Impact of early life stress on alcohol consumption and on the short- and long-term responses to alcohol in adolescent female rats

Behavioural Brain Research

Volumn 221, Issue 1, 2011, Pages 43-49

  Van Waes, V ^a   Darnaudery M ^b   Marrocco, J ^a   Gruber, S H ^c   Talavera, E ^a   Mairesse, J ^a   Van Camp, G ^a   Casolla, B ^d   Nicoletti, F ^d,e   Mathe A A ^c   Maccari, S ^a   Morley Fletcher, S ^a  

^a UNIV LILLE   (France)

^b CNRS   (France)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e IRCCS NEUROMED   (Italy)

Author keywords

Adolescence; CRH; Early life stress; Ethanol; MGlu1 receptors; NPY

Indexed keywords

ALCOHOL; CORTICOTROPIN RELEASING FACTOR; METABOTROPIC RECEPTOR 1; NEUROPEPTIDE Y;

ADOLESCENT; ALCOHOL CONSUMPTION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN LEVEL; CHILD BEHAVIOR; CONTROLLED STUDY; DEPRESSION; EARLY LIFE STRESS; FEMALE; FORCED SWIMMING TEST; HIPPOCAMPUS; IMMOBILIZATION; IMMOBILIZATION STRESS; MALE; NONHUMAN; PERINATAL PERIOD; PRENATAL RESTRAINT STRESS; PRIORITY JOURNAL; RAT;

ALCOHOL DRINKING; ANIMALS; CHOICE BEHAVIOR; CORPUS STRIATUM; CORTICOTROPIN-RELEASING HORMONE; ETHANOL; FEMALE; HIPPOCAMPUS; IMMOBILITY RESPONSE, TONIC; MALE; NEUROPEPTIDE Y; PREFRONTAL CORTEX; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SOCIAL ISOLATION; STRESS, PHYSIOLOGICAL;

EID: 79952846631     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.02.033     Document Type: Article

References (75)

1. Danielsson A.K., Wennberg P., Tengström A., Romelsjö A. Adolescent alcohol use trajectories: predictors and subsequent problems. Addict Behav 2010, 35:848-852.
2. Saban A., Flisher A.J. The association between psychopathology and substance use in young people: a review of the literature. J Psychoactive Drugs 2010, 42:37-47.
3. Nestler E.J., Hyman S.E. Animal models of neuropsychiatric disorders. Nat Neurosci 2010, 13:1161-1169.
4. Krishnan V., Nestler E.J. Linking molecules to mood: new insight into the biology of depression. Am J Psychiatry 2010, 167:1305-1320.
5. Laucht M., Treutlein J., Schmid B., Blomeyer D., Becker K., Buchmann A.F., et al. Impact of psychosocial adversity on alcohol intake in young adults: moderation by the LL genotype of the serotonin transporter polymorphism. Biol Psychiatry 2009, 66:102-109.
6. Schäfer I., Teske L., Schulze-Thüsing J., Homann K., Reimer J., Haasen C., et al. Impact of childhood trauma on hypothalamus-pituitary-adrenal axis activity in alcohol-dependent patients. Eur Addict Res 2010, 16:108-114.
7. Huot R.L., Thrivikraman K.V., Meaney M.J., Plotsky P.M. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology 2001, 158:366-373.
8. Advani T., Hensler J.G., Koek W. Effect of early rearing conditions on alcohol drinking and 5-HT1A receptor function in C57BL/6J mice. Int J Neuropsychopharmacol 2007, 10:595-607.
9. Schuckit M.A., Tipp J.E., Bergman M., Reich W., Hesselbrock V.M., Smith T.L. Comparison of induced and independent major depressive disorders in 2,945 alcoholics. Am J Psychiatry 1997, 154:948-957.
10. Hasin D.S., Grant B.F. Major depression in 6050 former drinkers: association with past alcohol dependence. Arch Gen Psychiatry 2002, 59:794-800.
11. Darnaudery M., Maccari S. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 2008, 57:571-585.
12. Maccari S., Morley-Fletcher S. Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 2007, 32(Suppl. 1):S10-15.
13. Maccari S., Piazza P.V., Kabbaj M., Barbazanges A., Simon H., Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 1995, 15:110-116.
14. Dugovic C., Maccari S., Weibel L., Turek F.W., Van Reeth O. High corticosterone levels in prenatally stressed rats predict persistent paradoxical sleep alterations. J Neurosci 1999, 19:8656-8664.
15. Maccari S., Van Reeth O Circadian rhythms, effects of prenatal stress in rodents. Encyclopedia of Stress 2007, Elsevier. 2 ed.
16. Vallee M., Mayo W., Dellu F., Le Moal M., Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 1997, 17:2626-2636.
17. Zuena A.R., Mairesse J., Casolini P., Cinque C., Alema G.S., Morley-Fletcher S., et al. Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE 2008, 3:e2170.
18. Morley-Fletcher S., Darnaudery M., Koehl M., Casolini P., Van Reeth O., Maccari S. Prenatal stress in rats predicts immobility behavior in the forced swim test. Effects of a chronic treatment with tianeptine. Brain Res 2003, 989:246-251.
19. Morley-Fletcher S., Darnaudery M., Mocaer E., Froger N., Lanfumey L., Laviola G., et al. Chronic treatment with imipramine reverses immobility behaviour, hippocampal corticosteroid receptors and cortical 5-HT(1A) receptor mRNA in prenatally stressed rats. Neuropharmacology 2004, 47:841-847.
20. Alonso S.J., Castellano M.A., Quintero M., Navarro E. Action of antidepressant drugs on maternal stress-induced hypoactivity in female rats. Methods Find Exp Clin Pharmacol 1999, 21:291-295.
21. Deminiere J.M., Piazza P.V., Guegan G., Abrous N., Maccari S., Le Moal M., et al. Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res 1992, 586:135-139.
22. Koehl M., Bjijou Y., Le Moal M., Cador M. Nicotine-induced locomotor activity is increased by preexposure of rats to prenatal stress. Brain Res 2000, 882:196-200.
23. Morley-Fletcher S., Puopolo M., Gentili S., Gerra G., Macchia T., Laviola G. Prenatal stress affects 3,4-methylenedioxymethamphetamine pharmacokinetics and drug-induced motor alterations in adolescent female rats. Eur J Pharmacol 2004, 489:89-92.
24. Kippin T.E., Szumlinski K.K., Kapasova Z., Rezner B., See R.E. Prenatal stress enhances responsiveness to cocaine. Neuropsychopharmacology 2007, 33:769-782.
25. Thomas M.B., Hu M., Lee T.M., Bhatnagar S., Becker J.B. Sex-specific susceptibility to cocaine in rats with a history of prenatal stress. Physiol Behav 2009, 25:270-277.
26. Van Waes V., Enache M., Dutriez I., Lesage J., Morley-Fletcher S., Vinner E., et al. Hypo-response of the hypothalamic-pituitary-adrenocortical axis after an ethanol challenge in prenatally stressed adolescent male rats. Eur J Neurosci 2006, 24:1193-1200.
27. King A., Munisamy G., de Wit H., Lin S. Attenuated cortisol response to alcohol in heavy social drinkers. Int J Psychophysiol 2006, 59:203-209.
28. Schuckit M.A., Gold E., Risch C. Plasma cortisol levels following ethanol in sons of alcoholics and controls. Arch Gen Psychiatry 1987, 44:942-945.
29. Schuckit M.A., Risch S.C., Gold E.O. Alcohol consumption, ACTH level, and family history of alcoholism. Am J Psychiatry 1988, 145:1391-1395.
30. Richardson H.N., Lee S.Y., O'Dell L.E., Koob G.F., Rivier C.L. Alcohol self-administration acutely stimulates the hypothalamic-pituitary-adrenal axis, but alcohol dependence leads to a dampened neuroendocrine state. Eur J Neurosci 2008, 28:1641-1653.
31. Van Waes V., Enache M., Berton O., Vinner E., Lhermitte M., Maccari S., Darnaudéry M. Effect of prenatal stress on alcohol preference and sensitivity to chronic alcohol exposure in male rats. Psychopharmacology (Berl) 2011, 214(1):197-208.
32. Van Waes V., Enache M., Zuena A., Mairesse J., Nicoletti F., Vinner E., et al. Ethanol attenuates spatial memory deficits and increases mglu1a receptor expression in the hippocampus of rats exposed to prenatal stress. Alcohol Clin Exp Res 2009, 33:1346-1354.
33. Weinberg J. Effects of early experience on responsiveness to ethanol: a preliminary report. Physiol Behav 1987, 40:401-406.
34. Lancaster F.E., Brown T.D., Coker K.L., Elliott J.A., Wren S.B. Sex differences in alcohol preference and drinking patterns emerge during the early postpubertal period. Alcohol Clin Exp Res 1998, 20:1043-1049.
35. Li T.K., Lumeng L. Alcohol preference and voluntary alcohol intakes of inbred rat strains and the National Institutes of Health heterogeneous stock of rats. Alcohol Clin Exp Res 1984, 8:485-486.
36. Darnaudery M., Louvart H., Defrance L., Leonhardt M., Morley-Fletcher S., Gruber S.H., et al. Impact of an intense stress on ethanol consumption in female rats characterized by their pre-stress preference: modulation by prenatal stress. Brain Res 2007, 1131:181-186.
37. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 1978, 47:379-391.
38. Mathé A.A., Jousisto-Hanson J., Stenfors C., Theodorsson E. Effect of lithium on tachykinins, calcitonin gene-related peptide, and neuropeptide Y in rat brain. J Neurosci Res 1990, 26:233-237.
39. Mathé A.A., Stenfors C., Brodin E., Theodorsson E. Neuropeptides in brain: effects of microwave irradiation and decapitation. Life Sci 1990, 46:287-293.
40. Mathé A.A., Gruber S.H., Jiménez P.A., Theodorsson E., Stenfors C. Effects of electroconvulsive stimuli and MK-801 on neuropeptide Y, neurokinin A, and calcitonin gene-related peptide in rat brain. Neurochem Res 1997, 22:629-636.
41. Stenfors C., Theodorsson E., Mathé A.A. Effect of repeated electroconvulsive treatment on regional concentrations of tachykinins, neurotensin, vasoactive intestinal polypeptide, neuropeptide Y, and galanin in rat brain. J Neurosci Res 1989, 24:445-450.
42. Walker B.M., Drimmer D.A., Walker J.L., Liu T., Mathé A.A., Ehlers C.L. Effects of prolonged ethanol vapor exposure on forced swim behavior, and neuropeptide Y and corticotropin-releasing factor levels in rat brains. Alcohol 2010, 44:487-493.
43. Tatarczynska E., Palucha A., Szewczyk B., Chojnacka-Wojcik E., Wieronska J., Pilc A. Anxiolytic- and antidepressant-like effects of group III metabotropic glutamate agonist (1S,3R,4S)-1-aminocyclopentane-1,3,4-tricarboxylic acid (ACPT-I) in rats. Pol J Pharmacol 2002, 54:707-710.
44. Belozertseva I.V., Kos T., Popik P., Danysz W., Bespalov A.Y. Antidepressant-like effects of mGluR1 and mGluR5 antagonists in the rat forced swim and the mouse tail suspension tests. Eur Neuropsychopharmacol 2007, 17:172-179.
45. Nicoletti F, Bockaert J, Collingridge GL, Conn PJ, Ferraguti F, Schoepp DD, et al. Metabotropic glutamate receptors: from the workbench to the bedside. Neuropharmacology (2010), doi:10.1016/j.neuropharm.2010.10.022.
46. Parker R.M., Herzog H. Regional distribution of Y-receptor subtype mRNAs in rat brain. Eur J Neurosci 1999, 11:1431-1448.
47. Koob G.F. A role for brain stress systems in addiction. Neuron 2008, 59:11-34.
48. Jimenez-Vasquez P.A., Overstreet D.H., Mathé A.A. Neuropeptide Y in male and female brains of Flinders Sensitive Line, a rat model of depression. Effects of electroconvulsive stimuli. J Psychiatr Res 2000, 34:405-412.
49. Jiménez-Vasquez P.A., Mathé A.A., Thomas J.D., Riley E.P., Ehlers C.L. Early maternal separation alters neuropeptide Y concentrations in selected brain regions in adult rats. Brain Res Dev Brain Res 2001, 131:149-152.
50. Jiménez-Vasquez P.A., Diaz-Cabiale Z., Caberlotto L., Bellido I., Overstreet D., Fuxe K., et al. Electroconvulsive stimuli selectively affect behavior and neuropeptide Y (NPY) and NPY Y(1) receptor gene expressions in hippocampus and hypothalamus of Flinders Sensitive Line rat model of depression. Eur Neuropsychopharmacol 2007, 17:298-308.
51. Redrobe J.P., Dumont Y., Fournier A., Baker G.B., Quirion R. Role of serotonin (5-HT) in the antidepressant-like properties of neuropeptide Y (NPY) in the mouse forced swim test. Peptides 2005, 26:1394-1400.
52. Luo D.D., An S.C., Zhang X. Involvement of hippocampal serotonin and neuropeptide Y in depression induced by chronic unpredicted mild stress. Brain Res Bull 2008, 77:8-12.
53. Christiansen S.H., Olesen M.V., Wörtwein G., Woldbye D.P. Fluoxetine reverts chronic restraint stress-induced depression-like behaviour and increases neuropeptide Y and galanin expression in mice. Behav Brain Res 2011, 216:585-591.
54. Morales-Medina J.C., Dumont Y., Quirion R. A possible role of neuropeptide Y in depression and stress. Brain Res 2010, 1314:194-205.
55. Lin E.J., Lin S., Aljanova A., During M.J., Herzog H. Adult-onset hippocampal-specific neuropeptide Y overexpression confers mild anxiolytic effectin mice. Eur Neuropsychopharmacol 2010, 20:164-175.
56. Lappalainen J., Kranzler H.R., Malison R., Price L.H., Van Dyck C., Rosenheck R.A., et al. A functional neuropeptide Y Leu7Pro polymorphism associated with alcohol dependence in a large population sample from the United States. Arch Gen Psychiatry 2002, 59:825-831.
57. Sjöholm L.K., Melas P.A., Forsell Y., Lavebratt C. PreproNPY Pro7 protects against depression despite exposure to environmental risk factors. J Affect Disord 2009, 118(November (1-3)):124-130.
58. Sommer W.H., Lidström J., Sun H., Passer D., Eskay R., Parker S.C., et al. Human NPY promoter variation rs16147:T>C as a moderator of prefrontal NPY gene expression and negative affect. Hum Mutat 2010, 31:E1594-E1608.
59. Lindberg C., Koefoed P., Hansen E.S., Bolwig T.G., Rehfeld J.F., Mellerup E., et al. No association between the -399C>T polymorphism of the neuropeptide Y gene and schizophrenia, unipolar depression or panic disorder in a Danish population. Acta Psychiatr Scand 2006, 113:54-58.
60. Heilig M., Zachrisson O., Thorsell A., Ehnvall A., Mottagui-Tabar S., Sjögren M., et al. Decreased cerebrospinal fluid neuropeptide Y (NPY) in patients with treatment refractory unipolar major depression: preliminary evidence for association with preproNPY gene polymorphism. J Psychiatr Res 2004, 38:113-121.
61. Hou C., Jia F., Liu Y., Li L. CSF serotonin, 5-hydroxyindolacetic acid and neuropeptide Y levels in severe major depressive disorder. Brain Res 2006, 1095:154-158.
62. Czermak C., Hauger R., Drevets W.C., Luckenbaugh D.A., Geraci M., Charney D.S., et al. Plasma NPY concentrations during tryptophan and sham depletion in medication-free patients with remitted depression. J Affect Disord 2008, 110:277-281.
63. Caberlotto L., Jimenez P., Overstreet D.H., Hurd Y.L., Mathé A.A., Fuxe K. Alterations in neuropeptide Y levels and Y1 binding sites in the Flinders Sensitive Line rats, a genetic animal model of depression. Neurosci Lett 1999, 265:191-194.
64. Husum H., Mikkelsen J.D., Hogg S., Mathé A.A., Mørk A. Involvement of hippocampal neuropeptide Y in mediating the chronic actions of lithium, electroconvulsive stimulation and citalopram. Neuropharmacology 2000, 39:1463-1473.
65. Husum H., Van Kammen D., Termeer E., Bolwig G., Mathé A. Topiramate normalizes hippocampal NPY-LI in flinders sensitive line 'depressed' rats and upregulates NPY, galanin, and CRH-LI in the hypothalamus: implications for mood-stabilizing and weight loss-inducing effects. Neuropsychopharmacology 2003 Jul, 28:1292-1299.
66. Bjørnebekk A., Mathé A.A., Brené S. The antidepressant effects of running and escitalopram are associated with levels of hippocampal NPY and Y1 receptor but not cell proliferation in a rat model of depression. 1. Hippocampus 2010, 20:820-828.
67. Caberlotto L., Hurd Y.L. Neuropeptide Y Y (1) and Y(2) receptor mRNA expression in the prefrontal cortex of psychiatric subjects. Relationship of Y(2) subtype to suicidal behavior. Neuropsychopharmacology 2001, 25:91-97.
68. Kuromitsu J., Yokoi A., Kawai T., Nagasu T., Aizawa T., Haga S., et al. Reduced neuropeptide Y mRNA levels in the frontal cortex of people with schizophrenia and bipolar disorder. Brain Res Gene Expr Patterns 2001, 1:17-21.
69. Linthorst A.C., Peñalva R.G., Flachskamm C., Holsboer F., Reul J.M. Forced swim stress activates rat hippocampal serotonergic neurotransmission involving a corticotropin-releasing hormone receptor-dependent mechanism. Eur J Neurosci 2002, 16:2441-2452.
70. Peñalva R.G., Flachskamm C., Zimmermann S., Wurst W., Holsboer F., Reul J.M., et al. Corticotropin-releasing hormone receptor type 1-deficiency enhances hippocampal serotonergic neurotransmission: an in vivo microdialysis study in mutant mice. Neuroscience 2002, 109:253-266.
71. Merali Z., Du L., Hrdina P., Palkovits M., Faludi G., Poulter M.O., et al. Dysregulation in the suicide brain: mRNA expression of corticotropin-releasing hormone receptors and GABA(A) receptor subunits in frontal cortical brain region. J Neurosci 2004, 24:1478-1485.
72. Husum H., Termeer E., Mathé A.A., Bolwig T.G., Ellenbroek B.A. Early maternal deprivation alters hippocampal levels of neuropeptide Y and calcitonin-gene related peptide in adult rats. Neuropharmacology 2002, 42:798-806.
73. De Bellis M.D. Developmental traumatology: a contributory mechanism for alcohol and substance use disorders. Psychoneuroendocrinology 2002, 27:155-170.
74. Markou A., Kosten T.R., Koob G.F. Neurobiological similarities in depression and drug dependence: a self-medication hypothesis. Neuropsychopharmacology. 1998, 18:135-174.
75. Shonkoff J.P., Boyce W.T., McEwen B.S. Neuroscience, molecular biology, and the childhood roots of health disparities: building a new framework for health promotion and disease prevention. JAMA 2009, 301:2252-2269.