Restoration of dioxin-induced damage to fetal steroidogenesis and gonadotropin formation by maternal co-treatment with α-lipoic acid
2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD), an endocrine disruptor, causes reproductive and developmental toxic effects in pups following maternal exposure in a number of animal models. Our previous studies have demonstrated that TCDD imprints sexual immaturity by suppressing the expression of fetal...
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Published in | PloS one Vol. 7; no. 7; p. e40322 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Public Library of Science
20.07.2012
Public Library of Science (PLoS) |
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Abstract | 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD), an endocrine disruptor, causes reproductive and developmental toxic effects in pups following maternal exposure in a number of animal models. Our previous studies have demonstrated that TCDD imprints sexual immaturity by suppressing the expression of fetal pituitary gonadotropins, the regulators of gonadal steroidogenesis. In the present study, we discovered that all TCDD-produced damage to fetal production of pituitary gonadotropins as well as testicular steroidogenesis can be repaired by co-treating pregnant rats with α-lipoic acid (LA), an obligate co-factor for intermediary metabolism including energy production. While LA also acts as an anti-oxidant, other anti-oxidants; i.e., ascorbic acid, butylated hydroxyanisole and edaravone, failed to exhibit any beneficial effects. Neither wasting syndrome nor CYP1A1 induction in the fetal brain caused through the activation of aryl hydrocarbon receptor (AhR) could be attenuated by LA. These lines of evidence suggest that oxidative stress makes only a minor contribution to the TCDD-induced disorder of fetal steroidogenesis, and LA has a restorative effect by targeting on mechanism(s) other than AhR activation. Following a metabolomic analysis, it was found that TCDD caused a more marked change in the hypothalamus, a pituitary regulator, than in the pituitary itself. Although the components of the tricarboxylic acid cycle and the ATP content of the fetal hypothalamus were significantly changed by TCDD, all these changes were again rectified by exogenous LA. We also provided evidence that the fetal hypothalamic content of endogenous LA is significantly reduced following maternal exposure to TCDD. Thus, the data obtained strongly suggest that TCDD reduces the expression of fetal pituitary gonadotropins to imprint sexual immaturity or disturb development by suppressing the level of LA, one of the key players serving energy production. |
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AbstractList | 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD), an endocrine disruptor, causes reproductive and developmental toxic effects in pups following maternal exposure in a number of animal models. Our previous studies have demonstrated that TCDD imprints sexual immaturity by suppressing the expression of fetal pituitary gonadotropins, the regulators of gonadal steroidogenesis. In the present study, we discovered that all TCDD-produced damage to fetal production of pituitary gonadotropins as well as testicular steroidogenesis can be repaired by co-treating pregnant rats with α-lipoic acid (LA), an obligate co-factor for intermediary metabolism including energy production. While LA also acts as an anti-oxidant, other anti-oxidants; i.e., ascorbic acid, butylated hydroxyanisole and edaravone, failed to exhibit any beneficial effects. Neither wasting syndrome nor CYP1A1 induction in the fetal brain caused through the activation of aryl hydrocarbon receptor (AhR) could be attenuated by LA. These lines of evidence suggest that oxidative stress makes only a minor contribution to the TCDD-induced disorder of fetal steroidogenesis, and LA has a restorative effect by targeting on mechanism(s) other than AhR activation. Following a metabolomic analysis, it was found that TCDD caused a more marked change in the hypothalamus, a pituitary regulator, than in the pituitary itself. Although the components of the tricarboxylic acid cycle and the ATP content of the fetal hypothalamus were significantly changed by TCDD, all these changes were again rectified by exogenous LA. We also provided evidence that the fetal hypothalamic content of endogenous LA is significantly reduced following maternal exposure to TCDD. Thus, the data obtained strongly suggest that TCDD reduces the expression of fetal pituitary gonadotropins to imprint sexual immaturity or disturb development by suppressing the level of LA, one of the key players serving energy production. 2,3,7,8-Tetrachlorodibenzo- p -dioxin (TCDD), an endocrine disruptor, causes reproductive and developmental toxic effects in pups following maternal exposure in a number of animal models. Our previous studies have demonstrated that TCDD imprints sexual immaturity by suppressing the expression of fetal pituitary gonadotropins, the regulators of gonadal steroidogenesis. In the present study, we discovered that all TCDD-produced damage to fetal production of pituitary gonadotropins as well as testicular steroidogenesis can be repaired by co-treating pregnant rats with α-lipoic acid (LA), an obligate co-factor for intermediary metabolism including energy production. While LA also acts as an anti-oxidant, other anti-oxidants; i.e. , ascorbic acid, butylated hydroxyanisole and edaravone, failed to exhibit any beneficial effects. Neither wasting syndrome nor CYP1A1 induction in the fetal brain caused through the activation of aryl hydrocarbon receptor (AhR) could be attenuated by LA. These lines of evidence suggest that oxidative stress makes only a minor contribution to the TCDD-induced disorder of fetal steroidogenesis, and LA has a restorative effect by targeting on mechanism(s) other than AhR activation. Following a metabolomic analysis, it was found that TCDD caused a more marked change in the hypothalamus, a pituitary regulator, than in the pituitary itself. Although the components of the tricarboxylic acid cycle and the ATP content of the fetal hypothalamus were significantly changed by TCDD, all these changes were again rectified by exogenous LA. We also provided evidence that the fetal hypothalamic content of endogenous LA is significantly reduced following maternal exposure to TCDD. Thus, the data obtained strongly suggest that TCDD reduces the expression of fetal pituitary gonadotropins to imprint sexual immaturity or disturb development by suppressing the level of LA, one of the key players serving energy production. |
Author | Ishii, Yuji Himeno, Masaru Koga, Takayuki Ishida, Takumi Tsukimori, Kiyomi Takeda, Tomoki Furue, Masutaka Yamamoto, Midori Uchi, Hiroshi Yamada, Hideyuki |
AuthorAffiliation | 3 Research and Clinical Center for Yusho and Dioxin, Kyushu University Hospital, Fukuoka, Japan 1 Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka, Japan Kaohsiung Chang Gung Memorial Hospital, Taiwan 5 Faculty of Pharmaceutical Sciences, Nagasaki International University, Sasebo, Japan 6 Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan 2 Faculty of Pharmaceutical Sciences, Sojo University, Kumamoto, Japan 4 Department of Obstetrics, Fukuoka Children’s Hospital, Fukuoka, Japan |
AuthorAffiliation_xml | – name: 2 Faculty of Pharmaceutical Sciences, Sojo University, Kumamoto, Japan – name: 4 Department of Obstetrics, Fukuoka Children’s Hospital, Fukuoka, Japan – name: 3 Research and Clinical Center for Yusho and Dioxin, Kyushu University Hospital, Fukuoka, Japan – name: 1 Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka, Japan – name: 6 Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan – name: Kaohsiung Chang Gung Memorial Hospital, Taiwan – name: 5 Faculty of Pharmaceutical Sciences, Nagasaki International University, Sasebo, Japan |
Author_xml | – sequence: 1 givenname: Takayuki surname: Koga fullname: Koga, Takayuki organization: Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka, Japan – sequence: 2 givenname: Takumi surname: Ishida fullname: Ishida, Takumi – sequence: 3 givenname: Tomoki surname: Takeda fullname: Takeda, Tomoki – sequence: 4 givenname: Yuji surname: Ishii fullname: Ishii, Yuji – sequence: 5 givenname: Hiroshi surname: Uchi fullname: Uchi, Hiroshi – sequence: 6 givenname: Kiyomi surname: Tsukimori fullname: Tsukimori, Kiyomi – sequence: 7 givenname: Midori surname: Yamamoto fullname: Yamamoto, Midori – sequence: 8 givenname: Masaru surname: Himeno fullname: Himeno, Masaru – sequence: 9 givenname: Masutaka surname: Furue fullname: Furue, Masutaka – sequence: 10 givenname: Hideyuki surname: Yamada fullname: Yamada, Hideyuki |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22911699$$D View this record in MEDLINE/PubMed |
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Copyright | 2012 Koga 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. Koga et al. 2012 |
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DocumentTitleAlternate | Recovery from TCDD Effect on Fetal Gonadotropin |
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Notes | Conceived and designed the experiments: TK TI MH MF HY. Performed the experiments: TK TT MY. Analyzed the data: TK YI KT HU MY HY. Contributed reagents/materials/analysis tools: TI TT YI KT MY MH. Wrote the paper: TK HY. |
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SubjectTerms | Acids Animal models Animals Antioxidants Antioxidants - pharmacology Aromatic compounds Ascorbic acid BHA Biology Brain Brain - drug effects Brain - metabolism Butylated hydroxyanisole Cytochrome P450 Dioxins Endocrine disruptors Energy metabolism Enzymes Exposure Female Fetal Development - drug effects Fetal Development - genetics Fetus - drug effects Fetus - metabolism Fetuses Gonadotropins Gonadotropins - genetics Gonadotropins - metabolism Hypothalamus Kinases Laboratory animals Lipoic acid Male Maternal Exposure Medicine Metabolism Metabolome Metabolomics Neurobiology Neurosciences Oxidants Oxidative stress Oxidizing agents PCB Pharmaceutical sciences Pituitary Pituitary (anterior) Polychlorinated biphenyls Polychlorinated Dibenzodioxins - toxicity Pregnancy Proteins Rats Receptors, Aryl Hydrocarbon - metabolism Regulators Restoration Rodents Sexual behavior Signal Transduction - drug effects Steroidogenesis TCDD Teratogens - toxicity Thioctic Acid - pharmacology Toxicity Tricarboxylic acid cycle |
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Title | Restoration of dioxin-induced damage to fetal steroidogenesis and gonadotropin formation by maternal co-treatment with α-lipoic acid |
URI | https://www.ncbi.nlm.nih.gov/pubmed/22911699 https://www.proquest.com/docview/1326217619/abstract/ https://pubmed.ncbi.nlm.nih.gov/PMC3401201 https://doaj.org/article/3d1a8f5502344467920dcd4f069e5a12 http://dx.doi.org/10.1371/journal.pone.0040322 |
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