Annual research review: Epigenetic mechanisms and environmental shaping of the brain during sensitive periods of development

Journal of Child Psychology and Psychiatry and Allied Disciplines

Volumn 52, Issue 4, 2011, Pages 398-408

  Roth, Tania L ^a   Sweatt, J David ^a  

^a University of Alabama at Birmingham   (United States)

Author keywords

DNA methylation; Early life experience; Epigenetic; Histone modification; Maternal care

Indexed keywords

HISTONE;

ANIMAL; BRAIN; COGNITIVE DEFECT; COPING BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; HUMAN; LIFE EVENT; MATERNAL BEHAVIOR; MENTAL DISEASE; MOUSE; NEWBORN; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; PSYCHOLOGICAL ASPECT; RAT; REVIEW; SOCIAL ENVIRONMENT;

ANIMALS; BRAIN; COGNITION DISORDERS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; HISTONES; HUMANS; INFANT, NEWBORN; LIFE CHANGE EVENTS; MATERNAL BEHAVIOR; MENTAL DISORDERS; MICE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RESILIENCE, PSYCHOLOGICAL; SOCIAL ENVIRONMENT; TRANSCRIPTION, GENETIC;

EID: 79952648592     PISSN: 00219630     EISSN: 14697610     Source Type: Journal    
DOI: 10.1111/j.1469-7610.2010.02282.x     Document Type: Review

References (81)

1. Abdolmaleky, H.M., Cheng, K.H., Russo, A., Smith, C.L., Faraone, S.V., Wilcox, M., Shafa, R., Glatt, S.J., Nguyen, G., Ponte, J.F., Thiagalingam, S., & Tsuang, M.T. (2005). Hypermethylation of the reelin (RELN) promoter in the brain of schizophrenic patients: A preliminary report. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 134, 60-66. (Pubitemid 40411111)
2. Barr, G. A., Moriceau, S., Shionoya, K., Muzny, K., Gao, P., Wang, S., & Sullivan, R.M. (2009). Transitions in infant learning are modulated by dopamine in the amygdala. Nature Neuroscience, 12, 1367-1369.
3. Barreto, G., Schafer, A., Marhold, J., Stach, D., Swaminathan, S.K., Handa, V., Doderlein, G., Maltry, N., Wu, W., Lyko, F., & Niehrs, C. (2007). Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature, 445, 671-675. (Pubitemid 46232889)
4. Berger, S.L. (2007). The complex language of chromatin regulation during transcription. Nature, 447, 407-412.
5. Bhattacharya, S.K., Ramchandani, S., Cervoni, N., & Szyf, M. (1999). A mammalian protein with specific demethylase activity for mCpG DNA. Nature, 397, 579-583.
6. Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes and Development, 16, 6-21.
7. Borrelli, E., Nestler, E.J., Allis, C.D., & Sassone-Corsi, P. (2008). Decoding the epigenetic language of neuronal plasticity. Neuron, 60, 961-974.
8. Branchi, I., Francia, N., & Alleva, E. (2004). Epigenetic control of neurobehavioural plasticity: The role of neurotrophins. Behavioural Pharmacology, 15, 353-362. (Pubitemid 39238345)
9. Bremner, J.D. (2003). Long-term effects of childhood abuse on brain and neurobiology. Child and Adolescent Psychiatric Clinics of North America, 12, 271-292.
10. Brown, G.W., & Harris, T.O. (2008). Depression and the serotonin transporter 5-HTTLPR polymorphism: A review and a hypothesis concerning gene-environment interaction. Journal of Affective Disorders, 111, 1-12.
11. Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P.M., & Meaney, M.J. (1998). Maternal care during infant regulates the development of neural systems mediating the expression of fearfulness in the rat. Proceedings of the National Academy of Sciences, 95, 5335-5340. (Pubitemid 28208598)
12. Casey, B.J., Glatt, C.E., Tottenham, N., Soliman, F., Bath, K., Amso, D., Altemus, M., Pattwell, S., Jones, R., Levita, L., McEwen, B., Magariños, A.M., Gunnar, M., Thomas, K.M., Mezey, J., Clark, A.G., Hempstead, B.L., & Lee, F.S. (2009). Brain-derived neurotrophic factor as a model system for examining gene by environment interactions across development. Neuroscience, 164, 108-120.
13. Caspi, A., McClay, J., Moffitt, T.E., Mill, J., Martin, J., Craig, I.W., Taylor, A., & Poulton, R. (2002). Role of genotype in the cycle of violence in maltreated children. Science, 297, 851-854. (Pubitemid 34839638)
14. Caspi, A., Sugden, K., Moffitt, T.E., Taylor, A., Craig, I.W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., & Poulton, R. (2003). Influence of life stress on depression: Moderation by a polymorphism in the 5-HT gene. Science, 301, 386-400.
15. Chahrour, M., Jung, S.Y., Shaw, C., Zhou, X., Wong, S.T.C., Qin, J., & Zoghbi, H.Y. (2008). MeCP2, a key contributor to neurological disease, activates and represses transcription. Science, 320, 1224-1229. (Pubitemid 351929512)
16. Champagne, F., Diorio, J., Sharma, S., & Meaney, M.J. (2001). Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proceedings of the National Academy of Sciences, 98, 12736-12741. (Pubitemid 33020015)
17. Champagne, F., Weaver, I., 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, 2909-2915. (Pubitemid 43764626)
18. 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 and Behavior, 79, 359-371. (Pubitemid 37098279)
19. Cohen, S., Zhou, Z., & Greenberg, M.E. (2008). Activating a repressor. Science, 320, 1172-1173.
20. Connor, C.M., & Akbarian, S. (2008). DNA methylation changes in schizophrenia and bipolar disorder. Epigenetics, 3, 55-58.
21. Costa, E., Chen, Y., Dong, E., Grayson, D.R., Kundakovic, M., Maloku, E., Ruzicka, W., Satta, R., Veldic, M., Zhubi, A., & Guidotti, A. (2009). GABAergic promoter hypermethylation as a model to study the neurochemistry of schizophrenia vulnerability. Expert Review of Neurotherapeutics, 9, 87-98.
22. Cottrell, E.C., & Seckl, J. (2009). Prenatal stress, glucocorticoids and the programming of adult disease. Frontiers in Behavioral Neuroscience, 3, Epub ahead of print Sep 7 2009.
23. De Bellis, M.D. (2005). The psychobiology of neglect. Child Maltreatment, 10, 150-172.
24. Duman, R.S., & Monteggia, L.M. (2006). A neurotrophic model for stress-related mood disorders. Biological Psychiatry, 59, 1116-1127.
25. Fagiolini, M., Jensen, C.L., & Champagne, F.A. (2009). Epigenetic influences on brain development and plasticity. Current Opinion in Neurobiology, 19, 207-212.
26. Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M., & Tsai, L.-H. (2007). Recovery of learning and memory is associated with chromatin remodeling. Nature, 447, 178-182.
27. Francis, D.D., Caldji, C., Champagne, F., Plotsky, P.M., & Meaney, M.J. (1999). The role of corticotropin-releasing factor-norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biological Psychiatry, 46, 1153-1166. (Pubitemid 30114434)
28. Franklin, T.B., & Mansuy, I.M. (2009). Epigenetic inheritance in mammals: Evidence for the impact of adverse environmental effects. Neurobiology of Disease, Epub ahead of print November 27, 2009.
29. Fumagalli, F., Molteni, R., Racagni, G., & Riva, M.A. (2007). Stress during development: Impact on neuroplasticity and relevance to psychopathology. Progress in Neurobiology, 81, 197-217. (Pubitemid 46498900)
30. Gavin, D.P., & Sharma, R.P. (2009). Chromatin from peripheral blood mononuclear cells as biomarkers for epigenetic abnormalities in schizophrenia. Cardiovascular Psychiatry and Neurology, 2009, Article ID 409562.
31. Goel, N., & Bale, T.L. (2009). Examining the intersection of sex and stress in modeling neuropsychiatric disorders. Journal of Neuroendocrinology, 21, 415-420.
32. Gräff, J., & Mansuy, I.M. (2008). Epigenetic codes in cognition and behaviour. Behavioural Brain Research, 192, 70-87.
33. Grayson, D., Chen, Y., Dong, E., Kundakovic, M., & Guidotti, A. (2009). From trans-methylation to cytosine methylation: Evolution of the methylation hypothesis of schizophrenia. Epigenetics, 4, 144-149.
34. Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145-173.
35. Haberland, M., Montgomery, R.L., & Olson, E.N. (2009). The many roles of histone deacetylases in development and physiology: Implications for disease and therapy. Nature Reviews Genetics, 10, 32-42.
36. Heim, C., & Nemeroff, C.B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49, 1023-1039. (Pubitemid 32595461)
37. Jirtle, R.L., & Skinner, M.K. (2007). Environmental epigenomics and disease susceptibility. Nature Reviews Genetics, 8, 253-262. (Pubitemid 46439287)
38. Kaffman, A., & Meaney, M.J. (2007). Neurodevelopmental sequelae of postnatal maternal care in rodents: Clinical and research implications of molecular insights. Journal of Child Psychology and Psychiatry, 48, 224-244. (Pubitemid 46372119)
39. Kaufman, J., Plotsky, P.M., Nemeroff, C.B., & Charney, D.S. (2000). Effects of early adverse experiences on brain structure and function: Clinical implications. Biological Psychiatry, 48, 778-790.
40. Kinsella, M.T., & Monk, C. (2009). Impact of maternal stress, depression and anxiety on fetal neurobehavioral development. Clinical Obstetrics and Gynecology, 52, 425-440.
41. Korosi, A., & Baram, T.Z. (2009). The pathways from mother's love to baby's future. Frontiers in Behavioral Neuroscience, 3, Epub ahead of print Sep 24 2009.
42. Kumsta, R., Stevens, S., Brookes, K., Schlotz, W., Castle, J., Beckett, C., Kreppner, J., Rutter, M., & Sonuga-Barke, E. (2010). 5HTT genotype moderates the influence of early institutional deprivation on emotional problems in adolescence: Evidence from the English and Romanian Adoptee (ERA) study. Journal of Child Psychology and Psychiatry, Epub ahead of print Mar 25, 2010.
43. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P.M., & Meaney, M.J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science, 277, 1659-1662. (Pubitemid 27446227)
44. Liu, L., Van Groen, T., Kadish, I., & Tollefsbol, T.O. (2009). DNA methylation impacts on learning and memory in aging. Neurobiology of Aging, 30, 549-560.
45. 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.
46. Lupien, S.J., McEwen, B.S., Gunnar, M.R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434-445.
47. Ma, D.K., Jang, M.-H., Guo, J.U., Kitabatake, Y., Chang, M.-L., Pow-Anpongkul, N., Flavell, R.A., Lu, B., Ming, G.-L., & Song, H. (2009). Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science, 323, 1074-1077.
48. Marmorstein, R., & Trievel, R.C. (2009). Histone modifying enzymes: Structures, mechanisms, and specificities. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 1789, 58-68.
49. McCarthy, M.M., Auger, A.P., Bale, T.L., De Vries, G.J., Dunn, G.A., Forger, N.G., Murray, E.K., Nugent, B.M., Schwarz, J.M., & Wilson, M.E. (2009). The Epigenetics of Sex Differences in the Brain. Journal of Neuroscience, 29, 12815-12823.
50. McEwen, B.S. (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiological Reviews, 87, 873-904.
51. McGowan, P.O., Sasaki, A., D'alessio, A.C., Dymov, S., Labonte, B., Szyf, M., Turecki, G., & Meaney, M.J. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience, 12, 342-348.
52. McGowan, P.O., & Szyf, M. (2010). The epigenetics of social adversity in early life: Implications for mental health outcomes. Neurobiology of Disease, Epub ahead of print January 4, 2010.
53. Meaney, M.J., Diorio, J., Francis, D., Weaver, S., Yau, J., Chapman, K., & Seckl, J.R. (2000). Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: The effects of thyroid hormones and serotonin. Journal of Neuroscience, 20, 3926-3935. (Pubitemid 30266253)
54. Mill, J., Tang, T., Kaminsky, Z., Khare, T., Yazdanpanah, S., Bouchard, L., Jia, P., Assadzadeh, A., Flanagan, J., Schumacher, A., Wang, S.-C., & Petronis, A. (2008). Epigenomic profiling reveals DNA-methylation changes associated with major psychosis. The American Journal of Human Genetics, 82, 696-711. (Pubitemid 351726115)
55. Miller, C.A., & Sweatt, J.D. (2007). Covalent modification of DNA regulates memory formation. Neuron, 53, 857-869. (Pubitemid 46367557)
56. Miranda, T.B., & Jones, P.A. (2007). DNA methylation: The nuts and bolts of repression. Journal of Cellular Physiology, 213, 384-390. (Pubitemid 47509717)
57. Moriceau, S., Shionoya, K., Jakubs, K., & Sullivan, R.M. (2009). Early-Life stress disrupts attachment learning: The role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine. Journal of Neuroscience, 29, 15745-15755.
58. Mueller, B.R., & Bale, T.L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience, 28, 9055-9065.
59. Murgatroyd, C., Patchev, A.V., Wu, Y., Micale, V., Bockmuhl, Y., Fischer, D., Holsboer, F., Wotjak, C.T., Almeida, O.F.X., & Spengler, D. (2009). Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nature Neuroscience, 12, 1559-1566.
60. Novikova, S.I., He, F., Bai, J., Cutrufello, N.J., Lidow, M.S., & Undieh, A.S. (2008). Maternal cocaine administration in mice alters DNA methylation and gene expression in hippocampal neurons of neonatal and prepubertal offspring. PLoS ONE, 3, e1919.
61. Oberlander, T., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, M.D. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics, 3, 97-106.
62. Peedicayil, J. (2008). Epigenetic biomarkers in psychiatric disorders. British Journal of Pharmacology, 155, 795-796.
63. Perry, B.D., Pollard, R., Blakely, T., Baker, W., & Vigilante, D. (1995). Childhood trauma, the neurobiology of adaptation and 'use-dependent' development of the brain: How 'states' become 'traits'. Infant Mental Health Journal, 16, 271-291.
64. Pryce, C.R., & Feldon, J. (2003). Long-term neurobehavioral impact of postnatal environment in rats: Manipulations, effects and mediating mechanisms. Neuroscience & Biobehavioral Reviews, 27, 57-71. (Pubitemid 36535390)
65. Roth, T.L., Lubin, F.D., Funk, A.J., & Sweatt, J.D. (2009a). Lasting epigenetic influence of early-life adversity on the BDNF gene. Biological Psychiatry, 65, 760-769.
66. Roth, T.L., Lubin, F.D., Sodhi, M., & Kleinman, J.E. (2009b). Epigenetic mechanisms in schizophrenia. Biochimica et Biophysica Acta (BBA) - General Subjects, 1790, 869-877.
67. Roth, T.L., & Sweatt, J.D. (2009). Regulation of chromatin structure in memory formation. Current Opinion in Neurobiology, 19, 336-342.
68. 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, 226-261. (Pubitemid 43356058)
69. Sanchez, M.M. (2006). The impact of early adverse care on HPA axis development: Nonhuman primate models. Hormones and Behavior, 50, 623-631.
70. Schlinzig, T., Johansson, S., Gunnar, A., Ekström, T.J., & Norman, M. (2009). Epigenetic modulation at birth - altered DNA-methylation in white blood cells after Caesarean section. Acta Pædiatrica, 98, 1096-1099.
71. Schore, A.N. (2002). Dysregulation of the right brain: A fundamental mechanism of traumatic attachment and the psychopathogenesis of posttraumatic stress disorder. Australian and New Zealand Journal of Psychiatry, 36, 9-30.
72. Strahl, B.D., & Allis, C.D. (2000). The language of covalent histone modifications. Nature, 403, 41-45. (Pubitemid 30038513)
73. Sullivan, R.M., Landers, M., Yeaman, B., & Wilson, D.A. (2000). Good memories of bad events in infancy. Nature, 407, 38-39.
74. Teicher, M.H., Andersen, S.L., Polcari, A., Anderson, C.M., Navalta, C.P., & Kim, D.M. (2003). The neurobiological consequences of early stress and childhood maltreatment. Neuroscience & Biobehavioral Reviews, 27, 33-44. (Pubitemid 36537818)
75. Tsankova, N., Berton, O., Renthal, W., Kumar, A., Neve, R., & Nestler, E. (2006). Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nature Neuroscience, 9, 519-525.
76. Tsankova, N., Renthal, W., Kumar, A., & Nestler, E.J. (2007). Epigenetic regulation in psychiatric disorders. Nature Reviews Neuroscience, 8, 355-367. (Pubitemid 46652469)
77. Weaver, I., Champagne, F., Brown, S., Dymov, S., Sharma, S., Meaney, M. J., & Szyf, M. (2005). Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: Altering epigenetic marking later in life. Journal of Neuroscience, 25, 11045-11054. (Pubitemid 41692634)
78. Weaver, I., Meaney, M.J., & Szyf, M. (2006). Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proceedings of the National Academy of Sciences, 103, 3480-3485. (Pubitemid 43346494)
79. Weaver, I.C.G., Cervoni, N., Champagne, F.A., D'alessio, A.C., Sharma, S., Seckl, J.R., Dymov, S., Szyf, M., & Meaney, M.J. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847-854.
80. Yasui, D.H., Peddada, S., Bieda, M.C., Vallero, R.O., Hogart, A., Nagarajan, R.P., Thatcher, K.N., Farnham, P.J., & Lasalle, J.M. (2007). Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proceedings of the National Academy of Sciences, 104, 19416-19421.
81. Zhang, T.-Y., & Meaney, M.J. (2010). Epigenetics and the environmental regulation of the genome and Its function. Annual Review of Psychology, 61, 439-466.