A novel mechanism for cyclic adenosine monophosphate–mediated memory formation: Role of amyloid beta
Roberta Ricciarelli PhD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorDaniela Puzzo MD, PhD
Department of Bio-Medical Sciences, Section of Physiology, University of Catania, Catania, Italy
Search for more papers by this authorOlga Bruno PhD
Department of Pharmacy, Section of Pharmacology and Toxicology and Section of Medicinal Chemistry, University of Genoa, Genoa, Italy
Search for more papers by this authorElisa Canepa PhD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorElena Gardella BSc
Department of Pharmacy, Section of Pharmacology and Toxicology and Section of Medicinal Chemistry, University of Genoa, Genoa, Italy
Search for more papers by this authorDaniela Rivera BSc
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorLucia Privitera PhD
Department of Bio-Medical Sciences, Section of Physiology, University of Catania, Catania, Italy
Search for more papers by this authorCinzia Domenicotti PhD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorBarbara Marengo PhD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorUmberto Maria Marinari MD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorAgostino Palmeri MD, PhD
Department of Bio-Medical Sciences, Section of Physiology, University of Catania, Catania, Italy
Search for more papers by this authorMaria Adelaide Pronzato BSc
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorCorresponding Author
Ottavio Arancio MD, PhD
Department of Pathology and Cell Biology, Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University, New York, NY
Address correspondence to: Dr Fedele, School of Medical and Pharmaceutical Sciences, Department of Pharmacy, Section of Pharmacology and Toxicology, University of Genoa, Genoa, Italy. E-mail: [email protected]; Dr Arancio, Department of Pathology and Cell Biology, Taub Institute for Research on Alzheimer's Disease and Aging Brain, Columbia University, New York, USA. E-Mail: [email protected].Search for more papers by this authorCorresponding Author
Ernesto Fedele BSc
Department of Pharmacy, Section of Pharmacology and Toxicology and Section of Medicinal Chemistry, University of Genoa, Genoa, Italy
Address correspondence to: Dr Fedele, School of Medical and Pharmaceutical Sciences, Department of Pharmacy, Section of Pharmacology and Toxicology, University of Genoa, Genoa, Italy. E-mail: [email protected]; Dr Arancio, Department of Pathology and Cell Biology, Taub Institute for Research on Alzheimer's Disease and Aging Brain, Columbia University, New York, USA. E-Mail: [email protected].Search for more papers by this authorRoberta Ricciarelli PhD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorDaniela Puzzo MD, PhD
Department of Bio-Medical Sciences, Section of Physiology, University of Catania, Catania, Italy
Search for more papers by this authorOlga Bruno PhD
Department of Pharmacy, Section of Pharmacology and Toxicology and Section of Medicinal Chemistry, University of Genoa, Genoa, Italy
Search for more papers by this authorElisa Canepa PhD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorElena Gardella BSc
Department of Pharmacy, Section of Pharmacology and Toxicology and Section of Medicinal Chemistry, University of Genoa, Genoa, Italy
Search for more papers by this authorDaniela Rivera BSc
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorLucia Privitera PhD
Department of Bio-Medical Sciences, Section of Physiology, University of Catania, Catania, Italy
Search for more papers by this authorCinzia Domenicotti PhD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorBarbara Marengo PhD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorUmberto Maria Marinari MD
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorAgostino Palmeri MD, PhD
Department of Bio-Medical Sciences, Section of Physiology, University of Catania, Catania, Italy
Search for more papers by this authorMaria Adelaide Pronzato BSc
Department of Experimental Medicine, Section of General Pathology, University of Genoa, Genoa, Italy
Search for more papers by this authorCorresponding Author
Ottavio Arancio MD, PhD
Department of Pathology and Cell Biology, Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University, New York, NY
Address correspondence to: Dr Fedele, School of Medical and Pharmaceutical Sciences, Department of Pharmacy, Section of Pharmacology and Toxicology, University of Genoa, Genoa, Italy. E-mail: [email protected]; Dr Arancio, Department of Pathology and Cell Biology, Taub Institute for Research on Alzheimer's Disease and Aging Brain, Columbia University, New York, USA. E-Mail: [email protected].Search for more papers by this authorCorresponding Author
Ernesto Fedele BSc
Department of Pharmacy, Section of Pharmacology and Toxicology and Section of Medicinal Chemistry, University of Genoa, Genoa, Italy
Address correspondence to: Dr Fedele, School of Medical and Pharmaceutical Sciences, Department of Pharmacy, Section of Pharmacology and Toxicology, University of Genoa, Genoa, Italy. E-mail: [email protected]; Dr Arancio, Department of Pathology and Cell Biology, Taub Institute for Research on Alzheimer's Disease and Aging Brain, Columbia University, New York, USA. E-Mail: [email protected].Search for more papers by this authorAbstract
Cyclic adenosine monophosphate (cAMP) regulates long-term potentiation (LTP) and ameliorates memory in healthy and diseased brain. Increasing evidence shows that, under physiological conditions, low concentrations of amyloid β (Aβ) are necessary for LTP expression and memory formation. Here, we report that cAMP controls amyloid precursor protein (APP) translation and Aβ levels, and that the modulatory effects of cAMP on LTP occur through the stimulation of APP synthesis and Aβ production. Ann Neurol 2014;75:602–607
References
- 1 Nguyen PV, Woo NH. Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 2003; 71: 401–437.
- 2 Kandel ER. The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol Brain 2012; 5: 14.
- 3 Wu ZL, Thomas SA, Villacres EC, et al. Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice. Proc Natl Acad Sci U S A 1995; 92: 220–224.
- 4 Nguyen PV, Kandel ER. Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem 1997; 4: 230–243.
- 5 Wong ST, Athos J, Figueroa XA, et al. Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 1999; 23: 787–798.
- 6 Wang H, Ferguson GD, Pineda VV, et al. Overexpression of type-1 adenylyl cyclase in mouse forebrain enhances recognition memory and LTP. Nat Neurosci 2004; 7: 635–642.
- 7 Reneerkens OA, Rutten K, Steinbusch HW, et al. Selective phosphodiesterase inhibitors: a promising target for cognition enhancement. Psychopharmacology (Berl) 2009; 202: 419–443.
- 8 Bruno O, Fedele E, Prickaerts J, et al. GEBR-7b, a novel PDE4D selective inhibitor that improves memory in rodents at non-emetic doses. Br J Pharmacol 2011; 164: 2054–2063.
- 9 Puzzo D, Privitera L, Leznik E, et al. Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus. J Neurosci 2008; 28: 14537–14545.
- 10 Puzzo D, Privitera L, Fa M, et al. Endogenous amyloid-beta is necessary for hippocampal synaptic plasticity and memory. Ann Neurol 2011; 69: 819–830.
- 11 Puzzo D, Privitera L, Palmeri A. Hormetic effect of amyloid-beta peptide in synaptic plasticity and memory. Neurobiol Aging 2012; 33: 1484.e1415–1484.e1424.
- 12 Puzzo D, Arancio O. Amyloid-beta peptide: Dr. Jekyll or Mr. Hyde? J Alzheimers Dis 2013; 33(suppl 1): S111–S120.
- 13 Canepa E, Domenicotti C, Marengo B, et al. Cyclic adenosine monophosphate as an endogenous modulator of the amyloid-beta precursor protein metabolism. IUBMB Life 2013; 65: 127–133.
- 14 Schmidt SD, Nixon RA, Mathews PM. ELISA method for measurement of amyloid-β levels. Methods Mol Biol 2005; 279–297.
- 15 Lee EK, Kim HH, Kuwano Y, et al. hnRNP C promotes APP translation by competing with FMRP for APP mRNA recruitment to P bodies. Nat Struct Mol Biol 2010; 17: 732–739.
- 16 Ahn JH, McAvoy T, Rakhilin SV, et al. Protein kinase A activates protein phosphatase 2A by phosphorylation of the B56delta subunit. Proc Natl Acad Sci U S A 2007; 104: 2979–2984.
- 17 Ceman S, O'Donnell WT, Reed M, et al. Phosphorylation influences the translation state of FMRP-associated polyribosomes. Hum Mol Genet 2003; 12: 3295–3305.
- 18 Narayanan U, Nalavadi V, Nakamoto M, et al. FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A. J Neurosci 2007; 27: 14349–14357.
- 19 Barad M, Bourtchouladze R, Winder DG, et al. Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci U S A 1998; 95: 15020–15025.
- 20 Navakkode S, Sajikumar S, Frey JU. The type IV-specific phosphodiesterase inhibitor rolipram and its effect on hippocampal long-term potentiation and synaptic tagging. J Neurosci 2004; 24: 7740–7744.
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