Differential effects of periodontal microbiome on the rheumatoid factor induction during rheumatoid arthritis pathogenesis
Abstract Association between exposure to periodontal bacteria and development of autoantibodies related to rheumatoid arthritis (RA) has been widely accepted; however, direct causal relationship between periodontal bacteria and rheumatoid factor (RF) is currently not fully understood. We investigate...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2022-11-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-21788-y |
| _version_ | 1811217665853751296 |
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| author | Ji-Won Kim Hyerin Jung In-Pyo Baek Yoojun Nam Jaewoo Kang Min Kyung Chung Jun-Beom Park Jennifer Lee Seung-Ki Kwok Wan-Uk Kim Sung-Hwan Park Ji Hyeon Ju |
| author_facet | Ji-Won Kim Hyerin Jung In-Pyo Baek Yoojun Nam Jaewoo Kang Min Kyung Chung Jun-Beom Park Jennifer Lee Seung-Ki Kwok Wan-Uk Kim Sung-Hwan Park Ji Hyeon Ju |
| author_sort | Ji-Won Kim |
| collection | DOAJ |
| description | Abstract Association between exposure to periodontal bacteria and development of autoantibodies related to rheumatoid arthritis (RA) has been widely accepted; however, direct causal relationship between periodontal bacteria and rheumatoid factor (RF) is currently not fully understood. We investigated whether periodontal bacteria could affect RF status. Patients with preclinical, new-onset, or chronic RA underwent periodontal examination, and investigation of subgingival microbiome via 16S rRNA sequencing. Degree of arthritis and RF induction was examined in collagen-induced arthritis (CIA) mice that were orally inoculated with different periodontal bacteria species. Subsequently, single-cell RNA sequencing analysis of the mouse spleen cells was performed. Patients with preclinical RA showed an increased abundance of the Porphyromonadacae family in the subgingival microbiome compared to those with new-onset or chronic RA, despite comparable periodontitis severity among them. Notably, a distinct subgingival microbial community was found between patients with high-positive RF and those with negative or low-positive RF (p=0.022). Oral infections with the periodontal pathogens P. gingivalis and Treponema denticola in CIA mice similarly enhanced arthritis score, but resulted in different levels of RF induction. Genes related to B cell receptor signaling, B cell proliferation, activation, and differentiation, and CD4+ T cell costimulation and cytokine production were involved in the differential induction of RF in mice exposed to different bacteria. In summary, periodontal microbiome might shape RF status by affecting the humoral immune response during RA pathogenesis. |
| first_indexed | 2024-04-12T06:58:36Z |
| format | Article |
| id | doaj.art-d19d2fa0de184b1782ad63f92dac6fb1 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-12T06:58:36Z |
| publishDate | 2022-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-d19d2fa0de184b1782ad63f92dac6fb12022-12-22T03:43:05ZengNature PortfolioScientific Reports2045-23222022-11-0112111110.1038/s41598-022-21788-yDifferential effects of periodontal microbiome on the rheumatoid factor induction during rheumatoid arthritis pathogenesisJi-Won Kim0Hyerin Jung1In-Pyo Baek2Yoojun Nam3Jaewoo Kang4Min Kyung Chung5Jun-Beom Park6Jennifer Lee7Seung-Ki Kwok8Wan-Uk Kim9Sung-Hwan Park10Ji Hyeon Ju11Division of Rheumatology, Department of Internal Medicine, Daegu Catholic University School of MedicineDivision of Rheumatology, Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of KoreaYiPSCELL Inc.Division of Rheumatology, Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of KoreaDivision of Rheumatology, Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of KoreaDivision of Rheumatology, Department of Internal Medicine, Ewha Womans University College of MedicineDepartment of Periodontics, College of Medicine, The Catholic University of KoreaDivision of Rheumatology, Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of KoreaDivision of Rheumatology, Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of KoreaDivision of Rheumatology, Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of KoreaDivision of Rheumatology, Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of KoreaDivision of Rheumatology, Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of KoreaAbstract Association between exposure to periodontal bacteria and development of autoantibodies related to rheumatoid arthritis (RA) has been widely accepted; however, direct causal relationship between periodontal bacteria and rheumatoid factor (RF) is currently not fully understood. We investigated whether periodontal bacteria could affect RF status. Patients with preclinical, new-onset, or chronic RA underwent periodontal examination, and investigation of subgingival microbiome via 16S rRNA sequencing. Degree of arthritis and RF induction was examined in collagen-induced arthritis (CIA) mice that were orally inoculated with different periodontal bacteria species. Subsequently, single-cell RNA sequencing analysis of the mouse spleen cells was performed. Patients with preclinical RA showed an increased abundance of the Porphyromonadacae family in the subgingival microbiome compared to those with new-onset or chronic RA, despite comparable periodontitis severity among them. Notably, a distinct subgingival microbial community was found between patients with high-positive RF and those with negative or low-positive RF (p=0.022). Oral infections with the periodontal pathogens P. gingivalis and Treponema denticola in CIA mice similarly enhanced arthritis score, but resulted in different levels of RF induction. Genes related to B cell receptor signaling, B cell proliferation, activation, and differentiation, and CD4+ T cell costimulation and cytokine production were involved in the differential induction of RF in mice exposed to different bacteria. In summary, periodontal microbiome might shape RF status by affecting the humoral immune response during RA pathogenesis.https://doi.org/10.1038/s41598-022-21788-y |
| spellingShingle | Ji-Won Kim Hyerin Jung In-Pyo Baek Yoojun Nam Jaewoo Kang Min Kyung Chung Jun-Beom Park Jennifer Lee Seung-Ki Kwok Wan-Uk Kim Sung-Hwan Park Ji Hyeon Ju Differential effects of periodontal microbiome on the rheumatoid factor induction during rheumatoid arthritis pathogenesis Scientific Reports |
| title | Differential effects of periodontal microbiome on the rheumatoid factor induction during rheumatoid arthritis pathogenesis |
| title_full | Differential effects of periodontal microbiome on the rheumatoid factor induction during rheumatoid arthritis pathogenesis |
| title_fullStr | Differential effects of periodontal microbiome on the rheumatoid factor induction during rheumatoid arthritis pathogenesis |
| title_full_unstemmed | Differential effects of periodontal microbiome on the rheumatoid factor induction during rheumatoid arthritis pathogenesis |
| title_short | Differential effects of periodontal microbiome on the rheumatoid factor induction during rheumatoid arthritis pathogenesis |
| title_sort | differential effects of periodontal microbiome on the rheumatoid factor induction during rheumatoid arthritis pathogenesis |
| url | https://doi.org/10.1038/s41598-022-21788-y |
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