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Mapping Pathways by Which Genetic Risk Influences Adolescent Externalizing Behavior: The Interplay Between Externalizing Polygenic Risk Scores, Parental Knowledge, and Peer Substance Use

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Abstract

Genetic predispositions and environmental influences both play an important role in adolescent externalizing behavior; however, they are not always independent. To elucidate gene–environment interplay, we examined the interrelationships between externalizing polygenic risk scores, parental knowledge, and peer substance use in impacting adolescent externalizing behavior across two time-points in a high-risk longitudinal sample of 1,200 adolescents (764 European and 436 African ancestry; Mage = 12.99) from the Collaborative Study on the Genetics of Alcoholism. Results from multivariate path analysis indicated that externalizing polygenic scores were directly associated with adolescent externalizing behavior but also indirectly via peer substance use, in the European ancestry sample. No significant polygenic association nor indirect effects of genetic risk were observed in the African ancestry group, likely due to more limited power. Our findings underscore the importance of gene–environment interplay and suggest peer substance use may be a mechanism through which genetic risk influences adolescent externalizing behavior.

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Acknowledgements

The Collaborative Study on the Genetics of Alcoholism (COGA), Principal Investigators B. Porjesz, V. Hesselbrock, T. Foroud; Scientific Director, A. Agrawal; Translational Director, D. Dick, includes eleven different centers: University of Connecticut (V. Hesselbrock); Indiana University (H.J. Edenberg, T. Foroud, J. Nurnberger Jr., Y. Liu); University of Iowa (S. Kuperman, J. Kramer); SUNY Downstate (B. Porjesz, J. Meyers, C. Kamarajan, A. Pandey); Washington University in St. Louis (L. Bierut, J. Rice, K. Bucholz, A. Agrawal); University of California at San Diego (M. Schuckit); Rutgers University (J. Tischfield, A. Brooks, R. Hart); The Children’s Hospital of Philadelphia, University of Pennsylvania (L. Almasy); Virginia Commonwealth University (D. Dick, J. Salvatore); Icahn School of Medicine at Mount Sinai (A. Goate, M. Kapoor, P. Slesinger); and Howard University (D. Scott). Other COGA collaborators include: L. Bauer (University of Connecticut); L. Wetherill, X. Xuei, D. Lai, S. O’Connor, M. Plawecki, S. Lourens (Indiana University); L. Acion (University of Iowa); G. Chan (University of Iowa; University of Connecticut); D.B. Chorlian, J. Zhang, S. Kinreich, G. Pandey (SUNY Downstate); M. Chao (Icahn School of Medicine at Mount Sinai); A. Anokhin, V. McCutcheon, S. Saccone (Washington University); F. Aliev, P. Barr (Virginia Commonwealth University); H. Chin and A. Parsian are the NIAAA Staff Collaborators. We continue to be inspired by our memories of Henri Begleiter and Theodore Reich, founding PI and Co-PI of COGA, and also owe a debt of gratitude to other past organizers of COGA, including Ting-Kai Li, P. Michael Conneally, Raymond Crowe, and Wendy Reich, for their critical contributions. This national collaborative study is supported by NIH Grant U10AA008401 from the National Institute on Alcohol Abuse and Alcoholism (NIAAA) and the National Institute on Drug Abuse (NIDA). The Externalizing Consortium: Principal Investigators: Danielle M. Dick, Philipp Koellinger, K. Paige Harden, Abraham A. Palmer. Lead Analysts: Richard Karlsson Linnér, Travis T. Mallard, Peter B. Barr, Sandra Sanchez-Roige. Significant Contributor: Irwin Waldman. The Externalizing Consortium has been supported by the National Institute of Alcohol Abuse and Alcoholism (R01AA015146 - administrative supplement), and the National Institute on Drug Abuse (R01DA050721). Additional funding for investigator effort has been provided by K02AA018755, U10AA008401, P50AA022537, as well as a European Research Council Consolidator Grant (647,648 EdGe). The content is solely the responsibility of the authors and does not necessarily represent the official views of the above funding bodies. The Externalizing Consortium would like to thank the following for making its research possible: 23andMe, Add Health, Vanderbilt University Medical Center’s BioVU, Collaborative Study on the Genetics of Alcoholism (COGA), the Psychiatric Genomics Consortium’s Substance Use Disorders working group, UK10K Consortium, UK Biobank, and Philadelphia Neurodevelopmental Cohort.

Funding

This study was funded by the National Institutes of Health through the National Institute on Alcohol Abuse and Alcoholism (U10AA008401, K02AA018755, K01AA024152) and the National Institute on Drug Abuse (R01DA050721).

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Authors and Affiliations

  1. Department of Psychology, Virginia Commonwealth University, Box 842018, 806 W Franklin St, Richmond, VA, 23284, USA

    Sally I-Chun Kuo, Jessica E. Salvatore, Peter B. Barr, Fazil Aliev & Danielle M. Dick

  2. Department of Psychiatry, Washington University in St. Louis, St. Louis, MO, USA

    Andrey Anokhin & Kathleen K. Bucholz

  3. Department of Psychiatry, University of Connecticut School of Medicine, Farmington, CT, USA

    Grace Chan & Victor Hesselbrock

  4. Department of Biochemistry and Molecular Biology, Indiana University, Indianapolis, IN, USA

    Howard J. Edenberg

  5. Department of Medical and Molecular Genetics, Indiana University, Indianapolis, IN, USA

    Howard J. Edenberg, Dongbing Lai & John I. Nurnberger Jr.

  6. Department of Psychiatry and Behavioral Sciences, State University of New York Downstate Medical Center, Brooklyn, NY, USA

    Chella Kamarajan & Gayathri Pandey

  7. Department of Psychiatry, University of Iowa, Iowa City, IA, USA

    John R. Kramer

  8. Department of Psychology, University of Texas at Austin, Austin, TX, USA

    Travis T. Mallard

  9. Department of Psychiatry, Indiana University, Indianapolis, IN, USA

    Martin H. Plawecki

  10. Department of Psychiatry, University of California San Diego, La Jolla, CA, USA

    Sandra Sanchez-Roige & Abraham A. Palmer

  11. Division of Genetic Medicine, Vanderbilt University Medical Center, Nashville, TN, USA

    Sandra Sanchez-Roige

  12. Department of Psychology, Emory University, Atlanta, GA, USA

    Irwin Waldman

  13. Institute of Genomic Medicine, University of California San Diego, La Jolla, CA, USA

    Abraham A. Palmer

  14. Department of Human and Molecular Genetics, Virginia Commonwealth University, Richmond, VA, USA

    Danielle M. Dick

Authors
  1. Sally I-Chun Kuo
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  2. Jessica E. Salvatore
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Externalizing Consortium

Corresponding author

Correspondence to Sally I-Chun Kuo.

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Conflict of interest

Authors Sally I-Chun Kuo, Jessica E. Salvatore, Peter B. Barr, Fazil Aliev, Andrey Anokhin, Kathleen K. Bucholz, Grace Chan, Howard J. Edenberg, Victor Hesselbrock, Chella Kamarajan, John R. Kramer, Dongbing Lai, Travis T. Mallard, John I. Nurnberger Jr., Gayathri Pandey, Martin H. Plawecki, Sandra Sanchez-Roige, Irwin Waldman, Abraham A. Palmer, Externalizing Consortium, and Danielle M. Dick declare that they have no conflict of interest to report.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Human and Animal Rights

No animal subjects were used in the studies and no human experimental protocols were carried out.

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Informed consent was obtained from all individual participants included in the study.

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Kuo, S.IC., Salvatore, J.E., Barr, P.B. et al. Mapping Pathways by Which Genetic Risk Influences Adolescent Externalizing Behavior: The Interplay Between Externalizing Polygenic Risk Scores, Parental Knowledge, and Peer Substance Use. Behav Genet 51, 543–558 (2021). https://doi.org/10.1007/s10519-021-10067-7

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