Dysbiosis Contributes to Arthritis Development via Activation of Autoreactive T Cells in the Intestine

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Dysbiosis Contributes to Arthritis Development via Activation of Autoreactive T Cells in the Intestine (1)

SKG mice, which bear a point mutation in the ZAP‐70 gene (Zap70), spontaneously develop Th17 cell−dependent arthritis in a conventional facility. However, SKG mice reared under germ‐free conditions do not develop arthritis, even after treatment with fungal components, which indicates the possible involvement of intestinal microbiota in disease onset. In RA patients, an altered composition of intestinal microbiota (called dysbiosis) has been shown. Another study demonstrated the expansion of Prevotella copri in patients with new‐onset RA in the US.

The microbiota of feces obtained from 17 patients with early RA, who were not treated with antirheumatic drugs and 14 healthy controls, were analyzed using 16S rRNA−based deep sequencing. Each cluster was characterized by a high abundance of the following genera: Ruminococcus in cluster 1, Bacteroides in cluster 2, Blautia and Faecalibacterium in cluster 3, and Prevotella in cluster 4. Cluster 4 was composed of only RA patients, whereas the other clusters included both RA patients and healthy controls. Among the OTUs that were assigned to Prevotella in cluster 4, the majority (79.2%) showed a high (>99%) similarity to P copri, followed by 10.3% of OTUs to Prevotella stercorea.

SPF‐housed SKG mice treated with a combination of antibiotics (ampicillin, vancomycin, neomycin, and metronidazole) did not develop arthritis after an intraperitoneal injection of zymosan (a fungal β‐glucan). A low dose of zymosan was injected intraperitoneally into RA‐SKG and HC‐SKG mice at 5 weeks after colonization with microbiota from patients with RA or control. RA‐SKG mice showed severe swelling in the joints. Moreover, RA‐SKG mice had marked hypertrophy of the popliteal lymph nodes. RA‐SKG mice had severe synovitis and destruction of cartilage and bone compared with HC‐SKG mice. RA‐SKG mice developed high titers of RF.

Cells were isolated from the regional lymph nodes, intestine, and spleen of RA‐SKG and HC‐SKG mice at 4 weeks after microbiota colonization, stimulated with RPL23A or control GST protein, and analyzed by ELISA for production of IL‐17A and IFNγ. RPL23A‐induced production of IL‐17A, but not IFNγ, in regional lymph node cells was higher in RA‐SKG mice than in HC‐SKG mice. RPL23A‐induced IL‐17A IFNγ production, but not IFNγ production, in cells from the large intestine was also highly enhanced in RA‐SKG mice compared with HC‐SKG mice. No significant difference in cytokine production in cells from the small intestine or spleen between RA‐SKG mice and HC‐SKG mice was observed.

Prevotella‐dominated RA microbiota, compared with healthy control microbiota, induced severe arthritis in SKG mice. However, the severity of arthritis in SKG mice colonized with human microbiota was milder than that in SKG mice reared under SPF conditions. The number of IL‐17−producing Th17 cells in the large intestine of SKG mice colonized with human microbiota was smaller than that in SPF‐housed SKG mice. P copri mainly colonizes in the large intestine and not the small intestine.

1. Y. Maeda, T. Kurakawa, E. Umemoto, D. Motooka, Y. Ito, K. Gotoh, K. Hirota, M. Matsushita, Y. Furuta, M. Narazaki, N. Sakaguchi, H. Kayama, S. Nakamura, T. Iida, Y. Saeki, A. Kumanogoh, S. Sakaguchi, K. Takeda, Dysbiosis Contributes to Arthritis Development via Activation of Autoreactive T Cells in the Intestine. Arthritis Rheumatol. 68, 2646–2661 (2016).

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