Protective role of colitis in inflammatory arthritis via propionate-producing Bacteroides in the gut
ObjectivesTo investigate whether and how inflammatory disease in the intestine influences the development of arthritis, considering that organ-to-organ communication is associated with many physiological and pathological events.MethodsFirst, mice were given drinking water containing dextran sodium s...
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Frontiers Media S.A.
2023-01-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1064900/full |
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| author | Hoh-Jeong Shon Hoh-Jeong Shon Yu-Mi Kim Yu-Mi Kim Kyeong Seog Kim Kyeong Seog Kim Jin-Ouk Choi Jin-Ouk Choi Sang-Hyun Cho Sujin An Sujin An Se-Hyeon Park Se-Hyeon Park Yong-Joon Cho Yong-Joon Cho Yong-Joon Cho Joo-Hong Park Sang-Uk Seo Joo-Youn Cho Joo-Youn Cho Wan-Uk Kim Wan-Uk Kim Wan-Uk Kim Donghyun Kim Donghyun Kim Donghyun Kim |
| author_facet | Hoh-Jeong Shon Hoh-Jeong Shon Yu-Mi Kim Yu-Mi Kim Kyeong Seog Kim Kyeong Seog Kim Jin-Ouk Choi Jin-Ouk Choi Sang-Hyun Cho Sujin An Sujin An Se-Hyeon Park Se-Hyeon Park Yong-Joon Cho Yong-Joon Cho Yong-Joon Cho Joo-Hong Park Sang-Uk Seo Joo-Youn Cho Joo-Youn Cho Wan-Uk Kim Wan-Uk Kim Wan-Uk Kim Donghyun Kim Donghyun Kim Donghyun Kim |
| author_sort | Hoh-Jeong Shon |
| collection | DOAJ |
| description | ObjectivesTo investigate whether and how inflammatory disease in the intestine influences the development of arthritis, considering that organ-to-organ communication is associated with many physiological and pathological events.MethodsFirst, mice were given drinking water containing dextran sodium sulfate (DSS) and then subjected to inflammatory arthritis. We compared the phenotypic symptoms between the cohoused and separately-housed mice. Next, donor mice were divided into DSS-treated and untreated groups and then cohoused with recipient mice. Arthritis was then induced in the recipients. The fecal microbiome was analyzed by 16S rRNA amplicon sequencing. We obtained type strains of the candidate bacteria and generated propionate-deficient mutant bacteria. Short-chain fatty acids were measured in the bacterial culture supernatant, serum, feces, and cecum contents using gas chromatography-mass spectrometry. Mice fed with candidate and mutant bacteria were subjected to inflammatory arthritis.ResultsContrary to expectations, the mice treated with DSS exhibited fewer symptoms of inflammatory arthritis. Intriguingly, the gut microbiota contributes, at least in part, to the improvement of colitis-mediated arthritis. Among the altered microorganisms, Bacteroides vulgatus and its higher taxonomic ranks were enriched in the DSS-treated mice. B. vulgatus, B. caccae, and B. thetaiotaomicron exerted anti-arthritic effects. Propionate production deficiency further prevented the protective effect of B. thetaiotaomicron on arthritis.ConclusionsWe suggest a novel relationship between the gut and joints and an important role of the gut microbiota as communicators. Moreover, the propionate-producing Bacteroides species examined in this study may be a potential candidate for developing effective treatments for inflammatory arthritis. |
| first_indexed | 2024-04-10T19:35:03Z |
| format | Article |
| id | doaj.art-f5660a197bcd42d5b5d96690299798d0 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-10T19:35:03Z |
| publishDate | 2023-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj.art-f5660a197bcd42d5b5d96690299798d02023-01-30T08:35:00ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-01-011410.3389/fimmu.2023.10649001064900Protective role of colitis in inflammatory arthritis via propionate-producing Bacteroides in the gutHoh-Jeong Shon0Hoh-Jeong Shon1Yu-Mi Kim2Yu-Mi Kim3Kyeong Seog Kim4Kyeong Seog Kim5Jin-Ouk Choi6Jin-Ouk Choi7Sang-Hyun Cho8Sujin An9Sujin An10Se-Hyeon Park11Se-Hyeon Park12Yong-Joon Cho13Yong-Joon Cho14Yong-Joon Cho15Joo-Hong Park16Sang-Uk Seo17Joo-Youn Cho18Joo-Youn Cho19Wan-Uk Kim20Wan-Uk Kim21Wan-Uk Kim22Donghyun Kim23Donghyun Kim24Donghyun Kim25Department of Biomedical Sciences, Seoul National University College of Medicine, Seoul, Republic of KoreaDepartment of Microbiology and Immunology, Seoul National University College of Medicine, Seoul, Republic of KoreaCenter for Integrative Rheumatoid Transcriptomics and Dynamics, The Catholic University of Korea, Seoul, Republic of KoreaDepartment of Biomedicine & Health Sciences, The Catholic University of Korea, Seoul, Republic of KoreaDepartment of Biomedical Sciences, Seoul National University College of Medicine, Seoul, Republic of KoreaDepartment of Clinical Pharmacology and Therapeutics, Seoul National University College of Medicine, Seoul, Republic of KoreaDepartment of Biomedical Sciences, Seoul National University College of Medicine, Seoul, Republic of KoreaDepartment of Microbiology and Immunology, Seoul National University College of Medicine, Seoul, Republic of KoreaSchool of Biological Sciences, Seoul National University, Seoul, Republic of KoreaDepartment of Biomedical Sciences, Seoul National University College of Medicine, Seoul, Republic of KoreaDepartment of Microbiology and Immunology, Seoul National University College of Medicine, Seoul, Republic of KoreaCenter for Integrative Rheumatoid Transcriptomics and Dynamics, The Catholic University of Korea, Seoul, Republic of KoreaDepartment of Biomedicine & Health Sciences, The Catholic University of Korea, Seoul, Republic of KoreaSchool of Biological Sciences, Seoul National University, Seoul, Republic of KoreaInstitute for Basic Science, Seoul, Republic of KoreaDepartment of Molecular Bioscience, College of Biomedical Science, Kangwon National University, Chuncheon, Republic of KoreaSchool of Biological Sciences, Seoul National University, Seoul, Republic of KoreaDepartment of Microbiology, College of Medicine, The Catholic University of Korea, Seoul, Republic of KoreaDepartment of Biomedical Sciences, Seoul National University College of Medicine, Seoul, Republic of KoreaDepartment of Clinical Pharmacology and Therapeutics, Seoul National University College of Medicine, Seoul, Republic of KoreaCenter for Integrative Rheumatoid Transcriptomics and Dynamics, The Catholic University of Korea, Seoul, Republic of KoreaDepartment of Biomedicine & Health Sciences, The Catholic University of Korea, Seoul, Republic of Korea0Division of Rheumatology, Department of Internal Medicine, the Catholic University of Korea, Seoul, Republic of KoreaDepartment of Biomedical Sciences, Seoul National University College of Medicine, Seoul, Republic of KoreaDepartment of Microbiology and Immunology, Seoul National University College of Medicine, Seoul, Republic of Korea1Institute of Endemic Diseases, Seoul National University Medical Research Center, Seoul, Republic of KoreaObjectivesTo investigate whether and how inflammatory disease in the intestine influences the development of arthritis, considering that organ-to-organ communication is associated with many physiological and pathological events.MethodsFirst, mice were given drinking water containing dextran sodium sulfate (DSS) and then subjected to inflammatory arthritis. We compared the phenotypic symptoms between the cohoused and separately-housed mice. Next, donor mice were divided into DSS-treated and untreated groups and then cohoused with recipient mice. Arthritis was then induced in the recipients. The fecal microbiome was analyzed by 16S rRNA amplicon sequencing. We obtained type strains of the candidate bacteria and generated propionate-deficient mutant bacteria. Short-chain fatty acids were measured in the bacterial culture supernatant, serum, feces, and cecum contents using gas chromatography-mass spectrometry. Mice fed with candidate and mutant bacteria were subjected to inflammatory arthritis.ResultsContrary to expectations, the mice treated with DSS exhibited fewer symptoms of inflammatory arthritis. Intriguingly, the gut microbiota contributes, at least in part, to the improvement of colitis-mediated arthritis. Among the altered microorganisms, Bacteroides vulgatus and its higher taxonomic ranks were enriched in the DSS-treated mice. B. vulgatus, B. caccae, and B. thetaiotaomicron exerted anti-arthritic effects. Propionate production deficiency further prevented the protective effect of B. thetaiotaomicron on arthritis.ConclusionsWe suggest a novel relationship between the gut and joints and an important role of the gut microbiota as communicators. Moreover, the propionate-producing Bacteroides species examined in this study may be a potential candidate for developing effective treatments for inflammatory arthritis.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1064900/fullarthritiscolitisgut microbiotaBacteroidespropionate |
| spellingShingle | Hoh-Jeong Shon Hoh-Jeong Shon Yu-Mi Kim Yu-Mi Kim Kyeong Seog Kim Kyeong Seog Kim Jin-Ouk Choi Jin-Ouk Choi Sang-Hyun Cho Sujin An Sujin An Se-Hyeon Park Se-Hyeon Park Yong-Joon Cho Yong-Joon Cho Yong-Joon Cho Joo-Hong Park Sang-Uk Seo Joo-Youn Cho Joo-Youn Cho Wan-Uk Kim Wan-Uk Kim Wan-Uk Kim Donghyun Kim Donghyun Kim Donghyun Kim Protective role of colitis in inflammatory arthritis via propionate-producing Bacteroides in the gut Frontiers in Immunology arthritis colitis gut microbiota Bacteroides propionate |
| title | Protective role of colitis in inflammatory arthritis via propionate-producing Bacteroides in the gut |
| title_full | Protective role of colitis in inflammatory arthritis via propionate-producing Bacteroides in the gut |
| title_fullStr | Protective role of colitis in inflammatory arthritis via propionate-producing Bacteroides in the gut |
| title_full_unstemmed | Protective role of colitis in inflammatory arthritis via propionate-producing Bacteroides in the gut |
| title_short | Protective role of colitis in inflammatory arthritis via propionate-producing Bacteroides in the gut |
| title_sort | protective role of colitis in inflammatory arthritis via propionate producing bacteroides in the gut |
| topic | arthritis colitis gut microbiota Bacteroides propionate |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1064900/full |
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