Consumption of diet containing free amino acids exacerbates colitis in mice

Detalhes bibliográficos
Autor(a) principal: Adna Luciana Souza
Data de Publicação: 2017
Outros Autores: Sarah Leão Fiorini Aguiar, Mariana Camila Gonçalves Miranda, Luisa Lemos, Mauro Andrade Freitas Guimaraes, Daniela Silva Reis, Patrícia Aparecida Vieira Barros, Emerson Soares Veloso, Toniana Gonçalves Carvalho, Fabiola Mara Ribeiro, Enio Ferreira, Denise Carmona Cara, Ana Cristina Gomes-Santos, Ana Maria Caetano Faria
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UFMG
Texto Completo: https://doi.org/10.3389/fimmu.2017.01587
http://hdl.handle.net/1843/56408
https://orcid.org/0000-0003-0198-0621
https://orcid.org/0000-0003-2553-8758
https://orcid.org/0000-0002-6475-9222
https://orcid.org/0000-0001-7042-9433
https://orcid.org/0000-0002-1835-0303
https://orcid.org/0000-0002-8748-2764
https://orcid.org/0000-0002-0604-8510
Resumo: Dietary proteins can influence the maturation of the immune system, particularly the gut-associated lymphoid tissue, when consumed from weaning to adulthood. Moreover, replacement of dietary proteins by amino acids at weaning has been shown to impair the generation of regulatory T cells in the gut as well as immune activities such as protective response to infection, induction of oral and nasal tolerance as well as allergic responses. Polymeric and elemental diets are used in the clinical practice, but the specific role of intact proteins and free amino acids during the intestinal inflammation are not known. It is plausible that these two dietary nitrogen sources would yield distinct immunological outcomes since proteins are recognized by the immune system as antigens and amino acids do not bind to antigen-recognition receptors but instead to intracellular receptors such as mammalian target of rapamycin (mTOR). In this study, our aim was to evaluate the effects of consumption of an amino acid-containing diet (AA diet) versus a control protein-containing diet in adult mice at steady state and during colitis development. We showed that consumption of a AA diet by adult mature mice lead to various immunological changes including decrease in the production of serum IgG as well as increase in the levels of IL-6, IL-17A, TGF-β, and IL-10 in the small and large intestines. It also led to changes in the intestinal morphology, to increase in intestinal permeability, in the number of total and activated CD4+ T cells in the small intestine as well as in the frequency of proliferating cells in the colon. Moreover, consumption of AA diet during and prior to development of dextran sodium sulfate-induced colitis exacerbated gut inflammation. Administration of rapamycin during AA diet consumption prevented colitis exacerbation suggesting that mTOR activation was involved in the effects triggered by the AA diet. Therefore, our study suggests that different outcomes can result from the use of diets containing either intact proteins or free amino acids such as elemental, semielemental, and polymeric diets during intestinal inflammation. These results may contribute to the design of nutritional therapeutic intervention for inflammatory bowel diseases.
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spelling 2023-07-17T17:44:18Z2023-07-17T17:44:18Z20178https://doi.org/10.3389/fimmu.2017.015871664-3224http://hdl.handle.net/1843/56408https://orcid.org/0000-0003-0198-0621https://orcid.org/0000-0003-2553-8758https://orcid.org/0000-0002-6475-9222https://orcid.org/0000-0001-7042-9433https://orcid.org/0000-0002-1835-0303https://orcid.org/0000-0002-8748-2764https://orcid.org/0000-0002-0604-8510Dietary proteins can influence the maturation of the immune system, particularly the gut-associated lymphoid tissue, when consumed from weaning to adulthood. Moreover, replacement of dietary proteins by amino acids at weaning has been shown to impair the generation of regulatory T cells in the gut as well as immune activities such as protective response to infection, induction of oral and nasal tolerance as well as allergic responses. Polymeric and elemental diets are used in the clinical practice, but the specific role of intact proteins and free amino acids during the intestinal inflammation are not known. It is plausible that these two dietary nitrogen sources would yield distinct immunological outcomes since proteins are recognized by the immune system as antigens and amino acids do not bind to antigen-recognition receptors but instead to intracellular receptors such as mammalian target of rapamycin (mTOR). In this study, our aim was to evaluate the effects of consumption of an amino acid-containing diet (AA diet) versus a control protein-containing diet in adult mice at steady state and during colitis development. We showed that consumption of a AA diet by adult mature mice lead to various immunological changes including decrease in the production of serum IgG as well as increase in the levels of IL-6, IL-17A, TGF-β, and IL-10 in the small and large intestines. It also led to changes in the intestinal morphology, to increase in intestinal permeability, in the number of total and activated CD4+ T cells in the small intestine as well as in the frequency of proliferating cells in the colon. Moreover, consumption of AA diet during and prior to development of dextran sodium sulfate-induced colitis exacerbated gut inflammation. Administration of rapamycin during AA diet consumption prevented colitis exacerbation suggesting that mTOR activation was involved in the effects triggered by the AA diet. Therefore, our study suggests that different outcomes can result from the use of diets containing either intact proteins or free amino acids such as elemental, semielemental, and polymeric diets during intestinal inflammation. These results may contribute to the design of nutritional therapeutic intervention for inflammatory bowel diseases.As proteínas dietéticas podem influenciar a maturação do sistema imunológico, particularmente o tecido linfóide associado ao intestino, quando consumidas desde o desmame até a idade adulta. Além disso, a substituição de proteínas dietéticas por aminoácidos no desmame demonstrou prejudicar a geração de células T reguladoras no intestino, bem como atividades imunes, como resposta protetora à infecção, indução de tolerância oral e nasal, bem como respostas alérgicas. Dietas poliméricas e elementares são utilizadas na prática clínica, mas o papel específico de proteínas intactas e aminoácidos livres durante a inflamação intestinal não é conhecido. É plausível que essas duas fontes dietéticas de nitrogênio produzam resultados imunológicos distintos, uma vez que as proteínas são reconhecidas pelo sistema imunológico como antígenos e os aminoácidos não se ligam a receptores de reconhecimento de antígenos, mas sim a receptores intracelulares, como o alvo mamífero da rapamicina (mTOR). Neste estudo, nosso objetivo foi avaliar os efeitos do consumo de uma dieta contendo aminoácidos (dieta AA) versus uma dieta contendo proteína controle em camundongos adultos em estado estacionário e durante o desenvolvimento da colite. Mostramos que o consumo de uma dieta AA por camundongos adultos maduros leva a várias alterações imunológicas, incluindo diminuição na produção de IgG sérica, bem como aumento nos níveis de IL-6, IL-17A, TGF-β e IL-10 em os intestinos delgado e grosso. Também levou a alterações na morfologia intestinal, aumento da permeabilidade intestinal, no número de células T CD4+ totais e ativadas no intestino delgado, bem como na frequência de proliferação de células no cólon. Além disso, o consumo de dieta AA durante e antes do desenvolvimento de colite induzida por sulfato de dextrano sódico exacerbou a inflamação intestinal. A administração de rapamicina durante o consumo da dieta AA preveniu a exacerbação da colite, sugerindo que a ativação do mTOR estava envolvida nos efeitos desencadeados pela dieta AA. Portanto, nosso estudo sugere que resultados diferentes podem resultar do uso de dietas contendo proteínas intactas ou aminoácidos livres, como dietas elementares, semielementares e poliméricas durante a inflamação intestinal. Esses resultados podem contribuir para o desenho de intervenção terapêutica nutricional para doenças inflamatórias intestinais.CNPq - Conselho Nacional de Desenvolvimento Científico e TecnológicoFAPEMIG - 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 MORFOLOGIAICB - DEPARTAMENTO DE PATOLOGIAFrontiers in ImmunologyCiências da NutriçãoAminoácidosColiteHomeostaseSirolimoNutritionAmino acidsColitisGut homeostasisMammalian target of rapamycinConsumption of diet containing free amino acids exacerbates colitis in miceConsumo de dieta contendo aminoácidos livres exacerba colite em camundongosinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttps://www.frontiersin.org/articles/10.3389/fimmu.2017.01587/fullAdna Luciana SouzaSarah Leão Fiorini AguiarMariana Camila Gonçalves MirandaLuisa LemosMauro Andrade Freitas GuimaraesDaniela Silva ReisPatrícia Aparecida Vieira BarrosEmerson Soares VelosoToniana Gonçalves CarvalhoFabiola Mara RibeiroEnio FerreiraDenise Carmona CaraAna Cristina Gomes-SantosAna Maria Caetano Fariaapplication/pdfinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UFMGinstname:Universidade Federal de Minas Gerais (UFMG)instacron:UFMGLICENSELicense.txtLicense.txttext/plain; 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dc.title.pt_BR.fl_str_mv Consumption of diet containing free amino acids exacerbates colitis in mice
dc.title.alternative.pt_BR.fl_str_mv Consumo de dieta contendo aminoácidos livres exacerba colite em camundongos
title Consumption of diet containing free amino acids exacerbates colitis in mice
spellingShingle Consumption of diet containing free amino acids exacerbates colitis in mice
Adna Luciana Souza
Nutrition
Amino acids
Colitis
Gut homeostasis
Mammalian target of rapamycin
Ciências da Nutrição
Aminoácidos
Colite
Homeostase
Sirolimo
title_short Consumption of diet containing free amino acids exacerbates colitis in mice
title_full Consumption of diet containing free amino acids exacerbates colitis in mice
title_fullStr Consumption of diet containing free amino acids exacerbates colitis in mice
title_full_unstemmed Consumption of diet containing free amino acids exacerbates colitis in mice
title_sort Consumption of diet containing free amino acids exacerbates colitis in mice
author Adna Luciana Souza
author_facet Adna Luciana Souza
Sarah Leão Fiorini Aguiar
Mariana Camila Gonçalves Miranda
Luisa Lemos
Mauro Andrade Freitas Guimaraes
Daniela Silva Reis
Patrícia Aparecida Vieira Barros
Emerson Soares Veloso
Toniana Gonçalves Carvalho
Fabiola Mara Ribeiro
Enio Ferreira
Denise Carmona Cara
Ana Cristina Gomes-Santos
Ana Maria Caetano Faria
author_role author
author2 Sarah Leão Fiorini Aguiar
Mariana Camila Gonçalves Miranda
Luisa Lemos
Mauro Andrade Freitas Guimaraes
Daniela Silva Reis
Patrícia Aparecida Vieira Barros
Emerson Soares Veloso
Toniana Gonçalves Carvalho
Fabiola Mara Ribeiro
Enio Ferreira
Denise Carmona Cara
Ana Cristina Gomes-Santos
Ana Maria Caetano Faria
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Adna Luciana Souza
Sarah Leão Fiorini Aguiar
Mariana Camila Gonçalves Miranda
Luisa Lemos
Mauro Andrade Freitas Guimaraes
Daniela Silva Reis
Patrícia Aparecida Vieira Barros
Emerson Soares Veloso
Toniana Gonçalves Carvalho
Fabiola Mara Ribeiro
Enio Ferreira
Denise Carmona Cara
Ana Cristina Gomes-Santos
Ana Maria Caetano Faria
dc.subject.por.fl_str_mv Nutrition
Amino acids
Colitis
Gut homeostasis
Mammalian target of rapamycin
topic Nutrition
Amino acids
Colitis
Gut homeostasis
Mammalian target of rapamycin
Ciências da Nutrição
Aminoácidos
Colite
Homeostase
Sirolimo
dc.subject.other.pt_BR.fl_str_mv Ciências da Nutrição
Aminoácidos
Colite
Homeostase
Sirolimo
description Dietary proteins can influence the maturation of the immune system, particularly the gut-associated lymphoid tissue, when consumed from weaning to adulthood. Moreover, replacement of dietary proteins by amino acids at weaning has been shown to impair the generation of regulatory T cells in the gut as well as immune activities such as protective response to infection, induction of oral and nasal tolerance as well as allergic responses. Polymeric and elemental diets are used in the clinical practice, but the specific role of intact proteins and free amino acids during the intestinal inflammation are not known. It is plausible that these two dietary nitrogen sources would yield distinct immunological outcomes since proteins are recognized by the immune system as antigens and amino acids do not bind to antigen-recognition receptors but instead to intracellular receptors such as mammalian target of rapamycin (mTOR). In this study, our aim was to evaluate the effects of consumption of an amino acid-containing diet (AA diet) versus a control protein-containing diet in adult mice at steady state and during colitis development. We showed that consumption of a AA diet by adult mature mice lead to various immunological changes including decrease in the production of serum IgG as well as increase in the levels of IL-6, IL-17A, TGF-β, and IL-10 in the small and large intestines. It also led to changes in the intestinal morphology, to increase in intestinal permeability, in the number of total and activated CD4+ T cells in the small intestine as well as in the frequency of proliferating cells in the colon. Moreover, consumption of AA diet during and prior to development of dextran sodium sulfate-induced colitis exacerbated gut inflammation. Administration of rapamycin during AA diet consumption prevented colitis exacerbation suggesting that mTOR activation was involved in the effects triggered by the AA diet. Therefore, our study suggests that different outcomes can result from the use of diets containing either intact proteins or free amino acids such as elemental, semielemental, and polymeric diets during intestinal inflammation. These results may contribute to the design of nutritional therapeutic intervention for inflammatory bowel diseases.
publishDate 2017
dc.date.issued.fl_str_mv 2017
dc.date.accessioned.fl_str_mv 2023-07-17T17:44:18Z
dc.date.available.fl_str_mv 2023-07-17T17:44:18Z
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/1843/56408
dc.identifier.doi.pt_BR.fl_str_mv https://doi.org/10.3389/fimmu.2017.01587
dc.identifier.issn.pt_BR.fl_str_mv 1664-3224
dc.identifier.orcid.pt_BR.fl_str_mv https://orcid.org/0000-0003-0198-0621
https://orcid.org/0000-0003-2553-8758
https://orcid.org/0000-0002-6475-9222
https://orcid.org/0000-0001-7042-9433
https://orcid.org/0000-0002-1835-0303
https://orcid.org/0000-0002-8748-2764
https://orcid.org/0000-0002-0604-8510
url https://doi.org/10.3389/fimmu.2017.01587
http://hdl.handle.net/1843/56408
https://orcid.org/0000-0003-0198-0621
https://orcid.org/0000-0003-2553-8758
https://orcid.org/0000-0002-6475-9222
https://orcid.org/0000-0001-7042-9433
https://orcid.org/0000-0002-1835-0303
https://orcid.org/0000-0002-8748-2764
https://orcid.org/0000-0002-0604-8510
identifier_str_mv 1664-3224
dc.language.iso.fl_str_mv eng
language eng
dc.relation.ispartof.pt_BR.fl_str_mv Frontiers in Immunology
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eu_rights_str_mv openAccess
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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 MORFOLOGIA
ICB - DEPARTAMENTO DE PATOLOGIA
publisher.none.fl_str_mv Universidade Federal de Minas Gerais
dc.source.none.fl_str_mv reponame:Repositório Institucional da UFMG
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