Improved long-term memory via enhancing cGMP-PKG signaling requires cAMP-PKA signaling

Neuropsychopharmacology

Volumn 39, Issue 11, 2014, Pages 2497-2505

  Bollen, Eva ^a,d   Puzzo, Daniela ^b   Rutten, Kris ^a,e   Privitera, Lucia ^b   De Vry, Jochen ^a   Vanmierlo, Tim ^a,f   Kenis, Gunter ^a   Palmeri, Agostino ^b   D'Hooge, Rudi ^c   Balschun, Detlef ^c   Steinbusch, Harry M W ^a   Blokland, Arjan ^a   Prickaerts, Jos ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF CATANIA   (Italy)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d INSTITUTE OF PHARMACOLOGY   (Poland)

^e GRÜNENTHAL GMBH   (Germany)

^f HASSELT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 2; PHOSPHODIESTERASE IV; PHOSPHODIESTERASE V;

ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; HIPPOCAMPAL CA1 REGION; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; METABOLISM; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; RECOGNITION; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUE; WISTAR RAT;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 2; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; LONG-TERM POTENTIATION; MALE; MEMORY, LONG-TERM; MICE, INBRED C57BL; NEUROPSYCHOLOGICAL TESTS; RATS, WISTAR; RECOGNITION (PSYCHOLOGY); SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES;

EID: 84930899312     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2014.106     Document Type: Article

References (43)

1. Akkerman S, Blokland A, Reneerkens O, van Goethem NP, Bollen E, Gijselaers HJ et al (2012). Object recognition testing: methodological considerations on exploration and discrimination measures. Behav Brain Res 232: 335-347.
2. Bach ME, Barad M, Son H, Zhuo M, Lu YF, Shih R et al (1999). Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc Natl Acad Sci USA 96: 5280-5285.
3. Barad M, Bourtchouladze R, Winder DG, Golan H, Kandel E (1998). Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci USA 95: 15020-15025.
4. Bernabeu R, Schmitz P, Faillace MP, Izquierdo I, Medina JH (1996). Hippocampal cGMP and cAMP are differentially involved in memory processing of inhibitory avoidance learning. Neuroreport 7: 585-588.
5. Blokland A, Schreiber R, Prickaerts J (2006). Improving memory: a role for phosphodiesterases. Curr Pharm Des 12: 2511-2523.
6. Boess FG, Hendrix M, van der Staay FJ, Erb C, Schreiber R, van Staveren W et al (2004). Inhibition of phosphodiesterase 2 increases neuronal cGMP, synaptic plasticity and memory performance. Neuropharmacology 47: 1081-1092.
7. Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER (1998). Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem 5: 365-374.
8. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M et al (1999). Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2: 271-276.
9. Devan BD, Pistell PJ, Daffin Jr LW, Nelson CM, Duffy KB, Bowker JL et al (2007). Sildenafil citrate attenuates a complex maze impairment induced by intracerebroventricular infusion of the NOS inhibitor N(omega)-nitro-L-arginine methyl ester. Eur J Pharmacol 563: 134-140.
10. Ennaceur A, Delacour J (1988). A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 31: 47-59.
11. Frey U, Huang YY, Kandel ER (1993). Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260: 1661-1664.
12. Izquierdo I, Bevilaqua LR, Rossato JI, Bonini JS, Medina JH, Cammarota M (2006). Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci 29: 496-505.
13. Izquierdo I, Medina JH (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.
14. Kandel ER (2001). The molecular biology of memory storage: a dialogue between genes and synapses. Science 294: 1030-1038.
15. Krause W, Kuhne G (1988). Pharmacokinetics of rolipram in the rhesus and cynomolgus monkeys, the rat and the rabbit. Studies on species differences. Xenobiotica 18: 561-571.
16. Kroker KS, Rast G, Giovannini R, Marti A, Dorner-Ciossek C, Rosenbrock H (2012). Inhibition of acetylcholinesterase and phosphodiesterase-9A has differential effects on hippocampal early and late LTP. Neuropharmacology 62: 1964-1974.
17. Lu YF, Hawkins RD (2002). Ryanodine receptors contribute to cGMP-induced late-phase LTP and CREB phosphorylation in the hippocampus. J Neurophysiol 88: 1270-1278.
18. Lu YF, Kandel ER, Hawkins RD (1999). Nitric oxide signaling contributes to late-phase LTP and CREB phosphorylation in the hippocampus. J Neurosci 19: 10250-10261.
19. Matsumoto Y, Unoki S, Aonuma H, Mizunami M (2006). Critical role of nitric oxide-cGMP cascade in the formation of cAMPdependent long-term memory. Learn Mem 13: 35-44.
20. Monti B, Berteotti C, Contestabile A (2006). Subchronic Rolipram Delivery Activates Hippocampal CREB and Arc, Enhances Retention and Slows Down Extinction of Conditioned Fear. Neuropsychopharmacology 31: 278-286.
21. Navakkode S, Sajikumar S, Frey JU (2004). The type IV-specific phosphodiesterase inhibitor rolipram and its effect on hippocampal long-term potentiation and synaptic tagging. J Neurosci 24: 7740-7744.
22. Palmeri A, Privitera L, Giunta S, Loreto C, Puzzo D (2013). Inhibition of phosphodiesterase-5 rescues age-related impairment of synaptic plasticity and memory. Behav Brain Res 240: 11-20.
23. Paterno R, Faraci FM, Heistad DD (1996). Role of Ca(2+)-dependent K+ channels in cerebral vasodilatation induced by increases in cyclic GMP and cyclic AMP in the rat. Stroke 27: 1603-1607; discussion 1607-1608.
24. Paxinos G, Watson C (1998). The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press: London.
25. Prickaerts J, de Vente J, Honig W, Steinbusch HW, Blokland A (2002a). cGMP, but not cAMP, in rat hippocampus is involved in early stages of object memory consolidation. Eur J Pharmacol 436: 83-87.
26. Prickaerts J, Sik A, van Staveren WC, Koopmans G, Steinbusch HW, van der Staay FJ et al (2004). Phosphodiesterase type 5 inhibition improves early memory consolidation of object information. Neurochem Int 45: 915-928.
27. Prickaerts J, Steinbusch HW, Smits JF, de Vente J (1997). Possible role of nitric oxide-cyclic GMP pathway in object recognition memory: effects of 7-nitroindazole and zaprinast. Eur J Pharmacol 337: 125-136.
28. Prickaerts J, van Staveren WC, Sik A, Markerink-van Ittersum M, Niewohner U, van der Staay FJ et al (2002b). Effects of two selective phosphodiesterase type 5 inhibitors, sildenafil and vardenafil, on object recognition memory and hippocampal cyclic GMP levels in the rat. Neuroscience 113: 351-361.
29. Puzzo D, Staniszewski A, Deng SX, Privitera L, Leznik E, Liu S et al (2009). Phosphodiesterase 5 inhibition improves synaptic function, memory, and amyloid-beta load in an Alzheimer's disease mouse model. J Neurosci 29: 8075-8086.
30. Reneerkens O, Rutten K, Blokland A, Prickaerts J (2009). Selective phosphodiesterase inhibitors: a promising target for cognition enhancement. Psychopharmacology 202: 419-443.
31. Reneerkens OA, Rutten K, Akkerman S, Blokland A, Shaffer CL, Menniti FS et al (2012). Phosphodiesterase type 5 (PDE5) inhibition improves object recognition memory: indications for central and peripheral mechanisms. Neurobiol Learn Mem 97: 370-379.
32. Reneerkens OA, Rutten K, Bollen E, Hage T, Blokland A, Steinbusch HW et al (2013). Inhibition of phoshodiesterase type 2 or type 10 reverses object memory deficits induced by scopolamine or MK-801. Behav Brain Res 236: 16-22.
33. Rose GM, Hopper A, De Vivo M, Tehim A (2005). Phosphodiesterase inhibitors for cognitive enhancement. Curr Pharm Design 11: 3329-3334.
34. Rutten K, Lieben C, Smits L, Blokland A (2007a). The PDE4 inhibitor rolipram reverses object memory impairment induced by acute tryptophan depletion in the rat. Psychopharmacology (Berl) 192: 275-282.
35. Rutten K, Prickaerts J, Blokland A (2006). Rolipram reverses scopolamine-induced and time-dependent memory deficits in object recognition by different mechanisms of action. Neurobiol Learn Mem 85: 132-138.
36. Rutten K, Prickaerts J, Hendrix M, van der Staay FJ, Sik A, Blokland A (2007b). 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 558: 107-112.
37. Rutten K, Van Donkelaar EL, Ferrington L, Blokland A, Bollen E, Steinbusch HW et al (2009). Phosphodiesterase inhibitors enhance object memory independent of cerebral blood flow and glucose utilization in rats. Neuropsychopharmacology 34: 1914-1925.
38. Rutten K, Vente JD, Sik A, Ittersum MM, Prickaerts J, Blokland A (2005). The selective PDE5 inhibitor, sildenafil, improves object memory in Swiss mice and increases cGMP levels in hippocampal slices. Behav Brain Res 164: 11-16.
39. Sakamoto K, Karelina K, Obrietan K (2011). CREB: a multifaceted regulator of neuronal plasticity and protection. J Neurochem 116: 1-9.
40. Son H, Lu YF, Zhuo M, Arancio O, Kandel ER, Hawkins RD (1998). The specific role of cGMP in hippocampal LTP. Learn Mem 5: 231-245.
41. Taqatqeh F, Mergia E, Neitz A, Eysel UT, Koesling D, Mittmann T (2009). More than a retrograde messenger: nitric oxide needs two cGMP pathways to induce hippocampal long-term potentiation. J Neurosci 29: 9344-9350.
42. Zakharenko SS, Patterson SL, Dragatsis I, Zeitlin SO, Siegelbaum SA, Kandel ER et al (2003). Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39: 975-990.
43. Zhang HT, Huang Y, Suvarna NU, Deng C, Crissman AM, Hopper AT et al (2005). Effects of the novel PDE4 inhibitors MEM1018 and MEM1091 on memory in the radial-arm maze and inhibitory avoidance tests in rats. Psychopharmacology (Berl) 179: 613-619.