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

E. Bollen, D. Puzzo, K. Rutten, L. Privitera, J. De Vry, T. Vanmierlo, G. Kenis, A. Palmeri, R. D'Hooge, D. Balschun, H.W.M. Steinbusch, A. Blokland, J. Prickaerts

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Abstract

Memory consolidation is defined by the stabilization of a memory trace after acquisition, and consists of numerous molecular cascades that mediate synaptic plasticity. Commonly, a distinction is made between an early and a late consolidation phase, in which early refers to the first hours in which labile synaptic changes occur, whereas late consolidation relates to stable and long-lasting synaptic changes induced by de novo protein synthesis. How these phases are linked at a molecular level is not yet clear. Here we studied the interaction of the cyclic nucleotide-mediated pathways during the different phases of memory consolidation in rodents. In addition, the same pathways were studied in a model of neuronal plasticity, long-term potentiation (LTP). We demonstrated that cGMP/PKG signaling mediates early memory consolidation as well as early-phase-LTP, while cAMP/PKA signaling mediates late consolidation and late-phase-like LTP. Additionally, we show for the first time that early-phase cGMP/PKG-signaling requires late-phase cAMP/PKA-signaling in both LTP and long-term memory formation.Neuropsychopharmacology accepted article preview online, 12 May 2014; doi:10.1038/npp.2014.106.
Original languageEnglish
Pages (from-to)2497-2505
JournalNeuropsychopharmacology
Volume39
Early online date12 May 2014
DOIs
Publication statusPublished - 12 May 2014

Cite this

Bollen, E. ; Puzzo, D. ; Rutten, K. ; Privitera, L. ; De Vry, J. ; Vanmierlo, T. ; Kenis, G. ; Palmeri, A. ; D'Hooge, R. ; Balschun, D. ; Steinbusch, H.W.M. ; Blokland, A. ; Prickaerts, J. / Improved long-term memory via enhancing cGMP-PKG signaling requires cAMP-PKA signaling. In: Neuropsychopharmacology. 2014 ; Vol. 39. pp. 2497-2505.
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abstract = "Memory consolidation is defined by the stabilization of a memory trace after acquisition, and consists of numerous molecular cascades that mediate synaptic plasticity. Commonly, a distinction is made between an early and a late consolidation phase, in which early refers to the first hours in which labile synaptic changes occur, whereas late consolidation relates to stable and long-lasting synaptic changes induced by de novo protein synthesis. How these phases are linked at a molecular level is not yet clear. Here we studied the interaction of the cyclic nucleotide-mediated pathways during the different phases of memory consolidation in rodents. In addition, the same pathways were studied in a model of neuronal plasticity, long-term potentiation (LTP). We demonstrated that cGMP/PKG signaling mediates early memory consolidation as well as early-phase-LTP, while cAMP/PKA signaling mediates late consolidation and late-phase-like LTP. Additionally, we show for the first time that early-phase cGMP/PKG-signaling requires late-phase cAMP/PKA-signaling in both LTP and long-term memory formation.Neuropsychopharmacology accepted article preview online, 12 May 2014; doi:10.1038/npp.2014.106.",
author = "E. Bollen and D. Puzzo and K. Rutten and L. Privitera and {De Vry}, J. and T. Vanmierlo and G. Kenis and A. Palmeri and R. D'Hooge and D. Balschun and H.W.M. Steinbusch and A. Blokland and J. Prickaerts",
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Bollen, E, Puzzo, D, Rutten, K, Privitera, L, De Vry, J, Vanmierlo, T, Kenis, G, Palmeri, A, D'Hooge, R, Balschun, D, Steinbusch, HWM, Blokland, A & Prickaerts, J 2014, 'Improved long-term memory via enhancing cGMP-PKG signaling requires cAMP-PKA signaling', Neuropsychopharmacology, vol. 39, pp. 2497-2505. https://doi.org/10.1038/npp.2014.106

Improved long-term memory via enhancing cGMP-PKG signaling requires cAMP-PKA signaling. / Bollen, E.; Puzzo, D.; Rutten, K.; Privitera, L.; De Vry, J.; Vanmierlo, T.; Kenis, G.; Palmeri, A.; D'Hooge, R.; Balschun, D.; Steinbusch, H.W.M.; Blokland, A.; Prickaerts, J.

In: Neuropsychopharmacology, Vol. 39, 12.05.2014, p. 2497-2505.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Bollen, E.

AU - Puzzo, D.

AU - Rutten, K.

AU - Privitera, L.

AU - De Vry, J.

AU - Vanmierlo, T.

AU - Kenis, G.

AU - Palmeri, A.

AU - D'Hooge, R.

AU - Balschun, D.

AU - Steinbusch, H.W.M.

AU - Blokland, A.

AU - Prickaerts, J.

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N2 - Memory consolidation is defined by the stabilization of a memory trace after acquisition, and consists of numerous molecular cascades that mediate synaptic plasticity. Commonly, a distinction is made between an early and a late consolidation phase, in which early refers to the first hours in which labile synaptic changes occur, whereas late consolidation relates to stable and long-lasting synaptic changes induced by de novo protein synthesis. How these phases are linked at a molecular level is not yet clear. Here we studied the interaction of the cyclic nucleotide-mediated pathways during the different phases of memory consolidation in rodents. In addition, the same pathways were studied in a model of neuronal plasticity, long-term potentiation (LTP). We demonstrated that cGMP/PKG signaling mediates early memory consolidation as well as early-phase-LTP, while cAMP/PKA signaling mediates late consolidation and late-phase-like LTP. Additionally, we show for the first time that early-phase cGMP/PKG-signaling requires late-phase cAMP/PKA-signaling in both LTP and long-term memory formation.Neuropsychopharmacology accepted article preview online, 12 May 2014; doi:10.1038/npp.2014.106.

AB - Memory consolidation is defined by the stabilization of a memory trace after acquisition, and consists of numerous molecular cascades that mediate synaptic plasticity. Commonly, a distinction is made between an early and a late consolidation phase, in which early refers to the first hours in which labile synaptic changes occur, whereas late consolidation relates to stable and long-lasting synaptic changes induced by de novo protein synthesis. How these phases are linked at a molecular level is not yet clear. Here we studied the interaction of the cyclic nucleotide-mediated pathways during the different phases of memory consolidation in rodents. In addition, the same pathways were studied in a model of neuronal plasticity, long-term potentiation (LTP). We demonstrated that cGMP/PKG signaling mediates early memory consolidation as well as early-phase-LTP, while cAMP/PKA signaling mediates late consolidation and late-phase-like LTP. Additionally, we show for the first time that early-phase cGMP/PKG-signaling requires late-phase cAMP/PKA-signaling in both LTP and long-term memory formation.Neuropsychopharmacology accepted article preview online, 12 May 2014; doi:10.1038/npp.2014.106.

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DO - 10.1038/npp.2014.106

M3 - Article

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EP - 2505

JO - Neuropsychopharmacology

JF - Neuropsychopharmacology

SN - 0893-133X

ER -

Bollen E, Puzzo D, Rutten K, Privitera L, De Vry J, Vanmierlo T et al. Improved long-term memory via enhancing cGMP-PKG signaling requires cAMP-PKA signaling. Neuropsychopharmacology. 2014 May 12;39:2497-2505. https://doi.org/10.1038/npp.2014.106