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
80	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Multigenerational Effects	One of the most important and fascinating implications of epigenetic modifications is the potential…
81	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Multigenerational Effects	directly assessed in the offspring, numerous reports of behavioral and physical abnormalities have…
82	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Multigenerational Effects	Similarly, significant evidence supports that developmental stress can have consequences that are…
83	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Multigenerational Effects	to that of F1 males (Franklin et al., 2010). Multigenerational transmission of epigenetic marks have…
84	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Multigenerational Effects	alterations in maternal behavior due to the fitness of the offspring or mating patterns of the male…
85	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Therapeutic Strategies	The epigenome remains malleable throughout the lifespan; consequently, outcomes of developmental…
86	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Therapeutic Strategies	a methyl-rich diet had beneficial effects on pup mortality rates, prenatal growth, and rate of…
87	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Therapeutic Strategies	Aside from pharmacological manipulations, environmental manipulations have likewise been shown to…
88	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Therapeutic Strategies	Increased opportunity for social interaction is an important part of environmental enrichment…
89	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Therapeutic Strategies	Because of data showing that developmental alcohol and stress act through epigenetic pathways,…
90	Future Directions: Combining Stress and Alcohol Models and Assessment of Multigenerational Effects and Therapeutics — Therapeutic Strategies	through histone deacetylase (HDAC) inhibitors are a pharmacological avenue worth exploring. HDACs…
91	Conclusions	Epigenetics is a growing and promising scientific field. As our understanding of the mechanisms and…

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

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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	→