A Shifted Urinary Microbiota Associated with Disease Activity and Immune Responses in Rheumatoid Arthritis

ABSTRACT Recent evidence emphasized the role of the microbiota in the etiopathogenesis of rheumatoid arthritis (RA). Indeed, it has been demonstrated that urinary tract infections are implicated in RA pathogenesis. However, a definitive association between the urinary tract microbiota and RA remains...

Full description

Bibliographic Details
Main Authors: Jiayang Jin, Jing Li, Meiling Hou, Xu Ding, Yan Zhong, Jing He, Xiaolin Sun, Hua Ye, Ru Li, Lijun Wu, Jun Wang, Jianping Guo, Zhanguo Li
Format: Article
Language:English
Published: American Society for Microbiology 2023-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.03662-22
_version_ 1797803487862456320
author Jiayang Jin
Jing Li
Meiling Hou
Xu Ding
Yan Zhong
Jing He
Xiaolin Sun
Hua Ye
Ru Li
Lijun Wu
Jun Wang
Jianping Guo
Zhanguo Li
author_facet Jiayang Jin
Jing Li
Meiling Hou
Xu Ding
Yan Zhong
Jing He
Xiaolin Sun
Hua Ye
Ru Li
Lijun Wu
Jun Wang
Jianping Guo
Zhanguo Li
author_sort Jiayang Jin
collection DOAJ
description ABSTRACT Recent evidence emphasized the role of the microbiota in the etiopathogenesis of rheumatoid arthritis (RA). Indeed, it has been demonstrated that urinary tract infections are implicated in RA pathogenesis. However, a definitive association between the urinary tract microbiota and RA remains to be investigated. Urine samples from 39 patients affected by RA, including treatment-naive patients, and 37 age- and sex-matched healthy individuals were collected. In RA patients, the urinary microbiota showed an increase in microbial richness and a decrease in microbial dissimilarity, especially in treatment-naive patients. A total of 48 altered genera with different absolute quantities were detected in patients with RA. The 37 enriched genera included Proteus, Faecalibacterium, and Bacteroides, while the 11 deficient genera included Gardnerella, Ruminococcus, Megasphaera, and Ureaplasma. Notably, the more abundant genera in RA patients were correlated with the disease activity score of 28 joints-erythrocyte sedimentation rates (DAS28-ESR) and an increase in plasma B cells. Furthermore, the altered urinary metabolites, such as proline, citric acid, and oxalic acid, were positively associated with RA patients, and they were closely correlated with urinary microbiota. These findings suggested a strong association between the altered urinary microbiota and metabolites with disease severity and dysregulated immune responses in RA patients. IMPORTANCE We revealed that the profile of the urinary tract microbiota in RA featured with increased microbial richness and shifted taxa, associated with immunological and metabolic changes of the disease, underlining the interplay between urinary microbiota and host autoimmunity.
first_indexed 2024-03-13T05:21:39Z
format Article
id doaj.art-c4236c905e2c4a21be2b3fb95228b801
institution Directory Open Access Journal
issn 2165-0497
language English
last_indexed 2024-03-13T05:21:39Z
publishDate 2023-06-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj.art-c4236c905e2c4a21be2b3fb95228b8012023-06-15T13:18:30ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.03662-22A Shifted Urinary Microbiota Associated with Disease Activity and Immune Responses in Rheumatoid ArthritisJiayang Jin0Jing Li1Meiling Hou2Xu Ding3Yan Zhong4Jing He5Xiaolin Sun6Hua Ye7Ru Li8Lijun Wu9Jun Wang10Jianping Guo11Zhanguo Li12Department of Rheumatology and Immunology, Peking University People’s Hospital, Beijing, ChinaDepartment of Rheumatology and Immunology, Peking University People’s Hospital, Beijing, ChinaTinyGene Bio-Tech (Shanghai) Co., Ltd., Shanghai, ChinaTinyGene Bio-Tech (Shanghai) Co., Ltd., Shanghai, ChinaDepartment of Rheumatology and Immunology, Peking University People’s Hospital, Beijing, ChinaDepartment of Rheumatology and Immunology, Peking University People’s Hospital, Beijing, ChinaDepartment of Rheumatology and Immunology, Peking University People’s Hospital, Beijing, ChinaDepartment of Rheumatology and Immunology, Peking University People’s Hospital, Beijing, ChinaDepartment of Rheumatology and Immunology, Peking University People’s Hospital, Beijing, ChinaDepartment of Rheumatology and Immunology, The People’s Hospital of Xin Jiang Uygur Autonomous Region, Urumqi, ChinaCAS Key Laboratory for Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaDepartment of Rheumatology and Immunology, Peking University People’s Hospital, Beijing, ChinaDepartment of Rheumatology and Immunology, Peking University People’s Hospital, Beijing, ChinaABSTRACT Recent evidence emphasized the role of the microbiota in the etiopathogenesis of rheumatoid arthritis (RA). Indeed, it has been demonstrated that urinary tract infections are implicated in RA pathogenesis. However, a definitive association between the urinary tract microbiota and RA remains to be investigated. Urine samples from 39 patients affected by RA, including treatment-naive patients, and 37 age- and sex-matched healthy individuals were collected. In RA patients, the urinary microbiota showed an increase in microbial richness and a decrease in microbial dissimilarity, especially in treatment-naive patients. A total of 48 altered genera with different absolute quantities were detected in patients with RA. The 37 enriched genera included Proteus, Faecalibacterium, and Bacteroides, while the 11 deficient genera included Gardnerella, Ruminococcus, Megasphaera, and Ureaplasma. Notably, the more abundant genera in RA patients were correlated with the disease activity score of 28 joints-erythrocyte sedimentation rates (DAS28-ESR) and an increase in plasma B cells. Furthermore, the altered urinary metabolites, such as proline, citric acid, and oxalic acid, were positively associated with RA patients, and they were closely correlated with urinary microbiota. These findings suggested a strong association between the altered urinary microbiota and metabolites with disease severity and dysregulated immune responses in RA patients. IMPORTANCE We revealed that the profile of the urinary tract microbiota in RA featured with increased microbial richness and shifted taxa, associated with immunological and metabolic changes of the disease, underlining the interplay between urinary microbiota and host autoimmunity.https://journals.asm.org/doi/10.1128/spectrum.03662-22rheumatoid arthritisurinary microbiotaurinary metabolitesimmune responses
spellingShingle Jiayang Jin
Jing Li
Meiling Hou
Xu Ding
Yan Zhong
Jing He
Xiaolin Sun
Hua Ye
Ru Li
Lijun Wu
Jun Wang
Jianping Guo
Zhanguo Li
A Shifted Urinary Microbiota Associated with Disease Activity and Immune Responses in Rheumatoid Arthritis
Microbiology Spectrum
rheumatoid arthritis
urinary microbiota
urinary metabolites
immune responses
title A Shifted Urinary Microbiota Associated with Disease Activity and Immune Responses in Rheumatoid Arthritis
title_full A Shifted Urinary Microbiota Associated with Disease Activity and Immune Responses in Rheumatoid Arthritis
title_fullStr A Shifted Urinary Microbiota Associated with Disease Activity and Immune Responses in Rheumatoid Arthritis
title_full_unstemmed A Shifted Urinary Microbiota Associated with Disease Activity and Immune Responses in Rheumatoid Arthritis
title_short A Shifted Urinary Microbiota Associated with Disease Activity and Immune Responses in Rheumatoid Arthritis
title_sort shifted urinary microbiota associated with disease activity and immune responses in rheumatoid arthritis
topic rheumatoid arthritis
urinary microbiota
urinary metabolites
immune responses
url https://journals.asm.org/doi/10.1128/spectrum.03662-22
work_keys_str_mv AT jiayangjin ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT jingli ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT meilinghou ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT xuding ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT yanzhong ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT jinghe ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT xiaolinsun ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT huaye ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT ruli ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT lijunwu ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT junwang ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT jianpingguo ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT zhanguoli ashiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT jiayangjin shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT jingli shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT meilinghou shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT xuding shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT yanzhong shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT jinghe shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT xiaolinsun shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT huaye shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT ruli shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT lijunwu shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT junwang shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT jianpingguo shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis
AT zhanguoli shiftedurinarymicrobiotaassociatedwithdiseaseactivityandimmuneresponsesinrheumatoidarthritis