Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota

Detalhes bibliográficos
Autor(a) principal: Gregório Grama Cavalcante
Data de Publicação: 2022
Outros Autores: Anna Gabriella Guimarães, Camila Pereira Queiroz-Glauss, Marcela Helena Gonçalves Pereira, Angélica Samer Lallo Dias, Laila Sampaio Horta, Jamil Silvano de Oliveira, Silvia Dantas Cangussú, Paula Prazeres Magalhães, Remo Castro Russo, Helton da Costa Santiago
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UFMG
Texto Completo: https://doi.org/10.1155/2022/1466011
http://hdl.handle.net/1843/61233
https://orcid.org/0000-0001-8402-1375
https://orcid.org/0000-0003-4511-3722
https://orcid.org/0000-0002-5753-624X
https://orcid.org/0000-0002-7821-6392
https://orcid.org/0000-0002-8664-9753
https://orcid.org/0000-0002-6291-0515
https://orcid.org/0000-0002-0851-5610
https://orcid.org/0000-0002-1061-6445
https://orcid.org/0000-0002-1715-3834
https://orcid.org/0000-0002-5695-8256
Resumo: Background. Asthma is a chronic pulmonary disease that affects about 300 million people worldwide. Previous studies have associated antimicrobial use with allergies, but the real impact of antibiotics on asthma is still elusive. We investigated the potential impact of amoxicillin (Amox), trimethoprim/sulfamethoxazole (TMP/SMX), and metronidazole (Metro) in a murine model of OVA-induced allergic airway inflammation. Methods. BALB/c mice received three cycles of 7 days of antibiotics in drinking water followed by 7 days washout and were sensitized i.p. with OVA/Alum at days 0 and 14. After the end of the last antibiotic washout, the mice were challenged with aerosolized OVA. Pulmonary parameters were evaluated, and serum, BAL, and feces were collected for analysis. Results. Amox- and TMP/SMX-treated animals displayed more severe allergic airway inflammation parameters with increased airway hyperresponsiveness, reduced lung alveolar volume, and increased levels in BAL of IL-4 and IL-6. In contrast, Metro-treated mice showed preserved FEV-50, decreased lung inflammation, and higher levels of butyrate and propionate in their feces. Metro treatment was associated with increased OVA-specific IgA in serum. BAL microbiota was abundant in allergic groups but not in nonallergic controls with the Amox-treated group displaying the increased frequency of Proteobacteria, while Metro and TMP/SMX showed increased levels of Firmicutes. In the gut, we observed the enrichment of Akkermansia muciniphila associated with reduced airway inflammation phenotype in the Metro group, even after the recovery period. Conclusion. Our data suggest that different antibiotic treatments may impact the course of experimental allergic airway inflammation in diverse ways by several mechanisms, including modulation of short-chain fat acids production by intestinal microbiota.
id UFMG_0be06ddc04952dae60c98e47bc20d04a
oai_identifier_str oai:repositorio.ufmg.br:1843/61233
network_acronym_str UFMG
network_name_str Repositório Institucional da UFMG
repository_id_str
spelling 2023-11-21T21:15:45Z2023-11-21T21:15:45Z20222022https://doi.org/10.1155/2022/14660112314-7156http://hdl.handle.net/1843/61233https://orcid.org/0000-0001-8402-1375https://orcid.org/0000-0003-4511-3722https://orcid.org/0000-0002-5753-624Xhttps://orcid.org/0000-0002-7821-6392https://orcid.org/0000-0002-8664-9753https://orcid.org/0000-0002-6291-0515https://orcid.org/0000-0002-0851-5610https://orcid.org/0000-0002-1061-6445https://orcid.org/0000-0002-1715-3834https://orcid.org/0000-0002-5695-8256Background. Asthma is a chronic pulmonary disease that affects about 300 million people worldwide. Previous studies have associated antimicrobial use with allergies, but the real impact of antibiotics on asthma is still elusive. We investigated the potential impact of amoxicillin (Amox), trimethoprim/sulfamethoxazole (TMP/SMX), and metronidazole (Metro) in a murine model of OVA-induced allergic airway inflammation. Methods. BALB/c mice received three cycles of 7 days of antibiotics in drinking water followed by 7 days washout and were sensitized i.p. with OVA/Alum at days 0 and 14. After the end of the last antibiotic washout, the mice were challenged with aerosolized OVA. Pulmonary parameters were evaluated, and serum, BAL, and feces were collected for analysis. Results. Amox- and TMP/SMX-treated animals displayed more severe allergic airway inflammation parameters with increased airway hyperresponsiveness, reduced lung alveolar volume, and increased levels in BAL of IL-4 and IL-6. In contrast, Metro-treated mice showed preserved FEV-50, decreased lung inflammation, and higher levels of butyrate and propionate in their feces. Metro treatment was associated with increased OVA-specific IgA in serum. BAL microbiota was abundant in allergic groups but not in nonallergic controls with the Amox-treated group displaying the increased frequency of Proteobacteria, while Metro and TMP/SMX showed increased levels of Firmicutes. In the gut, we observed the enrichment of Akkermansia muciniphila associated with reduced airway inflammation phenotype in the Metro group, even after the recovery period. Conclusion. Our data suggest that different antibiotic treatments may impact the course of experimental allergic airway inflammation in diverse ways by several mechanisms, including modulation of short-chain fat acids production by intestinal microbiota.Fundo. A asma é uma doença pulmonar crônica que afeta cerca de 300 milhões de pessoas em todo o mundo. Estudos anteriores associaram o uso de antimicrobianos a alergias, mas o real impacto dos antibióticos na asma ainda é incerto. Nós investigamos o impacto potencial da amoxicilina (Amox), trimetoprim/sulfametoxazol (TMP/SMX) e metronidazol (Metro) em um modelo murino de inflamação alérgica das vias aéreas induzida por OVA. Métodos. Camundongos BALB/c receberam três ciclos de 7 dias de antibióticos em água potável seguidos de 7 dias de lavagem e foram sensibilizados i.p. com OVA/Alum nos dias 0 e 14. Após o final da última lavagem com antibiótico, os ratos foram desafiados com OVA em aerossol. Os parâmetros pulmonares foram avaliados e soro, LBA e fezes foram coletados para análise. Resultados. Os animais tratados com Amox e TMP / SMX apresentaram parâmetros de inflamação alérgica das vias aéreas mais graves, com aumento da hiperresponsividade das vias aéreas, redução do volume alveolar pulmonar e aumento dos níveis de IL-4 e IL-6 no LBA. Em contraste, os ratos tratados com Metro apresentaram FEV-50 preservado, diminuição da inflamação pulmonar e níveis mais elevados de butirato e propionato nas fezes. O tratamento com Metro foi associado ao aumento de IgA específica para OVA no soro. A microbiota BAL foi abundante em grupos alérgicos, mas não em controles não alérgicos, com o grupo tratado com Amox exibindo maior frequência de Proteobactérias, enquanto Metro e TMP/SMX mostraram níveis aumentados de Firmicutes. No intestino, observamos o enriquecimento de Akkermansia muciniphila associado à redução do fenótipo de inflamação das vias aéreas no grupo Metro, mesmo após o período de recuperação. Conclusão. Nossos dados sugerem que diferentes tratamentos com antibióticos podem impactar o curso da inflamação alérgica experimental das vias aéreas de diversas maneiras por vários mecanismos, incluindo a modulação da produção de ácidos graxos de cadeia curta pela microbiota intestinal.FAPEMIG - Fundação de Amparo à Pesquisa do Estado de Minas GeraisCAPES - Coordenação de Aperfeiçoamento de Pessoal de Nível SuperiorengUniversidade Federal de Minas GeraisUFMGBrasilICB - DEPARTAMENTO DE BIOQUÍMICA E IMUNOLOGIAICB - DEPARTAMENTO DE FISIOLOGIA E BIOFÍSICAICB - DEPARTAMENTO DE MICROBIOLOGIAJournal of Immunology ResearchAsmaAntibióticosMicrobiotaAsthmaAntibioticsSymbiotic microbiotaTreatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiotaTratamento com classes distintas de antibióticos causa diferentes desfechos pulmonares na inflamação alérgica das vias aéreas associada à modulação da microbiota simbióticainfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttps://www.hindawi.com/journals/jir/2022/1466011/Gregório Grama CavalcanteAnna Gabriella GuimarãesCamila Pereira Queiroz-GlaussMarcela Helena Gonçalves PereiraAngélica Samer Lallo DiasLaila Sampaio HortaJamil Silvano de OliveiraSilvia Dantas CangussúPaula Prazeres MagalhãesRemo Castro RussoHelton da Costa Santiagoapplication/pdfinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UFMGinstname:Universidade Federal de Minas Gerais (UFMG)instacron:UFMGLICENSELicense.txtLicense.txttext/plain; charset=utf-82042https://repositorio.ufmg.br/bitstream/1843/61233/1/License.txtfa505098d172de0bc8864fc1287ffe22MD51ORIGINALTreatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota.pdfTreatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota.pdfapplication/pdf11227803https://repositorio.ufmg.br/bitstream/1843/61233/2/Treatment%20with%20distinct%20antibiotic%20classes%20causes%20different%20pulmonary%20outcomes%20on%20allergic%20airway%20inflammation%20associated%20with%20modulation%20of%20symbiotic%20microbiota.pdf67a3247da8803b2e6bc3d9f136b144abMD521843/612332023-11-21 18:15:46.013oai:repositorio.ufmg.br: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Repositório de PublicaçõesPUBhttps://repositorio.ufmg.br/oaiopendoar:2023-11-21T21:15:46Repositório Institucional da UFMG - Universidade Federal de Minas Gerais (UFMG)false
dc.title.pt_BR.fl_str_mv Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota
dc.title.alternative.pt_BR.fl_str_mv Tratamento com classes distintas de antibióticos causa diferentes desfechos pulmonares na inflamação alérgica das vias aéreas associada à modulação da microbiota simbiótica
title Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota
spellingShingle Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota
Gregório Grama Cavalcante
Asthma
Antibiotics
Symbiotic microbiota
Asma
Antibióticos
Microbiota
title_short Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota
title_full Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota
title_fullStr Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota
title_full_unstemmed Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota
title_sort Treatment with distinct antibiotic classes causes different pulmonary outcomes on allergic airway inflammation associated with modulation of symbiotic microbiota
author Gregório Grama Cavalcante
author_facet Gregório Grama Cavalcante
Anna Gabriella Guimarães
Camila Pereira Queiroz-Glauss
Marcela Helena Gonçalves Pereira
Angélica Samer Lallo Dias
Laila Sampaio Horta
Jamil Silvano de Oliveira
Silvia Dantas Cangussú
Paula Prazeres Magalhães
Remo Castro Russo
Helton da Costa Santiago
author_role author
author2 Anna Gabriella Guimarães
Camila Pereira Queiroz-Glauss
Marcela Helena Gonçalves Pereira
Angélica Samer Lallo Dias
Laila Sampaio Horta
Jamil Silvano de Oliveira
Silvia Dantas Cangussú
Paula Prazeres Magalhães
Remo Castro Russo
Helton da Costa Santiago
author2_role author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Gregório Grama Cavalcante
Anna Gabriella Guimarães
Camila Pereira Queiroz-Glauss
Marcela Helena Gonçalves Pereira
Angélica Samer Lallo Dias
Laila Sampaio Horta
Jamil Silvano de Oliveira
Silvia Dantas Cangussú
Paula Prazeres Magalhães
Remo Castro Russo
Helton da Costa Santiago
dc.subject.por.fl_str_mv Asthma
Antibiotics
Symbiotic microbiota
topic Asthma
Antibiotics
Symbiotic microbiota
Asma
Antibióticos
Microbiota
dc.subject.other.pt_BR.fl_str_mv Asma
Antibióticos
Microbiota
description Background. Asthma is a chronic pulmonary disease that affects about 300 million people worldwide. Previous studies have associated antimicrobial use with allergies, but the real impact of antibiotics on asthma is still elusive. We investigated the potential impact of amoxicillin (Amox), trimethoprim/sulfamethoxazole (TMP/SMX), and metronidazole (Metro) in a murine model of OVA-induced allergic airway inflammation. Methods. BALB/c mice received three cycles of 7 days of antibiotics in drinking water followed by 7 days washout and were sensitized i.p. with OVA/Alum at days 0 and 14. After the end of the last antibiotic washout, the mice were challenged with aerosolized OVA. Pulmonary parameters were evaluated, and serum, BAL, and feces were collected for analysis. Results. Amox- and TMP/SMX-treated animals displayed more severe allergic airway inflammation parameters with increased airway hyperresponsiveness, reduced lung alveolar volume, and increased levels in BAL of IL-4 and IL-6. In contrast, Metro-treated mice showed preserved FEV-50, decreased lung inflammation, and higher levels of butyrate and propionate in their feces. Metro treatment was associated with increased OVA-specific IgA in serum. BAL microbiota was abundant in allergic groups but not in nonallergic controls with the Amox-treated group displaying the increased frequency of Proteobacteria, while Metro and TMP/SMX showed increased levels of Firmicutes. In the gut, we observed the enrichment of Akkermansia muciniphila associated with reduced airway inflammation phenotype in the Metro group, even after the recovery period. Conclusion. Our data suggest that different antibiotic treatments may impact the course of experimental allergic airway inflammation in diverse ways by several mechanisms, including modulation of short-chain fat acids production by intestinal microbiota.
publishDate 2022
dc.date.issued.fl_str_mv 2022
dc.date.accessioned.fl_str_mv 2023-11-21T21:15:45Z
dc.date.available.fl_str_mv 2023-11-21T21:15:45Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/1843/61233
dc.identifier.doi.pt_BR.fl_str_mv https://doi.org/10.1155/2022/1466011
dc.identifier.issn.pt_BR.fl_str_mv 2314-7156
dc.identifier.orcid.pt_BR.fl_str_mv https://orcid.org/0000-0001-8402-1375
https://orcid.org/0000-0003-4511-3722
https://orcid.org/0000-0002-5753-624X
https://orcid.org/0000-0002-7821-6392
https://orcid.org/0000-0002-8664-9753
https://orcid.org/0000-0002-6291-0515
https://orcid.org/0000-0002-0851-5610
https://orcid.org/0000-0002-1061-6445
https://orcid.org/0000-0002-1715-3834
https://orcid.org/0000-0002-5695-8256
url https://doi.org/10.1155/2022/1466011
http://hdl.handle.net/1843/61233
https://orcid.org/0000-0001-8402-1375
https://orcid.org/0000-0003-4511-3722
https://orcid.org/0000-0002-5753-624X
https://orcid.org/0000-0002-7821-6392
https://orcid.org/0000-0002-8664-9753
https://orcid.org/0000-0002-6291-0515
https://orcid.org/0000-0002-0851-5610
https://orcid.org/0000-0002-1061-6445
https://orcid.org/0000-0002-1715-3834
https://orcid.org/0000-0002-5695-8256
identifier_str_mv 2314-7156
dc.language.iso.fl_str_mv eng
language eng
dc.relation.ispartof.pt_BR.fl_str_mv Journal of Immunology Research
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Universidade Federal de Minas Gerais
dc.publisher.initials.fl_str_mv UFMG
dc.publisher.country.fl_str_mv Brasil
dc.publisher.department.fl_str_mv ICB - DEPARTAMENTO DE BIOQUÍMICA E IMUNOLOGIA
ICB - DEPARTAMENTO DE FISIOLOGIA E BIOFÍSICA
ICB - DEPARTAMENTO DE MICROBIOLOGIA
publisher.none.fl_str_mv Universidade Federal de Minas Gerais
dc.source.none.fl_str_mv reponame:Repositório Institucional da UFMG
instname:Universidade Federal de Minas Gerais (UFMG)
instacron:UFMG
instname_str Universidade Federal de Minas Gerais (UFMG)
instacron_str UFMG
institution UFMG
reponame_str Repositório Institucional da UFMG
collection Repositório Institucional da UFMG
bitstream.url.fl_str_mv https://repositorio.ufmg.br/bitstream/1843/61233/1/License.txt
https://repositorio.ufmg.br/bitstream/1843/61233/2/Treatment%20with%20distinct%20antibiotic%20classes%20causes%20different%20pulmonary%20outcomes%20on%20allergic%20airway%20inflammation%20associated%20with%20modulation%20of%20symbiotic%20microbiota.pdf
bitstream.checksum.fl_str_mv fa505098d172de0bc8864fc1287ffe22
67a3247da8803b2e6bc3d9f136b144ab
bitstream.checksumAlgorithm.fl_str_mv MD5
MD5
repository.name.fl_str_mv Repositório Institucional da UFMG - Universidade Federal de Minas Gerais (UFMG)
repository.mail.fl_str_mv
_version_ 1803589263628959744