Allergic sensitization and exposure to ambient air pollution beginning early in life lead to a COPD-like phenotype in young adult mice

The perinatal period and early infancy are considered critical periods for lung development. During this period, adversities such as environmental exposures, allergic sensitization, and asthma are believed to impact lung health in adulthood. Therefore, we hypothesized that concomitant exposure to al...

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Main Authors: Natália de Souza Xavier Costa, Aila Mirtes Teles, Jôse Mára de Brito, Thaís de Barros Mendes Lopes, Renata Calciolari Rossi, Fernanda Magalhães Arantes Costa, Beatriz Mangueira Saraiva-Romanholo, Adenir Perini, Tatiane Katsue Furuya, Alexis Germán Murillo Carrasco, Mariana Matera Veras, Paulo Hilário Nascimento Saldiva, Roger Chammas, Thais Mauad
Format: Article
Language:English
Published: Elsevier 2022-08-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651322006613
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author Natália de Souza Xavier Costa
Aila Mirtes Teles
Jôse Mára de Brito
Thaís de Barros Mendes Lopes
Renata Calciolari Rossi
Fernanda Magalhães Arantes Costa
Beatriz Mangueira Saraiva-Romanholo
Adenir Perini
Tatiane Katsue Furuya
Alexis Germán Murillo Carrasco
Mariana Matera Veras
Paulo Hilário Nascimento Saldiva
Roger Chammas
Thais Mauad
author_facet Natália de Souza Xavier Costa
Aila Mirtes Teles
Jôse Mára de Brito
Thaís de Barros Mendes Lopes
Renata Calciolari Rossi
Fernanda Magalhães Arantes Costa
Beatriz Mangueira Saraiva-Romanholo
Adenir Perini
Tatiane Katsue Furuya
Alexis Germán Murillo Carrasco
Mariana Matera Veras
Paulo Hilário Nascimento Saldiva
Roger Chammas
Thais Mauad
author_sort Natália de Souza Xavier Costa
collection DOAJ
description The perinatal period and early infancy are considered critical periods for lung development. During this period, adversities such as environmental exposures, allergic sensitization, and asthma are believed to impact lung health in adulthood. Therefore, we hypothesized that concomitant exposure to allergic sensitization and urban-derived fine particulate matter (PM2.5) in the early postnatal period of mice would cause more profound alterations in lung alveolarization and growth and differently modulate lung inflammation and gene expression than either insult alone in adult life. BALB/c mice were sensitized with ovalbumin (OVA) and exposed to PM2.5 from the fifth day of life. Then, we assessed lung responsiveness, inflammation in BALF, lung tissue, and alveolarization by stereology. In addition, we performed a transcriptomic analysis of lung tissue on the 40th day of life. Our results showed that young adult mice submitted to allergic sensitization and exposure to ambient PM2.5 since early life presented decreased lung growth with impaired alveolarization, a mixed neutrophilic-eosinophilic pattern of lung inflammation, increased airway responsiveness, and increased expression of genes linked to neutrophil recruitment when compared to animals that were OVA-sensitized or PM2.5 exposed only. Both, early life allergic sensitization and PM2.5 exposure, induced inflammation and impaired lung growth, but concomitant exposure was associated with worsened inflammation parameters and caused alveolar enlargement. Our experimental data provide pathological support for the hypothesis that allergic or environmental insults in early life have permanent adverse consequences for lung growth. In addition, combined insults were associated with the development of a COPD-like phenotype in young adult mice. Together with our data, current evidence points to the urgent need for healthier environments with fewer childhood disadvantage factors during the critical windows of lung development and growth.
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spelling doaj.art-8238763b7fb34eb2be12ccd5fa80ae772022-12-22T01:26:09ZengElsevierEcotoxicology and Environmental Safety0147-65132022-08-01241113821Allergic sensitization and exposure to ambient air pollution beginning early in life lead to a COPD-like phenotype in young adult miceNatália de Souza Xavier Costa0Aila Mirtes Teles1Jôse Mára de Brito2Thaís de Barros Mendes Lopes3Renata Calciolari Rossi4Fernanda Magalhães Arantes Costa5Beatriz Mangueira Saraiva-Romanholo6Adenir Perini7Tatiane Katsue Furuya8Alexis Germán Murillo Carrasco9Mariana Matera Veras10Paulo Hilário Nascimento Saldiva11Roger Chammas12Thais Mauad13Laboratório de Patologia Ambiental e Experimental (LIM05), Departamento de Patologia, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilLaboratório de Patologia Ambiental e Experimental (LIM05), Departamento de Patologia, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilLaboratório de Patologia Ambiental e Experimental (LIM05), Departamento de Patologia, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilLaboratório de Patologia Ambiental e Experimental (LIM05), Departamento de Patologia, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilDepartment of Pathology, Universidade do Oeste Paulista UNOESTE, Presidente Prudente, SP, BrazilLaboratory of Experimental Therapeutics (LIM20), Department of Medicine, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilLaboratory of Experimental Therapeutics (LIM20), Department of Medicine, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilLaboratory of Experimental Therapeutics (LIM20), Department of Medicine, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilCenter of Translational Research in Oncology (LIM24), Instituto do Cancer do Estado de Sao Paulo (ICESP), Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilCenter of Translational Research in Oncology (LIM24), Instituto do Cancer do Estado de Sao Paulo (ICESP), Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilLaboratório de Patologia Ambiental e Experimental (LIM05), Departamento de Patologia, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilLaboratório de Patologia Ambiental e Experimental (LIM05), Departamento de Patologia, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilCenter of Translational Research in Oncology (LIM24), Instituto do Cancer do Estado de Sao Paulo (ICESP), Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, BrazilLaboratório de Patologia Ambiental e Experimental (LIM05), Departamento de Patologia, Faculdade de Medicina FMUSP, Universidade de São Paulo, São Paulo, SP, Brazil; Correspondence to: University of São Paulo School of Medicine, Department of Pathology, Av. Dr. Arnaldo, 455 – 1st floor – Room: 1155, Cerqueira Cesar, São Paulo 01246-903, SP, Brazil.The perinatal period and early infancy are considered critical periods for lung development. During this period, adversities such as environmental exposures, allergic sensitization, and asthma are believed to impact lung health in adulthood. Therefore, we hypothesized that concomitant exposure to allergic sensitization and urban-derived fine particulate matter (PM2.5) in the early postnatal period of mice would cause more profound alterations in lung alveolarization and growth and differently modulate lung inflammation and gene expression than either insult alone in adult life. BALB/c mice were sensitized with ovalbumin (OVA) and exposed to PM2.5 from the fifth day of life. Then, we assessed lung responsiveness, inflammation in BALF, lung tissue, and alveolarization by stereology. In addition, we performed a transcriptomic analysis of lung tissue on the 40th day of life. Our results showed that young adult mice submitted to allergic sensitization and exposure to ambient PM2.5 since early life presented decreased lung growth with impaired alveolarization, a mixed neutrophilic-eosinophilic pattern of lung inflammation, increased airway responsiveness, and increased expression of genes linked to neutrophil recruitment when compared to animals that were OVA-sensitized or PM2.5 exposed only. Both, early life allergic sensitization and PM2.5 exposure, induced inflammation and impaired lung growth, but concomitant exposure was associated with worsened inflammation parameters and caused alveolar enlargement. Our experimental data provide pathological support for the hypothesis that allergic or environmental insults in early life have permanent adverse consequences for lung growth. In addition, combined insults were associated with the development of a COPD-like phenotype in young adult mice. Together with our data, current evidence points to the urgent need for healthier environments with fewer childhood disadvantage factors during the critical windows of lung development and growth.http://www.sciencedirect.com/science/article/pii/S0147651322006613Air pollutionParticulate matterAsthmaAllergic sensitizationAlveolarization
spellingShingle Natália de Souza Xavier Costa
Aila Mirtes Teles
Jôse Mára de Brito
Thaís de Barros Mendes Lopes
Renata Calciolari Rossi
Fernanda Magalhães Arantes Costa
Beatriz Mangueira Saraiva-Romanholo
Adenir Perini
Tatiane Katsue Furuya
Alexis Germán Murillo Carrasco
Mariana Matera Veras
Paulo Hilário Nascimento Saldiva
Roger Chammas
Thais Mauad
Allergic sensitization and exposure to ambient air pollution beginning early in life lead to a COPD-like phenotype in young adult mice
Ecotoxicology and Environmental Safety
Air pollution
Particulate matter
Asthma
Allergic sensitization
Alveolarization
title Allergic sensitization and exposure to ambient air pollution beginning early in life lead to a COPD-like phenotype in young adult mice
title_full Allergic sensitization and exposure to ambient air pollution beginning early in life lead to a COPD-like phenotype in young adult mice
title_fullStr Allergic sensitization and exposure to ambient air pollution beginning early in life lead to a COPD-like phenotype in young adult mice
title_full_unstemmed Allergic sensitization and exposure to ambient air pollution beginning early in life lead to a COPD-like phenotype in young adult mice
title_short Allergic sensitization and exposure to ambient air pollution beginning early in life lead to a COPD-like phenotype in young adult mice
title_sort allergic sensitization and exposure to ambient air pollution beginning early in life lead to a copd like phenotype in young adult mice
topic Air pollution
Particulate matter
Asthma
Allergic sensitization
Alveolarization
url http://www.sciencedirect.com/science/article/pii/S0147651322006613
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