Acute administration of vinpocetine, a phosphodiesterase type 1 inhibitor, ameliorates hyperactivity in a mice model of fetal alcohol spectrum disorder

Drug and Alcohol Dependence

Volumn 119, Issue 1-2, 2011, Pages 81-87

  Nunes, Fernanda ^a   Ferreira Rosa, Kélvia ^a   Pereira, Maurício dos S ^b   Kubrusly, Regina C ^b   Manhães, Alex C ^a   Abreu Villaça, Yael ^a   Filgueiras, Cláudio C ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

Author keywords

Alcohol abuse; Alcoholism; Ethanol; Hyperactivity disorder; Type 1 phosphodiesterase

Indexed keywords

ALCOHOL; CYCLIC AMP; SODIUM CHLORIDE; VINPOCETINE;

ACUTE DRUG ADMINISTRATION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFICACY; DRUG SAFETY; ENVIRONMENTAL EXPOSURE; FETAL ALCOHOL SYNDROME; HIPPOCAMPUS; HYPERACTIVITY; LOCOMOTION; MOUSE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURVIVAL RATE; TREATMENT RESPONSE; WEIGHT GAIN;

ALCOHOL DRINKING; ANIMALS; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CYCLIC AMP; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; DRUG EVALUATION, PRECLINICAL; ETHANOL; FEMALE; FETAL ALCOHOL SYNDROME; HUMANS; MALE; MICE; MOTOR ACTIVITY; PHOSPHODIESTERASE INHIBITORS; PREGNANCY; PREGNANCY COMPLICATIONS; SINGLE-BLIND METHOD; SURVIVAL RATE; VINCA ALKALOIDS; WEIGHT GAIN;

ANIMALIA; MUS; RODENTIA;

EID: 80054991388     PISSN: 03768716     EISSN: 18790046     Source Type: Journal    
DOI: 10.1016/j.drugalcdep.2011.05.024     Document Type: Article

References (78)

1. Banaschewski T., Becker K., Scherag S., Franke B., Coghill D. Molecular genetics of attention-deficit/hyperactivity disorder: an overview. Eur. Child Adolesc. Psychiatry 2010, 19:237-257.
2. Bandeira F., Lent R., Herculano-Houzel S. Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14108-14113.
3. Bhatara V., Loudenberg R., Ellis R. Association of attention deficit hyperactivity disorder and gestational alcohol exposure: an exploratory study. J. Atten. Disord. 2006, 9:515-522.
4. Burd L., Klug M.G., Martsolf J.T., Kerbeshian J. Fetal alcohol syndrome: neuropsychiatric phenomics. Neurotoxicol. Teratol. 2003, 25:697-705.
5. Conway S., Garbouzova Y. Effect of fetal alcohol exposure on postnatal pituitary adenosine 3',5'-cyclic phosphate content and growth hormone release. Alcohol. Clin. Exp. Res. 1996, 20:1212-1220.
6. de Mello M.C., Ventura A.L., Paes de C.R., Klein W.L., de Mello F.G. Regulation of dopamine- and adenosine-dependent adenylate cyclase systems of chicken embryo retina cells in culture. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:5708-5712.
7. DeNoble V.J. Vinpocetine enhances retrieval of a step-through passive avoidance response in rats. Pharmacol. Biochem. Behav. 1987, 26:183-186.
8. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Hum. Dev. 1979, 3:79-83.
9. Doig J., McLennan J.D., Gibbard W.B. Medication effects on symptoms of attention-deficit/hyperactivity disorder in children with fetal alcohol spectrum disorder. J. Child Adolesc. Psychopharmacol. 2008, 18:365-371.
10. Eckardt M.J., File S.E., Gessa G.L., Grant K.A., Guerri C., Hoffman P.L., Kalant H., Koob G.F., Li T.K., Tabakoff B. Effects of moderate alcohol consumption on the central nervous system. Alcohol. Clin. Exp. Res. 1998, 22:998-1040.
11. Filgueiras C.C., Krahe T.E., Medina A.E. Phosphodiesterase type 1 inhibition improves learning in rats exposed to alcohol during the third trimester equivalent of human gestation. Neurosci. Lett. 2010, 473:202-207.
12. Filgueiras C.C., Ribeiro-Carvalho A., Nunes F., Abreu-Villaça Y., Manhães A.C. Early ethanol exposure in mice increases laterality of rotational side preference in the free-swimming test. Pharmacol. Biochem. Behav. 2009, 93:148-154.
13. Fryer S.L., McGee C.L., Matt G.E., Riley E.P., Mattson S.N. Evaluation of psychopathological conditions in children with heavy prenatal alcohol exposure. Pediatrics 2007, 119:e733-e741.
14. Gabryel B., Adamek M., Pudelko A., Malecki A., Trzeciak H.I. Piracetam and vinpocetine exert cytoprotective activity and prevent apoptosis of astrocytes in vitro in hypoxia and reoxygenation. Neurotoxicology 2002, 23:19-31.
15. Gil-Mohapel J., Boehme F., Kainer L., Christie B.R. Hippocampal cell loss and neurogenesis after fetal alcohol exposure: insights from different rodent models. Brain Res. Rev. 2010, 64:283-303.
16. Gilman A.G. A protein binding assay for adenosine 3':5'-cyclic monophosphate. Proc. Natl. Acad. Sci. U.S.A. 1970, 67:305-312.
17. Goodlett C.R., Horn K.H., Zhou F.C. Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Exp. Biol. Med. (Maywood) 2005, 230:394-406.
18. Goto Y., Grace A.A. The dopamine system and the pathophysiology of schizophrenia: a basic science perspective. Int. Rev. Neurobiol. 2007, 78:41-68.
19. Gurden H., Takita M., Jay T.M. Essential role of D1 but not D2 receptors in the NMDA receptor-dependent long-term potentiation at hippocampal-prefrontal cortex synapses in vivo. J. Neurosci. 2000, 20:RC106.
20. Gurden H., Tassin J.P., Jay T.M. Integrity of the mesocortical dopaminergic system is necessary for complete expression of in vivo hippocampal-prefrontal cortex long-term potentiation. Neuroscience 1999, 94:1019-1027.
21. Han J.Y., Joo Y., Kim Y.S., Lee Y.K., Kim H.J., Cho G.J., Choi W.S., Kang S.S. Ethanol induces cell death by activating caspase-3 in the rat cerebral cortex. Mol. Cells 2005, 20:189-195.
22. Ieraci A., Herrera D.G. Nicotinamide protects against ethanol-induced apoptotic neurodegeneration in the developing mouse brain. PLoS Med. 2006, 3:e101.
23. Ikonomidou C., Bittigau P., Ishimaru M.J., Wozniak D.F., Koch C., Genz K., Price M.T., Stefovska V., Horster F., Tenkova T., Dikranian K., Olney J.W. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 2000, 287:1056-1060.
24. Jensen V., Rinholm J.E., Johansen T.J., Medin T., Storm-Mathisen J., Sagvolden T., Hvalby O., Bergersen L.H. N-methyl-d-aspartate receptor subunit dysfunction at hippocampal glutamatergic synapses in an animal model of attention-deficit/hyperactivity disorder. Neuroscience 2009, 158:353-364.
25. Kehr W., Debus G., Neumeister R. Effects of rolipram, a novel antidepressant, on monoamine metabolism in rat brain. J. Neural Transm. 1985, 63:1-12.
26. Kelly S.J., Day N., Streissguth A.P. Effects of prenatal alcohol exposure on social behavior in humans and other species. Neurotoxicol. Teratol. 2000, 22:143-149.
27. Kelly S.J., Pierce D.R., West J.R. Microencephaly and hyperactivity in adult rats can be induced by neonatal exposure to high blood alcohol concentrations. Exp. Neurol. 1987, 96:580-593.
28. Kidd P.M. A review of nutrients and botanicals in the integrative management of cognitive dysfunction. Altern. Med. Rev. 1999, 4:144-161.
29. King J.A., Barkley R.A., Delville Y., Ferris C.F. Early androgen treatment decreases cognitive function and catecholamine innervation in an animal model of ADHD. Behav. Brain Res. 2000, 107:35-43.
30. Kodituwakku P., Coriale G., Fiorentino D., Aragon A.S., Kalberg W.O., Buckley D., Gossage J.P., Ceccanti M., May P.A. Neurobehavioral characteristics of children with fetal alcohol spectrum disorders in communities from Italy: preliminary results. Alcohol. Clin. Exp. Res. 2006, 30:1551-1561.
31. Kodituwakku P.W. Neurocognitive profile in children with fetal alcohol spectrum disorders. Dev. Disabil. Res Rev. 2009, 15:218-224.
32. Krahe T.E., Wang W., Medina A.E. Phosphodiesterase inhibition increases CREB phosphorylation and restores orientation selectivity in a model of fetal alcohol spectrum disorders. PLoS One 2009, 4:e6643.
33. Kumada T., Komuro Y., Li Y., Hu T., Wang Z., Littner Y., Komuro H. Inhibition of cerebellar granule cell turning by alcohol. Neuroscience 2010, 170:1328-1344.
34. Lalonde R., Strazielle C. The relation between open-field and emergence tests in a hyperactive mouse model. Neuropharmacology 2009, 57:722-724.
35. Lendvai B., Zelles T., Rozsa B., Vizi E.S. A vinca alkaloid enhances morphological dynamics of dendritic spines of neocortical layer 2/3 pyramidal cells. Brain Res. Bull. 2003, 59:257-260.
36. Lewis-Tuffin L.J., Quinn P.G., Chikaraishi D.M. Tyrosine hydroxylase transcription depends primarily on cAMP response element activity, regardless of the type of inducing stimulus. Mol. Cell. Neurosci. 2004, 25:536-547.
37. Lugnier C. Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol. Ther. 2006, 109:366-398.
38. Maas J.W., Indacochea R.A., Muglia L.M., Tran T.T., Vogt S.K., West T., Benz A., Shute A.A., Holtzman D.M., Mennerick S., Olney J.W., Muglia L.J. Calcium-stimulated adenylyl cyclases modulate ethanol-induced neurodegeneration in the neonatal brain. J. Neurosci. 2005, 25:2376-2385.
39. Maier S.E., West J.R. Drinking patterns and alcohol-related birth defects. Alcohol Res. Health 2001, 25:168-174.
40. Matsuzawa H., Nirenberg M. Receptor-mediated shifts in cGMP and cAMP levels in neuroblastoma cells. Proc. Natl. Acad. Sci. U.S.A. 1975, 72:3472-3476.
41. May P.A., Gossage J.P., Kalberg W.O., Robinson L.K., Buckley D., Manning M., Hoyme H.E. Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies. Dev. Disabil. Res. Rev. 2009, 15:176-192.
42. Medina A.E. Fetal alcohol spectrum disorders and abnormal neuronal plasticity. Neuroscientist 2011, 17:274-287.
43. Medina A.E. Therapeutic utility of phosphodiesterase type I inhibitors in neurological conditions. Front. Neurosci. 2011, 5:21.
44. Medina A.E., Krahe T.E. Neocortical plasticity deficits in fetal alcohol spectrum disorders: lessons from barrel and visual cortex. J. Neurosci. Res. 2008, 86:256-263.
45. Medina A.E., Krahe T.E., Ramoa A.S. Restoration of neuronal plasticity by a phosphodiesterase type 1 inhibitor in a model of fetal alcohol exposure. J. Neurosci. 2006, 26:1057-1060.
46. Melcer T., Gonzalez D., Barron S., Riley E.P. Hyperactivity in preweanling rats following postnatal alcohol exposure. Alcohol 1994, 11:41-45.
47. Missale C., Nash S.R., Robinson S.W., Jaber M., Caron M.G. Dopamine receptors: from structure to function. Physiol. Rev. 1998, 78:189-225.
48. Molnar P., Gaal L., Horvath C. The impairment of long-term potentiation in rats with medial septal lesion and its restoration by cognition enhancers. Neurobiology (Bp.) 1994, 2:255-266.
49. Navakkode S., Sajikumar S., Frey J.U. The type IV-specific phosphodiesterase inhibitor rolipram and its effect on hippocampal long-term potentiation and synaptic tagging. J. Neurosci. 2004, 24:7740-7744.
50. O'Malley K.D., Nanson J. Clinical implications of a link between fetal alcohol spectrum disorder and attention-deficit hyperactivity disorder. Can. J. Psychiatry 2002, 47:349-354.
51. Olney J.W., Tenkova T., Dikranian K., Qin Y.Q., Labruyere J., Ikonomidou C. Ethanol-induced apoptotic neurodegeneration in the developing C57BL/6 mouse brain. Brain Res. Dev. Brain Res. 2002, 133:115-126.
52. Olney J.W., Wozniak D.F., Jevtovic-Todorovic V., Farber N.B., Bittigau P., Ikonomidou C. Drug-induced apoptotic neurodegeneration in the developing brain. Brain Pathol. 2002, 12:488-498.
53. Paine T.A., Neve R.L., Carlezon W.A. Attention deficits and hyperactivity following inhibition of cAMP-dependent protein kinase within the medial prefrontal cortex of rats. Neuropsychopharmacology 2009, 34:2143-2155.
54. Parkitna J.R., Bilbao A., Rieker C., Engblom D., Piechota M., Nordheim A., Spanagel R., Schutz G. Loss of the serum response factor in the dopamine system leads to hyperactivity. FASEB J. 2010, 24:2427-2435.
55. Pascoli V., Valjent E., Corbille A.G., Corvol J.C., Tassin J.P., Girault J.A., Herve D. cAMP and extracellular signal-regulated kinase signaling in response to d-amphetamine and methylphenidate in the prefrontal cortex in vivo: role of beta 1-adrenoceptors. Mol. Pharmacol. 2005, 68:421-429.
56. Paul A.P., Pohl-Guimaraes F., Krahe T.E., Filgueiras C.C., Lantz C.L., Colello R.J., Wang W., Medina A.E. Overexpression of serum response factor restores ocular dominance plasticity in a model of fetal alcohol spectrum disorders. J. Neurosci. 2010, 30:2513-2520.
57. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 2003, 463:3-33.
58. Puglia M.P., Valenzuela C.F. Ethanol acutely inhibits ionotropic glutamate receptor-mediated responses and long-term potentiation in the developing CA1 hippocampus. Alcohol. Clin. Exp. Res. 2010, 34:594-606.
59. Puzzo D., Sapienza S., Arancio O., Palmeri A. Role of phosphodiesterase 5 in synaptic plasticity and memory. Neuropsychiatr. Dis. Treat. 2008, 4:371-387.
60. Rapoport J.L., Gogtay N. Brain neuroplasticity in healthy, hyperactive and psychotic children: insights from neuroimaging. Neuropsychopharmacology 2008, 33:181-197.
61. Riley E.P., Barron S., Melcer T., Gonzalez D. Alterations in activity following alcohol administration during the third trimester equivalent in P and NP rats. Alcohol. Clin. Exp. Res. 1993, 17:1240-1246.
62. Riley E.P., McGee C.L. Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Exp. Biol. Med. (Maywood) 2005, 230:357-365.
63. Roberson R., Cameroni I., Toso L., Abebe D., Bissel S., Spong C.Y. Alterations in phosphorylated cyclic adenosine monophosphate response element of binding protein activity: a pathway for fetal alcohol syndrome-related neurotoxicity. Am. J. Obstet. Gynecol. 2009, 200:193-195.
64. Rosdy B., Balazs M., Szporny L. Biochemical effects of ethyl apovincaminate. Arzneimittelforschung 1976, 26:1923-1926.
65. Russell V.A. Dopamine hypofunction possibly results from a defect in glutamate-stimulated release of dopamine in the nucleus accumbens shell of a rat model for attention deficit hyperactivity disorder-the spontaneously hypertensive rat. Neurosci. Biobehav. Rev. 2003, 27:671-682.
66. Russell V.A. Neurobiology of animal models of attention-deficit hyperactivity disorder. J. Neurosci. Methods 2007, 161:185-198.
67. Russell V.A., Oades R.D., Tannock R., Killeen P.R., Auerbach J.G., Johansen E.B., Sagvolden T. Response variability in attention-deficit/hyperactivity disorder: a neuronal and glial energetics hypothesis. Behav. Brain Funct. 2006, 2:30.
68. Sagvolden T., Russell V.A., Aase H., Johansen E.B., Farshbaf M. Rodent models of attention-deficit/hyperactivity disorder. Biol. Psychiatry 2005, 57:1239-1247.
69. Schoffelmeer A.N., Wardeh G., Mulder A.H. Cyclic AMP facilitates the electrically evoked release of radiolabelled noradrenaline, dopamine and 5-hydroxytryptamine from rat brain slices. Naunyn Schmiedebergs Arch. Pharmacol. 1985, 330:74-76.
70. Slawecki C.J., Thomas J.D., Riley E.P., Ehlers C.L. Neurophysiologic consequences of neonatal ethanol exposure in the rat. Alcohol 2004, 34:187-196.
71. Thomas J.D., Biane J.S., O'Bryan K.A., O'Neill T.M., Dominguez H.D. Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats. Behav. Neurosci. 2007, 121:120-130.
72. Thomas J.D., Fleming And S.L., Riley E.P. MK-801 can exacerbate or attenuate behavioral alterations associated with neonatal alcohol exposure in the rat, depending on the timing of administration. Alcohol. Clin. Exp. Res. 2001, 25:764-773.
73. Tsai S.J. Attention-deficit hyperactivity disorder may be associated with decreased central brain-derived neurotrophic factor activity: clinical and therapeutic implications. Med. Hypotheses 2007, 68:896-899.
74. Wainwright P.E. Issues of design and analysis relating to the use of multiparous species in developmental nutritional studies. J. Nutr. 1998, 128:661-663.
75. Wozniak D.F., Hartman R.E., Boyle M.P., Vogt S.K., Brooks A.R., Tenkova T., Young C., Olney J.W., Muglia L.J. Apoptotic neurodegeneration induced by ethanol in neonatal mice is associated with profound learning/memory deficits in juveniles followed by progressive functional recovery in adults. Neurobiol. Dis. 2004, 17:403-414.
76. Wu L., Zhao Q., Zhu X., Peng M., Jia C., Wu W., Zheng J., Wu X.Z. A novel function of microRNA let-7d in regulation of galectin-3 expression in attention deficit hyperactivity disorder rat brain. Brain Pathol. 2010, 20:1042-1054.
77. Yamashita N., Miyashiro M., Baba J., Sawa A. Rolipram, a selective inhibitor of phosphodiesterase type 4, pronouncedly enhanced the forskolin-induced promotion of dopamine biosynthesis in primary cultured rat mesencephalic neurons. Jpn. J. Pharmacol. 1997, 75:91-95.
78. Zigmond R.E., Schwarzschild M.A., Rittenhouse A.R. Acute regulation of tyrosine hydroxylase by nerve activity and by neurotransmitters via phosphorylation. Annu. Rev. Neurosci. 1989, 12:415-461.