Post-training administration of a synthetic peptide ligand of the neural cell adhesion molecule, C3d, attenuates long-term expression of contextual fear conditioning

Neuroscience

Volumn 122, Issue 1, 2003, Pages 183-191

  Cambon, K ^a,c   Venero, C ^a   Berezin, V ^b   Bock, E ^b   Sandi, C ^a,d  

^a UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c INSTITUT PASTEUR   (France)

^d EPFL   (Switzerland)

Author keywords

Amnesia; Emotional memory; Neural plasticity; Rat

Indexed keywords

COMPLEMENT COMPONENT C3D; LIGAND; MICROTUBULE ASSOCIATED PROTEIN 2; NERVE CELL ADHESION MOLECULE; PEPTIDE; SYNAPTOPHYSIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; EMOTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEAR; LOCOMOTION; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; NERVE FIBER GROWTH; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; TASK PERFORMANCE; TRAINING;

EID: 0142195830     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00597-9     Document Type: Article

References (64)

1. Alexinsky T., Przbyslawski J., Mileusnic R., Rose S.P.R., Sara S.J. Antibody to day-old chick brain glycoprotein induces amnesia in adult rats. Neurobiol Learn Mem. 67:1997;14-20.
2. Arami S., Jucker M., Schachner M., Welzl H. The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behav Brain Res. 81:1996;81-87.
3. Bailey C.H., Chen M., Keller F., Kandel E.R. Serotonin-mediated endocytosis of apNCAM an early step of learning-related synaptic growth in aplysia . Science. 256:1992;645-649.
4. Blanchard R.J., Blanchard D.C. Crouching as an index of fear. J Comp Physiol Psychol. 67:1969;370-375.
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein-dye binding. Anal Biochem. 72:1976;248-254.
6. Cahill L., McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 21:1998;294-299.
7. Cordero M.I., Sandi C. A role for brain glucocorticoid receptors in contextual fear conditioning dependence upon training intensity . Brain Res. 786:1998;11-17.
8. Cordero M.I., Kruyt N.D., Merino J.J., Sandi C. Glucocorticoid involvement on memory formation in a rat model for traumatic memory. Stress. 5:2002;73-79.
9. Cremer H., Chazal G., Carleton A., Goridis C., Vincent J.D., Lledo P.M. Long-term but not short-term plasticity at the mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc Natl Acad Sci USA. 95:1998;242-247.
10. Cremer H., Chazal G., Lledo P.M., Rougon G., Montaron M.F., Mayo W., LeMoal M., Abrous D.N. PSA-NCAM an important regulator of hippocampal plasticity . Int J Dev Neurosci. 18:2000;213-220.
11. Doherty P., Moolenaar C.E., Ashton S.V., Michalides R.J., Walsh F.S. The VASE exon downregulates the neurite growth-promoting activity of NCAM 140. Nature. 356:1992;791-793.
12. Doherty P., Walsh F.S. CAM-FGF receptors interactions a model for axonal growth . Mol Cell Neurosci. 8:1996;99-111.
13. Doyle E., Nolan P.M., Bell R., Regan C.M. Intraventricular infusions of anti-neural cell adhesion molecules in discrete posttraining period impair consolidation of a passive avoidance response in the rat. J Neurochem. 59:1992;1570-1573.
14. Dudai Y. Molecular bases of long-term memories a question of persistence . Curr Opin Neurobiol. 12:2002;211-216.
15. Foley A.G., Hartz B.P., Gallagher H.C., Rønn L.C., Berezin V., Bock E., Regan C.M. A synthetic peptide ligand of neural cell adhesion molecule (NCAM) IgI domain prevents NCAM internalization and disrupts passive avoidance learning. J Neurochem. 74:2000;2607-2613.
16. Friedman M.J., Southwick S.M. Toward pharmacotherapy for post-traumatic stress disorder. Friedman M.J., Charney D.S., Deutch A.Y. Neurobiological and clinical consequences of stress. 1995;151-162 Lippincott-Raven, Philadelphia.
17. Friedman M.J. Current and future drug treatment for posttraumatic stress disorder patients. Psychiatr Ann. 28:1998;461-468.
18. Galea S., Ahern J., Resnick H., Kilpatrick D., Bucuvalas M., Gold J., Vlahov D. Psychological sequelae of the September 11 terrorist attacks in New York City. N Engl J Med. 346:2002;982-987.
19. Gewirtz J.C., McNish K.A., Davis M. Is the hippocampus necessary for contextual fear conditioning? Behav Brain Res. 110:2000;83-95.
20. Goridis C., Brunet J.F. NCAM structural diversity, function and regulation of expression . Semin Cell Biol. 3:1992;189-197.
21. Jensen P.H., Soroka V., Thomsen N.K., Ralets I., Berezin V., Bock E., Poulsen F.M. Structure and interactions of NCAM modules 1 and 2, basic elements in neural cell adhesion. Nat Struct Biol. 6:1999;486-493.
22. Kendler K.S., Thornton L.M., Gardner C.O. Stressful life events and previous episodes in the etiology of major depression in women an evaluation of the 'kindling' hypothesis . Am J Psychiatry. 157:2000;1243-1251.
23. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science. 256:1992;675-677.
24. Kiryushko D, Kofoed T, Skladchikova G, Holm A, Berezin V, Bock E (2003) A synthetic peptide ligand of NCAM, C3d, promotes neuritogenesis and synaptogenesis and modulates presynaptic function in primary cultures of hippocampal neurons. J Biol Chem 278:12325-12334.
25. Kiselyov V.V., Berezin V., Maar T.E., Soroka V., Edvarsen K., Schousboe A. The first immunoglobulin-like neural cell adhesion molecule (NCAM) domain is involved in double-reciprocal interaction with the second immunoglobulin-like NCAm domain and in heparin binding. J Biol Chem. 272:1997;10125-10134.
26. Kiss J.Z., Wang C., Olive S., Rougon G., Lang J., Baetens D., Harry D., Pralong W. Activity-dependent mobilization of the adhesion molecule PSA-NCAM at the cell surface of neurones and endocrine cells. EMBO J. 13:1994;5284-5292.
27. Kiss J.Z., Troncoso E., Djebbara Z., Vutskits L., Muller D. The role of neural cell adhesion molecules in plasticity and repair. Brain Res Rev. 36:2001;175-184.
28. Kolkova K., Novitskaya V., Pedersen N., Berezin V., Bock E. Neural cell adhesion molecule-stimulated neurite outgrowth depends on activation of protein kinase C and the Ras-mitogen-activated protein kinase pathway. J Neurosci. 20:2000;2238-2246.
29. Kristiansen L.V., Marques F.A., Soroka V., Rønn L.C.B., Kiselyov V., Pedersen N., Berezin V., Bock E. Homophilic NCAM interactions interfere with L1 stimulated neurite outgrowth. FEBS Lett. 464:1999;30-34.
30. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci. 23:2000;155-184.
31. Luthi A., Laurent J.P., Figurov A., Muller D., Schachner M. Hippocampal long term potentiation and neural cell adhesion molecules L1 and NCAM. Nature. 372:1994;777-779.
32. Lynch M.A., Voss K.L. Presynaptic changes in long term potentiation elevated synaptosomal calcium concentrations and basal phosphoinositides turnover in dentate gyrus . J Neurochem. 56:1991;113-118.
33. Martin S.J., Grimwood P.D., Morris R.G.M. Synaptic plasticity and memory an evaluation of the hypothesis . Annu Rev Neurosci. 23:2000;649-711.
34. McGaugh J.L., Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol. 12:2002;205-210.
35. Merino J.J., Cordero M.I., Sandi C. Regulation of hippocampal cell adhesion molecules NCAM and L1 by contextual fear conditioning is dependent upon time and stressor intensity. Eur J Neurosci. 12:2000;3283-3290.
36. Mileusnic R., Rose S.P.R., Lancashire C., Bullock S. Characterisation of antibodies specific for chick brain neural cell adhesion molecules which cause amnesia for a passive avoidance task. J Neurochem. 64:1995;2598-2606.
37. Murphy K.J., O'Connell A.W., Regan C.M. Repetitive and transient increases in hippocampal neural cell adhesion molecule polysialylation state following multitrial spatial training. J Neurochem. 67:1996;1268-1274.
38. Murphy K.J., Regan C.M. Contributions of cell adhesion molecules to altered synaptic weightings during memory consolidation. Neurobiol Learn Mem. 70:1998;73-81.
39. O'Connell A.W., Fox G.B., Barry T., Murphy K.J., Fichera G., Foley A.G., Kelly J., Regan C.M. Spatial learning activates neural cell adhesion molecule polysialylation in a cortico-hippocampal pathway within the medial temporal lobe. J Neurochem. 68:1997;2538-2546.
40. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 1986;Academic Press, London.
41. Persohn E., Pollerberg G.E., Schachner M. Immuno-electron microscopic localization of the 180kD component of the neural cell adhesion molecule NCAM in postsynaptic membranes. J Comp Neurol. 288:1989;92-100.
42. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci. 106:1992;274-285.
43. Ramos A., Mormede P. Stress and emotionality a multidimensional and genetic approach . Neurosci Biobehav Rev. 22:1998;33-57.
44. Ranheim T.S., Edelman G.M., Cunningham B.A. Homophilic adhesion mediated by the neural cell adhesion molecule involves multiple immunoglobulin domains. Proc Natl Acad Sci USA. 93:1996;4071-4075.
45. Rao Y., Zhao X., Siu C.H. Mechanisms of homophilic binding mediated by the neural cell adhesion molecule NCAM evidence for isologous interaction . J Biol Chem. 269:1994;27540-27548.
46. Roberts W.W., Dember W.N., Brodwick M. Alternation and exploration in rats with hippocampal lesions. J Comp Neurol. 55:1962;695-700.
47. Rønn L.C.B., Olsen M., Ostergaard S., Kiselyov V., Berezin V., Mortensen M.T., Lerche M.H., Jensen P.H., Soroka V., Saffell J.L., Doherty P., Poulsen F.M., Bock E., Holm A. Identification of a neuritogenic ligand of the neural cell adhesion molecule using a combinatorial library of synthetic peptides. Nat Biotech. 17:1999;1000-1005.
48. Rønn L.C.B., Bock E., Linnemann D., Jahnsen H. NCAM-antibodies modulate induction of long-term potentiation in rat hippocampal CA1. Brain Res. 677:1995;145-151.
49. Rønn L.C.B., Berezin V., Bock E. The neural cell adhesion molecule in synaptic plasticity and ageing. Int J Dev Neurosci. 18:2000;193-199.
50. Rønn L.C.B., Dissing S., Holm A., Berezin V., Bock E. Increased intracellular calcium is required for neurite outgrowth induced by a synthetic peptide ligand of NCAM. FEBS Lett. 518:2002;60-66.
51. Rose S.P.R. Cell adhesion molecules, glucocorticoids and long term memory formation. Trends Neurosci. 18:1995;502-506.
52. Rougon G., Dubois C., Buckley N., Magnani J.L., Zollinger W. A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J Cell Biol. 103:1986;2429-2437.
53. Sacchetti B., Ambrogi Lorenzini C., Baldi E., Bucherelli C., Roberto M., Tassoni G., Brunelli M. Long-lasting hippocampal potentiation and contextual memory consolidation. Eur J Neurosci. 13:2001;2291-2298.
54. Sandi C, Merino JJ, Cordero MI, Kruyt ND, Murphy KJ, Regan CM (2003) Modulation of hippocampal NCAM polysialylation and spatial memory consolidation by fear conditioning. Biol Psychiatry 54: 599-607.
55. Sandi C., Rose S.P.R., Mileusnic R., Lancashire C. Corticosterone facilitates long-term memory formation via enhanced glycoprotein synthesis. Neuroscience. 69:1995;1087-1093.
56. Sandi C., Rose S.P.R. Protein synthesis and fucosylation-dependent mechanisms in corticosterone facilitation of long-term memory in the chick. Behav Neurosci. 111:1997;1098-1104.
57. Sandi C. The role and mechanisms of action of glucocorticoid involvement in memory storage. Neural Plast. 6:1998;41-52.
58. Schachner M. Neural recognition molecules and synaptic plasticity. Curr Opin Cell Biol. 9:1997;627-634.
59. Scholey A.B., Rose S.P.R., Zamani M.R., Bock E., Schachner M. A role for neural cell adhesion molecule in a late consolidation phase of glycoprotein synthesis 6 hours following passive avoidance training of the young chick. Neuroscience. 55:1993;499-509.
60. Schuster T., Krug M., Stalder M., Hackel N., Gerardy-Schahn R., Schachner M. Immunoelectron microscopic localization of the neural recognition molecules L1, NCAM, and its isoform NCAM180, the NCAM-associated polysialic acid, Beta1 integrin and the extracellular matrix molecule Tenascin-R in synapses of the adult rat hippocampus. J Neurobiol. 49:2001;142-158.
61. Solomon Z. The effect of prior stressful experience on coping with war trauma and captivity. Psychol Med. 25:1995;1289-1294.
62. Southwick S.M., Bremner J.D., Rasmusson A., Morgan C.A. III, Arnsten A., Charney D.S. Role of norepinephrine in the pathophysiology and treatment of posttraumatic stress disorder. Biol Psychiatry. 46:1999;1192-1204.
63. Walsh F.S., Furness J., Moore S.E., Ashton S., Doherty P. Use of the neural cell adhesion molecule VASE exon by neurons is associated with a specific down-regulation of neural cell adhesion molecule-dependent neurite outgrowth in the developing cerebellum and hippocampus. J Neurochem. 59:1992;1959-1962.
64. Yehuda R., Antelman S.M. Criteria for rationally evaluating animal models of posttraumatic stress disorder. Biol Psychiatry. 34:1993;479-486.