Impact of Endocrine Disruptors upon Non-Genetic Inheritance
Abstract
:1. Introduction
Non Genetic Inheritance Players
- (a)
- Methylation
- (b)
- Histone Modifications
- (c)
- Non-coding RNAs
- (d)
- Extracellular Vesicles
2. Endocrine-Disrupting Chemicals (EDCs) Transgenerational Impact
2.1. Dioxin
2.2. Diethylstilbestrol
2.3. Fungicides
2.4. Organochlorine Pesticides
2.5. Bisphenol A
2.6. PolyChlorinated Biphenyls
2.7. Phtalates
2.8. Perfluoroalkyl and Polyfluoroalkyl Substances
2.9. Flame Retardants
2.10. Polycyclic Aromatic Hydrocarbons
3. Epigenetic Inheritance
4. After-Effects of EDCs Exposure on Germ Cells
4.1. Epigenetic Sperm Modifications
4.2. Epigenetic Oocyte Modifications
5. Embryo Development and Critical Window
6. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
AMH | Anti-Mullerian hormone |
ART | Assisted reproductive techniques |
BDE-47 | 2,2′,4,4′-tetrabromodiphenyl ether |
BPA | Bisphenol A |
DES | Diethylstilbestrol |
DMRs | Differentially methylated regions |
DDT | 1,1,1-trichloro-2,2-bis(4-chlorophenyl)ethane |
DEHP | Di(2-ethylhexyl) phthalate |
EE2 | Ethinylestradiol |
EDCs | Endocrine-disrupting chemicals |
Endo-siRNAs | Endogenous-small interfering RNAs |
EVs | Extracellular vesicles |
FDA | U.S. Food and Drug Administration |
H3K9me3 | H3K9 trimethylation |
HAT | Histone acetyltransferase |
HPTE | 2,2-bis-(p-hydroxyphenyl)-1,1,1-trichloroethane |
Igf2 | Insulin-like growth factor 2 |
lincRNAs | Large intergenic non-coding RNAs |
LIF | Leukemia inhibitory factor |
lncRNA | Long non-coding RNA |
miRNAs | MicroRNAs |
mRNA | Messenger RNA |
MXC | Methoxychlor (1,1,1-trichloro-2,2-bis(p-methoxyphenyl) ethane) |
NOAEL | No-observed-adverse-effect level |
OP | Organophosphate |
OPFRs | Organophosphate flame retardants, |
piRNAs | Piwi-interacting RNAs |
PBDEs | Polybrominated diphenyl ethers |
PAHs | Polycyclic aromatic hydrocarbons |
PCBs | Polychlorinated biphenyls |
PCOS | Polycystic ovary syndrome |
PFOS | Perfluorooctane sulfonate |
PFOA | Perfluorooctanoate |
PGC | Primordial germ cells |
PPAR | Peroxisome proliferator-activated receptor |
snoRNAs | Small nucleolar RNAs |
sncRNA | Small non-coding RNAs |
SUV39H2 | SUppressor of Variegation 3-9 homolog 2 Histone Lysine Methyltransferase |
TBBPA | Tetrabromobisphenol A |
TBT | Tributyltin |
TCDD | 2,3,7,8-tetrachlordibenzo-p-dioxin |
TPT | Triphenyltin |
Xist | X-inactive specific transcript |
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Model | EDC | Transgenerational Effect | Reference |
---|---|---|---|
Daphnia magna microcrustacean | Flame retardants Tris(2-butoxyethyl) phosphate (TBOEP) | Levels of mRNA were found to be significantly different for genes known to be involved in endocrine-mediated mechanisms such as reproduction and growth between generations F0, F1, and F2, indicating the effects of parental exposure on offspring. | [89] |
Crepidula onyx gastropod | 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47) | Bioaccumulation and maternal transfer of BDE-47 were evident in all life stages of the F0 generation and in F1 eggs, respectively. Exposure to BDE-47 reduced fecundity, delayed sexual maturity, and impeded embryonic development in F0 to F2. | [147] |
Zebra fish (danio rerio) | Flame retardant Tetrabromobisphenol A (TBBPA) | Neurotoxicity and decreased content of dopamine in larval offspring. | [90] |
Medaka | BPA EE2 | BPA or EE2-induced transgenerational reproductive impairment in the F2 generation was associated with alterations in reproductive gene expression in brain and testis and global DNA methylation in testis. | [148] |
Gobiocypris rarus | BPA | Parental BPA exposure inhibited the ovary development of the offspring. | [149] |
Fish | Dioxin | Exposure to the environmental toxicants methylmercury or dioxin transmit to their grand-offspring behavioral changes, visual defects, increased body mass, skeletal abnormalities and/or decreased fertility, sometimes associated with changes in DNA methylation. | [150] |
Medaka | BPA EE2 | Medaka exposed to the endocrine disruptors BPA or ethinylestradiol produce grand-offspring and great-grand-offspring with reduced fertility. | [151] |
Bird | Genistein | In quail eggs exposed to the environmental estrogen genistein, the great-grand offspring age at which the first egg was laid was significantly greater. Embryonic environment affects the phenotype of offspring three generations later in quail. | [152] |
Rodent | Vinclozoline | Increased obesity risk in rats is inherited transgenerationally after ancestral exposure to DDT, plastic compounds, hydrocarbons and methoxychlor. | [130] |
Rodent | Vinclozoline | Endocrine disruptors have been shown in mouse models to induce transmissible changes over several generations, altering the quality of spermatogenesis in adulthood. | [11,130] |
Rodent | Chlordecone | Chlordecone increases prostatic epithelial neoplasia in F1 and F3 mice. Hoxa genes are affected both in the prostate and in sperm of F1 and F3 generations. | [24] |
Fish M. beryllina | Bifenthrin (pyrethroid insecticide) Levonorgestrel (synthetic progestin), Ethinylestradiol (synthetic estrogen), Trenbolone (synthetic androgen) | Differential methylation of EDC-responsive genes is inherited by the offspring of EDC-treated animals, sometimes in the F2 generation that was never exposed. Low environmentally relevant levels of EDCs can cause altered methylation in genes that are functionally relevant to impaired phenotypes documented in EDC-exposed animals. EDC exposure has the potential to affect epigenetic regulation in future generations of fish that have never been exposed. | [8] |
Zebrafish | TCDD (dioxin) | Multi- and transgenerational methylomic changes in testicular tissue and decreased reproductive capacity, significantly in the indirectly exposed F1 generation. Histone modification genes were both differentially methylated and expressed in all generations, and many differentially methylated genes overlapped between multiple generations. | [153] |
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Montjean, D.; Neyroud, A.-S.; Yefimova, M.G.; Benkhalifa, M.; Cabry, R.; Ravel, C. Impact of Endocrine Disruptors upon Non-Genetic Inheritance. Int. J. Mol. Sci. 2022, 23, 3350. https://doi.org/10.3390/ijms23063350
Montjean D, Neyroud A-S, Yefimova MG, Benkhalifa M, Cabry R, Ravel C. Impact of Endocrine Disruptors upon Non-Genetic Inheritance. International Journal of Molecular Sciences. 2022; 23(6):3350. https://doi.org/10.3390/ijms23063350
Chicago/Turabian StyleMontjean, Debbie, Anne-Sophie Neyroud, Marina G. Yefimova, Moncef Benkhalifa, Rosalie Cabry, and Célia Ravel. 2022. "Impact of Endocrine Disruptors upon Non-Genetic Inheritance" International Journal of Molecular Sciences 23, no. 6: 3350. https://doi.org/10.3390/ijms23063350