Atrazine induced epigenetic transgenerational inheritance of disease, lean phenotype and sperm epimutation pathology biomarkers
Ancestral environmental exposures to a variety of environmental toxicants and other factors have been shown to promote the epigenetic transgenerational inheritance of adult onset disease. The current study examined the potential transgenerational actions of the herbicide atrazine. Atrazine is one of...
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Published in | PloS one Vol. 12; no. 9; p. e0184306 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
20.09.2017
Public Library of Science (PLoS) |
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Abstract | Ancestral environmental exposures to a variety of environmental toxicants and other factors have been shown to promote the epigenetic transgenerational inheritance of adult onset disease. The current study examined the potential transgenerational actions of the herbicide atrazine. Atrazine is one of the most commonly used herbicides in the agricultural industry, in particular with corn and soy crops. Outbred gestating female rats were transiently exposed to a vehicle control or atrazine. The F1 generation offspring were bred to generate the F2 generation and then the F2 generation bred to generate the F3 generation. The F1, F2 and F3 generation control and atrazine lineage rats were aged and various pathologies investigated. The male sperm were collected to investigate DNA methylation differences between the control and atrazine lineage sperm. The F1 generation offspring (directly exposed as a fetus) did not develop disease, but weighed less compared to controls. The F2 generation (grand-offspring) was found to have increased frequency of testis disease and mammary tumors in males and females, early onset puberty in males, and decreased body weight in females compared to controls. The transgenerational F3 generation rats were found to have increased frequency of testis disease, early onset puberty in females, behavioral alterations (motor hyperactivity) and a lean phenotype in males and females. The frequency of multiple diseases was significantly higher in the transgenerational F3 generation atrazine lineage males and females. The transgenerational transmission of disease requires germline (egg or sperm) epigenetic alterations. The sperm differential DNA methylation regions (DMRs), termed epimutations, induced by atrazine were identified in the F1, F2 and F3 generations. Gene associations with the DMRs were identified. For the transgenerational F3 generation sperm, unique sets of DMRs (epimutations) were found to be associated with the lean phenotype or testis disease. These DMRs provide potential biomarkers for transgenerational disease. The etiology of disease appears to be in part due to environmentally induced epigenetic transgenerational inheritance, and epigenetic biomarkers may facilitate the diagnosis of the ancestral exposure and disease susceptibility. Observations indicate that although atrazine does not promote disease in the directly exposed F1 generation, it does have the capacity to promote the epigenetic transgenerational inheritance of disease. |
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AbstractList | Ancestral environmental exposures to a variety of environmental toxicants and other factors have been shown to promote the epigenetic transgenerational inheritance of adult onset disease. The current study examined the potential transgenerational actions of the herbicide atrazine. Atrazine is one of the most commonly used herbicides in the agricultural industry, in particular with corn and soy crops. Outbred gestating female rats were transiently exposed to a vehicle control or atrazine. The F1 generation offspring were bred to generate the F2 generation and then the F2 generation bred to generate the F3 generation. The F1, F2 and F3 generation control and atrazine lineage rats were aged and various pathologies investigated. The male sperm were collected to investigate DNA methylation differences between the control and atrazine lineage sperm. The F1 generation offspring (directly exposed as a fetus) did not develop disease, but weighed less compared to controls. The F2 generation (grand-offspring) was found to have increased frequency of testis disease and mammary tumors in males and females, early onset puberty in males, and decreased body weight in females compared to controls. The transgenerational F3 generation rats were found to have increased frequency of testis disease, early onset puberty in females, behavioral alterations (motor hyperactivity) and a lean phenotype in males and females. The frequency of multiple diseases was significantly higher in the transgenerational F3 generation atrazine lineage males and females. The transgenerational transmission of disease requires germline (egg or sperm) epigenetic alterations. The sperm differential DNA methylation regions (DMRs), termed epimutations, induced by atrazine were identified in the F1, F2 and F3 generations. Gene associations with the DMRs were identified. For the transgenerational F3 generation sperm, unique sets of DMRs (epimutations) were found to be associated with the lean phenotype or testis disease. These DMRs provide potential biomarkers for transgenerational disease. The etiology of disease appears to be in part due to environmentally induced epigenetic transgenerational inheritance, and epigenetic biomarkers may facilitate the diagnosis of the ancestral exposure and disease susceptibility. Observations indicate that although atrazine does not promote disease in the directly exposed F1 generation, it does have the capacity to promote the epigenetic transgenerational inheritance of disease. |
Audience | Academic |
Author | Nilsson, Eric Winchester, Paul Pappalardo, Michelle Houser, Elizabeth Skinner, Michael K McBirney, Margaux Beck, Daniel King, Stephanie E Sadler-Riggleman, Ingrid Unkefer, Margaret |
AuthorAffiliation | 1 Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America 2 Indiana University, School of Medicine, Department of Pediatrics, Indianapolis, Indiana, United States of America INIA, SPAIN |
AuthorAffiliation_xml | – name: 2 Indiana University, School of Medicine, Department of Pediatrics, Indianapolis, Indiana, United States of America – name: 1 Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – name: INIA, SPAIN |
Author_xml | – sequence: 1 givenname: Margaux surname: McBirney fullname: McBirney, Margaux organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – sequence: 2 givenname: Stephanie E surname: King fullname: King, Stephanie E organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – sequence: 3 givenname: Michelle surname: Pappalardo fullname: Pappalardo, Michelle organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – sequence: 4 givenname: Elizabeth surname: Houser fullname: Houser, Elizabeth organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – sequence: 5 givenname: Margaret surname: Unkefer fullname: Unkefer, Margaret organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – sequence: 6 givenname: Eric surname: Nilsson fullname: Nilsson, Eric organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – sequence: 7 givenname: Ingrid surname: Sadler-Riggleman fullname: Sadler-Riggleman, Ingrid organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – sequence: 8 givenname: Daniel surname: Beck fullname: Beck, Daniel organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America – sequence: 9 givenname: Paul surname: Winchester fullname: Winchester, Paul organization: Indiana University, School of Medicine, Department of Pediatrics, Indianapolis, Indiana, United States of America – sequence: 10 givenname: Michael K orcidid: 0000-0001-8224-2078 surname: Skinner fullname: Skinner, Michael K organization: Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28931070$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2017 Public Library of Science 2017 McBirney et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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. 2017 McBirney et al 2017 McBirney et al |
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Publisher | Public Library of Science Public Library of Science (PLoS) |
Publisher_xml | – name: Public Library of Science – name: Public Library of Science (PLoS) |
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Snippet | Ancestral environmental exposures to a variety of environmental toxicants and other factors have been shown to promote the epigenetic transgenerational... |
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SubjectTerms | Adipocytes - cytology Adipocytes - pathology Agricultural industry Animals Atrazine Atrazine - toxicity Behavior, Animal - drug effects Bioinformatics Biology Biology and Life Sciences Biomarkers Biomarkers - metabolism Body weight Body Weight - drug effects Breast cancer Corn Deoxyribonucleic acid Development and progression Disease control Disease susceptibility Disease transmission DNA DNA Methylation Epigenesis, Genetic - drug effects Epigenetics Etiology Exposure Female Females Fetuses Fuel consumption Gene expression Genetic aspects Herbicides Herbicides - toxicity Heredity Hyperactivity Kidney Diseases - epidemiology Kidney Diseases - etiology Male Males Medicine and Health Sciences Metabolic Diseases - epidemiology Metabolic Diseases - etiology Obesity Offspring Pesticides Phenotype Phenotypes Prostatic Diseases - epidemiology Prostatic Diseases - etiology Puberty Rats Rats, Sprague-Dawley Sexual Maturation - drug effects Sperm Spermatozoa - drug effects Spermatozoa - metabolism Stem cells Studies Toxicants Tumors Weight control |
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Title | Atrazine induced epigenetic transgenerational inheritance of disease, lean phenotype and sperm epimutation pathology biomarkers |
URI | https://www.ncbi.nlm.nih.gov/pubmed/28931070 https://www.proquest.com/docview/1940905729 https://pubmed.ncbi.nlm.nih.gov/PMC5606923 https://doaj.org/article/c41ec7e9d7a74d4da936a808fd9b8d9f http://dx.doi.org/10.1371/journal.pone.0184306 |
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