Effect of Carbon Black Nanoparticle on Neonatal Lymphoid Tissues Depending on the Gestational Period of Exposure in Mice

Introduction: Particulate air pollution, containing nanoparticles, enhances the risk of pediatric allergic diseases that is potentially associated with disruption of neonatal immune system. Previous studies have revealed that maternal exposure to carbon black nanoparticles (CB-NP) disturbs the devel...

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Main Authors: Atsuto Onoda, Saki Okamoto, Ryuhei Shimizu, Yasser S. El-Sayed, Shiho Watanabe, Shuhei Ogawa, Ryo Abe, Masao Kamimura, Kohei Soga, Ken Tachibana, Ken Takeda, Masakazu Umezawa
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-08-01
Series:Frontiers in Toxicology
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Online Access:https://www.frontiersin.org/articles/10.3389/ftox.2021.700392/full
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author Atsuto Onoda
Atsuto Onoda
Atsuto Onoda
Saki Okamoto
Ryuhei Shimizu
Yasser S. El-Sayed
Shiho Watanabe
Shuhei Ogawa
Shuhei Ogawa
Ryo Abe
Ryo Abe
Masao Kamimura
Kohei Soga
Ken Tachibana
Ken Tachibana
Ken Tachibana
Ken Takeda
Ken Takeda
Ken Takeda
Masakazu Umezawa
Masakazu Umezawa
Masakazu Umezawa
author_facet Atsuto Onoda
Atsuto Onoda
Atsuto Onoda
Saki Okamoto
Ryuhei Shimizu
Yasser S. El-Sayed
Shiho Watanabe
Shuhei Ogawa
Shuhei Ogawa
Ryo Abe
Ryo Abe
Masao Kamimura
Kohei Soga
Ken Tachibana
Ken Tachibana
Ken Tachibana
Ken Takeda
Ken Takeda
Ken Takeda
Masakazu Umezawa
Masakazu Umezawa
Masakazu Umezawa
author_sort Atsuto Onoda
collection DOAJ
description Introduction: Particulate air pollution, containing nanoparticles, enhances the risk of pediatric allergic diseases that is potentially associated with disruption of neonatal immune system. Previous studies have revealed that maternal exposure to carbon black nanoparticles (CB-NP) disturbs the development of the lymphoid tissues in newborns. Interestingly, the CB-NP-induced immune profiles were observed to be different depending on the gestational period of exposure. It is important to identify the critical exposure period to prevent toxic effects of nanoparticles on the development of the immune system. Therefore, the present study was aimed to investigate the effect of CB-NP on the development of neonatal lymphoid tissues in mice, depending on the gestational period of exposure.Methods: Pregnant ICR mice were treated with a suspension of CB-NP (95 μg/kg body weight) by intranasal instillation; the suspension was administered twice during each gestational period as follows: the pre-implantation period (gestational days 4 and 5), organogenesis period (gestational days 8 and 9), and fetal developmental period (gestational days 15 and 16). The spleen and thymus were collected from offspring mice at 1, 3, and 5-days post-partum. Splenocyte and thymocyte phenotypes were examined by flow cytometry. Gene expression in the spleen was examined by quantitative reverse transcription-polymerase chain reaction.Results: The numbers of total splenocytes and splenic CD3−B220− phenotype (non-T/non-B lymphocytes) in offspring on postnatal day 5 were significantly increased after exposure to CB-NP during the organogenesis period compared with other gestational periods of exposure and control (no exposure). In contrast, expression levels of mRNA associated with chemotaxis and differentiation of immune cells in the spleen were not affected by CB-NP exposure during any gestational period.Conclusion: The organogenesis period was the most susceptible period to CB-NP exposure with respect to lymphoid tissue development. Moreover, the findings of the present and previous studies suggested that long-term exposure to CB-NP across multiple gestational periods including the organogenesis period, rather than acute exposure only organogenesis period, may more severely affect the development of the immune system.
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spelling doaj.art-e71042dd49434d79acb849ba691242b42022-12-21T21:31:10ZengFrontiers Media S.A.Frontiers in Toxicology2673-30802021-08-01310.3389/ftox.2021.700392700392Effect of Carbon Black Nanoparticle on Neonatal Lymphoid Tissues Depending on the Gestational Period of Exposure in MiceAtsuto Onoda0Atsuto Onoda1Atsuto Onoda2Saki Okamoto3Ryuhei Shimizu4Yasser S. El-Sayed5Shiho Watanabe6Shuhei Ogawa7Shuhei Ogawa8Ryo Abe9Ryo Abe10Masao Kamimura11Kohei Soga12Ken Tachibana13Ken Tachibana14Ken Tachibana15Ken Takeda16Ken Takeda17Ken Takeda18Masakazu Umezawa19Masakazu Umezawa20Masakazu Umezawa21The Center for Environmental Health Science for the Next Generation, Research Institute for Science and Technology, Tokyo University of Science, Noda, JapanFaculty of Pharmaceutical Sciences, Tokyo University of Science, Noda, JapanFaculty of Pharmaceutical Sciences, Sanyo-Onoda City University, Sanyoonoda, JapanFaculty of Pharmaceutical Sciences, Tokyo University of Science, Noda, JapanFaculty of Pharmaceutical Sciences, Tokyo University of Science, Noda, JapanFaculty of Veterinary Medicine, Damanhour University, Damanhour, EgyptResearch Institute for Biomedical Sciences, Tokyo University of Science, Noda, JapanThe Center for Environmental Health Science for the Next Generation, Research Institute for Science and Technology, Tokyo University of Science, Noda, JapanResearch Institute for Biomedical Sciences, Tokyo University of Science, Noda, JapanResearch Institute for Biomedical Sciences, Tokyo University of Science, Noda, JapanAdvanced Comprehensive Research Center, Teikyo University, Hachioji, JapanDepartment of Materials Science and Technology, Faculty of Advanced Engineering, Tokyo University of Science, Katsushika, JapanDepartment of Materials Science and Technology, Faculty of Advanced Engineering, Tokyo University of Science, Katsushika, JapanThe Center for Environmental Health Science for the Next Generation, Research Institute for Science and Technology, Tokyo University of Science, Noda, JapanFaculty of Pharmaceutical Sciences, Tokyo University of Science, Noda, JapanFaculty of Pharmaceutical Sciences, Sanyo-Onoda City University, Sanyoonoda, JapanThe Center for Environmental Health Science for the Next Generation, Research Institute for Science and Technology, Tokyo University of Science, Noda, JapanFaculty of Pharmaceutical Sciences, Tokyo University of Science, Noda, JapanFaculty of Pharmaceutical Sciences, Sanyo-Onoda City University, Sanyoonoda, JapanThe Center for Environmental Health Science for the Next Generation, Research Institute for Science and Technology, Tokyo University of Science, Noda, JapanFaculty of Pharmaceutical Sciences, Tokyo University of Science, Noda, JapanDepartment of Materials Science and Technology, Faculty of Advanced Engineering, Tokyo University of Science, Katsushika, JapanIntroduction: Particulate air pollution, containing nanoparticles, enhances the risk of pediatric allergic diseases that is potentially associated with disruption of neonatal immune system. Previous studies have revealed that maternal exposure to carbon black nanoparticles (CB-NP) disturbs the development of the lymphoid tissues in newborns. Interestingly, the CB-NP-induced immune profiles were observed to be different depending on the gestational period of exposure. It is important to identify the critical exposure period to prevent toxic effects of nanoparticles on the development of the immune system. Therefore, the present study was aimed to investigate the effect of CB-NP on the development of neonatal lymphoid tissues in mice, depending on the gestational period of exposure.Methods: Pregnant ICR mice were treated with a suspension of CB-NP (95 μg/kg body weight) by intranasal instillation; the suspension was administered twice during each gestational period as follows: the pre-implantation period (gestational days 4 and 5), organogenesis period (gestational days 8 and 9), and fetal developmental period (gestational days 15 and 16). The spleen and thymus were collected from offspring mice at 1, 3, and 5-days post-partum. Splenocyte and thymocyte phenotypes were examined by flow cytometry. Gene expression in the spleen was examined by quantitative reverse transcription-polymerase chain reaction.Results: The numbers of total splenocytes and splenic CD3−B220− phenotype (non-T/non-B lymphocytes) in offspring on postnatal day 5 were significantly increased after exposure to CB-NP during the organogenesis period compared with other gestational periods of exposure and control (no exposure). In contrast, expression levels of mRNA associated with chemotaxis and differentiation of immune cells in the spleen were not affected by CB-NP exposure during any gestational period.Conclusion: The organogenesis period was the most susceptible period to CB-NP exposure with respect to lymphoid tissue development. Moreover, the findings of the present and previous studies suggested that long-term exposure to CB-NP across multiple gestational periods including the organogenesis period, rather than acute exposure only organogenesis period, may more severely affect the development of the immune system.https://www.frontiersin.org/articles/10.3389/ftox.2021.700392/fullcarbon black nanoparticlesair pollutionnanomaterialneonateslymphoid tissue developmentimmune response
spellingShingle Atsuto Onoda
Atsuto Onoda
Atsuto Onoda
Saki Okamoto
Ryuhei Shimizu
Yasser S. El-Sayed
Shiho Watanabe
Shuhei Ogawa
Shuhei Ogawa
Ryo Abe
Ryo Abe
Masao Kamimura
Kohei Soga
Ken Tachibana
Ken Tachibana
Ken Tachibana
Ken Takeda
Ken Takeda
Ken Takeda
Masakazu Umezawa
Masakazu Umezawa
Masakazu Umezawa
Effect of Carbon Black Nanoparticle on Neonatal Lymphoid Tissues Depending on the Gestational Period of Exposure in Mice
Frontiers in Toxicology
carbon black nanoparticles
air pollution
nanomaterial
neonates
lymphoid tissue development
immune response
title Effect of Carbon Black Nanoparticle on Neonatal Lymphoid Tissues Depending on the Gestational Period of Exposure in Mice
title_full Effect of Carbon Black Nanoparticle on Neonatal Lymphoid Tissues Depending on the Gestational Period of Exposure in Mice
title_fullStr Effect of Carbon Black Nanoparticle on Neonatal Lymphoid Tissues Depending on the Gestational Period of Exposure in Mice
title_full_unstemmed Effect of Carbon Black Nanoparticle on Neonatal Lymphoid Tissues Depending on the Gestational Period of Exposure in Mice
title_short Effect of Carbon Black Nanoparticle on Neonatal Lymphoid Tissues Depending on the Gestational Period of Exposure in Mice
title_sort effect of carbon black nanoparticle on neonatal lymphoid tissues depending on the gestational period of exposure in mice
topic carbon black nanoparticles
air pollution
nanomaterial
neonates
lymphoid tissue development
immune response
url https://www.frontiersin.org/articles/10.3389/ftox.2021.700392/full
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