The ubiquitin-proteasome cascade is required for mammalian long-term memory formation

European Journal of Neuroscience

Volumn 14, Issue 11, 2001, Pages 1820-1826

  Lopez Salon, Mariella ^a   Alonso, Mariana ^b   Vianna, Monica R M ^c   Viola, Haydee ^b   Mello e Souza, Tadeu ^c   Izquierdo, Ivan ^c   Pasquini, Juana M ^a   Medina, Jorge H ^b  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

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

Author keywords

cAMP dependent protein kinase; Hippocampus; IkB; Rat; Ubiquitination

Indexed keywords

LACTACYSTIN; PROTEASOME; PROTEASOME INHIBITOR; UBIQUITIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN REGION; CONTROLLED STUDY; HIPPOCAMPUS; LONG TERM MEMORY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; RETROGRADE AMNESIA;

AMNESIA, RETROGRADE; ANIMALS; CYSTEINE ENDOPEPTIDASES; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MEMORY; MULTIENZYME COMPLEXES; NEURONS; PEPTIDE HYDROLASES; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION; UBIQUITIN;

EID: 0035783657     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.0953-816X.2001.01806.x     Document Type: Article

References (43)

1. Abeliovich, A., Paylor, R., Chen, C., Kim, J.J., Wehner, J.M. & Tonegawa, S. (1993) PKC γ-mutant mice exhibit mild deficits in spatial and contextual learning. Cell, 75, 1263-1271.
2. Baldwin, A.S. (1996) The NF-kappa B and I kappa B proteins: New discoveries and insights. Annu. Rev. Immunol., 14, 649-683.
3. Bernabeu, R., Bevilaqua, L., Ardenghi, P., Bromberg, E., Schmitz, P., Bianchin, M., Izquierdo, I. & Medina, J.H. (1997) Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc. Natl. Acad. Sci. USA, 94, 7041-7046.
4. Calabresi, P., Napolitano, M., Centonze, D., Marfia, G.A., Gubellini, P., Teule, M.A., Berretta, N., Bernardi, G., Frati, L., Tolu, M. & Gulino, A. (2000) Tissue plasminogen activator controls multiple forms of synaptic plasticity and memory. Eur. J. Neurosci., 12, 1002-1012.
5. 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. Mol. Brain Res., 76, 36-46.
6. Chain, D.G., Casadio, A., Schacher, S., Hegde, A.H., Valbrun, M., Yamamoto, N., Goldberg, A.L., Bartsch, D., Kandel, E.R. & Schwartz, J.H. (1999) Mechanisms for generating the autonomous cAMP-dependent protein kinase required for long-term facilitation in Aplysia. Neuron, 22, 147-156.
7. Chain, D.G., Hegde, A.N., Yamamoto, N., Liu-Marsh, B. & Schwartz, J.H. (1995) Persistent activation of cAMP-dependent protein kinase by regulated proteolysis suggests a neuron-specific function of the ubiquitin system in Aplysia. J. Neurosci., 15, 7592-7603.
8. Chain, D.G., Schwartz, J.H. & Hegde, A.N. (2000) Ubiquitin-mediated proteolysis in learning and memory. Mol. Neurobiol., 20, 125-142.
9. Davis, H.P. & Squire, L.R. (1984) Protein synthesis and memory: A review. Psychol. Bull., 96, 518-559.
10. Doyle, E., Nolam, P.M., Bele, R. & Regan, C.M. (1992) Intraventricular infusions of antineural cell adhesion molecule in a discrete posttraining period impairs consolidation of a passive avoidance response in the rat. J. Neurochem., 59, 1570-1573.
11. Fenteany, G., Standaert, R.F., Lane, W.S., Choi, S., Corey, E.J. & Schreiber, S.L. (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science, 268, 726-731.
12. Foley, A.G., Hartz, B.P., Gallagher, H.C., Ronn, L.C., Berezin, V., Bock, E. & Regan, C.M. (2000) A synthetic peptide ligand of neural cell adhesion molecule (NCAM) IGI domain prevents NCAM internalization and disrupts passive avoidance learning. J. Neurochem., 74, 2607-2613.
13. Freudenthal, R. & Romano, A. (2000) Participation of Rel/NF-kB transcription factors in long-term memory in the crab Chasmagnathus. Brain Res., 855, 274-281.
14. Grunbaum, L. & Muller, U. (1998) Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J. Neurosci., 18, 4384-4392.
15. Hegde, A.N., Goldberg, A.L. & Schwartz, J.H. (1993) Regulatory subunits of cAMP-dependent protein kinase are degraded after conjugation to ubiquitin: A molecular mechanism underlying long-term synaptic plasticity. Proc. Natl. Acad. Sci. USA, 90, 7436-7440.
16. Hegde, A.N., Inokuchi, K., Pei, W., Casadio, A., Ghirardi, M., Chain, D.G., Martin, K.C., Kandel, E.R. & Schwartz, J.H. (1997) Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell, 89, 115-126.
17. Hershko, A. & Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem., 67, 425-479.
18. Izquierdo, I., Barros, D.M., Izquierdo, L., Mello e Souza, T., Souza, M. & Medina, J.H. (1998) Mechanisms for memory types differ. Nature, 393, 635-636.
19. Izquierdo, I. & McGaugh, J.L. (2000) Behavioural pharmacology and its contribution to the molecular basis of memory consolidation. Behav. Pharmacol., 11, 517-534.
20. Izquierdo, I. & Medina, J.H. (1997) Memory formation: The sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem., 68, 285-316.
21. Jerusalinsky, D., Quillfeldt, J.A., Walz, R., Da Silva, R.C., Medina, J.H. & Izquierdo, I. (1994) Post-training intrahippocampal infusion of protein kinase C inhibitors causes amnesia in rats. Behav. Neural Biol., 61, 107-109.
22. Jiang, Y.-H., Armstrong, D., Albretch, U., Atkins, C.M., Noebels, J.L., Eichele, G., Sweatt, J.D. & Beaudet, A.L. (1998) Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron, 21, 799-811.
23. Lopez-Salon, M., Morelli, L., Castano, E.M., Soto, E.F. & Pasquini, J.M. (2000) Defective ubiquitination of cerebral proteins in Alzheimer's disease. J. Neurosci. Res., 62, 302-310.
24. Lorenzini, C.A., Baldi, E., Bucherelli, C., Sacchetti, B. & Tassoni, G. (1996) Role of dorsal hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response: A tetrodotoxin functional inactivation study. Brain Res., 730, 32-39.
25. Lynch, G. & Baudry, M. (1984) The biochemistry of memory: A new and specific hypothesis. Science, 224, 1057-1063.
26. McGaugh, J.L. (2000) Memory - A century of consolidation. Science, 287, 248-251.
27. Meberg, P.J., Kinney, W.R., Valcourt, E.G. & Routtenberg, A. (1996) Gene expression of the transcription factor NF-kB in hippocampus: Regulation by synaptic activity. Mol. Brain Res., 38, 179-190.
28. Milner, B., Squire, L.R. & Kandel, E.R. (1998) Cognitive neuroscience and the study of memory. Neuron, 20, 445-468.
29. Muller, U. (2000) Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron, 27, 159-168.
30. Muller, U. & Carew, T.J. (1998) Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons. Neuron, 21, 1423-1434.
31. Noguès, X., Micheau, J. & Jaffard, R. (1994) Protein kinase C activity in the hippocampus following spatial learning in mice. Hippocampus, 4, 71-78.
32. O'Neill, L.A.J. & Kaltschmidt, C. (1997) NFk-B: A crucial transcription factor for glial and neuronal cell function. Trends Neurosci., 20, 252-258.
33. Olds, J., Andersson, M., McPhie, D.L., Staten, D. & Alkon, L. (1989) Imaging of memory-specific changes in the distribution of protein kinase C in the hippocampus. Science, 245, 866-869.
34. Paratcha, G., Furman, M., Bevilaqua, L., Cammarota, M., Vianna, M., Levi de Stein, M., Izquierdo, I. & Medina, J.H. (2000) Involvement of hippocampal PKCβI isoform in the early phase of memory formation of an inhibitory avoidance training. Brain Res., 855, 199-205.
35. Paxinos, G. & Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego, CA.
36. Qian, Z., Gilbert, M.E., Colicos, M.A., Kandel, E.R. & Kuhl, D. (1993) Tissue plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature, 136, 453-457.
37. Sheu, F.S., McCabe, B.J., Horn, B. & Routtenberg, A. (1993) Learning selectively increases protein kinase C subtrate phosphorylation in specific regions of the chick brain. Proc. Natl. Acad. Sci. U.S.A., 90, 2705-2709.
38. Smith, L., Chen, L., Reyland, M.E., DeVries, T.A., Talanian, R.V., Omura, S. & Smith, J.B. (2000) Activation of atypical protein kinase C ζ by caspase processing and degradation by ubiquitin-proteasome system. J. Biol. Chem., 275, 40620-40627.
39. Taubenfeld, S.M., Wiig, K.A., Bear, M.F. & Alberini, C.M. (1999) A molecular correlate of memory and amnesia in the hippocampus. Nature Neurosci., 2, 309-310.
40. Thompson, R. (1977) Localisation of a 'passive avoidance memory system' in the white rat. Physiol. Psychol., 6, 263-274.
41. Vianna, M.R.M., Izquierdo, L.A., Barros, D.M., Ardenghi, P., Pereira, P., Rodrigues, C., Moletta, B., Medina, J.H. & Izquierdo, I. (2000) Differential role of hippocampal c-AMP-dependent protein kinase in short- and long-term memory. Neurochem. Res., 25, 621-626.
42. Viola, H., Furman, M., Izquierdo, L.A., Alonso, M., Barros, D., de Souza, M.M., Izquierdo, I. & Medina, J.H. (2000) Phosphorylated cAMP response element-binding protein as a molecular marker of memory processing in rat hippocampus: Effect of novelty. J Neurosci., 20, RC112, 1-5.
43. Winocur, G. & Bindra, D. (1976) Effects of additional cues on passive avoidance learning and extinction in rats with hippocampal lesions. Physiol. Behav., 17, 915-920.