., Mellor J., Tong G., Nicoll R. The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 2000, 26:187-196.
11. Ruiz A., Walker M.C., Fabian-Fine R., Kullmann D.M. Endogenous zinc inhibits GABA(A) receptors in a hippocampal pathway. J Neurophysiol 2004, 91:1091-1096.
12. Mott D.D., Benveniste M., Dingledine R.J. pH-dependent inhibition of kainate receptors by zinc. J Neurosci 2008, 28:1659-1671.
13. Hirzel K., Muller U., Latal A.T., Hulsmann S., Grudzinska J., Seeliger M.W., et al. Hyperekplexia phenotype of glycine receptor alpha1 subunit mutant mice identifies Zn(2+) as an essential endogenous modulator of glycinergic neurotransmission. Neuron 2006, 52:679-690.
14. Deshpande A., Kawai H., Metherate R., Glabe C.G., Busciglio J. A role for synaptic zinc in activity-dependent Abeta oligomer formation and accumulation at excitatory synapses. J Neurosci 2009, 29:4004-4015.
15. Frederickson C.J., Hernandez M.D., McGinty J.F. Translocation of zinc may contribute to seizure-induced death of neurons. Brain Res 1989, 480:317-321.
16. Huang Y.Z., Pan E., Xiong Z.Q., McNamara J.O. Zinc-mediated transactivation of TrkB potentiates the hippocampal mossy fiber-CA3 pyramid synapse. Neuron 2008, 57:546-558.
17. Izumi Y., Auberson Y.P., Zorumski C.F. Zinc modulates bidirectional hippocampal plasticity by effects on NMDA receptors. J Neurosci 2006, 26:7181-7188.
18. Otto C., Kovalchuk Y., Wolfer D.P., Gass P., Martin M., Zuschratter W., et al. Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. J Neurosci 2001, 21:5520-5527.
19. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
20. Shumyatsky G.P., Tsvetkov E., Malleret G., Vronskaya S., Hatton M., Hampton L., et al. Identification of a signaling network in lateral nucleus of amygdala important for inhibiting memory specifically related to learned fear. Cell 2002, 111:905-918.
21. Cole T.B., Martyanova A., Palmiter R.D. Removing zinc from synaptic vesicles does not impair spatial learning, memory, or sensorimotor functions in the mouse. Brain Res 2001, 891:253-265.
22. Albasser M.M., Davies M., Futter J.E., Aggleton J.P. Magnitude of the object recognition deficit associated with perirhinal cortex damage in rats: effects of varying the lesion extent and the duration of the sample period. Behav Neurosci 2009, 123:115-124.
23. Adlard P.A., Parncutt J.M., Finkelstein D.I., Bush A.I. Cognitive loss in zinc transporter-3 knock-out mice: a phenocopy for the synaptic and memory deficits of Alzheimer's disease?. J Neurosci 2010, 30:1631-1636.
24. Bohbot V.D., Corkin S. Posterior parahippocampal place learning in H.M. Hippocampus 2007, 17:863-872.
25. Bohbot V.D., Kalina M., Stepankova K., Spackova N., Petrides M., Nadel L. Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia 1998, 36:1217-1238.
26. Sindreu C., Palmiter R.D., Storm D.R. Zinc transporter ZnT-3 regulates presynaptic Erk1/2 signaling and hippocampus-dependent memory. Proc Natl Acad Sci USA 2011, 108:3366-3370.
27. Suh S.W., Won S.J., Hamby A.M., Yoo B.H., Fan Y., Sheline C.T., et al. Decreased brain zinc availability reduces hippocampal neurogenesis in mice and rats. J Cereb Blood Flow Metab 2009, 29:1579-1588.
28. Phillips R.G., LeDoux J.E. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learn Mem 1994, 1:34-44.
29. Desmedt A., Garcia R., Jaffard R. Differential modulation of changes in hippocampal-septal synaptic excitability by the amygdala as a function of either elemental or contextual fear conditioning in mice. J Neurosci 1998, 18:480-487.
30. Wiltgen B.J., Sanders M.J., Anagnostaras S.G., Sage J.R., Fanselow M.S. Context fear learning in the absence of the hippocampus. J Neurosci 2006, 26:5484-5491.
31. Anagnostaras S.G., Gale G.D., Fanselow M.S. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 2001, 11:8-17.
32. Frankland P.W., Cestari V., Filipkowski R.K., McDonald R.J., Silva A.J. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 1998, 112:863-874.
33. Maren S., Aharonov G., Fanselow M.S. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res 1997, 88:261-274.
34. Bast T., Zhang W.N., Feldon J. Hippocampus and classical fear conditioning. Hippocampus 2001, 11:828-831.
35. Trifilieff P., Herry C., Vanhoutte P., Caboche J., Desmedt A., Riedel G., et al. Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. Learn Mem 2006, 13:349-358.
36. Kogan J.H., Frankland P.W., Silva A.J. Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 2000, 10:47-56.
37. Martel G., Nishi A., Shumyatsky G.P. Stathmin reveals dissociable roles of the basolateral amygdala in parental and social behaviors. Proc Natl Acad Sci USA 2008, 105:14620-14625.
38. Wada E., Watase K., Yamada K., Ogura H., Yamano M., Inomata Y., et al. Generation and characterization of mice lacking gastrin-releasing peptide receptor. Biochem Biophys Res Commun 1997, 239:28-33.
39. Winters B.D., Saksida L.M., Bussey T.J. Implications of animal object memory research for human amnesia. Neuropsychologia 2010, 48:2251-2261.
40. Broadbent N.J., Gaskin S., Squire L.R., Clark R.E. Object recognition memory and the rodent hippocampus. Learn Mem 2010, 17:5-11.
41. Squire L.R., Wixted J.T., Clark R.E. Recognition memory and the medial temporal lobe: a new perspective. Nat Rev Neurosci 2007, 8:872-883.