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Child dopamine active transporter 1 genotype and parenting: Evidence for evocative gene–environment correlations

  • Elizabeth P. Hayden (a1), Brigitte Hanna (a1), Haroon I. Sheikh (a1), Rebecca S. Laptook (a2), Jiyon Kim (a2), Shiva M. Singh (a1) and Daniel N. Klein (a2)...

Abstract

The dopamine active transporter 1 (DAT1) gene is implicated in psychopathology risk. Although the processes by which this gene exerts its effects on risk are poorly understood, a small body of research suggests that the DAT1 gene influences early emerging negative emotionality, a marker of children's psychopathology risk. As child negative emotionality evokes negative parenting practices, the DAT1 gene may also play a role in gene–environment correlations. To test this model, children (N = 365) were genotyped for the DAT1 gene and participated in standardized parent–child interaction tasks with their primary caregiver. The DAT1 gene 9-repeat variant was associated with child negative affect expressed toward the parent during parent–child interactions, and parents of children with a 9-repeat allele exhibited more hostility and lower guidance/engagement than parents of children without a 9-repeat allele. These gene–environment associations were partially mediated by child negative affect toward the parent. The findings implicate a specific polymorphism in eliciting negative parenting, suggesting that evocative associations play a role in elevating children's risk for emotional trajectories toward psychopathology risk.

Copyright

Corresponding author

Address correspondence and reprint requests to: Elizabeth Hayden, Department of Psychology, University of Western Ontario, London, ON N6A 3K7, Canada; E-mail: ehayden@uwo.ca.

References

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Auerbach, J. G., Faroy, M., Ebstein, R., Kahana, M., & Levine, J. (2001). The association of the dopamine D4 receptor gene (DRD4) and the serotonin transporter promoter gene (5-HTTLPR) with temperament in 12-month-old infants. Journal of Child Psychology and Psychiatry, 42, 777783.
Badgaiyan, R. D., Fischman, A. J., & Alpert, N. M. (2009). Dopamine release during human emotional processing. NeuroImage, 47, 20412045.
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2006). Gene–environment interaction of the dopamine D4 receptor (DRD4) and observed maternal insensitivity in predicting externalizing behavior in preschoolers. Developmental Psychobiology, 48, 406409.
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, 3952.
Belsky, J., & Barends, N. (2002). Personality and parenting. In Bornstein, M. H. (Ed.), Handbook of parenting: Vol. 3. Being and becoming a parent (2nd ed., pp. 415438). Mahwah, NJ: Erlbaum.
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885908.
Berridge, K. C., & Robinson, T. E. (1998). What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience? Brain Research Reviews, 28, 309369.
Bressan, R. A., & Crippa, J. A. (2005). The role of dopamine in reward and pleasure behavior—Review of data from preclinical research. Acta Psychiatrica Scandinavia, 111(Suppl. 427), 1421.
Burke, J. D., Pardini, D. A., & Loeber, R. (2008). Reciprocal relationships between parenting behavior and disruptive psychopathology from childhood through adolescence. Journal of Abnormal Child Psychology, 36, 679692.
Cameron, N. M., Parent, C., Champagne, F. A., Fish, E. W., Ozaki-Kuroda, K., & Meaney, M. J. (2005). The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neuroscience & Biobehavioral Reviews, 29, 843865.
Caron, A., Weiss, B., Harris, V., & Catron, T. (2006). Parenting behavior dimensions and child psychopathology: Specificity, task dependency, and interactive relations. Journal of Clinical Child and Adolescent Psychology, 35, 3445.
Carson, J. L., & Parke, R. D. (1996). Reciprocal negative affect in parent–child interactions and children's peer competency. Child Development, 67, 22172226.
Caspi, A., Hariri, A. R., Holmes, A., Uher, R., & Moffitt, T. E. (2010). Genetic sensitivity to the environment: The case of the serotonin transporter gene and its implications for studying complex diseases and traits. American Journal of Psychiatry, 167, 509527.
Chen, C., Chen, C., Moyzis, R., Stern, H., He, Q., Li, H., et al. (2011). Contributions of dopamine-related genes and environmental factors to highly sensitive personality: A multi-step neuronal system-level approach. PLoS ONE, 6, e21636.
Clark, L. A. (2005). Temperament as a unifying basis for personality and psychopathology. Journal of Abnormal Psychology, 114, 505521.
Clarke, H., Flint, J., Attwood, A. S., & Munafò, M. R. (2010). Association of the 5-HTTLPR genotype and unipolar depression: A meta-analysis. Psychological Medicine, 40, 17671778.
Cook, E. H., Stein, M. A., Krasowski, M. D., Cox, N. J., Olkon, D. M., Kieffer, J. E., et al. (1995). Association of attention-deficit disorder and the dopamine transporter gene. American Journal of Human Genetics, 56, 993998.
Coplan, R. J., Arbeau, K. A., & Armer, M. (2008). Don't fret, be supportive! Maternal characteristics linking child shyness to psychosocial and school adjustment in kindergarten. Journal of Abnormal Child Psychology, 36, 359371.
Deater-Deckard, K. (2000). Parenting and child behavioral adjustment in early childhood: A quantitative genetic approach to studying family processes. Child Development, 71, 468484.
Depue, R. A., & Morrone-Strupinsky, J. V. (2005). A neurobehavioral model of affiliative bonding: implications for conceptualizing a human trait of affiliation. Behavioral and Brain Sciences, 28, 313350.
DeRubeis, R. J., Hollon, S. D., Amsterdam, J. D., Shelton, R. C., Young, P. R., Salomon, R. M., et al. (2005). Cognitive therapy vs medications in the treatment of moderate to severe depression. Archives of General Psychiatry, 62, 409416.
Dick, D. M., Agrawal, A., Shuckit, M. A., Bierut, L., Hinrichs, A., Fox, L., et al. (2006). Marital status, alcohol dependence, and GABRA2: Evidence for gene–environment correlation and interaction. Journal of Studies on Alcohol, 67, 185194.
Dick, D. M., Latendresse, S. J., & Riley, B. (2011). Incorporating genetics into your studies: A guide for social scientists. Frontiers in Child and Neurodevelopmental Psychiatry, 17, 111.
Duncan, L. E., & Keller, M. C. (2011). A critical review of the first 10 years of candidate gene-by-environment interaction research in psychiatry. American Journal of Psychiatry, 168, 10411049.
Dunlop, B. W., & Nemeroff, C. B. (2007). The role of dopamine in the pathophysiology of depression. Archives of General Psychiatry, 64, 327337.
Dunn, L. M., & Dunn, L. M. (1997). Peabody Picture Vocabulary Test (3rd ed.). Circle Pines, MN: American Guidance Service.
Durston, S., Fossella, J. A., Mulder, M. J., Casey, B. J., Ziermans, T. B., Vessaz, M. N., et al. (2008). Dopamine transporter gene conveys familial risk of attention-deficit/hyperactivity disorder through striatal activation. Journal of the American Academy of Child & Adolescent Psychiatry, 47, 6167.
Egeland, B., Weinfield, N., Hiester, M., Lawrence, C., Pierce, S., Chippendale, K., et al. (1995). Teaching tasks administration and scoring manual. Minneapolis, MN: University of Minnesota Institute of Child Development.
Eisenberg, N., Valiente, C., Spinrad, T. L., Cumberland, A., Liew, J., Reiser, M., et al. (2009). Longitudinal relations of children's effortful control, impulsivity, and negative emotionality to their externalizing, internalizing, and co-occurring behavior problems. Developmental Psychology, 45, 9881008.
Eley, T. C., Napolitano, M., Lau, J. Y. F., & Gregory, A. M. (2010). Does childhood anxiety evoke maternal control? A genetically informed study. Journal of Child Psychology and Psychiatry, 51, 772779.
Elkin, I., Shea, M. T., Watkins, J. T., Impber, S. D., Sotsky, S. M., Collins, J. F., et al. (1989). NIMH Treatment of Depression Collaborative Research Program: General effectiveness of treatments. Archives of General Psychiatry, 46, 971982.
Englund, M. M., Luckner, A. E., Whaley, G. J. L., & Egeland, B. (2004). Children's achievement in early elementary school: Longitudinal effects of parental involvement, expectations, and quality of assistance. Journal of Educational Psychology, 96, 723730.
Forbes, E. E., Brown, S. M., Kimak, M., Ferrell, R. E., Manuck, S. B., & Hariri, A. R. (2009). Genetic variation in components of dopamine neurotransmission impacts ventral striatal reactivity associated with impulsivity. Molecular Psychiatry, 14, 6070.
Ge, X., Conger, R. D., Cadoret, R. J., Neiderhiser, J. M., Yates, W., Troughton, E., et al. (1996). The developmental interface between nature and nurture: A mutual influence model of child antisocial behavior and parent behaviors. Developmental Psychology, 32, 574589.
Goldsmith, H. H., Buss, K. A., & Lemery, K. S. (1997). Toddler and childhood temperament: Expanded content, stronger genetic evidence, new evidence for the importance of the environment. Developmental Psychology, 33, 891905.
Gunnar, M. R., & Vazquez, D. M. (2006). Stress neurobiology and developmental psychopathology. In Cicchetti, D. & Cohen, D. (Eds.), Developmental psychopathology: Developmental neuroscience (pp. 533577). Hoboken, NJ: Wiley.
Hasler, G., Drevets, W. C., Manji, H. K., & Charney, D. S. (2004). Discovering endophenotypes for major depression. Neuropsychopharmacology, 29, 17651781.
Hayden, E. P., Klein, D. N., Dougherty, L. R, Olino, T. M., Laptook, R. S., Dyson, M. W., et al. (2010). The dopamine D2 receptor gene and depressive and anxious symptoms in childhood: Associations and evidence for gene–environment correlation and gene–environment interaction. Psychiatric Genetics, 20, 304310.
Heinz, A., Goldman, D., Jones, D. W., Palmour, R., Hommer, D., Gorey, J. D., et al. (2000). Genotype influences in vivo dopamine transporter availability in human striatum. Neuropsychopharmacology, 22, 133139.
Hill, W. G., Goddard, M. E., & Visscher, P. M. (2008). Data and theory point to mainly additive genetic variance for complex traits. PLoS Genet, 4, e1000008.
Hollingshead, A. B. (1975). Four Factor Index of Social Status. Unpublished manuscript, Yale University.
Holmboe, K., Nemoda, Z., Fearon, R. M. P., Sasvari-Szekely, M., & Johnson, M. H. (2011). Dopamine D4 receptor and serotonin transporter gene effects on the longitudinal development of infant temperament. Genes, Brain, and Behavior, 10, 513522.
Hutchison, K. E., Stallings, M., McGeary, J., & Bryan, A. (2004). Population stratification in the candidate gene study: Fatal threat or red herring? Psychological Bulletin, 130, 6679.
Jaffee, S. R., & Price, T. S. (2007). Gene–environment correlations: A review of the evidence and implication for prevention of mental illness. Molecular Psychiatry, 12, 432442.
Jones, M. B., & Szatmari, P. (2002). A risk-factor model of epistatic interaction, focusing on autism. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 114, 558565.
Joyce, P. R., McHugh, P. C., Light, K. J., Rowe, S., Miller, A. L., & Kennedy, M. A. (2009). Relationships between angry–impulsive personality traits and genetic polymorphisms of the dopamine transporter. Biological Psychiatry, 66, 717721.
Kendler, K. S. (2005). “A gene for …”: The nature of gene action in psychiatric disorders. American Journal of Psychiatry, 162, 12431252.
Khan, A., Brodhead, A. E., Kolts, R. L., & Brown, W. A. (2005). Severity of depressive symptoms and response to antidepressants and placebo in antidepressant trials .Journal of Psychiatric Research, 39, 145150.
Lahey, B. B., Rathouz, P. J., Chronis-Tuscano, A., Waldman, I. D., Lee, S. S., Pelham, W. E., et al. (2011). Interactions between early parenting and a polymorphism of the child's dopamine transporter gene in predicting future child conduct disorder symptoms. Journal of Abnormal Psychology, 120, 3345.
Lawrence, A. D., Calder, A. J., McGowan, S. W., & Grasby, P. M. (2002). Selective disruption of the recognition of facial expressions of anger. NeuroReport, 13, 881884.
Lee, S. S., Chronis-Tuscano, A., Keenan, K., Pelham, W. E., Loney, J., Van Hulle, C. A., et al. (2010). Association of maternal dopamine transporter genotype with negative parenting: Evidence for gene x environment interaction with child disruptive behavior. Molecular Psychiatry, 15, 548558.
Lee, S. S., Lahey, B. B., Waldman, I., Van Hulle, C. A., Rathouz, P., Pelham, W. E., et al. (2007). Association of dopamine transporter genotype with disruptive behavior disorders in an eight-year longitudinal study of children and adolescents. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 144, 310317.
Lengua, L. J., & Kovacs, E. A. (2005). Bidirectional associations between temperament and parenting and the prediction of adjustment problems in middle childhood. Applied Developmental Psychology, 26, 2138.
Lettre, G., Lange, C., & Hirschhorn, J. N. (2007). Genetic model testing and statistical power in population-based association studies of quantitative traits. Genetic Epidemiology, 31, 358362.
Lucht, M., Barnow, S., Schroeder, W., Joergen Grabe, H., Finckh, U., John, U., et al. (2006). Negative perceived paternal parenting is associated with dopamine D2 receptor exon 8 and GABA(A) alpha 6 receptor variants: An explorative study. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 141, 167172.
MacKinnon, D. P., & Fairchild, A. J. (2009). Current directions in mediation analysis. Current Directions in Psychological Science, 18, 1620.
Martel, M. M., Nikolas, M., Jernigan, K., Friderici, K., & Nigg, J. T. (2010). Personality mediation of genetic effects on attention-deficit/hyperactivity disorder. Journal of Abnormal Child Psychology, 38, 633643.
McLeod, B. D., Weisz, J. R., & Wood, J. J. (2007). Examining the association between parenting and childhood depression: A meta-analysis. Clinical Psychology Review, 27, 9861003.
Meaney, M. J., & Szyf, M. (2005). Maternal care as a model for experience-dependent chromatin plasticity? Trends in Neuroscience, 28, 456463.
Mill, J. (2011). Epigenetic effects on gene function and their role in mediating gene–environment interactions. In Kendler, K. S., Jaffee, S. R., & Romer, D. (Eds.), The dynamic genome and mental health (pp. 145171). New York: Oxford University Press.
Miller, G. M., & Madras, B. K. (2002). Polymorphisms in the 3′-untranslated region of human and monkey dopamine transporter genes affect reporter gene expression. Molecular Psychiatry, 7, 4455.
Mills-Koonce, W. R., Propper, C. B., Gariepy, J.-L., Blair, C., Garrett-Peters, P., & Cox, M. J. (2007). Bidirectional genetic and environmental influences on mother and child behavior: The family system as the unit of analyses. Development and Psychopathology, 19, 10731087.
Montag, C., Buckholtz, J. W., Hartmann, P., Merz, M., Burk, C., Hennig, J., et al. (2008). COMT genetic variation affects fear processing: Psychophysiological evidence. Behavioral Neuroscience, 122, 901909.
Moore, J. H. (2003). The ubiquitous nature of epistasis in determining susceptibility to common human diseases. Human Heredity, 56, 7382.
Moore, P. S., Whaley, S. E., & Sigman, M. (2004). Interactions between mothers and children: Impacts of maternal and child anxiety. Journal of Abnormal Psychology, 113, 471476.
Munafò, M. R., Brown, S. M., & Hariri, A. R. (2008). Serotonin transporter (5-HTTLPR) genotype and amygdala activation: A meta-analysis. Biological Psychiatry, 63, 852857.
Pettit, G. S., Bates, J. E., & Dodge, K. A. (1997). Supportive parenting, ecological context, and children's adjustment: A seven-year longitudinal study. Child Development, 68, 908923.
Plomin, R., DeFries, J. C., & Loehlin, J. C. (1977). Genotype–environment interaction and correlation in the analysis of human behavior. Psychological Bulletin, 84, 309322.
Preacher, K. J., & Hayes, A. F. (2004). SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods, Instruments, and Computers, 36, 717731.
Preacher, K. J., & Hayes, A. F. (2008). Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods, 40, 879891.
Propper, C., Moore, G. A., Mills-Koonce, W. R., Tucker Halpern, C., Hill-Soderlung, A. L., Calkins, S. D., et al. (2008). Gene–environment contributions to the development of infant vagal reactivity: The interaction of dopamine and maternal sensitivity. Child Development, 79, 13771394.
Rhee, S. H., & Waldman, I. D. (2002). Genetic and environmental influences on antisocial behavior: A meta-analysis of twin and adoption studies. Psychological Bulletin, 128, 490529.
Rothbaum, F., & Weisz, J. R. (1994). Parenting caregiving and child externalizing in nonclinical samples: A meta-analysis. Psychological Bulletin, 116, 5574.
Rowe, D. C., Stever, C., Card, J. M. C., Cleveland, H. H., Sanders, M. L., Abramowitz, A., et al. (1998). The relation of the dopamine transporter gene (DAT1) to symptoms of internalizing disorders in children. Behavior Genetics, 28, 215225.
Rutter, M. (1991). Nature, nurture, and psychopathology: A new look at an old topic. Development and Psychopathology, 3, 125136.
Rutter, M. (2003). Commentary: Nature–nurture interplay in emotional disorders. Journal of Child Psychology and Psychiatry, 44, 934944.
Rutter, M. (2007). Gene–environment interdependence. Developmental Science, 10, 1218.
Rutter, M. (2009). Understanding and testing risk mechanisms for mental disorders. Journal of Child Psychology and Psychiatry, 50, 4452.
Rutter, M., Moffitt, T. E., & Caspi, A. (2006). Gene–environment interplay and psychopathology: Multiple varieties but real effects. Journal of Child Psychology and Psychiatry, 47, 226261.
Segman, R. H., Cooper-Kazaz, R., Macciardi, F., Goltser, T., Halfon, Y., Dobroborski, T., et al. (2002). Association between the dopamine transporter gene and posttraumatic stress disorder. Molecular Psychiatry, 7, 903907.
Sevy, S., Hassoun, Y., Bechara, A., Yechiam, E., Napolitano, B., Burdick, K., et al. (2006). Emotion-based decision making in healthy subjects: Short-term effects of reducing dopamine levels. Psychopharmacology, 188, 228235.
Sheese, B. E., Voelker, P. M., Rothbart, M. K., & Posner, M. I. (2007). Parenting quality interacts with genetic variation in dopamine receptor D4 to influence temperament in early childhood. Development and Psychopathology, 19, 10391046.
Sheffield Morris, A., Silk, J. S., Steinberg, L., Sessa, F. M., Avenevoli, S., & Essex, M. J. (2002). Temperamental vulnerability and negative parenting as interacting predictors of child adjustment. Journal of Marriage and Family, 64, 461471.
Smith, H. J., Sheikh, H. I., Dyson, M. W., Olino, T. M., Laptook, R. S., Durbin, C. E., et al. (in press). Parenting and child DRD4 genotype interact to predict children's early emerging effortful control. Child Development.
Spanagel, R., & Weiss, F. (1999). The dopamine hypothesis of reward: Past and current status. Trends in Neuroscience, 22, 521527.
Stormshak, E. A., Bierman, K. L., McMahon, R. J., & Lengua, L. J. (2000). Parenting practices and child disruptive behavior problems in early elementary school. Journal of Clinical Child Psychology, 29, 1729.
Ueno, S. (2003). Genetic polymorphisms of serotonin and dopamine in mental disorders. Journal of Medical Investigation, 50, 2531.
Uher, R., & McGuffin, P. (2010). The moderation by the serotonin transporter gene of environmental adversity in the etiology of depression: 2009 update. Molecular Psychiatry, 15, 1822.
van de Giessen, E. M., de Win, M. M. L., Tanck, M. W. T., van den Brink, W., Baas, F., & Booij, J. (2009). Striatal dopamine transporter availability associated with polymorphisms in the dopamine transporter gene SLC6A3. Journal of Nuclear Medicine, 50, 4552.
van Dyck, C. H., Malison, R. T., Jacobsen, L. K., Seibyl, J. P., Staley, J. K., Laruelle, M., et al. (2005). Increased dopamine transporter availability associated with the 9-repeat allele of the SLC6A3 gene. Journal of Nuclear Medicine, 46, 745751.
Wacholder, S., Rothman, N., & Caporaso, N. (2002). Counterpoint: Bias from population stratification is not a major threat to the validity of conclusions from epidemiological studies of common polymorphisms and cancer. Cancer Epidemiology, Biomarkers & Prevention, 11, 513520.
Wood, D., Bruner, J. S., & Ross, G. (1976). The role of tutoring in problem solving. Journal of Child Psychology and Psychiatry, 17, 89100.
Young, S. E., Smolen, A., Corley, R. P., Krauter, K. S., DeFries, J. C., Crowley, T. J., et al. (2002). Dopamine transporter polymorphism associated with externalizing behavior problems in children. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 114, 144149.
Zaslow, M. J., Weinfield, N. S., Gallagher, M., Hair, E. C., Ogawa, J. R., Egeland, B., et al. (2006). Longitudinal prediction of child outcomes from differing measures of parenting in a low-income sample. Developmental Psychology, 42, 2737.

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