Inhibition of hippocampal Jun N-terminal kinase enhances short-term memory but blocks long-term memory formation and retrieval of an inhibitory avoidance task

European Journal of Neuroscience

Volumn 17, Issue 4, 2003, Pages 897-902

  Bevilaqua, Lia R M ^a   Kerr, Daniel S ^a   Medina, Jorge H ^b   Izquierdo, Iván ^a   Cammarota, Martín ^a,b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Hippocampus; JNK; Memory; Rat; SP600125

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE 1,9 PYRAZOLOANTHRONE; ENZYME INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; PYRAZOLE DERIVATIVE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; DRUG INFUSION; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; LEARNING; LOCOMOTION; LONG TERM MEMORY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RECALL; SHORT TERM MEMORY; TASK PERFORMANCE;

ANIMALS; ANTHRACENES; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; ENZYME INHIBITORS; ESCAPE REACTION; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; IMMUNOBLOTTING; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEMORY; MEMORY, SHORT-TERM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; MOTOR ACTIVITY; NEURAL INHIBITION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, WISTAR; TIME FACTORS;

EID: 0037294435     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02524.x     Document Type: Article

References (39)

1. Alonso, M., Viola, H., Izquierdo, I. & Medina, J.H. (2002) Aversive experiences are associated with a rapid and transient activation of ERKs in the rat hippocampus. Neurobiol. Learn. Mem., 77, 119-124.
2. Anokhin, K.V. & Rose, S.P. (1991) Learning-induced increase of immediate early gene messenger RNA in the chick forebrain. Eur. J. Neurosci., 3, 162-167.
3. Barros, D.M., Mello e Souza, T., De David, T., Choi, H., Aguzzoli, A., Madche, C., Ardenghi, P., Medina, J.H. & Izquierdo, I. (2001a) Simultaneous modulation of retrieval by dopaminergic D(1), beta-noradrenergic, serotonergic-1A and cholinergic muscarinic receptors in cortical structures of the rat. Behav. Brain Res., 124, 1-7.
4. Barros, D.M., Mello e Souza, T., de Souza, M.M., Choi, H., DeDavid e Silva, T., Lenz, G., Medina, J.H. & Izquierdo, I. (2001b) LY294002, an inhibitor of phosphoinositide 3-kinase given into rat hippocampus impairs acquisition, consolidation and retrieval of memory for one-trial step-down inhibitory avoidance. Behav. Pharmacol., 12, 629-634.
5. Bennett, B.L., Sasaki, D.T., Murray, B.W., O'Leary, E.C., Sakata, S.T., Xu, W., Leisten, J.C., Motiwala, A., Pierce, S., Satoh, Y., Bhagwat, S.S., Manning, A.M. & Anderson, D.W. (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA, 98, 13681-13686.
6. Berman, D.E., Hazvi, S., Rosenblum, K., Seger, R. & Dudai, Y. (1998) Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J. Neurosci., 18, 10037-10044.
7. 2+/ calmodulin-dependent protein kinase II activity and AMPA GluR1 subunit immunoreactivity. Eur. J. Neurosci., 107 2669-2676.
8. Cammarota, M., Bevilaqua, L.R.M., Ardenghi, P., Paratcha, G., Levi de Stein, M., Izquierdo, I. & Medina, J.H. (2000) Learning-associated activation of nuclear MAPK, CREB and Elk-1, along with Fos production, in the rat hippocampus after a one-trial avoidance learning: abolition by NMDA receptor blockade. Brain Res. Mol. Brain Res., 76, 36-46.
9. Chihab, R., Ferry, C., Koziel, V., Monin, P. & Daval, J.L. (1998) Sequential activation of activator protein-1-related transcription factors and JNK protein kinases may contribute to apoptotic death induced by transient hypoxia in developing brain neurons. Brain Res. Mol. Brain Res., 63, 105-120.
10. Curtis, J. & Finkbeiner, S. (1999) Sending signals from the synapse to the nucleus: possible roles for CaMK, Ras/ERK, and SAPK pathways in the regulation of synaptic plasticity and neuronal growth. J. Neurosci. Res., 58, 88-95.
11. Freeman, F.M. & Rose, S.P. (1994) Expression of Fos and Jun proteins following passive avoidance training in the day-old chick. Learn Mem, 6, 389-397.
12. Freeman, F.M. & Rose, S.P. (1995) MK-801 blockade of Fos and Jun expression following passive avoidance training in the chick. Eur. J. Neurosci., 7, 563-569.
13. Gooney, M., Shaw, K., Kelly, A., O'Mara, S.M. & Lynch, M.A. (2002) Longterm potentiation and spatial learning are associated with increased phosphorylation of TrkB and extracellular signal-regulated kinase (ERK) in the dentate gyrus: evidence for a role for brain-derived neurotrophic factor. Behav. Neurosci., 116, 455-463.
14. Holscher, C., McGlinchey, L. & Rowan, M.J. (1996) L-AP4 (L-(+)-2-amino-4-phosphonobutyric acid) induced impairment of spatial learning in the rat is antagonized by MAP4 (S) -2-amino-2-methyl-4-phosphonobutanoic acid). Behav. Brain Res., 81, 69-79.
15. Izquierdo, L.A., Barros, D.M., Ardenghi, P.G., Pereira, P., Rodrigues, C., Choi, H., Medina, J.H. & Izquierdo, I. (2000) Different hippocampal molecular requirements for short- and long-term retrieval of one-trial avoidance learning. Behav. Brain Res., 111, 93-98.
16. Izquierdo, I., Barros, D.M., Mello e Souza, T., de Souza, M.M., Izquierdo, L.A. & Medina, J.H. (1998a) Mechanisms for memory types differ. Nature, 393, 635-636.
17. Izquierdo, L.A., Barros, D.M., Vianna, M.R., Coitinho, A., deDavid e Silva, T., Choi, H., Moletta, B., Medina, J.H. & Izquierdo, I. (2002) Molecular pharmacological dissection of short- and long-term memory. Cell Mol. Neurobiol., 22, 269-287.
18. Izquierdo, I., Izquierdo, L.A., Barros, D.M., Mello e Souza, T., de Souza, M.M., Quevedo, J., Rodrigues, C., Sant'Anna, M.K., Madruga, M. & Medina, J.H. (1998c) Differential involvement of cortical receptor mechanisms in working, short-term and long-term memory, Behav. Pharmacol., 9, 421-427.
19. Izquierdo, I., Medina, J.H., Izquierdo, L.A., Barros, D.M., de Souza, M.M. & Mello e Souza, T. (1998b) Short- and long-term memory are differentially regulated by monoaminergic systems in the rat brain. Neurobiol. Learn. Mem., 69, 219-224.
20. Izquierdo, I., Medina, J.H., Vianna, M.R., Izquìerdo, L.A. & Barros, D.M. (1999) Separate mechanisms for short- and long-term memory. Behav. Brain Res., 103, 1-11.
21. Kelly, A., Lynch, A., Vereker, E., Nolan, Y., Queenan, P., Whittaker, E., O'Neill, L.A. & Lynch, M.A. (2001) The anti-inflammatory cytokine, interleukin (IL) -10, blocks the inhibitory effect of IL-1 beta on long term potentiation. A role for JNK. J. Biol. Chem., 276, 45564-45572.
22. Kim, Y.H., Choi, S.S., Lee, J.K., Won, J.S., Choi, M.R. & Suh, H.W. (2001) Possible roles of JNK pathway in the regulation of hippocampal proenkephalin and immediate early gene expression induced by kainic acid. Mol. Cell, 11, 144-150.
23. Mazzucchelli, C., Vantaggiato, C., Ciamei, A., Fasano, S., Pakhotin, P., Krezel, W., Welzl, H., Wolfer, D.P., Pages, G., Valverde, O., Marowsky, A., Porrazzo, A., Orban, P.C., Maldonado, R., Ehrengruber, M.U., Cestari, V., Lipp, H.P., Chapman, P.F., Pouyssegur, J. & Brambilla, R. (2002) Knockout of ERKI MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron, 34, 807-820.
24. McGaugh, J.L. (1966) Time-dependent processes in memory storage. Science, 153, 1351-1358.
25. Nader, K., Schafe, G.E. & Le Doux, J.E. (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature, 406, 722-726.
26. Paxinos, G. & Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, San Diego, CA, USA.
27. Pellow, S., Chopin, P., File, S. & Briley, M. (1985) Validation of open-closed arms entries in an elevated plus maze as a measure of anxiety in the rats. J. Neurosci. Meth., 14, 149-167.
28. Pozas, E., Ballabriga, J., Planas, A.M. & Ferrer, I. (1997) Kainic acid-induced excitotoxicity is associated with a complex c-Fos and c-Jun response which does not preclude either cell death or survival. J. Neurobiol., 33, 232-246.
29. Sanyal, S., Sandstrom, D.J., Hoeffer, C.A. & Ramaswami, M. (2002) AP-1 functions upstream of CREB to control synaptic plasticity in Drosophila. Nature, 416, 870-874.
30. Sutton, M.A. & Masters SE, Bagnall MW & Carew TJ (2001) Molecular mechanisms underlying a unique intermediate phase of memory in aplysia. Neuron, 31, 143-154.
31. Sweatt, J.D. (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem., 76, 1-10.
32. Szapiro, G., Burros, D.M., Ardenghi, P., Vianna, M.R., Choi, H., Silva, T., Medina, J.H. & Izquierdo, I. (2001) Facilitation and inhibition of retrieval in two aversive tasks in rats by intrahippocampal infusion of agonists of specific glutamate metabotropic receptor subtypes. Psychopharmacology, 156, 397-401.
33. Szapiro, G., Izquierdo, L.A., Alonso, M., Barros, D., Paratcha, G., Ardenghi, P., Pereira, P., Medina, J.H. & Izquierdo, I. (2000) Participation of hippocampal metabotropic glutamate receptors, protein kinase A and mitogen-activated protein kinases in memory retrieval. Neuroscience, 99, 1-5.
34. Tischmeyer, W., Grimm, R., Schicknick, H., Brysch, W. & Schlingensiepen, K.H. (1994) Sequence-specific impairment of learning by c-jun antisense oligonucleotides. Neuroreport, 5, 1501-1504.
35. Vereker, E., O'Donnell, E. & Lynch, M.A. (2000) The inhibitory effect of interleukin-1beta on long-term potentiation is coupled with increased activity of stress-activated protein kinases. J. Neurosci., 20, 6811-6819.
36. Vianna, M.R., Barros, D.M., Silva, T., Choi, H., Madche, C., Rodrigues, C., Medina, J.H. & Izquierdo, I. (2000) Pharmacological demonstration of the differential involvement of protein kinase C isoforms in short- and long-term memory formation and retrieval of one-trial avoidance in rats. Psychopharmacology, 150, 77-84.
37. Vogt, P.K. (2001) Jun, the oncoprotein. Oncogene, 20, 2365-2377.
38. Walz, R., Roesler, R., Barros, D.M., de Souza, M.M., Rodrigues, C., Sant'Anna, M.K., Quevedo, J., Choi, H.K., Nero, W.P., DeDavid e Silva, T.L., Medina, J.H. & Izquierdo, I. (1999) Effects of post-training infusions of a mitogen-activated protein kinase kinase inhibitor into the hippocampus or entorhinal cortex on short- and long-term retention of inhibitory avoidance. Behav. Pharmacol., 10, 723-730.
39. Zhen, X., Du, W., Romano, A.G., Friedman, E. & Harvey, J.A. (2001) The p38 mitogen-activated protein kinase is involved in associative learning in rabbits. J. Neurosci., 21, 5513-5519.