Short-Chain Fatty Acids Promote Immunotherapy by Modulating Immune Regulatory Property in B Cells
The dysfunction of regulatory B cells (Breg) may result in immune inflammation such as allergic rhinitis (AR); the underlying mechanism is not fully understood yet. Short-chain fatty acids, such as propionic acid (PA), have immune regulatory functions. This study is aimed at testing a hypothesis tha...
Saved in:
Main Authors: | , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Wiley
2021-01-01
|
Series: | Journal of Immunology Research |
Online Access: | http://dx.doi.org/10.1155/2021/2684361 |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
_version_ | 1832546017586708480 |
---|---|
author | Cai-Jie Zhou Bai-Ling Xie Hai-Yang Han Yin Wang Yong-Hua Wang Jing-Yi Hong Yi-Xia Wei Zhi-Gang Liu Yan Feng Gui Yang Ping-Chang Yang |
author_facet | Cai-Jie Zhou Bai-Ling Xie Hai-Yang Han Yin Wang Yong-Hua Wang Jing-Yi Hong Yi-Xia Wei Zhi-Gang Liu Yan Feng Gui Yang Ping-Chang Yang |
author_sort | Cai-Jie Zhou |
collection | DOAJ |
description | The dysfunction of regulatory B cells (Breg) may result in immune inflammation such as allergic rhinitis (AR); the underlying mechanism is not fully understood yet. Short-chain fatty acids, such as propionic acid (PA), have immune regulatory functions. This study is aimed at testing a hypothesis that modulates PA production alleviating airway allergy through maintaining Breg functions. B cells were isolated from the blood obtained from AR patients and healthy control (HC) subjects. The stabilization of IL-10 mRNA in B cells was tested with RT-qPCR. An AR mouse model was developed to test the role of PA in stabilizing the IL-10 expression in B cells. We found that the serum PA levels were negatively correlated with the serum Th2 cytokine levels in AR patients. Serum PA levels were positively associated with peripheral CD5+ B cell frequency in AR patients; the CD5+ B cells were also IL-10+. The spontaneous IL-10 mRNA decay was observed in B cells, which was prevented by the presence of PA through activating GPR43. PA counteracted the effects of Tristetraprolin (TTP) on inducing IL-10 mRNA decay in B cells through the AKT/T-bet/granzyme B pathway. Administration of Yupinfeng San, a Chinese traditional medical formula, or indole-3-PA, induced PA production by intestinal bacteria to stabilize the IL-10 expression in B cells, which promoted the allergen specific immunotherapy, and efficiently alleviated experimental AR. In summary, the data show that CD5+ B cells produce IL-10. The serum lower PA levels are associated with the lower frequency of CD5+ B cells in AR patients. Administration with Yupinfeng San or indole-3-PA can improve Breg functions and alleviate experimental AR. |
format | Article |
id | doaj-art-cae56ac116f84668b4af3d862715e38e |
institution | Kabale University |
issn | 2314-7156 |
language | English |
publishDate | 2021-01-01 |
publisher | Wiley |
record_format | Article |
series | Journal of Immunology Research |
spelling | doaj-art-cae56ac116f84668b4af3d862715e38e2025-02-03T07:24:13ZengWileyJournal of Immunology Research2314-71562021-01-01202110.1155/2021/2684361Short-Chain Fatty Acids Promote Immunotherapy by Modulating Immune Regulatory Property in B CellsCai-Jie Zhou0Bai-Ling Xie1Hai-Yang Han2Yin Wang3Yong-Hua Wang4Jing-Yi Hong5Yi-Xia Wei6Zhi-Gang Liu7Yan Feng8Gui Yang9Ping-Chang Yang10Shenzhen HospitalGuangdong Provincial Key Laboratory of Regional Immunity and DiseasesGuangdong Provincial Key Laboratory of Regional Immunity and DiseasesShenzhen HospitalShenzhen HospitalGuangdong Provincial Key Laboratory of Regional Immunity and DiseasesShenzhen HospitalGuangdong Provincial Key Laboratory of Regional Immunity and DiseasesDepartment of OtolaryngologyDepartment of OtolaryngologyGuangdong Provincial Key Laboratory of Regional Immunity and DiseasesThe dysfunction of regulatory B cells (Breg) may result in immune inflammation such as allergic rhinitis (AR); the underlying mechanism is not fully understood yet. Short-chain fatty acids, such as propionic acid (PA), have immune regulatory functions. This study is aimed at testing a hypothesis that modulates PA production alleviating airway allergy through maintaining Breg functions. B cells were isolated from the blood obtained from AR patients and healthy control (HC) subjects. The stabilization of IL-10 mRNA in B cells was tested with RT-qPCR. An AR mouse model was developed to test the role of PA in stabilizing the IL-10 expression in B cells. We found that the serum PA levels were negatively correlated with the serum Th2 cytokine levels in AR patients. Serum PA levels were positively associated with peripheral CD5+ B cell frequency in AR patients; the CD5+ B cells were also IL-10+. The spontaneous IL-10 mRNA decay was observed in B cells, which was prevented by the presence of PA through activating GPR43. PA counteracted the effects of Tristetraprolin (TTP) on inducing IL-10 mRNA decay in B cells through the AKT/T-bet/granzyme B pathway. Administration of Yupinfeng San, a Chinese traditional medical formula, or indole-3-PA, induced PA production by intestinal bacteria to stabilize the IL-10 expression in B cells, which promoted the allergen specific immunotherapy, and efficiently alleviated experimental AR. In summary, the data show that CD5+ B cells produce IL-10. The serum lower PA levels are associated with the lower frequency of CD5+ B cells in AR patients. Administration with Yupinfeng San or indole-3-PA can improve Breg functions and alleviate experimental AR.http://dx.doi.org/10.1155/2021/2684361 |
spellingShingle | Cai-Jie Zhou Bai-Ling Xie Hai-Yang Han Yin Wang Yong-Hua Wang Jing-Yi Hong Yi-Xia Wei Zhi-Gang Liu Yan Feng Gui Yang Ping-Chang Yang Short-Chain Fatty Acids Promote Immunotherapy by Modulating Immune Regulatory Property in B Cells Journal of Immunology Research |
title | Short-Chain Fatty Acids Promote Immunotherapy by Modulating Immune Regulatory Property in B Cells |
title_full | Short-Chain Fatty Acids Promote Immunotherapy by Modulating Immune Regulatory Property in B Cells |
title_fullStr | Short-Chain Fatty Acids Promote Immunotherapy by Modulating Immune Regulatory Property in B Cells |
title_full_unstemmed | Short-Chain Fatty Acids Promote Immunotherapy by Modulating Immune Regulatory Property in B Cells |
title_short | Short-Chain Fatty Acids Promote Immunotherapy by Modulating Immune Regulatory Property in B Cells |
title_sort | short chain fatty acids promote immunotherapy by modulating immune regulatory property in b cells |
url | http://dx.doi.org/10.1155/2021/2684361 |
work_keys_str_mv | AT caijiezhou shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT bailingxie shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT haiyanghan shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT yinwang shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT yonghuawang shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT jingyihong shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT yixiawei shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT zhigangliu shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT yanfeng shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT guiyang shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells AT pingchangyang shortchainfattyacidspromoteimmunotherapybymodulatingimmuneregulatorypropertyinbcells |