Evaluation of Placentation and the Role of the Aryl Hydrocarbon Receptor Pathway in a Rat Model of Dioxin Exposure
Our environment is replete with chemicals that can affect embryonic and extraembryonic development. Dioxins, such as 2,3,7,8-tetrachlorodibenzo- -dioxin (TCDD), are compounds affecting development through the aryl hydrocarbon receptor (AHR). The purpose of this investigation was to examine the effec...
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Published in | Environmental health perspectives Vol. 129; no. 11; p. 117001 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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United States
National Institute of Environmental Health Sciences
01.11.2021
Environmental Health Perspectives |
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Abstract | Our environment is replete with chemicals that can affect embryonic and extraembryonic development. Dioxins, such as 2,3,7,8-tetrachlorodibenzo-
-dioxin (TCDD), are compounds affecting development through the aryl hydrocarbon receptor (AHR).
The purpose of this investigation was to examine the effects of TCDD exposure on pregnancy and placentation and to evaluate roles for AHR and cytochrome P450 1A1 (CYP1A1) in TCDD action.
Actions of TCDD were examined in wild-type and genome-edited rat models. Placenta phenotyping was assessed using morphological, biochemical, and molecular analyses.
TCDD exposures were shown to result in placental adaptations and at higher doses, pregnancy termination. Deep intrauterine endovascular trophoblast cell invasion was a prominent placentation site adaptation to TCDD. TCDD-mediated placental adaptations were dependent upon maternal AHR signaling but not upon placental or fetal AHR signaling nor the presence of a prominent AHR target, CYP1A1. At the placentation site, TCDD activated AHR signaling within endothelial cells but not trophoblast cells. Immune and trophoblast cell behaviors at the uterine-placental interface were guided by the actions of TCDD on endothelial cells.
We identified an AHR regulatory pathway in rats activated by dioxin affecting uterine and trophoblast cell dynamics and the formation of the hemochorial placenta. https://doi.org/10.1289/EHP9256. |
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AbstractList | Our environment is replete with chemicals that can affect embryonic and extraembryonic development. Dioxins, such as 2,3,7,8-tetrachlorodibenzo-
-dioxin (TCDD), are compounds affecting development through the aryl hydrocarbon receptor (AHR).
The purpose of this investigation was to examine the effects of TCDD exposure on pregnancy and placentation and to evaluate roles for AHR and cytochrome P450 1A1 (CYP1A1) in TCDD action.
Actions of TCDD were examined in wild-type and genome-edited rat models. Placenta phenotyping was assessed using morphological, biochemical, and molecular analyses.
TCDD exposures were shown to result in placental adaptations and at higher doses, pregnancy termination. Deep intrauterine endovascular trophoblast cell invasion was a prominent placentation site adaptation to TCDD. TCDD-mediated placental adaptations were dependent upon maternal AHR signaling but not upon placental or fetal AHR signaling nor the presence of a prominent AHR target, CYP1A1. At the placentation site, TCDD activated AHR signaling within endothelial cells but not trophoblast cells. Immune and trophoblast cell behaviors at the uterine-placental interface were guided by the actions of TCDD on endothelial cells.
We identified an AHR regulatory pathway in rats activated by dioxin affecting uterine and trophoblast cell dynamics and the formation of the hemochorial placenta. https://doi.org/10.1289/EHP9256. Background: Our environment is replete with chemicals that can affect embryonic and extraembryonic development. Dioxins, such as 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), are compounds affecting development through the aryl hydrocarbon receptor (AHR). Objectives: The purpose of this investigation was to examine the effects of TCDD exposure on pregnancy and placentation and to evaluate roles for AHR and cytochrome P450 1A1 (CYP1A1) in TCDD action. Methods: Actions of TCDD were examined in wild-type and genome-edited rat models. Placenta phenotyping was assessed using morphological, biochemical, and molecular analyses. Results: TCDD exposures were shown to result in placental adaptations and at higher doses, pregnancy termination. Deep intrauterine endovascular trophoblast cell invasion was a prominent placentation site adaptation to TCDD. TCDD-mediated placental adaptations were dependent upon maternal AHR signaling but not upon placental or fetal AHR signaling nor the presence of a prominent AHR target, CYP1A1. At the placentation site, TCDD activated AHR signaling within endothelial cells but not trophoblast cells. Immune and trophoblast cell behaviors at the uterine-placental interface were guided by the actions of TCDD on endothelial cells. Discussion: We identified an AHR regulatory pathway in rats activated by dioxin affecting uterine and trophoblast cell dynamics and the formation of the hemochorial placenta. Background: Our environment is replete with chemicals that can affect embryonic and extraembryonic development. Dioxins, such as 2,3,7,8-tetrachlorodibenzo-p p -dioxin (TCDD), are compounds affecting development through the aryl hydrocarbon receptor (AHR). Objectives: The purpose of this investigation was to examine the effects of TCDD exposure on pregnancy and placentation and to evaluate roles for AHR and cytochrome P450 1A1 (CYP1A1) in TCDD action. Methods: Actions of TCDD were examined in wild-type and genome-edited rat models. Placenta phenotyping was assessed using morphological, biochemical, and molecular analyses. Results: TCDD exposures were shown to result in placental adaptations and at higher doses, pregnancy termination. Deep intrauterine endovascular trophoblast cell invasion was a prominent placentation site adaptation to TCDD. TCDD-mediated placental adaptations were dependent upon maternal AHR signaling but not upon placental or fetal AHR signaling nor the presence of a prominent AHR target, CYP1A1. At the placentation site, TCDD activated AHR signaling within endothelial cells but not trophoblast cells. Immune and trophoblast cell behaviors at the uterine–placental interface were guided by the actions of TCDD on endothelial cells. Discussion: We identified an AHR regulatory pathway in rats activated by dioxin affecting uterine and trophoblast cell dynamics and the formation of the hemochorial placenta. |
Audience | Academic |
Author | Dhakal, Pramod Pierce, Stephen H Kozai, Keisuke Vyhlidal, Carrie A Iqbal, Khursheed Scott, Regan L Roby, Katherine F Soares, Michael J |
Author_xml | – sequence: 1 givenname: Khursheed orcidid: 0000-0002-6742-4591 surname: Iqbal fullname: Iqbal, Khursheed organization: Department of Pathology and Laboratory Medicine, KUMC, Kansas City, Kansas, USA – sequence: 2 givenname: Stephen H surname: Pierce fullname: Pierce, Stephen H organization: Department of Pathology and Laboratory Medicine, KUMC, Kansas City, Kansas, USA – sequence: 3 givenname: Keisuke orcidid: 0000-0003-2645-7431 surname: Kozai fullname: Kozai, Keisuke organization: Department of Pathology and Laboratory Medicine, KUMC, Kansas City, Kansas, USA – sequence: 4 givenname: Pramod surname: Dhakal fullname: Dhakal, Pramod organization: Department of Pathology and Laboratory Medicine, KUMC, Kansas City, Kansas, USA – sequence: 5 givenname: Regan L orcidid: 0000-0001-6294-5294 surname: Scott fullname: Scott, Regan L organization: Department of Pathology and Laboratory Medicine, KUMC, Kansas City, Kansas, USA – sequence: 6 givenname: Katherine F orcidid: 0000-0001-6667-9464 surname: Roby fullname: Roby, Katherine F organization: Department of Anatomy and Cell Biology, KUMC, Kansas City, Kansas, USA – sequence: 7 givenname: Carrie A surname: Vyhlidal fullname: Vyhlidal, Carrie A organization: Department of Pediatrics, University of Missouri-Kansas City School of Medicine, Kansas City, Missouri – sequence: 8 givenname: Michael J surname: Soares fullname: Soares, Michael J organization: Department of Obstetrics and Gynecology, KUMC, Kansas City, Kansas, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34747641$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_heliyon_2022_e11767 crossref_primary_10_1016_j_placenta_2024_05_134 crossref_primary_10_1016_S0378_4274_23_00817_2 crossref_primary_10_3390_ph15070828 crossref_primary_10_1016_j_tox_2021_153054 crossref_primary_10_1016_j_fct_2023_114086 crossref_primary_10_1073_pnas_2213622120 crossref_primary_10_3389_fcell_2022_1060298 crossref_primary_10_3390_ijms23062947 crossref_primary_10_1242_dev_202239 crossref_primary_10_1242_dev_201095 |
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Snippet | Our environment is replete with chemicals that can affect embryonic and extraembryonic development. Dioxins, such as 2,3,7,8-tetrachlorodibenzo-
-dioxin... Background: Our environment is replete with chemicals that can affect embryonic and extraembryonic development. Dioxins, such as... Background: Our environment is replete with chemicals that can affect embryonic and extraembryonic development. Dioxins, such as 2,3,7,8-tetrachlorodibenzo-p p... |
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SubjectTerms | Adaptation Age Animal models Animals Aromatic compounds Carbon dioxide Cardiovascular system CRISPR Cytochrome Cytochrome P-450 CYP1A1 - genetics Cytochrome P-450 CYP1A1 - metabolism Cytochrome P450 Cytochromes P450 Dioxin Dioxins Dioxins - toxicity Embryogenesis Embryos Endothelial cells Endothelial Cells - metabolism Environmental aspects Evaluation Exposure Female Females Fetuses Genetic aspects Genetic engineering Genomes Health aspects Hydrocarbons Ligands Mutation Ostomy Phenotyping Physiological aspects Placenta Placenta - metabolism Placentation Polychlorinated Dibenzodioxins - toxicity Pregnancy Rats Receptors Receptors, Aryl Hydrocarbon - metabolism Rodents Signal transduction Signaling TCDD Transcription factors Trophoblasts - drug effects Uterus |
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Title | Evaluation of Placentation and the Role of the Aryl Hydrocarbon Receptor Pathway in a Rat Model of Dioxin Exposure |
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