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Maternal exposure to ultrafine particles enhances influenza infection during pregnancy

BACKGROUND: Interactions between air pollution and infectious agents are increasingly recognized and critical to identify, especially to protect vulnerable populations. Pregnancy represents a vulnerable period for influenza infection and air pollution exposure, yet interactions during pregnancy rema...

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Autores principales: Drury, Nicholas L., Mustapha, Toriq, Shore, Ross A., Zhao, Jiayun, Wright, Gus A., Hoffmann, Aline Rodrigues, Talcott, Susanne U., Regan, Annette, Tighe, Robert M., Zhang, Renyi, Johnson, Natalie M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10106898/
https://www.ncbi.nlm.nih.gov/pubmed/37069680
http://dx.doi.org/10.1186/s12989-023-00521-1
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author Drury, Nicholas L.
Mustapha, Toriq
Shore, Ross A.
Zhao, Jiayun
Wright, Gus A.
Hoffmann, Aline Rodrigues
Talcott, Susanne U.
Regan, Annette
Tighe, Robert M.
Zhang, Renyi
Johnson, Natalie M.
author_facet Drury, Nicholas L.
Mustapha, Toriq
Shore, Ross A.
Zhao, Jiayun
Wright, Gus A.
Hoffmann, Aline Rodrigues
Talcott, Susanne U.
Regan, Annette
Tighe, Robert M.
Zhang, Renyi
Johnson, Natalie M.
author_sort Drury, Nicholas L.
collection PubMed
description BACKGROUND: Interactions between air pollution and infectious agents are increasingly recognized and critical to identify, especially to protect vulnerable populations. Pregnancy represents a vulnerable period for influenza infection and air pollution exposure, yet interactions during pregnancy remain unclear. Maternal exposure to ultrafine particles (UFPs, [Formula: see text] 100 nm diameter), a class of particulate matter ubiquitous in urban environments, elicits unique pulmonary immune responses. We hypothesized that UFP exposure during pregnancy would lead to aberrant immune responses to influenza enhancing infection severity. RESULTS: Building from our well-characterized C57Bl/6N mouse model employing daily gestational UFP exposure from gestational day (GD) 0.5–13.5, we carried out a pilot study wherein pregnant dams were subsequently infected with Influenza A/Puerto Rico/8/1934 (PR8) on GD14.5. Findings indicate that PR8 infection caused decreased weight gain in filtered air (FA) and UFP-exposed groups. Co-exposure to UFPs and viral infection led to pronounced elevation in PR8 viral titer and reduced pulmonary inflammation, signifying potential suppression of innate and adaptive immune defenses. Pulmonary expression of the pro-viral factor sphingosine kinase 1 (Sphk1) and pro-inflammatory cytokine interleukin-1β (IL-1 [Formula: see text] ) was significantly increased in pregnant mice exposed to UFPs and infected with PR8; expression correlated with higher viral titer. CONCLUSIONS: Results from our model provide initial insight into how maternal UFP exposure during pregnancy enhances respiratory viral infection risk. This model is an important first step in establishing future regulatory and clinical strategies for protecting pregnant women exposed to UFPs. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12989-023-00521-1.
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spelling pubmed-101068982023-04-18 Maternal exposure to ultrafine particles enhances influenza infection during pregnancy Drury, Nicholas L. Mustapha, Toriq Shore, Ross A. Zhao, Jiayun Wright, Gus A. Hoffmann, Aline Rodrigues Talcott, Susanne U. Regan, Annette Tighe, Robert M. Zhang, Renyi Johnson, Natalie M. Part Fibre Toxicol Research BACKGROUND: Interactions between air pollution and infectious agents are increasingly recognized and critical to identify, especially to protect vulnerable populations. Pregnancy represents a vulnerable period for influenza infection and air pollution exposure, yet interactions during pregnancy remain unclear. Maternal exposure to ultrafine particles (UFPs, [Formula: see text] 100 nm diameter), a class of particulate matter ubiquitous in urban environments, elicits unique pulmonary immune responses. We hypothesized that UFP exposure during pregnancy would lead to aberrant immune responses to influenza enhancing infection severity. RESULTS: Building from our well-characterized C57Bl/6N mouse model employing daily gestational UFP exposure from gestational day (GD) 0.5–13.5, we carried out a pilot study wherein pregnant dams were subsequently infected with Influenza A/Puerto Rico/8/1934 (PR8) on GD14.5. Findings indicate that PR8 infection caused decreased weight gain in filtered air (FA) and UFP-exposed groups. Co-exposure to UFPs and viral infection led to pronounced elevation in PR8 viral titer and reduced pulmonary inflammation, signifying potential suppression of innate and adaptive immune defenses. Pulmonary expression of the pro-viral factor sphingosine kinase 1 (Sphk1) and pro-inflammatory cytokine interleukin-1β (IL-1 [Formula: see text] ) was significantly increased in pregnant mice exposed to UFPs and infected with PR8; expression correlated with higher viral titer. CONCLUSIONS: Results from our model provide initial insight into how maternal UFP exposure during pregnancy enhances respiratory viral infection risk. This model is an important first step in establishing future regulatory and clinical strategies for protecting pregnant women exposed to UFPs. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12989-023-00521-1. BioMed Central 2023-04-17 /pmc/articles/PMC10106898/ /pubmed/37069680 http://dx.doi.org/10.1186/s12989-023-00521-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Drury, Nicholas L.
Mustapha, Toriq
Shore, Ross A.
Zhao, Jiayun
Wright, Gus A.
Hoffmann, Aline Rodrigues
Talcott, Susanne U.
Regan, Annette
Tighe, Robert M.
Zhang, Renyi
Johnson, Natalie M.
Maternal exposure to ultrafine particles enhances influenza infection during pregnancy
title Maternal exposure to ultrafine particles enhances influenza infection during pregnancy
title_full Maternal exposure to ultrafine particles enhances influenza infection during pregnancy
title_fullStr Maternal exposure to ultrafine particles enhances influenza infection during pregnancy
title_full_unstemmed Maternal exposure to ultrafine particles enhances influenza infection during pregnancy
title_short Maternal exposure to ultrafine particles enhances influenza infection during pregnancy
title_sort maternal exposure to ultrafine particles enhances influenza infection during pregnancy
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10106898/
https://www.ncbi.nlm.nih.gov/pubmed/37069680
http://dx.doi.org/10.1186/s12989-023-00521-1
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