Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis
Ulcerative colitis is an inflammatory disease of the colon that is associated with colonic neutrophil accumulation. Recent evidence indicates that diet alters the composition of the gut microbiota and influences host–pathogen interactions. Specifically, bacterial fermentation of dietary fiber produc...
Main Authors: | , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2021-02-01
|
Series: | Frontiers in Immunology |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.619366/full |
id |
doaj-9943529c49eb4304b3678e6721064290 |
---|---|
record_format |
Article |
spelling |
doaj-9943529c49eb4304b3678e67210642902021-02-23T05:49:47ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-02-011210.3389/fimmu.2021.619366619366Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental ColitisSj Shen0Kathryn Prame Kumar1Shu Wen Wen2Raymond Shim3Brooke J. Wanrooy4Dragana Stanley5Robert J. Moore6Robert J. Moore7Thi Thu Hao Van8Remy Robert9Michael J. Hickey10Connie H. Y. Wong11Centre for Inflammatory Diseases, Department of Medicine, School of Clinical Sciences at Monash Health, Monash Medical Centre, Monash University, Clayton, VIC, AustraliaCentre for Inflammatory Diseases, Department of Medicine, School of Clinical Sciences at Monash Health, Monash Medical Centre, Monash University, Clayton, VIC, AustraliaCentre for Inflammatory Diseases, Department of Medicine, School of Clinical Sciences at Monash Health, Monash Medical Centre, Monash University, Clayton, VIC, AustraliaCentre for Inflammatory Diseases, Department of Medicine, School of Clinical Sciences at Monash Health, Monash Medical Centre, Monash University, Clayton, VIC, AustraliaCentre for Inflammatory Diseases, Department of Medicine, School of Clinical Sciences at Monash Health, Monash Medical Centre, Monash University, Clayton, VIC, AustraliaSchool of Health Medical and Applied Sciences, Central Queensland University, Rockhamptom, QLD, AustraliaInfection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, VIC, AustraliaSchool of Science, Royal Melbourne Institute of Technology (RMIT) University, Melbourne, VIC, AustraliaSchool of Science, Royal Melbourne Institute of Technology (RMIT) University, Melbourne, VIC, AustraliaMonash Biomedicine Discovery Institute and Department of Physiology, Monash University, Clayton, VIC, AustraliaCentre for Inflammatory Diseases, Department of Medicine, School of Clinical Sciences at Monash Health, Monash Medical Centre, Monash University, Clayton, VIC, AustraliaCentre for Inflammatory Diseases, Department of Medicine, School of Clinical Sciences at Monash Health, Monash Medical Centre, Monash University, Clayton, VIC, AustraliaUlcerative colitis is an inflammatory disease of the colon that is associated with colonic neutrophil accumulation. Recent evidence indicates that diet alters the composition of the gut microbiota and influences host–pathogen interactions. Specifically, bacterial fermentation of dietary fiber produces metabolites called short-chain fatty acids (SCFAs), which have been shown to protect against various inflammatory diseases. However, the effect of fiber deficiency on the key initial steps of inflammation, such as leukocyte–endothelial cell interactions, is unknown. Moreover, the impact of fiber deficiency on neutrophil recruitment under basal conditions and during inflammation in vivo is unknown. Herein, we hypothesized that a fiber-deficient diet promotes an inflammatory state in the colon at baseline and predisposes the host to more severe colitis pathology. Mice fed a no-fiber diet for 14 days showed significant changes in the gut microbiota and exhibited increased neutrophil-endothelial interactions in the colonic microvasculature. Although mice fed a no-fiber diet alone did not have observable colitis-associated symptoms, these animals were highly susceptible to low dose (0.5%) dextran sodium sulphate (DSS)-induced model of colitis. Supplementation of the most abundant SCFA, acetate, prevented no-fiber diet-mediated enrichment of colonic neutrophils and colitis pathology. Therefore, dietary fiber, possibly through the actions of acetate, plays an important role in regulating neutrophil recruitment and host protection against inflammatory colonic damage in an experimental model of colitis.https://www.frontiersin.org/articles/10.3389/fimmu.2021.619366/fullneutrophilscolitisfiberinflammationdiet |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Sj Shen Kathryn Prame Kumar Shu Wen Wen Raymond Shim Brooke J. Wanrooy Dragana Stanley Robert J. Moore Robert J. Moore Thi Thu Hao Van Remy Robert Michael J. Hickey Connie H. Y. Wong |
spellingShingle |
Sj Shen Kathryn Prame Kumar Shu Wen Wen Raymond Shim Brooke J. Wanrooy Dragana Stanley Robert J. Moore Robert J. Moore Thi Thu Hao Van Remy Robert Michael J. Hickey Connie H. Y. Wong Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis Frontiers in Immunology neutrophils colitis fiber inflammation diet |
author_facet |
Sj Shen Kathryn Prame Kumar Shu Wen Wen Raymond Shim Brooke J. Wanrooy Dragana Stanley Robert J. Moore Robert J. Moore Thi Thu Hao Van Remy Robert Michael J. Hickey Connie H. Y. Wong |
author_sort |
Sj Shen |
title |
Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis |
title_short |
Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis |
title_full |
Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis |
title_fullStr |
Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis |
title_full_unstemmed |
Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis |
title_sort |
deficiency of dietary fiber modulates gut microbiota composition, neutrophil recruitment and worsens experimental colitis |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Immunology |
issn |
1664-3224 |
publishDate |
2021-02-01 |
description |
Ulcerative colitis is an inflammatory disease of the colon that is associated with colonic neutrophil accumulation. Recent evidence indicates that diet alters the composition of the gut microbiota and influences host–pathogen interactions. Specifically, bacterial fermentation of dietary fiber produces metabolites called short-chain fatty acids (SCFAs), which have been shown to protect against various inflammatory diseases. However, the effect of fiber deficiency on the key initial steps of inflammation, such as leukocyte–endothelial cell interactions, is unknown. Moreover, the impact of fiber deficiency on neutrophil recruitment under basal conditions and during inflammation in vivo is unknown. Herein, we hypothesized that a fiber-deficient diet promotes an inflammatory state in the colon at baseline and predisposes the host to more severe colitis pathology. Mice fed a no-fiber diet for 14 days showed significant changes in the gut microbiota and exhibited increased neutrophil-endothelial interactions in the colonic microvasculature. Although mice fed a no-fiber diet alone did not have observable colitis-associated symptoms, these animals were highly susceptible to low dose (0.5%) dextran sodium sulphate (DSS)-induced model of colitis. Supplementation of the most abundant SCFA, acetate, prevented no-fiber diet-mediated enrichment of colonic neutrophils and colitis pathology. Therefore, dietary fiber, possibly through the actions of acetate, plays an important role in regulating neutrophil recruitment and host protection against inflammatory colonic damage in an experimental model of colitis. |
topic |
neutrophils colitis fiber inflammation diet |
url |
https://www.frontiersin.org/articles/10.3389/fimmu.2021.619366/full |
work_keys_str_mv |
AT sjshen deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT kathrynpramekumar deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT shuwenwen deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT raymondshim deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT brookejwanrooy deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT draganastanley deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT robertjmoore deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT robertjmoore deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT thithuhaovan deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT remyrobert deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT michaeljhickey deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis AT conniehywong deficiencyofdietaryfibermodulatesgutmicrobiotacompositionneutrophilrecruitmentandworsensexperimentalcolitis |
_version_ |
1724255155754369024 |