Consumption of Diet Containing Free Amino Acids Exacerbates Colitis in Mice

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 a...

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Main Authors: 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
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-11-01
Series:Frontiers in Immunology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fimmu.2017.01587/full
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author Adna Luciana Souza
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 Cristina Gomes-Santos
Ana Maria Caetano Faria
author_facet Adna Luciana Souza
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 Cristina Gomes-Santos
Ana Maria Caetano Faria
author_sort Adna Luciana Souza
collection DOAJ
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.
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spelling doaj.art-c12f95cba41e47e7b7f0dc192076de5b2022-12-22T02:33:47ZengFrontiers Media S.A.Frontiers in Immunology1664-32242017-11-01810.3389/fimmu.2017.01587248857Consumption of Diet Containing Free Amino Acids Exacerbates Colitis in MiceAdna Luciana Souza0Adna Luciana Souza1Sarah Leão Fiorini Aguiar2Mariana Camila Gonçalves Miranda3Luisa Lemos4Mauro Andrade Freitas Guimaraes5Daniela Silva Reis6Patrícia Aparecida Vieira Barros7Emerson Soares Veloso8Toniana Gonçalves Carvalho9Fabiola Mara Ribeiro10Enio Ferreira11Denise Carmona Cara12Ana Cristina Gomes-Santos13Ana Cristina Gomes-Santos14Ana Maria Caetano Faria15Departamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilCentro das Ciências Biológicas e da Saúde, Universidade Federal do Oeste da Bahia, Barreiras, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Patologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Patologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilCentro Universitário UNA, Belo Horizonte, BrazilDepartamento de Bioquímica e Imunologia, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDietary 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.http://journal.frontiersin.org/article/10.3389/fimmu.2017.01587/fullnutritionamino acidscolitisgut homeostasismammalian target of rapamycin
spellingShingle Adna Luciana Souza
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 Cristina Gomes-Santos
Ana Maria Caetano Faria
Consumption of Diet Containing Free Amino Acids Exacerbates Colitis in Mice
Frontiers in Immunology
nutrition
amino acids
colitis
gut homeostasis
mammalian target of rapamycin
title 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_short Consumption of Diet Containing Free Amino Acids Exacerbates Colitis in Mice
title_sort consumption of diet containing free amino acids exacerbates colitis in mice
topic nutrition
amino acids
colitis
gut homeostasis
mammalian target of rapamycin
url http://journal.frontiersin.org/article/10.3389/fimmu.2017.01587/full
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