Immunoglobulin A Targets a Unique Subset of the Microbiota in Inflammatory Bowel Disease

Jason M. Shapiro; Marcel R. de Zoete; Noah W. Palm; Yaro Laenen; Rene Bright; Meaghan Mallette; Kevin Bu; Agata A. Bielecka; Fang Xu; Andres Hurtado-Lorenzo; Samir A. Shah; Judy H. Cho; Neal S. LeLeiko; Bruce E. Sands; Richard A. Flavell; J. C. Clemente

doi:10.1016/j.chom.2020.12.003

Immunoglobulin A Targets a Unique Subset of the Microbiota in Inflammatory Bowel Disease

Jason M. Shapiro, Marcel R. de Zoete, Noah W. Palm, Yaro Laenen, Rene Bright, Meaghan Mallette, Kevin Bu, Agata A. Bielecka, Fang Xu, Andres Hurtado-Lorenzo, Samir A. Shah, Judy H. Cho, Neal S. LeLeiko, Bruce E. Sands, Richard A. Flavell, J. C. Clemente

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Abstract

The immunopathogenesis of inflammatory bowel disease (IBD) has been attributed to a combination of host genetics and intestinal dysbiosis. Previous work in a small cohort of IBD patients suggested that pro-inflammatory bacterial taxa are highly coated with secretory immunoglobulin IgA. Using bacterial fluorescence-activated cell sorting coupled with 16S rRNA gene sequencing (IgA-SEQ), we profiled IgA coating of intestinal microbiota in a large cohort of IBD patients and identified bacteria associated with disease and treatment. Forty-three bacterial taxa displayed significantly higher IgA coating in IBD compared with controls, including 8 taxa exhibiting differential IgA coating but similar relative abundance. Patients treated with anti-TNF-α therapies exhibited dramatically altered microbiota-specific IgA responses compared with controls. Furthermore, increased IgA coating of Oscillospira was associated with a delay in time to surgery. These results demonstrate that investigating IgA responses to microbiota can uncover potential disease-modifying taxa and reveal improved biomarkers of clinical course in IBD.

Original language	English
Pages (from-to)	83-93.e3
Journal	Cell Host and Microbe
Volume	29
Issue number	1
DOIs	https://doi.org/10.1016/j.chom.2020.12.003
State	Published - 13 Jan 2021

Keywords

Crohn's disease
dysbiosis
immunoglobulin A
inflammatory bowel disease
microbiome
ulcerative colitis

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Shapiro, J. M., de Zoete, M. R., Palm, N. W., Laenen, Y., Bright, R., Mallette, M., Bu, K., Bielecka, A. A., Xu, F., Hurtado-Lorenzo, A., Shah, S. A., Cho, J. H., LeLeiko, N. S., Sands, B. E., Flavell, R. A., & Clemente, J. C. (2021). Immunoglobulin A Targets a Unique Subset of the Microbiota in Inflammatory Bowel Disease. Cell Host and Microbe, 29(1), 83-93.e3. https://doi.org/10.1016/j.chom.2020.12.003

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title = "Immunoglobulin A Targets a Unique Subset of the Microbiota in Inflammatory Bowel Disease",

abstract = "The immunopathogenesis of inflammatory bowel disease (IBD) has been attributed to a combination of host genetics and intestinal dysbiosis. Previous work in a small cohort of IBD patients suggested that pro-inflammatory bacterial taxa are highly coated with secretory immunoglobulin IgA. Using bacterial fluorescence-activated cell sorting coupled with 16S rRNA gene sequencing (IgA-SEQ), we profiled IgA coating of intestinal microbiota in a large cohort of IBD patients and identified bacteria associated with disease and treatment. Forty-three bacterial taxa displayed significantly higher IgA coating in IBD compared with controls, including 8 taxa exhibiting differential IgA coating but similar relative abundance. Patients treated with anti-TNF-α therapies exhibited dramatically altered microbiota-specific IgA responses compared with controls. Furthermore, increased IgA coating of Oscillospira was associated with a delay in time to surgery. These results demonstrate that investigating IgA responses to microbiota can uncover potential disease-modifying taxa and reveal improved biomarkers of clinical course in IBD.",

keywords = "Crohn's disease, dysbiosis, immunoglobulin A, inflammatory bowel disease, microbiome, ulcerative colitis",

author = "Shapiro, {Jason M.} and {de Zoete}, {Marcel R.} and Palm, {Noah W.} and Yaro Laenen and Rene Bright and Meaghan Mallette and Kevin Bu and Bielecka, {Agata A.} and Fang Xu and Andres Hurtado-Lorenzo and Shah, {Samir A.} and Cho, {Judy H.} and LeLeiko, {Neal S.} and Sands, {Bruce E.} and Flavell, {Richard A.} and Clemente, {J. C.}",

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year = "2021",

month = jan,

day = "13",

doi = "10.1016/j.chom.2020.12.003",

language = "English",

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Shapiro, JM, de Zoete, MR, Palm, NW, Laenen, Y, Bright, R, Mallette, M, Bu, K, Bielecka, AA, Xu, F, Hurtado-Lorenzo, A, Shah, SA, Cho, JH, LeLeiko, NS, Sands, BE, Flavell, RA & Clemente, JC 2021, 'Immunoglobulin A Targets a Unique Subset of the Microbiota in Inflammatory Bowel Disease', Cell Host and Microbe, vol. 29, no. 1, pp. 83-93.e3. https://doi.org/10.1016/j.chom.2020.12.003

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T1 - Immunoglobulin A Targets a Unique Subset of the Microbiota in Inflammatory Bowel Disease

AU - Shapiro, Jason M.

AU - de Zoete, Marcel R.

AU - Palm, Noah W.

AU - Laenen, Yaro

AU - Bright, Rene

AU - Mallette, Meaghan

AU - Bu, Kevin

AU - Bielecka, Agata A.

AU - Xu, Fang

AU - Hurtado-Lorenzo, Andres

AU - Shah, Samir A.

AU - Cho, Judy H.

AU - LeLeiko, Neal S.

AU - Sands, Bruce E.

AU - Flavell, Richard A.

AU - Clemente, J. C.

PY - 2021/1/13

Y1 - 2021/1/13

N2 - The immunopathogenesis of inflammatory bowel disease (IBD) has been attributed to a combination of host genetics and intestinal dysbiosis. Previous work in a small cohort of IBD patients suggested that pro-inflammatory bacterial taxa are highly coated with secretory immunoglobulin IgA. Using bacterial fluorescence-activated cell sorting coupled with 16S rRNA gene sequencing (IgA-SEQ), we profiled IgA coating of intestinal microbiota in a large cohort of IBD patients and identified bacteria associated with disease and treatment. Forty-three bacterial taxa displayed significantly higher IgA coating in IBD compared with controls, including 8 taxa exhibiting differential IgA coating but similar relative abundance. Patients treated with anti-TNF-α therapies exhibited dramatically altered microbiota-specific IgA responses compared with controls. Furthermore, increased IgA coating of Oscillospira was associated with a delay in time to surgery. These results demonstrate that investigating IgA responses to microbiota can uncover potential disease-modifying taxa and reveal improved biomarkers of clinical course in IBD.

AB - The immunopathogenesis of inflammatory bowel disease (IBD) has been attributed to a combination of host genetics and intestinal dysbiosis. Previous work in a small cohort of IBD patients suggested that pro-inflammatory bacterial taxa are highly coated with secretory immunoglobulin IgA. Using bacterial fluorescence-activated cell sorting coupled with 16S rRNA gene sequencing (IgA-SEQ), we profiled IgA coating of intestinal microbiota in a large cohort of IBD patients and identified bacteria associated with disease and treatment. Forty-three bacterial taxa displayed significantly higher IgA coating in IBD compared with controls, including 8 taxa exhibiting differential IgA coating but similar relative abundance. Patients treated with anti-TNF-α therapies exhibited dramatically altered microbiota-specific IgA responses compared with controls. Furthermore, increased IgA coating of Oscillospira was associated with a delay in time to surgery. These results demonstrate that investigating IgA responses to microbiota can uncover potential disease-modifying taxa and reveal improved biomarkers of clinical course in IBD.

KW - Crohn's disease

KW - dysbiosis

KW - immunoglobulin A

KW - inflammatory bowel disease

KW - microbiome

KW - ulcerative colitis

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JO - Cell Host and Microbe

JF - Cell Host and Microbe

IS - 1

ER -

Immunoglobulin A Targets a Unique Subset of the Microbiota in Inflammatory Bowel Disease

Abstract

Keywords

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