Gene-environment interaction in problematic substance use: Interaction between DRD4 and insecure attachments

Addiction Biology

Volumn 18, Issue 4, 2013, Pages 717-726

  Olsson, Craig A ^a,b,c   Moyzis, Robert K ^d   Williamson, Elizabeth ^c,e   Ellis, Justine A ^b,c   Parkinson Bates, Mandy ^b,c   Patton, George C ^b,c   Dwyer, Terry ^b,c   Romaniuk, Helena ^b,c   Moore, Elya E ^f  

^a DEAKIN UNIVERSITY   (Australia)

^b MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MONASH UNIVERSITY   (Australia)

^f ROYAL WOMEN'S HOSPITAL   (Australia)

Author keywords

Attachment style; cohort studies; DRD4 exon III VNTR; gene environment interaction; substance use; young adulthood

Indexed keywords

ALCOHOL; CANNABIS; DOPAMINE 4 RECEPTOR; DOPAMINE RECEPTOR;

ADOLESCENT; ADULT; ALCOHOL CONSUMPTION; ALLELE; ARTICLE; BINGE DRINKING; CHILD PARENT RELATION; CONTROLLED STUDY; DRUG DEPENDENCE; DRUG USE; EXON; FEMALE; GENE; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; LONGITUDINAL STUDY; MALE; PRIORITY JOURNAL; RISK; TANDEM REPEAT; TOBACCO;

ADOLESCENT; ALLELES; CONFOUNDING FACTORS (EPIDEMIOLOGY); EXONS; FEMALE; GENE-ENVIRONMENT INTERACTION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LONGITUDINAL STUDIES; MALE; MINISATELLITE REPEATS; MODELS, GENETIC; OBJECT ATTACHMENT; PARENT-CHILD RELATIONS; POLYMORPHISM, GENETIC; RECEPTORS, DOPAMINE D4; REWARD; RISK FACTORS; SUBSTANCE-RELATED DISORDERS; VICTORIA; YOUNG ADULT;

EID: 84879461256     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/j.1369-1600.2011.00413.x     Document Type: Article

References (63)

1. Ainsworth M, Blehar M, Waters E, Wall S, (1978) Patterns of Attachment: A Psychological Study of the Strange Situation. Hillsdale, NJ: Erlbaum.
2. Asghari V, Sanyal S, Buchwaldt S, Paterson A, Jovanovic V, Van Tol HH, (1995) Modulation of intracellular cyclic AMP levels by different human dopamine D4 receptor variants. J Neurochem 65: 1157-1165.
3. Bakermans-Kranenburg M, van Ijzendoorn M, Juffer F, (2003) Less is more: meta-analyses of sensitivity and attachment interventions in early childhood. Psychol Bull 129: 195-215. (Pubitemid 38389554)
4. Bakermans-Kranenburg MJ, van Ijzendoorn MH, (2006) Gene-environment interaction of the dopamine D4 receptor (DRD4) and observed maternal insensitivity predicting externalizing behavior in preschoolers. Dev Psychobiol 48: 406-409. (Pubitemid 44090286)
5. Belsky J, (1997) Theory testing, effect-size evaluation, and differential susceptibility to rearing influence: the case of mothering and attachment. Child Dev 68: 598-600. (Pubitemid 127454349)
6. Bierut LJ, Madden PAF, Breslau N, Johnson EO, Hatsukami D, Pomerleau OF, Swan GE, Rutter J, Bertelsen S, Fox L, Fugman D, Goate AM, Hinrichs AL, Konvicka K, Martin NG, Montgomery GW, Saccone NL, Saccone SF, Wang JC, Chase GA, Rice JP, Ballinger DG, (2007) Novel genes identified in a high-density genome wide association study for nicotine dependence. Hum Mol Genet 16: 24-35. (Pubitemid 46152542)
7. Bierut LJ, Agrawal A, Bucholz KK, Doheny KF, Laurie C, Pugh E, Fisher S, Fox L, Howells W, Bertelsen S, Hinrichs AL, Almasy L, Breslau N, Culverhouse RC, Dick DM, Edenberg HJ, Foroud T, Grucza RA, Hatsukami D, Hesselbrock V, Johnson EO, Kramer J, Krueger RF, Kuperman S, Lynskey M, Mann K, Neuman RJ, Nöthen MM, Nurnberger JIJ, Porjesz B, Ridinger M, Saccone NL, Saccone SF, Schuckit MA, Tischfield JA, Wang JC, Rietschel M, Goate AM, Rice JP, Gene-Environment- Association-Studies-Consortium (2010) A genome-wide association study of alcohol dependence. Proc Natl Acad Sci USA 107: 5082-5087.
8. Botto LD, (2007) Flavors in gene-environment interactions. Epidemiology 18: 431-432. (Pubitemid 46955308)
9. Botto LD, Khoury MJ, (2001) Commentary: facing the challenge of gene-environment interaction: the two-by-four table and beyond. Am J Epidemiol 153: 1016-1020. (Pubitemid 32423788)
10. Bowlby J, (1973) Attachment and Loss: Vol. 2. Separation: Anxiety and Anger. New York: Basic Books.
11. Castellanos FX, Sonuga-Barke EJS, Milham MP, Tannock R, (2006) Characterizing cognition in ADHD: beyond executive dysfunction. Trends Cogn Sci 10: 117-123.
12. Chen C, Chen C, Moyzis R, He Q, Li H, Li J, Zhu B, Lessard J, Stern H, Dong Q, (2011) Genetic variations in the dopaminergic system and alcohol use: a system-level analysis. Addict Biol. doi: 10.1111/j.1369-1600.2011.00348.x. [Epub ahead of print].
13. Comings DE, Blum K, (2000) Reward deficiency syndrome: genetic aspects of behavioral disorders. Prog Brain Res 126: 325-341. (Pubitemid 35461297)
14. Corrigall WA, Franklin KB, Coen KM, Clarke PB, (1992) The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology (Berl) 107: 285-289.
15. Das D, Tan X, Easteal S, (2011) Effect of model choice in genetic association studies: DRD4 Exon III VNTR and cigarette use in young adults. Am J Med Genet B Neuropsychiatr Genet 156: 346-351.
16. De Wolff M, van Ijzendoorn M, (1997) Sensitivity and attachment: a meta-analysis on parental antecedents of infant attachment. Child Dev 68: 571-591. (Pubitemid 127454346)
17. Ding Y-C, Chi H-C, Grady DL, Morishima A, Kidd JR, Kidd KK, Flodman P, Spence MA, Schuck S, Swanson JM, Zhang Y, Moyzis RK, (2002) Evidence of positive selection acting at the human dopamine receptor D4 gene locus. Proc Natl Acad Sci U S A 99: 309-314. (Pubitemid 34060359)
18. Faraone SV, Doyle AE, Mick E, Biederman J, (2001) Meta-analysis of the association between the 7-repeat allele of the dopamine D4 receptor gene and attention deficit hyperactivity disorder. Am J Psychiatry 158: 1052-1057. (Pubitemid 32623108)
19. Filbey FM, Claus ED, Morgan M, Forester GR, Hutchison K, (2011) Dopaminergic genes modulate response inhibition in alcohol abusing adults. Addict Biol. DOI: 10.1111/j.1369-1600.2011.00328.x.
20. Goodman A, (2007) Neurobiology of addiction: an integrated review. Biochem Pharmacol 75: 266-322.
21. Grady DL, Chi H-C, Ding Y-C, Smith M, Wang E, Schuck S, Flodman P, Spence MA, Swanson JM, Moyzis RK, (2003) High prevalence of rare dopamine receptor D4 alleles in children diagnosed with attention-deficit hyperactivity disorder. Mol Psychiatry 8: 536-545. (Pubitemid 36829695)
22. Hazan C, Shaver P, (1987) Romantic love conceptualised as an attachment process. J Pers Soc Psychol 52: 511-524.
23. Hosmer D, Lemeshow S, (1992) Confidence interval estimation of interaction. Epidemiology 3: 452-456.
24. van Ijzendoorn MH, Bakermans-Kranenburg MJ, (2006) DRD4 7-repeat polymorphism moderates the association between maternal unresolved loss or trauma and infant disorganization. Attach Hum Dev 8: 291-307. (Pubitemid 44964429)
25. Insel T, (1997) A neurobiological basis of social attachment. Am J Psychiatry 154: 726-735. (Pubitemid 27230093)
26. Koob GF, Le Moal M, (1997) Drug abuse: hedonic homeostatic dysregulation. Science 278: 52-58. (Pubitemid 27446270)
27. Laucht M, Becker K, Blomeyer D, Schmidt MH, (2007) Novelty seeking involved in mediating the association between the dopamine D4 receptor gene exon III polymorphism and heavy drinking in male adolescents: results from a high-risk community sample. Biol Psychiatry 61: 87-92. (Pubitemid 44855746)
28. Laucht M, Becker K, El-Faddagh M, Hohm E, Schmidt MH, (2005) Association of the DRD4 exon III polymorphism with smoking in fifteen-year-olds: a mediating role for novelty seeking? J Am Acad Child Adolesc Psychiatry 44: 477-484. (Pubitemid 40559696)
29. Lynskey MT, Agrawal A, Health AC, (2010) Genetically informative research on adolescent substance use: methods, findings and challenges. J Am Acad Child Adolesc Psychiatry 49: 1202-1213.
30. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M, Clark AG, Eichler EE, Gibson G, Haines JL, Mackay TF, McCarroll SA, Visscher PM, (2009) Finding the missing heritability of complex diseases. Nature 8: 747-753.
31. Maselko J, Kubzansky L, Lipsitt L, Buka SL, (2010) Mother's affection at 8 months predicts emotional distress in adulthood. J Epidemiol Community Health 65: 621-625.
32. McGeary JE, Esposito-Smythers C, Spirito A, Monti PM, (2007) Associations of the dopamine D4 receptor gene VNTR polymorphism with drug use in adolescent psychiatric inpatients. Pharmacol Biochem Behav 86: 401-406. (Pubitemid 46282054)
33. Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M, (2011) Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev 12: 524-538.
34. Midanik L, (1982) The validity of self-reported alcohol consumption and alcohol problems: a literature review. Br J Addict 77: 357-382. (Pubitemid 13189805)
35. de Minzi MCR, (2006) Loneliness and depression in middle and late childhood: the relationship to attachment and parental styles. J Genet Psychol 167: 189-210.
36. Murray L, Halligan SL, Adams G, Patterson P, Goodyer IM, (2006) Socioemotional development in adolescents at risk for depression: the role of maternal depression and attachment style. Dev Psychopathol 18: 489-516.
37. Nikolaidis A, Gray J, (2010) ADHD and the DRD4 exon III 7-repeat polymorphism: an international meta-analysis. Soc Cogn Affect Neurosci 5: 188-193.
38. Olsson CA, Byrnes G, Lotfi-Miri M, Collins V, Williamson R, Patton GC, Anney RJL, (2005) Association between 5-HTTLPR genotypes and persisting patterns of anxiety and alcohol use: results from a 10-year longitudinal study of adolescent mental health. Mol Psychiatry 10: 868-876. (Pubitemid 43080121)
39. Patton GC, Carlin JB, Coffey C, Wolfe R, Hibbert M, Bowes G, (1998) The course of early smoking: a population-based cohort study over three years. Addiction 93: 1251-1260. (Pubitemid 28370598)
40. Pierce C, 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. (Pubitemid 41821810)
41. Ray LA, Bryan A, MacKillop J, McGeary J, Hesterberg K, Hutchison KE, (2008) The dopamine D4 receptor (DRD4) gene exon III polymorphism, problematic alcohol use and novelty seeking: direct and mediated genetic effects. Addict Biol 14: 238-244.
42. Rosendall F, Siscovick D, Schwartz S, Beverly R, Psaty B, Longstreth W Jr, Raghunathan T, Koepsell T, Reitsma P, (1997) Factor V Leiden (resistance to activated protein C) increases the risk of myocardial infarction in young women. Blood 89: 2817-2821. (Pubitemid 27172567)
43. Rossing MA, (1998) Genetic influences on smoking: candidate genes. Environ Health Perspect 106: 231-238. (Pubitemid 28282501)
44. Rothman K, Greenland S, Lash T, (2008) Modern Epidemiology. Philadelphia, PA: Lippincott Williams & Wilkins.
45. Rubin DB, (1987) Multiple Imputation for Non-Response in Surveys. New York: Wiley.
46. Rubinstein M, Phillips TJ, Bunzow JR, Falzone TL, Dziewczapolski G, Zhang G, Fang Y, Larson JL, McDougall JA, Chester JA, Saez C, Pugsley TA, Gershanik O, Low MJ, Grandy DK, (1997) Mice lacking dopamine D4 receptors are supersensitive to ethanol, cocaine, and metamphetamine. Cell 90: 991-1001. (Pubitemid 27408513)
47. Saccone SF, Hinrichs AL, Saccone NL, Chase GA, Konvicka K, Madden PAF, Breslau N, Johnson EO, Hatsukami D, Pomerleau OF, Swan GE, Goate AM, Rutter J, Bertelsen S, Fox L, Fugman D, Martin NG, Montgomery GW, Wang E, Ballinger DG, Rice JP, Bierut LJ, (2007) Cholinergic nicotinic receptor genes implicated in a nicotine dependence association study targeting 348 candidate genes with 3713 SNPs. Hum Mol Genet 16: 36-49. (Pubitemid 46152543)
48. Saccone SF, Bierut LJ, Chesler EJ, Kalivas PW, Lerman C, Saccone NL, Uhl GR, Li CY, Philip VM, Edenberg HJ, S.T. S, Feolo M, Moyzis RK, Rutter JL, (2009) Supplementing high-density SNP microarrays for additional coverage of disease-related genes: addiction as a paradigm. PLoS One 4: e5225.
49. Schafer JL, (1997) Analysis of Incomplete Data. London: Chapman & Hall.
50. Schoots O, Van Tol HH, (2003) The human dopamine D4 receptor repeat sequences modulate expression. Pharmacogenomics J 3: 343-348. (Pubitemid 38072172)
51. Shaver PR, Schachner DA, Mikulincer M, (2005) Attachment style, excessive reassurance seeking, relationship processes, and depression. Pers Soc Psychol B 31: 343-359. (Pubitemid 40687377)
52. Shields PG, Lerman C, Audrain J, Bowman ED, Main D, Boyd NR, Caporaso NE, (1998) Dopamine D4 receptors and the risk of cigarette smoking in African-Americans and Caucasians. Cancer Epidemiol Biomarkers Prev 7: 453-458. (Pubitemid 28354105)
53. Spriggs M, Olsson CA, Hall W, (2008) How will information about the genetic risk of mental disorders impact on stigma? Aust N Z J Psychiatry 42: 214-220. (Pubitemid 351234191)
54. Sroufe L, Egeland B, Carlson E, (2005) The Development of the Person: The Minnesota Study of Risk and Adaptation from Birth to Adulthood. New York, NY: The Guilford Press.
55. Stanton WR, McClelland M, Elwood C, Ferry D, Silva PA, (1996) Prevalence, reliability and bias of adolescents' reports of smoking and quitting. Addict Biol 91: 1705-1714. (Pubitemid 26393431)
56. Vandenbergh DJ, O'Connor RJ, Grant MD, Jefferson AL, Vogler GP, Strasser AA, Kozlowski LT, (2007) Dopamine receptor genes (DRD2, DRD3 and DRD4) and gene-gene interactions associated with smoking-related behaviors. Addict Biol 12: 106-116. (Pubitemid 46406006)
57. Vandenbroucke J, Koster T, Briet E, Reitsma P, Bertina R, Rosendall F, (1994) Increased risk for venous thrombosis among oral contraceptive users who are carriers of factor V Leiden mutation. Lancet 344: 1453-1457. (Pubitemid 24351698)
58. Vandenbroucke JP, von Elm E, Altman DG, Gøtzsche PC, Mulrow CD, Pocock SJ, Poole C, Schlesselman JJ, Egger M, (2007) Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration. Ann Intern Med 147: W-163-W-194.
59. VanderWeele TJ, Vansteelandt S, Robins JM, (2010) Marginal structural models for sufficient cause interactions. Am J Epidemiol 171: 506-514.
60. Wang E, Ding Y-C, Flodman P, Kidd JR, Kidd KK, Grady DL, Ryder OA, Spence MA, Swanson JM, Moyzis RK, (2004) The genetic architecture of selection at the human dopamine receptor D4 (DRD4) gene locus. Am J Hum Genet 74: 931-944. (Pubitemid 38568966)
61. Wang ET, Kodama G, Baldi R, Moyzis RK, (2006) Global landscape of recent inferred Darwinian selection for Homo sapiens. PNAS 103: 135-140. (Pubitemid 43076117)
62. Weiss N, (2007) Assessing the influence of a genetic characteristic on disease in the presence of a strong environmental etiology. Epidemiology 18: 429-430. (Pubitemid 46955307)
63. van der Zwaluw CS, Larsen H, Engels RC, (2011) Best friends and alcohol use in adolescence: the role of the dopamine D4 receptor gene. Addict Biol. DOI: 10.1111/j.1369-1600.2010.00305.x. Epub ahead of print.