Epigenetic mechanisms in alcohol- and adversity-induced developmental origins of neurobehavioral functioning.

paper Cited Public

Authors: Boschen, K E; Keller, S M; Roth, T L; Klintsova, A Y
Year: 2018
Journal: Neurotoxicology and teratology
PMID: 29305195
DOI: 10.1016/j.ntt.2017.12.009
PMCID: PMC5856624

Figure 1

Overview of epigenetic modifications induced by prenatal alcohol exposure (PAE). The presence of permissive transcriptional marks, such as histone acetylation or trimethylation, results in transcription of DNA into mRNA and translation of mRNA into protein. Under control conditions, normal CNS, endocrine, and immune function take place. PAE can remove these pro-transcriptional marks or increase the presence of repressive transcriptional marks, such as DNA methylation. Methyl groups either directly disrupt the ability of transcription factors to bind to DNA or recruit other transcriptional repressor proteins (i.e. MeCP2), reducing gene expression. miRNAs act post-transcriptionally to prevent mRNA from being translated into protein. This is associated with increased cell death and oxidative stress, altered cell cycle progression, disrupted endocrine and hypothalamic–pituitary–adrenal (HPA) axis signaling, and behavioral and cognitive deficits.

Figure 2

In response to stress, activation of the HPA axis takes place. The paraventricular nucleus (PVN) of the hypothalamus releases corticotropin-releasing factor (CRF), which then prompts the pituitary to release adrenocorticotropic hormone (ACTH), ultimately resulting in the adrenal cortex releasing glucocorticoids (Cortisol, CORT). Glucocorticoids act on the hippocampus, which provides negative feedback turning off HPA axis activity. Developmental stress induces epigenetic changes that affect many genes involved in HPA axis regulation. Epigenetic changes result in altered HPA axis activity and in turn, help explain behavioral aberrations observed in animals with a history of developmental stress.

Figure 3

Epigenetic modifications represent an avenue through which adverse environmental conditions can affect generations beyond the animals that were directly exposed via intergenerational and transgenerational transmission. Epigenetic marks can be passed through the paternal germline (F0) following preconception exposure to stress or alcohol, resulting in physiological, behavioral, or altered levels of global methylation in the offspring (F1). Exposure of a fetus (via exposure of the F0 pregnant dam) or neonate (F1) to alcohol or stress affects not only the directly exposed animal but also the developing germline. Altered epigenetic marks can then be transmitted to animals that were never exposed to the stressor or alcohol in the F2 generation and beyond, resulting in changes to methylation associated with multiple genes and epigenetic regulators and persistent behavioral perturbations. AE: Alcohol exposure; ELS: Early life stress.

#	Section	Preview
40	Developmental Stress Exposure — Gestational stressors	Studies administering chronic, unpredictable stressors to pregnant dams have contributed to the…
41	Developmental Stress Exposure — Gestational stressors	variable maternal stress, offspring showed increased Bdnf exon IV methylation in the medial…
42	Developmental Stress Exposure — Gestational stressors	outcomes of stress exposure (Mychasiuk et al., 2011). While the reason underlying the impact of sex…
43	Developmental Stress Exposure — Gestational stressors	The intensity and duration of the prenatal stressor is another factor that mediates the long-term…
44	Developmental Stress Exposure — Maternal separation	Infant rodents are completely dependent on their mothers for survival during their first few weeks…
45	Developmental Stress Exposure — Maternal separation	in reduced Pomc expression in the hypothalamus, while increased expression of Dnmt1 was observed in…
46	Developmental Stress Exposure — Maternal separation	Maternal separation has been used as an animal model of depression, as exposure to early-life…
47	Developmental Stress Exposure — Maternal separation	Experiencing early-life stress can influence vulnerability to drug addiction in adulthood, and…
48	Developmental Stress Exposure — Maternal separation	individual to addiction (Anier et al., 2010). Another study determined that animals with a history…
49	Developmental Stress Exposure — Maternal separation	Consistent with cognitive deficits observed in human populations with a history of early-stress,…
50	Developmental Stress Exposure — Maternal separation	deficit was rescued by consuming a diet rich in the methyl-donor choline in periadolescence. Another…
51	Developmental Stress Exposure — Aversive Parental Care Including Maltreatment	Caregiver maltreatment, including neglect and abuse, is incurred by 10–15% of the population in…
52	Developmental Stress Exposure — Aversive Parental Care Including Maltreatment	litter is exposed to the maltreatment condition, 1/3 of the litter remains in the home cage with the…
53	Developmental Stress Exposure — Aversive Parental Care Including Maltreatment	The prefrontal cortex, a brain region implicated in the psychopathology of bipolar disorder and…
54	Developmental Stress Exposure — Aversive Parental Care Including Maltreatment	lysine 9/14 acetylation at the Bdnf exon IV promoter (Blaze et al., 2015). Alterations in both gene…
55	Developmental Stress Exposure — Aversive Parental Care Including Maltreatment	There is a dynamic nature to the epigenetic alterations we have observed across the lifespan. For…
56	Developmental Stress Exposure — Aversive Parental Care Including Maltreatment	Being subjected to abuse and/or neglect by the caregiver has likewise been linked with epigenetic…
57	Developmental Stress Exposure — Aversive Parental Care Including Maltreatment	Studies examining peripheral DNA methylation have also identified epigenetic signatures of childhood…
58	Developmental Stress Exposure — Aversive Parental Care Including Maltreatment	Data exist to support the notion that DNA methylation resulting from childhood maltreatment mediates…
59	Developmental Stress Exposure — Aversive Parental Care Including Maltreatment	to their methylation levels prior to treatment (Perroud et al., 2013). Further, single nucleotide…

Name	Type
5-hydroxymethylcytosine local	drug
5-methylcytosine local	drug
A2AR local	gene
ACTH	drug
addiction	phenotype
ADHD	phenotype
adiposity	phenotype
adolescent animals	cohort
adolescent female offspring local	cohort
adolescents	cohort
Adolescent socially enriched rats local	cohort
adult female rodents with maltreatment local	cohort
adult male rodents with maltreatment local	cohort
adult mice	cohort
Adult Outcomes local	phenotype
adult rats	cohort
adults with PTSD local	cohort
alcohol	phenotype
Alcohol-exposed embryos local	cohort
Alcohol-exposed rat pups local	cohort
Alcohol Exposure	phenotype
Alcohol-induced damage local	phenotype
Altered differentiation local	phenotype
altered passive stress coping local	phenotype
Altered social behavior local	phenotype
amygdala	anatomy
animal model of early-life stress local	cohort
animal model of FASD local	cohort
animal models	cohort
Animals exposed to low licking and grooming local	cohort
antidepressants	drug
Antioxidant local	drug
anxiety	phenotype
anxiety-like behavior	phenotype
apoptosis	phenotype
Apoptotic pathways local	phenotype
Arterial defects local	phenotype
autism	phenotype
aversive behaviors	phenotype
AVP	drug
Bax	gene
Bdnf	gene
Bdnf exon I local	variant
BDNF exon I local	gene
Bdnf exon I hypomethylation local	phenotype
BDNF exon IV local	gene
BDNF exon IX local	gene
behavioral abnormalities	phenotype
behavioral deficits	phenotype
Behavioral Interventions local	drug
behavior of offspring local	phenotype
behavior problems	phenotype
bipolar disorder	phenotype
Birthweight local	phenotype
BMI	phenotype
Body mass index (BMI)	phenotype
bone growth delay local	phenotype
borderline personality disorder	phenotype
Both sexes local	cohort
brain	anatomy
Brain and behavioral development local	phenotype
brain damage	phenotype
brain development	phenotype
Buccal cells local	cohort
Canadian children with FASD local	cohort
cardiovascular disease	phenotype
caregiver maltreatment local	phenotype
Caregiver maltreatment local	phenotype
Caspase-3	gene
cell cycle genes	gene
Cell cycle length local	phenotype
cell proliferation	phenotype
central obesity	phenotype
cerebellum	anatomy
choline	drug
citalopram	drug
clinical depression	phenotype
clozapine	drug
Clustered protocadherin genes local	gene
Cnr1	gene
CNS function local	phenotype
cocaine	phenotype
cognition	phenotype
Cognitive and behavioral impairments local	phenotype
Cognitive and behavioral outcomes local	phenotype
cognitive development	phenotype
congenital heart disease	phenotype
Cord blood mononuclear cells local	cohort
cortex	anatomy
cortical dysfunction local	phenotype
corticosterone	drug
cortisol	drug
cortisol response	phenotype
Craniofacial malformations local	phenotype
CREBBP	gene
CRF	drug
CRFR1 local	gene
CRHR2	gene
CTCF	gene
Cyclin family genes local	gene
Dam local	cohort
Dams local	cohort
Decreased H3K9 acetylation local	phenotype
decreased social interaction local	phenotype
DECREASED_SOCIAL_INTERACTION local	phenotype
delayed embryonic growth local	phenotype
Delayed motor maturity local	phenotype
Delayed orientation local	phenotype
Dendritic morphology local	phenotype
dentate gyrus	anatomy
depression	phenotype
depressive behavior	phenotype
depressive-like phenotype	phenotype
Developmental alcohol-exposed rats local	cohort
developmental delay	phenotype
developmental disorders	phenotype
developmental stress	phenotype
Developmental stress local	drug
Developmental Stress Exposure local	phenotype
DICER1	gene
digit malformations	phenotype
Disturbed development of offspring local	phenotype
DNA methylation	drug
DNA methyltransferase	drug
DNMT1	gene
Dnmt3a	gene
Dnmt3b	gene
DNMT3L local	gene
DNMTs	gene
dorsal hippocampus	anatomy
drug dependence	phenotype
drug-seeking behavior	phenotype
Dutch Hunger Winter local	cohort
early-stress local	phenotype
Early stress exposure local	drug
EHMT2 local	gene
Enhanced corticosterone response local	phenotype
environmental factors	drug
environmental influences	phenotype
epigenetic marks local	phenotype
Epigenetic modifications	phenotype
epigenetic regulators local	drug
Epigenetic Regulatory Molecules local	drug
epigenome local	drug
Epigenome local	phenotype
epigenome of offspring local	phenotype
escitalopram	drug
ESR1	gene
estrogen	drug
ethanol consumption	phenotype
executive functioning	phenotype
exploratory behavior	phenotype
Eye malformations local	phenotype
F1 females local	cohort
F1 males local	cohort
F2 females local	cohort
F2 males local	cohort
F3 generation local	cohort
F3 males local	cohort
famine exposure local	phenotype
FASD local	cohort
female adolescent rodents with maltreatment local	cohort
female children with FASD local	cohort
Female children with FASD local	cohort
female pups local	cohort
female rats	cohort
female rats prenatally exposed to alcohol local	cohort
female subjects	cohort
Fetal alcohol effects	phenotype
Fetal Alcohol Spectrum Disorder	phenotype
Fetal alcohol spectrum disorders	phenotype
fetal alcohol syndrome	phenotype
Fetal cortex local	anatomy
Fetal coupling local	phenotype
Fetal rat local	cohort
Fkbp5	gene
frontal cortex	anatomy
future stress exposure local	phenotype
GAD1	gene
GADD45B local	gene
germline transmission local	phenotype
Gestational day 7 alcohol exposure local	cohort
Gestational days 7–21 alcohol exposure local	cohort
Gestational Stress local	phenotype
global DNA methylation local	phenotype
Global methylation local	phenotype
glucocorticoid	drug
Glucocorticoid receptor (GR) local	drug
glucocorticoids	drug
GR-associated epigenetic marks local	phenotype
growth restriction local	phenotype
growth retardation	phenotype
H19 local	gene
H3K27me3	drug
H3K4me3	drug
Hdac1	gene
HDAC inhibitors	drug
HDACs	gene
Heart defects local	phenotype
Heart malformations local	phenotype
Hedonic behavior local	phenotype
higher basal corticosterone local	phenotype
High LG local	phenotype
High prenatal stress local	phenotype
Hippocampal dendritic complexity local	phenotype
hippocampus	anatomy
histone	drug
Histone 3 acetylation local	drug
Histone 3 lysine 4 trimethylation local	drug
Histone 3 lysine 9/14 acetylation local	drug
histone acetylation	drug
histone deacetylase inhibitor local	drug
Histone H3 local	drug
histone methylation local	drug
Histone trimethylation local	drug
Hormonal regulation local	phenotype
HPA axis	anatomy
HPA axis activation local	phenotype
HPA Axis Regulation local	phenotype
HSD11B2	gene
humans	cohort
Hydroxymethylation local	phenotype
hyperactive stress response local	phenotype
Hypermethylation of cyclin genes local	phenotype
Hypoactivity local	phenotype
hypothalamus	anatomy
Ice Storm local	cohort
IGF2	gene
Immobility (forced swim test) local	phenotype
Impaired behavioral performance local	phenotype
impaired motor coordination learning local	phenotype
Impaired response speed local	phenotype
impulsivity	phenotype
increased avoidance behavior local	phenotype
increased BDNF exon IV methylation local	phenotype
increased corticosterone response local	phenotype
increased CRFR1 expression local	phenotype
increased immobility local	phenotype
Increased methylation local	phenotype
Increased plasma corticosterone local	phenotype
individuals with borderline personality disorder local	cohort
Individuals with psychiatric illnesses local	cohort
infant caregiver experience local	phenotype
Infant rodents local	cohort
infants	cohort
infection local	drug
intimate partner violence	phenotype
intubation stress local	drug
Ki67	drug
learning and memory	phenotype
LEARNING_AND_MEMORY_DEFICITS local	phenotype
Limited nesting resources local	phenotype
Lipid peroxidase local	drug
lipopolysaccharide	drug
locomotor activity	phenotype
locomotor hyperactivity	phenotype
LOCOMOTOR_HYPERACTIVITY local	phenotype
Locomotor sensitization to cocaine local	phenotype
long-term potentiation	phenotype
low birth weight	phenotype
Lower birth weight local	phenotype
low LG local	phenotype
Low LG local	phenotype
Low licking and grooming local	phenotype
lysine 9/14 acetylation local	drug
male adult rats local	cohort
male children with FASD local	cohort
Male children with FASD local	cohort
male mating patterns local	phenotype
male pups local	cohort
male rat local	cohort
Male rat local	cohort
male rats	cohort
male rats prenatally exposed to alcohol local	cohort
male subjects	cohort
maltreated animals local	cohort
maternal attachment local	phenotype
maternal behavior	phenotype
maternal care	phenotype
Maternal maltreatment local	phenotype
Maternal resource deprivation local	phenotype
maternal separation local	cohort
maternal separation	phenotype
Maternal separation local	cohort
Maternal stress local	phenotype
MeCP2	gene
medial prefrontal cortex	anatomy
memory	phenotype
Mental dysfunction later in life local	phenotype
methamphetamine	drug
Methamphetamine self-administration local	phenotype
methyl-rich diet local	drug
Methyl-rich diet local	drug
mice	cohort
Mice prenatally exposed to alcohol local	cohort
microRNA	drug
Mild prenatal stress local	phenotype
Mineralocorticoid receptor local	drug
miR-103 local	gene
miR-103 local	variant
miR-140-3p local	variant
miR-151 local	gene
miR-151 local	variant
miR-153 local	variant
miR-20a local	gene
miR-20a local	variant
miR-21 local	variant
miR-30 local	variant
miR-335 local	variant
miR-9	drug
miR-9 local	gene
miRNA	drug
miRNA expression	phenotype
miRNAs	drug
mixed-litter local	cohort
MKI67	gene
monkeys	cohort
mood disorders	phenotype
Mother's cognitive appraisal local	drug
motor coordination	phenotype
Mouse embryonic fibroblasts local	cohort
Mouse model of FASD	cohort
MPOA local	anatomy
Multigenerational Effects of Alcohol and Stress local	phenotype
negative symptoms	phenotype
neglect	phenotype
Neural Development Genes local	gene
neural patterning	phenotype
neural stem cells	cohort
neural tube defects	phenotype
Neurodegenerative processes local	phenotype
neurodevelopment	phenotype
neurodevelopmental disorder	phenotype
neurogenesis	phenotype
neurological disorders	phenotype
neuronal differentiation	phenotype
neuroplasticity deficits local	phenotype
neuropsychiatric disorders	phenotype
newborn birthweight local	phenotype
newborn male offspring local	cohort
non-coding RNAs local	variant
non-exposed siblings local	cohort
Notch	gene
novel object and place recognition local	phenotype
NPY	gene
Nr3c1	gene
NR3C1 1B splice variant local	variant
NR3C1 1C splice variant local	variant
NR3C1 1F exon promoter local	variant
NR3C1 1H splice variant local	variant
NR3C1 methylation local	phenotype
nucleus accumbens	anatomy
nucleus accumbens core	anatomy
Nutritional Interventions local	drug
offspring	cohort
offspring fitness local	phenotype
One-carbon metabolism local	drug
OPRM1	cohort
Overactive corticosterone response to LPS local	phenotype
oxidative stress	phenotype
OXTR	gene
oxytocin	drug
Oxytocin binding local	phenotype
P7 alcohol exposure local	cohort
PAE local	drug
PAE adult rats local	cohort
paraventricular nucleus (PVN)	anatomy
Paternal alcohol exposure local	phenotype
paternal stress local	phenotype
PD7 local	cohort
perinatal alcohol exposure rats local	cohort
Perinatal exposure local	cohort
peripheral blood samples local	cohort
Pharmacological Interventions local	drug
Physical abnormalities local	phenotype
physical abuse	phenotype
Physical dysmorphologies local	phenotype
pituitary gland	anatomy
Pomc	gene
POMC hypermethylation local	phenotype
population	cohort
positive symptoms	phenotype
Postnatal alcohol exposure local	cohort
postnatal brain	anatomy
Postnatal day 21 (PD21) local	phenotype
postnatal stress local	phenotype
Postnatal Stress local	phenotype
postnatal stress (maltreatment) local	phenotype
posttranslational histone modifications local	drug
posttraumatic stress disorder	phenotype
Post-Traumatic Stress Disorder	phenotype
PP1	gene
preconception stress local	phenotype
predator odor local	drug
prefrontal cortex	anatomy
pregnant women	cohort
Prenatal alcohol-exposed rodents local	cohort
prenatal alcohol exposure	phenotype
prenatal chronic variable stress local	phenotype
prenatal growth local	phenotype
Prenatal growth local	phenotype
Prenatally stressed animals local	cohort
prenatally stressed fetus local	phenotype
prenatal stress	phenotype
Prenatal stress local	drug
prenatal stress (rodent model) local	cohort
protein oxidation	phenotype
Protocadherin genes local	gene
psychiatric disorders	phenotype
psychopathology	phenotype
Pup mortality local	phenotype
pup mortality rates local	phenotype
pup responsiveness local	phenotype
Pups local	cohort
PVN	anatomy
Quebec ice storm cohort local	cohort
RASGRF1	gene
rats	cohort
reactive oxygen species	drug
reduced BDNF expression local	phenotype
Reduced birth weight local	phenotype
Reduced differentiation potential local	phenotype
reduced fetal coupling local	phenotype
Reduced GR expression local	phenotype
reduced H3 acetylation local	phenotype
Reduced Pomc mRNA local	phenotype
reduced tail chasing behavior local	phenotype
reduced telomere length local	phenotype
Reduced transcription factor binding local	phenotype
Reln	gene
ribosomal RNA gene local	gene
ribosomal RNA gene promoter local	variant
Risk of incarceration local	phenotype
rodents	cohort
rs1360780	variant
schizophrenia	phenotype
SCHIZOPHRENIA_LIKE_PHENOTYPE local	phenotype
second-hit local	drug
Second trimester local	cohort
severe maltreatment local	phenotype
sex	phenotype
Sex-dependent effects local	phenotype
single-sex litter local	cohort
Slc17a6	gene
SLC6A4	gene
smaller embryos local	phenotype
social approach	phenotype
SOCIAL_APPROACH local	phenotype
social functioning	phenotype
spatial memory	phenotype
sperm miRNA local	drug
Stem cell population local	cohort
stress	phenotype
Stress during pregnancy local	phenotype
stress exposure	phenotype
stressful life events	phenotype
Stress hyporesponsive period local	phenotype
stress-induced pathology local	phenotype
stressor local	drug
Stress-related pathology local	phenotype
stress response	phenotype
striatal dysfunction local	phenotype
striatum	anatomy
substance abuse	phenotype
substance use	phenotype
suicide	phenotype
suicide completers with abuse history local	cohort
suicide completers without abuse history local	cohort
suicide victims local	phenotype
suicide victims with childhood abuse history local	cohort
suicide victims without childhood abuse history local	cohort
tail chasing behavior local	phenotype
telomere length	phenotype
teratogen local	drug
teratogens local	drug
Tet1	gene
TET family local	gene
Third trimester local	cohort
Third trimester-equivalent alcohol exposure local	cohort
Three month old infants local	cohort
Toxic stress local	drug
Toxic stress exposure local	phenotype
Tutsi genocide cohort local	cohort
Umbilical cord leukocytes local	cohort
US population	cohort
Valproic acid	drug
VALPROIC_ACID local	drug
variable maternal stress local	phenotype
vasopressin	drug
ventral hippocampus	anatomy
Ventricular defects local	phenotype
vertebral and digit malformations local	phenotype
Vertebral malformations local	phenotype
vGLUT2	gene
War-exposed mothers local	cohort
whole brain	anatomy
Whole embryo culture paradigm local	cohort
whole prefrontal cortex local	anatomy
zebularine local	drug

Citation	PMID	DOI	Status
2015, Fetal Alcohol Exposure Fact Sheet	—	—	—
2017, Fetal Alcohol Spectrum Disorders (FASDs)	—	—	—
Abel, EL et al., Alcoholism: Clinical and Experimental Research, 1988, Paternal alcohol exposure affects offspring behavior but not body or organ weights in mice	3044161	10.1111/j.1530-0277.1988.tb00205.x	Cited
Abel, T et al., Current Opinion in Pharmacology, 2008, Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders	18206423	10.1016/j.coph.2007.12.002	Cited
Adriani, W et al., Behavioural Pharmacology, 2004, Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model	15343057	10.1097/00008877-200409000-00005	Cited
Agid, O et al., Molecular Psychiatry, 1999, Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia	10208448	10.1038/sj.mp.4000473	Cited
Aihara, M et al., Psychiatry Research: Neuroimaging, 2007, HPA axis dysfunction in unmedicated major depressive disorder and its normalization by pharmacotherapy correlates with alteration of neural activity in prefrontal cortex and limbic/paralimbic regions	17587554	10.1016/j.pscychresns.2006.11.002	Cited
Alberry, B et al., Behavioural Brain Research, 2016, Developmental and behavioral consequences of early life maternal separation stress in a mouse model of fetal alcohol spectrum disorder	27102339	10.1016/j.bbr.2016.04.031	Cited
Albuquerque Filho, MO et al., Neuroscience, 2017, Dual influences of early-life maternal deprivation on histone deacetylase activity and recognition memory in rats	28089578	10.1016/j.neuroscience.2016.12.054	Cited
Amann, LC et al., Brain Research Bulletin, 2010, Mouse behavioral endophenotypes for schizophrenia	20433908	10.1016/j.brainresbull.2010.04.008	Cited
Anier, K et al., European Neuropsychopharmacology, 2014, Maternal separation is associated with DNA methylation and behavioural changes in adult rats	23972903	10.1016/j.euroneuro.2013.07.012	Cited
Anier, K et al., Neuropsychopharmacology, 2010, DNA methylation regulates cocaine-induced behavioral sensitization in mice	20720536	10.1038/npp.2010.128	Cited
Auger, AP et al., Hormones and Behavior, 2011, Epigenetic organization of brain sex differences and juvenile social play behavior	20619265	10.1016/j.yhbeh.2010.06.017	Cited
Baker, J et al., Cell, 1993, Role of insulin-like growth factors in embryonic and postnatal growth	8402902	—	Cited
Balaraman, S et al., Alcoholism: Clinical and Experimental Research, 2012, Opposing actions of ethanol and nicotine on microRNAs are mediated by nicotinic acetylcholine receptors in fetal cerebral cortical–derived neural progenitor cells	22458409	10.1111/j.1530-0277.2012.01793.x	Cited
Balaraman, S et al., Alcoholism: Clinical and Experimental Research, 2014, Maternal and neonatal plasma microRNA biomarkers for fetal alcohol exposure in an ovine model	24588274	10.1111/acer.12378	Cited
Beach, SR et al., American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 2010, Methylation at SLC6A4 is linked to family history of child abuse: an examination of the Iowa Adoptee sample	19739105	10.1002/ajmg.b.31028	Cited
Bekdash, RA et al., Alcoholism: Clinical and Experimental Research, 2013, Gestational Choline Supplementation Normalized Fetal Alcohol-Induced Alterations in Histone Modifications, DNA Methylation, and Proopiomelanocortin (POMC) Gene Expression in β-Endorphin-Producing POMC Neurons of the Hypothalamus	23413810	10.1111/acer.12082	Cited
Benoit, JD et al., Behavioural Brain Research, 2015, Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression	25496779	10.1016/j.bbr.2014.12.001	Cited
Berman, RF et al., Alcohol, 1996, Prenatal alcohol exposure and the effects of environmental enrichment on hippocampal dendritic spine density	8814658	10.1016/0741-8329(95)02049-7	Cited
Bertrand, J, Research in Developmental Disabilities, 2009, Interventions for children with fetal alcohol spectrum disorders (FASDs): overview of findings for five innovative research projects	19327965	10.1016/j.ridd.2009.02.003	Cited
Bielawski, DM et al., Alcohol, 1997, Acute treatment of paternal alcohol exposure produces malformations in offspring	9209556	10.1016/s0741-8329(97)87951-7	Cited
Bielawski, DM et al., Alcoholism: Clinical and Experimental Research, 2002, Paternal alcohol exposure affects sperm cytosine methyltransferase messenger RNA levels	11923587	—	Cited
Blair, R, Philosophical Transactions of the Royal Society of London B: Biological Sciences, 2008, The amygdala and ventromedial prefrontal cortex: functional contributions and dysfunction in psychopathy	18434283	10.1098/rstb.2008.0027	Cited
Blaze, J et al., Development and Psychopathology, 2017, Caregiver maltreatment causes altered neuronal DNA methylation in female rodents	28401839	10.1017/S0954579417000128	Cited
Blaze, J et al., Developmental Neuroscience, 2013, Differential methylation of genes in the medial prefrontal cortex of developing and adult rats following exposure to maltreatment or nurturing care during infancy	23751776	10.1159/000350716	Cited
Blaze, J et al., International Journal of Developmental Neuroscience, 2013, Exposure to caregiver maltreatment alters expression levels of epigenetic regulators in the medial prefrontal cortex	24120634	10.1016/j.ijdevneu.2013.10.001	Cited
Blaze, J et al., International Journal of Developmental Neuroscience, 2017, Intrauterine exposure to maternal stress alters Bdnf IV DNA methylation and telomere length in the brain of adult rat offspring	28330827	10.1016/j.ijdevneu.2017.03.007	Cited
Blaze, J et al., Stress, 2015, Long-term effects of early-life caregiving experiences on brain-derived neurotrophic factor histone acetylation in the adult rat mPFC	26305287	10.3109/10253890.2015.1071790	Cited
Boehme, F et al., European Journal of Neuroscience, 2011, Voluntary exercise induces adult hippocampal neurogenesis and BDNF expression in a rodent model of fetal alcohol spectrum disorders	21535455	10.1111/j.1460-9568.2011.07676.x	Cited
Boschen, K et al., Developmental Neurobiology, 2016, Impact of exercise and a complex environment on hippocampal dendritic morphology, Bdnf gene expression, and DNA methylation in male rat pups neonatally exposed to alcohol	27597545	10.1002/dneu.22448	Cited
Boschen, K et al., International Journal of Developmental Neuroscience, 2015, Effects of developmental alcohol exposure vs. intubation stress on BDNF and TrkB expression in the hippocampus and frontal cortex of neonatal rats	25805052	10.1016/j.ijdevneu.2015.03.008	Cited
Boschen, K et al., Vitamins and Hormones, 2017, Chapter Nine-Neurotrophins in the Brain: Interaction With Alcohol Exposure During Development	28215296	10.1016/bs.vh.2016.10.008	Cited
Boschen, KE et al., Alcohol, 2014, Activity and social behavior in a complex environment in rats neonatally exposed to alcohol	25150044	10.1016/j.alcohol.2014.07.005	Cited
Bourc'his, D et al., Science, 2001, Dnmt3L and the establishment of maternal genomic imprints	11719692	10.1126/science.1065848	Cited
Braithwaite, E et al., Epigenetics, 2015, Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation	25875334	10.1080/15592294.2015.1039221	Cited
Brocardo, PS et al., Neuropharmacology, 2012, Anxiety-and depression-like behaviors are accompanied by an increase in oxidative stress in a rat model of fetal alcohol spectrum disorders: Protective effects of voluntary physical exercise	22019722	10.1016/j.neuropharm.2011.10.006	Cited
Brown, AS et al., The British Journal of Psychiatry, 1995, Increased risk of affective disorders in males after second trimester prenatal exposure to the Dutch hunger winter of 1944–45	7620744	10.1192/bjp.166.5.601	Cited
Burd, L et al., Congenital Heart Disease, 2007, Congenital heart defects and fetal alcohol spectrum disorders	18377476	10.1111/j.1747-0803.2007.00105.x	Cited
Caldji, C et al., Proceedings of the National Academy of Sciences, 1998, Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat	9560276	10.1073/pnas.95.9.5335	Cited
Caldwell, KK et al., Pharmacology, Biochemistry and Behavior, 2008, Fetal alcohol spectrum disorder-associated depression: evidence for reductions in the levels of brain-derived neurotrophic factor in a mouse model	18558427	10.1016/j.pbb.2008.05.004	Cited
Cao-Lei, L et al., Early Human Development, 2016, Pregnant women's cognitive appraisal of a natural disaster affects their children's BMI and central adiposity via DNA methylation: Project Ice Storm	27718477	10.1016/j.earlhumdev.2016.09.013	Cited
Cao-Lei, L et al., Translational Psychiatry, 2015, Pregnant women’s cognitive appraisal of a natural disaster affects DNA methylation in their children 13 years later: Project Ice Storm	25710121	10.1038/tp.2015.13	Cited
Chai, XJ et al., Neuropsychopharmacology, 2011, Abnormal medial prefrontal cortex resting-state connectivity in bipolar disorder and schizophrenia	21654735	10.1038/npp.2011.88	Cited
Champagne, F et al., Proceedings of the National Academy of Sciences, 2001, Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors	11606726	10.1073/pnas.221224598	Cited
Champagne, FA et al., Behavioral Neuroscience, 2007, Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty	18085888	10.1037/0735-7044.121.6.1353	Cited
Champagne, FA et al., Endocrinology, 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	16513834	10.1210/en.2005-1119	Cited
Chater-Diehl, EJ et al., PloS One, 2016, Alteration of gene expression, DNA methylation, and histone methylation in free radical scavenging networks in adult mouse hippocampus following fetal alcohol exposure	27136348	10.1371/journal.pone.0154836	Cited
Chen, Y et al., PloS One, 2013, DNA methylation program in developing hippocampus and its alteration by alcohol	23544149	10.1371/journal.pone.0060503	Cited
Clayton, JA et al., Nature, 2014, NIH to balance sex in cell and animal studies	24834516	10.1038/509282a	Cited
Cohen, MM et al., Proceedings of the National Academy of Sciences, 2013, Early-life stress has persistent effects on amygdala function and development in mice and humans	24145410	10.1073/pnas.1310163110	Cited
Connor, PD et al., Developmental Neuropsychology, 2000, Direct and indirect effects of prenatal alcohol damage on executive function	11385829	10.1207/S1532694204Connor	Cited
Cornish, JL et al., Journal of Neuroscience, 2000, Glutamate transmission in the nucleus accumbens mediates relapse in cocaine addiction	10899176	10.1523/JNEUROSCI.20-15-j0006.2000	Cited
Costello, EJ et al., Archives of General Psychiatry, 2003, Prevalence and development of psychiatric disorders in childhood and adolescence	12912767	10.1001/archpsyc.60.8.837	Cited
Dasmahapatra, AK et al., Toxicology & Pharmacology, 2016, Modulation of DNA methylation machineries in Japanese rice fish (Oryzias latipes) embryogenesis by ethanol and 5-azacytidine. Comparative Biochemistry and Physiology Part C	26510680	10.1016/j.cbpc.2015.10.011	Cited
Devlin, AM et al., PLoS One, 2010, Prenatal exposure to maternal depressed mood and the MTHFR C677T variant affect SLC6A4 methylation in infants at birth	20808944	10.1371/journal.pone.0012201	Cited
DiPietro, JA, Journal of Adolescent Health, 2012, Maternal stress in pregnancy: considerations for fetal development	22794531	10.1016/j.jadohealth.2012.04.008	Cited
Doherty, TS et al., Behavioural Brain Research, 2016, Global and gene-specific DNA methylation alterations in the adolescent amygdala and hippocampus in an animal model of caregiver maltreatment	26027495	10.1016/j.bbr.2015.05.028	Cited
Dong, E et al., Biological Psychiatry, 2015, Brain-derived neurotrophic factor epigenetic modifications associated with schizophrenia-like phenotype induced by prenatal stress in mice	25444166	10.1016/j.biopsych.2014.08.012	Cited
Dong, E et al., Translational Psychiatry, 2012, Upregulation of TET1 and downregulation of APOBEC3A and APOBEC3C in the parietal cortex of psychotic patients	22948384	10.1038/tp.2012.86	Cited
Downing, C et al., Alcohol, 2011, Subtle decreases in DNA methylation and gene expression at the mouse Igf2 locus following prenatal alcohol exposure: effects of a methyl-supplemented diet	20705422	10.1016/j.alcohol.2010.07.006	Cited
Drevets, WC et al., Nature, 1997, Subgenual prefrontal cortex abnormalities in mood disorders	9126739	10.1038/386824a0	Cited
Driscoll, CD et al., Neurotoxicology and teratology, 1990, Prenatal alcohol exposure: comparability of effects in humans and animal models	2196422	10.1016/0892-0362(90)90094-s	Cited
Dunn, GA et al., Endocrinology, 2011, Maternal high-fat diet effects on third-generation female body size via the paternal lineage	21447631	10.1210/en.2010-1461	Cited
Enoch, M-A, Psychopharmacology, 2011, The role of early life stress as a predictor for alcohol and drug dependence	20596857	10.1007/s00213-010-1916-6	Cited
Essex, MJ et al., Development and Psychopathology, 2011, Influence of early life stress on later hypothalamic–pituitary–adrenal axis functioning and its covariation with mental health symptoms: a study of the allostatic process from childhood into adolescence	22018080	10.1017/S0954579411000484	Cited
Farber, NB et al., Neurobiology of Disease, 2010, Alcohol-induced neuroapoptosis in the fetal macaque brain	20580929	10.1016/j.nbd.2010.05.025	Cited
Feng, M-J et al., Brain Research, 2005, Effects of prenatal alcohol exposure on brain-derived neurotrophic factor and its receptor tyrosine kinase B in offspring	15854584	10.1016/j.brainres.2005.02.017	Cited
Fenoglio, KA et al., Frontiers in Neuroendocrinology, 2006, Hippocampal neuroplasticity induced by early-life stress: functional and molecular aspects	16603235	10.1016/j.yfrne.2006.02.001	Cited
Fleming, AS et al., Physiology & Behavior, 1983, Lesions of the medial preoptic area prevent the facilitation of maternal behavior produced by amygdala lesions	6657771	10.1016/0031-9384(83)90073-2	Cited
Fleming, AS et al., Psychoneuroendocrinology, 1994, Neuropsychology of maternal behavior in the rat: c-fos expression during mother-litter interactions	7938344	10.1016/0306-4530(94)90030-2	Cited
Franklin, L et al., American Journal of Occupational Therapy, 2008, Children with fetal alcohol spectrum disorders: problem behaviors and sensory processing	18557002	10.5014/ajot.62.3.265	Cited
Franklin, TB et al., Biological Psychiatry, 2010, Epigenetic transmission of the impact of early stress across generations	20673872	10.1016/j.biopsych.2010.05.036	Cited
Garro, AJ et al., Alcoholism: Clinical and Experimental Research, 1991, Ethanol consumption inhibits fetal DNA methylation in mice: implications for the fetal alcohol syndrome	1877725	10.1111/j.1530-0277.1991.tb00536.x	Cited
Gavin, DP et al., Neuropsychopharmacology, 2012, Growth arrest and DNA-damage-inducible, beta (GADD45b)-mediated DNA demethylation in major psychosis	22048458	10.1038/npp.2011.221	Cited
Gee, DG et al., Neurobiology of Stress, 2015, The impact of developmental timing for stress and recovery	25798454	10.1016/j.ynstr.2015.02.001	Cited
Gil-Mohapel, J et al., Brain Research Reviews, 2010, Hippocampal cell loss and neurogenesis after fetal alcohol exposure: insights from different rodent models	20471420	10.1016/j.brainresrev.2010.04.011	Cited
Gilbert, R et al., The Lancet, 2009, Burden and consequences of child maltreatment in high-income countries	19056114	10.1016/S0140-6736(08)61706-7	Cited
Gonzales, ML et al., Current Psychiatry Reports, 2010, The role of MeCP2 in brain development and neurodevelopmental disorders	20425298	10.1007/s11920-010-0097-7	Cited
Govorko, D et al., Biological Psychiatry, 2012, Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations	22622000	10.1016/j.biopsych.2012.04.006	Cited
Gregório, SP et al., Psychiatry Research, 2009, Polymorphisms in genes involved in neurodevelopment may be associated with altered brain morphology in schizophrenia: preliminary evidence	19054571	10.1016/j.psychres.2007.08.011	Cited
Grunstein, M, Nature, 1997, Histone acetylation in chromatin structure and transcription	9311776	10.1038/38664	Cited
Guan, J-S et al., Experimental Neurology, 2015, The role of epigenetic regulation in learning and memory	24837316	10.1016/j.expneurol.2014.05.006	Cited
Guibert, S et al., Current Topics in Developmental Biology, 2013, Functions of DNA methylation and hydroxymethylation in mammalian development	23587238	10.1016/B978-0-12-416027-9.00002-4	Cited
Guidotti, A et al., Archives of General Psychiatry, 2000, Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study	11074872	10.1001/archpsyc.57.11.1061	Cited
Guidotti, A et al., Psychopharmacology, 2005, GABAergic dysfunction in schizophrenia: new treatment strategies on the horizon	15864560	10.1007/s00213-005-2212-8	Cited
Guo, W et al., PloS One, 2011, Alcohol exposure decreases CREB binding protein expression and histone acetylation in the developing cerebellum	21655322	10.1371/journal.pone.0019351	Cited
Guo, Y et al., Alcoholism, Clinical and Experimental Research, 2012, Chronic intermittent ethanol exposure and its removal induce a different miRNA expression pattern in primary cortical neuronal cultures	22141737	10.1111/j.1530-0277.2011.01689.x	Cited
Gómez-Pinilla, F et al., Journal of Neurophysiology, 2002, Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity	12424260	10.1152/jn.00152.2002	Cited
Hamilton, G et al., Brain Research, 2011, Neonatal alcohol exposure disrupts hippocampal neurogenesis and contextual fear conditioning in adult rats	21816390	10.1016/j.brainres.2011.07.027	Cited
Hamilton, GF et al., Alcoholism: Clinical and Experimental Research, 2012, Housing in environmental complexity following wheel running augments survival of newly generated hippocampal neurons in a rat model of binge alcohol exposure during the third trimester equivalent	22324755	10.1111/j.1530-0277.2011.01726.x	Cited
Hamilton, GF et al., Synapse, 2010, Postnatal binge-like alcohol exposure decreases dendritic complexity while increasing the density of mature spines in mPFC Layer II/III pyramidal neurons	19771589	10.1002/syn.20711	Cited
Hamilton, GF et al., Synapse, 2015, Voluntary exercise partially reverses neonatal alcohol-induced deficits in mPFC layer II/III dendritic morphology of male adolescent rats	25967699	10.1002/syn.21827	Cited
Hanna, EZ et al., Journal of Substance Abuse, 1994, The motivational correlates of drinking, smoking, and illicit drug use during pregnancy	7804015	10.1016/s0899-3289(94)90181-3	Cited
Hao, Y et al., Frontiers in Psychiatry, 2011, Litter gender composition and sex affect maternal behavior and DNA methylation levels of the oprm1 gene in rat offspring	21629839	10.3389/fpsyt.2011.00021	Cited
Hariri, AR et al., Trends in Cognitive Sciences, 2006, Genetics of emotional regulation: the role of the serotonin transporter in neural function	16530463	10.1016/j.tics.2006.02.011	Cited
Hata, K et al., Development, 2002, Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice	11934864	10.1242/dev.129.8.1983	Cited
Haycock, PC et al., Biology of Reproduction, 2009, Exposure of mouse embryos to ethanol during preimplantation development: effect on DNA methylation in the h19 imprinting control region	19279321	10.1095/biolreprod.108.074682	Cited
He, L et al., Genetics, 2004, MicroRNAs: small RNAs with a big role in gene regulation. Nature reviews	15211354	10.1038/nrg1379	Cited
Heaton, MB et al., Developmental Brain Research, 2000, Ethanol-induced alterations in the expression of neurotrophic factors in the developing rat central nervous system	10837897	10.1016/s0165-3806(00)00032-8	Cited
Heaton, MB et al., Developmental Brain Research, 2003, Effects of ethanol on neurotrophic factors, apoptosis-related proteins, endogenous antioxidants, and reactive oxygen species in neonatal striatum: relationship to periods of vulnerability	12586429	10.1016/s0165-3806(02)00610-7	Cited
Heijmans, BT et al., Proceedings of the National Academy of Sciences, 2008, Persistent epigenetic differences associated with prenatal exposure to famine in humans	18955703	10.1073/pnas.0806560105	Cited
Helfer, JL et al., Brain Research, 2009, The effects of exercise on adolescent hippocampal neurogenesis in a rat model of binge alcohol exposure during the brain growth spurt	19647724	10.1016/j.brainres.2009.07.090	Cited
Hellemans, KG et al., Annals of the New York Academy of Sciences, 2008, Prenatal alcohol exposure increases vulnerability to stress and anxiety-like disorders in adulthood	19076375	10.1196/annals.1418.016	Cited
Hellemans, KG et al., Neuroscience & Biobehavioral Reviews, 2010, Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders	19545588	10.1016/j.neubiorev.2009.06.004	Cited
Herman, J et al., Brazilian Journal of Medical and Biological Research, 2012, Neural regulation of the stress response: glucocorticoid feedback mechanisms	22450375	10.1590/S0100-879X2012007500041	Cited
Herman, LE et al., Canadian Journal of Clinical Pharmacology, 2008, Gender and attention deficits in children diagnosed with a Fetal Alcohol Spectrum Disorder	18953085	—	Cited
Hicks, SD et al., Journal of Neurochemistry, 2010, Ethanol-induced methylation of cell cycle genes in neural stem cells	20626555	10.1111/j.1471-4159.2010.06886.x	Cited
Hill, KT et al., Behavioural Brain Research, 2014, The influence of infant-caregiver experiences on amygdala Bdnf, OXTr, and NPY expression in developing and adult male and female rats	25011012	10.1016/j.bbr.2014.07.001	Cited
Hirabayashi, T et al., Protocadherins in neurological diseases, Cell Adhesion Molecules, 2014	25300142	10.1007/978-1-4614-8090-7_13	Cited
Holmes, MR, Journal of Child Psychology and Psychiatry, 2013, The sleeper effect of intimate partner violence exposure: long-term consequences on young children's aggressive behavior	23550816	10.1111/jcpp.12071	Cited
Hompes, T et al., Journal of Psychiatric Research, 2013, Investigating the influence of maternal cortisol and emotional state during pregnancy on the DNA methylation status of the glucocorticoid receptor gene (NR3C1) promoter region in cord blood	23566423	10.1016/j.jpsychires.2013.03.009	Cited
Hunsberger, JG et al., Neuromolecular Medicine, 2009, MicroRNAs in mental health: from biological underpinnings to potential therapies	19544012	10.1007/s12017-009-8070-5	Cited
Ignacio, C et al., Frontiers in Pediatrics, 2014, Effects of Acute Prenatal Exposure to Ethanol on microRNA Expression are Ameliorated by Social Enrichment	25309888	10.3389/fped.2014.00103	Cited
Ignácio, ZM et al., Behavioural Brain r=Research, 2017, Quetiapine treatment reverses depressive-like behavior and reduces DNA methyltransferase activity induced by maternal deprivation	27913254	10.1016/j.bbr.2016.11.044	Cited
Ikonomidou, C et al., Science, 2000, Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome	10669420	10.1126/science.287.5455.1056	Cited
Irner, TB et al., Journal of Addictive Diseases, 2012, Cognitive and social development in preschool children born to women using substances	22356667	10.1080/10550887.2011.642766	Cited
Jenuwein, T et al., Science, 2001, Translating the histone code	11498575	10.1126/science.1063127	Cited
Jindal, RD et al., Schizophrenia Research, 2010, Decreased BDNF in patients with antipsychotic naive first episode schizophrenia	20096541	10.1016/j.schres.2009.12.035	Cited
Johnston, MV, Developmental Disabilities Research Reviews, 2009, Plasticity in the developing brain: implications for rehabilitation	19489084	10.1002/ddrr.64	Cited
Jones, PA et al., Science, 2001, The role of DNA methylation in mammalian epigenetics	11498573	10.1126/science.1063852	Cited
Jud, A et al., Child and Adolescent Psychiatry and Mental Health, 2016, On the incidence and prevalence of child maltreatment: a research agenda	27303442	10.1186/s13034-016-0105-8	Cited
Kember, R et al., Brain and Behavior, 2012, Maternal separation is associated with strain-specific responses to stress and epigenetic alterations to Nr3c1, Avp, and Nr4a1 in mouse	22950049	10.1002/brb3.69	Cited
Kendall-Tackett, K, Child Abuse & Neglect, 2002, The health effects of childhood abuse: four pathways by which abuse can influence health	12201164	10.1016/s0145-2134(02)00343-5	Cited
Kessler, RC et al., Psychological Medicine, 1997, Childhood adversity and adult psychiatric disorder in the US National Comorbidity Survey	9300515	10.1017/s0033291797005588	Cited
Kim, CK et al., Alcoholism: Clinical and Experimental Research, 1999, Effects of prenatal exposure to alcohol on the release of adenocorticotropic hormone, corticosterone, and proinflammatory cytokines	10029203	—	Cited
Kim, HJ et al., Journal of Pharmacology and Experimental Therapeutics, 2007, Histone deacetylase inhibitors exhibit anti-inflammatory and neuroprotective effects in a rat permanent ischemic model of stroke: multiple mechanisms of action	17371805	10.1124/jpet.107.120188	Cited
Kim, P et al., Neurochemical Research, 2013, Effects of ethanol exposure during early pregnancy in hyperactive, inattentive and impulsive behaviors and MeCP2 expression in rodent offspring	23283698	10.1007/s11064-012-0960-5	Cited
Kim, T-W et al., Journal of Exercise Rehabilitation, 2015, Postnatal treadmill exercise attenuates prenatal stress-induced apoptosis through enhancing serotonin expression in aged-offspring rats	25830139	10.12965/jer.150180	Cited
Klengel, T et al., Nature Neuroscience, 2013, Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions	23201972	10.1038/nn.3275	Cited
Klengel, T et al., Neuropsychopharmacology, 2016, Models of intergenerational and transgenerational transmission of risk for psychopathology in mice	26283147	10.1038/npp.2015.249	Cited
Klintsova, AY et al., Alcoholism: Clinical and Experimental Research, 2007, Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure	17949464	10.1111/j.1530-0277.2007.00528.x	Cited
Knezovich, JG et al., Frontiers in Genetics, 2012, The effect of preconception paternal alcohol exposure on epigenetic remodeling of the h19 and rasgrf1 imprinting control regions in mouse offspring	22371710	10.3389/fgene.2012.00010	Cited
Kolb, B et al., Cognitive Development, 2017, Stress and prefrontal cortical plasticity in the developing brain	—	—	—
Kosten, TA et al., Developmental Psychobiology, 2014, Sex and litter effects on anxiety and DNA methylation levels of stress and neurotrophin genes in adolescent rats	23460384	10.1002/dev.21106	Cited
Kundakovic, M et al., Genes, 2017, The Epigenetic link between prenatal adverse environments and neurodevelopmental disorders	28335457	10.3390/genes8030104	Cited
Labonte, B et al., Biological Psychiatry, 2012, Differential glucocorticoid receptor exon 1 B, 1 C, 1 H expression and methylation in suicide completers with a history of childhood abuse	22444201	10.1016/j.biopsych.2012.01.034	Cited
Ladd-Acosta, C et al., Molecular Psychiatry, 2014, Common DNA methylation alterations in multiple brain regions in autism	23999529	10.1038/mp.2013.114	Cited
Laird, PW, Nature Reviews Cancer, 2003, The power and the promise of DNA methylation markers	12671664	10.1038/nrc1045	Cited
Langley, B et al., Current Drug Targets-CNS and Neurological Disorders, 2005, Remodeling chromatin and stress resistance in the central nervous system: histone deacetylase inhibitors as novel and broadly effective neuroprotective agents	15723612	10.2174/1568007053005091	Cited
Laufer, BI et al., 2015, Associative DNA methylation changes in children with prenatal alcohol exposure	26178076	10.2217/epi.15.60	Cited
Laufer, BI et al., Alcohol, 2017, Long-term alterations to DNA methylation as a biomarker of prenatal alcohol exposure: From mouse models to human children with fetal alcohol spectrum disorders	28187949	10.1016/j.alcohol.2016.11.009	Cited
Laufer, BI et al., Disease Models & Mechanisms, 2013, Long-lasting alterations to DNA methylation and ncRNAs could underlie the effects of fetal alcohol exposure in mice	23580197	10.1242/dmm.010975	Cited
Ledig, M et al., Neuropharmacology, 1998, Paternal alcohol exposure: developmental and behavioral effects on the offspring of rats	9680259	10.1016/s0028-3908(97)00185-8	Cited
Levine, S, Annals of the New York Academy of Sciences, 1994, The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors	7825883	10.1111/j.1749-6632.1994.tb39245.x	Cited
Lewis, CR et al., Behavioural Pharmacology, 2014, Early life stress interactions with the epigenome: potential mechanisms driving vulnerability towards psychiatric illness	25003947	10.1097/FBP.0000000000000057	Cited
Lewis, CR et al., Frontiers in Psychiatry, 2013, The effects of maternal separation on adult methamphetamine self-administration, extinction, reinstatement, and MeCP2 immunoreactivity in the nucleus accumbens	23785337	10.3389/fpsyt.2013.00055	Cited
Liu, Y et al., Epigenetics, 2009, Alcohol exposure alters DNA methylation profiles in mouse embryos at early neurulation	20009564	10.4161/epi.4.7.9925	Cited
Liyanage, VRB et al., Experimental Neurology, 2015, Ethanol deregulates Mecp2/MeCP2 in differentiating neural stem cells via interplay between 5-methylcytosine and 5-hydroxymethylcytosine at the Mecp2 regulatory elements	25620416	10.1016/j.expneurol.2015.01.006	Cited
Lopez, J et al., Molecular Psychiatry, 2013, Epigenetic regulation of BDNF expression according to antidepressant response	22547115	10.1038/mp.2012.38	Cited
Luo, J et al., Alcoholism: Clinical and Experimental Research, 1999, Ethanol Induces Cell Death and Cell Cycle Delay in Cultures of Pheochromocytoma PC12 Cells	10235300	—	Cited
Luo, J et al., Brain Research Reviews, 1998, Growth factor-mediated neural proliferation: target of ethanol toxicity. Brain research	9622617	10.1016/s0165-0173(98)00009-5	Cited
Lupien, SJ et al., Neuroscience, 2009, Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews	19401723	10.1038/nrn2639	Cited
Marino, M et al., Current Genomics, 2006, Estrogen signaling multiple pathways to impact gene transcription	18369406	10.2174/138920206779315737	Cited
Matrisciano, F et al., Neuropharmacology, 2013, Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice	22564440	10.1016/j.neuropharm.2012.04.013	Cited
Mattson, SN et al., Alcoholism: Clinical and Experimental Research, 1999, Executive functioning in children with heavy prenatal alcohol exposure	10591598	—	Cited
McGowan, PO et al., Development and Psychopathology, 2015, Epigenetic pathways through which experiences become linked with biology	25997776	10.1017/S0954579415000206	Cited
McGowan, PO et al., Nature Neuroscience, 2009, Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse	19234457	10.1038/nn.2270	Cited
McGowan, PO et al., PLoS One, 2008, Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain	18461137	10.1371/journal.pone.0002085	Cited
McGowan, PO et al., PLoS One, 2011, Broad epigenetic signature of maternal care in the brain of adult rats	21386994	10.1371/journal.pone.0014739	Cited
Meaney, MJ et al., Dialogues in Clinical Neuroscience, 2005, Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome	16262207	10.31887/DCNS.2005.7.2/mmeaney	Cited
Meaney, MJ et al., Nature Neuroscience, 2010, Epigenetic regulation of the neural transcriptome: the meaning of the marks	20975754	10.1038/nn1110-1313	Cited
Mehta, D et al., Proceedings of the National Academy of Sciences, 2013, Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder	23630272	10.1073/pnas.1217750110	Cited
Mercer, TR et al., Genetics, 2009, Long non-coding RNAs: insights into functions. Nature reviews	19188922	10.1038/nrg2521	Cited
Middleton, FA et al., Developmental Neuroscience, 2012, Molecular substrates of social avoidance seen following prenatal ethanol exposure and its reversal by social enrichment	22572756	10.1159/000337858	Cited
Miller, BH et al., Brain Research, 2010, MicroRNA dysregulation in psychiatric disease	20303342	10.1016/j.brainres.2010.03.035	Cited
Monk, C et al., American Journal of Psychiatry, 2016, Distress during pregnancy: epigenetic regulation of placenta glucocorticoid-related genes and fetal neurobehavior	27013342	10.1176/appi.ajp.2015.15091171	Cited
Monk, M et al., Development, 1987, Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development	3653008	10.1242/dev.99.3.371	Cited
Mooney, SM et al., Behavioural Brain Research, 2011, Acute prenatal exposure to ethanol and social behavior: effects of age, sex, and timing of exposure	20728475	10.1016/j.bbr.2010.08.014	Cited
Moore, CL et al., Developmental Psychobiology, 1986, Behavioral responses of infant rats to maternal licking: variations with age and sex	3758488	10.1002/dev.420190504	Cited
Moore, CL et al., Journal of Comparative and Physiological Psychology, 1979, Mother rats interact differently with male and female offspring	479402	10.1037/h0077599	Cited
Moore, CL, Developmental Psychobiology, 1984, Maternal contributions to the development of masculine sexual behavior in laboratory rats	6745497	10.1002/dev.420170403	Cited
Moore, CL, Journal of Comparative Psychology, 1985, Sex differences in urinary odors produced by young laboratory rats (Rattus norvegicus)	4042618	—	Cited
Moreau, MP et al., Biological Psychiatry, 2011, Altered microRNA expression profiles in postmortem brain samples from individuals with schizophrenia and bipolar disorder	21183010	10.1016/j.biopsych.2010.09.039	Cited
Moreno Gudiño, H et al., Nutritional Neuroscience, 2017, Dietary choline during periadolescence attenuates cognitive damage caused by neonatal maternal separation in male rats	26714620	10.1080/1028415X.2015.1126444	Cited
Mueller, BR et al., Journal of Neuroscience, 2008, Sex-specific programming of offspring emotionality after stress early in pregnancy	18768700	10.1523/JNEUROSCI.1424-08.2008	Cited
Mukhopadhyay, P et al., Reproductive Toxicology, 2013, Alcohol modulates expression of DNA methyltranferases and methyl CpG-/CpG domain-binding proteins in murine embryonic fibroblasts	23395981	10.1016/j.reprotox.2013.01.003	Cited
Mulligan, C et al., Epigenetics, 2012, Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight	22810058	10.4161/epi.21180	Cited
Murgatroyd, C et al., Nature Neuroscience, 2009, Dynamic DNA methylation programs persistent adverse effects of early-life stress	19898468	10.1038/nn.2436	Cited
Mychasiuk, R et al., Neuroscience, 2011, Intensity matters: brain, behaviour and the epigenome of prenatally stressed rats	21335068	10.1016/j.neuroscience.2011.02.026	Cited
Mychasiuk, R et al., Neuroscience, 2013, Paternal stress prior to conception alters DNA methylation and behaviour of developing rat offspring	23531434	10.1016/j.neuroscience.2013.03.025	Cited
Nagarajan, R et al., Epigenetics, 2006, Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation	17486179	10.4161/epi.1.4.3514	Cited
Nagre, NN et al., Journal of Neurochemistry, 2015, CB1-receptor knockout neonatal mice are protected against ethanol-induced impairments of DNMT1, DNMT3A, and DNA methylation	25487288	10.1111/jnc.13006	Cited
Neumann, ID et al., Trends in Neurosciences, 2012, Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors	22974560	10.1016/j.tins.2012.08.004	Cited
Ngai, YF et al., American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 2015, Prenatal alcohol exposure alters methyl metabolism and programs serotonin transporter and glucocorticoid receptor expression in brain	26180184	10.1152/ajpregu.00075.2015	Cited
Nugent, BM et al., Nature Neuroscience, 2015, Brain feminization requires active repression of masculinization via DNA methylation	25821913	10.1038/nn.3988	Cited
Numan, M et al., Journal of Comparative and Physiological Psychology, 1977, Medial preoptic area and onset of maternal behavior in the rat	402400	10.1037/h0077304	Cited
Numan, M, Parenting, 2012, Maternal behavior: neural circuits, stimulus valence, and motivational processes	—	—	—
O'connor, MJ et al., Developmental Disabilities Research Reviews, 2009, Psychiatric conditions associated with prenatal alcohol exposure	19731386	10.1002/ddrr.74	Cited
Oberlander, TF et al., Epigenetics, 2008, Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses	18536531	10.4161/epi.3.2.6034	Cited
Okano, M et al., Cell, 1999, DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development	10555141	10.1016/s0092-8674(00)81656-6	Cited
Olney, JW et al., Brain Pathology, 2002, Drug-induced apoptotic neurodegeneration in the developing brain	12408236	10.1111/j.1750-3639.2002.tb00467.x	Cited
Otero, NK et al., Alcoholism: Clinical and Experimental Research, 2012, Choline supplementation and DNA methylation in the hippocampus and prefrontal cortex of rats exposed to alcohol during development	22509990	10.1111/j.1530-0277.2012.01784.x	Cited
Painter, RC et al., Reproductive Toxicology, 2005, Prenatal exposure to the Dutch famine and disease in later life: an overview	15893910	10.1016/j.reprotox.2005.04.005	Cited
Palacios-García, I et al., PLoS One, 2015, Prenatal stress down-regulates Reelin expression by methylation of its promoter and induces adult behavioral impairments in rats	25679528	10.1371/journal.pone.0117680	Cited
Pappalardo-Carter, DL et al., Alcoholism: Clinical and Experimental Research, 2013, Suppression and Epigenetic Regulation of MiR-9 Contributes to Ethanol Teratology: Evidence from Zebrafish and Murine Fetal Neural Stem Cell Models	23800254	10.1111/acer.12139	Cited
Park, SW et al., Neuroscience Letters, 2017, Epigenetic modification of glucocorticoid receptor promoter I 7 in maternally separated and restraint-stressed rats	28414132	10.1016/j.neulet.2017.04.024	Cited
Pedersen, CA et al., Behavioral Neuroscience, 1994, Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas	7893408	10.1037//0735-7044.108.6.1163	Cited
Pena, CJ et al., PloS One, 2012, Epigenetic effects of prenatal stress on 11 betahydroxysteroid dehydrogenase-2 in the placenta and fetal brain	22761903	10.1371/journal.pone.0039791	Cited
Perkins, A et al., International Journal of Developmental Neuroscience, 2013, Alcohol exposure during development: Impact on the epigenome	23542005	10.1016/j.ijdevneu.2013.03.010	Cited
Perroud, N et al., Translational Psychiatry, 2011, Increased methylation of glucocorticoid receptor gene (NR3C1) in adults with a history of childhood maltreatment: a link with the severity and type of trauma	22832351	10.1038/tp.2011.60	Cited
Perroud, N et al., Translational Psychiatry, 2013, Response to psychotherapy in borderline personality disorder and methylation status of the BDNF gene	23422958	10.1038/tp.2012.140	Cited
Perroud, N et al., World Journal of Biological Psychiatry, 2014, The Tutsi genocide and transgenerational transmission of maternal stress: epigenetics and biology of the HPA axis	24690014	10.3109/15622975.2013.866693	Cited
Petkov, VV et al., Biulleten' eksperimental'noi biologii i meditsiny, 1992, Lipid peroxidation changes in the brain in fetal alcohol syndrome	1421268	—	Cited
Peña, CJ et al., Endocrinology, 2013, Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats	24002038	10.1210/en.2013-1595	Cited
Pietrzykowski, AZ et al., Neuron, 2008, Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol	18667155	10.1016/j.neuron.2008.05.032	Cited
Portales-Casamar, E et al., Epigenetics & Chromatin, 2016, DNA methylation signature of human fetal alcohol spectrum disorder	27358653	10.1186/s13072-016-0074-4	Cited
Ptak, C et al., Dialogues in Clinical Neuroscience, 2010, Epigenetic approaches to psychiatric disorders	20373664	10.31887/DCNS.2010.12.1/cptak	Cited
Puglia, MP et al., Alcohol, 2010, Repeated third trimester-equivalent ethanol exposure inhibits long-term potentiation in the hippocampal CA1 region of neonatal rats	20488644	10.1016/j.alcohol.2010.03.001	Cited
Radtke, KM et al., Translational Psychiatry, 2011, Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor	22832523	10.1038/tp.2011.21	Cited
Rakic, S et al., European Journal of Neuroscience, 2000, Programmed cell death in the developing human telencephalon	10971615	10.1046/j.1460-9568.2000.00153.x	Cited
Ramachandran, V et al., Journal of Neuroscience Research, 2003, Ethanol-induced oxidative stress precedes mitochondrially mediated apoptotic death of cultured fetal cortical neurons	14598302	10.1002/jnr.10767	Cited
Rando, OJ, Cell, 2012, Daddy issues: paternal effects on phenotype	23141533	10.1016/j.cell.2012.10.020	Cited
Rasmussen, C et al., Journal of population therapeutics and clinical pharmacology, 2010, Executive functioning and working memory deficits on the CANTAB among children with prenatal alcohol exposure	21289378	—	Cited
Rasmussen, C et al., Journal of Special Education, 2011, The relation between mathematics and working memory in young children with fetal alcohol spectrum disorders	—	—	—
Redila, V et al., Neuroscience, 2006, Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus	16338077	10.1016/j.neuroscience.2005.10.050	Cited
Ridder, S et al., Journal of Neuroscience, 2005, Mice with genetically altered glucocorticoid receptor expression show altered sensitivity for stress-induced depressive reactions	15987954	10.1523/JNEUROSCI.0736-05.2005	Cited
Rodgers, AB et al., Journal of Neuroscience, 2013, Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation	23699511	10.1523/JNEUROSCI.0914-13.2013	Cited
Rodgers, AB et al., Proceedings of the National Academy of Sciences, 2015, Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress	26483456	10.1073/pnas.1508347112	Cited
Roth, TL et al., Biochimica et Biophysica Acta (BBA)-General Subjects, Epigenetic mechanisms in schizophrenia	19559755	10.1016/j.bbagen.2009.06.009	Cited
Roth, TL et al., Biological Psychiatry, Lasting epigenetic influence of early-life adversity on the BDNF gene	19150054	10.1016/j.biopsych.2008.11.028	Cited
Roth, TL et al., Developmental Psychobiology, 2014, Bdnf DNA methylation modifications in the hippocampus and amygdala of male and female rats exposed to different caregiving environments outside the homecage	24752649	10.1002/dev.21218	Cited
Roth, TL et al., Essays in Biochemistry, 2010, Epigenetic regulation of genes in learning and memory	20822498	10.1042/bse0480263	Cited
Roth, TL et al., Hormones and Behavior, 2011, Epigenetic marking of the BDNF gene by early-life adverse experiences	20483357	10.1016/j.yhbeh.2010.05.005	Cited
Roth, TL, Development and Psychopathology, 2013, Epigenetic mechanisms in the development of behavior: Advances, challenges, and future promises of a new field	24342840	10.1017/S0954579413000618	Cited
Roth, TL, Developmental Psychobiology, 2012, Epigenetics of neurobiology and behavior during development and adulthood	22714649	10.1002/dev.20550	Cited
Roy, A et al., Neuropsychopharmacology, 2007, Interaction between childhood trauma and serotonin transporter gene variation in suicide	17356577	10.1038/sj.npp.1301331	Cited
Ruzicka, W et al., Molecular Psychiatry, 2007, Selective epigenetic alteration of layer I GABAergic neurons isolated from prefrontal cortex of schizophrenia patients using laser-assisted microdissection	17264840	10.1038/sj.mp.4001954	Cited
Sathyan, P et al., Journal of Neuroscience, 2007, Competing interactions between micro-RNAs determine neural progenitor survival and proliferation after ethanol exposure: evidence from an ex vivo model of the fetal cerebral cortical neuroepithelium	17687032	10.1523/JNEUROSCI.1269-07.2007	Cited
Schenkel, LS et al., Schizophrenia Research, 2005, Histories of childhood maltreatment in schizophrenia: relationships with premorbid functioning, symptomatology, and cognitive deficits	15949659	10.1016/j.schres.2005.03.003	Cited
Schmidt, MV et al., Psychopharmacology, 2011, Early life stress paradigms in rodents: potential animal models of depression?	21086114	10.1007/s00213-010-2096-0	Cited
Schneider, ML et al., Child Development, 1997, Moderate alcohol consumption and psychological stress during pregnancy induce attention and neuromotor impairments in primate infants	29106730	10.1111/j.1467-8624.1997.tb01959.x	Cited
Schneider, ML et al., Prenatal stress influences on neurobehavior, stress reactivity, and dopaminergic function in rhesus macaques, Primate Models of Children’s Health and Developmental Disabilities, 2008	—	—	—
Seo, MK et al., Neuropharmacology, 2016, Early life stress increases stress vulnerability through BDNF gene epigenetic changes in the rat hippocampus	26877199	10.1016/j.neuropharm.2016.02.009	Cited
Shea, A et al., Psychoneuroendocrinology, 2005, Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females	15471614	10.1016/j.psyneuen.2004.07.001	Cited
Silberman, DM et al., Pharmacological Research, 2016, Long-term effects of early life stress exposure: role of epigenetic mechanisms	26774789	10.1016/j.phrs.2015.12.033	Cited
Skagerstróm, J et al., Journal of Women's Health, 2011, Predictors of drinking during pregnancy: a systematic review	21671775	10.1089/jwh.2010.2216	Cited
Soares, AR et al., Toxicological Sciences, 2012, Ethanol exposure induces up-regulation of specific microRNAs in zebrafish embryos	22298809	10.1093/toxsci/kfs068	Cited
St-Cyr, S et al., Frontiers in Behavioral Neuroscience, 2015, Programming of stress-related behavior and epigenetic neural gene regulation in mice offspring through maternal exposure to predator odor	26082698	10.3389/fnbeh.2015.00145	Cited
Steinhausen, HC et al., Alcoholism: Clinical and Experimental Research, 1998, Long-term outcome of children with fetal alcohol syndrome: Psychopathology, behavior, and intelligence	9581637	10.1111/j.1530-0277.1998.tb03657.x	Cited
Stevens, SA et al., Journal of Population Therapeutics and Clinical Pharmacology, 2012, Social problem solving in children with fetal alcohol spectrum disorders	22535836	—	Cited
Streissguth, AP et al., Journal of Developmental & Behavioral Pediatrics, 2004, Risk factors for adverse life outcomes in fetal alcohol syndrome and fetal alcohol effects	15308923	10.1097/00004703-200408000-00002	Cited
Stringer, RL et al., Clinical Epigenetics, 2013, Reduced expression of brain cannabinoid receptor 1 (Cnr1) is coupled with an increased complementary micro-RNA (miR-26b) in a mouse model of fetal alcohol spectrum disorders	23915435	10.1186/1868-7083-5-14	Cited
Struhl, K, Genes & Development, 1998, Histone acetylation and transcriptional regulatory mechanisms	9499396	10.1101/gad.12.5.599	Cited
Subbanna, S et al., Neurobiology of Disease, 2013, G9a-mediated histone methylation regulates ethanol-induced neurodegeneration in the neonatal mouse brain	23396011	10.1016/j.nbd.2013.01.022	Cited
Subbanna, S et al., Neuroscience, 2014, Ethanol induced acetylation of histone at G9a exon1 and G9a-mediated histone H3 dimethylation leads to neurodegeneration in neonatal mice	24300108	10.1016/j.neuroscience.2013.11.043	Cited
Szulwach, KE et al., Nature Neuroscience, 2011, 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging	22037496	10.1038/nn.2959	Cited
Tal, TL et al., Faseb J, 2012, MicroRNAs control neurobehavioral development and function in zebrafish	22253472	10.1096/fj.11-194464	Cited
Thomas, JD et al., Behavioral Neuroscience, 2007, Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats	17324056	10.1037/0735-7044.121.1.120	Cited
Thomas, JD et al., Hippocampus, 2012, Choline supplementation mitigates trace, but not delay, eyeblink conditioning deficits in rats exposed to alcohol during development	21542051	10.1002/hipo.20925	Cited
Thomas, JD et al., Neurotoxicology and Teratology, 2004, Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats	15001212	10.1016/j.ntt.2003.10.002	Cited
Tobi, EW et al., Human Molecular Genetics, 2009, DNA methylation differences after exposure to prenatal famine are common and timing-and sex-specific	19656776	10.1093/hmg/ddp353	Cited
Todkar, A et al., Frontiers in Molecular Neuroscience, 2015, HPA axis gene expression and DNA methylation profiles in rats exposed to early life stress, adult voluntary ethanol drinking and single housing	26858597	10.3389/fnmol.2015.00090	Cited
Tsankova, N et al., Nature Reviews Neuroscience, 2007, Epigenetic regulation in psychiatric disorders	17453016	10.1038/nrn2132	Cited
Veazey, KJ et al., Epigenetics & Chromatin, 2015, Dose-dependent alcohol-induced alterations in chromatin structure persist beyond the window of exposure and correlate with fetal alcohol syndrome birth defects	26421061	10.1186/s13072-015-0031-7	Cited
Vetulani, J, Pharmacological Reports, 2013, Early maternal separation: a rodent model of depression and a prevailing human condition	24552992	10.1016/s1734-1140(13)71505-6	Cited
Vijayendran, M et al., Frontiers in Psychiatry, 2012, Effects of genotype and child abuse on DNA methylation and gene expression at the serotonin transporter	22707942	10.3389/fpsyt.2012.00055	Cited
Walker, C-D et al., Stress, 2017, Chronic early life stress induced by limited bedding and nesting (LBN) material in rodents: critical considerations of methodology, outcomes and translational potential	28617197	10.1080/10253890.2017.1343296	Cited
Wang, A et al., PLoS One, 2014, Epigenetic upregulation of corticotrophin-releasing hormone mediates postnatal maternal separation-induced memory deficiency	24718660	10.1371/journal.pone.0094394	Cited
Wang, L-L et al., Human Reproduction, 2009, Ethanol exposure induces differential microRNA and target gene expression and teratogenic effects which can be suppressed by folic acid supplementation	19091803	10.1093/humrep/den439	Cited
Ward, ID et al., BMC Pregnancy and Childbirth, 2013, Transgenerational programming of maternal behaviour by prenatal stress	23446000	10.1186/1471-2393-13-S1-S9	Cited
Watson, JB et al., Development and Psychopathology, 1999, Prenatal teratogens and the development of adult mental illness	10532619	10.1017/s0954579499002151	Cited
Wearick-Silva, LE et al., Developmental Psychobiology, 2017, Running during adolescence rescues a maternal separation-induced memory impairment in female mice: Potential role of differential exon-specific BDNF expression	27807856	10.1002/dev.21487	Cited
Weaver, IC et al., Journal of Neuroscience, 2005, Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life	16306417	10.1523/JNEUROSCI.3652-05.2005	Cited
Weaver, IC et al., Nature Neuroscience, 2004, Epigenetic programming by maternal behavior	15220929	10.1038/nn1276	Cited
Weinberg, J et al., Journal of Neuroendocrinology, 2008, Prenatal alcohol exposure: Foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome	18266938	10.1111/j.1365-2826.2008.01669.x	Cited
Weiss, EL et al., American Journal of Psychiatry, 1999, Childhood sexual abuse as a risk factor for depression in women: psychosocial and neurobiological correlates	10360118	10.1176/ajp.156.6.816	Cited
Whitcher, LT et al., Synapse, 2008, Postnatal binge-like alcohol exposure reduces spine density without affecting dendritic morphology in rat mPFC	18512209	10.1002/syn.20532	Cited
Whitelaw, E, Genome Biology, 2015, Disputing Lamarckian epigenetic inheritance in mammals	25853737	10.1186/s13059-015-0626-0	Cited
Wu, Y et al., Endocrinology, 2014, Early-life stress reduces DNA methylation of the Pomc gene in male mice	24506071	10.1210/en.2013-1868	Cited
Yali, AM et al., Journal of Psychosomatic Obstetrics and Gynaecology, 1999, Coping and distress in pregnancy: an investigation of medically high risk women	10212886	10.3109/01674829909075575	Cited
Yang, B-Z et al., American Journal of Preventive Medicine, 2013, Child abuse and epigenetic mechanisms of disease risk	23332324	10.1016/j.amepre.2012.10.012	Cited
Yang, J et al., PloS One, 2015, Prenatal alcohol exposure and congenital heart defects: a meta-analysis	26110619	10.1371/journal.pone.0130681	Cited
Yehuda, R et al., Biological Psychiatry, 1991, Hypothalamicpituitary-adrenal dysfunction in posttraumatic stress disorder	1661614	10.1016/0006-3223(91)90123-4	Cited
Yehuda, R et al., Biological Psychiatry, 1993, Glucocorticoid receptor number and cortisol excretion in mood, anxiety, and psychotic disorders	8373936	10.1016/0006-3223(93)90252-9	Cited
Zaidan, H et al., Biological Psychiatry, 2013, Prereproductive stress to female rats alters corticotropin releasing factor type 1 expression in ova and behavior and brain corticotropin releasing factor type 1 expression in offspring	23726318	10.1016/j.biopsych.2013.04.014	Cited
Zhang, CR et al., Epigenetics & chromatin, 2015, Prenatal ethanol exposure alters adult hippocampal VGLUT2 expression with concomitant changes in promoter DNA methylation, H3K4 trimethylation and miR-467b-5p levels	26421062	10.1186/s13072-015-0032-6	Cited
Zhang, S et al., The FASEB Journal, 2010, Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring	20371620	10.1096/fj.09-154294	Cited
Zhang, W et al., Toxicology Letters, 2014, Prenatal alcohol exposure causes the over-expression of DHAND and EHAND by increasing histone H3K14 acetylation in C57 BL/6 mice	24857828	10.1016/j.toxlet.2014.05.011	Cited
Zhou, FC et al., Birth Defects Research Part A: Clinical and Molecular Teratology, 2011, Cellular DNA methylation program during neurulation and its alteration by alcohol exposure	21630420	10.1002/bdra.20820	Cited
Zierhut, K et al., Psychiatry Research: Neuroimaging, 2010, The role of hippocampus dysfunction in deficient memory encoding and positive symptoms in schizophrenia	20702070	10.1016/j.pscychresns.2010.03.007	Cited
Zucchi, FC et al., PLoS One, 2013, Maternal stress induces epigenetic signatures of psychiatric and neurological diseases in the offspring	23451123	10.1371/journal.pone.0056967	Cited

In this knowledge base

Title	Year	PMID
Genetics of Alcohol Use Disorder: A Role for Induced Pluripotent Stem Cells?	2018	29897633

External

Title	Authors	Journal	Year	Link
Anxiety, Depression, and Emotional Dysregulation Following Prenatal Substance Exposure.	Diaz MR et al.	—	2026	→
Research progress of DNA methylation on the regulation of substance use disorders and the mechanisms.	Liu Y et al.	—	2025	→
DNA Methylation in Alcohol Use Disorder.	Zheng Q et al.	—	2023	→
Epigenetics and Neuroinflammation Associated With Neurodevelopmental Disorders: A Microglial Perspective.	Komada M et al.	—	2022	→
DNA methylation at GRIN2B partially mediates the association between prenatal bisphenol F exposure and cognitive functions in 7-year-old children in the SELMA study.	Engdahl E et al.	—	2021	→
Nutrition and cognition across the lifetime: an overview on epigenetic mechanisms.	Polverino A et al.	—	2021	→
Early Developmental Stress Affects Subsequent Gene Expression Response to an Acute Stress in Atlantic Salmon: An Approach for Creating Robust Fish for Aquaculture?	Robinson NA et al.	—	2019	→
Environmental stressors and alcoholism development: Focus on molecular targets and their epigenetic regulation.	Pucci M et al.	—	2019	→
How alcohol drinking affects our genes: an epigenetic point of view.	Ciafrè S et al.	—	2019	→
Recent advances in fetal alcohol spectrum disorder for mental health professionals.	Mela M et al.	—	2019	→
Genetics of Alcohol Use Disorder: A Role for Induced Pluripotent Stem Cells?	Prytkova I et al.	—	2018	→
Insights from epigenetic studies on human health and evolution.	Mulligan CJ	—	2018	→
Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms.	Yehuda R et al.	—	2018	→