Sildenafil, a selective phosphodiesterase type 5 inhibitor, enhances memory reconsolidation of an inhibitory avoidance task in mice

Behavioural Brain Research

Volumn 220, Issue 2, 2011, Pages 319-324

  Boccia, M M ^a   Blake, M G ^a   Krawczyk, M C ^a   Baratti, C M ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Inhibitory avoidance; Memory; Mice; NO cGMP PKG pathway; Reconsolidation; Sildenafil

Indexed keywords

SILDENAFIL;

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG EFFICACY; DRUG MECHANISM; EPISODIC MEMORY; FEMALE; MALE; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYSTEMIC THERAPY; TASK PERFORMANCE;

AGE FACTORS; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROSHOCK; FEMALE; MALE; MEMORY; MICE; PHOSPHODIESTERASE 5 INHIBITORS; PIPERAZINES; PURINES; RETENTION (PSYCHOLOGY); STATISTICS, NONPARAMETRIC; SULFONES; TIME FACTORS;

EID: 79953278687     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.02.016     Document Type: Article

References (66)

1. Essayan D.M. Cyclic nucleotic phosphodiesterases. J Allergy Clin Immunol 2001, 108:671-680.
2. Bender A.T., Beavo J.A. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 2006, 58:488-520.
3. Puzzo D., Sapienza S., Arancio O., Palmeri A. Role of phosphodiesterase 5 in synaptic plasticity and memory. Neuropsychiatry Dis Treat 2008, 4:371-387.
4. Reneerkens O.A., Rutten K., Steinbusch H.W., Blokland A., Prickaerts J. Selective phosphodiesterases inhibitors: a promising target for cognition enhancement. Psychopharmacology 2009, 202:419-443.
5. Giordano D., De Stefano M.E., Citro G., Modica A., Giorgi M. Expression of cGMP-binding cGMP-specific phosphodiesterase (PDE5) in mouse tissues and cell lines using and antibody against the enzyme-terminal domain. Biochim Biophys Acta 2001, 1539:16-27.
6. Yanaka N., Kotera J., Ohtsuka A., Akatsuka H., Imai Y., Michibata H., et al. Expression, structure and chromosomal localization of the human cGMP-binding cGMP-specific phosphodiesterase PDE5A gene. Eur J Biochem 1998, 255:391-399.
7. van Staveren W.C., Steinbusch H.W., Markerink-van Ittersum M., Behrends S., de Vente J. Species differences in the localization of cGMP-producing and NO-responsive elements in the mouse and rat hippocampal using cGMP immunocytochemistry. Eur J Neurosci 2004, 19:2155-2168.
8. Lakics V., Karran E.H., Boess F.G. Quantitative comparison of phoshpdiesterase mRNA distribution in human brain and peripheral tissues. Neuropharmacology 2010, 59:367-374.
9. Murad F., Arnold W.P., Mittal C.K., Braughler J.M. Properties and regulation of guanylate cyclase and some proposed functions for cyclic GMP. Adv Cyclic Nucleotide Res 1979, 11:175-204.
10. Schmidt H.H.H.W., Lohmann S.M., Walter U. The nitric oxide and cGMP signal transduction system: regulation and mechanisms of action. Biochim Biophys Acta 1993, 1178:153-175.
11. Susswein A.J., Katzoff A., Miller N., Hurwitz I. Nitric oxide and memory. Neuroscientist 2004, 10:153-162.
12. Rickard N.S., Ng K.T., Gibbs M.E. Further support for nitric oxide-dependent memory processing in day-old chick. Neurobiol Learn Mem 1998, 69:79-86.
13. Baratti C.M., Kopf S.R. A nitric oxide synthase impairs memory storage in mice. Neurobiol Learn Mem 1996, 65:197-201.
14. Fin C., Cunha C.A., Bromberg E., Schmitz P.K., Bianchin M., Medina J.H., et al. Experiments suggesting a role for nitric oxide in the hippocampus in memory processes. Neurobiol Learn Mem 1995, 63:113-115.
15. Kirchner L., Weitzdoerfer R., Hoeger H., Url A., Schmidt P., Engelmann M., et al. Impaired cognitive performance in neuronal nitric oxide synthase knockout mice is associated with hippocampal protein dearrangements. Nitric Oxide 2004, 11:316-330.
16. Yamada K., Hiramatsu M., Noda Y., Mamiya T., Murai M., Kameyama T., et al. Role of nitric oxide and cyclic GMP in the dizocilpine-induced impairment of spontaneous alternation behavior in mice. Neuroscience 1996, 74:365-374.
17. Bennett B.M., Reynolds J.N., Prusky G.T., Douglas R.M., Sutherland R.J., Thatcher G.R. Cognitive deficits in rats alter forebrain cholinergic depletion are reversed by a NO mimetic nitrate ester. Neuropsychopharmacology 2007, 32:505-513.
18. 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.
19. Baratti C.M., Boccia M.M. Effects of sildenafil on long-term retention of an inhibitory avoidance response in mice. Behav Pharmacol 1999, 10:731-737.
20. Rutten K., De Vente J., Sik A., Markerink-Van Ittersum M., Prickaerts J., Blokland A. The selective PDE5 inhibitor, sildenafil improves object memory in Swiss mice and increases cGMP levels in hippocampal slices. Behav Brain Res 2005, 164:11-16.
21. Prickaerts J., Steinbusch H.W., Smits J.F., de Vente J. Possible role of nitric oxide-cyclic GMP pathway in object recognition memory: effects of 7-nitroindazole and zaprinast. Eur J Pharmacol 1997, 337:125-136.
22. Squire L.R., Alvarez P. Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol 1995, 5:169-177.
23. Baratti C.M., Boccia M.M., Blake M.G. Pharmacological effects and behavioral interventions on memory consolidation and reconsolidation. Braz J Med Biol Res 2009, 42:148-154.
24. Przybyslawski J., Sara S.J. Reconsolidation of memory after its reactivation. Behav Brain Res 1997, 84:241-246.
25. Miller C.A., Sweatt J.D. Amnesia or retrieval deficit? Implications of a molecular approach to the question of reconsolidation. Learn Mem 2006, 13:498-505.
26. Nader K., Einarsson E.O. Memory reconsolidation: an update. Ann N Y Acad Sci 2010, 1191:27-41.
27. Tronson N.C., Taylor J.R. Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci 2007, 8:262-275.
28. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001, 357:593-615.
29. Baratti C.M., Boccia M.M., Blake M.G., Acosta G.B. Reactivated memory of an inhibitory avoidance response in mice is sensitive to a nitric oxide synthase inhibitor. Neurobiol Learn Mem 2008, 89:426-440.
30. Itzhak Y., Anderson K.L. Memory reconsolidation of cocaine-associated context requires nitric oxide signaling. Synapse 2007, 61:1002-1005.
31. Schafe G.E., Bauer E.P., Rosis S., Farb C.R., Rodrigues S.M., Ledoux J.E. Memory consolidation of Pavlovian fear conditioning requires nitric oxide signaling in the lateral amygdala. Eur J Neurosci 2005, 22:201-211.
32. Alberini C.M., Milekic M.H., Tronel S. Mechanisms of memory stabilization and de-stabilization. Cell Mol Life Sci 2006, 63:999-1008.
33. Gold P.E. The use of avoidance training in studies of modulation of memory storage. Behav Neural Biol 1986, 46:87-98.
34. Siegel S. Non-parametric statistics for the behavioral sciences 1956, McGraw-Hill, New York.
35. Rutten K., Basile J.L., Prickaerts J., Blokland A., Vivian J.A. Selective PDE inhibitors rolipram and sildenafil improve object retrieval performance in adult cynomolgus macaques. Psychopharmacology 2008, 196:643-648.
36. Best J.D., Berghmans S., Hunt J.J., Clarke S.C., Fleming A., Goldsmith P., et al. Non-associative learning in larval zebrafish. Neuropsychopharmacology 2008, 33:1206-1215.
37. Schultheiss D., Müller S.V., Nager W., Stief C.G., Schlote N., Jonas U., et al. Central effects of sildenafil (Viagra) on auditory selective attention and verbal recognition memory in humans: a study with event-related brain potentials. World J Urol 2001, 19:46-50.
38. Prickaerts J., Van Staveren W.C.G., Sik A., Markerinik-Van Ittersum M., Niewohner U., Van der Staay F.J., et al. Effects of two selective phosphodiesterase type 5 inhibitors, sildenafil and vardenafil, on object recognition memory and hippocampal cyclic GMP levels in the rat. Neuroscience 2002, 113:351-361.
39. 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. J Neurosci 2009, 29:8075-8086.
40. Boccia M.M., Acosta G.B., Blake M.G., Baratti C.M. Memory consolidation and reconsolidation of an inhibitory avoidance response in mice: effects of i.c.v. injections of hemicholinium-3. Neuroscience 2004, 124:735-741.
41. Bustos S.G., Maldonado H., Molina V.A. Midazolam disrupts fear memory reconsolidation. Neuroscience 2006, 139:831-842.
42. Debiec J., Ledoux J.E. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 2004, 129:267-272.
43. Duvarci S., Nader K. Characterization of fear memory reconsolidation. J Neurosci 2004, 24:9269-9275.
44. Boccia M.M., Blake M.G., Acosta G.B., Baratti C.M. Memory consolidation and reconsolidation of an inhibitory avoidance task in mice. Effects of a new different learning task. Neuroscience 2005, 135:19-29.
45. Gordon W.C., Spear N.E. Effect of reactivation of a previously acquired memory on the interaction between memories in the rat. J Exp Psychol 1974, 99:349-355.
46. Misanin J.R., Miller R.R., Lewis D.J. Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science 1968, 160:554-555.
47. Sara S.J., Hars B. In memory of consolidation. Learn Mem 2006, 13:515-521.
48. Myers K.M., Davis M. Behavioral and neural analysis of extinction. Neuron 2002, 36:567-584.
49. Pedreira M.E., Pérez-Cuesta L.M., Maldonado H. Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction. Learn Mem 2004, 11:579-585.
50. Setter S.M., Iltz J.L., Fincham J.E., Campbell R.K., Baker D.E. Phosphodiesterase 5 inhibitors for erectile dysfunction. Ann Pharmacother 2005, 39:1286-1295.
51. McGaugh J.L. Memory-a century of consolidation. Science 2000, 287:248-251.
52. McGaugh J.L., Roozendaal B. Drug enhancement of memory consolidation: historical perspective and neurobiological implications. Psychopharmacology 2009, 202:3-14.
53. Rutten K., Prickaerts J., Hendrix M., Josef Van der Staay F., Sik A., Blokland A. Time-dependent involvement of cAMP and cGMP in consolidation of object memory: studies using selective phosphodiesterase type 2, 4 and 5 inhibitors. Eur J Pharmacol 2007, 558:107-112.
54. Boccia M.M., Blake M.G., Krawczyk M.C., Baratti C.M. Hippocampal alpha7 nicotinic receptors modulate memory reconsolidation of an inhibitory avoidance task in mice. Neuroscience 2010, 171:531-543.
55. Gordon W.C. Susceptibility of a reactivated memory to the effects of strychnine: a time-dependent phenomenon. Physiol Behav 1977, 18:95-99.
56. Horne C.A., Rodriguez W.A., Wright T.P., Padilla J.L. Time-dependent effects of fructose on the modulation of a reactivated memory. Prog Neuropsychopharmacol Biol Psychiatry 1997, 21:649-658.
57. Rodriguez W.A., Horne C.A., Padilla J.L. Effects of glucose and fructose of recently reactivated and recently acquired memories. Prog Neuropsychopharmacol Biol Psychiatry 1999, 23:1285-1317.
58. Albuquerque E.X., Pereira E.F.R., Alkongdon M., Rogers S.W. Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 2009, 89:73-120.
59. Alberini C.M. Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes?. Trends Neurosci 2005, 28:51-56.
60. Alberini C.M. The role of protein synthesis during the labile phases of memory: revisiting the skepticism. Neurobiol Learn Mem 2008, 89:234-246.
61. Boccia M.M., Blake M.G., Acosta G.B., Baratti C.M. Post-retrieval effects of icv infusions of hemicholinium in mice are dependent on the age of the original memory. Learn Mem 2006, 13:376-381.
62. Milekic M.H., Alberini C.M. Temporally graded requirement for protein synthesis following memory reactivation. Neuron 2002, 36:521-525.
63. Suzuki A., Josselyn S.A., Frankland P.W., Masushige S., Silva A.J., Kida S. Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 2004, 24:4787-4795.
64. Debiec J., LeDoux J.E., Nader K. Cellular and systems reconsolidation in the hippocampus. Neuron 2002, 36:527-538.
65. Izquierdo I. Different forms of post-training memory processing. Behav Neural Biol 1989, 51:171-202.
66. Arnold W.P., Mittal C.K., Katsuki S., Murad F. Nitric oxide activates guanylate cyclase and increases guanosine 3':5'-cyclic monophosphate levels in various tissue preparations. Proc Natl Acad Sci USA 1977, 74:3203-3207.