Inhibition of acetylcholinesterase and phosphodiesterase-9A has differential effects on hippocampal early and late LTP

Neuropharmacology

Volumn 62, Issue 5-6, 2012, Pages 1964-1974

  Kroker, Katja S ^a   Rast, Georg ^a   Giovannini, Riccardo ^b   Marti, Anelise ^a   Dorner Ciossek, Cornelia ^a   Rosenbrock, Holger ^a  

^a BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^b Boehringer Ingelheim Italia SpA   (Italy)

Author keywords

Acetylcholinesterase inhibitor; Alzheimer's disease; Donepezil; Hippocampus; LTP; Phosphodiesterase 9A inhibitor

Indexed keywords

1 (2 CHLOROPHENYL) 6 [3,3,3 TRIFLUORO 2 METHYLPROPYL] 1,5 DIHYDRO 4H PYRAZOLO[3,4 D]PYRIMIDINE 4 ONE; ACETYLCHOLINESTERASE; BAY 736691; CYCLIC GMP; DONEPEZIL; PHOSPHODIESTERASE; PHOSPHODIESTERASE 9A; PHOSPHODIESTERASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; DRUG DETERMINATION; DRUG MECHANISM; DRUG TARGETING; EARLY LONG TERM POTENTIATION; ENZYME ACTIVITY; ENZYME INHIBITION; HIPPOCAMPUS; LATE LONG TERM POTENTIATION; LONG TERM POTENTIATION; MALE; MEMORY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; RESPONSE TIME;

3',5'-CYCLIC-AMP PHOSPHODIESTERASES; ACETYLCHOLINESTERASE; ANIMALS; CHOLINESTERASE INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; INDANS; LONG-TERM POTENTIATION; MALE; PHOSPHODIESTERASE INHIBITORS; PIPERIDINES; PYRAZOLES; PYRIMIDINES; RATS; RATS, WISTAR;

EID: 84857055295     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.12.021     Document Type: Article

References (118)

1. B.C. Albensi, D.R. Oliver, J. Toupin, and G. Odero Electrical stimulation protocols for hippocampal synaptic plasticity and neuronal hyper-excitability: are they effective or relevant? Exp. Neurol. 204 1 2007 1 13 (Pubitemid 46330292)
2. S.G. Andreeva, P. Dikkes, P.M. Epstein, and P.A. Rosenberg Expression of cGMP-specific phosphodiesterase 9A mRNA in the rat brain J. Neurosci. 21 22 2001 9068 9076 (Pubitemid 33054868)
3. O. Arancio, I. Antonova, S. Gambaryan, S.M. Lohmann, J.S. Wood, D.S. Lawrence, and R.D. Hawkins Presynaptic role of cGMP-dependent protein kinase during long-lasting potentiation J. Neurosci. 21 1 2001 143 149 (Pubitemid 32098736)
4. M.B. Ashour, S.J. Gee, and B.D. Hammock Use of a 96-well microplate reader for measuring routine enzyme activities Anal. Biochem. 166 2 1987 353 360
5. A. Baddeley Working memory: looking back and looking forward Nat. Rev. Neurosci. 4 10 2003 829 839 (Pubitemid 37314405)
6. M. Barad, R. Bourtchouladze, D.G. Winder, H. Golan, and E. Kandel 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 25 1998 15020 15025 (Pubitemid 29003749)
7. C.A. Barnes, J. Meltzer, F. Houston, G. Orr, K. McGann, and G.L. Wenk Chronic treatment of old rats with donepezil or galantamine: effects on memory, hippocampal plasticity and nicotinic receptors Neuroscience 99 1 2000 17 23 (Pubitemid 30495548)
8. R.T. Bartus, R.L. Dean 3rd, B. Beer, and A.S. Lippa The cholinergic hypothesis of geriatric memory dysfunction Science 217 4558 1982 408 414
9. Z.I. Bashir, S. Alford, S.N. Davies, A.D. Randall, and G.L. Collingridge Long-term potentiation of NMDA receptor-mediated synaptic transmission in the hippocampus Nature 349 6305 1991 156 158 (Pubitemid 21912034)
10. J.A. Beavo Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms Physiol. Rev. 75 4 1995 725 748
11. J.S. Birks, and R. Harvey Donepezil for dementia due to Alzheimer's disease Cochrane Database Syst. Rev. 3 2003 CD001190
12. T.V.P. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 6407 1993 31 39 (Pubitemid 23020772)
13. A. Blokland, R. Schreiber, and J. Prickaerts Improving memory: a role for phosphodiesterases Curr. Pharm. Des. 12 20 2006 2511 2523
14. D. Boehning, and S.H. Snyder Novel neural modulators Annu. Rev. Neurosci. 26 2003 105 131 (Pubitemid 37064930)
15. F.G. Boess, M. Hendrix, F.J. van der Staay, C. Erb, R. Schreiber, W. van Staveren, J. de Vente, J. Prickaerts, A. Blokland, and G. Koenig Inhibition of phosphodiesterase 2 increases neuronal cGMP, synaptic plasticity and memory performance Neuropharmacology 47 7 2004 1081 1092 (Pubitemid 39535847)
16. G.A. Böhme, C. Bon, J.M. Stutzmann, A. Doble, and J.C. Blanchard Possible involvement of nitric oxide in long-term potentiation Eur. J. Pharmacol. 199 3 1991 379 381
17. P. Bonsi, G. Martella, D. Cuomo, P. Platania, G. Sciamanna, G. Bernardi, J. Wess, and A. Pisani Loss of muscarinic autoreceptor function impairs long-term depression but not long-term potentiation in the striatum J. Neurosci. 28 24 2008 6258 6263
18. K.A. Buchanan, M.M. Petrovic, S.E. Chamberlain, N.V. Marrion, and J.R. Mellor Facilitation of long-term potentiation by muscarinic M(1) receptors is mediated by inhibition of SK channels Neuron 68 5 2010 948 963
19. P.A. Buchs, and D. Muller Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses Proc. Natl. Acad. Sci. U S A 93 15 1996 8040 8045 (Pubitemid 26277161)
20. P. Calabresi, D. Centonze, P. Gubellini, and G. Bernardi Activation of M1-like muscarinic receptors is required for the induction of corticostriatal LTP Neuropharmacology 38 2 1999 323 326 (Pubitemid 29073555)
21. R.J. Castellani, R.K. Rolston, and M.A. Smith Alzheimer disease Dis. Mon. 56 9 2010 484 546
22. F.L. Chang, and W.T. Greenough Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice Brain Res. 309 1 1984 35 46 (Pubitemid 14067562)
23. D.M. Chetkovich, and J.D. Sweatt Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus J. Neurochem. 61 5 1993 1933 1942
24. K.S. Christopherson, B.J. Hillier, W.A. Lim, and D.S. Bredt PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain J. Biol. Chem. 274 39 1999 27467 27473
25. G.L. Collingridge, S.J. Kehl, and H. McLennan Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus J. Physiol. 334 1983 33 46 (Pubitemid 13176081)
26. M. Costa-Mattioli, W.S. Sossin, E. Klann, and N. Sonenberg Translational control of long-lasting synaptic plasticity and memory Neuron 61 1 2009 10 26
27. C. Courtney, D. Farrell, R. Gray, R. Hills, L. Lynch, E. Sellwood, S. Edwards, W. Hardyman, J. Raftery, P. Crome, C. Lendon, H. Shaw, P. Bentham, and AD2000 Collaborative Group Long-term donepezil treatment in 565 patients with Alzheimer's disease (AD2000): randomised double-blind trial Lancet 363 9427 2004 2105 2115
28. A. Das, M. Dikshit, and C. Nath Profile of acetylcholinesterase in brain areas of male and female rats of adult and old age Life Sci. 68 13 2001 1545 1555 (Pubitemid 32168082)
29. S.N. Davies, R.A. Lester, K.G. Reymann, and G.L. Collingridge Temporally distinct pre- and post-synaptic mechanisms maintain long-term potentiation Nature 338 6215 1989 500 503 (Pubitemid 19107990)
30. 2+/calmodulin- kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionate type glutamate receptors Proc. Natl. Acad. Sci. USA 96 6 1999 3269 3274 (Pubitemid 29148880)
31. N.L. Desmond, and W.B. Levy Synaptic interface surface area increases with long-term potentiation in the hippocampal dentate gyrus Brain Res. 453 1-2 1988 308 314
32. B.S. Diniz, J.A. Pinto Jr., M.L. Gonzaga, F.M. Guimarães, W.F. Gattaz, and O.V. Forlenza To treat or not to treat? A meta-analysis of the use of cholinesterase inhibitors in mild cognitive impairment for delaying progression to Alzheimer's disease Eur. Arch. Psychiatry Clin. Neurosci. 259 4 2009 248 256
33. W.G. Eberlein, W.W. Engel, G. Trummlitz, G. Schmidt, and R. Hammer Tricyclic compounds as selective antimuscarinics. 2. Structure-activity relationships of M1-selective antimuscarinics related to pirenzepine J. Med. Chem. 31 6 1988 1169 1174
34. G.L. Ellman, K.D. Courtney, V. Andres Jr., and R.M. Feather-Stone A new and rapid colorimetric determination of acetylcholinesterase activity Biochem. Pharmacol. 7 1961 88 95
35. A. Fischer, F. Sananbenesi, C. Schrick, J. Spiess, and J. Radulovic Cyclin-dependent kinase 5 is required for associative learning J. Neurosci. 22 9 2002 3700 3707 (Pubitemid 37465775)
36. P.T. Francis, A.M. Palmer, M. Snape, and G.K. Wilcock The cholinergic hypothesis of Alzheimer's disease: a review of progress J. Neurol. Neurosurg. Psychiatry 66 2 1999 137 147 (Pubitemid 29103513)
37. U. Frey, M. Krug, K.G. Reymann, and H. Matthies Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro Brain Res. 452 1-2 1988 57 65
38. J. Garthwaite Concepts of neural nitric oxide-mediated transmission Eur. J. Neurosci. 27 11 2008 2783 2802 (Pubitemid 351832227)
39. J. Garthwaite, E. Southam, C.L. Boulton, E.B. Nielsen, K. Schmidt, and B. Mayer Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one Mol. Pharmacol. 48 2 1995 184 188
40. H. Geerts, P.O. Guillaumat, C. Grantham, W. Bode, K. Anciaux, and S. Sachak Brain levels and acetylcholinesterase inhibition with galantamine and donepezil in rats, mice, and rabbits Brain Res. 1033 2 2005 186 193 (Pubitemid 40193413)
41. G. Grecksch, and H. Matthies Two sensitive periods for the amnesic effect of anisomycin Pharmacol. Biochem. Behav. 12 5 1980 663 665 (Pubitemid 10045707)
42. V.K. Gribkoff, and J.T. Lum-Ragan Evidence for nitric oxide synthase inhibitor-sensitive and insensitive hippocampal synaptic potentiation J. Neurophysiol. 68 2 1992 639 642
43. J.E. Haley, E. Schaible, P. Pavlidis, A. Murdock, and D.V. Madison Basal and apical synapses of CA1 pyramidal cells employ different LTP induction mechanisms Learn. Mem. 3 4 1996 289 295 (Pubitemid 27043301)
44. R. Helou, and M. Rhalimi Cholinesterase inhibitors and the risk of pulmonary disorders in hospitalized dementia patients J. Popul. Ther. Clin. Pharmacol. 17 3 2010 e379 e389
45. R.K. Hernandez, W. Farwell, M.D. Cantor, and E.V. Lawler Cholinesterase inhibitors and incidence of bradycardia in patients with dementia in the veterans affairs new England healthcare system J. Am. Geriatr. Soc. 57 11 2009 1997 2003
46. E.P. Huang Synaptic plasticity: going through phases with LTP Curr. Biol. 8 10 1998 R350 R352
47. Y.Y. Huang, and E.R. Kandel Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization Learn. Mem. 1 1 1994 74 82 (Pubitemid 2113963)
48. Y.Y. Huang, P.V. Nguyen, T. Abel, and E.R. Kandel Long-lasting forms of synaptic potentiation in the mammalian hippocampus Learn. Mem. 3 2-3 1996 74 85 (Pubitemid 26357733)
49. P.H. Hutson, E.N. Finger, B.C. Magliaro, S.M. Smith, A. Converso, P.E. Sanderson, D. Mullins, L.A. Hyde, B.K. Eschle, Z. Turnbull, H. Sloan, M. Guzzi, X. Zhang, A. Wang, D. Rindgen, R. Mazzola, J.A. Vivian, D. Eddins, J.M. Uslaner, R. Bednar, C. Gambone, W. Le-Mair, M.J. Marino, N. Sachs, G. Xu, and S. Parmentier-Batteur The selective phosphodiesterase 9 (PDE9) inhibitor PF-04447943 (6-[(3S,4S)-4-methyl-1-(pyrimidin-2-ylmethyl)pyrrolidin-3-yl]-1- (tetrahydro-2H-pyran-4-yl)-1,5-dihydro-4H-pyrazolo[3,4-d]pyrimidin-4-one) enhances synaptic plasticity and cognitive function in rodents Neuropharmacology 61 4 2011 665 676
50. L.A. Izquierdo, D.M. Barros, M.R. Vianna, A. Coitinho, T. deDavid e Silva, H. Choi, B. Moletta, J.H. Medina, and I. Izquierdo Molecular pharmacological dissection of short- and long-term memory Cell Mol. Neurobiol. 22 3 2002 269 287 (Pubitemid 35364886)
51. R. Jackisch, S. Förster, M. Kammerer, A.K. Rothmaier, A. Ehret, J. Zentner, and T.J. Feuerstein Inhibitory potency of choline esterase inhibitors on acetylcholine release and choline esterase activity in fresh specimens of human and rat neocortex J. Alzheimers Dis. 16 3 2009 635 647
52. S.A. Jacobson, and M.N. Sabbagh Donepezil: potential neuroprotective and disease-modifying effects Expert Opin. Drug Metab. Toxicol. 4 10 2008 1363 1369
53. M. Jevsek, T. Mars, K. Mis, and Z. Grubic Origin of acetylcholinesterase in the neuromuscular junction formed in the in vitro innervated human muscle Eur. J. Neurosci. 20 11 2004 2865 2871 (Pubitemid 40007280)
54. 2+ entry through non-alpha7 nicotinic acetylcholine receptors Eur. J. Neurosci. 31 3 2010 463 476
55. H. Kaduszkiewicz, T. Zimmermann, H.P. Beck-Bornholdt, and H. van den Bussche Cholinesterase inhibitors for patients with Alzheimer's disease: systematic review of randomised clinical trials BMJ 331 7512 2005 321 327
56. G.Y. Ko, and P.T. Kelly Nitric oxide acts as a postsynaptic signaling molecule in calcium/calmodulin-induced synaptic potentiation in hippocampal CA1 pyramidal neurons J. Neurosci. 19 16 1999 6784 6794 (Pubitemid 29380107)
57. K.S. Kroker, G. Rast, and H. Rosenbrock Differential effect of the mGlu5 receptor positive allosteric modulator ADX-47273 on early and late hippocampal LTP Neuropharmacology 61 4 2011 707 714
58. K.S. Kroker, H. Rosenbrock, and G. Rast A multi-slice recording system for stable late phase hippocampal long-term potentiation experiments J. Neurosci. Methods 194 2 2011 394 401
59. L. Lagostena, C. Trocme-Thibierge, P. Morain, and E. Cherubini The partial alpha7 nicotine acetylcholine receptor agonist S 24795 enhances long-term potentiation at CA3-CA1 synapses in the adult mouse hippocampus Neuropharmacology 54 4 2008 676 685
60. V. Lakics, E.H. Karran, and F.G. Boess Quantitative comparison of phosphodiesterase mRNA distribution in human brain and peripheral tissues Neuropharmacology 59 6 2010 367 374
61. A.U. Larkman, and J.J. Jack Synaptic plasticity: hippocampal LTP Curr. Opin. Neurobiol. 5 3 1995 324 334
62. K.S. Lee, F. Schottler, M. Oliver, and G. Lynch Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus J. Neurophysiol. 44 2 1980 247 258 (Pubitemid 10034532)
63. D. Liao, R.H. Scannevin, and R. Huganir Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors J. Neurosci. 21 16 2001 6008 6017 (Pubitemid 32737734)
64. J. Lisman Actin's actions in LTP-induced synapse growth Neuron 38 3 2003 361 362 (Pubitemid 36579137)
65. Y.F. Lu, E.R. Kandel, and R.D. Hawkins Nitric oxide signaling contributes to late-phase LTP and CREB phosphorylation in the hippocampus J. Neurosci. 19 23 1999 10250 10261 (Pubitemid 30228032)
66. W. Lu, H. Man, W. Ju, W.S. Trimble, J.F. MacDonald, and Y.T. Wang Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons Neuron 29 1 2001 243 254 (Pubitemid 32108736)
67. P.L. Malen, and P.F. Chapman Nitric oxide facilitates long-term potentiation, but not long-term depression J. Neurosci. 17 7 1997 2645 2651 (Pubitemid 27137430)
68. R.C. Malenka, and M.F. Bear LTP and LTD: an embarrassment of riches Neuron 44 1 2004 5 21 (Pubitemid 39348827)
69. R.C. Malenka, and R.A. Nicoll Long-term potentiation - a decade of progress? Science 285 5435 1999 1870 1874
70. R. Malinow AMPA receptor trafficking and long-term potentiation Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358 1432 2003 707 714 (Pubitemid 36536700)
71. A.D. McCarthy, I.J. Owens, A.T. Bansal, S.M. McTighe, T.J. Bussey, and L.M. Saksida FK962 and donepezil act synergistically to improve cognition in rats: potential as an add-on therapy for Alzheimer's disease Pharmacol. Biochem. Behav. 98 1 2011 76 80
72. F.S. Menniti, W.S. Faraci, and C.J. Schmidt Phosphodiesterases in the CNS: targets for drug development Nat. Rev. Drug Discov. 5 8 2006 660 670 (Pubitemid 44151604)
73. R.S. Naik, J. Hartmann, C. Kiewert, E.G. Duysen, O. Lockridge, and J. Klein Effects of rivastigmine and donepezil on brain acetylcholine levels in acetylcholinesterase-deficient mice J. Pharm. Pharm. Sci. 12 1 2009 79 85
74. A. Neitz, E. Mergia, U.T. Eysel, D. Koesling, and T. Mittmann Presynaptic nitric oxide/cGMP facilitates glutamate release via hyperpolarization-activated cyclic nucleotide-gated channels in the hippocampus Eur. J. Neurosci. 33 9 2011 1611 1621
75. P.V. Nguyen, and E.R. Kandel Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus Learn. Mem. 4 2 1997 230 243 (Pubitemid 27350040)
76. P.V. Nguyen, T. Abel, and E.R. Kandel Requirement of a critical period of transcription for induction of a late phase of LTP Science 265 5175 1991 1104 1107 (Pubitemid 24293080)
77. T. Nicholas, R. Evans, S. Styren, R. Qiu, E.Q. Wang, F. Nelson, V. Le, S. Grimwood, C. Christoffersen, S. Banerjee, B. Corrigan, G. Kocan, K. Geoghegan, C. Carrieri, N. Raha, P. Verhoest, and H. Soares PF-04447943, a novel PDE9A inhibitor, increases cGMP levels in cerebrospinal fluid: translation from non-clinical species to healthy human volunteers Alzheimer Demen. 5 2009 330 331
78. T.J. O'Dell, R.D. Hawkins, E.R. Kandel, and O. Arancio Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger Proc. Natl. Acad. Sci. USA 88 24 1991 11285 11289 (Pubitemid 21916025)
79. T.J. O'Dell, P.L. Huang, T.M. Dawson, J.L. Dinerman, S.H. Snyder, E.R. Kandel, and M.C. Fishman Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS Science 265 5171 1994 542 546 (Pubitemid 24265004)
80. P.T. Pang, and B. Lu Regulation of late-phase LTP and long-term memory in normal and aging hippocampus: role of secreted proteins tPA and BDNF Ageing Res. Rev. 3 4 2004 407 430 (Pubitemid 39487898)
81. J. Prickaerts, A. Sik, W.C. van Staveren, G. Koopmans, H.W. Steinbusch, F.J. van der Staay, J. de Vente, and A. Blokland Phosphodiesterase type 5 inhibition improves early memory consolidation of object information Neurochem. Int. 45 6 2004 915 928 (Pubitemid 39108064)
82. J. Prickaerts, A. Sik, F.J. van der Staay, J. de Vente, and A. Blokland Dissociable effects of acetylcholinesterase inhibitors and phosphodiesterase type 5 inhibitors on object recognition memory: acquisition versus consolidation Psychopharmacology (Berl) 177 4 2005 381 390 (Pubitemid 40228285)
83. O.A. Reneerkens, K. Rutten, H.W. Steinbusch, A. Blokland, and J. Prickaerts Selective phosphodiesterase inhibitors: a promising target for cognition enhancement Psychopharmacology (Berl) 202 1-3 2009 419 443
84. K.G. Reymann, and J.U. Frey The late maintenance of hippocampal LTP: requirements, phases, 'synaptic tagging', 'late-associativity' and implications Neuropharmacology 52 1 2007 24 40
85. S.L. Rogers, R.S. Doody, R.C. Mohs, and L.T. Friedhoff Donepezil improves cognition and global function in Alzheimer disease: a 15-week, double-blind, placebo-controlled study. Donepezil Study Group Arch. Intern. Med. 158 9 1998 1021 1031 (Pubitemid 28213580)
86. M.H. Rosenbloom, R. Finley, M.M. Scheinman, M.D. Feldman, B.L. Miller, and G.D. Rabinovici Donepezil-associated bradyarrhythmia in a patient with dementia with Lewy bodies (DLB) Alzheimer Dis. Assoc. Disord. 24 2 2010 209 211
87. L. Rozzini, D. Ghianda, M. Trabucchi, and A. Padovani Severe worsening of parkinsonism in Lewy body dementia due to donepezil Neurology 63 8 2004 1543 1544 (Pubitemid 39426311)
88. K. Rutten, J.D. Vente, A. Sik, M.M. Ittersum, J. Prickaerts, and A. Blokland The selective PDE5 inhibitor, sildenafil, improves object memory in Swiss mice and increases cGMP levels in hippocampal slices Behav. Brain Res. 164 1 2005 11 16 (Pubitemid 41253727)
89. K. Rutten, J. Prickaerts, M. Hendrix, F.J. van der Staay, A. Sik, and A. Blokland 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 1-3 2007 107 112 (Pubitemid 46328881)
90. K. Rutten, J.L. Basile, J. Prickaerts, A. Blokland, and J.A. Vivian Selective PDE inhibitors rolipram and sildenafil improve object retrieval performance in adult cynomolgus macaques Psychopharmacology (Berl) 196 4 2008 643 648
91. S.C. Santos, I. Vala, C. Miguel, J.T. Barata, P. Garão, P. Agostinho, M. Mendes, A.V. Coelho, A. Calado, C.R. Oliveira, J.M. e Silva, and C. Saldanha Expression and subcellular localization of a novel nuclear acetylcholinesterase protein J. Biol. Chem. 282 35 2007 25597 25603 (Pubitemid 47372784)
92. C.J. Schmidt Phosphodiesterase inhibitors as potential cognition enhancing agents Curr. Top. Med. Chem. 10 2 2010 222 230
93. C.J. Schmidt, J.F. Harms, F.D. Tingley, K. Schmidt, W.O. Adamowicz, A. Romegialli, R.J. Kleiman, C.J. Barry, T.M. Coskran, S.M. O'Neill, D.T. Stephenson, and F.S. Menniti PDE9A-mediated regulation of cGMP: developing a biomarker for a novel therapy for Alzheimer's disease Alzheimers Dement. 5 Suppl 2009 331
94. E.M. Schuman, and D.V. Madison A requirement for the intercellular messenger nitric oxide in long-term potentiation Science 254 5037 1991 1503 1506 (Pubitemid 21917489)
95. A receptor benzodiazepine site ligands Neuropharmacology 36 6 1997 823 830 (Pubitemid 27286736)
96. B. Seltzer, P. Zolnouni, M. Nunez, R. Goldman, D. Kumar, J. Ieni, and S. Richardson Donepezil "402" Study Group. Efficacy of donepezil in early-stage Alzheimer disease: a randomized placebo-controlled trial Arch. Neurol. 61 12 2004 1852 1856 (Pubitemid 39612945)
97. S.H. Shi, Y. Hayashi, R.S. Petralia, S.H. Zaman, R.J. Wenthold, K. Svoboda, and R. Malinow Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation Science 284 5421 1999 1811 1816
98. S. Shi, Y. Hayashi, J.A. Esteban, and R. Malinow Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons Cell 105 3 2001 331 343 (Pubitemid 32455340)
99. A.J. Silva, J.H. Kogan, P.W. Frankland, and S. Kida CREB and memory Annu. Rev. Neurosci. 21 1998 127 148 (Pubitemid 28150661)
100. H. Son, Y.F. Lu, M. Zhuo, O. Arancio, E.R. Kandel, and R.D. Hawkins The specific role of cGMP in hippocampal LTP Learn. Mem. 5 3 1998 231 245 (Pubitemid 29108882)
101. J.P. Spencer, L.J. Middleton, and C.H. Davies Investigation into the efficacy of the acetylcholinesterase inhibitor, donepezil, and novel procognitive agents to induce gamma oscillations in rat hippocampal slices Neuropharmacology 59 6 2010 437 443
102. M. Sternfeld, S. Shoham, O. Klein, C. Flores-Flores, T. Evron, G.H. Idelson, D. Kitsberg, J.W. Patrick, and H. Soreq Excess "read-through" acetylcholinesterase attenuates but the "synaptic" variant intensifies neurodeterioration correlates Proc. Natl. Acad. Sci. U S A 97 15 2000 8647 8652 (Pubitemid 30639727)
103. J.D. Sweatt Mechanisms of Memory second ed. 2009 Academic Press
104. K. Tabata, K. Matsumoto, and H. Watanabe Paeoniflorin, a major constituent of peony root, reverses muscarinic M1-receptor antagonist-induced suppression of long-term potentiation in the rat hippocampal slice Jpn. J. Pharmacol. 83 1 2000 25 30 (Pubitemid 30352653)
105. J.W. Tsao, and K.M. Heilman Donepezil improved memory in multiple sclerosis in a randomized clinical trial Neurology 64 10 2005 1823 author reply 1823 (Pubitemid 40695840)
106. N. Tsuno Donepezil in the treatment of patients with Alzheimer's disease Expert Rev. Neurother. 9 5 2009 591 598
107. F.J. van der Staay, and P.C. Bouger Effects of the cholinesterase inhibitors donepezil and metrifonate on scopolamine-induced impairments in the spatial cone field orientation task in rats Behav. Brain Res. 156 1 2005 1 10 (Pubitemid 39330431)
108. F.J. van der Staay, K. Rutten, L. Bärfacker, J. Devry, C. Erb, H. Heckroth, D. Karthaus, A. Tersteegen, M. van Kampen, A. Blokland, J. Prickaerts, K.G. Reymann, U.H. Schröder, and M. Hendrix The novel selective PDE9 inhibitor BAY 73-6691 improves learning and memory in rodents Neuropharmacology 55 5 2008 908 918
109. W.C. van Staveren, J. Glick, Ittersum M. Markerink-van, M. Shimizu, J.A. Beavo, H.W. Steinbusch, and J. de Vente Cloning and localization of the cGMP-specific phosphodiesterase type 9 in the rat brain J. Neurocytol. 31 8-9 2002 729 741 (Pubitemid 37386661)
110. P.R. Verhoest, C. Proulx-Lafrance, M. Corman, L. Chenard, C.J. Helal, X. Hou, R. Kleiman, S. Liu, E. Marr, F.S. Menniti, C.J. Schmidt, M. Vanase-Frawley, A.W. Schmidt, R.D. Williams, F.R. Nelson, K.R. Fonseca, and S. Liras Identification of a brain penetrant PDE9A inhibitor utilizing prospective design and chemical enablement as a rapid lead optimization strategy J. Med. Chem. 52 24 2009 7946 7949
111. Z. Wang, L. Kai, M. Day, J. Ronesi, H.H. Yin, J. Ding, T. Tkatch, D.M. Lovinger, and D.J. Surmeier Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons Neuron 50 3 2006 443 452
112. A. Whitehead, C. Perdomo, R.D. Pratt, J. Birks, G.K. Wilcock, and J.G. Evans Donepezil for the symptomatic treatment of patients with mild to moderate Alzheimer's disease: a meta-analysis of individual patient data from randomised controlled trials Int. J. Geriatr. Psychiatry 19 7 2004 624 633 (Pubitemid 38996839)
113. P.J. Whitehouse, D.L. Price, R.G. Struble, A.W. Clark, J.T. Coyle, and M.R. Delon Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain Science 215 4537 1982 1237 1239 (Pubitemid 12106486)
114. J.H. Williams, Y.G. Li, A. Nayak, M.L. Errington, K.P. Murphy, and T.V. Bliss The suppression of long-term potentiation in rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent Neuron 11 5 1993 877 884 (Pubitemid 23347472)
115. F. Wunder, A. Tersteegen, A. Rebmann, C. Erb, T. Fahrig, and M. Hendrix Characterization of the first potent and selective PDE9 inhibitor using a cGMP reporter cell line Mol. Pharmacol. 68 6 2005 1775 1781 (Pubitemid 41654360)
116. H.T. Zhang, and J.M. O'Donnell Effects of rolipram on scopolamine-induced impairment of working and reference memory in the radial-arm maze tests in rats Psychopharmacology (Berl) 150 3 2000 311 316 (Pubitemid 30447851)
117. M. Zhuo, Y. Hu, C. Schultz, E.R. Kandel, and R.D. Hawkins Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation Nature 368 6472 1994 635 639 (Pubitemid 24153387)
118. M. Zhuo, J.T. Laitinen, X.C. Li, and R.D. Hawkins On the respective roles of nitric oxide and carbon monoxide in long-term potentiation in the hippocampus Learn. Mem. 6 1 1999 63 76 (Pubitemid 29164549)