Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation

Autores
Schachter, Julieta; De Oliveira, Dayane Alvarinho; Da Silva, Camila Marques; De Barros Alencar, Alba Cristina Miranda; Duarte, Michelle; Müller Pereira da Silva, Matheus; De Paula Rosa Ignácio, Ana Claudia; Lopes Torres, Eduardo José
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Infections with Trichuris trichiura are among the most common causes of intestinal parasitism in children worldwide, and the diagnosis is based on microscopic egg identification in the chronic phase of the infection. During parasitism, the adult worm of the trichurid nematode maintains its anterior region inserted in the intestinal mucosa, which causes serious damage and which may open access for gut microorganisms through the intestinal tissue. The immune-regulatory processes taking place during the evolution of the chronic infection are still not completely understood. By use of the Swiss Webster outbred mouse model, mice were infected with 200 eggs, and tolerance to the establishment of a chronic Trichuris muris infection was induced by the administration of a short pulse of dexamethasone during nematode early larval development. The infected mice presented weight loss, anemia, an imbalance of the microbiota, and intense immunological cell infiltration in the large intestine. It was found that mice have a mixed Th1/Th2/Th17 response, with differences being found among the different anatomical locations. After 45 days of infection, the parasitism induced changes in the microbiota composition and bacterial invasion of the large intestine epithelium. In addition, we describe that the excretory-secretory products from the nematode have anti-inflammatory effects on mouse macrophages cultured in vitro, suggesting that T. muris may modulate the immune response at the site of insertion of the worm inside mouse tissue. The data presented in this study suggest that the host immune state at 45 days postinfection with T. muris during the chronic phase of infection is the result of factors derived from the worm as well as alterations to the microbiota and bacterial invasion. Taken together, these results provide new information about the parasite-host-microbiota relationship and open new treatment possibilities.
Fil: Schachter, Julieta. Universidade Federal do Rio de Janeiro; Brasil. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Química y Físico-Química Biológicas "Prof. Alejandro C. Paladini". Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Instituto de Química y Físico-Química Biológicas; Argentina
Fil: De Oliveira, Dayane Alvarinho. Universidade do Estado de Rio do Janeiro; Brasil
Fil: Da Silva, Camila Marques. Universidade Federal do Rio de Janeiro; Brasil
Fil: De Barros Alencar, Alba Cristina Miranda. Hospital Universitario Antonio Pedro; Brasil
Fil: Duarte, Michelle. Universidade Federal do Rio de Janeiro; Brasil
Fil: Müller Pereira da Silva, Matheus. Universidade Federal do Rio de Janeiro; Brasil
Fil: De Paula Rosa Ignácio, Ana Claudia. Universidade do Estado de Rio do Janeiro; Brasil
Fil: Lopes Torres, Eduardo José. Universidade do Estado de Rio do Janeiro; Brasil
Materia
EXCRETORY-SECRETORY
EXCRETORYSECRETORY PRODUCTS
HELMINTH
IMMUNE RESPONSE
INFECTIOUS DISEASE
INTESTINE
INTESTINE
MICROBIOTA
NEGLECTED DISEASE
NEMATODES
TRICHURIS
TRICHURIS MURIS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/149182

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oai_identifier_str oai:ri.conicet.gov.ar:11336/149182
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulationSchachter, JulietaDe Oliveira, Dayane AlvarinhoDa Silva, Camila MarquesDe Barros Alencar, Alba Cristina MirandaDuarte, MichelleMüller Pereira da Silva, MatheusDe Paula Rosa Ignácio, Ana ClaudiaLopes Torres, Eduardo JoséEXCRETORY-SECRETORYEXCRETORYSECRETORY PRODUCTSHELMINTHIMMUNE RESPONSEINFECTIOUS DISEASEINTESTINEINTESTINEMICROBIOTANEGLECTED DISEASENEMATODESTRICHURISTRICHURIS MURIShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Infections with Trichuris trichiura are among the most common causes of intestinal parasitism in children worldwide, and the diagnosis is based on microscopic egg identification in the chronic phase of the infection. During parasitism, the adult worm of the trichurid nematode maintains its anterior region inserted in the intestinal mucosa, which causes serious damage and which may open access for gut microorganisms through the intestinal tissue. The immune-regulatory processes taking place during the evolution of the chronic infection are still not completely understood. By use of the Swiss Webster outbred mouse model, mice were infected with 200 eggs, and tolerance to the establishment of a chronic Trichuris muris infection was induced by the administration of a short pulse of dexamethasone during nematode early larval development. The infected mice presented weight loss, anemia, an imbalance of the microbiota, and intense immunological cell infiltration in the large intestine. It was found that mice have a mixed Th1/Th2/Th17 response, with differences being found among the different anatomical locations. After 45 days of infection, the parasitism induced changes in the microbiota composition and bacterial invasion of the large intestine epithelium. In addition, we describe that the excretory-secretory products from the nematode have anti-inflammatory effects on mouse macrophages cultured in vitro, suggesting that T. muris may modulate the immune response at the site of insertion of the worm inside mouse tissue. The data presented in this study suggest that the host immune state at 45 days postinfection with T. muris during the chronic phase of infection is the result of factors derived from the worm as well as alterations to the microbiota and bacterial invasion. Taken together, these results provide new information about the parasite-host-microbiota relationship and open new treatment possibilities.Fil: Schachter, Julieta. Universidade Federal do Rio de Janeiro; Brasil. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Química y Físico-Química Biológicas "Prof. Alejandro C. Paladini". Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Instituto de Química y Físico-Química Biológicas; ArgentinaFil: De Oliveira, Dayane Alvarinho. Universidade do Estado de Rio do Janeiro; BrasilFil: Da Silva, Camila Marques. Universidade Federal do Rio de Janeiro; BrasilFil: De Barros Alencar, Alba Cristina Miranda. Hospital Universitario Antonio Pedro; BrasilFil: Duarte, Michelle. Universidade Federal do Rio de Janeiro; BrasilFil: Müller Pereira da Silva, Matheus. Universidade Federal do Rio de Janeiro; BrasilFil: De Paula Rosa Ignácio, Ana Claudia. Universidade do Estado de Rio do Janeiro; BrasilFil: Lopes Torres, Eduardo José. Universidade do Estado de Rio do Janeiro; BrasilAmerican Society for Microbiology2020-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/149182Schachter, Julieta; De Oliveira, Dayane Alvarinho; Da Silva, Camila Marques; De Barros Alencar, Alba Cristina Miranda; Duarte, Michelle; et al.; Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation; American Society for Microbiology; Infection and Immunity; 88; 3; 3-2020; 1-240019-9567CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1128/IAI.00642-19info:eu-repo/semantics/altIdentifier/url/https://journals.asm.org/doi/10.1128/IAI.00642-19info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:43:44Zoai:ri.conicet.gov.ar:11336/149182instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:43:44.883CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation
title Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation
spellingShingle Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation
Schachter, Julieta
EXCRETORY-SECRETORY
EXCRETORYSECRETORY PRODUCTS
HELMINTH
IMMUNE RESPONSE
INFECTIOUS DISEASE
INTESTINE
INTESTINE
MICROBIOTA
NEGLECTED DISEASE
NEMATODES
TRICHURIS
TRICHURIS MURIS
title_short Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation
title_full Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation
title_fullStr Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation
title_full_unstemmed Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation
title_sort Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation
dc.creator.none.fl_str_mv Schachter, Julieta
De Oliveira, Dayane Alvarinho
Da Silva, Camila Marques
De Barros Alencar, Alba Cristina Miranda
Duarte, Michelle
Müller Pereira da Silva, Matheus
De Paula Rosa Ignácio, Ana Claudia
Lopes Torres, Eduardo José
author Schachter, Julieta
author_facet Schachter, Julieta
De Oliveira, Dayane Alvarinho
Da Silva, Camila Marques
De Barros Alencar, Alba Cristina Miranda
Duarte, Michelle
Müller Pereira da Silva, Matheus
De Paula Rosa Ignácio, Ana Claudia
Lopes Torres, Eduardo José
author_role author
author2 De Oliveira, Dayane Alvarinho
Da Silva, Camila Marques
De Barros Alencar, Alba Cristina Miranda
Duarte, Michelle
Müller Pereira da Silva, Matheus
De Paula Rosa Ignácio, Ana Claudia
Lopes Torres, Eduardo José
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv EXCRETORY-SECRETORY
EXCRETORYSECRETORY PRODUCTS
HELMINTH
IMMUNE RESPONSE
INFECTIOUS DISEASE
INTESTINE
INTESTINE
MICROBIOTA
NEGLECTED DISEASE
NEMATODES
TRICHURIS
TRICHURIS MURIS
topic EXCRETORY-SECRETORY
EXCRETORYSECRETORY PRODUCTS
HELMINTH
IMMUNE RESPONSE
INFECTIOUS DISEASE
INTESTINE
INTESTINE
MICROBIOTA
NEGLECTED DISEASE
NEMATODES
TRICHURIS
TRICHURIS MURIS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Infections with Trichuris trichiura are among the most common causes of intestinal parasitism in children worldwide, and the diagnosis is based on microscopic egg identification in the chronic phase of the infection. During parasitism, the adult worm of the trichurid nematode maintains its anterior region inserted in the intestinal mucosa, which causes serious damage and which may open access for gut microorganisms through the intestinal tissue. The immune-regulatory processes taking place during the evolution of the chronic infection are still not completely understood. By use of the Swiss Webster outbred mouse model, mice were infected with 200 eggs, and tolerance to the establishment of a chronic Trichuris muris infection was induced by the administration of a short pulse of dexamethasone during nematode early larval development. The infected mice presented weight loss, anemia, an imbalance of the microbiota, and intense immunological cell infiltration in the large intestine. It was found that mice have a mixed Th1/Th2/Th17 response, with differences being found among the different anatomical locations. After 45 days of infection, the parasitism induced changes in the microbiota composition and bacterial invasion of the large intestine epithelium. In addition, we describe that the excretory-secretory products from the nematode have anti-inflammatory effects on mouse macrophages cultured in vitro, suggesting that T. muris may modulate the immune response at the site of insertion of the worm inside mouse tissue. The data presented in this study suggest that the host immune state at 45 days postinfection with T. muris during the chronic phase of infection is the result of factors derived from the worm as well as alterations to the microbiota and bacterial invasion. Taken together, these results provide new information about the parasite-host-microbiota relationship and open new treatment possibilities.
Fil: Schachter, Julieta. Universidade Federal do Rio de Janeiro; Brasil. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Química y Físico-Química Biológicas "Prof. Alejandro C. Paladini". Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Instituto de Química y Físico-Química Biológicas; Argentina
Fil: De Oliveira, Dayane Alvarinho. Universidade do Estado de Rio do Janeiro; Brasil
Fil: Da Silva, Camila Marques. Universidade Federal do Rio de Janeiro; Brasil
Fil: De Barros Alencar, Alba Cristina Miranda. Hospital Universitario Antonio Pedro; Brasil
Fil: Duarte, Michelle. Universidade Federal do Rio de Janeiro; Brasil
Fil: Müller Pereira da Silva, Matheus. Universidade Federal do Rio de Janeiro; Brasil
Fil: De Paula Rosa Ignácio, Ana Claudia. Universidade do Estado de Rio do Janeiro; Brasil
Fil: Lopes Torres, Eduardo José. Universidade do Estado de Rio do Janeiro; Brasil
description Infections with Trichuris trichiura are among the most common causes of intestinal parasitism in children worldwide, and the diagnosis is based on microscopic egg identification in the chronic phase of the infection. During parasitism, the adult worm of the trichurid nematode maintains its anterior region inserted in the intestinal mucosa, which causes serious damage and which may open access for gut microorganisms through the intestinal tissue. The immune-regulatory processes taking place during the evolution of the chronic infection are still not completely understood. By use of the Swiss Webster outbred mouse model, mice were infected with 200 eggs, and tolerance to the establishment of a chronic Trichuris muris infection was induced by the administration of a short pulse of dexamethasone during nematode early larval development. The infected mice presented weight loss, anemia, an imbalance of the microbiota, and intense immunological cell infiltration in the large intestine. It was found that mice have a mixed Th1/Th2/Th17 response, with differences being found among the different anatomical locations. After 45 days of infection, the parasitism induced changes in the microbiota composition and bacterial invasion of the large intestine epithelium. In addition, we describe that the excretory-secretory products from the nematode have anti-inflammatory effects on mouse macrophages cultured in vitro, suggesting that T. muris may modulate the immune response at the site of insertion of the worm inside mouse tissue. The data presented in this study suggest that the host immune state at 45 days postinfection with T. muris during the chronic phase of infection is the result of factors derived from the worm as well as alterations to the microbiota and bacterial invasion. Taken together, these results provide new information about the parasite-host-microbiota relationship and open new treatment possibilities.
publishDate 2020
dc.date.none.fl_str_mv 2020-03
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/149182
Schachter, Julieta; De Oliveira, Dayane Alvarinho; Da Silva, Camila Marques; De Barros Alencar, Alba Cristina Miranda; Duarte, Michelle; et al.; Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation; American Society for Microbiology; Infection and Immunity; 88; 3; 3-2020; 1-24
0019-9567
CONICET Digital
CONICET
url http://hdl.handle.net/11336/149182
identifier_str_mv Schachter, Julieta; De Oliveira, Dayane Alvarinho; Da Silva, Camila Marques; De Barros Alencar, Alba Cristina Miranda; Duarte, Michelle; et al.; Whipworm infection promotes bacterial invasion, intestinal microbiota imbalance, and cellular immunomodulation; American Society for Microbiology; Infection and Immunity; 88; 3; 3-2020; 1-24
0019-9567
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1128/IAI.00642-19
info:eu-repo/semantics/altIdentifier/url/https://journals.asm.org/doi/10.1128/IAI.00642-19
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
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:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432