Efficacy and safety of iguratimod on patients with primary Sjögren’s syndrome: a randomized, placebo-controlled clinical trial

References

• Youinou P, Pers JO. Primary Sjögren’s syndrome at a glance today. Joint Bone Spine 2015;82:75–6.
   PubMed Web of Science ®Google Scholar
• Ibrahem HM. B cell dysregulation in primary Sjögren’s syndrome: a review. Jpn Dent Sci Rev 2019;55:139–44.
   PubMed Web of Science ®Google Scholar
• Glauzy S, Sng J, Bannock JM, Gottenberg JE, Korganow AS, Cacoub P, et al. Defective early B cell tolerance checkpoints in Sjögren’s syndrome patients. Arthritis Rheumatol 2017;69:2203–8.
   PubMed Web of Science ®Google Scholar
• Theander E, Jonsson R, Sjöström B, Brokstad K, Olsson P, Henriksson G. Prediction of Sjögren’s syndrome years before diagnosis and identification of patients with early onset and severe disease course by autoantibody profiling. Arthritis Rheumatol 2015;67:2427–36.
   PubMed Web of Science ®Google Scholar
• Basset C, Durand V, Jamin C, Clément J, Pennec Y, Youinou P, et al. Increased N-linked glycosylation leading to oversialylation of monomeric immunoglobulin A1 from patients with Sjögren’s syndrome. Scand J Immunol 2000;51:300–6.
   PubMed Web of Science ®Google Scholar
• Risselada AP, Looije MF, Kruize AA, Bijlsma JWJ, van Roon JAG. The role of ectopic germinal centers in the immunopathology of primary Sjögren’s syndrome: a systematic review. Semin Arthritis Rheum 2013;42:368–76.
   PubMed Web of Science ®Google Scholar
• Nocturne G, Virone A, Hachulla E, Cornec D, Bienvenu B, Marcelli C, et al. Rheumatoid factor and disease activity are independent predictors of lymphoma in primary Sjögren’s syndrome. Arthritis Rheumatol 2016;68:977–85.
   PubMed Web of Science ®Google Scholar
• Ramos-Casals M, Brito-Zeron P, Siso-Almirall A, Bosch X, Tzioufas AG. Topical and systemic medications for the treatment of primary Sjögren’s syndrome. Nat Rev Rheumatol 2012;8:399–411.
   PubMed Web of Science ®Google Scholar
• Ramos-Casals M, Tzioufas AG, Stone JH, Sisó A, Bosch X. Treatment of primary Sjögren syndrome: a systematic review. JAMA 2010;304:452–60.
   PubMed Web of Science ®Google Scholar
• Gottenberg JE, Cinquetti G, Larroche C, Combe B, Hachulla E, Meyer O, et al. Efficacy of rituximab in systemic manifestations of primary Sjögren’s syndrome: results in 78 patients of the autoimmune and rituximab registry. Ann Rheum Dis 2013;72:1026–31.
   PubMed Web of Science ®Google Scholar
• Meiners PM, Vissink A, Kroese FG, Spijkervet FK, Smitt-Kamminga NS, Abdulahad WH, et al. Abatacept treatment reduces disease activity in early primary Sjögren’s syndrome (open-label proof of concept ASAP study). Ann Rheum Dis 2014;73:1393–6.
   PubMed Web of Science ®Google Scholar
• Mariette X, Seror R, Quartuccio L, Baron G, Salvin S, Fabris M, et al. Efficacy and safety of belimumab in primary Sjögren’s syndrome: results of the BELISS open-label phase II study. Ann Rheum Dis 2015;74:526–31.
   PubMed Web of Science ®Google Scholar
• Lu LJ, Bao CD, Dai M, Teng JL, Fan W, Du F, et al. Multicenter, randomized, double-blind, controlled trial of treatment of active rheumatoid arthritis with T-614 compared with methotrexate. Arthritis Rheum 2009;61:979–87.
   PubMed Web of Science ®Google Scholar
• Xiao W, Guo JP, Li C, Ye H, Wei W, Zou Y, et al. Genetic predictors of efficacy and toxicity of iguratimod in patients with rheumatoid arthritis. Pharmacogenomics 2018;19:383–92.
   PubMed Web of Science ®Google Scholar
• Tanaka K, Yamamoto T, Aikawa Y, Kizawa K, Muramoto K, Matsuno H, et al. Inhibitory effects of an anti-rheumatic agent T-614 on immunoglobulin production by cultured B cells and rheumatoid synovial tissues engrafted into SCID mice. Rheumatology (Oxford) 2003;42:1365–71.
   PubMed Web of Science ®Google Scholar
• Hara M, Ishiguro N, Katayama K, Kondo M, Sumida T, Mimori T, et al. Safety and efficacy of combination therapy of iguratimod with methotrexate for patients with active rheumatoid arthritis with an inadequate response to methotrexate: an open-label extension of a randomized, double-blind, placebo-controlled trial. Mod Rheumatol 2014;24:410–18.
   PubMed Web of Science ®Google Scholar
• Mucke HA. Iguratimod: a new disease-modifying antirheumatic drug. Drugs Today 2012;48:577–86.
   PubMed Web of Science ®Google Scholar
• Shiboski CH, Shiboski SC, Seror R, Criswell LA, Labetoulle M, Lietman TM, et al. International Sjögren’s Syndrome Criteria Working Group. 2016 American College of Rheumatology/European League Against Rheumatism classification criteria for primary Sjögren’s syndrome: a consensus and data-driven methodology involving three international patient cohorts. Ann Rheum Dis 2017;76:9–16.
   PubMed Web of Science ®Google Scholar
• Luciano N, Valentini V, Calabro A, Elefante E, Vitale A, Baldini C, et al. One year in review 2015: Sjögren’s syndrome. Clin Exp Rheumatol 2015;33:259–71.
   PubMed Web of Science ®Google Scholar
• Morgane M, Cornec D, Chastaing M, Griner V, Berrouiguet S, Nowak E, et al. Sicca symptoms are associated with similar fatigue, anxiety, depression, and quality-of-life impairments in patients with and without primary Sjögren’s syndrome. Jiont Bone Spine 2016;83:681–5.
   PubMed Web of Science ®Google Scholar
• Cui Y, Xia L, Li L, Zhao Q, Chen S, Gu Z. Anxiety and depression in primary Sjögren’s syndrome: a cross-sectional study. BMC Psychiatry 2018;18:131–8.
   PubMed Web of Science ®Google Scholar
• Mimori T, Harigai M, Atsumi T, Fujii T, Kuwana M, Matsuno H, et al. Safety and effectiveness of iguratimod in patients with rheumatoid arthritis: final report of a 52-week, multicenter postmarketing surveillance study. Mod Rheumatol 2019;29:314–23.
   PubMed Web of Science ®Google Scholar
• Nocturne G, Mariette X. Advances in understanding the pathogenesis of primary Sjögren’s syndrome. Nat Rev Rheumatol 2013;9:544–56.
   PubMed Web of Science ®Google Scholar
• Nocturne G, Mariette X. B cells in the pathogenesis of primary Sjögren’s syndrome. Nat Rev Rheumatol 2018;14:133–45.
   PubMed Web of Science ®Google Scholar
• Nilsson AM, Tufvesson E, Hesselstrand R, Olsson P, Wollmer P, Mandl T. Increased B-cell activating factor, interleukin-6, and interleukin-8 in induced sputum from primary Sjögren’s syndrome patients. Scand J Rheumatol 2019;48:149–56.
   PubMed Web of Science ®Google Scholar
• Quartuccio L, Salvin S, Fabris M, Maset M, Pontarini E, Isola M, et al. BLyS upregulation in Sjögren’s syndrome associated with lymphoproliferative disorders, higher ESSDAI score and B-cell clonal expansion in the salivary glands. Rheumatology (Oxford) 2013;52:276–81.
   PubMed Web of Science ®Google Scholar
• Mariette X, Roux S, Zhang J, Bengoufa D, Lavie F, Zhou T, et al. The level of BLyS (BAFF) correlates with the titre of autoantibodies in human Sjögren’s syndrome. Ann Rheum Dis 2003;62:168–71.
   PubMed Web of Science ®Google Scholar
• Daridon C, Devauchelle V, Hutin P, Bendaoud B, Dueymes M, Saraux A, et al. Aberrant expression of BAFF by B lymphocytes infiltrating the salivary glands of patients with primary Sjögren’s syndrome. Arthritis Rheum 2007;56:1134–44.
   PubMed Web of Science ®Google Scholar
• Deng F, Chen J, Zheng J, Chen Y, Huang R, Yin J, et al. Association of BAFF and IL-17A with subphenotypes of primary Sjögren’s syndrome. Int J Rheum Dis 2016;9:715–20.
   Web of Science ®Google Scholar
• Nocturne G, Seror R, Fogel O, Belkhir R, Boudaoud S, Saraux A, et al. CXCL13 and CCL11 serum levels and lymphoma and disease activity in primary Sjögren’s syndrome. Arthritis Rheumatol 2015;67:3226–33.
   PubMed Web of Science ®Google Scholar
• Pontarini E, Fabris M, Quartuccio L, Cappeletti M, Calcaterra F, Roberto A, et al. Treatment with belimumab restores B cell subsets and their expression of B cell activating factor receptor in patients with primary Sjögren’s syndrome. Rheumatology (Oxford) 2015;54:1429–34.
   PubMed Web of Science ®Google Scholar
• Salazar-Camarena DC, Ortiz-Lazareno PC, Cruz A, Oregon-Romero E, Machado-Contreras JR, Muñoz-Valle JF, et al. Association of BAFF, APRIL serum levels, BAFF-R, TACI and BCMA expression on peripheral B-cell subsets with clinical manifestations in systemic lupus erythematosus. Lupus 2016;25:582–92.
   PubMed Web of Science ®Google Scholar
• Ding J, Zhang W, Haskett S, Pellerin A, Xu S, Petersenet B, et al. BAFF overexpression increases lymphocytic infiltration in Sjögren’s target tissue, but only inefficiently promotes ectopic B-cell differentiation. Clin Immunol 2016;169:69–79.
   PubMed Web of Science ®Google Scholar
• Yan Q, Du F, Huang X, Chen S, Dai D, Bao C, et al. Prevention of immune nephritis by the small molecular weight immunomodulator iguratimod in MRL/lpr mice. PLoS One 2014;9:e108273.
   PubMed Web of Science ®Google Scholar
• Zhang P, Gong Y, Liu Z, Liu Y, Lin W, Zhang W, et al. Efficacy and safety of iguratimod plus corticosteroid as bridge therapy in treating mild IgG4-related diseases: a prospective clinical trial. Int J Rheum Dis 2019:00;1–10.
   Google Scholar
• Mingueneau M, Boudaoud S, Haskett S, Reynolds TL, Nocturne G, Norton E, et al. Cytometry by time-of-flight immunophenotyping identifies a blood Sjögren’s signature correlating with disease activity and glandular inflammation. J Allergy Clin Immunol 2016;137:1809–21.
   PubMed Web of Science ®Google Scholar
• Jasiek M, Karras A, Guern VL, Krastinova E, Mesbah R, Faguer S, et al. A multicentre study of 95 biopsy-proven cases of renal disease in primary Sjögren’s syndrome. Rheumatology (Oxford) 2017;56:362–70.
   PubMed Web of Science ®Google Scholar
• Szyszko EA, Brokstad KA, Oijordsbakken G, Jonsson MV, Jonsson R, Skarstein K, et al. Salivary glands of primary Sjögren’s syndrome patients express factors vital for plasma cell survival. Arthritis Res Ther 2011;13:R2.
   PubMed Web of Science ®Google Scholar
• Aqrawi LA, Skarstein K, Oijordsbakken G, Brokstad KA. Ro52-and Ro60-specific B cell pattern in the salivary glands of patients with primary Sjögren’s syndrome. Clin Exp Immunol 2013;172:228–37.
   PubMed Web of Science ®Google Scholar
• Ye Y, Liu M, Tang L, Du F, Liu Y, Bao C, et al. Iguratimod represses B cell terminal differentiation linked with the inhibition of PKC/EGR1 axis. Arthritis Res Ther 2019;21:92–104.
   PubMed Web of Science ®Google Scholar
• Jiang C, Loo WM, Greenley EJ, Tung KS, Erickson LD. B cell maturation antigen deficiency exacerbates lymphoproliferation and autoimmunity in murine lupus. J Immunol 2011;186:6136–47.
   PubMed Web of Science ®Google Scholar
• Killedar SJ, Eckenrode SE, McIndoe RA, She JX, Nguyen CQ, Peck AB, et al. Early pathogenic events associated with Sjögren’s syndrome (SjS)-like disease of the NOD mouse using microarray analysis. Lab Invest 2006;86:1243–60.
   PubMed Web of Science ®Google Scholar
• Ou X, Xu S, Lam K-P. Deficiency in TNFRSF13B (TACI) expands T-follicular helper and germinal center B cells via increased ICOS-ligand expression but impairs plasma cell survival. Proc Natl Acad Sci USA 2012;109:15401–6.
   PubMed Web of Science ®Google Scholar
• Tsuji S, Cortesão C, Bram RJ, Platt JL, Cascalho M. TACI deficiency impairs sustained Blimp-1 expression in B cells decreasing long-lived plasma cells in the bone marrow. Blood 2011;118:5832–9.
   PubMed Web of Science ®Google Scholar
• Haselmayer P, Vigolo M, Nys J, Schneider P, Hess H. A mouse model of systemic lupus erythematosus responds better to soluble TACI than to soluble BAFFR, correlating with depletion of plasma cells. Eur J Immunol 2017;47:1075–85.
   PubMed Web of Science ®Google Scholar