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Beyond risk: Prospective effects of GABA Receptor Subunit Alpha-2 (GABRA2) × Positive Peer Involvement on adolescent behavior

Published online by Cambridge University Press:  17 June 2016

Elisa M. Trucco ,
Sandra Villafuerte ,
Margit Burmeister  and
Robert A. Zucker
Elisa M. Trucco*
Affiliation:
University of Michigan
Sandra Villafuerte
Affiliation:
University of Michigan
Margit Burmeister
Affiliation:
University of Michigan
Robert A. Zucker
Affiliation:
University of Michigan
*
Address correspondence and reprint requests to: Elisa M. Trucco, Center for Children and Families, Florida International University, AHC-1, Room 237, 11200 SW 8th Street, Miami, FL 33199; E-mail: [email protected].
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Abstract

Research on Gene × Environment interactions typically focuses on maladaptive contexts and outcomes. However, the same genetic factors may also impact susceptibility to positive social contexts, leading to adaptive behavior. This paper examines whether the GABA receptor subunit alpha-2 (GABRA2) single nucleotide polymorphism rs279858 moderates the influence of positive peer affiliation on externalizing behavior and various forms of competence. Regions of significance were calculated to determine whether the form of the interaction supported differential susceptibility (increased sensitivity to both low and high positive peer affiliation) or vantage sensitivity (increased sensitivity to high positive peer affiliation). It was hypothesized that those carrying the homozygous minor allele (GG) would be more susceptible to peer effects. A sample (n = 300) of primarily male (69.7%) and White (93.0%) adolescents from the Michigan Longitudinal Study was assessed from ages 12 to 17. There was evidence for prospective Gene × Environment interactions in three of the four models. At low levels of positive peer involvement, those with the GG genotype were rated as having fewer adaptive outcomes, while at high levels they were rated as having greater adaptive outcomes. This supports differential susceptibility. Conceptualizing GABRA2 variants as purely risk factors may be inaccurate. Genetic differences in susceptibility to adaptive environmental exposures warrants further investigation.

Type
Regular Articles
Information
Development and Psychopathology , Volume 29 , Issue 3 , August 2017 , pp. 711 - 724
Copyright
Copyright © Cambridge University Press 2016 

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Footnotes

We thank the families participating in the Michigan Longitudinal Study. This research was supported by Grants K08 AA023290 (to E.M.T.), R01 DA027261 (to R.A.Z., M.M.H., and J.K.Z.), and R01 AA007065 (to R.A.Z. and M.M.H.), T32 AA007477 (to R.A.Z. and K.B.) and the Ruth L. Kirchstein National Research Service Award T32 DA007267 (to M.G.). The contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH. Funding was also received from a pilot grant from the University of Michigan MICHR CTSA program, supported in part by the National Center for Research Resources (Grant UL1RR024986), which is now at the National Center for Advancing Translational Sciences (Grant 2UL1TR000433).

References

Achenbach, T. (1991). Manual for the Youth Self-Report Form and 1991 Profile. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Achenbach, T. M., Dumenci, L., & Rescorla, L. A. (2002). Ten-year comparison of problems and competencies for national samples of youth: Self, parent, and teacher reports. Journal of Emotional and Behavioral Disorders, 10, 194–203. doi:10.1177/10634266020100040101 CrossRefGoogle Scholar
Agrawal, A., Edenberg, H. J., Foroud, T., Bierut, L. J., Dunne, G., Hinrichs, A. L., et al. (2006). Assocition of GABRA2 with drug dependence in the Collaborative Study of the Genetics of Alcoholism sample. Behavior Genetics, 36, 640–650. doi:10.1007/s10519-006-9069-4 CrossRefGoogle Scholar
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Differential susceptibility to rearing environment depending on dopamine-related genes: New evidence and a meta-analysis. Development and Psychopathology, 23, 39–52. doi:10.1017/S0954579410000635 CrossRefGoogle ScholarPubMed
Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Pijlman, F. T., Mesman, J., & Juffer, F. (2008). Experimental evidence for differential susceptibility: Dopamine D4 receptor polymorphism (DRD4 VNTR) moderates intervention effects on toddlers’ externalizing behavior in a randomized controlled trial. Developmental Psychology, 44, 293–300. doi:10.1037/0012-1649.44.1.293 CrossRefGoogle ScholarPubMed
Belsky, J., & Beaver, K. M. (2011). Cumulative-genetic plasticity, parenting and adolescent self-regulation. Journal of Child Psychology and Psychiatry, 52, 619–626. doi:10.1111/j.1469-7610.2010.02327.x CrossRefGoogle ScholarPubMed
Belsky, J., & Pluess, M. (2009). The nature (and nurture?) of plasticity in early human development. Perspectives on Psychological Science, 4, 345–351. doi:10.1111/j.1745-6924.2009.01136.x CrossRefGoogle ScholarPubMed
Bingham, C. R., Fitzgerald, H. E., & Zucker, R. A. (1995). Peer Behavior Profile/Peer Activities Questionnaire. Unpublished manuscript, Michigan State University.Google Scholar
Brody, G. H., Chen, Y., & Beach, S. R. (2013). Differential susceptibilty to prevention: GABAergic, dopaminergic, and multilocus effects. Journal of Child Psychology and Psychiatry, 54, 863–871. doi:10.1111/jcpp.12042 CrossRefGoogle Scholar
Conley, D., Rauscher, E., & Siegal, M. L. (2013). Beyond orchids and dandelions: Testing the 5-HTT “risky” allele for evidence of phenotypic capacitance and frequency-dependent selection. Biodemography and Social Biology, 59, 37–56. doi:10.1080/19485565.2013.774620 CrossRefGoogle ScholarPubMed
Covault, J., Gelernter, J., Hesselbrock, V., Nellissery, M., & Kranzler, H. R. (2004). Allelic and haplotypic association of GABRA2 with alcohol depenence. American Journal of Medical Genetics, 129B, 104–109.Google Scholar
Dick, D. M., Bierut, L., Hinrichs, A., Fox, L., Bucholz, K. K., Kramer, J., et al. (2006). The role of GABRA2 in risk for conduct disorder and alcohol and drug dependence across developmental stages. Behavior Genetics, 36, 577–590.CrossRefGoogle ScholarPubMed
Dick, D. M., Latendresse, S. J., Lansford, J. E., Budde, J. P., Goate, A., Dodge, K. A., et al. (2009). Role of GABRA2 in trajectories of externalizing behavior across development and evidence of moderation by parental monitoring. Archives of General Psychiatry, 66, 649–657. doi:10.1001/archgenpsychiatry.2009.48 CrossRefGoogle ScholarPubMed
Edenberg, H. J., Dick, D. M., Xuei, X., Tian, H., Almasy, L., Bauer, L. O., et al. (2004). Variations in GABRA2, encoding the α2 subunit of the GABAA receptor, are associated with alcohol dependence and with brain oscillations. American Journal of Human Genetics, 74, 705–714. doi:10.1086/383283 CrossRefGoogle Scholar
Elek, E., Miller-Day, M., & Hecht, M. L. (2006). Influences on personal, injunctive, and descriptive norms on early adolescent substance use. Journal of Drug Issues, 36, 147–172. doi:10.1177/002204260603600107 CrossRefGoogle Scholar
Enoch, M. A. (2008). The role of GABAA receptors in the development of alcoholism. Pharmacology Biochemistry and Behavior, 90, 95–104. doi:10.1016/j.pbb.2008.03.007 CrossRefGoogle ScholarPubMed
Enoch, M. A., Hodgkinson, C. A., Yuan, Q., Albaugh, B., Virkkunen, M., & Goldman, D. (2009). GABRG1 and GABRA2 as independent predictors for alcoholism in two populations. Neuropsychopharmacology, 34, 1245–1254. doi:10.1038/npp.2008.171 CrossRefGoogle ScholarPubMed
Guyer, A. E., McClure-Tone, E. B., Shiffrin, N. D., Pine, D. S., & Nelson, E. E. (2009). Probing the neural correlates of anticipated peer evaluation in adolescence. Child Development, 80, 1000–1015. doi:10.1111/j.1467-8624.2009.01313.x CrossRefGoogle ScholarPubMed
Heitzeg, M. M., Villafuerte, S., Weiland, B. J., Enoch, M. A., Burmeister, M., Zubieta, J. K., et al. (2014). Effect of GABRA2 genotype on development of incentive-motivation circuitry in a sample enriched for alcoholism risk. Neuropsychopharmacology, 39, 3077–3086. doi:10.1038/npp.2014.161 CrossRefGoogle Scholar
Hirschi, T. (1969). Causes of delinquency. Berkeley, CA: University of California Press.Google Scholar
Hodgkinson, C. A., Yuan, Q., Xu, K., Shen, P. H., Heinz, E., Lobos, E. A., et al. (2008). Addictions biology: Haplotype-based analysis for 130 candidate genes on a single array. Alcohol and Alcoholism, 43, 505–515. doi:10.1093/alcalc/agn032 CrossRefGoogle ScholarPubMed
Hymel, S., Comfort, C., Schonert-Reichl, K., & McDougall, P. (1996). Academic failure and school dropout: The influence of peers. In Wentzel, K. & Juvonen, J. (Eds.), Social motivation: Understanding children's school adjustment. Cambridge: Cambridge University Press.Google Scholar
Jessor, R., Costa, F., Jessor, L., & Donovan, J. E. (1983). Time of first intercourse: A prospective study. Journal of Personality and Social Psychology, 44, 608–626.CrossRefGoogle Scholar
Kochanska, G., Kim, S., Barry, R. A., & Philibert, R. A. (2011). Children's genotypes interact with maternal responsive care in predicting children's competence: Diathesis–stress or differential susceptibility? Development and Psychopathology, 23, 605–616. doi:10.1017/S0954579411000071 CrossRefGoogle ScholarPubMed
Kretschmer, T., Dijkstra, J. K., Ormel, J., Verhurlst, F. C., & Veenstra, R. (2013). Dopamine receptor D4 gene moderates the effect of positive and negative peer experiences on later delinquency: The Tracking Adolescents’ Individual Lives Survey study. Development and Psychopathology, 25, 1107–1117. doi:10.1017/S0954579413000400 CrossRefGoogle ScholarPubMed
Kretschmer, T., Vitaro, F., & Barker, E. D. (2014). The association between peer and own aggression is moderated by the BDNF val-met polymorphism. Journal of Research on Adolescence, 24, 177–185. doi:10.1111/jora.12050 CrossRefGoogle ScholarPubMed
Masten, A. S., Morison, O., & Pellegrini, D. S. (1985). A revised class play method of peer assessment. Developmental Psychology, 21, 523–533.CrossRefGoogle Scholar
Masten, C. L., Eisenberger, N. I., Borofsky, L. A., Pfeifer, J. H., McNealy, K., Mazziotta, J. C., et al. (2009). Neural correlates of social exclusion during adolescence: Understanding the distress of peer rejection. Social Cognitive and Affective Neuroscience, 4, 143–157. doi:10.1093/scan/nsp007 CrossRefGoogle ScholarPubMed
Nederhof, E., Belsky, J., Ormel, J., & Oldehinkel, A. J. (2012). Effects of divorce on Dutch boys’ and girls’ externalizing behavior in Gene × Environment perspective: Diathesis stress or differential susceptibility in the Dutch Tracking Adolescents’ Individual Lives Survey study? Development and Psychopathology, 24, 929–939. doi:10.1017/S0954579412000454 CrossRefGoogle ScholarPubMed
Padilla-Walker, L. M., & Bean, R. A. (2009). Negative and positive peer influence: Relations to positive and negative behaviors for African American, European American, and Hispanic adolescents. Journal of Adolescence, 32, 323–337. doi:10.1016/j.adolescence.2008.02.003 CrossRefGoogle ScholarPubMed
Perry, B. L., Pescosolido, B. A., Bucholz, K., Edenberg, H., Kramer, J., Kuperman, S., et al. (2013). Gender-specific gene-environment interaction in alcohol dependence: The impact of daily life events and GABRA2. Behavior Genetics, 43, 402–414. doi:10.1007/s10519-013-9607-9 CrossRefGoogle ScholarPubMed
Pluess, M. (2015). Vantage sensitivity: Environmental sensitivity to positive experiences as a function of genetic differences. Journal of Personality. Advance online publication. doi:10.1111/jopy.12218 Google ScholarPubMed
Pluess, M., & Belsky, J. (2012). Vantage sensitivty: Individual differences in response to postive experiences. Psychological Bulletin, 139, 901–916. doi:10.1037/a0030196 CrossRefGoogle Scholar
Preacher, K. J., Curran, P. J., & Bauer, D. J. (2006). Computational tools for probing interactions in multiple linear regression, multilevel modeling, and latent curve analysis. Journal of Educational and Behavioral Statistics, 31, 437–448. doi:10.3102/10769986031004437 CrossRefGoogle Scholar
Prinstein, M. J., & Wang, S. S. (2005). False consensus and adolescent peer contagion: Examining discrepancies between perceptions and actual reported levels of friends’ deviant and health risk behaviors. Journal of Abnormal Child Psychology, 33, 293–306. doi:10.1007/s10802-005-3566-4 CrossRefGoogle ScholarPubMed
Roisman, G. I., Newman, D. A., Fraley, R. C., Haltigan, J. D., Groh, A. M., & Haydon, K. C. (2012). Distinguishing differential susceptibility from diathesis–stress: Recommendations for evaluating interaction effects. Development and Psychopathology, 24, 389–409. doi:10.1017/S0954579412000065 CrossRefGoogle ScholarPubMed
Rose, R. J., Dick, D. M., Viken, R. J., Pulkkinen, L., & Kaprio, J. (2001). Drinking or abstaining at age 14? A genetic epidemiology study. Alcoholism, Clinical, and Experimental Research, 25, 1594–1604.CrossRefGoogle ScholarPubMed
SAS Institute Inc. (2011). SAS® 9.3 system options: Reference (2nd ed.). Cary, NC: Author.Google Scholar
Siddiqui, O., Mott, J., Andersen, T., & Flay, B. R. (1999). The application of poisson random-effects regression models of analyses of adolescents’ current level of smoking. Preventive Medicine, 29, 92–101. doi:10.1006/pmed.1999.0517 CrossRefGoogle ScholarPubMed
Spreckelmeyer, K. N., Krach, S., Kohls, G., Rademacher, L., Irmak, A., Konrad, K., et al. (2009). Anticipation of monetary and social reward differntly activates mesolimbic brain structures in men and women. Social Cognitive and Affective Neuroscience, 4, 158–165. doi:10.1093/scan/nsn051 CrossRefGoogle Scholar
Steinberg, L. (2008). A social neuroscience perspective on adolescent risk-taking. Developmental Review, 28, 78–106. doi:10.1016/j.dr.2007.08.002 CrossRefGoogle ScholarPubMed
Steinberg, L., & Monahan, K. C. (2007). Age differences in resistance to peer influence. Developmental Psychology, 43, 1531–1543. doi:10.1037/0012-1649.43.6.1531 CrossRefGoogle ScholarPubMed
Taylor, S. E., Way, B. M., Welch, W. T., Hilmert, C. J., Lehman, B. J., & Eisenberger, N. I. (2006). Early family environment, current adversity, the serotonin transporter promoter polymorphism, and depressive symptomatology. Biological Psychiatry, 60, 671–676. doi:10.1016/j.biopsych.2006.04.019 CrossRefGoogle ScholarPubMed
Tolan, P., Henry, D., Schoeny, M., Bass, A., Lovegrove, P., & Nichols, E. (2013). Mentoring interventions to affect juvenile delinquency and associated problems: A systematic review. Campbell Systematic Reviews, 10. doi:10.4073/csr.2013.10 Google Scholar
Trucco, E. M., Villafuerte, S., Heitzeg, M. M., Burmeister, M., & Zucker, R. A. (2014). Rule breaking mediates the developmental association between GABRA2 and adolescent susbtance abuse. Journal of Child Psychology and Psychiatry, 55, 1372–1379. doi:10.1111/jcpp.12244 CrossRefGoogle Scholar
Trucco, E. M., Villafuerte, S., Heitzeg, M. M., Burmeister, M., & Zucker, R. A. (2016). Susceptibility effects of GABA receptor subunit alpha-2 (GABRA2) variants and parental monitoring on externalizing behavior trajectories: Risk and protection conveyed by the minor allele. Development and Psychopathology, 28, 15–26. doi:10.1017/S0954579414000255 CrossRefGoogle Scholar
Villafuerte, S., Heitzeg, M. M., Foley, S., Wendy Yau, W. Y., Majczenko, K., Zubieta, J. K., et al. (2012). Impulsiveness and insula activation during reward anticipation are associated with genetic variants in GABRA2 in a family sample enriched for alcoholism. Molecular Psychiatry, 17, 511–519. doi:10.1038/mp.2011.33 CrossRefGoogle Scholar
Zucker, R. A., Ellis, D. A., Fitzgerald, H. E., Bingham, C. R., & Sanford, K. P. (1996). Other evidence for at least two alcoholisms: Part II. Life course variation in antisociality and heterogeneity of alcoholic outcome. Development and Psychopathology, 8, 831–848. doi:10.1017/S0954579400007458.CrossRefGoogle Scholar
Zuckerman, M. (1999). Vulnerability to psychopathology: A biosocial model. Washington, DC: American Psychological Association.CrossRefGoogle Scholar