Maternal nano-titanium dioxide inhalation exposure alters placental cyclooxygenase and oxidant balance in a sexually dimorphic manner

The placenta plays a critical role in nutrient-waste exchange between the maternal and fetal circulation, and thus impacts fetal growth and development. We have previously shown that nano-titanium dioxide (nano-TiO2) inhalation exposure during gestation decreased fetal female pup and placenta mass [...

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Main Authors: Julie A. Griffith, Rachel D. King, Allison C. Dunn, Sara E. Lewis, Brooke A. Maxwell, Timothy R. Nurkiewicz, William T. Goldsmith, Eric E. Kelley, Elizabeth C. Bowdridge
Format: Article
Language:English
Published: Elsevier 2024-04-01
Series:Advances in Redox Research
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2667137923000309
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author Julie A. Griffith
Rachel D. King
Allison C. Dunn
Sara E. Lewis
Brooke A. Maxwell
Timothy R. Nurkiewicz
William T. Goldsmith
Eric E. Kelley
Elizabeth C. Bowdridge
author_facet Julie A. Griffith
Rachel D. King
Allison C. Dunn
Sara E. Lewis
Brooke A. Maxwell
Timothy R. Nurkiewicz
William T. Goldsmith
Eric E. Kelley
Elizabeth C. Bowdridge
author_sort Julie A. Griffith
collection DOAJ
description The placenta plays a critical role in nutrient-waste exchange between the maternal and fetal circulation, and thus impacts fetal growth and development. We have previously shown that nano-titanium dioxide (nano-TiO2) inhalation exposure during gestation decreased fetal female pup and placenta mass [1], which persists in the following generation [2]. In utero exposed females, once mated, their offspring's placentas had increased capacity for H2O2 production. Generation of oxidants such as hydrogen peroxide (H2O2), have been shown to impact cyclooxygenase activity, specifically metabolites such as prostacyclin (PGI2) or thromboxane (TXA2). Therefore, we hypothesized that maternal nano-TiO2 inhalation exposure during gestation results in alterations in placental production of prostacyclin and thromboxane mediated by enhanced H2O2 production in a sexually dimorphic manner. Pregnant Sprague-Dawley rats were exposed to nano-TiO2 aerosols or filtered air (sham-control) from gestational day (GD) 10–19. Dams were euthanized on GD 20, and fetal serum and placental tissue were collected based on fetal sex. Fetal placental zones (junctional zone (JZ) and labyrinth zone (LZ)) were assessed for xanthine oxidoreductase (XOR) activity, H2O2, and catalase activity, as well as 6-keto-PGF1α and TXB2 levels. Nano-TiO2 exposed fetal female LZ demonstrated significantly greater XOR activity compared to exposed males. Exposed fetal female LZ also demonstrated significantly diminished catalase activity compared to sham-control females. Exposed fetal female LZ had significantly increased abundance of 6-keto-PGF1α compared to sham-control females and increased TXB2 compared to exposed males. In the aggregate these data indicate that maternal nano-TiO2 inhalation exposure has a greater impact on redox homeostasis and PGI2/TXA2 balance in the fetal female LZ. Future studies need to address if treatment with an XO inhibitor during gestation can prevent diminished fetal female growth during maternal nano-TiO2 inhalation exposure.
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spelling doaj.art-462084994b304c8d88396bb92fb0046a2024-03-16T05:09:53ZengElsevierAdvances in Redox Research2667-13792024-04-0110100090Maternal nano-titanium dioxide inhalation exposure alters placental cyclooxygenase and oxidant balance in a sexually dimorphic mannerJulie A. Griffith0Rachel D. King1Allison C. Dunn2Sara E. Lewis3Brooke A. Maxwell4Timothy R. Nurkiewicz5William T. Goldsmith6Eric E. Kelley7Elizabeth C. Bowdridge8Department of Physiology, Pharmacology and Toxicology, West Virginia University School of Medicine, Morgantown, WV, USA; Center for Inhalation Toxicology, West Virginia University School of Medicine, Morgantown, WV, USADepartment of Biochemistry, West Virginia University School of Medicine, Morgantown, WV, USADepartment of Physiology, Pharmacology and Toxicology, West Virginia University School of Medicine, Morgantown, WV, USA; Center for Inhalation Toxicology, West Virginia University School of Medicine, Morgantown, WV, USADepartment of Physiology, Pharmacology and Toxicology, West Virginia University School of Medicine, Morgantown, WV, USADepartment of Physiology, Pharmacology and Toxicology, West Virginia University School of Medicine, Morgantown, WV, USADepartment of Physiology, Pharmacology and Toxicology, West Virginia University School of Medicine, Morgantown, WV, USA; Center for Inhalation Toxicology, West Virginia University School of Medicine, Morgantown, WV, USADepartment of Physiology, Pharmacology and Toxicology, West Virginia University School of Medicine, Morgantown, WV, USA; Center for Inhalation Toxicology, West Virginia University School of Medicine, Morgantown, WV, USADepartment of Physiology, Pharmacology and Toxicology, West Virginia University School of Medicine, Morgantown, WV, USA; Center for Inhalation Toxicology, West Virginia University School of Medicine, Morgantown, WV, USADepartment of Physiology, Pharmacology and Toxicology, West Virginia University School of Medicine, Morgantown, WV, USA; Center for Inhalation Toxicology, West Virginia University School of Medicine, Morgantown, WV, USA; Corresponding author at: Department of Physiology, Pharmacology, and Toxicology, University of West Virginia, School of Medicine, 3076 Health Sciences Center North, PO Box 9229, Morgantown, WV 26506-9229, USA.The placenta plays a critical role in nutrient-waste exchange between the maternal and fetal circulation, and thus impacts fetal growth and development. We have previously shown that nano-titanium dioxide (nano-TiO2) inhalation exposure during gestation decreased fetal female pup and placenta mass [1], which persists in the following generation [2]. In utero exposed females, once mated, their offspring's placentas had increased capacity for H2O2 production. Generation of oxidants such as hydrogen peroxide (H2O2), have been shown to impact cyclooxygenase activity, specifically metabolites such as prostacyclin (PGI2) or thromboxane (TXA2). Therefore, we hypothesized that maternal nano-TiO2 inhalation exposure during gestation results in alterations in placental production of prostacyclin and thromboxane mediated by enhanced H2O2 production in a sexually dimorphic manner. Pregnant Sprague-Dawley rats were exposed to nano-TiO2 aerosols or filtered air (sham-control) from gestational day (GD) 10–19. Dams were euthanized on GD 20, and fetal serum and placental tissue were collected based on fetal sex. Fetal placental zones (junctional zone (JZ) and labyrinth zone (LZ)) were assessed for xanthine oxidoreductase (XOR) activity, H2O2, and catalase activity, as well as 6-keto-PGF1α and TXB2 levels. Nano-TiO2 exposed fetal female LZ demonstrated significantly greater XOR activity compared to exposed males. Exposed fetal female LZ also demonstrated significantly diminished catalase activity compared to sham-control females. Exposed fetal female LZ had significantly increased abundance of 6-keto-PGF1α compared to sham-control females and increased TXB2 compared to exposed males. In the aggregate these data indicate that maternal nano-TiO2 inhalation exposure has a greater impact on redox homeostasis and PGI2/TXA2 balance in the fetal female LZ. Future studies need to address if treatment with an XO inhibitor during gestation can prevent diminished fetal female growth during maternal nano-TiO2 inhalation exposure.http://www.sciencedirect.com/science/article/pii/S2667137923000309Titanium dioxideThromboxaneProstacyclinSexual dimorphismOxidantsXanthine oxidoreductase
spellingShingle Julie A. Griffith
Rachel D. King
Allison C. Dunn
Sara E. Lewis
Brooke A. Maxwell
Timothy R. Nurkiewicz
William T. Goldsmith
Eric E. Kelley
Elizabeth C. Bowdridge
Maternal nano-titanium dioxide inhalation exposure alters placental cyclooxygenase and oxidant balance in a sexually dimorphic manner
Advances in Redox Research
Titanium dioxide
Thromboxane
Prostacyclin
Sexual dimorphism
Oxidants
Xanthine oxidoreductase
title Maternal nano-titanium dioxide inhalation exposure alters placental cyclooxygenase and oxidant balance in a sexually dimorphic manner
title_full Maternal nano-titanium dioxide inhalation exposure alters placental cyclooxygenase and oxidant balance in a sexually dimorphic manner
title_fullStr Maternal nano-titanium dioxide inhalation exposure alters placental cyclooxygenase and oxidant balance in a sexually dimorphic manner
title_full_unstemmed Maternal nano-titanium dioxide inhalation exposure alters placental cyclooxygenase and oxidant balance in a sexually dimorphic manner
title_short Maternal nano-titanium dioxide inhalation exposure alters placental cyclooxygenase and oxidant balance in a sexually dimorphic manner
title_sort maternal nano titanium dioxide inhalation exposure alters placental cyclooxygenase and oxidant balance in a sexually dimorphic manner
topic Titanium dioxide
Thromboxane
Prostacyclin
Sexual dimorphism
Oxidants
Xanthine oxidoreductase
url http://www.sciencedirect.com/science/article/pii/S2667137923000309
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