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Simple Summary: The use of medicinal traditional plants and plant-derived compounds in the treatment of inflammatory states, including rheumatoid arthritis, is gaining attention due to their anti-inflammatory and immunomodulatory properties and fewer side effects compared to conventional drugs. The current study aimed to evaluate the therapeutic effects of the Mediterranean plant Teucrium montanum L. on collagen-induced arthritis in rats, in an in vivo animal model of rheumatoid arthritis. The effect of the Teucrium montanum extract was evaluated by examining the cellular and molecular components of innate and adaptive immunity that have been shown to play an important role in the pathogenesis of both rheumatoid arthritis and collagen-induced arthritis. The Teucrium montanum extract alleviated the clinical manifestation and improved the histopathological findings of arthritis in CIA. The extract improved the anti-/pro-oxidative balance in serum, suppressed the production of pro-inflammatory cytokines in affected joints, and suppressed the T cell responses in secondary lymphoid organs and the production of autoantibodies. Our results suggest the anti-inflammatory/immunomodulatory properties of Teucrium montanum extract and represent a basis for the further exploration of the possible therapeutic use of the extract or its compound/s. The anti-inflammatory/immunomodulatory effects of Teucrium montanum L. (TM), a plant distributed in the Mediterranean region, have been insufficiently examined. The effects of the TM ethanol extract were tested in a rat collagen-induced arthritis (CIA) model of rheumatoid arthritis. LC-MS was used for the phytochemical analysis of the TM extract. Dark Agouti rats were immunized with bovine type II collagen (CII) in incomplete Freund's adjuvant for CIA, and treated with 100 or 200 mg/kg of TM extract daily via oral administration. Clinical and histopathological evaluations and a flow cytometric analysis of the phenotypic and functional characteristics of splenocytes and draining lymph node cells were performed. The cytokines in the paw tissue culture supernatants and anti-CII antibodies in serum were determined by ELISA. The TM extract, with the dominant components verbascoside and luteolin 7-O-rutinoside, reduced the arthritic score and ankle joint inflammation in CIA rats, promoted the antioxidant profile in serum, and lowered pro-inflammatory TNF-α, IL-6 and IL-1β production. It suppressed the activation status of CD11b+ cells by lowering CD86, MHCII and TLR-4 expression, and promoted the Th17/T regulatory cell (Tregs) balance towards Tregs. A lower frequency of B cells was accompanied by a lower level of anti-CII antibodies in treated rats. These findings imply the favorable effect of TM extract on the clinical presentation of CIA, suggesting its anti-inflammatory/immunomodulatory action and potential therapeutic effect. [ABSTRACT FROM AUTHOR]