Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome.
paper
Cited
Public
- Authors
- Meaney, Michael J; Szyf, Moshe
- Year
- 2005
- Journal
- Dialogues in clinical neuroscience
- PMID
- 16262207
- DOI
- 10.31887/DCNS.2005.7.2/mmeaney
- PMCID
- PMC3181727
Early experience permanently alters behavior and physiology. These effects are, in part, mediated by sustained alterations in gene expression in selected brain regions. The critical question concerns the mechanism of these environmental "programming" effects. We examine this issue with an animal model that studies the consequences of variations in mother-infant interactions on the development of individual differences in behavioral and endocrine responses to stress in adulthood. Increased levels of pup licking/grooming by rat mothers in the first week of life alter DNA structure at a glucocorticoid receptor gene promoter in the hippocampus of the offspring. Differences in the DNA methylation pattern between the offspring of high- and low-licking/grooming mothers emerge over the first week of life; they are reversed with cross-fostering; they persist into adulthood; and they are associated with altered histone acetylation and transcription factor (nerve growth factor-induced clone A [NGFIA]) binding to the glucocorticoid receptor promoter. DNA methylation alters glucocorticoid receptor expression through modifications of chromatin structure. Pharmacological reversal of the effects on chromatin structure completely eliminates the effects of maternal care on glucocorticoid receptor expression and hypothalamic-pituitary-adrenal (HPA) responses to stress, thus suggesting a causal relation between the maternally induced, epigenetic modification of the glucocorticoid receptor gene and the effects on stress responses in the offspring. These findings demonstrate that the structural modifications of the DNA can be established through environmental programming and that, in spite of the inherent stability of this epigenomic marker, it is dynamic and potentially reversible.
Lactating female Long-Evans rat nursing litter in arched-back posture while licking/grooming an individual pup.
Map of the noncoding exon 1 region of the glucocorticoid receptor (GR) gene cloned from rat hippocampus.83 The sequence of the critical exon 17 region is provided below, highlighting the NGFIA (nerve growth factor-induced clone A) consensus sequence. The 5' CpG site is differentially methylated as a function of maternal care. Reproduced from reference 83: McCormick JA, Lyons V, Jacobson MD, et al. 5' Heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: differential regulation of variant transcripts by early life events. Mol Endocrinol. 2000;14:506-517. Copyright Β© 2000. The Endocrine Society.
Nucleosome core particle: ribbon traces for the 146-bp DNA phosphodiester backbones (brown and turquoise) and eight histone protein chains.87 The configuration is maintained, in part, through electrostatic bonds between the positively charged histones and negatively charged DNA. The N-terminal histone 3 tail (in blue) is a major site for enzymatic modification. Acetylation of the lysine residues in proximity to the DNA neutralizes the histone charge and opens the configuration permitting transcription factor binding. Reproduced from reference 87: Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of nucelosome core particle at 2. 8 A resolution. Nature. 1997;389:251-260. CopyrightΒ© 1997. Nature Publishing Group.
| Name | Type |
|---|---|
| 32P-labelled synthetic oligonucleotide local | drug |
| 3' CpG site local | drug |
| 3' CpG site local | variant |
| 5' CpG dinucleotide local | drug |
| 5' CpG site local | variant |
| 5' CpG site methylation of NFIA consensus sequence in exon 17 NR3C1 promoter local | phenotype |
| 5-CT local | drug |
| 5' cytosine point mutation local | variant |
| 5-HT | drug |
| 5-HT1A receptor | drug |
| 5-HT7 receptor | drug |
| 5-HT7 receptor antagonist local | drug |
| 5-HT signaling local | drug |
| 8-bromo-cAMP local | drug |
| 8-bromocAMP local | drug |
| acetylated H3 local | drug |
| Acetylated H3 local | drug |
| acetylation | drug |
| ACTH | drug |
| active chromatin local | drug |
| Active demethylation local | phenotype |
| adenosine | drug |
| adenylyl cyclase | drug |
| Adult low-LG offspring local | cohort |
| adult offspring of high-LG mothers local | cohort |
| adult postmitotic tissues local | cohort |
| adverse childhood experiences | phenotype |
| Alternative exon 1 sequences local | variant |
| Amnion's Horn local | anatomy |
| amygdala | anatomy |
| Amygdala-locus ceruleus activity local | phenotype |
| anterior pituitary | anatomy |
| Anxiolytic response to acute benzodiazepine administration local | phenotype |
| basolateral amygdala | anatomy |
| B cell local | drug |
| behavioral and neuroendocrine responses to stress local | phenotype |
| behavioral responses to stress local | phenotype |
| behavioral response to stress local | phenotype |
| Behavioral response to stress local | phenotype |
| Behavioral sensitivity to acute benzodiazepine administration local | phenotype |
| behavioral stress response local | phenotype |
| benzodiazepines | drug |
| BIRC5 local | gene |
| BrdU | drug |
| BZ agonists local | drug |
| cAMP | drug |
| CBP | gene |
| central nucleus of amygdala local | anatomy |
| Central nucleus of amygdala local | anatomy |
| chromatin | drug |
| Contact time with pups local | phenotype |
| cortex | anatomy |
| corticosterone | drug |
| corticosterone response magnitude local | phenotype |
| CpG local | drug |
| CREB1 | gene |
| CREBBP | gene |
| CRF | drug |
| CRF mRNA local | gene |
| CRF receptor local | gene |
| CRH | gene |
| cytosine | drug |
| Dampened HPA response to stress local | phenotype |
| day-6 rat pups local | cohort |
| decreased CRF mRNA expression local | phenotype |
| decreased CRF receptor levels local | phenotype |
| decreased hypothalamic CRF mRNA expression local | phenotype |
| decreased startle response local | phenotype |
| defensive responses local | phenotype |
| demethylases local | gene |
| de novo methylation local | phenotype |
| dMBD2/3 local | gene |
| DNA | drug |
| DNA demethylase local | drug |
| DNA demethylation local | phenotype |
| DNA methylation | drug |
| DNA methylation pattern local | phenotype |
| DNA methyltransferase | drug |
| DNMTs | gene |
| DOI local | drug |
| Early life events local | phenotype |
| early maternal behavior local | phenotype |
| Egr1 | gene |
| endocrine responses to stress local | phenotype |
| endocrine response to stress local | phenotype |
| enhanced glucocorticoid negative-feedback sensitivity local | phenotype |
| environmental conditions local | drug |
| environmental programming local | phenotype |
| enzyme | drug |
| epigenomic changes local | drug |
| epigenomic modifications local | drug |
| Epstein-Barr virus | drug |
| ERBB2 local | gene |
| Exon 17 GR promoter local | variant |
| exon 17 NR3C1 promoter methylation local | phenotype |
| exon 17 promoter local | drug |
| Extracellular signals local | drug |
| fearful response to stress local | phenotype |
| fear under novelty local | phenotype |
| GABA | phenotype |
| GABAA/BZ receptor local | gene |
| GABAA/BZ receptor binding local | phenotype |
| GABAA receptor subunit expression local | phenotype |
| Gabra1 | gene |
| GABRA3 | gene |
| Gabra4 | gene |
| Gabrg1 | gene |
| Gabrg2 | gene |
| Gastric cancer | phenotype |
| gene | gene |
| gene expression | phenotype |
| gene function local | phenotype |
| gene silencing | phenotype |
| glucocorticoid receptor | gene |
| glucocorticoids | drug |
| greater burying of electrified probe local | phenotype |
| GR exon 17 mRNA variant local | variant |
| GR exon 17 promoter local | drug |
| GR exon 17 promoter hypomethylation local | phenotype |
| GR exon 17 splice variant local | variant |
| H3 acetylation local | phenotype |
| H8 local | drug |
| handling local | drug |
| handling local | phenotype |
| HATs | gene |
| HDAC inhibitors | drug |
| HDACs | gene |
| HEK293 local | drug |
| HEK293 cells | cohort |
| high-LG local | cohort |
| high-LG local | phenotype |
| High-LG local | cohort |
| High-LG cohort local | cohort |
| high-LG dams local | phenotype |
| High-LG group local | cohort |
| high-LG mothers local | cohort |
| High-LG mothers local | cohort |
| High-LG mothers local | phenotype |
| high-LG offspring local | cohort |
| High-LG offspring local | cohort |
| High-LG offspring local | phenotype |
| Hippocampal GR expression local | phenotype |
| hippocampal GR mRNA level local | phenotype |
| hippocampus | anatomy |
| histone | drug |
| histone acetylation | drug |
| histone acetyltransferase local | drug |
| histone acetyltransferase local | gene |
| Histone deacetylases local | drug |
| histone tail local | drug |
| HK2 local | gene |
| HOXA5 local | gene |
| HOXB5 | gene |
| HPA activity | phenotype |
| HPA responses local | phenotype |
| HPA responses to stress local | phenotype |
| HPA response to stress local | phenotype |
| HPA stress response local | phenotype |
| Htr7 | gene |
| hypothalamic CRF mRNA expression local | phenotype |
| hypothalamus | anatomy |
| IL-2 local | gene |
| increased exploration in novel environment local | phenotype |
| increased GABAA/BZ receptor levels local | phenotype |
| increased GR expression local | phenotype |
| Increased hippocampal GR expression local | phenotype |
| increased hippocampal GR mRNA expression local | phenotype |
| infant mice local | cohort |
| Intracellular second-messenger systems local | drug |
| Lactating female rats local | cohort |
| licking/grooming (LG) local | phenotype |
| Licking/Grooming (LG) local | phenotype |
| locus ceruleus | anatomy |
| low-LG local | cohort |
| low-LG local | phenotype |
| Low-LG local | cohort |
| Low-LG cohort local | cohort |
| Low-LG group local | cohort |
| low-LG mothers local | cohort |
| low-LG mothers local | phenotype |
| Low-LG mothers local | cohort |
| Low-LG mothers local | phenotype |
| low-LG offspring local | cohort |
| Low-LG offspring local | cohort |
| Low-LG offspring local | phenotype |
| luciferase | drug |
| luciferase reporter local | drug |
| lung cancer | phenotype |
| maintenance DNA methyltransferase local | drug |
| maternal behavior | phenotype |
| maternal care local | drug |
| maternal care | phenotype |
| maternal effects local | phenotype |
| maternal high LG local | phenotype |
| maternal LG local | phenotype |
| Maternal LG local | phenotype |
| maternal LG frequency local | phenotype |
| Maternal licking/grooming local | phenotype |
| Maternal licking/grooming (LG) local | phenotype |
| MBD2 local | gene |
| MeCP2 | gene |
| Metastatic breast cancer local | phenotype |
| methiothepin local | drug |
| methylated DNA binding protein local | gene |
| Methylated DNA binding proteins local | drug |
| methyl cytosines local | drug |
| mineralocorticoid receptor local | gene |
| Mineralocorticoid receptor local | gene |
| Myc | gene |
| Neonatal handling local | phenotype |
| Neonatal rats | cohort |
| neonates | cohort |
| neuroendocrine response to stress local | phenotype |
| neurons | phenotype |
| Newborn offspring of high-LG mothers local | cohort |
| Newborn offspring of low-LG mothers local | cohort |
| NFIA | gene |
| NGFIA response element local | drug |
| noradrenaline | drug |
| Nr3c1 | gene |
| NR3C1 exon 17 promoter local | gene |
| nucleosome | drug |
| Number of pups to weaning local | phenotype |
| offspring | cohort |
| offspring of high-LG mothers local | cohort |
| offspring of high-LG mothers fostered to low-LG dams local | cohort |
| offspring of low-LG mothers cross-fostered to high-LG dams local | cohort |
| ovarian cancer | phenotype |
| paraformaldehyde | drug |
| paraventricular nucleus | anatomy |
| paraventricular nucleus (PVN) | anatomy |
| parental care local | phenotype |
| Parental care local | phenotype |
| parental imprinting local | phenotype |
| phenotype | phenotype |
| phosphorylation | drug |
| Pindolol local | drug |
| PKA | drug |
| Plasma corticosterone level local | phenotype |
| PLAU local | gene |
| postnatal day-6 pups local | cohort |
| postnatal handling local | cohort |
| postnatal handling local | drug |
| Postnatal handling local | phenotype |
| prefrontal cortex | anatomy |
| pup LG frequency local | phenotype |
| Pup weaning weight local | phenotype |
| PVN | anatomy |
| Quipazine local | drug |
| Rat pup local | cohort |
| reduced plasma ACTH response local | phenotype |
| reduced plasma corticosterone response local | phenotype |
| Repressor complexes local | drug |
| response element local | drug |
| ribosylation local | drug |
| septum local | anatomy |
| serotonin | drug |
| shorter latency to eat in novel environment local | phenotype |
| single cytosine epimutation local | variant |
| sodium bisulfite | drug |
| Sp1 | gene |
| stable adult behavior local | phenotype |
| stress | phenotype |
| stress-induced illness local | phenotype |
| stressβinduced increase in noradrenaline local | phenotype |
| stress-reactive offspring local | phenotype |
| stress response | phenotype |
| stressβresponsive brain regions local | anatomy |
| TFMPP local | drug |
| transcription factor | drug |
| transcription factors | drug |
| Trichostatin A local | drug |
| TSA local | drug |
| Valproic acid | drug |
| weaning weight | phenotype |
| Y chromosome | drug |
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