Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response

Detalhes bibliográficos
Autor(a) principal: Miranda, Farlen José Bebber
Data de Publicação: 2021
Outros Autores: Rocha, Bruno Coelho, Almeida, Milton Cesar De, Pereira, Larissa Marina Nogueira, Souza, Erikson Henrique Martins De, Marino, Ana Paula Maia Peixoto, Costa, Pedro Augusto Carvalho, Santos, Daniel V. Vasconcelos, Antonelli, Lis Ribeiro do Valle, Gazzinelli, Ricardo Tostes
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da FIOCRUZ (ARCA)
Texto Completo: https://www.arca.fiocruz.br/handle/icict/56005
Resumo: Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil.
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spelling Miranda, Farlen José BebberRocha, Bruno CoelhoAlmeida, Milton Cesar DePereira, Larissa Marina NogueiraSouza, Erikson Henrique Martins DeMarino, Ana Paula Maia PeixotoCosta, Pedro Augusto CarvalhoSantos, Daniel V. VasconcelosAntonelli, Lis Ribeiro do ValleGazzinelli, Ricardo Tostes2022-12-16T13:20:55Z2022-12-16T13:20:55Z2021MIRANDA Farlen José Bebber , et al. Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response. mBio, v. 12, n. 5, e0130721, 2021. doi: 10.1128/mBio.01307-21.2150-7511https://www.arca.fiocruz.br/handle/icict/56005engAmerican Society for MicrobiologyToxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Responseinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleFundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil.Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil.Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil/Department of Medicine. University of Massachusetts Medical Schoolgrid. Worcester, MA, USA.Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil/Universidade Federal de Minas Gerais. Departamento de Bioquímica e Imunologia. Belo Horizonte, MG, Brazil.Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil.Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil.Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil.Universidade Federal de Minas Gerais. Faculdade de Medicina. Departamento de Oftalmologia e Otorrinolaringologia. Belo Horizonte, MG, Brazil.Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil.Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil/Department of Medicine. University of Massachusetts Medical Schoolgrid. Worcester, MA, USA/Universidade Federal de Minas Gerais. Departamento de Bioquímica e Imunologia. Belo Horizonte, MG, Brazil.Toxoplasmosis affects one-third of the human population worldwide. Humans are accidental hosts and are infected after consumption of undercooked meat and water contaminated with Toxoplasma gondii cysts and oocysts, respectively. Neutrophils have been shown to participate in the control of T. gondii infection in mice through a variety of effector mechanisms, such as reactive oxygen species (ROS) and neutrophil extracellular trap (NET) formation. However, few studies have demonstrated the role of neutrophils in individuals naturally infected with T. gondii. In the current study, we evaluated the activation status of neutrophils in individuals with acute or chronic toxoplasmosis and determined the role of T. gondii-induced NET formation in the amplification of the innate and adaptive immune responses. We observed that neutrophils are highly activated during acute infection through increased expression of CD66b. Moreover, neutrophils from healthy donors (HDs) cocultured with tachyzoites produced ROS and formed NETs, with the latter being dependent on glycolysis, succinate dehydrogenase, gasdermin D, and neutrophil elastase. Furthermore, we observed elevated levels of the chemokines (CXC motif) CXCL8 and (CC motif) CCL4 ligands in plasma from patients with acute toxoplasmosis and production by neutrophils from HDs exposed to T. gondii. Finally, we showed that T. gondii-induced NETs activate neutrophils and promote the recruitment of autologous CD4+ T cells and the production of interferon gamma (IFN-γ), tumor necrosis factor (TNF), interleukin 6 (IL-6), IL-17, and IL-10 by peripheral blood mononuclear cells. In conclusion, we demonstrated that T. gondii activates neutrophils and promotes the release of NETs, which amplify human innate and adaptive immune responses. IMPORTANCE Approximately one-third of the human population is estimated to be chronically infected with the obligate intracellular parasite Toxoplasma gondii. Humans are accidental hosts that are infected with T. gondii after consumption of undercooked meat or contaminated water. Neutrophils have been shown to control T. gondii growth by different mechanisms, including neutrophil extracellular traps (NETs). In the current study, we observed that neutrophils are highly activated during acute toxoplasmosis. We also determined that T. gondii-induced NETs are dependent on the energetic profile of neutrophils as well as the production of ROS and gasdermin D (GSDMD) cleavage. In addition, we showed that T. gondii-induced NETs activate neutrophils, promote the recruitment of autologous CD4+ T cells, and induce the production of cytokines by peripheral blood mononuclear cells, amplifying the innate and adaptive immune responses.NETToxoplasma gondiineutrophilsinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da FIOCRUZ (ARCA)instname:Fundação Oswaldo Cruz (FIOCRUZ)instacron:FIOCRUZLICENSElicense.txtlicense.txttext/plain; charset=utf-82991https://www.arca.fiocruz.br/bitstream/icict/56005/1/license.txt5a560609d32a3863062d77ff32785d58MD51ORIGINALToxoplasma gondii-Induced Neutrophil Extracellular.pdfToxoplasma gondii-Induced Neutrophil Extracellular.pdfapplication/pdf3553640https://www.arca.fiocruz.br/bitstream/icict/56005/2/Toxoplasma%20gondii-Induced%20Neutrophil%20Extracellular.pdfe48a6d73175111f2fc2ab87604268ce1MD52icict/560052022-12-16 10:20:57.216oai:www.arca.fiocruz.br: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ório 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dc.title.en_US.fl_str_mv Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response
title Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response
spellingShingle Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response
Miranda, Farlen José Bebber
NET
Toxoplasma gondii
neutrophils
title_short Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response
title_full Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response
title_fullStr Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response
title_full_unstemmed Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response
title_sort Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response
author Miranda, Farlen José Bebber
author_facet Miranda, Farlen José Bebber
Rocha, Bruno Coelho
Almeida, Milton Cesar De
Pereira, Larissa Marina Nogueira
Souza, Erikson Henrique Martins De
Marino, Ana Paula Maia Peixoto
Costa, Pedro Augusto Carvalho
Santos, Daniel V. Vasconcelos
Antonelli, Lis Ribeiro do Valle
Gazzinelli, Ricardo Tostes
author_role author
author2 Rocha, Bruno Coelho
Almeida, Milton Cesar De
Pereira, Larissa Marina Nogueira
Souza, Erikson Henrique Martins De
Marino, Ana Paula Maia Peixoto
Costa, Pedro Augusto Carvalho
Santos, Daniel V. Vasconcelos
Antonelli, Lis Ribeiro do Valle
Gazzinelli, Ricardo Tostes
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Miranda, Farlen José Bebber
Rocha, Bruno Coelho
Almeida, Milton Cesar De
Pereira, Larissa Marina Nogueira
Souza, Erikson Henrique Martins De
Marino, Ana Paula Maia Peixoto
Costa, Pedro Augusto Carvalho
Santos, Daniel V. Vasconcelos
Antonelli, Lis Ribeiro do Valle
Gazzinelli, Ricardo Tostes
dc.subject.en.en_US.fl_str_mv NET
Toxoplasma gondii
neutrophils
topic NET
Toxoplasma gondii
neutrophils
description Fundação Oswaldo Cruz. Instituto Rene Rachou. Belo Horizonte, MG, Brazil.
publishDate 2021
dc.date.issued.fl_str_mv 2021
dc.date.accessioned.fl_str_mv 2022-12-16T13:20:55Z
dc.date.available.fl_str_mv 2022-12-16T13:20:55Z
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.citation.fl_str_mv MIRANDA Farlen José Bebber , et al. Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response. mBio, v. 12, n. 5, e0130721, 2021. doi: 10.1128/mBio.01307-21.
dc.identifier.uri.fl_str_mv https://www.arca.fiocruz.br/handle/icict/56005
dc.identifier.issn.en_US.fl_str_mv 2150-7511
identifier_str_mv MIRANDA Farlen José Bebber , et al. Toxoplasma gondii-Induced Neutrophil Extracellular Traps Amplify the Innate and Adaptive Response. mBio, v. 12, n. 5, e0130721, 2021. doi: 10.1128/mBio.01307-21.
2150-7511
url https://www.arca.fiocruz.br/handle/icict/56005
dc.language.iso.fl_str_mv eng
language eng
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:Repositório Institucional da FIOCRUZ (ARCA)
instname:Fundação Oswaldo Cruz (FIOCRUZ)
instacron:FIOCRUZ
instname_str Fundação Oswaldo Cruz (FIOCRUZ)
instacron_str FIOCRUZ
institution FIOCRUZ
reponame_str Repositório Institucional da FIOCRUZ (ARCA)
collection Repositório Institucional da FIOCRUZ (ARCA)
bitstream.url.fl_str_mv https://www.arca.fiocruz.br/bitstream/icict/56005/1/license.txt
https://www.arca.fiocruz.br/bitstream/icict/56005/2/Toxoplasma%20gondii-Induced%20Neutrophil%20Extracellular.pdf
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repository.name.fl_str_mv Repositório Institucional da FIOCRUZ (ARCA) - Fundação Oswaldo Cruz (FIOCRUZ)
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