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Distinct B cell subsets in Peyer's patches convey probiotic effects by Limosilactobacillus reuteri

Liu, Hao-Yu and Giraud, Antoine and Seignez, Cedric and Ahl, David and Guo, Feilong and Sedin, John and Walden, Tomas and Oh, Jee-Hwan and van Pijkeren, Jan Peter and Holm, Lena and Roos, Stefan and Bertilsson, Stefan and Phillipson, Mia (2021). Distinct B cell subsets in Peyer's patches convey probiotic effects by Limosilactobacillus reuteri. Microbiome. 9 , 198
[Research article]

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Abstract

Background: Intestinal Peyer's patches (PPs) form unique niches for bacteria-immune cell interactions that direct host immunity and shape the microbiome. Here we investigate how peroral administration of probiotic bacterium Limosilactobacillus reuteri R2LC affects B lymphocytes and IgA induction in the PPs, as well as the downstream consequences on intestinal microbiota and susceptibility to inflammation.Results: The B cells of PPs were separated by size to circumvent activation-dependent cell identification biases due to dynamic expression of markers, which resulted in two phenotypically, transcriptionally, and spatially distinct subsets: small IgD(+)/GL7(-)/S1PR1(+)/Bcl6, CCR6-expressing pre-germinal center (GC)-like B cells with innate-like functions located subepithelially, and large GL7(+)/S1PR1(-)/Ki67(+)/Bcl6, CD69-expressing B cells with strong metabolic activity found in the GC. Peroral L. reuteri administration expanded both B cell subsets and enhanced the innate-like properties of pre-GC-like B cells while retaining them in the sub-epithelial compartment by increased sphingosine-1-phosphate/S1PR1 signaling. Furthermore, L. reuteri promoted GC-like B cell differentiation, which involved expansion of the GC area and autocrine TGF beta-1 activation. Consequently, PD-1-T follicular helper cell-dependent IgA induction and production was increased by L. reuteri, which shifted the intestinal microbiome and protected against dextran-sulfate-sodium induced colitis and dysbiosis.Conclusions: The Peyer's patches sense, enhance and transmit probiotic signals by increasing the numbers and effector functions of distinct B cell subsets, resulting in increased IgA production, altered intestinal microbiota, and protection against inflammation.

Authors/Creators:Liu, Hao-Yu and Giraud, Antoine and Seignez, Cedric and Ahl, David and Guo, Feilong and Sedin, John and Walden, Tomas and Oh, Jee-Hwan and van Pijkeren, Jan Peter and Holm, Lena and Roos, Stefan and Bertilsson, Stefan and Phillipson, Mia
Title:Distinct B cell subsets in Peyer's patches convey probiotic effects by Limosilactobacillus reuteri
Series Name/Journal:Microbiome
Year of publishing :2021
Volume:9
Article number:198
Number of Pages:18
Publisher:BMC
ISSN:2049-2618
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Microbiology (Microbiology in the medical area to be 30109)
Keywords:Innate-like B lymphocytes, Inflammatory bowel disease, Gut microbiome, PD-1 dependent, Probiotics, R2LC
URN:NBN:urn:nbn:se:slu:epsilon-p-113967
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-113967
Additional ID:
Type of IDID
DOI10.1186/s40168-021-01128-4
Web of Science (WoS)000702996300001
ID Code:25667
Faculty:NJ - Fakulteten för naturresurser och jordbruksvetenskap
Department:(NL, NJ) > Department of Molecular Sciences
(NL, NJ) > Dept. of Aquatic Sciences and Assessment
Deposited By: SLUpub Connector
Deposited On:14 Oct 2021 15:25
Metadata Last Modified:14 Oct 2021 15:31

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