SNAP-25 in hippocampal CA1 region is involved in memory consolidation

European Journal of Neuroscience

Volumn 20, Issue 6, 2004, Pages 1593-1603

  Hou, Qiuling ^a   Gao, Xiang ^b   Zhang, Xuehan ^a   Kong, Lingwei ^b   Wang, Xinming ^a   Bian, Wei ^b   Tu, Yanyang ^b   Jin, Meilei ^c   Zhao, Guoping ^d   Li, Baoming ^a   Jing, Naihe ^b   Yu, Lei ^e  

^a FUDAN UNIVERSITY   (China)

^b INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^c Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^d CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

^e UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Antisense oligonucleotides; Hippocampus; Long term potentiation; Memory; Rat; SNAP 25

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; SYNAPTOSOMAL ASSOCIATED PROTEIN 25;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEAR; GENE EXPRESSION; GENE INACTIVATION; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; PRESYNAPTIC NERVE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SHORT TERM MEMORY; SIGNAL TRANSDUCTION; SPATIAL MEMORY; TRAINING;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELLS, CULTURED; CONDITIONING, CLASSICAL; ELECTRIC STIMULATION; FEAR; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IN SITU HYBRIDIZATION; INHIBITION (PSYCHOLOGY); LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEMBRANE PROTEINS; MEMORY; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDES, ANTISENSE; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPATIAL BEHAVIOR; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; TIME FACTORS;

EID: 4644249146     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03600.x     Document Type: Article

References (51)

1. Abel, T., Nguyen, P.V., Barad, M., Deuel, T.A., Kandel, E.R. & Bourtchouladze, R. (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell, 88, 615-626.
2. Anagnostaras, S.G., Maren, S. & Fanselow, M.S. (1999) Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J. Neurosci., 19, 1106-1114.
3. 2+-dependent exocytosis. J. Biol. Chem., 271, 20 227-20 230.
4. Bevilaqua, L., Ardenghi, P., Schroder, N., Bromberg, E., Schmitz, P.K., Schaeffer, E., Quevedo, J., Bianchin, M., Walz, R., Medina, J.H. & Izquierdo, I. (1997) Drugs acting upon the cyclic adenosine monophosphate/ protein kinase A signalling pathway modulate memory consolidation when given late after training into rat hippocampus but not amygdala. Behav. Pharmacol., 8, 331-338.
5. Bliss, T.V. & Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31-39.
6. Branks, P.L. & Wilson, M.C. (1986) Patterns of gene expression in the murine brain revealed by in situ hybridization of brain-specific mRNAs. Mol. Brain Res., 1, 1-16.
7. Brewer, G.J. (1997) Isolation and culture of adult rat hippocampal neurons. J. Neurosci. Meth., 71, 143-155.
8. Brewer, G.J. (1999) Regeneration and proliferation of embryonic and adult rat hippocampal neurons in culture. Exp. Neurol., 159, 237-247.
9. Crooke, S.T. (2000) Progress in antisense technology: the end of the beginning. Meth. Enzymol., 313, 3-45.
10. Eichenbaum, H. & Otto, T. (1993) LTP and memory: can we enhance the connection? Trends Neurosci., 16, 163-164.
11. Elgersma, Y. & Silva, A.J. (1999) Molecular mechanisms of synaptic plasticity and memory. Curr. Opin. Neurobiol., 9, 209-213.
12. Geddes, J.W., Hess, E.J., Hart, R.A., Kesslak, J.P., Cotman, C.W. & Wilson, M.C. (1990) Lesions of hippocampal circuitry define synaptosomal- associated protein-25 (SNAP-25) as a novel presynaptic marker. Neuroscience, 38, 515-525.
13. Goosens, K.A. & Maren, S. (2001) Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn. Mem., 8, 148-155.
14. Grosse, G., Grosse, J., Tapp, R., Kuchinke, J., Gorsleben, M., Fetter, I., Hohne-Zell, B., Gratzl, M. & Bergmann, M. (1999) SNAP-25 requirement for dendritic growth of hippocampal neurons. J. Neurosci. Res., 56, 539-546.
15. Guzowski, J.F. & McGaugh, J.L. (1997) Antisense oligodeoxynucleotide- mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc. Natl Acad. Sci. U.S.A., 94, 2693-2698.
16. Heise, G.A. (1984) Behavioral methods for measuring effects of drugs on learning and memory in animals. Med. Res. Rev., 4, 535-558.
17. Huang, Y.Y., Kandel, E.R., Varshavsky, L., Brandon, E.P., Qi, M., Idzerda, R.L., McKnight, G.S. & Bourtchouladze, R. (1995) A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell, 83, 1211-1222.
18. Ikegami, S. & Inokuchi, K. (2000) Antisense DNA against calcineurin facilitates memory in contextual fear conditioning by lowering the threshold for hippocampal long-term potentiation induction. Neuroscience, 98, 637-646.
19. Izquierdo, I., Fin, C., Schmitz, P.K., Da Silva, R.C., Jerusalinsky, D., Quillfeldt, J.A., Ferreira, MB., Medina, J.H. & Bazan, N.G. (1995) Memory enhancement by intrahippocampal, intraamygdala, or intraentorhinal infusion of platelet-activating factor measured in an inhibitory avoidance task. Proc. Natl Acad. Sci. USA, 92, 5047-5051.
20. Izquierdo, I., Barros, D.M., Mello e Souza, T., de Souza, M.M., Izquierdo, L.A. & Medina, J.H. (1998) Mechanisms for memory types differ. Nature, 393, 635-636.
21. Kim, J.J. & Fanselow, M.S. (1992) Modality-specific retrograde amnesia of fear. Science, 256, 675-677.
22. Kim, J.J., Rison, R.A. & Fanselow, M.S. (1993) Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav. Neurosci., 107, 1093-1098.
23. Lan, J.Y., Skeberdis, V.A., Jover, T., Grooms, S.Y., Lin, Y., Araneda, R.C., Zheng, X., Bennett, M.V. & Zukin, R.S. (2001a) Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci., 4, 382-390.
24. Lan, J.Y., Skeberdis, V.A., Jover, T., Zheng, X., Bennett, M.V. & Zukin, R.S. (2001b) Activation of metabotropic glutamate receptor 1 accelerates NMDA receptor trafficking. J. Neurosci., 21, 6058-6068.
25. Logue, S.F., Paylor, R. & Wehner, J.M. (1997) Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task. Behav. Neurosci., 111, 104-113.
26. Low, P., Norlin, T., Risinger, C., Larhammar, D., Pieribone, V.A., Shupliakov, O. & Brodin, L. (1999) Inhibition of neurotransmitter release in the lamprey reticulospinal synapse by antibody-mediated disruption of SNAP-25 function. Eur. J. Cell Biol., 78, 787-793.
27. Maren, S., Aharonov, G. & Fanselow, M.S. (1997) Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav. Brain Res., 88, 261-274.
28. Martin, S.J., Grimwood, P.D. & Morris, R.G. (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci., 23, 649-711.
29. McGaugh, J.L. (2000) Memory - a century of consolidation. Science, 287, 248-251.
30. Mehta, P.P., Battenberg, E. & Wilson, M.C. (1996) SNAP-25 and synaptotagmin involvement in the final Ca(2+)-dependent triggering of neurotransmitter exocytosis. Proc. Natl Acad. Sci. U.S.A., 93, 10 471-10 476.
31. Morris, R.G. (1989) Synaptic plasticity and learning: selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J. Neurosci., 9, 3040-3057.
32. Morris, R.G., Anderson, E., Lynch, G.S. & Baudry, M. (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature, 319, 774-776.
33. Morris, R.G., Garrud, P., Rawlins, J.N. & O'Keefe, J. (1982) Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681-683.
34. Osen-Sand, A., Catsicas, M., Staple, J.K., Jones, K.A., Ayala, G., Knowles, J., Grenningloh, G. & Catsicas, S. (1993) Inhibition of axonal growth by SNAP-25 antisense oligonucleotides in vitro and in vivo. Nature, 364, 445-448.
35. Oyler, G.A., Higgins, G.A., Hart, R.A., Battenberg, E., Billingsley, M., Bloom, F.E. & Wilson, M.C. (1989) The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations. J. Cell Biol., 109, 3039-3052.
36. Oyler, G.A., Polli, J.W., Higgins, G.A., Wilson, M.C. & Billingsley, M.L. (1992) Distribution and expression of SNAP-25 immunoreactivity in rat brain, rat PC-12 cells and human SMS-KCNR neuroblastoma cells. Brain Res. Dev. Brain Res., 65, 133-146.
37. Paxinos, G. & Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego, CA.
38. Phillips, R.G. & LeDoux, J.E. (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci., 106, 274-285.
39. Phillips, R.G. & LeDoux, J.E. (1995) Lesions of the fomix but not the entorhinal or perirhinal cortex interfere with contextual fear conditioning. J. Neurosci., 15, 5308-5315.
40. Roberts, L. A., Morris, B.J. & O'Shaughnessy, C.T. (1998) Involvement of two isoforms of SNAP-25 in the expression of long-term potentiation in the rat hippocampus. Neuroreport, 9, 33-36.
41. Roozendaal, B. & McGaugh, J.L. (1997) Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur. J. Neurosci., 9, 76-83.
42. Roozendaal, B., Nguyen, B.T., Power, A.E. & McGaugh, J.L. (1999) Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc. Natl Acad. Sci. USA, 96, 11 642-11 647.
43. Sandin, J., Georgieva, J., Schott, P.A., Ogren, S.O. & Terenius, L. (1997) Nociceptin/orphanin FQ microinjected into hippocampus impairs spatial learning in rats. Eur. J. Neurosci., 9, 194-197.
44. Sanes, J.R. & Lichtman, J.W. (1999) Can molecules explain long-term potentiation? Nat. Neurosci., 2, 597-604.
45. Selden, N.R., Everitt, B.J., Jarrard, L.E. & Robbins, T.W. (1991) Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience, 42, 335-350.
46. Silva, A.J., Kogan, J.H., Frankland, P.W. & Kida, S. (1998) CREB and memory. Annu. Rev. Neurosci., 21, 127-148.
47. Squire, L.R. & Kandel, E.R. (1999) Memory: From Mind to Molecules. Scientific American Library, New York.
48. Stevens, C.F. (1998) A million dollar question: does LTP = memory? Neuron, 20, 1-2.
49. Sutherland, R.J., Kolb, B. & Whishaw, I.Q. (1982) Spatial mapping: definitive disruption by hippocampal or medial frontal cortical damage in the rat. Neurosci. Lett., 31, 271-276.
50. Tang, Y.P., Wang, H., Feng, R., Kyin, M. & Tsien, J.Z. (2001) Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacology, 41, 779-790.
51. Yang, J., Bian, W., Gao, X., Chen, L. & Jing, N. (2000) Nestin expression during mouse eye and lens development. Mech. Dev., 94, 287-291.