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Steamed broccoli sprouts alleviate DSS-induced inflammation and retain gut microbial biogeography in mice

Inflammatory bowel diseases (IBDs) are devastating conditions of the gastrointestinal tract with limited treatments, and dietary intervention may be effective and affordable for managing symptoms. Glucosinolate compounds are highly concentrated in broccoli sprouts, especially glucoraphanin (GLR), an...

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Autores principales: Holman, Johanna M., Colucci, Louisa, Baudewyns, Dorien, Balkan, Joe, Hunt, Timothy, Hunt, Benjamin, Kinney, Marissa, Holcomb, Lola, Stratigakis, Allesandra, Chen, Grace, Moses, Peter L., Mawe, Gary M., Zhang, Tao, Li, Yanyan, Ishaq, Suzanne L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10654075/
https://www.ncbi.nlm.nih.gov/pubmed/37702510
http://dx.doi.org/10.1128/msystems.00532-23
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author Holman, Johanna M.
Colucci, Louisa
Baudewyns, Dorien
Balkan, Joe
Hunt, Timothy
Hunt, Benjamin
Kinney, Marissa
Holcomb, Lola
Stratigakis, Allesandra
Chen, Grace
Moses, Peter L.
Mawe, Gary M.
Zhang, Tao
Li, Yanyan
Ishaq, Suzanne L.
author_facet Holman, Johanna M.
Colucci, Louisa
Baudewyns, Dorien
Balkan, Joe
Hunt, Timothy
Hunt, Benjamin
Kinney, Marissa
Holcomb, Lola
Stratigakis, Allesandra
Chen, Grace
Moses, Peter L.
Mawe, Gary M.
Zhang, Tao
Li, Yanyan
Ishaq, Suzanne L.
author_sort Holman, Johanna M.
collection PubMed
description Inflammatory bowel diseases (IBDs) are devastating conditions of the gastrointestinal tract with limited treatments, and dietary intervention may be effective and affordable for managing symptoms. Glucosinolate compounds are highly concentrated in broccoli sprouts, especially glucoraphanin (GLR), and can be metabolized by certain mammalian gut bacteria into anti-inflammatory isothiocyanates, such as sulforaphane. Gut microbiota exhibit biogeographic patterns, but it is unknown if colitis alters these or whether the location of glucoraphanin-metabolizing bacteria affects anti-inflammatory benefits. We fed specific pathogen-free C57BL/6 mice either a control diet or a 10% steamed broccoli sprout diet and gave a three-cycle regimen of 2.5% dextran sodium sulfate (DSS) in drinking water over a 34-day experiment to simulate chronic, relapsing ulcerative colitis (UC). We monitored body weight, fecal characteristics, lipocalin, serum cytokines, and bacterial communities from the luminal- and mucosal-associated populations in the jejunum, cecum, and colon. Mice fed the broccoli sprout diet with DSS treatment performed better than mice fed the control diet with DSS, and had significantly more weight gain, lower Disease Activity Index scores, lower plasma lipocalin and proinflammatory cytokines, and higher bacterial richness in all gut locations. Bacterial communities were assorted by gut location but were more homogenous across locations in the control diet + DSS mice. Importantly, our results showed that broccoli sprout feeding abrogated the effects of DSS on gut microbiota, as bacterial richness and biogeography were similar between mice receiving broccoli sprouts with and without DSS. Collectively, these results support the protective effect of steamed broccoli sprouts against dysbiosis and colitis induced by DSS. IMPORTANCE: Evaluating bacterial communities across different locations in the gut provides a greater insight than fecal samples alone and provides an additional metric by which to evaluate beneficial host-microbe interactions. Here, we show that 10% steamed broccoli sprouts in the diet protects mice from the negative effects of dextran sodium sulfate-induced colitis, that colitis erases biogeographic patterns of bacterial communities in the gut, and that the cecum is not likely to be a significant contributor to colonic bacteria of interest in the DSS mouse model of ulcerative colitis. Mice fed the broccoli sprout diet during colitis performed better than mice fed the control diet while receiving DSS. The identification of accessible dietary components and concentrations that help maintain and correct the gut microbiome may provide universal and equitable approaches to IBD prevention and recovery, and broccoli sprouts represent a promising strategy.
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spelling pubmed-106540752023-09-13 Steamed broccoli sprouts alleviate DSS-induced inflammation and retain gut microbial biogeography in mice Holman, Johanna M. Colucci, Louisa Baudewyns, Dorien Balkan, Joe Hunt, Timothy Hunt, Benjamin Kinney, Marissa Holcomb, Lola Stratigakis, Allesandra Chen, Grace Moses, Peter L. Mawe, Gary M. Zhang, Tao Li, Yanyan Ishaq, Suzanne L. mSystems Research Article Inflammatory bowel diseases (IBDs) are devastating conditions of the gastrointestinal tract with limited treatments, and dietary intervention may be effective and affordable for managing symptoms. Glucosinolate compounds are highly concentrated in broccoli sprouts, especially glucoraphanin (GLR), and can be metabolized by certain mammalian gut bacteria into anti-inflammatory isothiocyanates, such as sulforaphane. Gut microbiota exhibit biogeographic patterns, but it is unknown if colitis alters these or whether the location of glucoraphanin-metabolizing bacteria affects anti-inflammatory benefits. We fed specific pathogen-free C57BL/6 mice either a control diet or a 10% steamed broccoli sprout diet and gave a three-cycle regimen of 2.5% dextran sodium sulfate (DSS) in drinking water over a 34-day experiment to simulate chronic, relapsing ulcerative colitis (UC). We monitored body weight, fecal characteristics, lipocalin, serum cytokines, and bacterial communities from the luminal- and mucosal-associated populations in the jejunum, cecum, and colon. Mice fed the broccoli sprout diet with DSS treatment performed better than mice fed the control diet with DSS, and had significantly more weight gain, lower Disease Activity Index scores, lower plasma lipocalin and proinflammatory cytokines, and higher bacterial richness in all gut locations. Bacterial communities were assorted by gut location but were more homogenous across locations in the control diet + DSS mice. Importantly, our results showed that broccoli sprout feeding abrogated the effects of DSS on gut microbiota, as bacterial richness and biogeography were similar between mice receiving broccoli sprouts with and without DSS. Collectively, these results support the protective effect of steamed broccoli sprouts against dysbiosis and colitis induced by DSS. IMPORTANCE: Evaluating bacterial communities across different locations in the gut provides a greater insight than fecal samples alone and provides an additional metric by which to evaluate beneficial host-microbe interactions. Here, we show that 10% steamed broccoli sprouts in the diet protects mice from the negative effects of dextran sodium sulfate-induced colitis, that colitis erases biogeographic patterns of bacterial communities in the gut, and that the cecum is not likely to be a significant contributor to colonic bacteria of interest in the DSS mouse model of ulcerative colitis. Mice fed the broccoli sprout diet during colitis performed better than mice fed the control diet while receiving DSS. The identification of accessible dietary components and concentrations that help maintain and correct the gut microbiome may provide universal and equitable approaches to IBD prevention and recovery, and broccoli sprouts represent a promising strategy. American Society for Microbiology 2023-09-13 /pmc/articles/PMC10654075/ /pubmed/37702510 http://dx.doi.org/10.1128/msystems.00532-23 Text en Copyright © 2023 Holman et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Holman, Johanna M.
Colucci, Louisa
Baudewyns, Dorien
Balkan, Joe
Hunt, Timothy
Hunt, Benjamin
Kinney, Marissa
Holcomb, Lola
Stratigakis, Allesandra
Chen, Grace
Moses, Peter L.
Mawe, Gary M.
Zhang, Tao
Li, Yanyan
Ishaq, Suzanne L.
Steamed broccoli sprouts alleviate DSS-induced inflammation and retain gut microbial biogeography in mice
title Steamed broccoli sprouts alleviate DSS-induced inflammation and retain gut microbial biogeography in mice
title_full Steamed broccoli sprouts alleviate DSS-induced inflammation and retain gut microbial biogeography in mice
title_fullStr Steamed broccoli sprouts alleviate DSS-induced inflammation and retain gut microbial biogeography in mice
title_full_unstemmed Steamed broccoli sprouts alleviate DSS-induced inflammation and retain gut microbial biogeography in mice
title_short Steamed broccoli sprouts alleviate DSS-induced inflammation and retain gut microbial biogeography in mice
title_sort steamed broccoli sprouts alleviate dss-induced inflammation and retain gut microbial biogeography in mice
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10654075/
https://www.ncbi.nlm.nih.gov/pubmed/37702510
http://dx.doi.org/10.1128/msystems.00532-23
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