Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-26T08:46:07.643Z Has data issue: false hasContentIssue false
  • English
  • Français

Epigenetic correlates of neonatal contact in humans

Published online by Cambridge University Press:  22 November 2017

Sarah R. Moore ,
Lisa M. McEwen ,
Jill Quirt ,
Alex Morin ,
Sarah M. Mah ,
Ronald G. Barr ,
W. Thomas Boyce  and
Michael S. Kobor
Sarah R. Moore*
Affiliation:
British Columbia Children's Hospital University of British Columbia
Lisa M. McEwen
Affiliation:
British Columbia Children's Hospital University of British Columbia
Jill Quirt
Affiliation:
British Columbia Children's Hospital
Alex Morin
Affiliation:
British Columbia Children's Hospital
Sarah M. Mah
Affiliation:
British Columbia Children's Hospital
Ronald G. Barr
Affiliation:
British Columbia Children's Hospital Canadian Institute for Advanced Research
W. Thomas Boyce
Affiliation:
University of British Columbia University of California, San Francisco Canadian Institute for Advanced Research
Michael S. Kobor
Affiliation:
British Columbia Children's Hospital University of British Columbia Canadian Institute for Advanced Research
*
Address correspondence and reprint requests to: Sarah R. Moore, Centre for Molecular Medicine and Therapeutics, British Columbia Children's Hospital, Department of Medical Genetics, University of British Columbia, 950 West 28th Avenue, Vancouver, British Columbia V5Z 4H4, Canada; E-mail: smoore@cmmt.ubc.ca.
Get access Rights & Permissions [Opens in a new window]

Abstract

Animal models of early postnatal mother–infant interactions have highlighted the importance of tactile contact for biobehavioral outcomes via the modification of DNA methylation (DNAm). The role of normative variation in contact in early human development has yet to be explored. In an effort to translate the animal work on tactile contact to humans, we applied a naturalistic daily diary strategy to assess the link between maternal contact with infants and epigenetic signatures in children 4–5 years later, with respect to multiple levels of child-level factors, including genetic variation and infant distress. We first investigated DNAm at four candidate genes: the glucocorticoid receptor gene, nuclear receptor subfamily 3, group C, member 1 (NR3C1), μ-opioid receptor M1 (OPRM1) and oxytocin receptor (OXTR; related to the neurobiology of social bonds), and brain-derived neurotrophic factor (BDNF; involved in postnatal plasticity). Although no candidate gene DNAm sites significantly associated with early postnatal contact, when we next examined DNAm across the genome, differentially methylated regions were identified between high and low contact groups. Using a different application of epigenomic information, we also quantified epigenetic age, and report that for infants who received low contact from caregivers, greater infant distress was associated with younger epigenetic age. These results suggested that early postnatal contact has lasting associations with child biology.

Type
Special Issue Articles
Information
Development and Psychopathology , Volume 29 , Special Issue 5: Biological and Behavioral Effects of Early Adversity on Multiple Levels of Development , December 2017 , pp. 1517 - 1538
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

We express our deepest gratitude to Dr. Meaghan Jones and Dr. Nicole Bush for their helpful feedback on earlier versions of this manuscript.

References

Baker-Andresen, D., Flavell, C. R., Li, X., & Bredy, T. W. (2013). Activation of BDNF signaling prevents the return of fear in female mice. Learning & Memory, 20, 237–240. doi:10.1101/lm.029520.112 CrossRefGoogle ScholarPubMed
Baker-Andresen, D., Ratnu, V. S., & Bredy, T. W. (2013). Dynamic DNA methylation: A prime candidate for genomic metaplasticity and behavioral adaptation. Trends in Neurosciences, 36, 3–13. doi:10.1016/j.tins.2012.09.003 Google Scholar
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2014). A sociability gene? Meta-analysis of oxytocin receptor genotype effects in humans. Psychiatric Genetics, 24, 45–51. doi:10.1097/YPG.0b013e3283643684 Google Scholar
Barr, C. S., Schwandt, M. L., Lindell, S. G., Higley, J. D., Maestripieri, D., Goldman, D., … Heilig, M. (2008). Variation at the mu-opioid receptor gene (OPRM1) influences attachment behavior in infant primates. Proceedings of the National Academy of Sciences, 105, 5277–5281. doi:10.1073/pnas.0710225105 Google Scholar
Barr, R. G. (2010). The normal crying curve: What do we really know? Developmental Medicine & Child Neurology, 32, 356–362. doi:10.1111/j.1469-8749.1990.tb16949.x Google Scholar
Barr, R. G., Barr, M., Fujiwara, T., Conway, J., Catherine, N., & Brant, R. (2009). Do educational materials change knowledge and behaviour about crying and shaken baby syndrome? A randomized controlled trial. Canadian Medical Association Journal, 180, 727–733. doi:10.1503/cmaj.081419 Google Scholar
Barr, R. G., & Gunnar, M. (2000). Colic: The “transient responsivity” hypothesis. In Barr, R. G., Hopkins, B., & Green, J. A. (Eds.), Crying as a sign, a symptom, and a signal: Clinical, emotional, and developmental aspects of infant and toddler crying (pp. 41–66). London: Mac Keith Press.Google Scholar
Barr, R. G., Kramer, M. S., Boisjoly, C., McVey-White, L., & Pless, I. B. (1988). Parental diary of infant cry and fuss behaviour. Archives of Disease in Childhood, 63, 380–387.Google Scholar
Beery, A. K., McEwen, L. M., MacIsaac, J. L., Francis, D. D., & Kobor, M. S. (2016). Natural variation in maternal care and cross-tissue patterns of oxytocin receptor gene methylation in rats. Hormones and Behavior, 77, 42–52. doi:10.1016/j.yhbeh.2015.05.022 CrossRefGoogle ScholarPubMed
Bertoletti, E., Zanoni, A., Giorda, R., & Battaglia, M. (2012). Influence of the OPRM1 gene polymorphism upon children's degree of withdrawal and brain activation in response to facial expressions. Developmental Cognitive Neuroscience, 2, 103–109. doi:10.1016/j.dcn.2011.05.001 Google Scholar
Bibikova, M., Barnes, B., Tsan, C., Ho, V., Klotzle, B., Le, J. M., … Shen, R. (2011). High density DNA methylation array with single CpG site resolution. Genomics, 98, 288–295. doi:10.1016/j.ygeno.2011.07.007 Google Scholar
Bodnar, R. J. (2014). Endogenous opiates and behavior: 2013. Peptides, 62 C, 67–136. doi:10.1016/j.peptides.2014.09.013 Google Scholar
Bohlin, J., Håberg, S. E., Magnus, P., Reese, S. E., Gjessing, H. K., Magnus, M. C., … Nystad, W. (2016). Prediction of gestational age based on genome-wide differentially methylated regions. Genome Biology, 17, 207. doi:10.1186/s13059-016-1063-4Google Scholar
Bond, C., LaForge, K. S., Tian, M., Melia, D., Zhang, S., Borg, L., … Yu, L. (1998). Single-nucleotide polymorphism in the human mu opioid receptor gene alters endorphin binding and activity: Possible implications for opiate addiction. Proceedings of the National Academy of Sciences, 95, 9608–9613. doi:10.1073/pnas.95.16.9608 Google Scholar
Border, R., & Keller, M. C. (2017). Commentary: Fundamental problems with candidate gene-by-environment interaction studies—Reflections on Moore and Thoemmes (2016). Journal of Child Psychology and Psychiatry, 58, 328–330. doi:10.1111/jcpp.12669 Google Scholar
Bornstein, M. H., Hahn, C.-S., & Haynes, O. M. (2010). Social competence, externalizing, and internalizing behavioral adjustment from early childhood through early adolescence: Developmental cascades. Development and Psychopathology, 22, 717–735. doi:10.1017/S0954579410000416 Google Scholar
Boyce, W. T., & Kobor, M. S. (2015). Development and the epigenome: The “synapse” of gene-environment interplay. Developmental Science, 18, 1–23. doi:10.1111/desc.12282 Google Scholar
Bradley, R. H., & Corwyn, R. F. (2002). Socioeconomic status and child development. Annual Review of Psychology, 53, 371–399. doi:10.1146/annurev.psych.53.100901.135233 Google Scholar
Breton, C. V., Marsit, C. J., Faustman, E., Nadeau, K., Goodrich, J. M., Dolinoy, D. C., … Murphy, S. K. (2017). Small-magnitude effect sizes in epigenetic end points are important in children's environmental health studies: The Children's Environmental Health and Disease Prevention Research Center's Epigenetics Working Group. Environmental Health Perspectives, 125, 511–526. doi:10.1289/EHP595 Google Scholar
Burton, C. L., Chatterjee, D., Chatterjee-Chakraborty, M., Lovic, V., Grella, S. L., Steiner, M., & Fleming, A. S. (2007). Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague-Dawley rats. Brain Research, 1158, 28–38. doi:10.1016/j.brainres.2007.05.003 Google Scholar
Bush, N. R., & Boyce, W. T. (2016). Differential sensitivity to context: Implications for developmental psychopathology. In Developmental Psychopathology (pp. 1–31). Hoboken, NJ: Wiley.Google Scholar
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proceedings of the National Academy of Sciences, 95, 5335–5340.Google Scholar
Carter, C. S. (2014). Oxytocin pathways and the evolution of human behavior. Annual Review of Psychology, 65, 17–39. doi:10.1146/annurevpsych-010213-115110 Google Scholar
Carter, C. S., Boone, E. M., Pournajafi-Nazarloo, H., & Bales, K. L. (2009). Consequences of early experiences and exposure to oxytocin and vasopressin are sexually dimorphic. Developmental Neuroscience, 31, 332–341. doi:10.1159/000216544 CrossRefGoogle ScholarPubMed
Cecil, C. A. M., Walton, E., & Viding, E. (2015). DNA methylation, substance use and addiction: A systematic review of recent animal and human research from a developmental perspective. Current Addiction Reports, 2, 331–346. doi:10.1007/s40429-015-0072-9 Google Scholar
Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003). Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiology & Behavior, 79, 359–371.Google Scholar
Chen, B. H., Marioni, R. E., Colicino, E., Peters, M. J., Ward-Caviness, C. K., Tsai, P.-C., … Horvath, S. (2016). DNA methylation-based measures of biological age: Meta-analysis predicting time to death. Aging, 8, 1844–1865. doi:10.18632/aging.101020 Google Scholar
Chen, L., Pan, H., Tuan, T. A., Teh, A. L., MacIsaac, J. L., Mah, S. M., … Holbrook, J. D. (2015). Brain-derived neurotrophic factor (BDNF) Val66Met polymorphism influences the association of the methylome with maternal anxiety and neonatal brain volumes. Development and Psychopathology, 27, 137–150. doi:10.1017/S0954579414001357 Google Scholar
Choe, D. E., Olson, S. L., & Sameroff, A. J. (2013). Effects of early maternal distress and parenting on the development of children's self-regulation and externalizing behavior. Development and Psychopathology, 25, 437–453. doi:10.1017/S0954579412001162 Google Scholar
Cicchetti, D., Hetzel, S., Rogosch, F. A., Handley, E. D., & Toth, S. L. (2016). Genome-wide DNA methylation in 1-year-old infants of mothers with major depressive disorder. Development and Psychopathology, 28(4, Pt. 2), 1413–1419. doi:10.1017/S0954579416000912 Google Scholar
Crockford, C., Deschner, T., Ziegler, T. E., & Wittig, R. M. (2014). Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: A review. Frontiers in Behavioral Neuroscience, 8, 68. doi:10.3389/fnbeh.2014.00068 Google Scholar
Curley, J. P. (2011). The mu-opioid receptor and the evolution of mother-infant attachment: Theoretical comment on Higham et al. (2011). Behavioral Neuroscience, 125, 273–278. doi:10.1037/a0022939 Google Scholar
Day, J. J., & Sweatt, J. D. (2011). Cognitive neuroepigenetics: A role for epigenetic mechanisms in learning and memory. Neurobiology of Learning and Memory, 96, 2–12. doi:10.1016/j.nlm.2010.12.008 Google Scholar
Deb, I., Chakraborty, J., Gangopadhyay, P. K., Choudhury, S. R., & Das, S. (2010). Single-nucleotide polymorphism (A118G) in exon 1 of OPRM1 gene causes alteration in downstream signaling by mu-opioid receptor and may contribute to the genetic risk for addiction. Journal of Neurochemistry, 112, 486–496. doi:10.1111/j.1471-4159.2009.06472.x Google Scholar
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, 313-50-95. doi:10.1017/S0140525X05000063 Google Scholar
Du, P., Zhang, X., Huang, C.-C., Jafari, N., Kibbe, W. A., Hou, L., & Lin, S. M. (2010). Comparison of beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics, 11, 587. doi:10.1186/1471-2105-11-587 Google Scholar
Dunbar, R. I. M. (2010). The social role of touch in humans and primates: Behavioural function and neurobiological mechanisms. Neuroscience & Biobehavioral Reviews, 34, 260–268. doi:10.1016/j.neubiorev.2008.07.001 Google Scholar
Duncan, L. E., Pollastri, A. R., & Smoller, J. W. (2014). Mind the gap: Why many geneticists and psychological scientists have discrepant views about gene–environment interaction (G × E) research. American Psychologist, 69, 249–268. doi:10.1037/a0036320 Google Scholar
Edgar, R. D., Jones, M. J., Robinson, W. P., & Kobor, M. S. (2017). An empirically driven data reduction method on the human 450K methylation array to remove tissue specific non-variable CpGs. Clinical Epigenetics, 9, 11. doi:10.1186/s13148-017-0320-z CrossRefGoogle ScholarPubMed
Egan, M. F., Weinberger, D. R., & Lu, B. (2003). Schizophrenia, III. American Journal of Psychiatry, 160, 1242. doi:10.1176/appi.ajp.160.7.1242 Google Scholar
Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Differential susceptibility to the environment: An evolutionary–neurodevelopmental theory. Development and Psychopathology, 23, 7–28. doi:10.1017/S0954579410000611 Google Scholar
Esposito, E. A., Jones, M. J., Doom, J. R., MacIsaac, J. L., Gunnar, M. R., & Kobor, M. S. (2016). Differential DNA methylation in peripheral blood mononuclear cells in adolescents exposed to significant early but not later childhood adversity. Development and Psychopathology, 28, 1385–1399. doi:10.1017/S0954579416000055 Google Scholar
Feldman, R., Singer, M., & Zagoory, O. (2010). Touch attenuates infants’ physiological reactivity to stress. Developmental Science, 13, 271–278. doi:10.1111/j.1467-7687.2009.00890.x CrossRefGoogle ScholarPubMed
Field, T. (2010). Touch for socioemotional and physical well-being: A review. Developmental Review, 30, 367–383. doi:10.1016/j.dr.2011.01.001 Google Scholar
Field, T. M. (1984). Early interactions between infants and their postpartum depressed mothers. Infant Behavior and Development, 7, 517–522. doi:10.1016/S0163-6383(84)80010-7 CrossRefGoogle Scholar
Fox, S. E., Levitt, P., & Nelson, C. A. (2010). How the timing and quality of early experiences influence the development of brain architecture. Child Development, 81, 28–40. doi:10.1111/j.1467-8624.2009.01380.x Google Scholar
Francis, D. D., Champagne, F. C., & Meaney, M. J. (2000). Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. Journal of Neuroendocrinology, 12, 1145–1458.Google Scholar
Fuchs, A., Möhler, E., Reck, C., Resch, F., & Kaess, M. (2016). The early mother-to-child bond and its unique prospective contribution to child behavior evaluated by mothers and teachers. Psychopathology, 49, 211–216. doi:10.1159/000445439 Google Scholar
Gao, X., Jia, M., Zhang, Y., Breitling, L. P., & Brenner, H. (2015). DNA methylation changes of whole blood cells in response to active smoking exposure in adults: A systematic review of DNA methylation studies. Clinical Epigenetics, 7, 113. doi:10.1186/s13148-015-0148-3 Google Scholar
Girchenko, P., Lahti, J., Czamara, D., Knight, A. K., Jones, M. J., Suarez, A., … Räikkönen, K. (2017). Associations between maternal risk factors of adverse pregnancy and birth outcomes and the offspring epigenetic clock of gestational age at birth. Clinical Epigenetics, 9, 49. doi:10.1186/s13148-017-0349-z Google Scholar
Gong, P., Fan, H., Liu, J., Yang, X., Zhang, K., & Zhou, X. (2017). Revisiting the impact of OXTR rs53576 on empathy: A population-based study and a meta-analysis. Psychoneuroendocrinology, 80, 131–136. doi:10.1016/j.psyneuen.2017.03.005 Google Scholar
Gunnar, M. R., Wenner, J. A., Thomas, K. M., Glatt, C. E., McKenna, M. C., & Clark, A. G. (2012). The brain-derived neurotrophic factor Val66Met polymorphism moderates early deprivation effects on attention problems. Development and Psychopathology, 24, 1215–1223. doi:10.1017/S095457941200065X Google Scholar
Guo, J. U., Ma, D. K., Mo, H., Ball, M. P., Jang, M.-H., Bonaguidi, M. A., … Song, H. (2011). Neuronal activity modifies the DNA methylation landscape in the adult brain. Nature Neuroscience, 14, 1345–1351. doi:10.1038/nn.2900 Google Scholar
Gutierrez-Arcelus, M., Lappalainen, T., Montgomery, S. B., Buil, A., Ongen, H., Yurovsky, A., … Dermitzakis, E. T. (2013). Passive and active DNA methylation and the interplay with genetic variation in gene regulation. eLife, 2. doi:10.7554/eLife.00523 Google Scholar
Hane, A. A., & Fox, N. A. (2006). Ordinary variations in maternal caregiving influence human infants’ stress reactivity. Psychological Science, 17, 550–556. doi:10.1111/j.1467-9280.2006.01742.x Google Scholar
Hane, A. A., Henderson, H. A., Reeb-Sutherland, B. C., & Fox, N. A. (2010). Ordinary variations in human maternal caregiving in infancy and biobehavioral development in early childhood: A follow-up study. Developmental Psychobiology, 52, 558–567. doi:10.1002/dev.20461 Google Scholar
Hane, A. A., & Philbrook, L. E. (2012). Beyond licking and grooming: Maternal regulation of infant stress in the context of routine care. Parenting, Science and Practice, 12, 144–153. doi:10.1080/15295192.2012.683341 CrossRefGoogle ScholarPubMed
Hannum, G., Guinney, J., Zhao, L., Zhang, L., Hughes, G., Sadda, S., … Zhang, K. (2013). Genome-wide methylation profiles reveal quantitative views of human aging rates. Molecular Cell, 49, 359–367. doi:10.1016/j.molcel.2012.10.016 Google Scholar
Harlow, H. F. (1958). The nature of love. American Psychologist, 13, 673–685.Google Scholar
Hayden, E. P., Klein, D. N., Dougherty, L. R., Olino, T. M., Dyson, M. W., Durbin, C. E., … Singh, S. M. (2010). The role of brain-derived neurotrophic factor genotype, parental depression, and relationship discord in predicting early-emerging negative emotionality. Psychological Science, 21, 1678–1685. doi:10.1177/0956797610385357 Google Scholar
Heinrichs, M., & Domes, G. (2008). Neuropeptides and social behaviour: Effects of oxytocin and vasopressin in humans. Progress in Brain Research, 170, 337–350. doi:10.1016/S0079-6123(08)00428-7 Google Scholar
Henikoff, S., & Greally, J. M. (2016). Epigenetics, cellular memory and gene regulation. Current Biology, 26, R644–R648. doi:10.1016/j.cub.2016.06.011 CrossRefGoogle ScholarPubMed
Higham, J. P., Barr, C. S., Hoffman, C. L., Mandalaywala, T. M., Parker, K. J., & Maestripieri, D. (2011). Mu-opioid receptor (OPRM1) variation, oxytocin levels and maternal attachment in free-ranging rhesus macaques Macaca mulatta. Behavioral Neuroscience, 125, 131–136. doi:10.1037/a0022695 Google Scholar
Hochberg, Y., & Benjamini, Y. (1990). More powerful procedures for multiple significance testing. Statistics in Medicine, 9, 811–818.Google Scholar
Horvath, S. (2013). DNA methylation age of human tissues and cell types. Genome Biology, 14, R115. doi:10.1186/gb-2013-14-10-r115 Google Scholar
Horvath, S., Zhang, Y., Langfelder, P., Kahn, R. S., Boks, M. P., van Eijk, K., … Ophoff, R. A. (2012). Aging effects on DNA methylation modules in human brain and blood tissue. Genome Biology, 13, R97. doi:10.1186/gb-2012-13-10-r97 Google Scholar
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014). Psychobiological mechanisms underlying the social buffering of the hypothalamic–pituitary–adrenocortical axis: A review of animal models and human studies across development. Psychological Bulletin, 140, 256–282. doi:10.1037/a0032671 Google Scholar
Huang, E. J., & Reichardt, L. F. (2001). Neurotrophins: Roles in neuronal development and function. Annual Review of Neuroscience, 24, 677–736. doi:10.1146/annurev.neuro.24.1.677 Google Scholar
Hull, J. G., Tedlie, J. C., & Lehn, D. A. (1992). Moderator variables in personality research: The problem of controlling for plausible alternatives. Personality and Social Psychology Bulletin, 18, 115–117. doi:10.1177/0146167292182001 Google Scholar
Humphreys, K. L., Gleason, M. M., Drury, S. S., Miron, D., Nelson, C. A., Fox, N. A., & Zeanah, C. H. (2015). Effects of institutional rearing and foster care on psychopathology at age 12 years in Romania: Follow-up of an open, randomised controlled trial. Lancet Psychiatry, 2, 625–634. doi:10.1016/S2215-0366(15)00095-4 Google Scholar
Illingworth, R. S., & Bird, A. P. (2009). CpG islands—“A rough guide.” FEBS Letters, 583, 1713–1720. doi:10.1016/j.febslet.2009.04.012 Google Scholar
Inagaki, T. K., Ray, L. A., Irwin, M. R., Way, B. M., & Eisenberger, N. I. (2016). Opioids and social bonding: Naltrexone reduces feelings of social connection. Social Cognitive and Affective Neuroscience, 11, 728–735. doi:10.1093/scan/nsw006 Google Scholar
Johnson, W. E., Li, C., & Rabinovic, A. (2007). Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics, 8, 118–127. doi:10.1093/biostatistics/kxj037 Google Scholar
Jones, M. J., Goodman, S. J., & Kobor, M. S. (2015). DNA methylation and healthy human aging. Aging Cell, 14, 924–932. doi:10.1111/acel.12349 Google Scholar
Jones, P. A. (2012). Functions of DNA methylation: Islands, start sites, gene bodies and beyond. Nature Reviews Genetics, 13, 484–492. doi:10.1038/nrg3230 Google Scholar
Juhász, G., Földi, I., & Penke, B. (2011). Systems biology of Alzheimer's disease: How diverse molecular changes result in memory impairment in AD. Neurochemistry International, 58, 739–750. doi:10.1016/j.neuint.2011.02.008 Google Scholar
Jutapakdeegul, N., Casalotti, S. O., Govitrapong, P., & Kotchabhakdi, N. (2003). Postnatal touch stimulation acutely alters corticosterone levels and glucocorticoid receptor gene expression in the neonatal rat. Developmental Neuroscience, 25, 26–33.Google Scholar
Karpova, N. N. (2014). Role of BDNF epigenetics in activity-dependent neuronal plasticity. Neuropharmacology, 76(Pt. C), 709–718. doi:10.1016/j.neuropharm.2013.04.002 Google Scholar
Kieffer, B. L., & Evans, C. J. (2009). Opioid receptors: From binding sites to visible molecules in vivo. Neuropharmacology, 56(Suppl. 1), 205–212. doi:10.1016/j.neuropharm.2008.07.033 Google Scholar
Knight, A. K., Craig, J. M., Theda, C., Bækvad-Hansen, M., Bybjerg-Grauholm, J., Hansen, C. S., … Smith, A. K. (2016). An epigenetic clock for gestational age at birth based on blood methylation data. Genome Biology, 17, 206. doi:10.1186/s13059-016-1068-z Google Scholar
Koepp, M. J., Hammers, A., Lawrence, A. D., Asselin, M. C., Grasby, P. M., & Bench, C. J. (2009). Evidence for endogenous opioid release in the amygdala during positive emotion. NeuroImage, 44, 252–256. doi:10.1016/j.neuroimage.2008.08.032 Google Scholar
Kundakovic, M., Gudsnuk, K., Herbstman, J. B., Tang, D., Perera, F. P., & Champagne, F. A. (2015). DNA methylation of BDNF as a biomarker of early-life adversity. Proceedings of the National Academy of Sciences, 112, 6807–6813. doi:10.1073/pnas.1408355111 Google Scholar
Lam, J., Barr, R. G., Catherine, N., Tsui, H., Hahnhaussen, C. L., Pauwels, J., & Brant, R. (2010). Electronic and paper diary recording of infant and caregiver behaviors. Journal of Developmental and Behavioral Pediatrics, 31, 1. doi:10.1097/DBP.0b013e3181e416ae Google Scholar
Le Merrer, J., Becker, J. A. J., Befort, K., & Kieffer, B. L. (2009). Reward processing by the opioid system in the brain. Physiological Reviews, 89, 1379–1412. doi:10.1152/physrev.00005.2009 Google Scholar
Lemire, M., Zaidi, S. H. E., Ban, M., Ge, B., Aïssi, D., Germain, M., … Hudson, T. J. (2015). Long-range epigenetic regulation is conferred by genetic variation located at thousands of independent loci. Nature Communications, 6, 6326. doi:10.1038/ncomms7326 Google Scholar
Lim, M. M., & Young, L. J. (2006). Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Hormones and Behavior, 50, 506–517. doi:10.1016/j.yhbeh.2006.06.028 Google Scholar
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience, 3, 799–806. doi:10.1038/77702 CrossRefGoogle ScholarPubMed
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., … Meaney, M. J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science, 277.Google Scholar
Löken, L. S., Wessberg, J., Morrison, I., McGlone, F., & Olausson, H. (2009). Coding of pleasant touch by unmyelinated afferents in humans. Nature Neuroscience, 12, 547–548. doi:10.1038/nn.2312 Google Scholar
LoParo, D., & Waldman, I. D. (2015). The oxytocin receptor gene (OXTR) is associated with autism spectrum disorder: A meta-analysis. Molecular Psychiatry, 20, 640–646. doi:10.1038/mp.2014.77 Google Scholar
Lowe, R., Gemma, C., Beyan, H., Hawa, M. I., Bazeos, A., Leslie, R. D., … Ramagopalan, S. V. (2013). Buccals are likely to be a more informative surrogate tissue than blood for epigenome-wide association studies. Epigenetics, 8, 445–454. doi:10.4161/epi.24362 Google Scholar
Lubin, F. D., Roth, T. L., & Sweatt, J. D. (2008). Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. Journal of Neuroscience, 28, 10576–10586. doi:10.1523/jneurosci.1786-08.2008 Google Scholar
Machin, A. J., & Dunbar, R. I. (2011). The brain opioid theory of social attachment: A review of the evidence. Behaviour, 148, 985–1025. doi:10.1163/000579511X596624 Google Scholar
Macrì, S., Laviola, G., Leussis, M. P., & Andersen, S. L. (2010). Abnormal behavioral and neurotrophic development in the younger sibling receiving less maternal care in a communal nursing paradigm in rats. Psychoneuroendocrinology, 35, 392–402. doi:10.1016/j.psyneuen.2009.07.016 Google Scholar
Marioni, R. E., Shah, S., McRae, A. F., Chen, B. H., Colicino, E., Harris, S. E., … Deary, I. J. (2015). DNA methylation age of blood predicts all-cause mortality in later life. Genome Biology, 16, 25. doi:10.1186/s13059-015-0584-6 Google Scholar
Mata, J., Thompson, R. J., & Gotlib, I. H. (2010). BDNF genotype moderates the relation between physical activity and depressive symptoms. Health Psychology, 29, 130–133. doi:10.1037/a0017261 Google Scholar
McGlone, F., & Spence, C. (2010). The cutaneous senses: Touch, temperature, pain/itch, and pleasure. Neuroscience & Biobehavioral Reviews, 34, 145–147. doi:10.1016/j.neubiorev.2009.08.008 Google Scholar
Meaney, M. J. (2010). Epigenetics and the biological definition of Gene × Environment interactions. Child Development, 81, 41–79. doi:10.1111/j.1467-8624.2009.01381.x Google Scholar
Miller, G., Chen, E., & Cole, S. W. (2009). Health psychology: Developing biologically plausible models linking the social world and physical health. Annual Review of Psychology, 60, 501–524. doi:10.1146/annurev.psych.60.110707.163551 Google Scholar
Moles, A., Kieffer, B. L., & D'Amato, F. R. (2004). Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science, 304, 1983–1986. doi:10.1126/science.1095943 Google Scholar
Montag, C., Brockmann, E.-M., Lehmann, A., Müller, D. J., Rujescu, D., & Gallinat, J. (2012). Association between oxytocin receptor gene polymorphisms and self-rated “empathic concern” in schizophrenia. PLOS ONE, 7, e51882. doi:10.1371/journal.pone.0051882 Google Scholar
Moore, S. R. (2017). Commentary: What is the case for candidate gene approaches in the era of high-throughput genomics? A response to Border and Keller (2017). Journal of Child Psychology and Psychiatry, 58, 331–334. doi:10.1111/jcpp.12697 Google Scholar
Moore, S. R., & Depue, R. A. (2016). Neurobehavioral foundation of environmental reactivity. Psychological Bulletin, 142, 107–164. doi:10.1037/bul0000028 Google Scholar
Mueller, C., Klega, A., Buchholz, H.-G., Rolke, R., Magerl, W., Schirrmacher, R., … Schreckenberger, M. (2010). Basal opioid receptor binding is associated with differences in sensory perception in healthy human subjects: A [18F]diprenorphine PET study. NeuroImage, 49, 731–737. doi:10.1016/j.neuroimage.2009.08.033 Google Scholar
Naumova, O. Y., Lee, M., Koposov, R., Szyf, M., Dozier, M., & Grigorenko, E. L. (2012). Differential patterns of whole-genome DNA methylation in institutionalized children and children raised by their biological parents. Development and Psychopathology, 24, 143–155. doi:10.1017/S0954579411000605 Google Scholar
Palma-Gudiel, H., Córdova-Palomera, A., Leza, J. C., & Fañanás, L. (2015). Glucocorticoid receptor gene (NR3C1) methylation processes as mediators of early adversity in stress-related disorders causality: A critical review. Neuroscience & Biobehavioral Reviews, 55, 520–535. doi:10.1016/j.neubiorev.2015.05.016 Google Scholar
Pan, P., Fleming, A. S., Lawson, D., Jenkins, J. M., & McGowan, P. O. (2014). Within- and between-litter maternal care alter behavior and gene regulation in female offspring. Behavioral Neuroscience, 128, 736–748. doi:10.1037/bne0000014 Google Scholar
Pemberton, C. K., Neiderhiser, J. M., Leve, L. D., Natsuaki, M. N., Shaw, D. S., Reiss, D., & Ge, X. (2010). Influence of parental depressive symptoms on adopted toddler behaviors: An emerging developmental cascade of genetic and environmental effects. Development and Psychopathology, 22, 803–818. doi:10.1017/S0954579410000477 CrossRefGoogle ScholarPubMed
Peters, T. J., Buckley, M. J., Statham, A. L., Pidsley, R., Samaras, K., Van Lord, R., … Molloy, P. L. (2015). De novo identification of differentially methylated regions in the human genome. Epigenetics and Chromatin, 8, 6. doi:10.1186/1756-8935-8-6 Google Scholar
Pickles, A., Sharp, H., Hellier, J., & Hill, J. (2017). Prenatal anxiety, maternal stroking in infancy, and symptoms of emotional and behavioral disorders at 3.5 years. European Child and Adolescent Psychiatry, 26, 325–334. doi:10.1007/s00787-016-0886-6 Google Scholar
Pinkernelle, J., Abraham, A., Seidel, K., & Braun, K. (2009). Paternal deprivation induces dendritic and synaptic changes and hemispheric asymmetry of pyramidal neurons in the somatosensory cortex. Developmental Neurobiology, 69, 663–673. doi:10.1002/dneu.20726 Google Scholar
Pivac, N., Kim, B., Nedić, G., Joo, Y. H., Kozarić-Kovacić, D., Hong, J. P., & Muck-Seler, D. (2009). Ethnic differences in brain-derived neurotrophic factor Val66Met polymorphism in Croatian and Korean healthy participants. Croatian Medical Journal, 50, 43–48. doi:10.3325/cmj.2009.50.43 Google Scholar
Pratt, M., Singer, M., Kanat-Maymon, Y., & Feldman, R. (2015). Infant negative reactivity defines the effects of parent-child synchrony on physiological and behavioral regulation of social stress. Development and Psychopathology, 27, 1191–1204. doi:10.1017/S0954579415000760 Google Scholar
Price, M. E., Cotton, A. M., Lam, L. L., Farré, P., Emberly, E., Brown, C. J., … Kobor, M. S. (2013). Additional annotation enhances potential for biologically-relevant analysis of the Illumina Infinium HumanMethylation450 BeadChip array. Epigenetics and Chromatin, 6, 4. doi:10.1186/1756-8935-6-4 Google Scholar
Reece, C., Ebstein, R., Cheng, X., Ng, T., & Schirmer, A. (2016). Maternal touch predicts social orienting in young children. Cognitive Development, 39, 128–140. doi:10.1016/j.cogdev.2016.05.001 Google Scholar
Romens, S. E., McDonald, J., Svaren, J., & Pollak, S. D. (2015). Associations between early life stress and gene methylation in children. Child Development, 86, 303–309. doi:10.1111/cdev.12270 Google Scholar
Roth, T. L., & Sullivan, R. M. (2006). Examining the role of endogenous opioids in learned odor-stroke associations in infant rats. Developmental Psychobiology, 48, 71–78. doi:10.1002/dev.20107 Google Scholar
Saxonov, S., Berg, P., & Brutlag, D. L. (2006). A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proceedings of the National Academy of Sciences, 103, 1412–1417. doi:10.1073/pnas.0510310103 Google Scholar
Seelke, A. M. H., Perkeybile, A. M., Grunewald, R., Bales, K. L., & Krubitzer, L. A. (2016). Individual differences in cortical connections of somatosensory cortex are associated with parental rearing style in prairie voles (Microtus ochrogaster). Journal of Comparative Neurology, 524, 564–577. doi:10.1002/cne.23837 Google Scholar
Sharp, H., Pickles, A., Meaney, M., Marshall, K., Tibu, F., & Hill, J. (2012). Frequency of infant stroking reported by mothers moderates the effect of prenatal depression on infant behavioural and physiological outcomes. PLOS ONE, 7, e45446. doi:10.1371/journal.pone.0045446 Google Scholar
Shayit, M., Nowak, R., Keller, M., & Weller, A. (2003). Establishment of a preference by the newborn lamb for its mother: The role of opioids. Behavioral Neuroscience, 117, 446–454.CrossRefGoogle ScholarPubMed
Shoemaker, R., Deng, J., Wang, W., & Zhang, K. (2010). Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome. Genome Research, 20, 883–889.Google Scholar
Sigal, J. J., Perry, J. C., Rossignol, M., & Ouimet, M. C. (2003). Unwanted infants: Psychological and physical consequences of inadequate orphanage care 50 years later. American Journal of Orthopsychiatry, 73, 3–12.Google Scholar
Simpkin, A. J., Howe, L. D., Tilling, K., Gaunt, T. R., Lyttleton, O., McArdle, W. L., … Relton, C. L. (2017). The epigenetic clock and physical development during childhood and adolescence: Longitudinal analysis from a UK birth cohort. International Journal of Epidemiology, 11, dyw307. doi:10.1093/ije/dyw307 Google Scholar
Smith, A. K., Kilaru, V., Klengel, T., Mercer, K. B., Bradley, B., Conneely, K. N., … Binder, E. B. (2015). DNA extracted from saliva for methylation studies of psychiatric traits: Evidence tissue specificity and relatedness to brain. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 168, 36–44. doi:10.1002/ajmg.b.32278 Google Scholar
Smit-Rigter, L. A., Champagne, D. L., & van Hooft, J. A. (2009). Lifelong impact of variations in maternal care on dendritic structure and function of cortical layer 2/3 pyramidal neurons in rat offspring. PLOS ONE, 4, e5167. doi:10.1371/journal.pone.0005167 Google Scholar
St. James-Roberts, I., & Plewis, I. (1996). Individual differences, daily fluctuations, and developmental changes in amounts of infant waking, fussing, crying, feeding, and sleeping. Child Development, 67, 2527–2540.Google Scholar
Stoop, R. (2014). Neuromodulation by oxytocin and vasopressin in the central nervous system as a basis for their rapid behavioral effects. Current Opinion in Neurobiology, 29, 187–193. doi:10.1016/j.conb.2014.09.012 Google Scholar
Suderman, M., Borghol, N., Pappas, J. J., Pinto Pereira, S. M., Pembrey, M., Hertzman, C., … Szyf, M. (2014). Childhood abuse is associated with methylation of multiple loci in adult DNA. BMC Medical Genomics, 7, 13. doi:10.1186/1755-8794-7-13Google Scholar
Sullivan, R. M., Taborsky-Barba, S., Mendoza, R., Itano, A., Leon, M., Cotman, C. W., … Lott, I. (1991). Olfactory classical conditioning in neonates. Pediatrics, 87, 511–518.Google Scholar
Székely, E., Lucassen, N., Tiemeier, H., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Kok, R., … Herba, C. M. (2014). Maternal depressive symptoms and sensitivity are related to young children's facial expression recognition: The Generation R Study. Development and Psychopathology, 26, 333–345. doi:10.1017/S0954579413001028 Google Scholar
Takatsuru, Y., Yoshitomo, M., Nemoto, T., Eto, K., & Nabekura, J. (2009). Maternal separation decreases the stability of mushroom spines in adult mice somatosensory cortex. Brain Research, 1294, 45–51. doi:10.1016/j.brainres.2009.07.092 Google Scholar
Taylor, S. E. (2006). Tend and befriend: Biobehavioral bases of affiliation under stress. Current Directions in Psychological Science, 15, 273–277. doi:10.1111/j.1467-8721.2006.00451.x Google Scholar
Teh, A. L., Pan, H., Chen, L., Ong, M.-L., Dogra, S., Wong, J., … Holbrook, J. D. (2014). The effect of genotype and in utero environment on interindividual variation in neonate DNA methylomes. Genome Research, 24, 1064–1074. doi:10.1101/gr.171439.113 Google Scholar
Teschendorff, A. E. (2013). Epigenetic aging: Insights from network biology. Aging, 5, 719–720. doi:10.18632/aging.100610 Google Scholar
Teschendorff, A. E., Marabita, F., Lechner, M., Bartlett, T., Tegner, J., Gomez-Cabrero, D., & Beck, S. (2013). A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics, 29, 189–196. doi:10.1093/bioinformatics/bts680 Google Scholar
Teschendorff, A. E., West, J., & Beck, S. (2013). Age-associated epigenetic drift: Implications, and a case of epigenetic thrift? Human Molecular Genetics, 22, R7–R15. doi:10.1093/hmg/ddt375 Google Scholar
Troisi, A., Frazzetto, G., Carola, V., Di Lorenzo, G., Coviello, M., D'Amato, F. R., … Gross, C. (2011). Social hedonic capacity is associated with the A118G polymorphism of the mu-opioid receptor gene (OPRM1) in adult healthy volunteers and psychiatric patients. Social Neuroscience, 6, 88–97.Google Scholar
Troisi, A., Frazzetto, G., Carola, V., Di Lorenzo, G., Coviello, M., Siracusano, A., & Gross, C. (2012). Variation in the μ-opioid receptor gene (OPRM1) moderates the influence of early maternal care on fearful attachment. Social Cognitive and Affective Neuroscience, 7, 542–547. doi:10.1093/scan/nsr037 Google Scholar
Turecki, G., & Meaney, M. J. (2016). Effects of the social environment and stress on glucocorticoid receptor gene methylation: A systematic review. Biological Psychiatry, 79, 87–96. doi:10.1016/j.biopsych.2014.11.022 Google Scholar
van IJzendoorn, M. H., Palacios, J., Sonuga-Barke, E. J. S., Gunnar, M. R., Vorria, P., McCall, R. B., … Juffer, F. (2011). Children in institutional care: Delayed development and resilience. Monographs of the Society for Research in Child Development, 76, 8–30. doi:10.1111/j.1540-5834.2011.00626.x Google Scholar
Wagner, J. R., Busche, S., Ge, B., Kwan, T., Pastinen, T., & Blanchette, M. (2014). The relationship between DNA methylation, genetic and expression inter-individual variation in untransformed human fibroblasts. Genome Biology, 15, R37. doi:10.1186/gb-2014-15-2-r37 Google Scholar
Walker, S. C., Trotter, P. D., Swaney, W. T., Marshall, A., & McGlone, F. P. (2017). C-tactile afferents: Cutaneous mediators of oxytocin release during affiliative tactile interactions? Neuropeptides . Advance online publication . doi:10.1016/j.npep.2017.01.001 Google Scholar
Walum, H., Lichtenstein, P., Neiderhiser, J. M., Reiss, D., Ganiban, J. M., Spotts, E. L., … Westberg, L. (2012). Variation in the oxytocin receptor gene is associated with pair-bonding and social behavior. Biological Psychiatry, 71, 419–426. doi:10.1016/j.biopsych.2011.09.002 Google Scholar
Wang, Z., Tang, B., He, Y., & Jin, P. (2016). DNA methylation dynamics in neurogenesis. Epigenomics, 8, 401–414. doi:10.2217/epi.15.119 Google Scholar
Way, B. M., Taylor, S. E., & Eisenberger, N. I. (2009). Variation in the mu-opioid receptor gene (OPRM1) is associated with dispositional and neural sensitivity to social rejection. Proceedings of the National Academy of Sciences, 106, 15079–15084. doi:10.1073/pnas.0812612106 Google Scholar
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., … Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854. doi:10.1038/nn1276 Google Scholar
White, B. P., Gunnar, M. R., Larson, M. C., Donzella, B., & Barr, R. G. (2000). Behavioral and physiological responsivity, sleep, and patterns of daily cortisol production in infants with and without colic. Child Development, 71, 862–877.Google Scholar
Willoughby, M. T., Mills-Koonce, R., Propper, C. B., & Waschbusch, D. A. (2013). Observed parenting behaviors interact with a polymorphism of the brain-derived neurotrophic factor gene to predict the emergence of oppositional defiant and callous–unemotional behaviors at age 3 years. Development and Psychopathology, 25, 903–917. doi:10.1017/S0954579413000266 Google Scholar
Wu, H., & Zhang, Y. (2014). Reversing DNA methylation: Mechanisms, genomics, and biological functions. Cell, 156, 45–68. doi:10.1016/j.cell.2013.12.019 Google Scholar
Yu, N.-K., Baek, S. H., & Kaang, B.-K. (2011). DNA methylation-mediated control of learning and memory. Molecular Brain, 4, 5. doi:10.1186/1756-6606-4-5 CrossRefGoogle ScholarPubMed
Yzerbyt, V. Y., Muller, D., & Judd, C. M. (2004). Adjusting researchers’ approach to adjustment: On the use of covariates when testing interactions. Journal of Experimental Social Psychology, 40, 424–431. doi:10.1016/j.jesp.2003.10.001 Google Scholar
Zannas, A. S. (2016). Editorial perspective: Psychological stress and epigenetic aging—What can we learn and how can we prevent? Journal of Child Psychology and Psychiatry, 57, 674–675. doi:10.1111/jcpp.12535 Google Scholar
Zeanah, C. H., Gunnar, M. R., McCall, R. B., Kreppner, J. M., & Fox, N. A. (2011). Sensitive periods. Monographs of the Society for Research in Child Development, 76, 147–162. doi:10.1111/j.1540-5834.2011.00631.x Google Scholar
Zubieta, J. K., Smith, Y. R., Bueller, J. A., Xu, Y., Kilbourn, M. R., Jewett, D. M., … Stohler, C. S. (2001). Regional mu opioid receptor regulation of sensory and affective dimensions of pain. Science, 293, 311–315. doi:10.1126/science.1060952 Google Scholar
Supplementary material: File

Moore et al supplementary material 1

Moore et al supplementary material

Download Moore et al supplementary material 1(File)
File 157.1 KB