Transformation of fibroblast‐like synoviocytes in rheumatoid arthritis; from a friend to foe

Springer Science and Business Media LLC - Tập 12 - Trang 1-13 - 2021
Mohammad Javad Mousavi1,2,3, Jafar Karami1,4,5, Saeed Aslani2, Mohammad Naghi Tahmasebi6, Arash Sharafat Vaziri6, Ahmadreza Jamshidi1, Elham Farhadi1,7, Mahdi Mahmoudi1,7
1Rheumatology Research Center, Tehran University of Medical Sciences, Tehran, Iran
2Department of Immunology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
3Department of Hematology, Faculty of Allied Medicine, Bushehr University of Medical Sciences, Bushehr, Iran
4Department of Immunology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
5Department of Laboratory Sciences, Khomein University of Medical Sciences, Khomein, Iran
6Joint Reconstruction Reseach Center, Tehran University of Medical Sciences, Tehran, Iran
7Inflammation Research Center, Tehran University of Medical Sciences, Tehran, Iran

Tóm tắt

Swelling and the progressive destruction of articular cartilage are major characteristics of rheumatoid arthritis (RA), a systemic autoimmune disease that directly affects the synovial joints and often causes severe disability in the affected positions. Recent studies have shown that type B synoviocytes, which are also called fibroblast-like synoviocytes (FLSs), as the most commonly and chiefly resident cells, play a crucial role in early-onset and disease progression by producing various mediators. During the pathogenesis of RA, the FLSs’ phenotype is altered, and represent invasive behavior similar to that observed in tumor conditions. Modified and stressful microenvironment by FLSs leads to the recruitment of other immune cells and, eventually, pannus formation. The origins of this cancerous phenotype stem fundamentally from the significant metabolic changes in glucose, lipids, and oxygen metabolism pathways. Moreover, the genetic abnormalities and epigenetic alterations have recently been implicated in cancer-like behaviors of RA FLSs. In this review, we will focus on the mechanisms underlying the transformation of FLSs to a cancer-like phenotype during RA. A comprehensive understanding of these mechanisms may lead to devising more effective and targeted treatment strategies.

Tài liệu tham khảo

Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet. 2010;376(9746):1094–108.

Amaya-Amaya J, Botello-Corzo D, Calixto OJ, Calderon-Rojas R, Dominguez AM, Cruz-Tapias P, et al. Usefulness of patients-reported outcomes in rheumatoid arthritis focus group. Arthritis. 2012;2012:935187.

Sokka T, Krishnan E, Hakkinen A, Hannonen P. Functional disability in rheumatoid arthritis patients compared with a community population in Finland. Arthritis Rheum. 2003;48(1):59–63.

Cadena J, Vinaccia S, Perez A, Rico MI, Hinojosa R, Anaya JM. The impact of disease activity on the quality of life, mental health status, and family dysfunction in colombian patients with rheumatoid arthritis. J Clin Rheumatol. 2003;9(3):142–50.

Sokka T, Abelson B, Pincus T. Mortality in rheumatoid arthritis: 2008 update. Clin Exp Rheumatol. 2008;26(5 Suppl 51):35–61.

MacGregor AJ, Snieder H, Rigby AS, Koskenvuo M, Kaprio J, Aho K, et al. Characterizing the quantitative genetic contribution to rheumatoid arthritis using data from twins. Arthritis Rheum. 2000;43(1):30–7.

Karami J, Aslani S, Jamshidi A, Garshasbi M, Mahmoudi M. Genetic implications in the pathogenesis of rheumatoid arthritis; an updated review. Gene. 2019;9:78.

Bang SY, Lee KH, Cho SK, Lee HS, Lee KW, Bae SC. Smoking increases rheumatoid arthritis susceptibility in individuals carrying the HLA-DRB1 shared epitope, regardless of rheumatoid factor or anti-cyclic citrullinated peptide antibody status. Arthritis Rheum. 2010;62(2):369–77.

Bartok B, Firestein GS. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev. 2010;233(1):233–55.

Bottini N, Firestein GS. Duality of fibroblast-like synoviocytes in RA: passive responders and imprinted aggressors. Nat Rev Rheumatol. 2013;9(1):24–33.

Ganesan R, Rasool M. Fibroblast-like synoviocytes-dependent effector molecules as a critical mediator for rheumatoid arthritis: current status and future directions. Int Rev Immunol. 2017;36(1):20–30.

McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med. 2011;365(23):2205–19.

Izquierdo E, Canete JD, Celis R, Del Rey MJ, Usategui A, Marsal S, et al. Synovial fibroblast hyperplasia in rheumatoid arthritis: clinicopathologic correlations and partial reversal by anti-tumor necrosis factor therapy. Arthritis Rheum. 2011;63(9):2575–83.

Rooney M, Condell D, Quinlan W, Daly L, Whelan A, Feighery C, et al. Analysis of the histologic variation of synovitis in rheumatoid arthritis. Arthritis Rheum. 1988;31(8):956–63.

Guo J, Zhao W, Cao X, Yang H, Ding J, Ding J, et al. SIRT1 promotes tumor-like invasion of fibroblast-like synoviocytes in rheumatoid arthritis via targeting TIMP1. Oncotarget. 2017;8(51):88965–73.

Liu Y, Pan YF, Xue YQ, Fang LK, Guo XH, Guo X, et al. uPAR promotes tumor-like biologic behaviors of fibroblast-like synoviocytes through PI3K/Akt signaling pathway in patients with rheumatoid arthritis. Cell Mol Immunol. 2018;15(2):171–81.

Bhattaram P, Jones K. Regulation of fibroblast-like synoviocyte transformation by transcription factors in arthritic diseases. Biochem Pharmacol. 2019;2:345.

Liu T, Zhou L, Li D, Andl T, Zhang Y. Cancer-associated fibroblasts build and secure the tumor microenvironment. Front Cell Develop Biol. 2019;7:7.

Pap T, Muller-Ladner U, Gay RE, Gay S. Fibroblast biology. Role of synovial fibroblasts in the pathogenesis of rheumatoid arthritis. Arthritis Res. 2000;2(5):361–7.

Kiener HP, Niederreiter B, Lee DM, Jimenez-Boj E, Smolen JS, Brenner MB. Cadherin 11 promotes invasive behavior of fibroblast-like synoviocytes. Arthritis Rheum. 2009;60(5):1305–10.

Lee DM, Kiener HP, Agarwal SK, Noss EH, Watts GF, Chisaka O, et al. Cadherin-11 in synovial lining formation and pathology in arthritis. Science. 2007;315(5814):1006–10.

Firestein GS, Kelley WN. Kelley’s textbook of rheumatology. Philadelphia: Elsevier/Saunders; 2013.

Tran CN, Thacker SG, Louie DM, Oliver J, White PT, Endres JL, et al. Interactions of T cells with fibroblast-like synoviocytes: role of the B7 family costimulatory ligand B7-H3. J Immunol. 2008;180(5):2989–98.

Tran CN, Lundy SK, White PT, Endres JL, Motyl CD, Gupta R, et al. Molecular interactions between T cells and fibroblast-like synoviocytes: role of membrane tumor necrosis factor-alpha on cytokine-activated T cells. Am J Pathol. 2007;171(5):1588–98.

Yamamura Y, Gupta R, Morita Y, He X, Pai R, Endres J, et al. Effector function of resting T cells: activation of synovial fibroblasts. J Immunol. 2001;166(4):2270–5.

Tsai C, Diaz LA Jr, Singer NG, Li LL, Kirsch AH, Mitra R, et al. Responsiveness of human T lymphocytes to bacterial superantigens presented by cultured rheumatoid arthritis synoviocytes. Arthritis Rheum. 1996;39(1):125–36.

Shiozawa S, Shiozawa K, Fujita T. Morphologic observations in the early phase of the cartilage-pannus junction. Light and electron microscopic studies of active cellular pannus. Arthritis Rheum. 1983;26(4):472–8.

Firestein GS. Invasive fibroblast-like synoviocytes in rheumatoid arthritis. Passive responders or transformed aggressors? Arthritis Rheum. 1996;39(11):1781–90.

Muller-Ladner U, Kriegsmann J, Franklin BN, Matsumoto S, Geiler T, Gay RE, et al. Synovial fibroblasts of patients with rheumatoid arthritis attach to and invade normal human cartilage when engrafted into SCID mice. Am J Pathol. 1996;149(5):1607–15.

Ai R, Whitaker JW, Boyle DL, Tak PP, Gerlag DM, Wang W, et al. DNA Methylome Signature in Synoviocytes From Patients With Early Rheumatoid Arthritis Compared to Synoviocytes From Patients With Longstanding Rheumatoid Arthritis. Arthritis Rheumatol. 2015;67(7):1978–80.

Lefevre S, Knedla A, Tennie C, Kampmann A, Wunrau C, Dinser R, et al. Synovial fibroblasts spread rheumatoid arthritis to unaffected joints. Nat Med. 2009;15(12):1414–20.

Smolen JS, Aletaha D, Barton A, Burmester GR, Emery P, Firestein GS, et al. Rheumatoid arthritis. Nat Rev Dis Primers. 2018;4:18001.

Ramsay EE, Hogg PJ, Dilda PJ. Mitochondrial metabolism inhibitors for cancer therapy. Pharm Res. 2011;28(11):2731–44.

MacIver NJ, Michalek RD, Rathmell JC. Metabolic regulation of T lymphocytes. Annu Rev Immunol. 2013;31:259–83.

Ghesquiere B, Wong BW, Kuchnio A, Carmeliet P. Metabolism of stromal and immune cells in health and disease. Nature. 2014;511(7508):167–76.

Yin Y, Choi SC, Xu Z, Perry DJ, Seay H, Croker BP, et al. Normalization of CD4 + T cell metabolism reverses lupus. Sci Transl Med. 2015;7(274):274ra18.

McDonald G, Deepak S, Miguel L, Hall CJ, Isenberg DA, Magee AI, et al. Normalizing glycosphingolipids restores function in CD4 + T cells from lupus patients. J Clin Invest. 2014;124(2):712–24.

Metsios GS, Stavropoulos-Kalinoglou A, Nevill AM, Douglas KM, Koutedakis Y, Kitas GDJ. Cigarette smoking significantly increases basal metabolic rate in patients with rheumatoid arthritis. Gene. 2008;67(1):70–3.

Rall L, Roubenoff R. Rheumatoid cachexia: metabolic abnormalities, mechanisms and interventions. Rheumatology. 2004;43(10):1219–23.

Guma M, Tiziani S, Firestein GS. Metabolomics in rheumatic diseases: desperately seeking biomarkers. Nat Rev Rheumatol. 2016;12(5):269–81.

Bustamante MF, Garcia-Carbonell R, Whisenant KD, Guma M. Fibroblast-like synoviocyte metabolism in the pathogenesis of rheumatoid arthritis. Arthritis Res Ther. 2017;19(1):110.

Ahn JK, Kim S, Hwang J, Kim J, Kim KH, Cha HS. GC/TOF-MS-based metabolomic profiling in cultured fibroblast-like synoviocytes from rheumatoid arthritis. Joint Bone Spine. 2016;83(6):707–13.

Kim S, Hwang J, Xuan J, Jung YH, Cha H-S, Kim KH. Global metabolite profiling of synovial fluid for the specific diagnosis of rheumatoid arthritis from other inflammatory arthritis. PLoS One. 2014;9(6):e97501.

Garcia-Carbonell R, Divakaruni AS, Lodi A, Vicente-Suarez I, Saha A, Cheroutre H, et al. Critical Role of Glucose Metabolism in Rheumatoid Arthritis Fibroblast-like Synoviocytes. Arthritis Rheumatol. 2016;68(7):1614–26.

Volchenkov R, Dung Cao M, Elgstoen KB, Goll GL, Eikvar K, Bjorneboe O, et al. Metabolic profiling of synovial tissue shows altered glucose and choline metabolism in rheumatoid arthritis samples. Scand J Rheumatol. 2017;46(2):160–1.

Ahn JK, Kim S, Hwang J, Kim J, Kim KH, Cha H-S. GC/TOF-MS-based metabolomic profiling in cultured fibroblast-like synoviocytes from rheumatoid arthritis. Joint Bone Spine. 2016;83(6):707–13.

Guma M, Sanchez-Lopez E, Lodi A, Garcia-Carbonell R, Tiziani S, Karin M, et al. Choline kinase inhibition in rheumatoid arthritis. Ann Rheum Dis. 2015;74(7):1399–407.

Matsui T, Nakata N, Nagai S, Nakatani A, Takahashi M, Momose T, et al. Inflammatory cytokines and hypoxia contribute to 18F-FDG uptake by cells involved in pannus formation in rheumatoid arthritis. J Nucl Med. 2009;50(6):920–6.

de Oliveira PG, Farinon M, Sanchez-Lopez E, Miyamoto S, Guma M. Fibroblast-like synoviocytes glucose metabolism as a therapeutic target in rheumatoid arthritis. Front Immunol. 2019;10:1743.

Young SP, Kapoor SR, Viant MR, Byrne JJ, Filer A, Buckley CD, et al. The impact of inflammation on metabolomic profiles in patients with arthritis. Arthr Rhuem. 2013;65(8):2015–23.

Jiang M, Chen T, Feng H, Zhang Y, Li L, Zhao A, et al. Serum metabolic signatures of four types of human arthritis. J Proteome Res. 2013;12(8):3769–79.

de Molina AR, Gallego-Ortega D, Sarmentero-Estrada J, Lagares D, del Pulgar TG, Bandrés E, et al. Choline kinase as a link connecting phospholipid metabolism and cell cycle regulation: Implications in cancer therapy. Int J Biochem Cell Biol. 2008;40(9):1753–63.

Glunde K, Bhujwalla ZM, Ronen SM. Choline metabolism in malignant transformation. Nat Rev Cancer. 2011;11(12):835.

de Molina AR, Bánez-Coronel M, Gutiérrez R, Rodríguez-González A, Olmeda D, Megías D, et al. Choline kinase activation is a critical requirement for the proliferation of primary human mammary epithelial cells and breast tumor progression. Cancer Res. 2004;64(18):6732–9.

Biniecka M, Canavan M, McGarry T, Gao W, McCormick J, Cregan S, et al. Dysregulated bioenergetics: a key regulator of joint inflammation. Ann Rheum Dis. 2016;75(12):2192–200.

Mills E, O’Neill LA. Succinate: a metabolic signal in inflammation. Trends Cell Biol. 2014;24(5):313–20.

Zhu H, Chen L, Zhou W, Huang Z, Hu J, Dai S, et al. Over-expression of the ATP5J gene correlates with cell migration and 5-fluorouracil sensitivity in colorectal cancer. PloS one. 2013;8(10):e76846.

Cojocaru M, Cojocaru IM, Silosi I, Vrabie CDJM. Metabolic syndrome in rheumatoid arthritis. Mediators Inflamm. 2012;7(2):148.

Matsuo Y, Mizoguchi F, Saito T, Kawahata K, Ueha S, Matsushima K, et al. Local fibroblast proliferation but not influx is responsible for synovial hyperplasia in a murine model of rheumatoid arthritis. Biochem Biophys Res Commun. 2016;470(3):504–9.

Matsumoto S, Muller-Ladner U, Gay RE, Nishioka K, Gay S. Ultrastructural demonstration of apoptosis, Fas and Bcl-2 expression of rheumatoid synovial fibroblasts. J Rhuematol. 1996;23(8):1345–52.

Lee SY, Kwok SK, Son HJ, Ryu JG, Kim EK, Oh HJ, et al. IL-17-mediated Bcl-2 expression regulates survival of fibroblast-like synoviocytes in rheumatoid arthritis through STAT3 activation. Arthritis Res Ther. 2013;15(1):R31.

Cha HS, Rosengren S, Boyle DL, Firestein GS. PUMA regulation and proapoptotic effects in fibroblast-like synoviocytes. Arthritis Rheum. 2006;54(2):587–92.

You X, Boyle DL, Hammaker D, Firestein GS. PUMA-mediated apoptosis in fibroblast-like synoviocytes does not require p53. Arthritis Res Ther. 2006;8(6):R157.

Aupperle KR, Boyle DL, Hendrix M, Seftor EA, Zvaifler NJ, Barbosa M, et al. Regulation of synoviocyte proliferation, apoptosis, and invasion by the p53 tumor suppressor gene. Am J Pathol. 1998;152(4):1091–8.

Yu X, Li S. Non-metabolic functions of glycolytic enzymes in tumorigenesis. Oncogene. 2017;36(19):2629–36.

Tas SW, Maracle CX, Balogh E, Szekanecz Z. Targeting of proangiogenic signalling pathways in chronic inflammation. Nat Rev Rheumatol. 2016;12(2):111–22.

Del Rey MJ, Izquierdo E, Usategui A, Gonzalo E, Blanco FJ, Acquadro F, et al. The transcriptional response of normal and rheumatoid arthritis synovial fibroblasts to hypoxia. Arthritis Rheum. 2010;62(12):3584–94.

Biniecka M, Fox E, Gao W, Ng CT, Veale DJ, Fearon U, et al. Hypoxia induces mitochondrial mutagenesis dysfunction in inflammatory arthritis. 2011;63(8):2172–82.

Veale DJ, Fearon U. Inhibition of angiogenic pathways in rheumatoid arthritis: potential for therapeutic targeting. Best Pract Res Clin Rheumatol. 2006;20(5):941–7.

Lu Y, Yu SS, Zong M, Fan SS, Lu TB, Gong RH, et al. Glucose-6-Phosphate Isomerase (G6PI) Mediates Hypoxia-Induced Angiogenesis in Rheumatoid Arthritis. Sci Rep. 2017;7:40274.

Sapieha P, Sirinyan M, Hamel D, Zaniolo K, Joyal JS, Cho JH, et al. The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis. Nat Med. 2008;14(10):1067–76.

MacDonald IJ, Liu SC, Su CM, Wang YH, Tsai CH, Tang CH. Implications of angiogenesis involvement in arthritis. Int J Mol Sci. 2018;19:7.

Elshabrawy HA, Chen Z, Volin MV, Ravella S, Virupannavar S, Shahrara S. The pathogenic role of angiogenesis in rheumatoid arthritis. Angiogenesis. 2015;18(4):433–48.

Scott BB, Weisbrot LM, Greenwood JD, Bogoch ER, Paige CJ, Keystone EC. Rheumatoid arthritis synovial fibroblast and U937 macrophage/monocyte cell line interaction in cartilage degradation. Arthritis Rheum. 1997;40(3):490–8.

Peters MA, Wendholt D, Strietholt S, Frank S, Pundt N, Korb-Pap A, et al. The loss of alpha2beta1 integrin suppresses joint inflammation and cartilage destruction in mouse models of rheumatoid arthritis. Arthritis Rheum. 2012;64(5):1359–68.

Morales-Ducret J, Wayner E, Elices MJ, Alvaro-Gracia JM, Zvaifler NJ, Firestein GS. Alpha 4/beta 1 integrin (VLA-4) ligands in arthritis. Vascular cell adhesion molecule-1 expression in synovium and on fibroblast-like synoviocytes. J Immunol. 1992;149(4):1424–31.

McInnes IB, Leung BP, Liew FY. Cell-cell interactions in synovitis. Interactions between T lymphocytes and synovial cells. Arthritis Res. 2000;2(5):374–8.

Ata R, Antonescu CN. Integrins and cell metabolism: an intimate relationship impacting cancer. Int J Mol Sci. 2017;18:1.

Suto T, Karonitsch T. The immunobiology of mTOR in autoimmunity. J Autoimmun. 2020;110:102373.

Cantor JM, Ginsberg MH. CD98 at the crossroads of adaptive immunity and cancer. J Cell Sci. 2012;125(Pt 6):1373–82.

Tang MW, Malvar Fernandez B, Newsom SP, van Buul JD, Radstake T, Baeten DL, et al. Class 3 semaphorins modulate the invasive capacity of rheumatoid arthritis fibroblast-like synoviocytes. Rheumatology. 2018;57(5):909–20.

Remmers EF, Sano H, Wilder RL. Platelet-derived growth factors and heparin-binding (fibroblast) growth factors in the synovial tissue pathology of rheumatoid arthritis. Semin Arthritis Rheum. 1991;21(3):191–9.

Shibuya H, Yoshitomi H, Murata K, Kobayashi S, Furu M, Ishikawa M, et al. TNFalpha, PDGF, and TGFbeta synergistically induce synovial lining hyperplasia via inducible PI3Kdelta. Mod Rheumatol. 2015;25(1):72–8.

Thornton SC, Por SB, Penny R, Richter M, Shelley L, Breit SN. Identification of the major fibroblast growth factors released spontaneously in inflammatory arthritis as platelet derived growth factor and tumour necrosis factor-alpha. Clin Exp Immunol. 1991;86(1):79–86.

Rosengren S, Corr M, Boyle DL. Platelet-derived growth factor and transforming growth factor beta synergistically potentiate inflammatory mediator synthesis by fibroblast-like synoviocytes. Arthritis Res Ther. 2010;12(2):R65.

Lauzier A, Lavoie RR, Charbonneau M, Gouin-Boisvert B, Harper K, Dubois CM. Snail Is a Critical Mediator of Invadosome Formation and Joint Degradation in Arthritis. Am J Pathol. 2016;186(2):359–74.

Laragione T, Brenner M, Li W, Gulko PS. Cia5d regulates a new fibroblast-like synoviocyte invasion-associated gene expression signature. Arthritis Res Ther. 2008;10(4):R92.

Xue SN, Lei J, Lin DZ, Yang C, Yan L. Changes in biological behaviors of rat dermal fibroblasts induced by high expression of MMP9. World J Emerg Med. 2014;5(2):139–43.

Ai R, Laragione T, Hammaker D, Boyle DL, Wildberg A, Maeshima K, et al. Comprehensive epigenetic landscape of rheumatoid arthritis fibroblast-like synoviocytes. Nat Commun. 2018;9(1):1921.

Li D, Chen F, Ding J, Lin N, Li Z, Wang X. Knockdown of HIP1 expression promotes ligand–induced endocytosis of EGFR in HeLa cells. Oncol Rep. 2017;38(6):3387–91.

Wang J, Yu M, Guo Q, Ma Q, Hu C, Ma Z, et al. Prognostic significance of huntingtin interacting protein 1 expression on patients with acute myeloid leukemia. Sci Rep. 2017;7:45960.

Wang J, Yu M, Guo Q, Ma Q, Hu C, Ma Z, et al. Prognostic significance of huntingtin interacting protein 1 expression on patients with acute myeloid leukemia. Sci Rep. 2017;7:45960.

Igarashi H, Hirano H, Yahagi A, Saika T, Ishihara KJCI. Anti-apoptotic roles for the mutant p53R248Q through suppression of p53-regulated apoptosis-inducing protein 1 in the RA-derived fibroblast-like synoviocyte cell line MH7A. Resist. 2014;150(1):12–21.

Yamanishi Y, Boyle DL, Green DR, Keystone EC, Connor A, Zollman S, et al. p53 tumor suppressor gene mutations in fibroblast-like synoviocytes from erosion synovium and non-erosion synovium in rheumatoid arthritis. Gene. 2004;7(1):R12.

Lee YH, Ji JD, Kim A, Kim CH, Song GGJTKjoim. Expression of p53 protein in rheumatoid arthritis synovium. An immunohistochemical analysis. 1999;14(1):59.

Firestein GS, Nguyen K, Aupperle KR, Yeo M, Boyle DL, Zvaifler NJ. Apoptosis in rheumatoid arthritis: p53 overexpression in rheumatoid arthritis synovium. Am J Pathol. 1996;149(6):2143.

Xiao P, Hao Y, Zhu X, Wu X. p53 contributes to quercetin-induced apoptosis in human rheumatoid arthritis fibroblast-like synoviocytes. Inflammation. 2013;36(2):272–8.

Zhang T, Li H, Shi J, Li S, Li M, Zhang L, et al. p53 predominantly regulates IL-6 production and suppresses synovial inflammation in fibroblast-like synoviocytes and adjuvant-induced arthritis. Arthritis research therapy. 2016;18(1):271.

Rème T, Travaglio A, Gueydon E, Adla L, Jorgensen C, Sany JJC, et al. Mutations of the p53 tumour suppressor gene in erosive rheumatoid synovial tissue. Gene 1998;111(2):353.

Guo X, Zhang D, Zhang X, Jiang J, Xue P, Wu C, et al. Dyrk1A promotes the proliferation, migration and invasion of fibroblast-like synoviocytes in rheumatoid arthritis via down-regulating Spry2 and activating the ERK MAPK pathway. 2018;55:63–70.

Weisbart RH, Chan G, Heinze E, Mory R, Nishimura RN, Colburn KJJoBC. BRAF drives synovial fibroblast transformation in rheumatoid arthritis. 2010;285(45):34299–303.

Liu F, Feng XX, Zhu SL, Huang HY, Chen YD, Pan YF, et al. Sonic Hedgehog Signaling Pathway Mediates Proliferation and Migration of Fibroblast-Like Synoviocytes in Rheumatoid Arthritis via MAPK/ERK Signaling Pathway. Front Immunol. 2018;9:2847.

Lard L, Van Gaalen F, Schonkeren J, Pieterman E, Stoeken G, Vos K, et al. Association of the–2849 interleukin-10 promoter polymorphism with autoantibody production and joint destruction in rheumatoid arthritis. 2003;48(7):1841–8.

Aslani S, Mahmoudi M, Karami J, Jamshidi AR, Malekshahi Z, Nicknam MH. Epigenetic alterations underlying autoimmune diseases. Autoimmunity. 2016;49(2):69–83.

Karami J, Aslani S, Tahmasebi MN, Mousavi MJ, Sherafat Vaziri A, Jamshidi A, et al. Epigenetics in rheumatoid arthritis; fibroblast-like synoviocytes as an emerging paradigm in the disease pathogenesis. Immunology and Cell Biology. 2019.

Nakano K, Whitaker JW, Boyle DL, Wang W, Firestein GS. DNA methylome signature in rheumatoid arthritis. Ann Rheum Dis. 2013;72(1):110–7.

Frank-Bertoncelj M, Trenkmann M, Klein K, Karouzakis E, Rehrauer H, Bratus A, et al. Epigenetically-driven anatomical diversity of synovial fibroblasts guides joint-specific fibroblast functions. Nat Commun. 2017;8:14852.

Rhead B, Holingue C, Cole M, Shao X, Quach HL, Quach D, et al. Rheumatoid Arthritis Naive T Cells Share Hypermethylation Sites With Synoviocytes. Arthritis Rheumatol. 2017;69(3):550–9.

Bottini N, Firestein GS. Duality of fibroblast-like synoviocytes in RA: passive responders and imprinted aggressors. Nat Rev Rheumatol. 2013;9(1):24.

Ai R, Whitaker JW, Boyle DL, Tak PP, Gerlag DM, Wang W, et al. DNA methylome signature in synoviocytes from patients with early rheumatoid arthritis compared to synoviocytes from patients with longstanding rheumatoid arthritis. Arthritis rheumatology. 2015;67(7):1978–80.

Matsuda S, Hammaker D, Topolewski K, Briegel KJ, Boyle DL, Dowdy S, et al. Regulation of the cell cycle and inflammatory arthritis by the transcription cofactor LBH gene. The Journal of Immunology. 2017:ji1700719.

Hammaker D, Whitaker JW, Maeshima K, Boyle DL, Ekwall AKH, Wang W, et al. LBH gene transcription regulation by the interplay of an enhancer risk allele and DNA methylation in rheumatoid arthritis. Arthritis Rheumatology. 2016;68(11):2637–45.

Maeshima K, Stanford SM, Hammaker D, Sacchetti C, Zeng L-F, Ai R, et al. Abnormal PTPN11 enhancer methylation promotes rheumatoid arthritis fibroblast-like synoviocyte aggressiveness and joint inflammation. JCI Insight. 2016;1:7.

Neidhart M, Rethage J, Kuchen S, Künzler P, Crowl RM, Billingham ME, et al. Retrotransposable L1 elements expressed in rheumatoid arthritis synovial tissue: association with genomic DNA hypomethylation and influence on gene expression. Arthr Rhuem. 2000;43(12):2634–47.

Suzuki M, Tetsuka T, Yoshida S, Watanabe N, Kobayashi M, Matsui N, et al. The role of p38 mitogen-activated protein kinase in IL‐6 and IL‐8 production from the TNF‐α‐or IL‐1β‐stimulated rheumatoid synovial fibroblasts. FEBS Lett. 2000;465(1):23–7.

Ravanti L, Heino J, López-Otín C, Kähäri V-M. Induction of collagenase-3 (MMP-13) expression in human skin fibroblasts by three-dimensional collagen is mediated by p38 mitogen-activated protein kinase. J Biol Chem. 1999;274(4):2446–55.

Horiuchi M, Morinobu A, Chin T, Sakai Y, Kurosaka M, Kumagai S. Expression and function of histone deacetylases in rheumatoid arthritis synovial fibroblasts. J Rhuematol. 2009;36(8):1580–9.

Glozak M, Seto E. Histone deacetylases and cancer. Oncogene. 2007;26(37):5420.

Grabiec AM, Korchynskyi O, Tak PP, Reedquist KA. Histone deacetylase inhibitors suppress rheumatoid arthritis fibroblast-like synoviocyte and macrophage IL-6 production by accelerating mRNA decay. Ann Rheum Dis. 2012;71(3):424–31.

Jüngel A, Baresova V, Ospelt C, Simmen BR, Michel BA, Gay RE, et al. Trichostatin A sensitises rheumatoid arthritis synovial fibroblasts for TRAIL-induced apoptosis. Ann Rheum Dis. 2006;65(7):910–2.

Morinobu A, Wang B, Liu J, Yoshiya S, Kurosaka M, Kumagai S. Trichostatin A cooperates with Fas-mediated signal to induce apoptosis in rheumatoid arthritis synovial fibroblasts. J Rhuematol. 2006;33(6):1052–60.

Nakamura C, Matsushita I, Kosaka E, Kondo T, Kimura T. Anti-arthritic effects of combined treatment with histone deacetylase inhibitor and low-intensity ultrasound in the presence of microbubbles in human rheumatoid synovial cells. Rheumatology. 2008;47(4):418–24.

Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov. 2006;5(9):769.

Joosten LA, Leoni F, Meghji S, Mascagni P. Inhibition of HDAC activity by ITF2357 ameliorates joint inflammation and prevents cartilage and bone destruction in experimental arthritis. Molecular medicine. 2011;17(5–6):391–6.

Juan L-J, Shia W-J, Chen M-H, Yang W-M, Seto E, Lin Y-S, et al. Histone deacetylases specifically down-regulate p53-dependent gene activation. J Biol Chem. 2000;275(27):20436–43.

Nasu Y, Nishida K, Miyazawa S, Komiyama T, Kadota Y, Abe N, et al. Trichostatin A, a histone deacetylase inhibitor, suppresses synovial inflammation and subsequent cartilage destruction in a collagen antibody-induced arthritis mouse model. Osteoarthritis Cartilage. 2008;16(6):723–32.

Lin HS, Hu CY, Chan HY, Liew YY, Huang HP, Lepescheux L, et al. Anti-rheumatic activities of histone deacetylase (HDAC) inhibitors in vivo in collagen-induced arthritis in rodents. Br J Pharmacol. 2007;150(7):862–72.

Mu N, Gu J, Huang T, Zhang C, Shu Z, Li M, et al. A novel NF-κB/YY1/microRNA-10a regulatory circuit in fibroblast-like synoviocytes regulates inflammation in rheumatoid arthritis. Scientific reports. 2016;6:20059.

Hussain N, Zhu W, Jiang C, Xu J, Wu X, Geng M, et al. Down-regulation of miR‐10a‐5p in synoviocytes contributes to TBX5‐controlled joint inflammation. J Cell Mol Med. 2018;22(1):241–50.

Li D, Wang Y, Xu N, Wei Q, Wu M, Li X, et al. Follistatin-like protein 1 is elevated in systemic autoimmune diseases and correlated with disease activity in patients with rheumatoid arthritis. Arthritis research therapy. 2011;13(1):R17.

Hong W, Zhang P, Wang X, Tu J, Wei W. The Effects of MicroRNAs on Key Signalling Pathways and Epigenetic Modification in Fibroblast-Like Synoviocytes of Rheumatoid Arthritis. Mediators of inflammation. 2018;2018.

Salehi E, Eftekhari R, Oraei M, Gharib A, Bidad K. MicroRNAs in rheumatoid arthritis. Clin Rheumatol. 2015;34(4):615–28.

Niederer F, Trenkmann M, Ospelt C, Karouzakis E, Neidhart M, Stanczyk J, et al. Down-regulation of microRNA‐34a* in rheumatoid arthritis synovial fibroblasts promotes apoptosis resistance. Arthr Rhuem. 2012;64(6):1771–9.

Vicente R, Noël D, Pers Y-M, Apparailly F, Jorgensen C. Deregulation and therapeutic potential of microRNAs in arthritic diseases. Nat Rev Rheumatol. 2016;12(4):211.

Gao J, Zhou X-L, Kong R-N, Ji L-M, He L-L, Zhao D-B. microRNA-126 targeting PIK3R2 promotes rheumatoid arthritis synovial fibro-blasts proliferation and resistance to apoptosis by regulating PI3K/AKT pathway. Exp Mol Pathol. 2016;100(1):192–8.

Zhou Q, Long L, Shi G, Zhang J, Wu T, Zhou B. Research of the methylation status of miR-124a gene promoter among rheumatoid arthritis patients. Clinical and Developmental Immunology. 2013;2013.

Singh RP, Massachi I, Manickavel S, Singh S, Rao NP, Hasan S, et al. The role of miRNA in inflammation and autoimmunity. Autoimmun rev. 2013;12(12):1160–5.

Saferding V, Puchner A, Goncalves-Alves E, Hofmann M, Bonelli M, Brunner JS, et al. MicroRNA-146a governs fibroblast activation and joint pathology in arthritis. J Autoimmun. 2017;82:74–84.

Chen X-M, Huang Q-C, Yang S-L, Chu Y-L, Yan Y-H, Han L, et al. Role of micro RNAs in the pathogenesis of rheumatoid arthritis: novel perspectives based on review of the literature. Medicine. 2015;94(31).

Yang S, Yang Y. Downregulation of microRNA–221 decreases migration and invasion in fibroblast–like synoviocytes in rheumatoid arthritis. Mol Med Rep. 2015;12(2):2395–401.

Miao C-g, Shi W-j, Xiong Y-y, Yu H, Zhang X-l, Qin M-s, et al. MicroRNA-663 activates the canonical Wnt signaling through the adenomatous polyposis coli suppression. Immunology letters. 2015;166(1):45–54.

Chen Y, Xian P-F, Yang L, Wang S-X. MicroRNA-21 promotes proliferation of fibroblast-like synoviocytes through mediation of NF-κB nuclear translocation in a rat model of collagen-induced rheumatoid arthritis. BioMed research international. 2016;2016.

Shi X, Sun M, Liu H, Yao Y, Song YJCl. Long non-coding RNAs: a new frontier in the study of human diseases. 2013;339(2):159–66.

Mercer TR, Dinger ME, Mattick JSJNrg. Long non-coding RNAs: insights into functions. 2009;10(3):155.

Ye Y, Gao X, Yang N. LncRNA ZFAS1 promotes cell migration and invasion of fibroblast-like synoviocytes by suppression of miR-27a in rheumatoid arthritis. Hum Cell. 2018;31(1):14–21.

Pan F, Zhu L, Lv H, Pei C. Quercetin promotes the apoptosis of fibroblast-like synoviocytes in rheumatoid arthritis by upregulating lncRNA MALAT1. Int J Mol Med. 2016;38(5):1507–14.

Miao C-g, Yang Y-y, He X, Xu T, Huang C, Huang Y, et al. New advances of microRNAs in the pathogenesis of rheumatoid arthritis, with a focus on the crosstalk between DNA methylation and the microRNA machinery. Cellular signalling. 2013;25(5):1118–25.

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