The Epigenetic Link between Prenatal Adverse Environments and Neurodevelopmental Disorders
Abstract
:1. Prenatal Adversity and Neurodevelopmental Disorders
2. Epigenetic Mechanisms and Prenatal Programming of Brain Function
3. Experimental Evidence from Animal Studies
3.1. Maternal Stress
3.2. Maternal Toxicological Exposures
3.3. Maternal Immune Activation
3.4. Maternal Exposure to Drugs
3.4.1. Cannabis
3.4.2. Cocaine
3.4.3. Ethanol
4. Evidence from Human Studies
4.1. Dutch Famine Study
4.2. Prenatal Stress and Maternal Depression
4.3. Toxicological Exposures
5. Future Directions and Challenges
5.1. Dose and Developmental Window of Exposure
5.2. Sex-Specific Effects
5.3. Peripheral Biomarkers
5.4. Technological Advancements and Integrative Approaches
Acknowledgments
Conflicts of Interest
References
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Study | Species (Strain) | Stress Paradigm | Offspring Sex and Age | Brain Area | Analysis | Gene (Epigenetic Changes) | Epigenetic Regulators | Neurobehavioral Outcome | Sex Specificity |
---|---|---|---|---|---|---|---|---|---|
Basil et al., 2014 [49] | Mouse (C57BL/6N) | Maternal immune activation (GD17) | Males and females, PD42 | Hy | Sequenom EpiTYPER assay | Mecp2, LINE1 | - | - | Males and females; more profound changes in females |
DiNieri et al., 2011 [50] | Rat (Long Evans) | THC rat model (GD5-PD2) | Males, PD62 | NAc | ChIP (H3K9me2, H3K4me3, RNA polymerase II) | Drd2 | - | Increased sensitivity to opiate reward; Drd2 transcriptional changes | - |
Dong et al., 2015 [51] | Mouse (Swiss albino ND4) | Restrain stress (GD7-GD21) | Males, PD75 | FC, Hy | MeDIP, hMeDIP, ChIP | Bdnf | Dnmt1, Tet1 | Hyperactivity; Impaired social interaction; Bdnf transcriptional changes | - |
Kaminen-Ahola et al., 2010 [52] | Mouse (C57BL/6J Agoutivy) | Ethanol exposure (GD0.5-GD8.5) | Males and females, PD28–30 | FB | Bisulfite Sequencing, Gene Expression Arrays | IAPs | - | Fetal alcohol syndrome-like features | - |
Kundakovic et al., 2013 [53] | Mouse (BALB/c) | BPA exposure (GD0-GD19) | Males and females, PD30–70 | PFC, Hi, Hy | Bisulfite Pyrosequencing | Esr1 | Dnmt1, Dnmt3a | Disrupted exploratory, social and anxiety-like behavior; transcriptional changes in Esr1, Esr2 and Esrrg | Sex specific changes |
Kundakovic et al., 2015 [48] | Mouse (BALB/c) | BPA exposure (GD0-GD19) | Males and females, PD28 and PD60 | Hi | Bisulfite Pyrosequencing | Bdnf IV, Bdnf IX, Grin2b | Dnmt1, Gadd45b | Disrupted exploration of a novel object; Bdnf and Grin2b transcriptional changes | Changes were observed in males |
Labouesse et al., 2015 [54] | Mouse (C57BL/6N) | Maternal immune activation (GD17) | PD80–100 | mPFC | MeDIP, hMeDIP, ChIP (MeCP2) | Gad1, Gad2 | MeCP2 | Impaired working memory and social interaction deficits; Gad1 and Gad2 transcriptional changes | - |
Mueller and Bale, 2008 [55] | Mouse (C57BL/6N:129) | Chronic, variable stress during early, mid and late gestation | Males and females, 6–16 weeks | Hi, Am | Bisulfite Pyrosequencing | Crf, Nr3c1 | - | Maladaptive behavioral stress-responsivity, anhedonia, and an increased sensitivity to SSRI treatment in males | Sex specific changes |
Matrisciano et al., 2013 [56] | Mouse (Swiss albino ND4) | Restrain stress (GD7-GD21) | Males, PD60 | PFC, Hi | MeDIP, hMeDIP, ChIP (Dnmt1, MeCP2) | Reelin, Gad1 | Dnmt 1, Dnmt 3a | Hyperactivity; Impaired social interaction, prepulse inhibition, and fear conditioning; Reelin and Gad1 transcriptional changes | |
Novikova et al., 2008 [57] | Mouse (CD1) | Cocaine exposure (GD8-GD19) | Males, PD3 and PD30 | Hi | Bisulfite sequencing, MeDIP/CGI array | Genome-wide | Dnmt1, Dnmt 3a | Transcriptional changes in Gpr73, Plk2, Prpn5, Mapk1, Impa1, Pyrk3, Gata4, Mtap6, Gtf3c1, Coq7 | - |
Onishchenko et al., 2008 [58] | Mouse (C57BL/6/Bkl) | MeHg exposure (GD7-PD7) | Males, 9 weeks | DG | ChIP (H3ac, H3K27me3), Ms-SNuPE | Bdnf | Depresion like behavior; transcriptional changes in Bdnf | - | |
Richetto et al., 2017 [59] | Mouse (C57BL6/N) | Maternal immune activation (GD9 and GD17) | Males, PD100 | mPFC | SureSelectXT capture sequencing assay and EpiTYPER | Genome wide (Dlx1, Lhx5, Lhx8, Wnt3, Wnt8a, Wnt7b, Efnb3, Mid1, Nlgn1, Nrxn2, Nf2, etc.) | - | Impaired sensorimotor gating, social interaction and spatial memory; transcriptional changes in Dlx1, Wnt3, Mid1, Nlgn1, Nf2 | - |
Schraut et al., 2014 [60] | Mouse (C57BL6/J, 5-Htt +/+ and 5-Htt +/−) | Restrain stress (GD13-GD17) | Females, PD95 | Hi | MeDIP-on-Chip | Genome wide | - | Anxiety-related behavior; Mdb transcriptional changes | - |
St-Cyr S and McGowan, 2015 [61] | Mouse (C57BL/6N) | Exposure to predator odor (GD11-GD18) | Females and males, PD90 | Hi, Am | Bisulfite Pyrosequencing | Bdnf | - | Increased avoidance and decreased predator-odor associated activity; Bdnf and Crhr1 transcriptional changes | Males and females, but females showed a greater increase in CORT level |
Zheng et al., 2016 [62] | Mouse (Kunming) | Restrain stress (GD5-delivery) | Males, PD40 | Hi | MeDIP,ChiP (H3K14ac) | Bdnf | Dnmt1, Hdac1, Hdac2, | Depressive-like and anxiety-like behaviors, Bdnf transcriptional changes | - |
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Kundakovic, M.; Jaric, I. The Epigenetic Link between Prenatal Adverse Environments and Neurodevelopmental Disorders. Genes 2017, 8, 104. https://doi.org/10.3390/genes8030104
Kundakovic M, Jaric I. The Epigenetic Link between Prenatal Adverse Environments and Neurodevelopmental Disorders. Genes. 2017; 8(3):104. https://doi.org/10.3390/genes8030104
Chicago/Turabian StyleKundakovic, Marija, and Ivana Jaric. 2017. "The Epigenetic Link between Prenatal Adverse Environments and Neurodevelopmental Disorders" Genes 8, no. 3: 104. https://doi.org/10.3390/genes8030104
APA StyleKundakovic, M., & Jaric, I. (2017). The Epigenetic Link between Prenatal Adverse Environments and Neurodevelopmental Disorders. Genes, 8(3), 104. https://doi.org/10.3390/genes8030104