NF-κB signaling in rheumatoid arthritis with focus on fibroblast-like synoviocytes

Arend WP, Dayer JM. Inhibition of the production and effects of interleukins-1 and tumor necrosis factor α in rheumatoid arthritis. Arthritis Rheum Official J American College Rheumatol. 1995;38:151–60. Bartok B, Firestein GS. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev. 2010;233:233–55. Mor A, Abramson SB, Pillinger MH. The fibroblast-like synovial cell in rheumatoid arthritis: a key player in inflammation and joint destruction. Clinical Immunol. 2005;115:118–28. Rhee DK, Marcelino J, Baker M, Gong Y, Smits P, Lefebvre V, et al. The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. J Clin Investig. 2005;115:622–31. Valin A, Pablos JL. The role of the transcriptional regulation of stromal cells in chronic inflammation. Biomolecules. 2015;5:2723–57. Bhatt D, Ghosh S. Regulation of the NF-κB-mediated transcription of inflammatory genes. Front Immunol. 2014;5:71. Dejardin E, Droin NM, Delhase M, Haas E, Cao Y, Makris C, et al. The lymphotoxin-β receptor induces different patterns of gene expression via two NF-κB pathways. Immunity. 2002;17:525–35. Udalova IA, Mott R, Field D, Kwiatkowski D. Quantitative prediction of NF-κB DNA–protein interactions. Proc Natl Acad Sci. 2002;99:8167–72. Sun S-C, Liu Z-G. A special issue on NF-κB signaling and function. Nature Publishing Group; 2011. Zhang H, Sun S-C. NF-κB in inflammation and renal diseases. Cell Biosci. 2015;5:63. Chen ZJ. Ubiquitination in signaling to and activation of IKK. Immunol Rev. 2012;246:95–106. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu Rev Immunol. 2000;18:621–63. Carlsen H, Alexander G, Austenaa LM, Ebihara K, Blomhoff R. Molecular imaging of the transcription factor NF-κB, a primary regulator of stress response. Mutation Res Fund Mol Mechanisms Mutagene. 2004;551:199–211. Yap HY, Tee SZY, Wong MMT, Chow SK, Peh SC, Teow SY. Pathogenic role of immune cells in rheumatoid arthritis: implications in clinical treatment and biomarker development. Cells. 2018;7:161. Isler P, Vey E, Zhang J-H, Dayer J-M. Cell surface glycoproteins expressed on activated human T cells induce production of interleukin-1 beta by monocytic cells: a possible role of CD69. Eur Cytokine Netw. 1993;4:15–23. Boniface K, Moynet D, Mossalayi MD. Role of Th17 cells in the pathogenesis of rheumatoid arthritis. World J Rheumatol. 2013;3:25–31. Smolen JS, Aletaha D, Barton A, Burmester GR, Emery P, Firestein GS, et al. Rheumatoid Arthritis. Nat Rev Dis Primers. 2018;4:18001. Walsh NC, Gravallese EM. Bone remodeling in rheumatic disease: a question of balance. Immunol Rev. 2010;233:301–12. Pennock ND, White JT, Cross EW, Cheney EE, Tamburini BA, Kedl RM. T cell responses: naive to memory and everything in between. Adv Physiol Educ. 2013;37:273–83. Hwang S-Y, Kim J-Y, Kim K-W, Park M-K, Moon Y, Kim W-U, et al. IL-17 induces production of IL-6 and IL-8 in rheumatoid arthritis synovial fibroblasts via NF-κB-and PI3-kinase/Akt-dependent pathways. Arthritis Res Ther. 2004;6:R120. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124:783–801. Lebre MC, Jongbloed SL, Tas SW, Smeets TJ, McInnes IB, Tak PP. Rheumatoid arthritis synovium contains two subsets of CD83 − DC-LAMP − dendritic cells with distinct cytokine profiles. The American journal of pathology. 2008;172:940-50. Santiago-Schwarz F, Anand P, Liu S, Carsons SE. Dendritic cells (DCs) in rheumatoid arthritis (RA): progenitor cells and soluble factors contained in RA synovial fluid yield a subset of myeloid DCs that preferentially activate Th1 inflammatory-type responses. J Immunol. 2001;167:1758–68. Tran CN, Lundy SK, Fox DA. Synovial biology and T cells in rheumatoid arthritis. Pathophysiology. 2005;12:183–9. Samuels J, Ng YS, Coupillaud C, Paget D, Meffre E. Impaired early B cell tolerance in patients with rheumatoid arthritis. J Exp Med. 2005;201:1659–67. Edwards JC, Szczepański L, Szechiński J, Filipowicz-Sosnowska A, Emery P, Close DR, et al. Efficacy of B-cell–targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med. 2004;350:2572–81. Moore J, Ma D, Will R, Cannell P, Handel M, Milliken S. A phase II study of Rituximab in rheumatoid arthritis patients with recurrent disease following haematopoietic stem cell transplantation. Bone Marrow Transplant. 2004;34:241. Ehrhardt GR, Hijikata A, Kitamura H, Ohara O, Wang J-Y, Cooper MD. Discriminating gene expression profiles of memory B cell subpopulations. J Exp Med. 2008;205:1807–17. Meednu N, Zhang H, Owen T, Sun W, Wang V, Cistrone C, et al. Production of RANKL by memory B cells: a link between B cells and bone erosion in rheumatoid arthritis. Arthritis Rheumatol. 2016;68:805–16. Li Y, Toraldo G, Li A, Yang X, Zhang H, Qian W-P, et al. B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood. 2007;109:3839–48. Pistoia V. Production of cytokines by human B cells in health and disease. Immunol Today. 1997;18:343–50. Miranda-Carús M-E, Balsa A, Benito-Miguel M, de Ayala CP, Martín-Mola E. IL-15 and the initiation of cell contact-dependent synovial fibroblast-T lymphocyte cross-talk in rheumatoid arthritis: effect of methotrexate. J Immunol. 2004;173:1463–76. Nakatsuka K, Tanaka Y, Hubscher S, Abe M, Wake A, Saito K, et al. Rheumatoid synovial fibroblasts are stimulated by the cellular adhesion to T cells through lymphocyte function associated antigen-1/intercellular adhesion molecule-1. J Rheumatol. 1997;24:458–64. 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;166:2270–5. Goronzy JJ, Henel G, Sawai H, Singh K, Lee EB, Pryshchep S, et al. Costimulatory pathways in rheumatoid synovitis and T-cell senescence. Ann N Y Acad Sci. 2005;1062:182–94. Sawai H, Park YW, He X, Goronzy JJ, Weyand CM. Fractalkine mediates T cell–dependent proliferation of synovial fibroblasts in rheumatoid arthritis. Arthritis Rheum. 2007;56:3215–25. Vallabhapurapu S, Karin M. Regulation and function of NF-κB transcription factors in the immune system. Annu Rev Immunol. 2009;27:693–733. Tas SW, de Jong EC, Hajji N, May MJ, Ghosh S, Vervoordeldonk MJ, et al. Selective inhibition of NF-κB in dendritic cells by the NEMO-binding domain peptide blocks maturation and prevents T cell proliferation and polarization. Eur J Immunol. 2005;35:1164–74. Tas SW, Vervoordeldonk MJ, Hajji N, Schuitemaker JH, van der Sluijs KF, May MJ, et al. Noncanonical NF-κB signaling in dendritic cells is required for indoleamine 2, 3-dioxygenase (IDO) induction and immune regulation. Blood. 2007;110:1540–9. Hofmann J, Mair F, Greter M, Schmidt-Supprian M, Becher B. NIK signaling in dendritic cells but not in T cells is required for the development of effector T cells and cell-mediated immune responses. J Exp Med. 2011;208:1917–29. Kaileh M, Sen R. NF-κB function in B lymphocytes. Immunol Rev. 2012;246:254–71. Mills DM, Bonizzi G, Karin M, Rickert RC. Regulation of late B cell differentiation by intrinsic IKKα-dependent signals. Proc Natl Acad Sci. 2007;104:6359–64. Gardam S, Sierro F, Basten A, Mackay F, Brink R. TRAF2 and TRAF3 signal adapters act cooperatively to control the maturation and survival signals delivered to B cells by the BAFF receptor. Immunity. 2008;28:391–401. McCarthy BA, Yang L, Ding J, Ren M, King W, ElSalanty M, et al. NF-κB2 mutation targets survival, proliferation and differentiation pathways in the pathogenesis of plasma cell tumors. BMC Cancer. 2012;12:203. Oh H, Ghosh S. NF-κB: roles and regulation in different CD 4 + T-cell subsets. Immunol Rev. 2013;252:41–51. Chang M, Jin W, Chang J-H, Xiao Y, Brittain GC, Yu J, et al. The ubiquitin ligase Peli1 negatively regulates T cell activation and prevents autoimmunity. Nat Immunol. 2011;12:1002. Aronica MA, Mora AL, Mitchell DB, Finn PW, Johnson JE, Sheller JR, et al. Preferential role for NF-κB/Rel signaling in the type 1 but not type 2 T cell-dependent immune response in vivo. J Immunol. 1999;163:5116–24. Ruan Q, Kameswaran V, Zhang Y, Zheng S, Sun J, Wang J, et al. The Th17 immune response is controlled by the Rel–RORγ–RORγT transcriptional axis. J Exp Med. 2011;208:2321–33. Long M, Park S-G, Strickland I, Hayden MS, Ghosh S. Nuclear factor-κB modulates regulatory T cell development by directly regulating expression of Foxp3 transcription factor. Immunity. 2009;31:921–31. Ruan Q, Kameswaran V, Tone Y, Li L, Liou H-C, Greene MI, et al. Development of Foxp3 + regulatory T cells is driven by the c-Rel enhanceosome. Immunity. 2009;31:932–40. Dhar A, Chawla M, Chattopadhyay S, Oswal N, Umar D, Gupta S, et al. Role of NF-kappaB2-p100 in regulatory T cell homeostasis and activation. Sci Rep. 2019;9:1–18. Murray SE. Cell-intrinsic role for NF-kappa B-inducing kinase in peripheral maintenance but not thymic development of Foxp3 + regulatory T cells in mice. PloS one. 2013;8. Noort AR, Tak PP, Tas SW. Non-canonical NF-κB signaling in rheumatoid arthritis: Dr Jekyll and Mr Hyde? Arthritis Res Ther. 2015;17:15. Kang YM, Kim SY, Kang JH, Han SW, Nam EJ, Kyung HS, et al. LIGHT up-regulated on B lymphocytes and monocytes in rheumatoid arthritis mediates cellular adhesion and metalloproteinase production by synoviocytes. Arthritis Rheum. 2007;56:1106–17. Lee HY, Jeon HS, Song EK, Han MK, Park SI, Lee SI, et al. CD40 ligation of rheumatoid synovial fibroblasts regulates RANKL-medicated osteoclastogenesis: Evidence of NF-κB–dependent, CD40-mediated bone destruction in rheumatoid arthritis. Arthritis Rheum. 2006;54:1747–58. van Amelsfort JM, Jacobs KM, Bijlsma JW, Lafeber FP, Taams LS. CD4 + CD25 + regulatory T cells in rheumatoid arthritis: differences in the presence, phenotype, and function between peripheral blood and synovial fluid. Arthritis RheumOfficial J Am College Rheumatol. 2004;50:2775–85. Beavis PA, Gregory B, Green P, Cribbs AP, Kennedy A, Amjadi P, et al. Resistance to regulatory T cell-mediated suppression in rheumatoid arthritis can be bypassed by ectopic foxp3 expression in pathogenic synovial T cells. Proc Natl Acad Sci. 2011;108:16717–22. Nie H, Zheng Y, Li R, Guo TB, He D, Fang L, et al. Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNF-α in rheumatoid arthritis. Nat Med. 2013;19:322. Lohr J, Knoechel B, Abbas AK. Regulatory T cells in the periphery. Immunol Rev. 2006;212:149–62. Josefowicz SZ, Lu L-F, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol. 2012;30:531–64. Isomura I, Palmer S, Grumont RJ, Bunting K, Hoyne G, Wilkinson N, et al. c-Rel is required for the development of thymic Foxp3 + CD4 regulatory T cells. J Exp Med. 2009;206:3001–14. Polesso F, Sarker M, Anderson A, Parker DC, Murray SE. Constitutive expression of NF-κB inducing kinase in regulatory T cells impairs suppressive function and promotes instability and pro-inflammatory cytokine production. Sci Rep. 2017;7:14779. Nagar M, Jacob-Hirsch J, Vernitsky H, Berkun Y, Ben-Horin S, Amariglio N, et al. TNF Activates a NF-κB–Regulated Cellular Program in Human CD45RA–Regulatory T Cells that Modulates Their Suppressive Function. J Immunol. 2010;184:3570–81. Schaer DA, Budhu S, Liu C, Bryson C, Malandro N, Cohen A, et al. GITR pathway activation abrogates tumor immune suppression through loss of regulatory T-cell lineage stability. Cancer Immunol Res. 2013;1:320–31. Voo KS, Bover L, Harline ML, Vien LT, Facchinetti V, Arima K, et al. Antibodies targeting human OX40 expand effector T cells and block inducible and natural regulatory T cell function. J Immunol. 2013;191:3641–50. Kleijwegt FS, Laban S, Duinkerken G, Joosten AM, Zaldumbide A, Nikolic T, et al. Critical role for TNF in the induction of human antigen-specific regulatory T cells by tolerogenic dendritic cells. J Immunol. 2010;185:1412–8. Okubo Y, Mera T, Wang L, Faustman DL. Homogeneous expansion of human T-regulatory cells via tumor necrosis factor receptor 2. Sci Rep. 2013;3:3153. Ruby CE, Yates MA, Hirschhorn-Cymerman D, Chlebeck P, Wolchok JD, Houghton AN, et al. Cutting Edge: OX40 agonists can drive regulatory T cell expansion if the cytokine milieu is right. J Immunol. 2009;183:4853–7. Matsumura T, Saito Y, Suzuki T, Teramoto A, Ozasa Y, Yamashita T, et al. Phosphorylated platelet-derived growth factor receptor-positive cells with anti-apoptotic properties accumulate in the synovium of patients with rheumatoid arthritis. Front Immunol. 2019;10:241. Allen JB, Manthey CL, Hand AR, Ohura K, Ellingsworth L, Wahl S. Rapid onset synovial inflammation and hyperplasia induced by transforming growth factor beta. J Exp Med. 1990;171:231–47. Ota F, Maeshima A, Yamashita S, Ikeuchi H, Kaneko Y, Kuroiwa T, et al. Activin A induces cell proliferation of fibroblast-like synoviocytes in rheumatoid arthritis. Arthritis Rheum Official J Am College Rheumatol. 2003;48:2442–9. Han Z, Boyle DL, Aupperle KR, Bennett B, Manning AM, Firestein GS. Jun N-terminal kinase in rheumatoid arthritis. J Pharmacol Exp Ther. 1999;291:124–30. Müller-Ladner U, Kriegsmann J, Gay RE, Gay S. Oncogenes in rheumatoid arthritis. Rheum Dis Clin North Am. 1995;21:675–90. Sun Y, Cheung HS, editors. p53, proto-oncogene and rheumatoid arthritis. Seminars in arthritis and rheumatism; 2002: Elsevier. Makarov SS. NF-κB in rheumatoid arthritis: a pivotal regulator of inflammation, hyperplasia, and tissue destruction. Arthritis Res Ther. 2001;3:200. Romashkova JA, Makarov SS. NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature. 1999;401:86. Niedermeier M, Pap T, Korb A. Therapeutic opportunities in fibroblasts in inflammatory arthritis. Best Pract Res Clin Rheumatol. 2010;24:527–40. García S, Liz M, Gómez-Reino JJ, Conde C. Akt activity protects rheumatoid synovial fibroblasts from Fas-induced apoptosis by inhibition of Bid cleavage. Arthritis Research Ther. 2010;12:R33. Firestein GS, Yeo M, Zvaifler NJ. Apoptosis in rheumatoid arthritis synovium. J Clin Investig. 1995;96:1631–8. Jeong S-J, Pise-Masison CA, Radonovich MF, Park HU, Brady JN. A novel NF-κB pathway involving IKKβ and p65/RelA Ser-536 phosphorylation results in p53 inhibition in the absence of NF-κB transcriptional activity. J Biol Chem. 2005;280:10326–32. Simmonds RE, Foxwell BM. Signalling, inflammation and arthritis: NF-κ B and its relevance to arthritis and inflammation. Rheumatology. 2008;47:584–90. Li G, Xia Z, Liu Y, Meng F, Wu X, Fang Y, et al. SIRT1 inhibits rheumatoid arthritis fibroblast-like synoviocyte aggressiveness and inflammatory response via suppressing NF-κB pathway. Biosci Rep. 2018;38:BSR20180541. Micheau O, Lens S, Gaide O, Alevizopoulos K, Tschopp J. NF-κB signals induce the expression of c-FLIP. Mol Cell Biol. 2001;21:5299–305. Urbano PCM, Soccol VT, Azevedo VF. Apoptosis and the FLIP and NF-kappa B proteins as pharmacodynamic criteria for biosimilar TNF-alpha antagonists. Biologics: targets & therapy. 2014;8:211. Zhang HG, Hyde K, Page GP, Brand JP, Zhou J, Yu S, et al. Novel tumor necrosis factor α–regulated genes in rheumatoid arthritis. Arthritis Rheum Official J Am College Rheumatol. 2004;50:420–31. Yoshitomi H. Regulation of immune responses and chronic inflammation by fibroblast-like synoviocytes. Front Immunol. 2019;10:1395. Okazaki Y, Sawada T, Nagatani K, Komagata Y, Inoue T, Muto S, et al. Effect of nuclear factor-kappaB inhibition on rheumatoid fibroblast-like synoviocytes and collagen induced arthritis. J Rheumatol. 2005;32:1440–7. Aupperle KR, Bennett BL, Han Z, Boyle DL, Manning AM, Firestein GS. NF-κB regulation by IκB kinase-2 in rheumatoid arthritis synoviocytes. J Immunol. 2001;166:2705–11. Sweeney SE, Hammaker D, Boyle DL, Firestein GS. Regulation of c-Jun phosphorylation by the IκB kinase-ε complex in fibroblast-like synoviocytes. J Immunol. 2005;174:6424–30. Crow MK. Type I interferon in organ-targeted autoimmune and inflammatory diseases. Arthritis Res Ther. 2010;12:S5. Brennan FM, McInnes IB. Evidence that cytokines play a role in rheumatoid arthritis. J Clin Investig. 2008;118:3537–45. Bottini N, Firestein GS. Duality of fibroblast-like synoviocytes in RA: passive responders and imprinted aggressors. Nat Rev Rheumatol. 2013;9:24. Müller-Ladner U, Elices M, Kriegsmann J, Strahl D, Gay R, Firestein G, et al. Alternatively spliced CS-1 fibronectin isoform and its receptor VLA-4 in rheumatoid arthritis synovium. J Rheumatol. 1997;24:1873–80. Lindy O, Konttinen YT, Sorsa T, Ding Y, Santavirta S, Ceponis A, et al. Matrix metalloproteinase 13 (collagenase 3) in human rheumatoid synovium. Arthritis Rheum Official J Am College Rheumatol. 1997;40:1391–9. Martel-Pelletier J, Welsch DJ, Pelletier J-P. Metalloproteases and inhibitors in arthritic diseases. Best Pract Res Clin Rheumatol. 2001;15:805–29. Seemayer CA, Kuchen S, Kuenzler P, Řihošková V, Rethage J, Aicher WK, et al. Cartilage destruction mediated by synovial fibroblasts does not depend on proliferation in rheumatoid arthritis. Am J Pathol. 2003;162:1549–57. Sorsa T, Konttinen Y, Lindy O, Ritchlin C, Saari H, Suomalainen K, et al., editors. Collagenase in synovitis of rheumatoid arthritis. Seminars in arthritis and rheumatism; 1992: Elsevier. Tolboom T, Pieterman E, Van der Laan W, Toes R, Huidekoper A, Nelissen R, et al. Invasive properties of fibroblast-like synoviocytes: correlation with growth characteristics and expression of MMP-1, MMP-3, and MMP-10. Ann Rheum Dis. 2002;61:975–80. Chabaud M, Fossiez F, Taupin J-L, Miossec P. Enhancing effect of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor production by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines. J Immunol. 1998;161:409–14. Burrage PS, Mix KS, Brinckerhoff CE. Matrix metalloproteinases: role in arthritis. Front Biosci. 2006;11:529–43. Xue M, McKelvey K, Shen K, Minhas N, March L, Park S-Y, et al. Endogenous MMP-9 and not MMP-2 promotes rheumatoid synovial fibroblast survival, inflammation and cartilage degradation. Rheumatology. 2014;53:2270–9. Jiménez MJ, Balbín M, López JM, Alvarez J, Komori T, López-Otín C. Collagenase 3 is a target of Cbfa1, a transcription factor of the runt gene family involved in bone formation. Mol Cell Biol. 1999;19:4431–42. Mengshol JA, Vincenti MP, Brinckerhoff CE. IL-1 induces collagenase-3 (MMP-13) promoter activity in stably transfected chondrocytic cells: requirement for Runx-2 and activation by p38 MAPK and JNK pathways. Nucleic Acids Res. 2001;29:4361–72.