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We demonstrate that P2X7R is robustly expressed in RA synovium, correlating with increased synovitis and systemic inflammation. Single-cell transcriptome analysis indicated that P2X7R was enriched in specific SF associated with refractory RA. Then, we applied a highly selective human P2X7R antagonist, EVT-401, which promoted apoptosis and induced cell cycle arrest in RA SF, reduced the production of proinflammatory and joint-destructive mediators, and mitigated aggressive phenotypes. Furthermore, we demonstrated that EVT-401 markedly reduced synovial inflammation and arthritis severity in a nonhuman primate model of autoimmune arthritis. 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