A biphasic and brain-region selective down-regulation of cyclic adenosine monophosphate concentrations supports object recognition in the rat

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Hotte, Maïte ^a,b   Dauphin, François ^a   Freret, Thomas ^a   Boulouard, Michel ^a   Levallet, Guenaëlle ^a,c  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITÉ DE ROUEN   (France)

^c CAEN UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 AMINO 5 CHLORO 2 METHOXYPHENYL) 3 (1 BUTYL 4 PIPERIDINYL) 1 PROPANONE; CYCLIC AMP; MILRINONE; PHOSPHODIESTERASE IV; ROLIPRAM; SEROTONIN 4 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN DEPTH STIMULATION; BRAIN REGION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME ASSAY; EPISODIC MEMORY; HIPPOCAMPUS; INTERMETHOD COMPARISON; LOCOMOTION; MALE; NONHUMAN; PATTERN RECOGNITION; PERIRHINAL CORTEX; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREFRONTAL CORTEX; PROTEIN CONTENT; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TASK PERFORMANCE; UPREGULATION; VISUAL MEMORY; WESTERN BLOTTING; ANIMAL; BRAIN; MEMORY; METABOLISM; PHYSIOLOGY; REACTION TIME; RECOGNITION; TEMPORAL LOBE;

ANIMALS; BRAIN; CYCLIC AMP; DOWN-REGULATION; HIPPOCAMPUS; MEMORY; PREFRONTAL CORTEX; RATS; REACTION TIME; RECOGNITION (PSYCHOLOGY); TEMPORAL LOBE;

EID: 84857133765     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032244     Document Type: Article

References (99)

1. 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.
2. Hoyer D, Pompe B, Friedrich H, Zwiener U, Baranowski R, et al. (2004) Autonomic Information Flow during awakeness, sleep, and multiple organ dysfunction syndrome assessed by mutual information function of heart rate fluctuations. Conf Proc IEEE Eng Med Biol Soc 1: 628-630.
3. Bach ME, Barad M, Son H, Zhuo M, Lu YF, 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 U S A 96: 5280-5285.
4. 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 U S A 95: 15020-15025.
5. 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.
6. Bernabeu R, Cammarota M, Izquierdo I, Medina JH, (1997) Involvement of hippocampal AMPA glutamate receptor changes and the cAMP/protein kinase A/CREB-P signalling pathway in memory consolidation of an avoidance task in rats. Braz J Med Biol Res 30: 961-965.
7. 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.
8. Prickaerts J, de Vente J, Honig W, Steinbusch HW, Blokland A, (2002) cGMP, but not cAMP, in rat hippocampus is involved in early stages of object memory consolidation. Eur J Pharmacol 436: 83-87.
9. Rutten K, Prickaerts J, Hendrix M, van der Staay FJ, Sik A, et al. (2007) 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.
10. Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, et al. (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.
11. Taylor JR, Birnbaum S, Ubriani R, Arnsten AF, (1999) Activation of cAMP-dependent protein kinase A in prefrontal cortex impairs working memory performance. J Neurosci 19: RC23.
12. Connolly DA, Hockley WE, Pratt MW, (1996) A developmental evaluation of frequency memory for actions presented in lists, scripts, and stories. Memory 4: 243-263.
13. Pineda VV, Athos JI, Wang H, Celver J, Ippolito D, et al. (2004) Removal of G(ialpha1) constraints on adenylyl cyclase in the hippocampus enhances LTP and impairs memory formation. Neuron 41: 153-163.
14. Ramos BP, Birnbaum SG, Lindenmayer I, Newton SS, Duman RS, et al. (2003) Dysregulation of protein kinase a signaling in the aged prefrontal cortex: new strategy for treating age-related cognitive decline. Neuron 40: 835-845.
15. 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.
16. Lamirault L, Guillou C, Thal C, Simon H, (2003) Combined treatment with galanthaminium bromide, a new cholinesterase inhibitor, and RS 67333, a partial agonist of 5-HT4 receptors, enhances place and object recognition in young adult and old rats. Prog Neuropsychopharmacol Biol Psychiatry 27: 185-195.
17. Lamirault L, Simon H, (2001) Enhancement of place and object recognition memory in young adult and old rats by RS 67333, a partial agonist of 5-HT4 receptors. Neuropharmacology 41: 844-853.
18. Levallet G, Hotte M, Boulouard M, Dauphin F, (2009) Increased particulate phosphodiesterase 4 in the prefrontal cortex supports 5-HT4 receptor-induced improvement of object recognition memory in the rat. Psychopharmacology (Berl) 202: 125-139.
19. Moser PC, Bergis OE, Jegham S, Lochead A, Duconseille E, et al. (2002) SL65.0155, a novel 5-hydroxytryptamine(4) receptor partial agonist with potent cognition-enhancing properties. J Pharmacol Exp Ther 302: 731-741.
20. Fontana DJ, Daniels SE, Wong EH, Clark RD, Eglen RM, (1997) The effects of novel, selective 5-hydroxytryptamine (5-HT)4 receptor ligands in rat spatial navigation. Neuropharmacology 36: 689-696.
21. Galeotti N, Ghelardini C, Bartolini A, (1998) Role of 5-HT4 receptors in the mouse passive avoidance test. J Pharmacol Exp Ther 286: 1115-1121.
22. Lelong V, Dauphin F, Boulouard M, (2001) RS 67333 and D-cycloserine accelerate learning acquisition in the rat. Neuropharmacology 41: 517-522.
23. Letty S, Child R, Dumuis A, Pantaloni A, Bockaert J, et al. (1997) 5-HT4 receptors improve social olfactory memory in the rat. Neuropharmacology 36: 681-687.
24. Marchetti E, Dumuis A, Bockaert J, Soumireu-Mourat B, Roman FS, (2000) Differential modulation of the 5-HT(4) receptor agonists and antagonist on rat learning and memory. Neuropharmacology 39: 2017-2027.
25. Marchetti E, Jacquet M, Jeltsch H, Migliorati M, Nivet E, et al. (2008) Complete recovery of olfactory associative learning by activation of 5-HT4 receptors after dentate granule cell damage in rats. Neurobiol Learn Mem 90: 185-191.
26. Meneses A, (2007) Stimulation of 5-HT1A, 5-HT1B, 5-HT2A/2C, 5-HT3 and 5-HT4 receptors or 5-HT uptake inhibition: short- and long-term memory. Behav Brain Res 184: 81-90.
27. Orsetti M, Dellarole A, Ferri S, Ghi P, (2003) Acquisition, retention, and recall of memory after injection of RS67333, a 5-HT(4) receptor agonist, into the nucleus basalis magnocellularis of the rat. Learn Mem 10: 420-426.
28. Perez-Garcia G, Meneses A, (2008) Ex vivo study of 5-HT(1A) and 5-HT(7) receptor agonists and antagonists on cAMP accumulation during memory formation and amnesia. Behav Brain Res 195: 139-146.
29. Restivo L, Roman F, Dumuis A, Bockaert J, Marchetti E, et al. (2008) The promnesic effect of G-protein-coupled 5-HT4 receptors activation is mediated by a potentiation of learning-induced spine growth in the mouse hippocampus. Neuropsychopharmacology 33: 2427-2434.
30. Terry AV Jr, Buccafusco JJ, Jackson WJ, Prendergast MA, Fontana DJ, et al. (1998) Enhanced delayed matching performance in younger and older macaques administered the 5-HT4 receptor agonist, RS 17017. Psychopharmacology (Berl) 135: 407-415.
31. King MV, Marsden CA, Fone KC, (2008) A role for the 5-HT(1A), 5-HT4 and 5-HT6 receptors in learning and memory. Trends Pharmacol Sci 29: 482-492.
32. Egawa T, Mishima K, Matsumoto Y, 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.
33. 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.
34. Zhang HT, Zhao Y, Huang Y, Dorairaj NR, Chandler LJ, et al. (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.
35. Rutten K, Wallace TL, Works M, Prickaerts J, Blokland A, et al. (2011) Enhanced long-term depression and impaired reversal learning in phosphodiesterase 4B-knockout (PDE4B(-/-)) mice. Neuropharmacology 61: 138-147.
36. Burgin AB, Magnusson OT, Singh J, Witte P, Staker BL, et al. (2010) Design of phosphodiesterase 4D (PDE4D) allosteric modulators for enhancing cognition with improved safety. Nat Biotechnol 28: 63-70.
37. Li YF, Cheng YF, Huang Y, Conti M, Wilson SP, et al. (2011) Phosphodiesterase-4D knock-out and RNA interference-mediated knock-down enhance memory and increase hippocampal neurogenesis via increased cAMP signaling. J Neurosci 31: 172-183.
38. Randt CT, Judge ME, Bonnet KA, Quartermain D, (1982) Brain cyclic AMP and memory in mice. Pharmacol Biochem Behav 17: 677-680.
39. Gong B, Vitolo OV, Trinchese F, Liu S, Shelanski M, et al. (2004) Persistent improvement in synaptic and cognitive functions in an Alzheimer mouse model after rolipram treatment. J Clin Invest 114: 1624-1634.
40. Bourtchouladze R, Lidge R, Catapano R, Stanley J, Gossweiler S, et al. (2003) A mouse model of Rubinstein-Taybi syndrome: defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4. Proc Natl Acad Sci U S A 100: 10518-10522.
41. 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.
42. Rutten K, Van Donkelaar EL, Ferrington L, Blokland A, Bollen E, et al. (2009) Phosphodiesterase inhibitors enhance object memory independent of cerebral blood flow and glucose utilization in rats. Neuropsychopharmacology 34: 1914-1925.
43. Houslay MD, (2001) PDE4 cAMP-specific phosphodiesterases. Prog Nucleic Acid Res Mol Biol 69: 249-315.
44. Zhang HT, (2009) Cyclic AMP-specific phosphodiesterase-4 as a target for the development of antidepressant drugs. Curr Pharm Des 15: 1688-1698.
45. Hoffmann R, Baillie GS, MacKenzie SJ, Yarwood SJ, Houslay MD, (1999) The MAP kinase ERK2 inhibits the cyclic AMP-specific phosphodiesterase HSPDE4D3 by phosphorylating it at Ser579. EMBO J 18: 893-903.
46. Richter W, Day P, Agrawal R, Bruss MD, Granier S, et al. (2008) Signaling from beta1- and beta2-adrenergic receptors is defined by differential interactions with PDE4. EMBO J 27: 384-393.
47. van Donkelaar EL, Rutten K, Blokland A, Akkerman S, Steinbusch HW, et al. (2008) Phosphodiesterase 2 and 5 inhibition attenuates the object memory deficit induced by acute tryptophan depletion. Eur J Pharmacol 600: 98-104.
48. Zhao J, Harada N, Kurihara H, Nakagata N, Okajima K, (2010) Cilostazol improves cognitive function in mice by increasing the production of insulin-like growth factor-I in the hippocampus. Neuropharmacology 58: 774-783.
49. O'Donnell JM, Frith S, (1999) Behavioral effects of family-selective inhibitors of cyclic nucleotide phosphodiesterases. Pharmacol Biochem Behav 63: 185-192.
50. Edelson J, Stroshane R, Benziger DP, Cody R, Benotti J, et al. (1986) Pharmacokinetics of the bipyridines amrinone and milrinone. Circulation 73: III145-152.
51. Lindsay CA, Barton P, Lawless S, Kitchen L, Zorka A, et al. (1998) Pharmacokinetics and pharmacodynamics of milrinone lactate in pediatric patients with septic shock. J Pediatr 132: 329-334.
52. 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.
53. Feschenko MS, Stevenson E, Nairn AC, Sweadner KJ, (2002) A novel cAMP-stimulated pathway in protein phosphatase 2A activation. J Pharmacol Exp Ther 302: 111-118.
54. Moon EY, Lerner A, (2003) PDE4 inhibitors activate a mitochondrial apoptotic pathway in chronic lymphocytic leukemia cells that is regulated by protein phosphatase 2A. Blood 101: 4122-4130.
55. Pullar CE, Grahn JC, Liu W, Isseroff RR, (2006) Beta2-adrenergic receptor activation delays wound healing. FASEB J 20: 76-86.
56. Oliver CJ, Shenolikar S, (1998) Physiologic importance of protein phosphatase inhibitors. Front Biosci 3: D961-972.
57. Resjo S, Oknianska A, Zolnierowicz S, Manganiello V, Degerman E, (1999) Phosphorylation and activation of phosphodiesterase type 3B (PDE3B) in adipocytes in response to serine/threonine phosphatase inhibitors: deactivation of PDE3B in vitro by protein phosphatase type 2A. Biochem J 341 (Pt 3): 839-845.
58. Levallet G, Levallet J, Bonnamy PJ, (2008) FSH-induced phosphoprotein phosphatase 2A-mediated deactivation of particulate phosphodiesterase-4 activities is abolished after alteration in proteoglycan synthesis in immature rat Sertoli cells. J Endocrinol 197: 45-54.
59. Desjardins S, Cauchy MJ, (1995) Comparative cardiac effects of milrinone and sodium nitroprusside in conscious rats. Drug Chem Toxicol 18: 43-59.
60. 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.
61. Silvestre JS, Fernandez AG, Palacios JM, (1999) Effects of rolipram on the elevated plus-maze test in rats: a preliminary study. J Psychopharmacol 13: 274-277.
62. Sik A, van Nieuwehuyzen P, Prickaerts J, Blokland A, (2003) Performance of different mouse strains in an object recognition task. Behav Brain Res 147: 49-54.
63. Rodriguez R, Molino B, Weiss HR, Scholz PM, (2004) Negative metabolic and coronary flow effects of decreases in cAMP and increases in cGMP in control and renal hypertensive rabbit hearts. J Appl Physiol 97: 439-445.
64. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
65. Thompson WJ, Appleman MM, (1971) Multiple cyclic nucleotide phosphodiesterase activities from rat brain. Biochemistry 10: 311-316.
66. Bussey TJ, Duck J, Muir JL, Aggleton JP, (2000) Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behav Brain Res 111: 187-202.
67. Ennaceur A, Neave N, Aggleton JP, (1997) Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 113: 509-519.
68. Hotte M, Thuault S, Lachaise F, Dineley KT, Hemmings HC, et al. (2006) D1 receptor modulation of memory retrieval performance is associated with changes in pCREB and pDARPP-32 in rat prefrontal cortex. Behav Brain Res 171: 127-133.
69. Parker A, Gaffan D, (1998) Interaction of frontal and perirhinal cortices in visual object recognition memory in monkeys. Eur J Neurosci 10: 3044-3057.
70. Warburton EC, Brown MW, (2010) Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory. Neuropsychologia 48: 2262-2272.
71. Bonaventure P, Hall H, Gommeren W, Cras P, Langlois X, et al. (2000) Mapping of serotonin 5-HT(4) receptor mRNA and ligand binding sites in the post-mortem human brain. Synapse 36: 35-46.
72. Eglen RM, Bonhaus DW, Johnson LG, Leung E, Clark RD, (1995) Pharmacological characterization of two novel and potent 5-HT4 receptor agonists, RS 67333 and RS 67506, in vitro and in vivo. Br J Pharmacol 115: 1387-1392.
73. Vilaro MT, Cortes R, Gerald C, Branchek TA, Palacios JM, et al. (1996) Localization of 5-HT4 receptor mRNA in rat brain by in situ hybridization histochemistry. Brain Res Mol Brain Res 43: 356-360.
74. Chini CC, Grande JP, Chini EN, Dousa TP, (1997) Compartmentalization of cAMP signaling in mesangial cells by phosphodiesterase isozymes PDE3 and PDE4. Regulation of superoxidation and mitogenesis. J Biol Chem 272: 9854-9859.
75. Dousa TP, (1998) Signaling role of PDE isozymes in pathobiology of glomerular mesangial cells. Studies in vitro and in vivo. Cell Biochem Biophys 29: 19-34.
76. Dousa TP, (1999) Cyclic-3′,5′-nucleotide phosphodiesterase isozymes in cell biology and pathophysiology of the kidney. Kidney Int 55: 29-62.
77. Matousovic K, Grande JP, Chini CC, Chini EN, Dousa TP, (1995) Inhibitors of cyclic nucleotide phosphodiesterase isozymes type-III and type-IV suppress mitogenesis of rat mesangial cells. J Clin Invest 96: 401-410.
78. Aujla H, Beninger RJ, (2001) Hippocampal-prefrontocortical circuits: PKA inhibition in the prefrontal cortex impairs delayed nonmatching in the radial maze in rats. Behav Neurosci 115: 1204-1211.
79. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, et al. (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88: 615-626.
80. Frankland PW, Bontempi B, (2005) The organization of recent and remote memories. Nat Rev Neurosci 6: 119-130.
81. Kelly MP, Cheung YF, Favilla C, Siegel SJ, Kanes SJ, et al. (2008) Constitutive activation of the G-protein subunit Galphas within forebrain neurons causes PKA-dependent alterations in fear conditioning and cortical Arc mRNA expression. Learn Mem 15: 75-83.
82. 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.
83. Rutten K, Basile JL, Prickaerts J, Blokland A, Vivian JA, (2008) Selective PDE inhibitors rolipram and sildenafil improve object retrieval performance in adult cynomolgus macaques. Psychopharmacology (Berl) 196: 643-648.
84. Dodge-Kafka KL, Bauman A, Mayer N, Henson E, Heredia L, et al. (2010) cAMP-stimulated protein phosphatase 2A activity associated with muscle A kinase-anchoring protein (mAKAP) signaling complexes inhibits the phosphorylation and activity of the cAMP-specific phosphodiesterase PDE4D3. J Biol Chem 285: 11078-11086.
85. Besheer J, Jensen HC, Bevins RA, (1999) Dopamine antagonism in a novel-object recognition and a novel-object place conditioning preparation with rats. Behav Brain Res 103: 35-44.
86. Fischmeister R, Castro LR, Abi-Gerges A, Rochais F, Jurevicius J, et al. (2006) Compartmentation of cyclic nucleotide signaling in the heart: the role of cyclic nucleotide phosphodiesterases. Circ Res 99: 816-828.
87. Xiang Y, Naro F, Zoudilova M, Jin SL, Conti M, et al. (2005) Phosphodiesterase 4D is required for beta2 adrenoceptor subtype-specific signaling in cardiac myocytes. Proc Natl Acad Sci U S A 102: 909-914.
88. Zaccolo M, Pozzan T, (2002) Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295: 1711-1715.
89. Cong M, Perry SJ, Lin FT, Fraser ID, Hu LA, et al. (2001) Regulation of membrane targeting of the G protein-coupled receptor kinase 2 by protein kinase A and its anchoring protein AKAP79. J Biol Chem 276: 15192-15199.
90. Baillie GS, Sood A, McPhee I, Gall I, Perry SJ, et al. (2003) beta-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc Natl Acad Sci U S A 100: 940-945.
91. Li X, Huston E, Lynch MJ, Houslay MD, Baillie GS, (2006) Phosphodiesterase-4 influences the PKA phosphorylation status and membrane translocation of G-protein receptor kinase 2 (GRK2) in HEK-293beta2 cells and cardiac myocytes. Biochem J 394: 427-435.
92. Xin W, Tran TM, Richter W, Clark RB, Rich TC, (2008) Roles of GRK and PDE4 activities in the regulation of beta2 adrenergic signaling. J Gen Physiol 131: 349-364.
93. Janssens V, Goris J, (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353: 417-439.
94. Sim AT, Ludowyke RI, Verrills NM, (2006) Mast cell function: regulation of degranulation by serine/threonine phosphatases. Pharmacol Ther 112: 425-439.
95. Huang Z, Ducharme Y, Macdonald D, Robichaud A, (2001) The next generation of PDE4 inhibitors. Curr Opin Chem Biol 5: 432-438.
96. Lugnier C, (2006) Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol Ther 109: 366-398.
97. Maurice DH, Palmer D, Tilley DG, Dunkerley HA, Netherton SJ, et al. (2003) Cyclic nucleotide phosphodiesterase activity, expression, and targeting in cells of the cardiovascular system. Mol Pharmacol 64: 533-546.
98. Zamah AM, Delahunty M, Luttrell LM, Lefkowitz RJ, (2002) Protein kinase A-mediated phosphorylation of the beta 2-adrenergic receptor regulates its coupling to Gs and Gi. Demonstration in a reconstituted system. J Biol Chem 277: 31249-31256.
99. Houslay MD, Baillie GS, (2003) The role of ERK2 docking and phosphorylation of PDE4 cAMP phosphodiesterase isoforms in mediating cross-talk between the cAMP and ERK signalling pathways. Biochem Soc Trans 31: 1186-1190.