Exposure to nicotine and ethanol in adolescent mice: Effects on depressive-like behavior during exposure and withdrawal

Behavioural Brain Research

Volumn 221, Issue 1, 2011, Pages 282-289

  Ribeiro Carvalho, Anderson ^a,b   Lima, Carla S ^a   Nunes Freitas, André L ^a   Filgueiras, Cláudio C ^a   Manhães, Alex C ^a   Abreu Villaça, Yael ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO FEDERAL DE EDUCAÇÃO   (Brazil)

Author keywords

Adolescence; Alcohol; Development; Mood disorders; Tobacco

Indexed keywords

ALCOHOL; NICOTINE;

ADOLESCENT; ALCOHOL WITHDRAWAL; ALCOHOLISM; ANHEDONIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; C57BL 6 MOUSE; CONTROLLED STUDY; DEPRESSION; DISEASE ASSOCIATION; FEMALE; MALE; MOUSE; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; SEX DIFFERENCE; TOBACCO DEPENDENCE; WITHDRAWAL SYNDROME;

ANIMALS; BODY WEIGHT; CHOICE BEHAVIOR; DEPRESSION; DISEASE MODELS, ANIMAL; DRUG INTERACTIONS; ETHANOL; FEMALE; IMMOBILITY RESPONSE, TONIC; MALE; MICE; MICE, INBRED C57BL; NICOTINE; PHYSICAL ENDURANCE; SEX CHARACTERISTICS; SUBSTANCE WITHDRAWAL SYNDROME; SUCROSE; TIME FACTORS;

EID: 79954631681     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.03.014     Document Type: Article

References (69)

1. Abreu-Villaça Y., Medeiros A.H., Lima C.S., Faria F.P., Filgueiras C.C., Manhães A.C. Combined exposure to nicotine and ethanol in adolescent mice differentially affects memory and learning during exposure and withdrawal. Behav Brain Res 2007, 181:136-146.
2. Abreu-Villaça Y., Nunes F., do E Queiroz-Gomes, Manhães A.C., Filgueiras C.C. Combined exposure to nicotine and ethanol in adolescent mice differentially affects anxiety levels during exposure, short-term, and long-term withdrawal. Neuropsychopharmacology 2008, 33:599-610.
3. Abreu-Villaça Y., Queiroz-Gomes F.E., Dal Monte A.P., Filgueiras C.C., Manhães A.C. Individual differences in novelty-seeking behavior but not in anxiety response to a new environment can predict nicotine consumption in adolescent C57BL/6 mice. Behav Brain Res 2006, 167:175-182.
4. Abreu-Villaça Y., Seidler F.J., Slotkin T.A. Impact of adolescent nicotine exposure on adenylyl cyclase-mediated cell signaling: enzyme induction, neurotransmitter-specific effects, regional selectivities, and the role of withdrawal. Brain Res 2003, 988:164-172.
5. Abreu-Villaça Y., Seidler F.J., Slotkin T.A. Does prenatal nicotine exposure sensitize the brain to nicotine-induced neurotoxicity in adolescence?. Neuropsychopharmacology 2004, 29:1440-1450.
6. Abreu-Villaça Y., Seidler F.J., Tate C.A., Cousins M.M., Slotkin T.A. Prenatal nicotine exposure alters the response to nicotine administration in adolescence: effects on cholinergic systems during exposure and withdrawal. Neuropsychopharmacology 2004, 29:879-890.
7. Anisman H., Matheson K. Stress, depression, and anhedonia: caveats concerning animal models. Neurosci Biobehav Rev 2005, 29:525-546.
8. Bobo J.K., Gilchrist L.D., Schilling R.F., Noach B., Schinke S.P. Cigarette smoking cessation attempts by recovering alcoholics. Addict Behav 1987, 12:209-215.
9. Brook J.S., Cohen P., Brook D.W. Longitudinal study of co-occurring psychiatric disorders and substance use. J Am Acad Child Adolesc Psychiatry 1998, 37:322-330.
10. Caraballo R.S., Giovino G.A., Pechacek T.F. Self-reported cigarette smoking vs. serum cotinine among U.S. adolescents. Nicotine Tob Res 2004, 6:19-25.
11. Carpenter K.M., Hasin D.S. Drinking to cope with negative affect and DSM-IV alcohol use disorders: a test of three alternative explanations. J Stud Alcohol 1999, 60:694-704.
12. Carroll M.E., Anderson M.M., Morgan A.D. Regulation of intravenous cocaine self-administration in rats selectively bred for high (HiS) and low (LoS) saccharin intake. Psychopharmacology (Berl) 2007, 190:331-341.
13. Centers for Disease Control Prevention. Trends in cigarette smoking among high school students: United States 2000-2009. Morb Mortal Wkly Rep 2010;59:1063-8.
14. Courtet P., Baud P., Abbar M., Boulenger J.P., Castelnau D., Mouthon D., et al. Association between violent suicidal behavior and the low activity allele of the serotonin transporter gene. Mol Psychiatry 2001, 6:338-341.
15. Cryan J.F., Valentino R.J., Lucki I. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 2005, 29:547-569.
16. D'Andrea I., Gracci F., Alleva E., Branchi I. Early social enrichment provided by communal nest increases resilience to depression-like behavior more in female than in male mice. Behav Brain Res 2010, 215:71-76.
17. Dagyte G., Den Boer J.A., Trentani A. The cholinergic system and depression. Behav Brain Res 2010.
18. Dawson D.A. Drinking as a risk factor for sustained smoking. Drug Alcohol Depend 2000, 59:235-249.
19. Detke M.J., Wieland S., Lucki I. Blockade of the antidepressant-like effects of 8-OH-DPAT, buspirone and desipramine in the rat forced swim test by 5HT1A receptor antagonists. Psychopharmacology (Berl) 1995, 119:47-54.
20. Drevets W.C. Neuroimaging studies of mood disorders. Biol Psychiatry 2000, 48:813-829.
21. Eckardt M.J., File S.E., Gessa G.L., Grant K.A., Guerri C., Hoffman P.L., et al. Effects of moderate alcohol consumption on the central nervous system. Alcohol Clin Exp Res 1998, 22:998-1040.
22. Ernst M., Korelitz K.E. Cerebral maturation in adolescence: behavioral vulnerability. Encephale 2009, 35(Suppl. 6):S182-S189.
23. Filgueiras C.C., Abreu-Villaça Y., Krahe T.E., Manhães A.C. Unilateral hemispherectomy at adulthood asymmetrically affects immobile behavior of male Swiss mice. Behav Brain Res 2006, 172:33-38.
24. Getachew B., Hauser S.R., Taylor R.E., Tizabi Y. Desipramine blocks alcohol-induced anxiety- and depressive-like behaviors in two rat strains. Pharmacol Biochem Behav 2008, 91:97-103.
25. Grant B.F. Age at smoking onset and its association with alcohol consumption and DSM-IV alcohol abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse 1998, 10:59-73.
26. Hajnal A., Norgren R. Accumbens dopamine mechanisms in sucrose intake. Brain Res 2001, 904:76-84.
27. Hayatbakhsh M.R., Najman J.M., Jamrozik K., Mamun A.A., Alati R., Bor W. Cannabis and anxiety and depression in young adults: a large prospective study. J Am Acad Child Adolesc Psychiatry 2007, 46:408-417.
28. Ikeuchi M., Koyama T., Takahashi J., Yazawa K. Effects of astaxanthin supplementation on exercise-induced fatigue in mice. Biol Pharm Bull 2006, 29:2106-2110.
29. Iniguez S.D., Warren B.L., Parise E.M., Alcantara L.F., Schuh B., Maffeo M.L., et al. Nicotine exposure during adolescence induces a depression-like state in adulthood. Neuropsychopharmacology 2009, 34:1609-1624.
30. Kandel D.B., Johnson J.G., Bird H.R., Weissman M.M., Goodman S.H., Lahey B.B., et al. Psychiatric comorbidity among adolescents with substance use disorders: findings from the MECA Study. J Am Acad Child Adolesc Psychiatry 1999, 38:693-699.
31. Kessler R.C., Avenevoli S., Ries M.K. Mood disorders in children and adolescents: an epidemiologic perspective. Biol Psychiatry 2001, 49:1002-1014.
32. Kitada Y., Miyauchi T., Satoh A., Satoh S. Effects of antidepressants in the rat forced swimming test. Eur J Pharmacol 1981, 72:145-152.
33. Klein L.C., Stine M.M., Pfaff D.W., Vandenbergh D.J. Laternal nicotine exposure increases nicotine preference in periadolescent male but not female C57B1/6J mice. Nicotine Tob Res 2003, 5:117-124.
34. Klein L.C., Stine M.M., Vandenbergh D.J., Whetzel C.A., Kamens H.M. Sex differences in voluntary oral nicotine consumption by adolescent mice: a dose-response experiment. Pharmacol Biochem Behav 2004, 78:13-25.
35. Krahe T.E., Filgueiras C.C., Caparelli-Daquer E.M., Schmidt S.L. Contralateral rotatory bias in the free-swimming test after unilateral hemispherectomy in adult Swiss mice. Int J Neurosci 2001, 108:21-30.
36. Kristofikova Z., Platilova V., Klaschka J. Age- and sex-dependent effects of ethanol on hippocampal hemicholinium-3 sensitive choline carriers during postnatal development of rats. Neurochem Res 2003, 28:397-405.
37. Lee C.W., Kahende J. Factors associated with successful smoking cessation in the United States, 2000. Am J Public Health 2007, 97:1503-1509.
38. Lima C.S., Ribeiro-Carvalho A., Filgueiras C.C., Manhães A.C., Meyer A., Abreu-Villaça Y. Exposure to methamidophos at adulthood elicits depressive-like behavior in mice. Neurotoxicology 2009, 30:471-478.
39. Lopez-Rubalcava C., Lucki I. Strain differences in the behavioral effects of antidepressant drugs in the rat forced swimming test. Neuropsychopharmacology 2000, 22:191-199.
40. Manninen L., Poikolainen K., Vartiainen E., Laatikainen T. Heavy drinking occasions and depression. Alcohol Alcohol 2006, 41:293-299.
41. Mannucci C., Tedesco M., Bellomo M., Caputi A.P., Calapai G. Long-term effects of nicotine on the forced swimming test in mice: an experimental model for the study of depression caused by smoke. Neurochem Int 2006, 49:481-486.
42. Markou A., Kosten T.R., Koob G.F. Neurobiological similarities in depression and drug dependence: a self-medication hypothesis. Neuropsychopharmacology 1998, 18:135-174.
43. Meyerhoff D.J., Tizabi Y., Staley J.K., Durazzo T.C., Glass J.M., Nixon S.J. Smoking comorbidity in alcoholism: neurobiological and neurocognitive consequences. Alcohol Clin Exp Res 2006, 30:253-264.
44. Mourlon V., Baudin A., Blanc O., Lauber A., Giros B., Naudon L., et al. Maternal deprivation induces depressive-like behaviours only in female rats. Behav Brain Res 2010, 213:278-287.
45. Nelson D.E., Giovino G.A., Shopland D.R., Mowery P.D., Mills S.L., Eriksen M.P. Trends in cigarette smoking among US adolescents, 1974 through 1991. Am J Public Health 1995, 85:34-40.
46. Oliveira-da-Silva A., Manhaes A.C., Cristina-Rodrigues F., Filgueiras C.C., breu-Villaca Y. Hippocampal increased cell death and decreased cell density elicited by nicotine and/or ethanol during adolescence are reversed during drug withdrawal. Neuroscience 2010, 167:163-173.
47. Oliveira-da-Silva A., Vieira F.B., Cristina-Rodrigues F., Filgueiras C.C., Manhaes A.C., breu-Villaca Y. Increased apoptosis and reduced neuronal and glial densities in the hippocampus due to nicotine and ethanol exposure in adolescent mice. Int J Dev Neurosci 2009, 27:539-548.
48. Paljarvi T., Koskenvuo M., Poikolainen K., Kauhanen J., Sillanmaki L., Makela P. Binge drinking and depressive symptoms: a 5-year population-based cohort study. Addiction 2009, 104:1168-1178.
49. 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.
50. Ribeiro-Carvalho A., Lima C.S., Filgueiras C.C., Manhães A.C., Abreu-Villaça Y. Nicotine and ethanol interact during adolescence: effects on the central cholinergic systems. Brain Res 2008, 1232:48-60.
51. Ribeiro-Carvalho A., Lima C.S., Medeiros A.H., Siqueira N.R., Filgueiras C.C., Manhães A.C., et al. Combined exposure to nicotine and ethanol in adolescent mice: effects on the central cholinergic systems during short and long term withdrawal. Neuroscience 2009, 162:1174-1186.
52. Rodgers B., Korten A.E., Jorm A.F., Christensen H., Henderson S., Jacomb P.A. Risk factors for depression and anxiety in abstainers, moderate drinkers and heavy drinkers. Addiction 2000, 95:1833-1845.
53. Salin-Pascual R.J., de la Fuente J.R., Galicia-Polo L., Drucker-Colin R. Effects of transderman nicotine on mood and sleep in nonsmoking major depressed patients. Psychopharmacology (Berl) 1995, 121:476-479.
54. Schmidt S.L., Filgueiras C.C., Krahe T.E. Effects of sex and laterality on the rotatory swimming behavior of normal mice. Physiol Behav 1999, 65:607-616.
55. Sihvola E., Rose R.J., Dick D.M., Pulkkinen L., Marttunen M., Kaprio J. Early-onset depressive disorders predict the use of addictive substances in adolescence: a prospective study of adolescent Finnish twins. Addiction 2008, 103:2045-2053.
56. Slawecki C.J., Thorsell A., Ehlers C.L. Long-term neurobehavioral effects of alcohol or nicotine exposure in adolescent animal models. Ann N Y Acad Sci 2004, 1021:448-452.
57. Snedecor GW, Cochran WG. Statistical methods. 6th ed. Iowa; 1967.
58. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000, 24:417-463.
59. Spear L.P. The adolescent brain and the college drinker: biological basis of propensity to use and misuse alcohol. J Stud Alcohol Suppl 2002, 71-81.
60. Stage K.B., Glassman A.H., Covey L.S. Depression after smoking cessation: case reports. J Clin Psychiatry 1996, 57:467-469.
61. Stansfield K.H., Kirstein C.L. Chronic cocaine or ethanol exposure during adolescence alters novelty-related behaviors in adulthood. Pharmacol Biochem Behav 2007, 86:637-642.
62. Stevenson J.R., Schroeder J.P., Nixon K., Besheer J., Crews F.T., Hodge C.W. Abstinence following alcohol drinking produces depression-like behavior and reduced hippocampal neurogenesis in mice. Neuropsychopharmacology 2009, 34:1209-1222.
63. Suemaru K., Yasuda K., Cui R., Li B., Umeda K., Amano M., et al. Antidepressant-like action of nicotine in forced swimming test and brain serotonin in mice. Physiol Behav 2006, 88:545-549.
64. Tizabi Y., Hauser S.R., Tyler K.Y., Getachew B., Madani R., Sharma Y., et al. Effects of nicotine on depressive-like behavior and hippocampal volume of female WKY rats. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:62-69.
65. Uzbay I.T., Usanmaz S.E., Tapanyigit E.E., Aynacioglu S., Akarsu E.S. Dopaminergic and serotonergic alterations in the rat brain during ethanol withdrawal: association with behavioral signs. Drug Alcohol Depend 1998, 53:39-47.
66. Vieyra-Reyes P., Picciotto M.R., Mineur Y.S. Voluntary oral nicotine intake in mice down-regulates GluR2 but does not modulate depression-like behaviors. Neurosci Lett 2008, 434:18-22.
67. Willner P., Towell A., Sampson D., Sophokleous S., Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl) 1987, 93:358-364.
68. Wood T., Wewers M.E., Groner J., Ahijevych K. Smoke constituent exposure and smoking topography of adolescent daily cigarette smokers. Nicotine Tob Res 2004, 6:853-862.
69. Zaniewska M., McCreary A.C., Wydra K., Filip M. Effects of serotonin (5-HT)2 receptor ligands on depression-like behavior during nicotine withdrawal. Neuropharmacology 2010, 58:1140-1146.