Inhibition of phosphodiesterase-4 reverses memory deficits produced by Aβ25–35 or Aβ1–40 peptide in rats

Abel T, Nguyen PV (2008) Regulation of hippocampus-dependent memory by cyclic AMP-dependent protein kinase. Prog Brain Res 169:97–115 Ahn J, Um M, Choi W, Kim S, Ha T (2006) Protective effects of Glycyrrhiza uralensis Fisch. on the cognitive deficits caused by beta-amyloid peptide 25–35 in young mice. Biogerontology 7:239–247 Arendash GW, Gordon MN, Diamond DM, Austin LA, Hatcher JM, Jantzen P, DiCarlo G, Wilcock D, Morgan D (2001) Behavioral assessment of Alzheimer's transgenic mice following long-term Abeta vaccination: task specificity and correlations between Abeta deposition and spatial memory. DNA Cell Biol 20:737–744 Bach ME, Barad M, Son H, Zhuo M, Lu YF, Shih R, Mansuy I, Hawkins RD, Kandel ER (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 Bailey CH, Bartsch D, Kandel ER (1996) Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA 93:13445–13452 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 Bontempi B, Laurent-Demir C, Destrade C, Jaffard R (1999) Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400:671–675 Bourtchouladze R, Lidge R, Catapano R, Stanley J, Gossweiler S, Romashko D, Scott R, Tully T (2003) A mouse model of Rubinstein-Taybi syndrome: defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4. Proc Natl Acad Sci USA 100:10518–10522 Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59–68 Butterfield DA, Boyd-Kimball D (2005) The critical role of methionine 35 in Alzheimer's amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity. Biochim Biophys Acta 1703:149–156 Cao M, Han Y, Wang J, Wang Y (2007) Modulation of fibrillogenesis of Amyloid beta(1–40) peptide with cationic gemini surfactant. J Phys Chem B 111:13436–13443 Chen SY, Wright JW, Barnes CD (1996) The neurochemical and behavioral effects of beta-amyloid peptide (25–35). Brain Res 720:54–60 Chen QS, Kagan BL, Hirakura Y, Xie CW (2000) Impairment of hippocampal long-term potentiation by Alzheimer amyloid beta-peptides. J Neurosci Res 60:65–72 Chiba T, Yamada M, Hashimoto Y, Sato M, Sasabe J, Kita Y, Terashita K, Aiso S, Nishimoto I, Matsuoka M (2005) Development of a femtomolar-acting humanin derivative named colivelin by attaching activity-dependent neurotrophic factor to its N terminus: characterization of colivelin-mediated neuroprotection against Alzheimer's disease-relevant insults in vitro and in vivo. J Neurosci 25:10252–10261 Cleary J, Hittner JM, Semotuk M, Mantyh P, O'Hare E (1995) Beta-amyloid(1–40) effects on behavior and memory. Brain Res 682:69–74 Comery TA, Martone RL, Aschmies S, Atchison KP, Diamantidis G, Gong X, Zhou H, Kreft AF, Pangalos MN, Sonnenberg-Reines J, Jacobsen JS, Marquis KL (2005) Acute gamma-secretase inhibition improves contextual fear conditioning in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 25:8898–8902 Delobette S, Privat A, Maurice T (1997) In vitro aggregation facilities beta amyloid peptide-(25–35) induced amnesia in the rat. Eur J Pharmacol 319:1–4 Egawa T, Mishima K, Matsumoto Y, Iwasaki K, Iwasaki K, Fujiwara M (1997) Rolipram and its optical isomers, phosphodiesterase 4 inhibitors, attenuated the scopolamine-induced impairments of learning and memory in rats. Jpn J Pharmacol 75:275–281 Fang F, Liu GT (2006) Protective effects of compound FLZ on beta-amyloid peptide-(25–35)-induced mouse hippocampal injury and learning and memory impairment. Acta Pharmacol Sin 27:651–658 Frautschy SA, Yang F, Calderón L, Cole GM (1996) Rodent models of Alzheimer's disease: rat A beta infusion approaches to amyloid deposits. Neurobiol Aging 17:311–321 Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661–1664 Gengler S, Gault VA, Harriott P, Hölscher C (2007) Impairments of hippocampal synaptic plasticity induced by aggregated beta-amyloid (25–35) are dependent on stimulation-protocol and genetic background. Exp Brain Res 179:621–630 Giorgi M, Modica A, Pompili A, Pacitti C, Gasbarri A (2004) The induction of cyclic nucleotide phosphodiesterase 4 gene (PDE4D) impairs memory in a water maze task. Behav Brain Res 154:99–106 Golde TE (2003) Alzheimer disease therapy: can the amyloid cascade be halted? J Clin Invest 111:11–18 Gong B, Vitolo OV, Trinchese F, Liu S, Shelanski M, Arancio O (2004) Persistent improvement in synaptic and cognitive functions in an Alzheimer mouse model after rolipram treatment. J Clin Invest 114:1624–1634 Griebel G, Misslin R, Vogel E, Bourguignon JJ (1991) Behavioral effects of rolipram and structurally related compounds in mice: behavioral sedation of cAMP phosphodiesterase inhibitors. Pharmacol Biochem Behav 39:321–323 Hashimoto M, Tanabe Y, Fujii Y, Kikuta T, Shibata H, Shido O (2005) Chronic administration of docosahexaenoic acid ameliorates the impairment of spatial cognition learning ability in amyloid beta-infused rats. J Nutr 135:549–555 Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99–102 Imanishi T, Sawa A, Ichimaru Y, Miyashiro M, Kato S, Yamamoto T, Ueki S (1997) Ameliorating effects of rolipram on experimentally induced impairments of learning and memory in rodents. Eur J Pharmacol 321:273–278 Jin DQ, Park BC, Lee JS, Choi HD, Lee YS, Yang JH, Kim JA (2004) Mycelial extract of Cordyceps ophioglossoides prevents neuronal cell death and ameliorates beta-amyloid peptide-induced memory deficits in rats. Biol Pharm Bull 27:1126–1129 Josselyn SA, Shi C, Carlezon WA Jr, Neve RL, Nestler EJ, Davis M (2001) Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J Neurosci 21:2404–2412 Kim DH, Kim S, Jeon SJ, Son KH, Lee S, Yoon BH, Cheong JH, Ko KH, Ryu JH (2008) The effects of acute and repeated oroxylin A treatments on Abeta(25–35)-induced memory impairment in mice. Neuropharmacology 55:639–647 Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bächinger HP, Brennan RG, Roberts SG, Green MR, Goodman RH (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370:223–226 Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448–6453 Li Y, Qin HQ, Chen QS, Wang JJ (2005) Retraction notice to “Neurochemical and behavioral effects of the intrahippocampal co-injection of beta-amyloid protein1–40 and ibotenic acid in rats”. Life Sci 76:1189–1197 Li YF, Huang Y, Amsdell SL, Xiao L, O'Donnell JM, Zhang HT (2009) Antidepressant- and anxiolytic-like effects of the phosphodiesterase-4 inhibitor rolipram on behavior depend on cyclic AMP response element binding protein-mediated neurogenesis in the hippocampus. Neuropsychopharmacology 34:2404–2419 Lin HB, Yang XM, Li TJ, Cheng YF, Zhang HT, Xu JP (2009) Memory deficits and neurochemical changes induced by C-reactive protein in rats: implication in Alzheimer’s disease. Psychopharmacology 204:705–714 Lippa CF, Nee LE, Mori H, St George-Hyslop P (1998) Abeta-42 deposition precedes other changes in PS-1 Alzheimer's disease. Lancet 352:1117–1118 Liu R, Barkhordarian H, Emadi S, Park CB, Sierks MR (2005) Trehalose differentially inhibits aggregation and neurotoxicity of beta-amyloid 40 and 42. Neurobiol Dis 20:74–81 MacKenzie SJ, Houslay MD (2000) Action of rolipram on specific PDE4 cAMP phosphodiesterase isoforms and on the phosphorylation of cAMP-response-element-binding protein (CREB) and p38 mitogen-activated protein (MAP) kinase in U937 monocytic cells. Biochem J 347:571–578 Matsuzaki K, Yamakuni T, Hashimoto M, Haque AM, Shido O, Mimaki Y, Sashida Y, Ohizumi Y (2006) Nobiletin restoring beta-amyloid-impaired CREB phosphorylation rescues memory deterioration in Alzheimer's disease model rats. Neurosci Lett 400:230–234 Maurice T, Lockhart BP, Privat A (1996) Amnesia induced in mice by centrally administered beta-amyloid peptides involves cholinergic dysfunction. Brain Res 706:181–193 Medina JH, Schroder N, Izquierdo I (1999) Two different properties of short- and long-term memory. Behav Brain Res 103:119–121 Miguel-Hidalgo JJ, Cacabelos R (1998) Beta-amyloid(1–40)-induced neurodegeneration in the rat hippocampal neurons of the CA1 subfield. Acta Neuropathol (Berl) 95:455–465 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 Nakamura S, Murayama N, Noshita T, Annoura H, Ohno T (2001) Progressive brain dysfunction following intracerebroventricular infusion of beta(1-42)-amyloid peptide. Brain Res 912:128–136 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 Olariu A, Tran MH, Yamada K, Mizuno M, Hefco V, Nabeshima T (2001) Memory deficits and increased emotionality induced by beta-amyloid (25–35) are correlated with the reduced acetylcholine release and altered phorbol dibutyrate binding in the hippocampus. J Neural Transm 108:1065–1079 Pakaski M, Kalman J (2008) Interactions between the amyloid and cholinergic mechanisms in Alzheimer's disease. Neurochem Int 53:103–111 Puzzo D, Vitolo O, Trinchese F, Jacob JP, Palmeri A, Arancio O (2005) Amyloid-beta peptide inhibits activation of the nitric oxide/cGMP/cAMP-responsive element-binding protein pathway during hippocampal synaptic plasticity. J Neurosci 25:6887–6897 Roesler R, Luft T, Oliveira SH, Farias CB, Almeida VR, Quevedo J, Dal Pizzol F, Schröder N, Izquierdo I, Schwartsmann G (2006) Molecular mechanisms mediating gastrin-releasing peptide receptor modulation of memory consolidation in the hippocampus. Neuropharmacology 51:350–357 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 Schmitt TL, Steiner E, Trieb K, Grubeck-Loebenstein B (1997) Amyloid beta-protein (25–35) increases cellular APP and inhibits the secretion of APPs in human extraneuronal cells. Exp Cell Res 234:336–340 Selkoe DJ (2001) Alzheimer’s disease: genes, proteins, and therapy. Physiol Rev 81:741–766 Silvestre JS, Fernandez AG, Palacios JM (1999) Preliminary evidence for an involvement of the cholinergic system in the sedative effects of rolipram in rats. Pharmacol Biochem Behav 64:1–5 Sinha S, Lieberburg I (1999) Cellular mechanisms of beta-amyloid production and secretion. Proc Natl Acad Sci USA 96:11049–11053 Smith DF (1990) Effects of lithium and rolipram enantiomers on locomotor activity in inbred mice. Pharmacol Toxicol 66:142–145 Smith DL, Pozueta J, Gong B, Arancio O, Shelanski M (2009) Reversal of long-term dendritic spine alterations in Alzheimer disease models. Proc Natl Acad Sci USA 106:16877–16882 Stepanichev MYu, Moiseeva YuV, Lazareva NA, Onufriev MV, Gulyaeva NV (2003) Single intracerebroventricular administration of amyloid beta (25–35) peptide induces impairment in short-term rather than long-term memory in rats. Brain Res Bull 61:197–205 Suh YH, Checler F (2002) Amyloid precursor protein, presenilins, and alpha-synuclein: molecular pathogenesis and pharmacological applications in Alzheimer's disease. Pharmacol Rev 54:469–525 Sun MK, Alkon DL (2002) Impairment of hippocampal CA1 heterosynaptic transformation and spatial memory by beta-amyloid (25–35). J Neurophysiol 87:2441–2449 Sweeney WA, Luedtke J, McDonald MP, Overmier JB (1997) Intrahippocampal injections of exogenous beta-amyloid induce postdelay errors in an eight-arm radial maze. Neurobiol Learn Mem 68:97–101 Tong L, Thornton PL, Balazs R, Cotman CW (2001) Beta-amyloid-(1-42) impairs activity-dependent cAMP-response element-binding protein signaling in neurons at concentrations in which cell survival is not compromised. J Biol Chem 276:17301–17306 Tong L, Balazs R, Thornton PL, Cotman CW (2004) Beta-amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons. J Neurosci 24:6799–6809 Tsuruma K, Tanaka Y, Shimazawa M, Hara H (2010) Induction of amyloid precursor protein by the neurotoxic peptide, amyloid-beta 25–35, causes retinal ganglion cell death. J Neurochem, Epub ahead of print Um MY, Choi WH, Aan JY, Kim SR, Ha TY (2006) Protective effect of Polygonum multiflorum Thunb on amyloid beta-peptide 25–35 induced cognitive deficits in mice. J Ethnopharmacol 104:144–148 Vianna MR, Szapiro G, McGaugh JL, Medina JH, Izquierdo I (2001) Retrieval of memory for fear-motivated training initiates extinction requiring protein synthesis in the rat hippocampus. Proc Natl Acad Sci USA 98:12251–12254 Vitolo OV, Sant'Angelo A, Costanzo V, Battaglia F, Arancio O, Shelanski M (2002) Amyloid beta -peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc Natl Acad Sci USA 99:13217–13221 Wang H, Chou C, Liao J, Chen C (2001) Dehydroevodiamine attenuates β-amyloid peptide-induced amnesia in mice. Eur J Pharmacol 413:221–225 Wang Z, Liu Q, Zhang R, Liu S, Xia Z, Hu Y (2009) Catalpol ameliorates beta amyloid-induced degeneration of cholinergic neurons by elevating brain-derived neurotrophic factors. Neuroscience 163:1363–1372 Yamada K, Tanaka T, Senzaki K, Kameyama T, Nabeshima T (1998) Propentofylline improves learning and memory deficits in rats induced by beta-amyloid protein-(1–40). Eur J Pharmacol 349:15–22 Yamada K, Tanaka T, Zou LB, Senzaki K, Yano K, Osada T, Ana O, Ren X, Kameyama T, Nabeshima T (1999) Long-term deprivation of oestrogens by ovariectomy potentiates beta-amyloid-induced working memory deficits in rats. Br J Pharmacol 128:419–427 Yamada M, Chiba T, Sasabe J, Terashita K, Aiso S, Matsuoka M (2008) Nasal Colivelin treatment ameliorates memory impairment related to Alzheimer's disease. Neuropsychopharmacology 33:2020–2032 Yamaguchi Y, Miyashita H, Tsunekawa H, Mouri A, Kim HC, Saito K, Matsuno T, Kawashima S, Nabeshima T (2006) Effects of a novel cognitive enhancer, spiro[imidazo-[1, 2-a]pyridine-3, 2-indan]-2(3H)-one (ZSET1446), on learning impairments induced by amyloid-beta1–40 in the rat. J Pharmacol Exp Ther 317:1079–1087 Yin JC, Wallach JS, Del Vecchio M, Wilder EL, Zhou H, Quinn WG, Tully T (1994) Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79:49–58 Yin JC, Del Vecchio M, Zhou H, Tully T (1995) CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81:107–115 Zhang HT, O'Donnell JM (2000) Effects of rolipram on scopolamine-induced impairment of working and reference memory in the radial-arm maze tests in rats. Psychopharmacology (Berl) 150:311–316 Zhang HT, Crissman AM, Dorairaj NR, Chandler LJ, O'Donnell JM (2000) Inhibition of cyclic AMP phosphodiesterase (PDE4) reverses memory deficits associated with NMDA receptor antagonism. Neuropsychopharmacology 23:198–204 Zhang HT, Huang Y, Jin SL, Frith SA, Suvarna N, Conti M, O'Donnell JM (2002) Antidepressant-like profile and reduced sensitivity to rolipram in mice deficient in the PDE4D phosphodiesterase enzyme. Neuropsychopharmacology 27:587–595 Zhang HT, Zhao Y, Huang Y, Dorairaj NR, Chandler LJ, O'Donnell JM (2004) 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 29:1432–1439 Zhang HT, Huang Y, Suvarna NU, Deng C, Crissman AM, Hopper AT, De Vivo M, Rose GM, O'Donnell JM (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