384
Views
5
CrossRef citations to date
0
Altmetric
Review

Epigenetic Alterations in Rheumatoid Arthritis Fibroblast-Like Synoviocytes

, &
Pages 479-492 | Received 31 Oct 2016, Accepted 02 Feb 2017, Published online: 21 Mar 2017

References

  • Aho K , KoskenvuoM , TuominenJ , KaprioJ . Occurrence of rheumatoid arthritis in a nationwide series of twins . J. Rheumatol.13 ( 5 ), 899 – 902 ( 1986 ).
  • Macgregor AJ , SniederH , RigbyASet al. Characterizing the quantitative genetic contribution to rheumatoid arthritis using data from twins . Arthritis Rheum.43 ( 1 ), 30 – 37 ( 2000 ).
  • Okada Y , WuD , TrynkaGet al. Genetics of rheumatoid arthritis contributes to biology and drug discovery . Nature506 ( 7488 ), 376 – 381 ( 2014 ).
  • Stahl EA , RaychaudhuriS , RemmersEFet al. Genome-wide association study meta-analysis identifies seven new rheumatoid arthritis risk loci . Nat. Genet.42 ( 6 ), 508 – 514 ( 2010 ).
  • Svendsen AJ , KyvikKO , HouenGet al. On the origin of rheumatoid arthritis: the impact of environment and genes – a population based twin study . PLoS ONE8 ( 2 ), e57304 ( 2013 ).
  • Sparks JA , ChangSC , DeaneKDet al. Associations of smoking and age with inflammatory joint signs among first-degree relatives without rheumatoid arthritis: results from the Studies of the Etiology of RA . Arthritis Rheumatol.68 ( 8 ), 1828 – 1838 ( 2016 ).
  • Pedersen M , JacobsenS , GarredPet al. Strong combined gene-environment effects in anti-cyclic citrullinated peptide-positive rheumatoid arthritis: a nationwide case-control study in Denmark . Arthritis Rheum.56 ( 5 ), 1446 – 1453 ( 2007 ).
  • Zhang X , ZhangD , JiaHet al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment . Nat. Med.21 ( 8 ), 895 – 905 ( 2015 ).
  • Jacobsson LT , JacobssonME , AsklingJ , KnowlerWC . Perinatal characteristics and risk of rheumatoid arthritis . BMJ326 ( 7398 ), 1068 – 1069 ( 2003 ).
  • Karlson EW , MandlLA , HankinsonSE , GrodsteinF . Do breast-feeding and other reproductive factors influence future risk of rheumatoid arthritis? Results from the Nurses’ Health Study . Arthritis Rheum.50 ( 11 ), 3458 – 3467 ( 2004 ).
  • Bartok B , FiresteinGS . Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis . Immunol. Rev.233 ( 1 ), 233 – 255 ( 2010 ).
  • Bottini N , FiresteinGS . Duality of fibroblast-like synoviocytes in RA: passive responders and imprinted aggressors . Nat. Rev. Rheumatol.9 ( 1 ), 24 – 33 ( 2013 ).
  • Lefevre S , KnedlaA , TennieCet al. Synovial fibroblasts spread rheumatoid arthritis to unaffected joints . Nat. Med.15 ( 12 ), 1414 – 1420 ( 2009 ).
  • Robertson KD . DNA methylation and human disease . Nat. Rev. Genet.6 ( 8 ), 597 – 610 ( 2005 ).
  • Jin B , LiY , RobertsonKD . DNA methylation: superior or subordinate in the epigenetic hierarchy?Genes Cancer2 ( 6 ), 607 – 617 ( 2011 ).
  • Schubeler D . Function and information content of DNA methylation . Nature517 ( 7534 ), 321 – 326 ( 2015 ).
  • Subramaniam D , ThombreR , DharA , AnantS . DNA methyltransferases: a novel target for prevention and therapy . Front. Oncol.4 , 80 ( 2014 ).
  • Klutstein M , NejmanD , GreenfieldR , CedarH . DNA methylation in cancer and aging . Cancer Res.76 ( 12 ), 3446 – 3450 ( 2016 ).
  • Klein HU , De JagerPL . Uncovering the role of the methylome in dementia and neurodegeneration . Trends Mol. Med.22 ( 8 ), 687 – 700 ( 2016 ).
  • Gupta B , HawkinsRD . Epigenomics of autoimmune diseases . Immunol. Cell Biol.93 ( 3 ), 271 – 276 ( 2015 ).
  • Bottini N , FiresteinGS . Epigenetics in rheumatoid arthritis: a primer for rheumatologists . Curr. Rheumatol. Rep.15 ( 11 ), 372 ( 2013 ).
  • Cribbs A , FeldmannM , OppermannU . Towards an understanding of the role of DNA methylation in rheumatoid arthritis: therapeutic and diagnostic implications . Ther. Adv. Musculoskelet. Dis.7 ( 5 ), 206 – 219 ( 2015 ).
  • Corvetta A , Della BittaR , LuchettiMM , PomponioG . 5-Methylcytosine content of DNA in blood, synovial mononuclear cells and synovial tissue from patients affected by autoimmune rheumatic diseases . J. Chromatogr.566 ( 2 ), 481 – 491 ( 1991 ).
  • Karouzakis E , GayRE , MichelBA , GayS , NeidhartM . DNA hypomethylation in rheumatoid arthritis synovial fibroblasts . Arthritis Rheum.60 ( 12 ), 3613 – 3622 ( 2009 ).
  • Kazazian HH Jr . Genetics. L1 retrotransposons shape the mammalian genome . Science289 ( 5482 ), 1152 – 1153 ( 2000 ).
  • Yang AS , EstecioMR , DoshiK , KondoY , TajaraEH , IssaJP . A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements . Nucleic Acids Res.32 ( 3 ), e38 ( 2004 ).
  • Nakano K , WhitakerJW , BoyleDL , WangW , FiresteinGS . DNA methylome signature in rheumatoid arthritis . Ann. Rheum. Dis.72 ( 1 ), 110 – 117 ( 2013 ).
  • Whitaker JW , ShoemakerR , BoyleDLet al. An imprinted rheumatoid arthritis methylome signature reflects pathogenic phenotype . Genome Med.5 ( 4 ), 40 ( 2013 ).
  • Ai R , WhitakerJW , BoyleDLet al. DNA methylome signature in synoviocytes from patients with early rheumatoid arthritis compared to synoviocytes from patients with longstanding rheumatoid arthritis . Arthritis Rheumatol.67 ( 7 ), 1978 – 1980 ( 2015 ).
  • Ai R , HammakerD , BoyleDLet al. Joint-specific DNA methylation and transcriptome signatures in rheumatoid arthritis identify distinct pathogenic processes . Nat Commun7 , 11849 ( 2016 ).
  • Glossop JR , HaworthKE , EmesRDet al. DNA methylation profiling of synovial fluid FLS in rheumatoid arthritis reveals changes common with tissue-derived FLS . Epigenomics7 ( 4 ), 539 – 551 ( 2015 ).
  • Karouzakis E , GayRE , GayS , NeidhartM . Increased recycling of polyamines is associated with global DNA hypomethylation in rheumatoid arthritis synovial fibroblasts . Arthritis Rheum.64 ( 6 ), 1809 – 1817 ( 2012 ).
  • Nakano K , BoyleDL , FiresteinGS . Regulation of DNA methylation in rheumatoid arthritis synoviocytes . J. Immunol.190 ( 3 ), 1297 – 1303 ( 2013 ).
  • Karouzakis E , RengelY , JungelAet al. DNA methylation regulates the expression of CXCL12 in rheumatoid arthritis synovial fibroblasts . Genes Immun.12 ( 8 ), 643 – 652 ( 2011 ).
  • Karouzakis E , TrenkmannM , GayRE , MichelBA , GayS , NeidhartM . Epigenome analysis reveals TBX5 as a novel transcription factor involved in the activation of rheumatoid arthritis synovial fibroblasts . J. Immunol.193 ( 10 ), 4945 – 4951 ( 2014 ).
  • Whitaker JW , BoyleDL , BartokBet al. Integrative omics analysis of rheumatoid arthritis identifies non-obvious therapeutic targets . PLoS ONE10 ( 4 ), e0124254 ( 2015 ).
  • Ekwall AK , WhitakerJW , HammakerD , BugbeeWD , WangW , FiresteinGS . The rheumatoid arthritis risk gene LBH regulates growth in fibroblast-like synoviocytes . Arthritis Rheumatol.67 ( 5 ), 1193 – 1202 ( 2015 ).
  • Hammaker D , WhitakerJW , MaeshimaKet al. Limb bud and heart development gene transcription is regulated by the interplay of an enhancer risk allele and DNA methylation in rheumatoid arthritis . Arthritis Rheumatol.68 ( 11 ), 2637 – 2645 ( 2016 ).
  • Maeshima K , StanfordSM , HammakerDet al. Abnormal PTPN11 enhancer methylation promotes rheumatoid arthritis fibroblast-like synoviocyte aggressiveness and joint inflammation . JCI Insight1 ( 7 ), e86580 ( 2016 ).
  • Stanford SM , MaestreMF , CampbellAMet al. Protein tyrosine phosphatase expression profile of rheumatoid arthritis fibroblast-like synoviocytes: a novel role of SH2 domain-containing phosphatase 2 as a modulator of invasion and survival . Arthritis Rheum.65 ( 5 ), 1171 – 1180 ( 2013 ).
  • Tessarz P , KouzaridesT . Histone core modifications regulating nucleosome structure and dynamics . Nat. Rev. Mol. Cell Biol.15 ( 11 ), 703 – 708 ( 2014 ).
  • Wang F , ChenFF , GaoWBet al. Identification of citrullinated peptides in the synovial fluid of patients with rheumatoid arthritis using LC-MALDI-TOF/TOF . Clin. Rheumatol.35 ( 9 ), 2185 – 2194 ( 2016 ).
  • Falkenberg KJ , JohnstoneRW . Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders . Nat. Rev. Drug Discov.13 ( 9 ), 673 – 691 ( 2014 ).
  • Chen HP , ZhaoYT , ZhaoTC . Histone deacetylases and mechanisms of regulation of gene expression . Crit. Rev. Oncog.20 ( 1–2 ), 35 – 47 ( 2015 ).
  • Huber LC , BrockM , HemmatazadHet al. Histone deacetylase/acetylase activity in total synovial tissue derived from rheumatoid arthritis and osteoarthritis patients . Arthritis Rheum.56 ( 4 ), 1087 – 1093 ( 2007 ).
  • Kawabata T , NishidaK , TakasugiKet al. Increased activity and expression of histone deacetylase 1 in relation to tumor necrosis factor-alpha in synovial tissue of rheumatoid arthritis . Arthritis Res. Ther.12 ( 4 ), R133 ( 2010 ).
  • Horiuchi M , MorinobuA , ChinT , SakaiY , KurosakaM , KumagaiS . Expression and function of histone deacetylases in rheumatoid arthritis synovial fibroblasts . J. Rheumatol.36 ( 8 ), 1580 – 1589 ( 2009 ).
  • Lee A , QiaoY , GrigorievGet al. Tumor necrosis factor alpha induces sustained signaling and a prolonged and unremitting inflammatory response in rheumatoid arthritis synovial fibroblasts . Arthritis Rheum.65 ( 4 ), 928 – 938 ( 2013 ).
  • Sohn C , LeeA , QiaoY , LoupasakisK , IvashkivLB , KallioliasGD . Prolonged tumor necrosis factor alpha primes fibroblast-like synoviocytes in a gene-specific manner by altering chromatin . Arthritis Rheumatol.67 ( 1 ), 86 – 95 ( 2015 ).
  • Angiolilli C , GrabiecAM , FergusonBSet al. Inflammatory cytokines epigenetically regulate rheumatoid arthritis fibroblast-like synoviocyte activation by suppressing HDAC5 expression . Ann. Rheum. Dis.75 ( 2 ), 430 – 438 ( 2016 ).
  • Glozak MA , SetoE . Histone deacetylases and cancer . Oncogene26 ( 37 ), 5420 – 5432 ( 2007 ).
  • Yoshida M , KijimaM , AkitaM , BeppuT . Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A . J. Biol. Chem.265 ( 28 ), 17174 – 17179 ( 1990 ).
  • Jungel A , BaresovaV , OspeltCet al. Trichostatin A sensitises rheumatoid arthritis synovial fibroblasts for TRAIL-induced apoptosis . Ann. Rheum. Dis.65 ( 7 ), 910 – 912 ( 2006 ).
  • Morinobu A , WangB , LiuJ , YoshiyaS , KurosakaM , KumagaiS . Trichostatin A cooperates with FAS-mediated signal to induce apoptosis in rheumatoid arthritis synovial fibroblasts . J. Rheumatol.33 ( 6 ), 1052 – 1060 ( 2006 ).
  • Nakamura C , MatsushitaI , KosakaE , KondoT , KimuraT . 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 (Oxford)47 ( 4 ), 418 – 424 ( 2008 ).
  • Zhang Y , ZhangB . Trichostatin A, an inhibitor of histone deacetylase, inhibits the viability and invasiveness of hypoxic rheumatoid arthritis fibroblast-like synoviocytes via PI3K/Akt signaling . J. Biochem. Mol. Toxicol.30 ( 4 ), doi:10.1002/jbt ( 2015 ) ( Epub ahead of print ).
  • Grabiec AM , KorchynskyiO , TakPP , ReedquistKA . Histone deacetylase inhibitors suppress rheumatoid arthritis fibroblast-like synoviocyte and macrophage IL-6 production by accelerating mRNA decay . Ann. Rheum. Dis.71 ( 3 ), 424 – 431 ( 2012 ).
  • Chung YL , LeeMY , WangAJ , YaoLF . A therapeutic strategy uses histone deacetylase inhibitors to modulate the expression of genes involved in the pathogenesis of rheumatoid arthritis . Mol. Ther.8 ( 5 ), 707 – 717 ( 2003 ).
  • Joosten LA , LeoniF , MeghjiS , MascagniP . Inhibition of HDAC activity by ITF2357 ameliorates joint inflammation and prevents cartilage and bone destruction in experimental arthritis . Mol. Med.17 ( 5–6 ), 391 – 396 ( 2011 ).
  • Vojinovic J , DamjanovN , D’urzoCet al. Safety and efficacy of an oral histone deacetylase inhibitor in systemic-onset juvenile idiopathic arthritis . Arthritis Rheum.63 ( 5 ), 1452 – 1458 ( 2011 ).
  • Nishida K , KomiyamaT , MiyazawaSet al. Histone deacetylase inhibitor suppression of autoantibody-mediated arthritis in mice via regulation of p16INK4a and p21(WAF1/Cip1) expression . Arthritis Rheum.50 ( 10 ), 3365 – 3376 ( 2004 ).
  • Choo QY , HoPC , TanakaY , LinHS . Histone deacetylase inhibitors MS-275 and SAHA induced growth arrest and suppressed lipopolysaccharide-stimulated NF-kappaB p65 nuclear accumulation in human rheumatoid arthritis synovial fibroblastic E11 cells . Rheumatology (Oxford)49 ( 8 ), 1447 – 1460 ( 2010 ).
  • Chen H , PanJ , WangJD , LiaoQM , XiaXR . Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, induces apoptosis in rheumatoid arthritis fibroblast-like synoviocytes . Inflammation39 ( 1 ), 39 – 46 ( 2016 ).
  • Wang J , ZhangW , ZouHet al. 10-Hydroxy-2-decenoic acid inhibiting the proliferation of fibroblast-like synoviocytes by PI3K-AKT pathway . Int. Immunopharmacol.28 ( 1 ), 97 – 104 ( 2015 ).
  • Li M , LiuX , SunXet al. Therapeutic effects of NK-HDAC-1, a novel histone deacetylase inhibitor, on collagen-induced arthritis through the induction of apoptosis of fibroblast-like synoviocytes . Inflammation36 ( 4 ), 888 – 896 ( 2013 ).
  • Lee J , HongEC , JeongHet al. A novel histone deacetylase 6-selective inhibitor suppresses synovial inflammation and joint destruction in a collagen antibody-induced arthritis mouse model . Int. J. Rheum. Dis.18 ( 5 ), 514 – 523 ( 2015 ).
  • Filippakopoulos P , KnappS . Targeting bromodomains: epigenetic readers of lysine acetylation . Nat. Rev. Drug Discov.13 ( 5 ), 337 – 356 ( 2014 ).
  • Park-Min KH , LimE , LeeMJet al. Inhibition of osteoclastogenesis and inflammatory bone resorption by targeting BET proteins and epigenetic regulation . Nat. Commun.5 , 5418 ( 2014 ).
  • Zhang QG , QianJ , ZhuYC . Targeting bromodomain-containing protein 4 (BRD4) benefits rheumatoid arthritis . Immunol. Lett.166 ( 2 ), 103 – 108 ( 2015 ).
  • Klein K , KabalaPA , GrabiecAMet al. The bromodomain protein inhibitor I-BET151 suppresses expression of inflammatory genes and matrix degrading enzymes in rheumatoid arthritis synovial fibroblasts . Ann. Rheum. Dis.75 ( 2 ), 422 – 429 ( 2016 ).
  • Hammond SM . An overview of microRNAs . Adv. Drug Deliv. Rev.87 , 3 – 14 ( 2015 ).
  • Di Leva G , GarofaloM , CroceCM . MicroRNAs in cancer . Annu. Rev. Pathol.9 , 287 – 314 ( 2014 ).
  • Simpson LJ , AnselKM . MicroRNA regulation of lymphocyte tolerance and autoimmunity . J. Clin. Invest.125 ( 6 ), 2242 – 2249 ( 2015 ).
  • Vicente R , NoelD , PersYM , ApparaillyF , JorgensenC . Deregulation and therapeutic potential of microRNAs in arthritic diseases . Nat. Rev. Rheumatol.12 ( 4 ), 211 – 220 ( 2016 ).
  • Nakamachi Y , KawanoS , TakenokuchiMet al. MicroRNA-124a is a key regulator of proliferation and monocyte chemoattractant protein 1 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis . Arthritis Rheum.60 ( 5 ), 1294 – 1304 ( 2009 ).
  • Pandis I , OspeltC , KaragianniNet al. Identification of microRNA-221/222 and microRNA-323–3p association with rheumatoid arthritis via predictions using the human tumour necrosis factor transgenic mouse model . Ann. Rheum. Dis.71 ( 10 ), 1716 – 1723 ( 2012 ).
  • De La Rica L , UrquizaJM , Gomez-CabreroDet al. Identification of novel markers in rheumatoid arthritis through integrated analysis of DNA methylation and microRNA expression . J. Autoimmun.41 , 6 – 16 ( 2013 ).
  • Yang S , YangY . Downregulation of microRNA221 decreases migration and invasion in fibroblastlike synoviocytes in rheumatoid arthritis . Mol. Med. Rep.12 ( 2 ), 2395 – 2401 ( 2015 ).
  • Stanczyk J , OspeltC , KarouzakisEet al. Altered expression of microRNA-203 in rheumatoid arthritis synovial fibroblasts and its role in fibroblast activation . Arthritis Rheum.63 ( 2 ), 373 – 381 ( 2011 ).
  • Miao CG , ShiWJ , XiongYYet al. MicroRNA-663 activates the canonical Wnt signaling through the adenomatous polyposis coli suppression . Immunol. Lett.166 ( 1 ), 45 – 54 ( 2015 ).
  • Stanczyk J , PedrioliDM , BrentanoFet al. Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis . Arthritis Rheum.58 ( 4 ), 1001 – 1009 ( 2008 ).
  • Long L , YuP , LiuYet al. Upregulated microRNA-155 expression in peripheral blood mononuclear cells and fibroblast-like synoviocytes in rheumatoid arthritis . Clin. Dev. Immunol. 2013296139 ( 2013 ).
  • Kurowska-Stolarska M , AliverniniS , BallantineLEet al. MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis . Proc. Natl Acad. Sci. USA108 ( 27 ), 11193 – 11198 ( 2011 ).
  • Kawano S , NakamachiY . miR-124a as a key regulator of proliferation and MCP-1 secretion in synoviocytes from patients with rheumatoid arthritis . Ann. Rheum. Dis.70 ( Suppl. 1 ), i88 – i91 ( 2011 ).
  • Nakamachi Y , OhnumaK , UtoK , NoguchiY , SaegusaJ , KawanoS . MicroRNA-124 inhibits the progression of adjuvant-induced arthritis in rats . Ann. Rheum. Dis.75 ( 3 ), 601 – 608 ( 2016 ).
  • Niederer F , TrenkmannM , OspeltCet al. Down-regulation of microRNA-34a* in rheumatoid arthritis synovial fibroblasts promotes apoptosis resistance . Arthritis Rheum.64 ( 6 ), 1771 – 1779 ( 2012 ).
  • Zhu S , PanW , SongXet al. The microRNA miR-23b suppresses IL-17-associated autoimmune inflammation by targeting TAB2, TAB3 and IKK-alpha . Nat. Med.18 ( 7 ), 1077 – 1086 ( 2012 ).
  • Zhang Y , XuYZ , SunNet al. Long noncoding RNA expression profile in fibroblast-like synoviocytes from patients with rheumatoid arthritis . Arthritis Res. Ther.18 ( 1 ), 227 ( 2016 ).
  • Tsaprouni LG , YangTP , BellJet al. Cigarette smoking reduces DNA methylation levels at multiple genomic loci but the effect is partially reversible upon cessation . Epigenetics9 ( 10 ), 1382 – 1396 ( 2014 ).
  • Mu N , GuJ , HuangTet al. A novel NF-kappaB/YY1/microRNA-10a regulatory circuit in fibroblast-like synoviocytes regulates inflammation in rheumatoid arthritis . Sci. Rep.6 , 20059 ( 2016 ).
  • Trenkmann M , BrockM , GayRE , MichelBA , GayS , HuberLC . Tumor necrosis factor alpha-induced microRNA-18a activates rheumatoid arthritis synovial fibroblasts through a feedback loop in NF-kappaB signaling . Arthritis Rheum.65 ( 4 ), 916 – 927 ( 2013 ).
  • Philippe L , AlsalehG , SuffertGet al. TLR2 expression is regulated by microRNA miR-19 in rheumatoid fibroblast-like synoviocytes . J. Immunol.188 ( 1 ), 454 – 461 ( 2012 ).
  • Gantier MP , StundenHJ , MccoyCEet al. A miR-19 regulon that controls NF-kappaB signaling . Nucleic Acids Res.40 ( 16 ), 8048 – 8058 ( 2012 ).
  • Philippe L , AlsalehG , PichotAet al. MiR-20a regulates ASK1 expression and TLR4-dependent cytokine release in rheumatoid fibroblast-like synoviocytes . Ann. Rheum. Dis.72 ( 6 ), 1071 – 1079 ( 2013 ).
  • Alsaleh G , SuffertG , SemaanNet al. Bruton’s tyrosine kinase is involved in miR-346-related regulation of IL-18 release by lipopolysaccharide-activated rheumatoid fibroblast-like synoviocytes . J. Immunol.182 ( 8 ), 5088 – 5097 ( 2009 ).
  • Semaan N , FrenzelL , AlsalehGet al. miR-346 controls release of TNF-alpha protein and stability of its mRNA in rheumatoid arthritis via tristetraprolin stabilization . PLoS ONE6 ( 5 ), e19827 ( 2011 ).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.