Peptidylarginine deiminase 2 is required for tumor necrosis factor alpha-induced citrullination and arthritis, but not neutrophil extracellular trap formation

van Venrooij, 2011, Anti-CCP antibodies: the past, the present and the future, Nat. Rev. Rheumatol., 7, 391, 10.1038/nrrheum.2011.76 Makrygiannakis, 2006, Citrullination is an inflammation-dependent process, Ann. Rheum. Dis., 65, 1219, 10.1136/ard.2005.049403 Kinloch, 2008, Synovial fluid is a site of citrullination of autoantigens in inflammatory arthritis, Arthritis Rheum., 58, 2287, 10.1002/art.23618 Hou, 2013, PADI4 polymorphisms and susceptibility to rheumatoid arthritis: a meta-analysis, Mod. Rheumatol., 23, 50, 10.3109/s10165-012-0639-4 Kang, 2006, A functional haplotype of the PADI4 gene associated with increased rheumatoid arthritis susceptibility in Koreans, Arthritis Rheum., 54, 90, 10.1002/art.21536 Gandjbakhch, 2009, A functional haplotype of PADI4 gene in rheumatoid arthritis: positive correlation in a French population, J. Rheumatol., 36, 881, 10.3899/jrheum.080398 Panati, 2012, Association of single nucleotide polymorphisms (SNPs) of PADI4 gene with rheumatoid arthritis (RA) in Indian population, Genes Genet. Syst., 87, 191, 10.1266/ggs.87.191 Plenge, 2005, Replication of putative candidate-gene associations with rheumatoid arthritis in >4,000 samples from North America and Sweden: association of susceptibility with PTPN22, CTLA4, and PADI4, Am. J. Hum. Genet., 77, 1044, 10.1086/498651 Suzuki, 2003, Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginine deiminase 4, are associated with rheumatoid arthritis, Nat. Genet., 34, 395, 10.1038/ng1206 Takata, 2008, Replication of reported genetic associations of PADI4, FCRL3, SLC22A4 and RUNX1 genes with rheumatoid arthritis: results of an independent Japanese population and evidence from meta-analysis of East Asian studies, J. Hum. Genet., 53, 163, 10.1007/s10038-007-0232-4 Too, 2012, Polymorphisms in peptidylarginine deiminase associate with rheumatoid arthritis in diverse Asian populations: evidence from MyEIRA study and meta-analysis, Arthritis Res. Ther., 14, R250, 10.1186/ar4093 Chang, 2013, PADI2 is significantly associated with rheumatoid arthritis, PLoS One, 8, e81259, 10.1371/journal.pone.0081259 Darrah, 2012, Peptidylarginine deiminase 2, 3 and 4 have distinct specificities against cellular substrates: novel insights into autoantigen selection in rheumatoid arthritis, Ann. Rheum. Dis., 71, 92, 10.1136/ard.2011.151712 Chang, 2005, Localization of peptidylarginine deiminase 4 (PADI4) and citrullinated protein in synovial tissue of rheumatoid arthritis, Rheumatol. Oxf., 44, 40, 10.1093/rheumatology/keh414 Vossenaar, 2004, Expression and activity of citrullinating peptidylarginine deiminase enzymes in monocytes and macrophages, Ann. Rheum. Dis., 63, 373, 10.1136/ard.2003.012211 Foulquier, 2007, Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation, Arthritis Rheum., 56, 3541, 10.1002/art.22983 Makrygiannakis, 2012, Local administration of glucocorticoids decrease synovial citrullination in rheumatoid arthritis, Arthritis Res. Ther., 14, R20, 10.1186/ar3702 Willis, 2011, N-alpha-benzoyl-N5-(2-chloro-1-iminoethyl)-L-ornithine amide, a protein arginine deiminase inhibitor, reduces the severity of murine collagen-induced arthritis, J. Immunol., 186, 4396, 10.4049/jimmunol.1001620 Romero, 2013, Immune-mediated pore-forming pathways induce cellular hypercitrullination and generate citrullinated autoantigens in rheumatoid arthritis, Sci. Transl. Med., 5, 10.1126/scitranslmed.3006869 Andrade, 2010, Autocitrullination of human peptidyl arginine deiminase type 4 regulates protein citrullination during cell activation, Arthritis Rheum., 62, 1630, 10.1002/art.27439 Lewallen, 2015, Chemical proteomic platform to identify citrullinated proteins, ACS Chem. Biol., 10, 2520, 10.1021/acschembio.5b00438 Blachere, 2016, High titer rheumatoid arthritis antibodies preferentially bind fibrinogen citrullinated by peptidyl arginine deiminase 4, Arthritis Rheumatol. Subramanian, 2015, Design, synthesis, and biological evaluation of tetrazole analogs of Cl-amidine as protein arginine deiminase inhibitors, J. Med. Chem., 58, 1337, 10.1021/jm501636x Lewis, 2015, Inhibition of PAD4 activity is sufficient to disrupt mouse and human NET formation, Nat. Chem. Biol., 11, 189, 10.1038/nchembio.1735 Shelef, 2014, Peptidylarginine deiminase 4 contributes to tumor necrosis factor alpha-induced inflammatory arthritis, Arthritis Rheumatol., 66, 1482, 10.1002/art.38393 Suzuki, 2016, Decreased severity of experimental autoimmune arthritis in peptidylarginine deiminase type 4 knockout mice, BMC Musculoskelet. Disord., 17, 205, 10.1186/s12891-016-1055-2 Seri, 2015, Peptidylarginine deiminase type 4 deficiency reduced arthritis severity in a glucose-6-phosphate isomerase-induced arthritis model, Sci. Rep., 5, 13041, 10.1038/srep13041 Li, 2010, PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps, J. Exp. Med., 207, 1853, 10.1084/jem.20100239 Hemmers, 2011, PAD4-mediated neutrophil extracellular trap formation is not required for immunity against influenza infection, PLoS One, 6, e22043, 10.1371/journal.pone.0022043 Khandpur, 2013, NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis, Sci. Transl. Med., 5, 10.1126/scitranslmed.3005580 Bawadekar, 2016, Tumor necrosis factor alpha, citrullination, and peptidylarginine deiminase 4 in lung and joint inflammation, Arthritis Res. Ther., 18, 173, 10.1186/s13075-016-1068-0 Damgaard, 2016, Increased levels of peptidylarginine deiminase 2 in synovial fluid from anti-CCP-positive rheumatoid arthritis patients: association with disease activity and inflammatory markers, Rheumatol. Oxf., 55, 918, 10.1093/rheumatology/kev440 van Beers, 2013, Peptidylarginine deiminase expression and activity in PAD2 knock-out and PAD4-low mice, Biochimie, 95, 299, 10.1016/j.biochi.2012.09.029 Raijmakers, 2006, Experimental autoimmune encephalomyelitis induction in peptidylarginine deiminase 2 knockout mice, J. Comp. Neurol., 498, 217, 10.1002/cne.21055 Assohou-Luty, 2014, The human peptidylarginine deiminases type 2 and type 4 have distinct substrate specificities, Biochim. Biophys. Acta, 1844, 829, 10.1016/j.bbapap.2014.02.019 Spengler, 2015, Release of active peptidyl arginine deiminases by neutrophils can explain production of extracellular citrullinated autoantigens in rheumatoid arthritis synovial fluid, Arthritis Rheumatol., 67, 3135, 10.1002/art.39313 Zhang, 2012, Peptidylarginine deiminase 2-catalyzed histone H3 arginine 26 citrullination facilitates estrogen receptor alpha target gene activation, Proc. Natl. Acad. Sci. U. S. A., 109, 13331, 10.1073/pnas.1203280109 Douni, 1995, Transgenic and knockout analyses of the role of TNF in immune regulation and disease pathogenesis, J. Inflamm., 47, 27 Damgaard, 2014, Generation of monoclonal antibodies against peptidylarginine deiminase 2 (PAD2) and development of a PAD2-specific enzyme-linked immunosorbent assay, J. Immunol. Methods, 405, 15, 10.1016/j.jim.2013.12.008 Nett, 2011, Optimizing a Candida biofilm microtiter plate model for measurement of antifungal susceptibility by tetrazolium salt assay, J. Clin. Microbiol., 49, 1426, 10.1128/JCM.02273-10 Johnson, 2016, The extracellular matrix of Candida albicans biofilms impairs formation of neutrophil extracellular traps, PLoS Pathog., 12, e1005884, 10.1371/journal.ppat.1005884 Gillum, 1984, Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations, Mol. Gen. Genet., 198, 179, 10.1007/BF00328721 Urban, 2006, Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms, Cell. Microbiol., 8, 668, 10.1111/j.1462-5822.2005.00659.x Urban, 2006, Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms, Cell Microbiol., 8, 668, 10.1111/j.1462-5822.2005.00659.x Shapiro-Shelef, 2005, Regulation of plasma-cell development, Nat. Rev. Immunol., 5, 230, 10.1038/nri1572 Takahara, 1983, Purification and characterization of peptidylarginine deiminase from rabbit skeletal muscle, J. Biochem., 94, 1945, 10.1093/oxfordjournals.jbchem.a134548 Bicker, 2012, Seeing citrulline: development of a phenylglyoxal-based probe to visualize protein citrullination, J. Am. Chem. Soc., 134, 17015, 10.1021/ja308871v Nicholas, 2002, Preparation of a monoclonal antibody to citrullinated epitopes: its characterization and some applications to immunohistochemistry in human brain, Glia, 37, 328, 10.1002/glia.10039 Bang, 2010, Peptidyl arginine deiminase type IV (PADI4) haplotypes interact with shared epitope regardless of anti-cyclic citrullinated peptide antibody or erosive joint status in rheumatoid arthritis: a case control study, Arthritis Res. Ther., 12, R115, 10.1186/ar3051 Chen, 2008, Haplotypes of PADI4 susceptible to rheumatoid arthritis are also associated with ulcerative colitis in the Japanese population, Clin. Immunol., 126, 165, 10.1016/j.clim.2007.09.001 Schellekens, 1998, Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies, J. Clin. Invest., 101, 273, 10.1172/JCI1316 Nakashima, 2013, PAD4 regulates proliferation of multipotent haematopoietic cells by controlling c-myc expression, Nat. Commun., 4, 1836, 10.1038/ncomms2862 Jourdan, 2014, IL-6 supports the generation of human long-lived plasma cells in combination with either APRIL or stromal cell-soluble factors, Leukemia, 28, 1647, 10.1038/leu.2014.61 McNee, 2017, Citrullination of histone H3 drives IL-6 production by bone marrow mesenchymal stem cells in MGUS and multiple myeloma, Leukemia, 31, 373, 10.1038/leu.2016.187