Hippocampal PKA/CREB pathway is involved in the improvement of memory induced by spermidine in rats

Neurobiology of Learning and Memory

Volumn 96, Issue 2, 2011, Pages 324-332

  Guerra, Gustavo Petri ^a   Mello, Carlos Fernando ^a   Bochi, Guilherme Vargas ^a   Pazini, Andréia Martini ^a   Fachinetto, Roselei ^a   Dutra, Rafael C ^b   Calixto, João Batista ^b   Ferreira, Juliano ^a   Rubin, Maribel Antonello ^a  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

CAMP dependent protein kinase; CREB; Memory; Polyamine; Spermidine

Indexed keywords

ARCAINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; SPERMIDINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN REGION; CONTROLLED STUDY; HIPPOCAMPUS; MEMORY CONSOLIDATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; AVOIDANCE LEARNING; BIGUANIDES; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HIPPOCAMPUS; MEMORY; PHOSPHORYLATION; RATS; SIGNAL TRANSDUCTION; SPERMIDINE;

EID: 79960838425     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2011.06.007     Document Type: Article

References (71)

1. 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. Cell 1997, 88:615-626.
2. Ahi J., Radulovic J., Spiess J. The role of hippocampal signaling cascades in consolidation of fear memory. Behavioural Brain Research 2004, 149:17-31.
3. Barad M., Bourtchouladze R., Winder D.G., Golan H., Kandel E. Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:15020-15025.
4. Berlese D.B., Sauzem P.D., Carati M.C., Guerra G.P., Stiegemeier J.A., Mello C.F., et al. Time-dependent modulation of inhibitory avoidance memory by spermidine in rats. Neurobiology of Learning and Memory 2005, 83:48-53.
5. Bernabeu R., Bevilaqua L., Ardenghi P., Bromberg E., Schmitz P., Bianchin M., et al. Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:7041-7046.
6. Bernabeu R., Cammarota M., Izquierdo I., Medina J.H. Involvement of hippocampal AMPA glutamate receptor changes and the cAMP/protein kinase A/CREB-P signalling pathway in memory consolidation of an avoidance task in rats. Brazilian Journal of Medical and Biological Research 1997, 30:961-965.
7. Bernabeu R., Izquierdo I., Cammarota M., Jerusalinsky D., Medina J.H. Learning-specific, time-dependent increase in [3H]phorbol dibutyrate binding to protein kinase C in selected regions of the rat brain. Brain Research 1995, 685:163-168.
8. Bernabeu R., Schmitz P., Faillace M.P., Izquierdo I., Medina J.H. Hippocampal cGMP and cAMP are differentially involved in memory processing of inhibitory avoidance learning. NeuroReport 1996, 7:585-588.
9. Bernabeu R., Schroder N., Quevedo J., Cammarota M., Izquierdo I., Medina J.H. Further evidence for the involvement of a hippocampal cGMP/cGMP-dependent protein kinase cascade in memory consolidation. NeuroReport 1997, 8:2221-2224.
10. Bevilaqua L., Ardenghi P., Schroder N., Bromberg E., Schmitz P.K., Schaeffer E., et al. 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. Behavioural Pharmacology 1997, 8:331-338.
11. Boundy V.A., Chen J., Nestler E.J. Regulation of cAMP-dependent protein kinase subunit expression in CATH a and SH-SY5Y cells. Journal of Pharmacology and Experimental Therapeutics 1998, 286:1058-1065.
12. 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. Learning and Memory 1998, 5:365-374.
13. Cadd G., McKnight G.S. Distinct patterns of cAMP-dependent protein kinase gene expression in mouse brain. Neuron 1989, 3:71-79.
14. Camera K., Mello C.F., Ceretta A.P., Rubin M.A. Systemic administration of polyaminergic agents modulate fear conditioning in rats. Psychopharmacology (Berl) 2007, 192:457-464.
15. Cammarota M., Bevilaqua L.R., Ardenghi P., Paratcha G., Levi de Stein M., Izquierdo I., et al. 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 Research and Molecular Brain Research 2000, 76:36-46.
16. Carter C. The Neuropharmacology of Polyamines 1994, Academic Press, London.
17. Casu M.A., Sanna A., Spada G.P., Falzoi M., Mongeau R., Pani L. Effects of acute and chronic valproate treatments on p-CREB levels in the rat amygdala and nucleus accumbens. Brain Research 2007, 1141:15-24.
18. Chetkovich D.M., Gray R., Johnston D., Sweatt J.D. N-methyl-D-aspartate receptor activation increases cAMP levels and voltage-gated Ca2+ channel activity in area CA1 of hippocampus. Proceedings of the National Academy of Sciences of the United States of America 1991, 88:6467-6471.
19. Chetkovich D.M., Sweatt J.D. NMDA receptor activation increases cyclic AMP in area CA1 of the hippocampus via calcium/calmodulin stimulation of adenylyl cyclase. Journal of Neurochemistry 1993, 61:1933-1942.
20. Chijiwa T., Mishima A., Hagiwara M., Sano M., Hayashi K., Inoue T., et al. Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. Journal of Biological Chemistry 1990, 265:5267-5272.
21. Dash P.K., Karl K.A., Colicos M.A., Prywes R., Kandel E.R. CAMP response element-binding protein is activated by Ca2+/calmodulin- as well as cAMP-dependent protein kinase. Proceedings of the National Academy of Sciences of the United States of America 1991, 88:5061-5065.
22. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochemical Journal 2000, 351:95-105.
23. Doskeland S.O., Maronde E., Gjertsen B.T. The genetic subtypes of cAMP-dependent protein kinase-functionally different or redundant?. Biochimica et Biophysica Acta 1993, 1178:249-258.
24. Eliot L.S., Dudai Y., Kandel E.R., Abrams T.W. Ca2+/calmodulin sensitivity may be common to all forms of neural adenylate cyclase. Proceedings of the National Academy of Sciences of the United States of America 1989, 86:9564-9568.
25. Gibbs C.S., Knighton D.R., Sowadski J.M., Taylor S.S., Zoller M.J. Systematic mutational analysis of cAMP-dependent protein kinase identifies unregulated catalytic subunits and defines regions important for the recognition of the regulatory subunit. Journal of Biological Chemistry 1992, 267:4806-4814.
26. Giese K.P., Fedorov N.B., Filipkowski R.K., Silva A.J. Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 1998, 279:870-873.
27. Gomes G.M., Mello C.F., da Rosa M.M., Bochi G.V., Ferreira J., Barron S., et al. Polyaminergic agents modulate contextual fear extinction in rats. Neurobiological Learning and Memory 2010, 93:589-595.
28. Gonzalez G.A., Montminy M.R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989, 59:675-680.
29. Guerra G.P., Mello C.F., Sauzem P.D., Berlese D.B., Furian A.F., Tabarelli Z., et al. Nitric oxide is involved in the memory facilitation induced by spermidine in rats. Psychopharmacology (Berl) 2006, 186:150-158.
30. 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. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:7436-7440.
31. Hidaka H., Hagiwara M., Chijiwa T. Molecular pharmacology of protein kinases. Neurochemical Research 1990, 15:431-434.
32. Huang Y.Y., Kandel E.R. Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 1998, 21:169-178.
33. Impey S., Obrietan K., Wong S.T., Poser S., Yano S., Wayman G., et al. Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 1998, 21:869-883.
34. Isiegas C., Park A., Kandel E.R., Abel T., Lattal K.M. Transgenic inhibition of neuronal protein kinase A activity facilitates fear extinction. The Journal of Neuroscience 2006, 26:12700-12707.
35. Izquierdo I., Medina J.H. Memory formation: The sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiological Learning and Memory 1997, 68:285-316.
36. Kishi A., Ohno M., Watanabe S. Concurrent activation of hippocampal glycine and polyamine sites of the N-methyl-D-aspartate receptor synergistically reverses working memory deficits in rats. Neuroscience Letters 1998, 257:131-134.
37. Kishi A., Ohno M., Watanabe S. Spermidine, a polyamine site agonist, attenuates working memory deficits caused by blockade of hippocampal muscarinic receptors and mGluRs in rats. Brain Research 1998, 793:311-314.
38. Liang Z., Liu F., Grundke-Iqbal I., Iqbal K., Gong C.X. Down-regulation of cAMP-dependent protein kinase by over-activated calpain in Alzheimer disease brain. The Journal of Neurochemistry 2007, 103:2462-2470.
39. Liu P., Gupta N., Jing Y., Zhang H. Age-related changes in polyamines in memory-associated brain structures in rats. Neuroscience 2008, 155:789-796.
40. Lopez-Salon M., Alonso M., Vianna M.R., Viola H., Mello e Souza T., Izquierdo I., et al. The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. European Journal of Neuroscience 2001, 14:1820-1826.
41. Mayford M., Abel T., Kandel E.R. Transgenic approaches to cognition. Current Opinion in Neurobiology 1995, 5:141-148.
42. Mayford M., Wang J., Kandel E.R., O'Dell T.J. CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP. Cell 1995, 81:891-904.
43. McKnight G.S., Clegg C.H., Uhler M.D., Chrivia J.C., Cadd G.G., Correll L.A., et al. Analysis of the cAMP-dependent protein kinase system using molecular genetic approaches. Recent Progress in Hormone Research 1988, 44:307-335.
44. Medeiros R., Prediger R.D., Passos G.F., Pandolfo P., Duarte F.S., Franco J.L., et al. Connecting TNF-alpha signaling pathways to iNOS expression in a mouse model of Alzheimer's disease: Relevance for the behavioral and synaptic deficits induced by amyloid beta protein. The Journal of Neuroscience 2007, 27:5394-5404.
45. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1986, Academic Press, Sydney; Orlando. 2nd ed.
46. Pereira P., Ardenghi P., Mello e Souza T., Medina J.H., Izquierdo I. Training in the step-down inhibitory avoidance task time-dependently increases cAMP-dependent protein kinase activity in the entorhinal cortex. Behavioural Pharmacology 2001, 12:217-220.
47. Poser S., Storm D.R. Role of Ca2+-stimulated adenylyl cyclases in LTP and memory formation. International Journal of Developmental Neuroscience 2001, 19:387-394.
48. Puzzo D., Staniszewski A., Deng S.X., Privitera L., Leznik E., Liu S., et al. Phosphodiesterase 5 inhibition improves synaptic function, memory, and amyloid-beta load in an Alzheimer's disease mouse model. The Journal of Neuroscience 2009, 29:8075-8086.
49. Quevedo J., Vianna M.R., Martins M.R., Barichello T., Medina J.H., Roesler R., et al. Protein synthesis, PKA, and MAP kinase are differentially involved in short- and long-term memory in rats. Behavioural Brain Research 2004, 154:339-343.
50. Quevedo J., Vianna M.R., Roesler R., Martins M.R., de-Paris F., Medina J.H., et al. Pretraining but not preexposure to the task apparatus prevents the memory impairment induced by blockade of protein synthesis, PKA or MAP kinase in rats. Neurochemical Research 2005, 30:61-67.
51. Romero-Calvo I., Ocon B., Martinez-Moya P., Suarez M.D., Zarzuelo A., Martinez-Augustin O., et al. Reversible Ponceau staining as a loading control alternative to actin in Western blots. Analytical Biochemistry 2010, 401:318-320.
52. Rubin M.A., Berlese D.B., Stiegemeier J.A., Volkweis M.A., Oliveira D.M., dos Santos T.L., et al. Intra-amygdala administration of polyamines modulates fear conditioning in rats. The Journal of Neuroscience 2004, 24:2328-2334.
53. Rubin M.A., Boemo R.L., Jurach A., Rojas D.B., Zanolla G.R., Obregon A.D., et al. Intrahippocampal spermidine administration improves inhibitory avoidance performance in rats. Behavioural Pharmacology 2000, 11:57-61.
54. Rubin M.A., Jurach A., Zanolla G.R., Boemo R.L., Souza D.O., de Mello C.F. Intrahippocampal GMP administration improves inhibitory avoidance performance through GABAergic and glutamatergic mechanisms in rats. NeuroReport 1997, 8:3713-3716.
55. Rubin M.A., Stiegemeier J.A., Volkweis M.A., Oliveira D.M., Fenili A.C., Boemo R.L., et al. Intra-amygdala spermidine administration improves inhibitory avoidance performance in rats. European Journal of Pharmacology 2001, 423:35-39.
56. Sharifzadeh M., Haghighat A., Tahsili-Fahadan P., Khalaj S., Zarrindast M.R., Zamanian A.R. Intra-hippocampal inhibition of protein kinase AII attenuates morphine-induced conditioned place preference. Pharmacology, Biochemistry and Behavior 2006, 85:705-712.
57. Sharifzadeh M., Sharifzadeh K., Naghdi N., Ghahremani M.H., Roghani A. Posttraining intrahippocampal infusion of a protein kinase AII inhibitor impairs spatial memory retention in rats. The Journal of Neuroscience Research 2005, 79:392-400.
58. Shimada A., Spangler E.L., London E.D., Ingram D.K. Spermidine potentiates dizocilpine-induced impairment of learning performance by rats in a 14-unit T-maze. European Journal of Pharmacology 1994, 263:293-300.
59. Silva A.J., Stevens C.F., Tonegawa S., Wang Y. Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 1992, 257:201-206.
60. Tasken K., Aandahl E.M. Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiological Reviews 2004, 84:137-167.
61. Taylor S.S., Buechler J.A., Yonemoto W. CAMP-dependent protein kinase: Framework for a diverse family of regulatory enzymes. Annual Review of Biochemistry 1990, 59:971-1005.
62. Vianna M.R., Izquierdo L.A., Barros D.M., Ardenghi P., Pereira P., Rodrigues C., et al. Differential role of hippocampal cAMP-dependent protein kinase in short- and long-term memory. Neurochemical Research 2000, 25:621-626.
63. Vitolo O.V., Sant'Angelo A., Costanzo V., Battaglia F., Arancio O., Shelanski M. Amyloid beta -peptide inhibition of the PKA/CREB pathway and long-term potentiation: Reversibility by drugs that enhance cAMP signaling. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:13217-13221.
64. Wallenstein G.V., Vago D.R., Walberer A.M. Time-dependent involvement of PKA/PKC in contextual memory consolidation. Behavioural Brain Research 2002, 133:159-164.
65. Wang H., Ferguson G.D., Pineda V.V., Cundiff P.E., Storm D.R. Overexpression of type-1 adenylyl cyclase in mouse forebrain enhances recognition memory and LTP. Natural Neuroscience 2004, 7:635-642.
66. Wang L.Y., Salter M.W., MacDonald J.F. Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases. Science 1991, 253:1132-1135.
67. Wolfman C., Fin C., Dias M., Bianchin M., Da Silva R.C., Schmitz P.K., et al. Intrahippocampal or intraamygdala infusion of KN62, a specific inhibitor of calcium/calmodulin-dependent protein kinase II, causes retrograde amnesia in the rat. Behavioral and Neural Biology 1994, 61:203-205.
68. Wong S.T., Athos J., Figueroa X.A., Pineda V.V., Schaefer M.L., Chavkin C.C., et al. Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 1999, 23:787-798.
69. Wu Z.L., Thomas S.A., Villacres E.C., Xia Z., Simmons M.L., Chavkin C., et al. Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:220-224.
70. Zhang H.T., Crissman A.M., Dorairaj N.R., Chandler L.J., O'Donnell J.M. Inhibition of cyclic AMP phosphodiesterase (PDE4) reverses memory deficits associated with NMDA receptor antagonism. Neuropsychopharmacology 2000, 23:198-204.
71. Zhang H.T., Zhao Y., Huang Y., Dorairaj N.R., Chandler L.J., O'Donnell J.M. Inhibition of the phosphodiesterase 4 (PDE4) enzyme reverses memory deficits produced by infusion of the MEK inhibitor U0126 into the CA1 subregion of the rat hippocampus. Neuropsychopharmacology 2004, 29:1432-1439.