Exposure to caregiver maltreatment alters expression levels of epigenetic regulators in the medial prefrontal cortex

International Journal of Developmental Neuroscience

Volumn 31, Issue 8, 2013, Pages 804-810

  Blaze, Jennifer ^a   Roth, Tania L ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Dnmt; Early life stress; Epigenetics; Gadd45b; Hdac; Maternal care; MeCP2; MPFC

Indexed keywords

DNA; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; HISTONE DEACETYLASE 1; MESSENGER RNA; METHYL CPG BINDING PROTEIN 2; TUBULIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CAGE; CAREGIVER; CONTROLLED STUDY; DNA METHYLATION; DNMT1 GENE; DNMT3A GENE; EARLY LIFE STRESS; EPIGENETICS; FEMALE; FOSTER CARE; GADD45B GENE; GENE EXPRESSION; HDAC1 GENE; MALE; MATERNAL BEHAVIOR; MECP2 GENE; NONHUMAN; NURTURING BEHAVIOR; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; VOCALIZATION;

BDNF; BRAIN-DERIVED NEUROTROPHIC FACTOR; DNA METHYLTRANSFERASE; DNMT; EARLY-LIFE STRESS; EPIGENETICS; GADD45B; GROWTH ARREST AND DNA-DAMAGE-INDUCIBLE BETA; HAT; HDAC; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; MATERNAL CARE; MECP2; MEDIAL PREFRONTAL CORTEX; METHYL-CPG BINDING PROTEIN-2; MPFC; PN; POSTNATAL DAY;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, DIFFERENTIATION; CAREGIVERS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DYNAMINS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE DEACETYLASE 1; MALE; METHYL-CPG-BINDING PROTEIN 2; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS;

EID: 84886473181     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2013.10.001     Document Type: Article

References (60)

1. Akbarian S., Chen R.Z., Gribnau J., Rasmussen T.P., Fong H.-f., Jaenisch R., Jones E.G. Expression pattern of the rett syndrome gene mecp2 in primate prefrontal cortex. Neurobiol. Dis. 2001, 8:784-791.
2. Ballas N., Grunseich C., Lu D.D., Speh J.C., Mandel G. Rest and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 2005, 121:645-657.
3. Balmer D., Goldstine J., Rao Y.M., LaSalle J. Elevated methyl-cpg-binding protein 2 expression is acquired during postnatal human brain development and is correlated with alternative polyadenylation. J. Mol. Med. 2003, 81:61-68.
4. Benes F.M., Taylor J.B., Cunningham M.C. Convergence and plasticity of monoaminergic systems in the medial prefrontal cortex during the postnatal period: implications for the development of psychopathology. Cereb. Cortex 2000, 10:1014-1027.
5. Blaze J., Scheuing L., Roth T.L. Differential methylation of genes in the medial prefrontal cortex of developing and adult rats following exposure to maltreatment or nurturing care during infancy. Dev. Neurosci. 2013, 35:306-316.
6. Caldji C., Diorio J., Meaney M.J. Variations in maternal care in infancy regulate the development of stress reactivity. Biol. Psychiatry 2000, 48:1164-1174.
7. Caldji C., Hellstrom I.C., Zhang T.-Y., Diorio J., Meaney M.J. Environmental regulation of the neural epigenome. FEBS Lett. 2011, 585:2049-2058.
8. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T., Qin J., Zoghbi H.Y. Mecp2, a key contributor to neurological disease, activates and represses transcription. Science 2008, 320:1224-1229.
9. Chen R.Z., Akbarian S., Tudor M., Jaenisch R. Deficiency of methyl-cpg binding protein-2 in cns neurons results in a rett-like phenotype in mice. Nat. Genet. 2001, 27:327-331.
10. Cicchetti D., Toth S.L. Child maltreatment. Ann. Rev. Clin. Psychol. 2005, 1:409-438.
11. Day J.J., Sweatt J.D. Epigenetic modifications in neurons are essential for formation and storage of behavioral memory. Neuropsychopharmacology 2011, 36:357-358.
12. Diorio D., Viau V., Meaney M. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 1993, 13:3839-3847.
13. Feng J., Chang H., Li E., Fan G. Dynamic expression of de novo DNA methyltransferases dnmt3a and dnmt3b in the central nervous system. J. Neurosci. Res. 2005, 79:734-746.
14. Gavin D.P., Sharma R.P., Chase K.A., Matrisciano F., Dong E., Guidotti A. Growth arrest and DNA-damage-inducible, beta (gadd45b)-mediated DNA demethylation in major psychosis. Neuropsychopharmacology 2012, 37:531-542.
15. Goto K., Numata M., Komura J.-I., Ono T., Bestor T.H., Kondo H. Expression of DNA methyltransferase gene in mature and immature neurons as well as proliferating cells in mice. Differentiation 1994, 56:39-44.
16. Hao Y., Huang W., Nielsen D.A., Kosten T.A. Litter gender composition and sex affect maternal behavior and DNA methylation levels of the oprm1 gene in rat offspring. Front. Psychiatry 2011, 2:21.
17. Inano K., Suetake I., Ueda T., Miyake Y., Nakamura M., Okada M., Tajima S. Maintenance-type DNA methyltransferase is highly expressed in post-mitotic neurons and localized in the cytoplasmic compartment. J. Biochem. 2000, 128:315-321.
18. Ivy A.S., Brunson K.L., Sandman C., Baram T.Z. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience 2008, 154:1132-1142.
19. Jensen Peña C., Monk C., Champagne F.A. Epigenetic effects of prenatal stress on 11β-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS ONE 2012, 7:e39791.
20. Jessen H.M., Auger A.P. Sex differences in epigenetic mechanisms may underlie risk and resilience for mental health disorders. Epigenetics 2011, 6:857-861.
21. Jones P.L., Jan Veenstra G.C., Wade P.A., Vermaak D., Kass S.U., Landsberger N., Strouboulis J., Wolffe A.P. Methylated DNA and mecp2 recruit histone deacetylase to repress transcription. Nat. Genet. 1998, 19:187-191.
22. Jorgensen H.F., Bird A. Mecp2 and other methyl-cpg binding proteins. Ment. Retard. Dev. Disabil. Res. Rev. 2002, 8:87-93.
23. Kaufmann W.E., Johnston M.V., Blue M.E. Mecp2 expression and function during brain development: Implications for rett syndrome's pathogenesis and clinical evolution. Brain Dev. 2005, 27:S77-S87.
24. Kolodkin M.H., Auger A.P. Sex difference in the expression of DNA methyltransferase 3a in the rat amygdala during development. J. Neuroendocrinol. 2011, 23:577-583.
25. Kurian J.R., Bychowski M.E., Forbes-Lorman R.M., Auger C.J., Auger A.P. Mecp2 organizes juvenile social behavior in a sex-specific manner. J. Neurosci. 2008, 28:7137-7142.
26. Kurian J.R., Forbes-Lorman R.M., Auger A.P. Sex difference in mecp2 expression during a critical period of rat brain development. Epigenetics 2007, 2:173-178.
27. Leach P.T., Poplawski S.G., Kenney J.W., Hoffman B., Liebermann D.A., Abel T., Gould T.J. Gadd45b knockout mice exhibit selective deficits in hippocampus-dependent long-term memory. Learn. Mem. 2012, 19:319-324.
28. Levine A., Worrell T.R., Zimnisky R., Schmauss C. Early life stress triggers sustained changes in histone deacetylase expression and histone h4 modifications that alter responsiveness to adolescent antidepressant treatment. Neurobiol. Dis. 2012, 45:488-498.
29. Lewis C.R., Staudinger K., Scheck L., Olive M.F. The effects of maternal separation on adult methamphetamine self-administration, extinction, reinstatement, and mecp2 immunoreactivity in the nucleus accumbens. Front. Psychiatry 2013, 4:55.
30. Lister R., Mukamel E.A., Nery J.R., Urich M., Puddifoot C.A., Johnson N.D., Lucero J., Huang Y., Dwork A.J., Schultz M.D., Yu M., Tonti-Filippini J., Heyn H., Hu S., Wu J.C., Rao A., Esteller M., He C., Haghighi F.G., Sejnowski T.J., Behrens M.M., Ecker J.R. Global epigenomic reconfiguration during mammalian brain development. Science 2013, epub ahead of print.
31. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative pcr and the 2-δδct method. Methods 2001, 25:402-408.
32. Ma D.K., Guo J.U., Ming G.L., Song H. DNA excision repair proteins and gadd45 as molecular players for active DNA demethylation. Cell Cycle 2009, 8:1526-1531.
33. 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. Neuronal activity-induced gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 2009, 323:1074-1077.
34. Matrisciano F., Tueting P., Maccari S., Nicoletti F., Guidotti A. Pharmacological activation of group-ii metabotropic glutamate receptors corrects a schizophrenia-like phenotype induced by prenatal stress in mice. Neuropsychopharmacology 2012, 37:929-938.
35. 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. The epigenetics of sex differences in the brain. J. Neurosci. 2009, 29:12815-12823.
36. Miller B.H., Zeier Z., Xi L., Lanz T.A., Deng S., Strathmann J., Willoughby D., Kenny P.J., Elsworth J.D., Lawrence M.S., Roth R.H., Edbauer D., Kleiman R.J., Wahlestedt C. Microrna-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:3125-3130.
37. Moore C.L., Morelli G.A. Mother rats interact differently with male amd female offspring. J. Comp. Physiol. Psychol. 1979, 93:677-684.
38. Moore L.D., Le T., Fan G. DNA methylation and its basic function. Neuropsychopharmacology 2012, 38:23-38.
39. Murgatroyd C., Patchev A.V., Wu Y., Micale V., Bockmuhl Y., Fischer D., Holsboer F., Wotjak C.T., Almeida O.F.X., Spengler D. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 2009, 12:1559-1566.
40. Nagarajan R., Hogart A., Gwye Y., Martin M.R., LaSalle J.M. Reduced mecp2 expression is frequent in autism frontal cortex and correlates with aberrant mecp2 promoter methylation. Epigenetics 2006, 1:172-182.
41. Numata S., Ye T., Hyde T.M., Guitart-Navarro X., Tao R., Wininger M., Colantuoni C., Weinberger D.R., Kleinman J.E., Lipska B.K. DNA methylation signatures in development and aging of the human prefrontal cortex. Am. J. Hum. Genet. 2012, 90:260-272.
42. Roth T.L. Epigenetics of neurobiology and behavior during development and adulthood. Dev. Psychobiol. 2012, 54:590-597.
43. Roth T.L., Lubin F.D., Funk A.J., Sweatt J.D. Lasting epigenetic influence of early-life adversity on the bdnf gene. Biol. Psychiatry 2009, 65:760-769.
44. Roth T.L., Sullivan R.M. Memory of early maltreatment: neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning. Biol. Psychiatry 2005, 57:823-831.
45. Sanchez M.M. The impact of early adverse care on hpa axis development: nonhuman primate models. Horm. Behav. 2006, 50:623-631.
46. Schwarz J.M., Nugent B.M., McCarthy M.M. Developmental and hormone-induced epigenetic changes to estrogen and progesterone receptor genes in brain are dynamic across the life span. Endocrinology 2010, 151:4871-4881.
47. Shahbazian M.D., Antalffy B., Armstrong D.L., Zoghbi H.Y. Insight into rett syndrome: Mecp2 levels display tissue- and cell-specific differences and correlate with neuronal maturation. Hum. Mol. Genet. 2002, 11:115-124.
48. Sharma R.P., Grayson D.R., Gavin D.P. Histone deactylase 1 expression is increased in the prefrontal cortex of schizophrenia subjects: analysis of the national brain databank microarray collection. Schizophr. Res. 2008, 98:111-117.
49. Shulha H.P., Cheung I., Guo Y., Akbarian S., Weng Z. Coordinated cell type-specific epigenetic remodeling in prefrontal cortex begins before birth and continues into early adulthood. PLoS Genet. 2013, 9:e1003433.
50. Siegmund K.D., Connor C.M., Campan M., Long T.I., Weisenberger D.J., Biniszkiewicz D., Jaenisch R., Laird P.W., Akbarian S. DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS ONE 2007, 2:e895.
51. Simmons R.K., Howard J.L., Simpson D.N., Akil H., Clinton S.M. DNA methylation in the developing hippocampus and amygdala of anxiety-prone versus risk-taking rats. Dev. Neurosci. 2012, 34:58-67.
52. Spinelli S., Chefer S., Suomi S.J., Higley J., Barr C.S., Stein E. Early-life stress induces long-term morphologic changes in primate brain. Arch. Gen. Psychiatry 2009, 66:658-665.
53. Stearns N.A., Schaevitz L.R., Bowling H., Nag N., Berger U.V., Berger-Sweeney J. Behavioral and anatomical abnormalities in mecp2 mutant mice: a model for rett syndrome. Neuroscience 2007, 146:907-921.
54. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
55. Sultan F.A., Wang J., Tront J., Liebermann D.A., Sweatt J.D. Genetic deletion of gadd45b, a regulator of active DNA demethylation, enhances long-term memory and synaptic plasticity. J. Neurosci. 2012, 32:17059-17066.
56. Suri D., Veenit V., Sarkar A., Thiagarajan D., Kumar A., Nestler E.J., Galande S., Vaidya V.A. Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, bdnf expression, and cognition. Biol. Psychiatry 2013, 73:658-666.
57. Uchida S., Hara K., Kobayashi A., Funato H., Hobara T., Otsuki K., Yamagata H., McEwen B.S., Watanabe Y. Early life stress enhances behavioral vulnerability to stress through the activation of rest4-mediated gene transcription in the medial prefrontal cortex of rodents. J. Neurosci. 2010, 30:15007-15018.
58. Uchida S., Hara K., Kobayashi A., Otsuki K., Yamagata H., Hobara T., Suzuki T., Miyata N., Watanabe Y. Epigenetic status of gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron 2011, 69:359-372.
59. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
60. Xie L., Korkmaz K.S., Braun K., Bock J. Early life stress-induced histone acetylations correlate with activation of the synaptic plasticity genes arc and egr1 in the mouse hippocampus. J. Neurochem. 2013, 125:457-464.