Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures
Environmental factors during fetal development can induce a permanent epigenetic change in the germ line (sperm) that then transmits epigenetic transgenerational inheritance of adult-onset disease in the absence of any subsequent exposure. The epigenetic transgenerational actions of various environm...
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Published in | PloS one Vol. 7; no. 2; p. e31901 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
28.02.2012
Public Library of Science (PLoS) |
Subjects | |
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Abstract | Environmental factors during fetal development can induce a permanent epigenetic change in the germ line (sperm) that then transmits epigenetic transgenerational inheritance of adult-onset disease in the absence of any subsequent exposure. The epigenetic transgenerational actions of various environmental compounds and relevant mixtures were investigated with the use of a pesticide mixture (permethrin and insect repellant DEET), a plastic mixture (bisphenol A and phthalates), dioxin (TCDD) and a hydrocarbon mixture (jet fuel, JP8). After transient exposure of F0 gestating female rats during the period of embryonic gonadal sex determination, the subsequent F1-F3 generations were obtained in the absence of any environmental exposure. The effects on the F1, F2 and F3 generations pubertal onset and gonadal function were assessed. The plastics, dioxin and jet fuel were found to promote early-onset female puberty transgenerationally (F3 generation). Spermatogenic cell apoptosis was affected transgenerationally. Ovarian primordial follicle pool size was significantly decreased with all treatments transgenerationally. Differential DNA methylation of the F3 generation sperm promoter epigenome was examined. Differential DNA methylation regions (DMR) were identified in the sperm of all exposure lineage males and found to be consistent within a specific exposure lineage, but different between the exposures. Several genomic features of the DMR, such as low density CpG content, were identified. Exposure-specific epigenetic biomarkers were identified that may allow for the assessment of ancestral environmental exposures associated with adult onset disease. |
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AbstractList | Environmental factors during fetal development can induce a permanent epigenetic change in the germ line (sperm) that then transmits epigenetic transgenerational inheritance of adult-onset disease in the absence of any subsequent exposure. The epigenetic transgenerational actions of various environmental compounds and relevant mixtures were investigated with the use of a pesticide mixture (permethrin and insect repellant DEET), a plastic mixture (bisphenol A and phthalates), dioxin (TCDD) and a hydrocarbon mixture (jet fuel, JP8). After transient exposure of F0 gestating female rats during the period of embryonic gonadal sex determination, the subsequent F1-F3 generations were obtained in the absence of any environmental exposure. The effects on the F1, F2 and F3 generations pubertal onset and gonadal function were assessed. The plastics, dioxin and jet fuel were found to promote early-onset female puberty transgenerationally (F3 generation). Spermatogenic cell apoptosis was affected transgenerationally. Ovarian primordial follicle pool size was significantly decreased with all treatments transgenerationally. Differential DNA methylation of the F3 generation sperm promoter epigenome was examined. Differential DNA methylation regions (DMR) were identified in the sperm of all exposure lineage males and found to be consistent within a specific exposure lineage, but different between the exposures. Several genomic features of the DMR, such as low density CpG content, were identified. Exposure-specific epigenetic biomarkers were identified that may allow for the assessment of ancestral environmental exposures associated with adult onset disease. |
Audience | Academic |
Author | Tracey, Rebecca Manikkam, Mohan Guerrero-Bosagna, Carlos Haque, Md M Skinner, Michael K |
AuthorAffiliation | Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America Massachusetts General Hospital, United States of America |
AuthorAffiliation_xml | – name: Massachusetts General Hospital, United States of America – name: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America |
Author_xml | – sequence: 1 givenname: Mohan surname: Manikkam fullname: Manikkam, Mohan organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – sequence: 2 givenname: Carlos surname: Guerrero-Bosagna fullname: Guerrero-Bosagna, Carlos – sequence: 3 givenname: Rebecca surname: Tracey fullname: Tracey, Rebecca – sequence: 4 givenname: Md M surname: Haque fullname: Haque, Md M – sequence: 5 givenname: Michael K surname: Skinner fullname: Skinner, Michael K |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22389676$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | COPYRIGHT 2012 Public Library of Science 2012 Manikkam et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Manikkam et al. 2012 |
Copyright_xml | – notice: COPYRIGHT 2012 Public Library of Science – notice: 2012 Manikkam et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: Manikkam et al. 2012 |
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Notes | Conceived and designed the experiments: MKS. Performed the experiments: MM CG RT MMH. Analyzed the data: MKS MM CG RT MMH. Wrote the paper: MKS MM CG. |
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References | G Ritchie (ref23) 2003; 6 V Corbel (ref17) 2009; 7 RA Waterland (ref7) 2009; 71 N Watanabe (ref35) 2001; 109 S Salian (ref9) 2009; 85 PA Hunt (ref14) 2009; 81 PC Das (ref16) 2008; 23 AF Heder (ref19) 2001; 62 JS Fisher (ref30) 2004; 127 W Zhang (ref49) 2007; 23 MK Skinner (ref1) 2010; 21 CE Talsness (ref12) 2009; 364 R Hauser (ref31) 2008; 89 S Meredith (ref44) 2000; 119 JC Rockett (ref29) 2004; 112 S Olgun (ref20) 2004; 196 R Kavlock (ref4) 2005; 35 MJ Engelbregt (ref37) 2000; 48 D Pimentel (ref11) 2007; 35 SK Cesario (ref27) 2007; 36 A Baccarelli (ref22) 2009; 21 H Tateno (ref45) 2000; 63 MI Torres-Altoro (ref18) 2011; 119 SA DiVall (ref25) 2009; 16 WS Ward (ref46) 1999; 60 FM Biro (ref26) 2010; 126 F Martinato (ref47) 2008; 3 EE Nilsson (ref43) 2008; 135 C Guerrero-Bosagna (ref41) 2011 C Guerrero-Bosagna (ref5) 2010; 5 SS Wong (ref24) 2008; 254 AK Hotchkiss (ref34) 2007; 96 S Honma (ref36) 2002; 16 S Kumar (ref33) 2004; 46 MK Skinner (ref39) 2005; 11 AB Brinkman (ref40) 2010; 52 C Stouder (ref10) 2010; 139 S Vujovic (ref32) 2009; 15 RL Jirtle (ref3) 2007; 8 AJ Bernal (ref13) 2010; 88 D Crews (ref42) 2007; 104 C Traggiai (ref28) 2003; 17 B Sadikovic (ref48) 2008; 3 MD Anway (ref38) 2008; 91 MD Anway (ref6) 2006; 147 KL Bruner-Tran (ref8) 2011; 31 LS Birnbaum (ref21) 2003; 111 LW Kitchen (ref15) 2009; 34 MD Anway (ref2) 2005; 308 |
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SubjectTerms | Age Agrochemicals Animals Apoptosis Benzhydryl Compounds Bioindicators Biological markers Biology Biomarkers Bisphenol A CpG islands DEET DEET - toxicity Deoxyribonucleic acid Development and progression Dioxins Disease transmission DNA DNA methylation DNA Methylation - drug effects Embryos Environmental assessment Environmental effects Environmental factors Environmental toxicology Epigenesis, Genetic - drug effects Epigenetic inheritance Epigenetics Exposure Female Fetal development Fetuses Heredity Hydrocarbons - toxicity Infertility Insects Jet engine fuels Jet fuels Male Males Medicine Methylation Ovarian Follicle - drug effects Permethrin Permethrin - toxicity Pesticides Pesticides - toxicity Phenols Phenols - toxicity Phthalate plasticizers Phthalates Plastics Polymers Puberty Rats Reproduction - drug effects Sex determination Sex Determination Processes - drug effects Sperm Spermatozoa - drug effects TCDD |
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Title | Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures |
URI | https://www.ncbi.nlm.nih.gov/pubmed/22389676 https://www.proquest.com/docview/1332824836 https://pubmed.ncbi.nlm.nih.gov/PMC3289630 https://doaj.org/article/8532ad40efc14364a36d471dfb939bb3 http://dx.doi.org/10.1371/journal.pone.0031901 |
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