Introduction
Approximately 50% of patients with new-onset rheumatoid arthritis (RA) do not achieve remission within the first year on conventional synthetic disease modifying anti-rheumatic drugs (csDMARDs). Early and sustained remission confers better long-term outcomes, including a greater potential to stop treatment. Anti-citrullinated protein antibodies (ACPA) reactivity includes citrullinated (Cit)-vimentin epitopes, in particular Vimentin59-71Cit64 and Vimentin66-78Cit71, which are T cell epitopes presented by HLA-DR molecules of B cells and other antigen-presenting cells.
Methods
Twenty-one drug-naïve new-onset HLA-DRB1*04:01, *01:01 or *04:04+ RA patients recruited into the Australian Autoimmune Arthritis Biobank Collaborative were treated with methotrexate, hydroxychloroquine, sulfasalazine, and leflunomide, singly or in combination. Disease activity scores using 28 joint counts and C-reactive protein (DAS28-CRP) and peripheral blood mononuclear cells (PBMCs) were collected at baseline, 6, 12 and 24 months. Stable remission was defined as DAS28-CRP<2.4 at 6 and 12 months, slow/intermittent remission as DAS28-CRP≥2.4 at either 6 or 12 months, and non-remission as DAS28-CRP≥2.4 at both 6 and 12 months. PBMCs were assessed using a 17-marker spectral flow panel, including HLA-DRB1*04:01/01:01-Vimentin59-71Cit64 or HLA-DRB1*04:04-Vimentin66-78Cit71 tetramers, and clustered using both supervised and non-supervised methods. Changes in the number of T cell subsets over time between 4 groups; remission samples from stable remission and slow/intermittent remission patients, and low and moderate/high disease activity samples from all patients, were assessed using a generalized linear mixed model with a negative binomial distribution.
Results
Of 21 patients (85.7% ACPA+), 11 achieved stable remission, 7 intermittent remission, and 3 did not achieve remission. CD4⁺ CXCR5-PD1+ Tph, including citrullinated-vimentin-specific CD4⁺ CXCR5-PD1+ Tph, CD4⁺ CCR7+CXCR5-PD1+ Stem-like Tph, CD4⁺ PD1⁺TIGIT⁺ T cells and CD4⁺ TIGIT⁺ T cells were increased with moderate/high disease activity, while citrullinated-vimentin-specific CD4⁺GPR56+CD45RA+CCR7- TemRA, were decreased with low and moderate/high disease activity, as compared to remission in stable remission patients, at baseline. Biplot analysis identified these populations as key determinants distinguishing response groups at 6 and 12 months.
Conclusion
Baseline frequencies of CD4⁺ Tph, stem-like Tph, including those recognizing citrullinated vimentin, are negatively associated with stable remission trajectory, while CD4+ TemRA expressing the GPR56 marker of cytotoxicity are positively associated with stable remission trajectory, in csDMARD-treated recent-onset RA patients. These data suggest that CD4+ helper T cells promote B cells activation, while cytotoxic CD4+ TemRA kills B cells presenting Cit-vimentin in RA to prevent or support remission on csDMARDs.