Skip to main content Accessibility help
×
Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-27T13:19:47.396Z Has data issue: false hasContentIssue false

3 - Dynamic Epigenetic Impact of the Environment on the Developing Brain

from Part I - Foundations

Published online by Cambridge University Press:  26 September 2020

Jeffrey J. Lockman
Affiliation:
Tulane University, Louisiana
Catherine S. Tamis-LeMonda
Affiliation:
New York University
Get access

Summary

Development is a dynamic process shaped by the interactions between genes and environments. Within the field of developmental biology, the complex interactions between genes and their products that create the foundation for cellular differentiation and the formation of the nervous system have been well described. Advances in molecular biology have permitted increasing precision in the characterization of the cascade of molecular changes that link genes to specific developmental endpoints. However, beyond addressing questions regarding the processes linking a gene to a phenotypic outcome, description of these molecular changes has also provided insight into the ways in which the environment induces lasting biological effects. Though environments – particularly characteristics of the social world around us – are typically viewed as a separate and distinct influence from genes, there is increasing understanding of the interplay between genes and environments.

Type
Chapter
Information
The Cambridge Handbook of Infant Development
Brain, Behavior, and Cultural Context
, pp. 70 - 93
Publisher: Cambridge University Press
Print publication year: 2020

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.)

References

Almas, A. N., Degnan, K. A., Radulescu, A., Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2012). Effects of early intervention and the moderating effects of brain activity on institutionalized children’s social skills at age 8. Proceedings of the National Academy of Sciences of the United States of America, 109(Suppl. 2), 1722817231. https://doi.org/10.1073/pnas.1121256109Google Scholar
Baccarelli, A., & Bollati, V. (2009). Epigenetics and environmental chemicals. Current Opinion in Pediatrics, 21(2), 243251.Google Scholar
Baedke, J. (2013). The epigenetic landscape in the course of time: Conrad Hal Waddington’s methodological impact on the life sciences. Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences, 44(4, Part B), 756773. https://doi.org/10.1016/j.shpsc.2013.06.001Google Scholar
Ben Maamar, M., Sadler-Riggleman, I., Beck, D., McBirney, M., Nilsson, E., Klukovich, R., … Skinner, M. K. (2018). Alterations in sperm DNA methylation, non-coding RNA expression, and histone retention mediate vinclozolin-induced epigenetic transgenerational inheritance of disease. Environmental Epigenetics, 4(2), dvy010. https://doi.org/10.1093/eep/dvy010Google Scholar
Bernard, K., Frost, A., Bennett, C. B., & Lindhiem, O. (2017). Maltreatment and diurnal cortisol regulation: A meta-analysis. Psychoneuroendocrinology, 78, 5767. https://doi.org/10.1016/j.psyneuen.2017.01.005Google Scholar
Bowers, M. E., & Yehuda, R. (2016). Intergenerational transmission of stress in humans. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 41(1), 232244. https://doi.org/10.1038/npp.2015.247Google Scholar
Bowlby, J., & World Health Organization. (1952). Maternal care and mental health : A report prepared on behalf of the World Health Organization as a contribution to the United Nations programme for the welfare of homeless children (2nd ed.). Geneva: World Health Organization.Google Scholar
Braithwaite, E. C., Kundakovic, M., Ramchandani, P. G., Murphy, S. E., & Champagne, F. A. (2015). Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation. Epigenetics, 10(5), 408417. https://doi.org/10.1080/15592294.2015.1039221Google Scholar
Brody, G. H., Yu, T., Chen, E., Beach, S. R. H., & Miller, G. E. (2016). Family-centered prevention ameliorates the longitudinal association between risky family processes and epigenetic aging. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 57(5), 566574. https://doi.org/10.1111/jcpp.12495Google Scholar
Brown, A. S., Gyllenberg, D., Malm, H., McKeague, I. W., Hinkka-Yli-Salomäki, S., Artama, M., … Sourander, A. (2016). Association of selective serotonin reuptake inhibitor exposure during pregnancy with speech, scholastic, and motor disorders in offspring. JAMA Psychiatry, 73(11), 11631170. https://doi.org/10.1001/jamapsychiatry.2016.2594Google Scholar
Bush, N. R., Edgar, R. D., Park, M., MacIsaac, J. L., McEwen, L. M., Adler, N. E., … Boyce, W. T. (2018). The biological embedding of early-life socioeconomic status and family adversity in children’s genome-wide DNA methylation. Epigenomics, 10(11), 14451461. https://doi.org/10.2217/epi-2018-0042Google Scholar
Busso, D. S., McLaughlin, K. A., Brueck, S., Peverill, M., Gold, A. L., & Sheridan, M. A. (2017). Child abuse, neural structure, and adolescent psychopathology: A longitudinal study. Journal of the American Academy of Child & Adolescent Psychiatry, 56(4), 321–328.e1. https://doi.org/10.1016/j.jaac.2017.01.013Google 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 of the United States of America, 95(9), 53355340.Google Scholar
Cecil, C. A. M., Walton, E., Smith, R. G., Viding, E., McCrory, E. J., Relton, C. L., … Barker, E. D. (2016). DNA methylation and substance-use risk: A prospective, genome-wide study spanning gestation to adolescence. Translational Psychiatry, 6(12), e976. https://doi.org/10.1038/tp.2016.247Google Scholar
Champagne, F. A. (2008). Epigenetic mechanisms and the transgenerational effects of maternal care. Frontiers in Neuroendocrinology, 29(3), 386397. https://doi.org/10.1016/j.yfrne.2008.03.003Google Scholar
Champagne, F. A. (2016). Epigenetic legacy of parental experiences: Dynamic and interactive pathways to inheritance. Development and Psychopathology, 28(4 Pt. 2), 12191228. https://doi.org/10.1017/S0954579416000808Google Scholar
Champagne, F. A., & Meaney, M. J. (2006). Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biological Psychiatry, 59(12), 12271235. https://doi.org/10.1016/j.biopsych.2005.10.016Google Scholar
Champagne, F. A., (2007). Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behavioral Neuroscience, 121(6), 13531363. https://doi.org/10.1037/0735-7044.121.6.1353Google Scholar
Champagne, F. A., Weaver, I. C. G., Diorio, J., Dymov, S., Szyf, M., & Meaney, M. J. (2006). Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology, 147(6), 29092915. https://doi.org/10.1210/en.2005-1119Google Scholar
Cheung, P., Allis, C. D., & Sassone-Corsi, P. (2000). Signaling to chromatin through histone modifications. Cell, 103(2), 263271.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), 14131419. https://doi.org/10.1017/S0954579416000912Google Scholar
Cortessis, V. K., Thomas, D. C., Levine, A. J., Breton, C. V., Mack, T. M., Siegmund, K. D., … Laird, P. W. (2012). Environmental epigenetics: prospects for studying epigenetic mediation of exposure–response relationships. Human Genetics, 131(10), 15651589. https://doi.org/10.1007/s00439-012-1189-8Google Scholar
Curley, J. P., Mashoodh, R., & Champagne, F. A. (2011). Epigenetics and the origins of paternal effects. Hormones and Behavior, 59(3), 306314. https://doi.org/10.1016/j.yhbeh.2010.06.018Google Scholar
Danchin, É., Charmantier, A., Champagne, F. A., Mesoudi, A., Pujol, B., & Blanchet, S. (2011). Beyond DNA: Integrating inclusive inheritance into an extended theory of evolution. Nature Reviews. Genetics, 12(7), 475486. https://doi.org/10.1038/nrg3028Google Scholar
D’Elia, A. T. D., Matsuzaka, C. T., Neto, J. B. B., Mello, M. F., Juruena, M. F., & Mello, A. F. (2018). Childhood sexual abuse and indicators of immune activity: A systematic review. Frontiers in Psychiatry, 9, 354. https://doi.org/10.3389/fpsyt.2018.00354Google Scholar
Dias, B. G., & Ressler, K. J. (2014). Parental olfactory experience influences behavior and neural structure in subsequent generations. Nature Neuroscience, 17(1), 8996. https://doi.org/10.1038/nn.3594Google Scholar
Dupont, C., Armant, D. R., & Brenner, C. A. (2009). Epigenetics: Definition, mechanisms and clinical perspective. Seminars in Reproductive Medicine, 27(5), 351357. https://doi.org/10.1055/s-0029-1237423Google Scholar
Eddy, S. R. (2001). Non–coding RNA genes and the modern RNA world. Nature Reviews Genetics, 2(12), 919929. https://doi.org/10.1038/35103511Google Scholar
Fan, Y., Tian, C., Liu, Q., Zhen, X., Zhang, H., Zhou, L., … Zhu, M. (2018). Preconception paternal bisphenol A exposure induces sex-specific anxiety and depression behaviors in adult rats. PloS One, 13(2), e0192434. https://doi.org/10.1371/journal.pone.0192434Google Scholar
Fareri, D. S., Gabard-Durnam, L., Goff, B., Flannery, J., Gee, D. G., Lumian, D. S., … Tottenham, N. (2017). Altered ventral striatal-medial prefrontal cortex resting-state connectivity mediates adolescent social problems after early institutional care. Development and Psychopathology, 29(5), 18651876. https://doi.org/10.1017/S0954579417001456Google Scholar
Farrell, C., Doolin, K., O’ Leary, N., Jairaj, C., Roddy, D., Tozzi, L., … O’Keane, V. (2018). DNA methylation differences at the glucocorticoid receptor gene in depression are related to functional alterations in hypothalamic-pituitary-adrenal axis activity and to early life emotional abuse. Psychiatry Research, 265, 341348. https://doi.org/10.1016/j.psychres.2018.04.064Google Scholar
Feil, R., & Fraga, M. F. (2012). Epigenetics and the environment: Emerging patterns and implications. Nature Reviews. Genetics, 13(2), 97109. https://doi.org/10.1038/nrg3142Google Scholar
Fiorito, G., Polidoro, S., Dugué, P. -A., Kivimaki, M., Ponzi, E., Matullo, G., … Vineis, P. (2017). Social adversity and epigenetic aging: A multi-cohort study on socioeconomic differences in peripheral blood DNA methylation. Scientific Reports, 7(1), 16266. https://doi.org/10.1038/s41598-017-16391-5Google Scholar
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999). Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science, 286(5442), 11551158.Google Scholar
Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., … Mansuy, I. M. (2010). Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry, 68(5), 408415. https://doi.org/10.1016/j.biopsych.2010.05.036Google Scholar
Gapp, K., Jawaid, A., Sarkies, P., Bohacek, J., Pelczar, P., Prados, J., … Mansuy, I. M. (2014). Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nature Neuroscience, 17(5), 667669. https://doi.org/10.1038/nn.3695Google Scholar
Garg, E., Chen, L., Nguyen, T. T. T., Pokhvisneva, I., Chen, L. M., Unternaehrer, E., … Mavan Study Team. (2018). The early care environment and DNA methylome variation in childhood. Development and Psychopathology, 30(3), 891903. https://doi.org/10.1017/S0954579418000627Google Scholar
Gould, K. L., Coventry, W. L., Olson, R. K., & Byrne, B. (2018). Gene–environment interactions in ADHD: The roles of SES and chaos. Journal of Abnormal Child Psychology, 46(2), 251263. https://doi.org/10.1007/s10802-017-0268-7Google Scholar
Guibert, S., & Weber, M. (2013). Functions of DNA methylation and hydroxymethylation in mammalian development. Current Topics in Developmental Biology, 104, 4783. https://doi.org/10.1016/B978-0-12-416027-9.00002-4Google Scholar
Gurnot, C., Martin-Subero, I., Mah, S. M., Weikum, W., Goodman, S. J., Brain, U., … Hensch, T. K. (2015). Prenatal antidepressant exposure associated with CYP2E1 DNA methylation change in neonates. Epigenetics, 10(5), 361372. https://doi.org/10.1080/15592294.2015.1026031Google 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(6), 558567. https://doi.org/10.1002/dev.20461Google Scholar
Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., … Lumey, L. H. (2008). Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proceedings of the National Academy of Sciences of the United States of America, 105(44), 1704617049. https://doi.org/10.1073/pnas.0806560105Google Scholar
Hobel, C. J., Goldstein, A., & Barrett, E. S. (2008). Psychosocial stress and pregnancy outcome. Clinical Obstetrics and Gynecology, 51(2), 333348. https://doi.org/10.1097/GRF.0b013e31816f2709Google Scholar
Hodel, A. S., Hunt, R. H., Cowell, R. A., van den Heuvel, S. E., Gunnar, M. R., & Thomas, K. M. (2015). Duration of early adversity and structural brain development in post-institutionalized adolescents. NeuroImage, 105, 112119. https://doi.org/10.1016/j.neuroimage.2014.10.020Google Scholar
Horvath, S. (2013). DNA methylation age of human tissues and cell types. Genome Biology, 14(10), R115. https://doi.org/10.1186/gb-2013-14-10-r115Google Scholar
Houtepen, L. C., Hardy, R., Maddock, J., Kuh, D., Anderson, E. L., Relton, C. L., … Howe, L. D. (2018). Childhood adversity and DNA methylation in two population-based cohorts. Translational Psychiatry, 8(1), 266. https://doi.org/10.1038/s41398-018-0307-3Google Scholar
Hu, F. B., Persky, V., Flay, B. R., Zelli, A., Cooksey, J., & Richardson, J. (1997). Prevalence of asthma and wheezing in public schoolchildren: Association with maternal smoking during pregnancy. Annals of Allergy, Asthma & Immunology: Official Publication of the American College of Allergy, Asthma, & Immunology, 79(1), 8084. https://doi.org/10.1016/S1081-1206(10)63090–6Google Scholar
Jaffee, S. R., & Price, T. S. (2007). Gene–environment correlations: A review of the evidence and implications for prevention of mental illness. Molecular Psychiatry, 12(5), 432442. https://doi.org/10.1038/sj.mp.4001950Google Scholar
Jenuwein, T., & Allis, C. D. (2001). Translating the histone code. Science, 293(5532), 10741080. https://doi.org/10.1126/science.1063127Google Scholar
Jones, P. A. (2012). Functions of DNA methylation: Islands, start sites, gene bodies and beyond. Nature Reviews Genetics, 13(7), 484492.Google Scholar
Kertes, D. A., Bhatt, S. S., Kamin, H. S., Hughes, D. A., Rodney, N. C., & Mulligan, C. J. (2017). BNDF methylation in mothers and newborns is associated with maternal exposure to war trauma. Clinical Epigenetics, 9, 68. https://doi.org/10.1186/s13148-017-0367-xGoogle 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 of the United States of America, 112(22), 68076813. https://doi.org/10.1073/pnas.1408355111Google Scholar
Labonté, B., Suderman, M., Maussion, G., Navaro, L., Yerko, V., Mahar, I., … Turecki, G. (2012). Genome-wide epigenetic regulation by early-life trauma. Archives of General Psychiatry, 69(7), 722731. https://doi.org/10.1001/archgenpsychiatry.2011.2287Google Scholar
Lawn, R. B., Anderson, E. L., Suderman, M., Simpkin, A. J., Gaunt, T. R., Teschendorff, A. E., … Howe, L. D. (2018). Psychosocial adversity and socioeconomic position during childhood and epigenetic age: Analysis of two prospective cohort studies. Human Molecular Genetics, 27(7), 13011308. https://doi.org/10.1093/hmg/ddy036Google Scholar
Lester, B. M., Marsit, C. J., Giarraputo, J., Hawes, K., LaGasse, L. L., & Padbury, J. F. (2015). Neurobehavior related to epigenetic differences in preterm infants. Epigenomics, 7(7), 11231136. https://doi.org/10.2217/epi.15.63Google 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(8), 799806. https://doi.org/10.1038/77702Google Scholar
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(5332), 16591662.Google Scholar
Mashoodh, R., Habrylo, I. B., Gudsnuk, K. M., Pelle, G., & Champagne, F. A. (2018). Maternal modulation of paternal effects on offspring development. Proceedings. Biological Sciences, 285(1874). https://doi.org/10.1098/rspb.2018.0118Google Scholar
McGowan, P. O., Sasaki, A., D’Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., … Meaney, M. J. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience, 12(3), 342348. https://doi.org/10.1038/nn.2270Google Scholar
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C. T., Hallett, M., Meaney, M. J., & Szyf, M. (2011). Broad epigenetic signature of maternal care in the brain of adult rats. PloS One, 6(2), e14739. https://doi.org/10.1371/journal.pone.0014739Google Scholar
McLaughlin, K. A., & Lambert, H. K. (2017). Child trauma exposure and psychopathology: Mechanisms of risk and resilience. Current Opinion in Psychology, 14, 2934. https://doi.org/10.1016/j.copsyc.2016.10.004Google Scholar
Meaney, M. J. (2010). Epigenetics and the biological definition of gene x environment interactions. Child Development, 81(1), 4179. https://doi.org/10.1111/j.1467-8624.2009.01381.xGoogle Scholar
Melchior, M., Hersi, R., van der Waerden, J., Larroque, B., Saurel-Cubizolles, M. -J., Chollet, A., … EDEN MotherChild Cohort Study Group. (2015). Maternal tobacco smoking in pregnancy and children’s socio-emotional development at age 5: The EDEN mother–child birth cohort study. European Psychiatry: The Journal of the Association of European Psychiatrists, 30(5), 562568. https://doi.org/10.1016/j.eurpsy.2015.03.005Google Scholar
Milaniak, I., Cecil, C. A. M., Barker, E. D., Relton, C. L., Gaunt, T. R., McArdle, W., & Jaffee, S. R. (2017). Variation in DNA methylation of the oxytocin receptor gene predicts children’s resilience to prenatal stress. Development and Psychopathology, 29(5), 16631674. https://doi.org/10.1017/S0954579417001316Google Scholar
Millard, S. J., Weston-Green, K., & Newell, K. A. (2017). The effects of maternal antidepressant use on offspring behaviour and brain development: Implications for risk of neurodevelopmental disorders. Neuroscience and Biobehavioral Reviews, 80, 743765. https://doi.org/10.1016/j.neubiorev.2017.06.008Google Scholar
Miller, G. E., Yu, T., Chen, E., & Brody, G. H. (2015). Self-control forecasts better psychosocial outcomes but faster epigenetic aging in low-SES youth. Proceedings of the National Academy of Sciences of the United States of America, 112(33), 1032510330. https://doi.org/10.1073/pnas.1505063112Google Scholar
Mitsuya, K., Parker, A. N., Liu, L., Ruan, J., Vissers, M. C. M., & Myatt, L. (2017). Alterations in the placental methylome with maternal obesity and evidence for metabolic regulation. PloS One, 12(10), e0186115. https://doi.org/10.1371/journal.pone.0186115Google Scholar
Mohn, F., & Schübeler, D. (2009). Genetics and epigenetics: Stability and plasticity during cellular differentiation. Trends in Genetics: TIG, 25(3), 129136. https://doi.org/10.1016/j.tig.2008.12.005Google Scholar
Moisiadis, V. G., Constantinof, A., Kostaki, A., Szyf, M., & Matthews, S. G. (2017). Prenatal glucocorticoid exposure modifies endocrine function and behaviour for 3 generations following maternal and paternal transmission. Scientific Reports, 7(1), 11814. https://doi.org/10.1038/s41598-017-11635-wGoogle Scholar
Monk, C., Feng, T., Lee, S., Krupska, I., Champagne, F. A., & Tycko, B. (2016). Distress during pregnancy: Epigenetic regulation of placenta glucocorticoid-related genes and fetal neurobehavior. American Journal of Psychiatry, 173(7), 705713. https://doi.org/10.1176/appi.ajp.2015.15091171Google Scholar
Monk, C., Spicer, J., & Champagne, F. A. (2012). Linking prenatal maternal adversity to developmental outcomes in infants: The role of epigenetic pathways. Development and Psychopathology, 24(4), 13611376. https://doi.org/10.1017/S0954579412000764Google 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(1), 143155. https://doi.org/10.1017/S0954579411000605Google Scholar
Ng, S. -F., Lin, R. C. Y., Laybutt, D. R., Barres, R., Owens, J. A., & Morris, M. J. (2010). Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature, 467(7318), 963966. https://doi.org/10.1038/nature09491Google Scholar
Nigg, J., Nikolas, M., & Burt, S. A. (2010). Measured gene-by-environment interaction in relation to attention-deficit/hyperactivity disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 49(9), 863873. https://doi.org/10.1016/j.jaac.2010.01.025Google Scholar
Nilsson, E. E., Sadler-Riggleman, I., & Skinner, M. K. (2018). Environmentally induced epigenetic transgenerational inheritance of disease. Environmental Epigenetics, 4(2), dvy016. https://doi.org/10.1093/eep/dvy016Google Scholar
Noble, D. (2015). Conrad Waddington and the origin of epigenetics. Journal of Experimental Biology, 218(6), 816818. https://doi.org/10.1242/jeb.120071Google Scholar
Non, A. L., Binder, A. M., Kubzansky, L. D., & Michels, K. B. (2014). Genome-wide DNA methylation in neonates exposed to maternal depression, anxiety, or SSRI medication during pregnancy. Epigenetics, 9(7), 964972. https://doi.org/10.4161/epi.28853Google Scholar
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics, 3(2), 97106.Google Scholar
Papale, L. A., Seltzer, L. J., Madrid, A., Pollak, S. D., & Alisch, R. S. (2018). Differentially methylated genes in saliva are linked to childhood stress. Scientific Reports, 8(1), 10785. https://doi.org/10.1038/s41598-018-29107-0Google Scholar
Paquette, A. G., Houseman, E. A., Green, B. B., Lesseur, C., Armstrong, D. A., Lester, B., & Marsit, C. J. (2016). Regions of variable DNA methylation in human placenta associated with newborn neurobehavior. Epigenetics, 11(8), 603613. https://doi.org/10.1080/15592294.2016.1195534Google Scholar
Paquette, A. G., Lester, B. M., Koestler, D. C., Lesseur, C., Armstrong, D. A., & Marsit, C. J. (2014). Placental FKBP5 genetic and epigenetic variation is associated with infant neurobehavioral outcomes in the RICHS cohort. PloS One, 9(8), e104913. https://doi.org/10.1371/journal.pone.0104913Google Scholar
Parade, S. H., Parent, J., Rabemananjara, K., Seifer, R., Marsit, C. J., Yang, B. -Z., … Tyrka, A. R. (2017). Change in FK506 binding protein 5 (FKBP5) methylation over time among preschoolers with adversity. Development and Psychopathology, 29(5), 16271634. https://doi.org/10.1017/S0954579417001286Google Scholar
Parent, C. I., & Meaney, M. J. (2008). The influence of natural variations in maternal care on play fighting in the rat. Developmental Psychobiology, 50(8), 767776. https://doi.org/10.1002/dev.20342Google Scholar
Pauwels, S., Ghosh, M., Duca, R. C., Bekaert, B., Freson, K., Huybrechts, I., … Godderis, L. (2016). Dietary and supplemental maternal methyl-group donor intake and cord blood DNA methylation. Epigenetics, 12(1), 110. https://doi.org/10.1080/15592294.2016.1257450Google Scholar
Peña, C. J., Neugut, Y. D., & Champagne, F. A. (2013). Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats. Endocrinology, 154(11), 43404351. https://doi.org/10.1210/en.2013-1595Google Scholar
Perera, F., Vishnevetsky, J., Herbstman, J. B., Calafat, A. M., Xiong, W., Rauh, V., & Wang, S. (2012). Prenatal bisphenol A exposure and child behavior in an inner-city cohort. Environmental Health Perspectives, 120(8), 11901194. https://doi.org/10.1289/ehp.1104492Google Scholar
Razin, A. (1998). CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO Journal, 17(17), 49054908. https://doi.org/10.1093/emboj/17.17.4905Google Scholar
Razin, A., & Riggs, A. D. (1980). DNA methylation and gene function. Science, 210(4470), 604610.Google Scholar
Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S., & Bale, T. L. (2013). Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 33(21), 90039012. https://doi.org/10.1523/JNEUROSCI.0914-13.2013Google Scholar
Rogers, C. E., Lean, R. E., Wheelock, M. D., & Smyser, C. D. (2018). Aberrant structural and functional connectivity and neurodevelopmental impairment in preterm children. Journal of Neurodevelopmental Disorders, 10(1), 38. https://doi.org/10.1186/s11689-018-9253-xGoogle Scholar
Schieve, L. A., Tian, L. H., Rankin, K., Kogan, M. D., Yeargin-Allsopp, M., Visser, S., & Rosenberg, D. (2016). Population impact of preterm birth and low birth weight on developmental disabilities in US children. Annals of Epidemiology, 26(4), 267274. https://doi.org/10.1016/j.annepidem.2016.02.012Google Scholar
Sharp, G. C., Salas, L. A., Monnereau, C., Allard, C., Yousefi, P., Everson, T. M., … Relton, C. L. (2017). Maternal BMI at the start of pregnancy and offspring epigenome-wide DNA methylation: Findings from the pregnancy and childhood epigenetics (PACE) consortium. Human Molecular Genetics, 26(20), 40674085. https://doi.org/10.1093/hmg/ddx290Google Scholar
Shorey-Kendrick, L. E., McEvoy, C. T., Ferguson, B., Burchard, J., Park, B. S., Gao, L., … Spindel, E. R. (2017). Vitamin C prevents offspring DNA methylation changes associated with maternal smoking in pregnancy. American Journal of Respiratory and Critical Care Medicine, 196(6), 745755. https://doi.org/10.1164/rccm.201610-2141OCGoogle Scholar
Simpkin, A. J., Hemani, G., Suderman, M., Gaunt, T. R., Lyttleton, O., Mcardle, W. L., … Smith, G. D. (2016). Prenatal and early life influences on epigenetic age in children: A study of mother–offspring pairs from two cohort studies. Human Molecular Genetics, 25(1), 191201. https://doi.org/10.1093/hmg/ddv456Google Scholar
Sonuga-Barke, E. J. S., Kennedy, M., Kumsta, R., Knights, N., Golm, D., Rutter, M., … Kreppner, J. (2017). Child-to-adult neurodevelopmental and mental health trajectories after early life deprivation: The young adult follow-up of the longitudinal English and Romanian Adoptees study. Lancet, 389(10078), 15391548. https://doi.org/10.1016/S0140-6736(17)30045-4Google Scholar
Stamoulis, C., Vanderwert, R. E., Zeanah, C. H., Fox, N. A., & Nelson, C. A. (2017). Neuronal networks in the developing brain are adversely modulated by early psychosocial neglect. Journal of Neurophysiology, 118(4), 22752288. https://doi.org/10.1152/jn.00014.2017Google Scholar
Staneva, A., Bogossian, F., Pritchard, M., & Wittkowski, A. (2015). The effects of maternal depression, anxiety, and perceived stress during pregnancy on preterm birth: A systematic review. Women and Birth: Journal of the Australian College of Midwives, 28(3), 179193. https://doi.org/10.1016/j.wombi.2015.02.003Google Scholar
Susser, E. S., & Lin, S. P. (1992). Schizophrenia after prenatal exposure to the Dutch Hunger Winter of 1944–1945. Archives of General Psychiatry, 49(12), 983988.Google Scholar
Talati, A., Wickramaratne, P. J., Wesselhoeft, R., & Weissman, M. M. (2017). Prenatal tobacco exposure, birthweight, and offspring psychopathology. Psychiatry Research, 252, 346352. https://doi.org/10.1016/j.psychres.2017.03.016Google Scholar
Torche, F., & Kleinhaus, K. (2012). Prenatal stress, gestational age and secondary sex ratio: The sex-specific effects of exposure to a natural disaster in early pregnancy. Human Reproduction, 27(2), 558567. https://doi.org/10.1093/humrep/der390Google Scholar
Troller-Renfree, S., McDermott, J. M., Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2015). The effects of early foster care intervention on attention biases in previously institutionalized children in Romania. Developmental Science, 18(5), 713722. https://doi.org/10.1111/desc.12261Google Scholar
Tserga, A., Binder, A. M., & Michels, K. B. (2017). Impact of folic acid intake during pregnancy on genomic imprinting of IGF2/H19 and 1-carbon metabolism. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 31(12), 51495158. https://doi.org/10.1096/fj.201601214RRGoogle Scholar
Vassoler, F. M., White, S. L., Schmidt, H. D., Sadri-Vakili, G., & Pierce, R. C. (2013). Epigenetic inheritance of a cocaine-resistance phenotype. Nature Neuroscience, 16(1), 4247. https://doi.org/10.1038/nn.3280Google Scholar
Waddington, C. H. (1940). Organisers & genes. Cambridge, UK: Cambridge University Press.Google Scholar
Wadhwa, P. D., Entringer, S., Buss, C., & Lu, M. C. (2011). The contribution of maternal stress to preterm birth: Issues and considerations. Clinics in Perinatology, 38(3), 351384. https://doi.org/10.1016/j.clp.2011.06.007Google 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(8), 847854. https://doi.org/10.1038/nn1276Google Scholar
Weinstock, M., Fride, E., & Hertzberg, R. (1988). Prenatal stress effects on functional development of the offspring. Progress in Brain Research, 73, 319331. https://doi.org/10.1016/S0079-6123(08)60513-0Google Scholar
Welch, M. G., Firestein, M. R., Austin, J., Hane, A. A., Stark, R. I., Hofer, M. A., … Myers, M. M. (2015). Family nurture intervention in the neonatal intensive care unit improves social-relatedness, attention, and neurodevelopment of preterm infants at 18 months in a randomized controlled trial. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 56(11), 12021211. https://doi.org/10.1111/jcpp.12405Google Scholar
Welch, M. G., Stark, R. I., Grieve, P. G., Ludwig, R. J., Isler, J. R., Barone, J. L., & Myers, M. M. (2017). Family nurture intervention in preterm infants increases early development of cortical activity and independence of regional power trajectories. Acta Paediatrica, 106(12), 19521960. https://doi.org/10.1111/apa.14050Google Scholar
Wilkinson, L. S., Davies, W., & Isles, A. R. (2007). Genomic imprinting effects on brain development and function. Nature Reviews. Neuroscience, 8(11), 832843. https://doi.org/10.1038/nrn2235Google Scholar
Wilson, R. D., Davies, G., Désilets, V., Reid, G. J., Summers, A., Wyatt, P., … Genetics Committee and Executive and Council of the Society of Obstetricians and Gynaecologists of Canada (2003). The use of folic acid for the prevention of neural tube defects and other congenital anomalies. Journal of Obstetrics and Gynaecology Canada, 25(11), 959973.Google Scholar
Winther, G., Eskelund, A., Bay-Richter, C., Elfving, B., Müller, H. K., Lund, S., & Wegener, G. (2019). Grandmaternal high-fat diet primed anxiety-like behaviour in the second-generation female offspring. Behavioural Brain Research, 359, 4755. https://doi.org/10.1016/j.bbr.2018.10.017Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×