Impact of Endocrine Disruptors Upon Non-Genetic Inheritance

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2022 Mar 25

PMID 35328771

Authors

Debbie Montjean

Anne-Sophie Neyroud

Marina G Yefimova

Moncef Benkhalifa

Rosalie Cabry

Celia Ravel

Affiliations

Soon will be listed here.

Abstract

Similar to environmental factors, EDCs (endocrine-disrupting chemicals) can influence gene expression without modifying the DNA sequence. It is commonly accepted that the transgenerational inheritance of parentally acquired traits is conveyed by epigenetic alterations also known as "epimutations". DNA methylation, acetylation, histone modification, RNA-mediated effects and extracellular vesicle effects are the mechanisms that have been described so far to be responsible for these epimutations. They may lead to the transgenerational inheritance of diverse phenotypes in the progeny when they occur in the germ cells of an affected individual. While EDC-induced health effects have dramatically increased over the past decade, limited effects on sperm epigenetics have been described. However, there has been a gain of interest in this issue in recent years. The gametes (sperm and oocyte) represent targets for EDCs and thus a route for environmentally induced changes over several generations. This review aims at providing an overview of the epigenetic mechanisms that might be implicated in this transgenerational inheritance.

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References

Lumey L, Ekamper P, Bijwaard G, Conti G, van Poppel F . Overweight and obesity at age 19 after pre-natal famine exposure. Int J Obes (Lond). 2021; 45(8):1668-1676. PMC: 8310790. DOI: 10.1038/s41366-021-00824-3. View

Jenkins T, Aston K, Pflueger C, Cairns B, Carrell D . Age-associated sperm DNA methylation alterations: possible implications in offspring disease susceptibility. PLoS Genet. 2014; 10(7):e1004458. PMC: 4091790. DOI: 10.1371/journal.pgen.1004458. View

Spadafora C . Transgenerational epigenetic reprogramming of early embryos: a mechanistic model. Environ Epigenet. 2020; 6(1):dvaa009. PMC: 7368376. DOI: 10.1093/eep/dvaa009. View

Akemann C, Meyer D, Gurdziel K, Baker T . TCDD-induced multi- and transgenerational changes in the methylome of male zebrafish gonads. Environ Epigenet. 2020; 6(1):dvaa010. PMC: 7660120. DOI: 10.1093/eep/dvaa010. View

Po B, Chiu J . Transgenerational impairments of reproduction and development of the marine invertebrate Crepidula onyx resulted from long-term dietary exposure of 2,2',4,4'-tetrabromodiphenyl ether (BDE-47). Environ Pollut. 2018; 235:730-738. DOI: 10.1016/j.envpol.2017.12.087. View

Chan J, Morgan C, Leu N, Shetty A, Cisse Y, Nugent B . Reproductive tract extracellular vesicles are sufficient to transmit intergenerational stress and program neurodevelopment. Nat Commun. 2020; 11(1):1499. PMC: 7083921. DOI: 10.1038/s41467-020-15305-w. View

Hatcher K, Willing J, Chiang C, Rattan S, Flaws J, Mahoney M . Exposure to di-(2-ethylhexyl) phthalate transgenerationally alters anxiety-like behavior and amygdala gene expression in adult male and female mice. Physiol Behav. 2019; 207:7-14. PMC: 6545259. DOI: 10.1016/j.physbeh.2019.04.018. View

Mori M, Ludwig R, Garcia-Martin R, Brandao B, Kahn C . Extracellular miRNAs: From Biomarkers to Mediators of Physiology and Disease. Cell Metab. 2019; 30(4):656-673. PMC: 6774861. DOI: 10.1016/j.cmet.2019.07.011. View

Heijmans B, Tobi E, Stein A, Putter H, Blauw G, Susser E . Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008; 105(44):17046-9. PMC: 2579375. DOI: 10.1073/pnas.0806560105. View

10.

McCarrey J . Distinctions between transgenerational and non-transgenerational epimutations. Mol Cell Endocrinol. 2014; 398(1-2):13-23. DOI: 10.1016/j.mce.2014.07.016. View

11.

Barile L, Vassalli G . Exosomes: Therapy delivery tools and biomarkers of diseases. Pharmacol Ther. 2017; 174:63-78. DOI: 10.1016/j.pharmthera.2017.02.020. View

12.

Heindel J, Vandenberg L . Developmental origins of health and disease: a paradigm for understanding disease cause and prevention. Curr Opin Pediatr. 2015; 27(2):248-53. PMC: 4535724. DOI: 10.1097/MOP.0000000000000191. View

13.

Manikkam M, Haque M, Guerrero-Bosagna C, Nilsson E, Skinner M . Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult-onset disease through the female germline. PLoS One. 2014; 9(7):e102091. PMC: 4109920. DOI: 10.1371/journal.pone.0102091. View

14.

Skinner M, Guerrero-Bosagna C . Role of CpG deserts in the epigenetic transgenerational inheritance of differential DNA methylation regions. BMC Genomics. 2014; 15:692. PMC: 4149044. DOI: 10.1186/1471-2164-15-692. View

15.

Mimouni N, Paiva I, Barbotin A, Timzoura F, Plassard D, Le Gras S . Polycystic ovary syndrome is transmitted via a transgenerational epigenetic process. Cell Metab. 2021; 33(3):513-530.e8. PMC: 7928942. DOI: 10.1016/j.cmet.2021.01.004. View

16.

Osada S, Nishikawa J, Nakanishi T, Tanaka K, Nishihara T . Some organotin compounds enhance histone acetyltransferase activity. Toxicol Lett. 2004; 155(2):329-35. DOI: 10.1016/j.toxlet.2004.10.009. View

17.

Margolis L, Sadovsky Y . The biology of extracellular vesicles: The known unknowns. PLoS Biol. 2019; 17(7):e3000363. PMC: 6667152. DOI: 10.1371/journal.pbio.3000363. View

18.

Chen J, Wu S, Wen S, Shen L, Peng J, Yan C . The Mechanism of Environmental Endocrine Disruptors (DEHP) Induces Epigenetic Transgenerational Inheritance of Cryptorchidism. PLoS One. 2015; 10(6):e0126403. PMC: 4452760. DOI: 10.1371/journal.pone.0126403. View

19.

Nilsson E, Ben Maamar M, Skinner M . Role of epigenetic transgenerational inheritance in generational toxicology. Environ Epigenet. 2022; 8(1):dvac001. PMC: 8848501. DOI: 10.1093/eep/dvac001. View

20.

Percy Z, La Guardia M, Xu Y, C Hale R, Dietrich K, Lanphear B . Concentrations and loadings of organophosphate and replacement brominated flame retardants in house dust from the home study during the PBDE phase-out. Chemosphere. 2019; 239:124701. PMC: 6854320. DOI: 10.1016/j.chemosphere.2019.124701. View