A phosphodiesterase inhibitor, cilomilast, enhances cAMP activity to restore conditioned odor preference memory after serotonergic depletion in the neonate rat

Neurobiology of Learning and Memory

Volumn 92, Issue 1, 2009, Pages 63-69

  McLean, John H ^a   Smith, Andrew ^a   Rogers, Stacey ^a   Clarke, Kimberley ^a   Darby King, Andrea ^a   Harley, Carolyn W ^b  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Adrenoceptor agonist; 5,7 Dihydroxytryptamine; cAMP; Isoproterenol; Memory; Neonate rat

Indexed keywords

BETA 1 ADRENERGIC RECEPTOR; CILOMILAST; CYCLIC AMP; ISOPRENALINE; PHOSPHODIESTERASE IV; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONING; ENZYME INHIBITION; FEMALE; LEARNING; LEARNING DISORDER; MALE; MEMORY; NEWBORN; NONHUMAN; ODOR; RAT; SEROTONIN RELEASE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CARBOXYLIC ACIDS; CONDITIONING (PSYCHOLOGY); CYCLIC AMP; FEMALE; IMMUNOENZYME TECHNIQUES; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; NITRILES; ODORS; OLFACTORY BULB; PHOSPHODIESTERASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; TIME FACTORS;

EID: 67349217908     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2009.02.003     Document Type: Article

References (56)

1. Barad M., Bourtchouladze R., Winder D.G., Golan H., and Kandel E.R. Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proceedings of the National Academy of Sciences 95 (1998) 15020-15025
2. Bell J.D., and Brunton L.L. Multiple effects of phorbol esters on hormone-sensitive adenylate cyclase activity in S49 lymphoma cells. American Journal of Physiology 252 (1987) E783-E789
3. Berg K.A., Clarke W.P., Chen Y., Ebersole B.J., McKay R.D.G., and Maayani S. 5-Hydroxytryptamine type 2A receptors regulate cyclic AMP accumulation in a neuronal cell line by protein kinase C-dependent and calcium/calmodulin-dependent mechanisms. Molecular Pharmacology 45 (1994) 826-836
4. Bourtchouladze R., Lidge R., Catapano R., Stanley J., Gossweiler S., Romashko D., et al. A mouse model of Rubinstein-Taybi syndrome: Defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4. Proceedings of the National Academy of Sciences 100 (2003) 10518-10522
5. Choi E.J., Xia Z., and Storm D.R. Stimulation of the type III olfactory adenylyl cyclase by calcium and calmodulin. Biochemistry 31 (1992) 6492-6498
6. Cornea-Hébert V., Riad M., Wu C., Singh S.K., and Descarries L. Cellular and subcellular distribution of the serotonin 5-HT2A receptor in the central nervous system of adult rat. Journal of Comparative Neurology 409 (1999) 187-209
7. Cui W., Smith A., Darby-King A., Harley C.W., and McLean J.H. A temporal-specific and transient cAMP increase characterizes odorant classical conditioning. Learning and Memory 14 (2007) 126-133
8. De Blasi A. Advances on beta-adrenergic receptors: Molecular structure and functional regulation. American Journal of Hypertension 2 (1989) 252S-256S
9. Egawa T., Mishima K., Matsumoto Y., Iwasaki K., Iwasaki K., and Fujiwara M. Rolipram and its optical isomers, phosphodiesterase 4 inhibitors, attenuated the scopolamine-induced impairments of learning and memory in rats. Japanese Journal of Pharmacology 75 (1997) 275-281
10. Gereau R.W., and Conn P.J. A cyclic AMP-dependent form of associative synaptic plasticity induced by coactivation of beta-adrenergic receptors and metabotropic glutamate receptors in rat hippocampus. Journal of Neuroscience 14 (1994) 3310-3318
11. Gomez C., Brinon J.G., Colado M.I., Orio L., Vidal M., Barbado M.V., et al. Differential effects of unilateral olfactory deprivation on noradrenergic and cholinergic systems in the main olfactory bulb of the rat. Neuroscience (2006)
12. Gomez C., Brinon J.G., Orio L., Colado M.I., Lawrence A.J., Zhou F.C., et al. Changes in the serotonergic system in the main olfactory bulb of rats unilaterally deprived from birth to adulthood. Journal of Neurochemistry 100 (2007) 924-938
13. Harley C.W., Darby-King A., McCann J., and McLean J.H. Beta1-adrenoceptor or alpha1-adrenoceptor activation initiates early odor preference learning in rat pups: Support for the mitral cell/cAMP model of odor preference learning. Learning and Memory 13 (2006) 8-13
14. Imanishi T., Sawa A., Ichimaru Y., Miyashiro M., Kato S., Yamamoto T., et al. Ameliorating effects of rolipram on experimentally induced impairments of learning and memory in rodents. European Journal of Pharmacology 321 (1997) 273-278
15. Kandel E.R., Schwartz J.H., and Jessel T.M. Principles of neural science. 4th ed. (2000), McGraw-Hill, New York
16. Katada T., Gilman A.G., Watanabe Y., Bauer S., and Jakobs K.H. Protein kinase C phosphorylates the inhibitory guanine-nucleotide-binding regulatory component and apparently suppresses its function in hormonal inhibition of adenylate cyclase. European Journal of Biochemistry 151 (1985) 431-437
17. Kramer H.K., Poblete J.C., and Azmitia E.C. Activation of protein kinase C (PKC) by 3,4- methylenedioxymethamphetamine (MDMA) occurs through the stimulation of serotonin receptors and transporter. Neuropsychopharmacology 17 (1997) 117-129
18. Langdon P.E., Harley C.W., and McLean J.H. Increased β adrenoceptor activation overcomes conditioned olfactory learning deficits induced by serotonin depletion. Developmental Brain Research 102 (1997) 291-293
19. Le Jeune H., Aubert I., Jourdan F., and Quirion R. Comparative laminar distribution of various autoradiographic cholinergic markers in adult rat main olfactory bulb. Journal of Chemical Neuroanatomy 9 (1995) 99-112
20. Liu C., Crandes P., Matute C., Cuenod M., and Streit P. Glutamate-like immunoreactivity revealed in rat olfactory bulb, hippocampus and cerebellum by monoclonal antibody and sensitive staining method. Histochemistry 90 (1989) 427-445
21. Liu Y., Jia W., Strosberg A.D., and Cynader M. Development and regulation of beta adrenergic receptors in kitten visual cortex: An immunocytochemical and autoradiographic study. Brain Research 632 (1993) 274-286
22. McLean J.H., and Darby-King A. Lack of evidence for serotonergic effect on the cellular development of the olfactory bulb in the postnatal rat. Brain Research Bulletin 34 (1994) 249-259
23. McLean J.H., Darby-King A., and Harley C.W. Potentiation and prolongation of long-term odor memory in neonate rats using a phosphodiesterase inhibitor. Neuroscience 135 (2005) 329-334
24. 2 receptor involvement in conditioned olfactory learning in the neonate rat pup. Behavioral Neuroscience 110 (1996) 1426-1434
25. McLean J.H., Darby-King A., Sullivan R.M., and King S.R. Serotonergic influence on olfactory learning in the neonate rat. Behavioral and Neural Biology 60 (1993) 152-162
26. McLean J.H., and Shipley M.T. Serotonergic afferents to the rat olfactory bulb: I Origins and laminar specificity of serotonergic inputs in the adult rat. Journal of Neuroscience 7 (1987) 3016-3028
27. McLean J.H., and Shipley M.T. Serotonergic afferents to the rat olfactory bulb: II. Changes in fiber distribution during development. Journal of Neuroscience 7 (1987) 3029-3039
28. McLean J.H., and Shipley M.T. Postnatal development of the noradrenergic projection from locus coeruleus to the olfactory bulb in the rat. Journal of Comparative Neurology 304 (1991) 467-477
29. McLean J.H., Shipley M.T., Nickell W.T., Aston-Jones G., and Reyher C.K. Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat. Journal of Comparative Neurology 285 (1989) 339-349
30. Mobley P.L., and Sulser F. Norepinephrine stimulated cyclic AMP accumulation in rat limbic forebrain slices: Partial mediation by a subpopulation of receptors with neither alpha nor beta characteristics. European Journal of Pharmacology 60 (1979) 221-227
31. Morin D., Sapena R., Zini R., and Tillement J.-P. Serotonin enhances the β-adrenergic response in rat brain cortical slices. European Journal of Pharmacology 225 (1992) 273-274
32. Moudy A.M., and Schwartzkroin P.A. Pyramidal neurons in immature rat hippocampus are sensitive to beta-adrenergic agents. Brain Research, Developmental Brain Research 67 (1992) 57-66
33. Nakahara M., Shimozawa M., Nakamura Y., Irino Y., Morita M., Kudo Y., et al. A novel phospholipase C, PLC(eta)2, is a neuron-specific isozyme. European Journal of Biochemistry 280 (2005) 29128-29134
34. Nakamura S., Kimura F., and Sakaguchi T. Postnatal development of electrical activity in the locus ceruleus. Journal of Neurophysiology 58 (1987) 510-524
35. Price T.L., Darby-King A., Harley C.W., and McLean J.H. Serotonin plays a permissive role in conditioned olfactory learning induced by norepinephrine in the neonate rat. Behavioral Neuroscience 112 (1998) 1430-1437
36. Ramos B.P., Birnbaum S.G., Lindenmayer I., Newton S.S., Duman R.S., and Arnsten A.F. Dysregulation of protein kinase A signaling in the aged prefrontal cortex: New strategy for treating age-related cognitive decline. Neuron 40 (2003) 835-845
37. Randt C.T., Judge M.E., Bonnet K.A., and Quartermain D. Brain cyclic AMP and memory in mice. Pharmacology Biochemistry and Behaviour 17 (1982) 677-680
38. Rangel S., and Leon M. Early odor preference training increases olfactory bulb norepinephrine. Developmental Brain Research 85 (1995) 187-191
39. Romano A., Delorenzi A., Pedreira M.E., Tomsic D., and Maldonado H. Acute administration of a permeant analog of cAMP and a phosphodiesterase inhibitor improve long-term habituation in the crab Chasmagnathus. Behavioural Brain Research 75 (1996) 119-125
40. Rutten K., Lieben C., Smits L., and Blokland A. The PDE4 inhibitor rolipram reverses object memory impairment induced by acute tryptophan depletion in the rat. Psychopharmacology (Berl) 192 (2007) 275-282
41. Sara S.J., Vankov A., and Hervé A. Locus coeruleus-evoked responses in behaving rats: A clue to the role of noradrenaline in memory. Brain Research Bulletin 35 (1994) 457-465
42. Sibley D.R., Jeffs R.A., Daniel K., Nambi P., and Lefkowitz R.J. Phorbol diester treatment promotes enhanced adenylate cyclase activity in frog erythrocytes. Archives of Biochemistry Biophysics 244 (1986) 373-381
43. Sibley D.R., Nambi P., Peters J.R., and Lefkowitz R.J. Phorbol diesters promote beta-adrenergic receptor phosphorylation and adenylate cyclase desensitization in duck erythrocytes. Biochemical and Biophysical Research Communications 121 (1984) 973-979
44. Sossin W.S., and Schwartz J.H. Selective activation of Ca(2+)-activated PKCs in Aplysia neurons by 5-HT. Journal of Neuroscience 12 (1992) 1160-1168
45. Sullivan R.M., McGaugh J.L., and Leon M. Norepinephrine-induced plasticity and one-trial olfactory learning in neonatal rats. Developmental Brain Research 60 (1991) 219-228
46. Sullivan R.M., Stackenwalt G., Nasr F., Lemon C., and Wilson D.A. Association of an odor with activation of olfactory bulb noradrenergic beta-receptors or locus coeruleus stimulation is sufficient to produce learned approach responses to that odor in neonatal rats. Behavioral Neuroscience 114 (2000) 957-962
47. Thompson B.E., Sachs B.D., Kantak K.M., and Cherry J.A. The Type IV phosphodiesterase inhibitor rolipram interferes with drug-induced conditioned place preference but not immediate early gene induction in mice. European Journal of Neuroscience 19 (2004) 2561-2568
48. Villiger J.W., and Dunn A.J. Phosphodiesterase inhibitors facilitate memory for passive avoidance conditioning. Behavioral and Neural Biology 31 (1981) 354-359
49. Weishaar R.E., Cain M.H., and Bristol J.A. A new generation of phosphodiesterase inhibitors: Multiple molecular forms of phosphodiesterase and the potential for drug selectivity. Journal of Medicinal Chemistry 28 (1985) 537-545
50. Whitaker-Azmitia P.M. Serotonin and brain development: Role in human developmental diseases. Brain Research Bulletin 56 (2001) 479-485
51. Whitaker-Azmitia P.M. Behavioral and cellular consequences of increasing serotonergic activity during brain development: A role in autism?. International Journal of Developmental Neuroscience 23 (2005) 75-83
52. Yoshimasa T., Sibley D.R., Bouvier M., Lefkowitz R.J., and Caron M.G. Cross-talk between cellular signalling pathways suggested by phorbol-ester-induced adenylate cyclase phosphorylation. Nature 327 (1987) 67-70
53. Yoshimasa T., Sibley D.R., Bouvier M., Lefkowitz R.J., and Caron M.G. Cross-talk between cellular signalling pathways suggested by phorbol-ester-induced adenylate cyclase phosphorylation. Nature 327 (1987) 67-70
54. Yuan Q., Harley C.W., Bruce A.J., Darby-King A., and McLean J.H. Isoproterenol increases CREB phosphorylation and olfactory nerve-evoked potentials in normal and 5-HT-depleted olfactory bulbs in rat pups only at doses that produce odor preference learning. Learning and Memory 7 (2000) 413-421
55. 2A receptor colocalization and cAMP coregulation: A new model of norepinephrine-induced learning in the olfactory bulb. Learning and Memory 10 (2003) 5-15
56. Zifa E., and Fillion G. 5-Hydroxytryptamine receptors. Pharmacology Reviews 44 3 (1992) 401-458