Artículo

La versión final de este artículo es de uso interno de la institución.
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The isoforms of cAMP-dependent protein kinase (PKA) show distinct biochemical properties and subcellular localization, suggesting different physiological functions, and conferring the fine-tuning between the activation of cAMP-PKA cascade and the cellular response. The critical role of PKA in memory and synaptic plasticity has been extensively demonstrated both in vertebrates and invertebrates, but the role of PKA isoforms is a matter of debate. Here we present experimental data showing differential PKA activation profiles after two different experiences: an instance of associative contextual learning (context-signal learning) and a single exposure to a novel context, both in the learning and memory model of the crab Chasmagnathus. Differences were found in the temporal course of activation and in the involvement of PKA isoforms. We found increased PKA activity immediately and 6 h after context-signal training correlating with the critical periods during which pharmacological inhibition of PKA disrupts memory formation. In contrast, PKA activity increased immediately but not 6 h after single exposure to a novel context. The amounts of PKA I and PKA II holoenzymes were analyzed to determine changes in holoenzyme levels and/or differential activation induced by both experiences. Results indicate that context-induced PKA activation is at least in part due to PKA II, and that PKA activation 6 h after context-signal learning coincides with an increase in the total level of PKA I. Considering the higher sensitivity of PKA I to cAMP, its increment can account for the PKA activation found 6 h after training and is proposed as a novel mechanism providing the prolonged PKA activation during memory consolidation. © 2005 Elsevier Inc. All rights reserved.

Registro:

Documento: Artículo
Título:Differential activity profile of cAMP-dependent protein kinase isoforms during long-term memory consolidation in the crab Chasmagnathus
Autor:Locatelli, F.; Romano, A.
Filiación:Lab. de Neurbio. de la Memoria, Depto. Fisiol., Biol. Molec. Y Cel., Pab II, (1428) Buenos Aires, Argentina
Institut für Biologie, Freie Universität Berlin, Neurobiologie, Königin-Luise-Strasse 28/30, D-14195 Berlin, Germany
Palabras clave:cAMP pathway; Crab; Invertebrates; Long-term memory; PKA isoforms; cyclic AMP; holoenzyme; isoprotein; protein kinase; animal experiment; article; crab; enzyme activation; enzyme activity; enzyme inhibition; experience; long term memory; male; memory consolidation; nonhuman; signal transduction; state dependent learning; training
Año:2005
Volumen:83
Número:3
Página de inicio:232
Página de fin:242
DOI: http://dx.doi.org/10.1016/j.nlm.2005.01.002
Título revista:Neurobiology of Learning and Memory
Título revista abreviado:Neurobiol. Learn. Mem.
ISSN:10747427
CODEN:NLMEF
CAS:cyclic AMP, 60-92-4; protein kinase, 9026-43-1
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_10747427_v83_n3_p232_Locatelli

Referencias:

  • Abel, T., Nguyen, P.V., Barad, M., Deuel, T.A., Kandel, E.R., Bourtchouladze, R., Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory (1997) Cell, 88 (5), pp. 615-626
  • Alberini, C.M., Ghirardi, M., Metz, R., Kandel, E.R., C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia (1994) Cell, 76 (6), pp. 1099-1114
  • Beebe, S.J., Corbin, J.D., Cyclic nucleotide-dependent protein kinases (1986) The Enzymes, 17, pp. 43-111. , E. G. Krebs & P. D. Boyer (Eds.) 3rd ed., London: Academic Press
  • Bernabeu, R., Bevilaqua, L., Ardenghi, P., Bromberg, E., Schmitz, P., Bianchin, M., Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats (1997) Proceedings of the National Academy of Sciences of the United States of America, 94 (13), pp. 7041-7046
  • Bourtchouladze, R., Abel, T., Berman, N., Gordon, R., Lapidus, K., Kandel, E.R., Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA (1998) Learning and Memory, 5 (4-5), pp. 365-374
  • Brandon, E.P., Zhuo, M., Huang, Y.Y., Qi, M., Gerhold, K.A., Burton, K.A., Hippocampal long-term depression and depotentiation are defective in mice carrying a targeted disruption of the gene encoding the RI beta subunit of cAMP-dependent protein kinase (1995) Proceedings of the National Academy of Sciences of the United States of America, 92 (19), pp. 8851-8855
  • Cadd, G.G., Uhler, M.D., McKnight, G., Holoenzymes of cAMP-dependent protein kinase containing the neural form of type I regulatory subunit have an increased sensitivity to cyclic nucleotides (1990) Journal of Biological Chemistry, 265 (32), pp. 19502-19506
  • Chain, D.G., Hegde, A.N., Yamamoto, N., Liu-Marsh, B., Schwartz, J.H., Persistent activation of cAMP-dependent protein kinase by regulated proteolysis suggests a neuron-specific function of the ubiquitin system in Aplysia (1995) Journal of Neuroscience, 15 (11), pp. 7592-7603
  • Chew, C.S., Parietal cell protein kinases. Selective activation of type I cAMP-dependent protein kinase by histamine (1985) Journal of Biological Chemistry, 260 (12), pp. 7540-7550
  • Cho-Chung, Y.S., Clair, T., The regulatory subunit of cAMP-dependent protein kinase as a target for chemotherapy of cancer and other cellular dysfunctional-related diseases (1993) Pharmacology and Therapeutics, 60 (2), pp. 265-288
  • Corbin, J.D., Soderling, T.R., Park, C.R., Regulation of adenosine 3′,5′-monophosphate-dependent protein kinase. I. Preliminary characterization of the adipose tissue enzyme in crude extracts (1973) Journal of Biological Chemistry, 248 (5), pp. 1813-1821
  • Fiala, A., Müller, U., Menzel, R., Reversible downregulation of protein kinase a during olfactory learning using antisense technique impairs long-term memory formation in the honeybee, Apis mellifera (1999) Journal of Neuroscience, 19 (22), pp. 10125-10134
  • Foster, J.L., Guttman, J.J., Hall, L.M., Rosen, O.M., Drosophila cAMP-dependent protein kinase (1984) Journal of Biological Chemistry, 259 (21), pp. 13049-13055
  • Freudenthal, R., Romano, A., Participation of Rel/NF-kappaB transcription factors in long-term memory in the crab Chasmagnathus (2000) Brain Research, 855 (2), pp. 274-281
  • Goodwin, S.F., Del Vecchio, M., Velinzon, K., Hogel, C., Russell, S.R., Tully, T., Defective learning in mutants of the Drosophila gene for a regulatory subunit of cAMP-dependent protein kinase (1997) Journal of Neuroscience, 17 (22), pp. 8817-8827
  • Hegde, A.N., Goldberg, A.L., Schwartz, J.H., Regulatory subunits of cAMP-dependent protein kinases are degraded after conjugation to ubiquitin: A molecular mechanism underlying long-term synaptic plasticity (1993) Proceedings of the National Academy of Sciences of the United States of America, 90 (16), pp. 7436-7440
  • Hildebrandt, H., Muller, U., PKA activity in the antennal lobe of honeybees is regulated by chemosensory stimulation in vivo (1995) Brain Research, 679 (2), pp. 281-288
  • Huang, Y.Y., Kandel, E.R., Varshavsky, L., Brandon, E.P., Qi, M., Idzerda, R.L., A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning (1995) Cell, 83 (7), pp. 1211-1222
  • Kandel, E.R., Schwartz, J.H., Molecular biology of learning: Modulation of transmitter release (1982) Science, 218 (4571), pp. 433-443
  • Keely, S.L., Corbin, J.D., Park, C.R., Regulation of adenosine 3:5-monophosphate-dependent protein kinase (1975) Journal of Biological Chemistry, 250 (13), pp. 4832-4840
  • Kemp, B.E., Graves, D.J., Benjamini, E., Krebs, E.G., Role of multiple basic residues in determining the substrate specificity of cyclic AMP-dependent protein kinase (1977) Journal of Biological Chemistry, 252 (14), pp. 4888-4894
  • Locatelli, F., Lafourcade, C., Maldonado, H., Romano, A., Characterisation of cAMP-dependent protein kinase isoforms in the brain of the crab Chasmagnathus (2001) Journal of Comparative Physiology B, 171 (1), pp. 33-40
  • Locatelli, F., Maldonado, H., Romano, A., Two critical periods for cAMP-dependent protein kinase activity during long-term memory consolidation in the crab Chasmagnathus (2002) Neurobiology of Learning and Memory, 77 (2), pp. 234-249
  • Lopez-Salon, M., Alonso, M., Vianna, M.R., Viola, H., Mello Souza, T., Izquierdo, I., The ubiquitin-proteasome cascade is required for mammalian long-term memory formation (2001) European Journal of Neuroscience, 14 (11), pp. 1820-1826
  • Lozada, M., Romano, A., Maldonado, H., Long-term habituation to a danger stimulus in the crab Chasmagnathus granulatus (1990) Physiology and Behaviour, 47 (1), pp. 35-41
  • Maldonado, H., Romano, A., Tomsic, D., Long-term habituation (LTH) in the crab Chasmagnathus: A model for behavioral and mechanistic studies of memory (1997) Brazilian Journal of Medical and Biological Research, 30 (7), pp. 813-826
  • Müller, U., Spatz, H.C., Ca2+-dependent proteolytic modification of the cAMP-dependent protein kinase in Drosophila wild-type and dunce memory mutants (1989) Journal of Neurogenetics, 6, pp. 95-114
  • Müller, U., Neuronal cAMP-dependent protein kinase type II is concentrated in mushroom bodies of Drosophila melanogaster and the honeybee Apis mellifera (1997) Journal of Neurobiology, 33 (1), pp. 33-44
  • Müller, U., Carew, T.J., Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons (1998) Neuron, 21 (6), pp. 1423-1434
  • Müller, U., Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees (2000) Neuron, 27 (1), pp. 159-168
  • Palmer, W.K., McPherson, J.M., Walsh, D.A., Critical controls in the evaluation of cAMP-dependent protein kinase activity ratios as indices of hormonal action (1980) Journal of Biological Chemistry, 255 (7), pp. 2663-2666
  • Pedreira, M.E., Dimant, B., Tomsic, D., Quesada-Allue, L.A., Maldonado, H., Cycloheximide inhibits context memory and long-term habituation in the crab Chasmagnathus (1995) Pharmacology, Biochemistry and Behaviour, 52 (2), pp. 385-395
  • Pedreira, M.E., Dimant, B., Maldonado, H., Inhibitors of protein and RNA synthesis block context memory and long term habituation in the crab Chasmagnathus (1996) Pharmacology, Biochemistry and Behavior, 54, pp. 611-617
  • Rangel-Aldao, R., Rosen, O.M., Dissociation and reassociation of the phosphorylated and nonphosphorylated forms of adenosine 3′:5′-monophosphate-dependent protein kinase from bovine cardiac muscle (1976) Journal of Biological Chemistry, 251 (11), pp. 3375-3380
  • Roberson, E.D., Sweatt, J.D., Transient activation of cyclic AMP-dependent protein kinase during hippocampal long-term potentiation (1996) Journal of Biological Chemistry, 271 (48), pp. 30436-30441
  • Romano, A., Lozada, M., Maldonado, H., Effect of naloxone pretreatment on habituation in the crab Chasmagnathus granulatus (1990) Behavioral and Neural Biology, 53 (1), pp. 113-122
  • Romano, A., Delorenzi, A., Pedreira, M.E., Tomsic, D., Maldonado, H., Acute administration of a permeant analog of cAMP and a phosphodiesterase inhibitor improve long-term habituation in the crab Chasmagnathus (1996) Behavioral Brain Research, 75 (1-2), pp. 119-125
  • Romano, A., Locatelli, F., Delorenzi, A., Pedreira, M.E., Maldonado, H., Effects of activation and inhibition of cAMP-dependent protein kinase on long-term habituation in the crab Chasmagnathus (1996) Brain Research, 735 (1), pp. 131-140
  • Rosen, O.M., Erlichman, J., Reversible autophosphorylation of a cyclic 3′:5′-AMP- dependent protein kinase from bovine cardiac muscle (1975) Journal of Biological Chemistry, 250 (19), pp. 7788-7794
  • Skålhegg, B.S., Tasken, K., Specificity in the cAMP/PKA signalling pathway. Differential expression, regulation, and subcellular localization of subunits of PKA (2000) Frontiers in Bioscience, 5, pp. 678-D693
  • Skoulakis, E.M., Kalderon, D., Davis, R.L., Preferential expression in mushroom bodies of the catalytic subunit of protein kinase a and its role in learning and memory (1993) Neuron, 11 (2), pp. 197-208
  • Taylor, S.S., Bubis, J., Toner-Webb, J., Saraswat, L.D., First, E.A., Buechler, J.A., CAMP-dependent protein kinase: Prototype for a family of enzymes (1988) FASEB Journal, 2 (11), pp. 2677-2685
  • Tomsic, D., Romano, A., Maldonado, H., Behavioral and mechanistic bases of long-term habituation in the crab Chasmagnathus (1998) Advances in Experimental Medicine and Biology, 446, pp. 17-35
  • Vianna, M.R., Alonso, M., Viola, H., Quevedo, J., De Paris, F., Furman, M., Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat (2000) Learning and Memory, 7 (5), pp. 333-340
  • Walsh, D.A., Ashby, C.D., Gonzalez, C., Calkins, D., Fischer, E.H., Krebs, E.G., Purification and characterization of a protein inhibitor of adenosine 3′,5′-monophosphate-dependent protein kinases (1971) Journal of Biological Chemistry, 246 (7), pp. 1977-1985
  • Woo, N.H., Duffy, S.N., Abel, T., Nguyen, P.V., Genetic and pharmacological demonstration of differential recruitment of cAMP-dependent protein kinases by synaptic activity (2000) Journal of Neurophysiology, 84 (6), pp. 2739-2745
  • Zhao, W.Q., Polya, G.M., Wang, B.H., Gibbs, M.E., Sedman, G.L., Ng, K.T., Inhibitors of cAMP-dependent protein kinase impair long-term memory formation in one day-old chicks (1995) Neurobiology of Learning and Memory, 64 (2), pp. 106-118

Citas:

---------- APA ----------
Locatelli, F. & Romano, A. (2005) . Differential activity profile of cAMP-dependent protein kinase isoforms during long-term memory consolidation in the crab Chasmagnathus. Neurobiology of Learning and Memory, 83(3), 232-242.
http://dx.doi.org/10.1016/j.nlm.2005.01.002
---------- CHICAGO ----------
Locatelli, F., Romano, A. "Differential activity profile of cAMP-dependent protein kinase isoforms during long-term memory consolidation in the crab Chasmagnathus" . Neurobiology of Learning and Memory 83, no. 3 (2005) : 232-242.
http://dx.doi.org/10.1016/j.nlm.2005.01.002
---------- MLA ----------
Locatelli, F., Romano, A. "Differential activity profile of cAMP-dependent protein kinase isoforms during long-term memory consolidation in the crab Chasmagnathus" . Neurobiology of Learning and Memory, vol. 83, no. 3, 2005, pp. 232-242.
http://dx.doi.org/10.1016/j.nlm.2005.01.002
---------- VANCOUVER ----------
Locatelli, F., Romano, A. Differential activity profile of cAMP-dependent protein kinase isoforms during long-term memory consolidation in the crab Chasmagnathus. Neurobiol. Learn. Mem. 2005;83(3):232-242.
http://dx.doi.org/10.1016/j.nlm.2005.01.002