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Gene–environment interactions in vulnerability to cocaine intravenous self-administration: a brief social experience affects intake in DBA/2J but not in C57BL/6J mice

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Abstract

Rationale

Individual differences in cocaine-taking behavior and liability to develop abuse are clearly observed, but underlying mechanisms are still poorly understood. A role for gene–environment interactions has been proposed but remains hypothetical.

Objectives

We investigated whether gene–environment interactions influence intravenous cocaine self-administration (SA) in mice. We tested the effect of a past short group housing experience on cocaine SA in two inbred strains of mice, the C57BL/6J (C57) and DBA/2J (DBA).

Methods

Adult C57 and DBA mice were individually housed upon arrival in the laboratory. After 3 weeks, half of the animals of each strain were group housed for 19 days. One week after the end of group housing, cocaine SA or measurement of brain cocaine levels took place.

Results

Individually and ex-group-housed C57 mice did not differ for cocaine SA. On the contrary, the ex-group-housed DBA mice showed an upward shift in the dose-response curve as compared to individually housed DBA. Differences in brain cocaine levels could not account for the observed behavioral differences.

Conclusions

These results demonstrate that vulnerability to cocaine reinforcing effects can be affected by gene–environment interactions. We propose a mouse model for the characterization of gene–environment interactions in the vulnerability to cocaine-taking behavior.

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References

  • Alcaro A, Cabib S, Ventura R, Puglisi-Allegra S (2002) Genotype- and experience-dependent susceptibility to depressive-like responses in the forced-swimming test. Psychopharmacology (Berl) 164:138–143

    Article  CAS  Google Scholar 

  • Avitsur R, Stark JL, Dhabhar FS, Kramer KA, Sheridan JF (2003) Social experience alters the response to social stress in mice. Brain Behav Immun 17:426–437

    Article  PubMed  Google Scholar 

  • Badiani A, Cabib S, Puglisi-Allegra S (1992) Chronic stress induces strain-dependent sensitization to the behavioral effects of amphetamine in the mouse. Pharmacol Biochem Behav 43:53–60

    Article  PubMed  CAS  Google Scholar 

  • Cabib S, Bonaventura N (1997) Parallel strain-dependent susceptibility to environmentally-induced stereotypes and stress-induced behavioral sensitization in mice. Physiol Behav 61:499–506

    Article  PubMed  CAS  Google Scholar 

  • Cabib S, Algeri S, Perego C, Puglisi-Allegra S (1990) Behavioral and biochemical changes monitored in two inbred strains of mice during exploration of an unfamiliar environment. Physiol Behav 47:749–753

    Article  PubMed  CAS  Google Scholar 

  • Cabib S, Orsini C, Le Moal M, Piazza PV (2000) Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience. Science 289:463–465

    Article  PubMed  CAS  Google Scholar 

  • Cabib S, Ventura R, Puglisi-Allegra S (2002a) Opposite imbalances between mesocortical and mesoaccumbens dopamine responses to stress by the same genotype depending on living conditions. Behav Brain Res 129:179–185

    Article  PubMed  CAS  Google Scholar 

  • Cabib S, Puglisi-Allegra S, Ventura R (2002b) The contribution of comparative studies in inbred strains of mice to the understanding of the hyperactive phenotype. Behav Brain Res 130:103–109

    Article  PubMed  CAS  Google Scholar 

  • Cadoret RJ, Yates WR, Troughton E, Woodworth G, Stewart MA (1995) Genetic-environmental interaction in the genesis of aggressivity and conduct disorders. Arch Gen Psychiatry 52:916–924

    PubMed  CAS  Google Scholar 

  • Capone F, Venerosi A, Puopolo M, Alleva E, Cirulli F (2005) Behavioral responses of 129/Sv, C57BL/6J and DBA/2J mice to a non-predator aversive olfactory stimulus. Acta Neurobiol Exp (Wars) 65:29–38

    Google Scholar 

  • Caspi A, Moffitt TE (2006) Gene–environment interactions in psychiatry: joining forces with neuroscience. Nat Rev Neurosci 7:583–590

    Article  PubMed  CAS  Google Scholar 

  • Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, Taylor A, Poulton R (2002) Role of genotype in the cycle of violence in maltreated children. Science 297:851–854

    Article  PubMed  CAS  Google Scholar 

  • Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, McClay J, Mill J, Martin J, Braithwaite A, Poulton R (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301:386–389

    Article  PubMed  CAS  Google Scholar 

  • Caspi A, Moffitt TE, Cannon M, McClay J, Murray R, Harrington H, Taylor A, Arseneault L, Williams B, Braithwaite A, Poulton R, Craig IW (2005) Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene × environment interaction. Biol Psychiatry 57:1117–1127

    Article  PubMed  CAS  Google Scholar 

  • Conversi D, Bonito-Oliva A, Orsini C, Cabib S (2006) Habituation to the test cage influences amphetamine-induced locomotion and Fos expression and increases FosB/DeltaFosB-like immunoreactivity in mice. Neuroscience 141:597–605

    Article  PubMed  CAS  Google Scholar 

  • Crabbe JC, Wahlsten D, Dudek BC (1999) Genetics of mouse behavior: interactions with laboratory environment. Science 284:1670–1672

    Article  PubMed  CAS  Google Scholar 

  • Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl) 132:107–124

    Article  CAS  Google Scholar 

  • de Jong IE, de Kloet ER (2004) Glucocorticoids and vulnerability to psychostimulant drugs: toward substrate and mechanism. Ann N Y Acad Sci 1018:192–198

    Article  PubMed  CAS  Google Scholar 

  • de Jong IE, Oitzl MS, de Kloet ER (2007) Adrenalectomy prevents behavioural sensitisation of mice to cocaine in a genotype-dependent manner. Behav Brain Res 177:329–339

    Article  PubMed  CAS  Google Scholar 

  • Deroche V, Caine SB, Heyser CJ, Polis I, Koob GF, Gold LH (1997) Differences in the liability to self-administer intravenous cocaine between C57BL/6×SJL and BALB/cByJ mice. Pharmacol Biochem Behav 57:429–440

    Article  PubMed  CAS  Google Scholar 

  • Deroche-Gamonet V, Sillaber I, Aouizerate B, Izawa R, Jaber M, Ghozland S, Kellendonk C, Le Moal M, Spanagel R, Schutz G, Tronche F, Piazza PV (2003) The glucocorticoid receptor as a potential target to reduce cocaine abuse. J Neurosci 23:4785–4790

    PubMed  CAS  Google Scholar 

  • de Vries TJ, Schoffelmeer AN (2005) Cannabinoid CB1 receptors control conditioned drug seeking. Trends Pharmacol Sci 26:420–426

    Article  PubMed  CAS  Google Scholar 

  • de Visser L, van den BR, Stoker AK, Kas MJ, Spruijt BM (2007) Effects of genetic background and environmental novelty on wheel running as a rewarding behaviour in mice. Behav Brain Res 177:290–297

    Article  PubMed  Google Scholar 

  • Doyle GA, Sheng XR, Schwebel CL, Ferraro TN, Berrettini WH, Buono RJ (2006) Identification and functional significance of polymorphisms in the mu-opioid receptor gene (Oprm) promoter of C57BL/6 and DBA/2 mice. Neurosci Res 55:244–254

    Article  PubMed  CAS  Google Scholar 

  • DuBois DW, Perlegas A, Floyd DW, Weiner JL, McCool BA (2006) Distinct functional characteristics of the lateral/basolateral amygdala GABAergic system in C57BL/6J and DBA/2J mice. J Pharmacol Exp Ther 318:629–640

    Article  PubMed  CAS  Google Scholar 

  • Fadda P, Scherma M, Fresu A, Collu M, Fratta W (2005) Dopamine and serotonin release in dorsal striatum and nucleus accumbens is differentially modulated by morphine in DBA/2J and C57BL/6J mice. Synapse 56:29–38

    Article  PubMed  CAS  Google Scholar 

  • Goeders NE (2002) The HPA axis and cocaine reinforcement. Psychoneuroendocrinology 27:13–33

    Article  PubMed  CAS  Google Scholar 

  • Grahame NJ, Cunningham CL (1995) Genetic differences in intravenous cocaine self-administration between C57BL/6J and DBA/2J mice. Psychopharmacology (Berl) 122:281–291

    Article  CAS  Google Scholar 

  • Hackler EA, Airey DC, Shannon CC, Sodhi MS, Sanders-Bush E (2006) 5-HT(2C) receptor RNA editing in the amygdala of C57BL/6J, DBA/2J, and BALB/cJ mice. Neurosci Res 55:96–104

    Article  PubMed  CAS  Google Scholar 

  • Hwang BH, Kunkler PE, Tarricone BJ, Hingtgen JN, Nurnberger JI Jr (1999) Stress-induced changes of norepinephrine uptake sites in the locus coeruleus of C57BL/6J and DBA/2J mice: a quantitative autoradiographic study using [3H]-tomoxetine. Neurosci Lett 265:151–154

    Article  PubMed  CAS  Google Scholar 

  • Jacobs EH, Smit AB, de Vries TJ, Schoffelmeer AN (2003) Neuroadaptive effects of active versus passive drug administration in addiction research. Trends Pharmacol Sci 24:566–573

    Article  PubMed  CAS  Google Scholar 

  • Jaffee SR, Caspi A, Moffitt TE, Dodge KA, Rutter M, Taylor A, Tully LA (2005) Nature X nurture: genetic vulnerabilities interact with physical maltreatment to promote conduct problems. Dev Psychopathol 17:67–84

    Article  PubMed  Google Scholar 

  • Jamensky NT, Gianoulakis C (1999) Comparison of the proopiomelanocortin and proenkephalin opioid peptide systems in brain regions of the alcohol-preferring C57BL/6 and alcohol-avoiding DBA/2 mice. Alcohol 18:177–187

    Article  PubMed  CAS  Google Scholar 

  • Jones BC, Sarrieau A, Reed CL, Azar MR, Mormede P (1998) Contribution of sex and genetics to neuroendocrine adaptation to stress in mice. Psychoneuroendocrinology 23:505–517

    Article  PubMed  CAS  Google Scholar 

  • Kelai S, Hanoun N, Aufrere G, Beauge F, Hamon M, Lanfumey L (2006) Cannabinoid-serotonin interactions in alcohol-preferring vs. alcohol-avoiding mice. J Neurochem 99:308–320

    Article  PubMed  CAS  Google Scholar 

  • Lu L, Shepard JD, Hall FS, Shaham Y (2003) Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 27:457–491

    Article  PubMed  CAS  Google Scholar 

  • Marinelli M, Piazza PV (2002) Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur J Neurosci 16:387–394

    Article  PubMed  Google Scholar 

  • Marinelli M, Rouge-Pont F, Deroche V, Barrot M, Jesus-Oliveira C, Le Moal M, Piazza PV (1997) Glucocorticoids and behavioral effects of psychostimulants. I: locomotor response to cocaine depends on basal levels of glucocorticoids. J Pharmacol Exp Ther 281:1392–1400

    PubMed  CAS  Google Scholar 

  • McNamara RK, Levant B, Taylor B, Ahlbrand R, Liu Y, Sullivan JR, Stanford K, Richtand NM (2006) C57BL/6J mice exhibit reduced dopamine D3 receptor-mediated locomotor-inhibitory function relative to DBA/2J mice. Neuroscience 143:141–153

    Article  PubMed  CAS  Google Scholar 

  • Michel A, Tirelli E (2002) Effects of the social conditions of housing through testing on cocaine-induced contextual sensitisation and conditioned locomotion in C57BL/6J mice. Prog Neuropsychopharmacol Biol Psychiatry 26:1185–1191

    Article  PubMed  CAS  Google Scholar 

  • Moffitt TE, Caspi A, Rutter M (2006) Measured gene–environment interactions in psychopathology. Perspect Psychol Sci 1:5–27

    Article  Google Scholar 

  • O’Callaghan MJ, Croft AP, Jacquot C, Little HJ (2005) The hypothalamopituitary-adrenal axis and alcohol preference. Brain Res Bull 68:171–178

    Article  PubMed  CAS  Google Scholar 

  • Phillips TJ, Roberts AJ, Lessov CN (1997) Behavioral sensitization to ethanol: genetics and the effects of stress. Pharmacol Biochem Behav 57:487–493

    Article  PubMed  CAS  Google Scholar 

  • Piazza PV, Le Moal ML (1996) Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids, and dopaminergic neurons. Annu Rev Pharmacol Toxicol 36:359–378

    Article  PubMed  CAS  Google Scholar 

  • Pierce RC, Kumaresan V (2006) The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse? Neurosci Biobehav Rev 30:215–238

    Article  PubMed  CAS  Google Scholar 

  • Pothion S, Bizot JC, Trovero F, Belzung C (2004) Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav Brain Res 155:135–146

    Article  PubMed  Google Scholar 

  • Puglisi-Allegra S, Cabib S (1997) Psychopharmacology of dopamine: the contribution of comparative studies in inbred strains of mice. Prog Neurobiol 51:637–661

    Article  PubMed  CAS  Google Scholar 

  • Rocha BA, Odom LA, Barron BA, Ator R, Wild SA, Forster MJ (1998) Differential responsiveness to cocaine in C57BL/6J and DBA/2J mice. Psychopharmacology (Berl) 138:82–88

    Article  CAS  Google Scholar 

  • Sarnyai Z, Shaham Y, Heinrichs SC (2001) The role of corticotropin-releasing factor in drug addiction. Pharmacol Rev 53:209–243

    PubMed  CAS  Google Scholar 

  • Schroff KC, Cowen MS, Koch S, Spanagel R (2004) Strain-specific responses of inbred mice to ethanol following food shortage. Addict Biol 9:265–271

    Article  PubMed  CAS  Google Scholar 

  • Shanks N, Anisman H (1988) Stressor-provoked behavioral changes in six strains of mice. Behav Neurosci 102:894–905

    Article  PubMed  CAS  Google Scholar 

  • Shanks N, Griffiths J, Zalcman S, Zacharko RM, Anisman H (1990) Mouse strain differences in plasma corticosterone following uncontrollable footshock. Pharmacol Biochem Behav 36:515–519

    Article  PubMed  CAS  Google Scholar 

  • Shanks N, Zalcman S, Zacharko RM, Anisman H (1991) Alterations of central norepinephrine, dopamine and serotonin in several strains of mice following acute stressor exposure. Pharmacol Biochem Behav 38:69–75

    Article  PubMed  CAS  Google Scholar 

  • Silberg J, Rutter M, Neale M, Eaves L (2001) Genetic moderation of environmental risk for depression and anxiety in adolescent girls. Br J Psychiatry 179:116–121

    Article  PubMed  CAS  Google Scholar 

  • Tienari P, Wynne LC, Sorri A, Lahti I, Laksy K, Moring J, Naarala M, Nieminen P, Wahlberg KE (2004) Genotype-environment interaction in schizophrenia-spectrum disorder. Long-term follow-up study of Finnish adoptees. Br J Psychiatry 184:216–222

    Article  PubMed  Google Scholar 

  • van der Kam EL, Ellenbroek BA, Cools AR (2005) Gene–environment interactions determine the individual variability in cocaine self-administration. Neuropharmacology 48:685–695

    Article  PubMed  CAS  Google Scholar 

  • Ventura R, Puglisi-Allegra S (2005) Environment makes amphetamine-induced dopamine release in the nucleus accumbens totally impulse-dependent. Synapse 58:211–214

    Article  PubMed  CAS  Google Scholar 

  • Ventura R, Alcaro A, Cabib S, Conversi D, Mandolesi L, Puglisi-Allegra S (2004) Dopamine in the medial prefrontal cortex controls genotype-dependent effects of amphetamine on mesoaccumbens dopamine release and locomotion. Neuropsychopharmacology 29:72–80

    Article  PubMed  CAS  Google Scholar 

  • Wahlsten D, Metten P, Phillips TJ, Boehm SL, Burkhart-Kasch S, Dorow J, Doerksen S, Downing C, Fogarty J, Rodd-Henricks K, Hen R, McKinnon CS, Merrill CM, Nolte C, Schalomon M, Schlumbohm JP, Sibert JR, Wenger CD, Dudek BC, Crabbe JC (2003) Different data from different labs: lessons from studies of gene–environment interaction. J Neurobiol 54:283–311

    Article  PubMed  Google Scholar 

  • Womer DE, Jones BC, Erwin VG (1994) Characterization of dopamine transporter and locomotor effects of cocaine, GBR 12909, epidepride, and SCH 23390 in C57BL and DBA mice. Pharmacol Biochem Behav 48:327–335

    Article  PubMed  CAS  Google Scholar 

  • Zacharko RM, Gilmore W, MacNeil G, Kasian M, Anisman H (1990) Stressor induced variations of intracranial self-stimulation from the mesocortex in several strains of mice. Brain Res 533:353–357

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Beaulieu JM, Sotnikova TD, Gainetdinov RR, Caron MG (2004) Tryptophan hydroxylase-2 controls brain serotonin synthesis. Science 305:217

    Article  PubMed  CAS  Google Scholar 

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Acknowledgement

This research was supported by the NWO/INSERM/ZON grants AH002G and 985-10-01, Région Aquitaine and the University of Bordeaux 2.

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Correspondence to Véronique Deroche-Gamonet.

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van der Veen, R., Piazza, P.V. & Deroche-Gamonet, V. Gene–environment interactions in vulnerability to cocaine intravenous self-administration: a brief social experience affects intake in DBA/2J but not in C57BL/6J mice. Psychopharmacology 193, 179–186 (2007). https://doi.org/10.1007/s00213-007-0777-0

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  • DOI: https://doi.org/10.1007/s00213-007-0777-0

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