Reactive oxygen species inhibit catalytic activity of peptidylarginine deiminase

References

• Takahara H, Okamoto H, Sugawara K. Calcium-dependent properties of peptidylarginine deiminase from rabbit skeletal muscle. Agric Biol Chem 1986;50:2899–904.
   Web of Science ®Google Scholar
• Vossenaar ER, Zendman AJ, van Venrooij WJ, Pruijn GJ. PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. Bioessays 2003;25:1106–18.
   PubMed Web of Science ®Google Scholar
• Foulquier C, Sebbag M, Clavel C, et al. 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 2007;56:3541–53.
   PubMed Web of Science ®Google Scholar
• Harauz G, Musse AA. A tale of two citrullines – structural and functional aspects of myelin basic protein deimination in health and disease. Neurochem Res 2007;32:137–58.
   PubMed Web of Science ®Google Scholar
• Rondas D, Crevecoeur I, D’Hertog W, et al. Citrullinated glucose-regulated protein 78 is an autoantigen in type 1 diabetes. Diabetes 2015;64:573–86.
   PubMed Web of Science ®Google Scholar
• Herrera-Esparza R, Rodriguez-Rodriguez M, Perez-Perez ME, et al. Posttranslational protein modification in the salivary glands of Sjogren’s syndrome patients. Autoimmune Dis 2013;2013:548064.
   PubMedGoogle Scholar
• Cherrington BD, Zhang X, McElwee JL, et al. Potential role for PAD2 in gene regulation in breast cancer cells. PLoS One 2012;7(7):e41242.
   PubMed Web of Science ®Google Scholar
• Terakawa H, Takahara H, Sugawara K. Three types of mouse peptidylarginine deiminase: characterization and tissue distribution. J Biochem 1991;110:661–6.
   PubMed Web of Science ®Google Scholar
• Griffith OW. Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic Biol Med 1999;27:922–35.
   PubMed Web of Science ®Google Scholar
• Jones DP. Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol 2002;348:93–112.
   PubMed Web of Science ®Google Scholar
• Damgaard D, Bjorn ME, Steffensen MA, et al. Reduced glutathione as a physiological co-activator in the activation of peptidylarginine deiminase. Arthritis Res Ther 2016;18:102.
   PubMed Web of Science ®Google Scholar
• Babior BM, Kipnes RS, Curnutte JT. Biological defense mechanisms. The production by leukocytes of superoxide, a potential bactericidal agent. J Clin Invest 1973;52:741–4.
   PubMed Web of Science ®Google Scholar
• Rossi F, Zatti M. Biochemical aspects of phagocytosis in polymorphonuclear leucocytes. NADH and NADPH oxidation by the granules of resting and phagocytizing cells. Experientia 1964;20:21–3.
   PubMedGoogle Scholar
• Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 1998;92:3007–17.
   PubMed Web of Science ®Google Scholar
• Winterbourn CC, Kettle AJ, Hampton MB. Reactive Oxygen Species and Neutrophil Function. Annu Rev Biochem 2016;85:765–92.
   PubMed Web of Science ®Google Scholar
• Nathan CF. Neutrophil activation on biological surfaces. Massive secretion of hydrogen peroxide in response to products of macrophages and lymphocytes. J Clin Invest 1987;80:1550–60.
   PubMed Web of Science ®Google Scholar
• Robinson JM. Reactive oxygen species in phagocytic leukocytes. Histochem Cell Biol 2008;130:281–97.
   PubMed Web of Science ®Google Scholar
• Galgiani JN. Differences in oxidant release by human polymorphonuclear leukocytes produced by stimulation with different phases of Coccidioides immitis. J Infect Dis 1995;172:199–203.
   PubMed Web of Science ®Google Scholar
• Goldstein IM, Roos D, Kaplan HB, Weissmann G. Complement and immunoglobulins stimulate superoxide production by human leukocytes independently of phagocytosis. J Clin Invest 1975;56:1155–63.
   PubMed Web of Science ®Google Scholar
• Sumimoto H, Takeshige K, Minakami S. Superoxide production of human polymorphonuclear leukocytes stimulated by leukotriene B4. Biochim Biophys Acta 1984 16;803:271–7.
   PubMed Web of Science ®Google Scholar
• Tzeng DY, Deuel TF, Huang JS, et al. Platelet-derived growth factor promotes polymorphonuclear leukocyte activation. Blood 1984;64:1123–8.
   PubMed Web of Science ®Google Scholar
• Badwey JA, Curnutte JT, Karnovsky ML. cis-Polyunsaturated fatty acids induce high levels of superoxide production by human neutrophils. J Biol Chem 1981;256:12640–3.
   PubMed Web of Science ®Google Scholar
• Li P, Li M, Lindberg MR, et al. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med 2010 30;207:1853–62.
   PubMed Web of Science ®Google Scholar
• Neeli I, Khan SN, Radic M. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 2008;180:1895–902.
   PubMed Web of Science ®Google Scholar
• Fuchs TA, Abed U, Goosmann C, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007;176:231–41.
   PubMed Web of Science ®Google Scholar
• Rohrbach AS, Slade DJ, Thompson PR, Mowen KA. Activation of PAD4 in NET formation. Front Immunol 2012;3:360.
   PubMed Web of Science ®Google Scholar
• Wang F, Chen FF, Gao WB, et al. Identification of citrullinated peptides in the synovial fluid of patients with rheumatoid arthritis using LC-MALDI-TOF/TOF. Clin Rheumatol 2016;35:2185–94.
   PubMed Web of Science ®Google Scholar
• van Beers JJ, Schwarte CM, Stammen-Vogelzangs J, et al. The rheumatoid arthritis synovial fluid citrullinome reveals novel citrullinated epitopes in apolipoprotein E, myeloid nuclear differentiation antigen, and beta-actin. Arthritis Rheum 2013;65:69–80.
   PubMed Web of Science ®Google Scholar
• Raijmakers R, Zendman AJ, Egberts WV, et al. Methylation of arginine residues interferes with citrullination by peptidylarginine deiminases in vitro. J Mol Biol 2007;367:1118–29.
   PubMed Web of Science ®Google Scholar
• O’Donnell BV, Tew DG, Jones OT, England PJ. Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem J 1993;290:41–9.
   PubMed Web of Science ®Google Scholar
• Damgaard D, Palarasah Y, Skjodt K, et al. Generation of monoclonal antibodies against peptidylarginine deiminase 2 (PAD2) and development of a PAD2-specific enzyme-linked immunosorbent assay. J Immunol Methods 2014;405:15–22.
   PubMed Web of Science ®Google Scholar
• Nakayama-Hamada M, Suzuki A, Kubota K, et al. Comparison of enzymatic properties between hPADI2 and hPADI4. Biochem Biophys Res Commun 2005;327:192–200.
   PubMed Web of Science ®Google Scholar
• Damgaard D, Senolt L, Nielsen M, et al. Demonstration of extracellular peptidylarginine deiminase (PAD) activity in synovial fluid of patients with rheumatoid arthritis using a novel assay for citrullination of fibrinogen. Arthritis Res Ther 2014;16:498.
   PubMed Web of Science ®Google Scholar
• Sim S, Yong TS, Park SJ, et al. NADPH oxidase-derived reactive oxygen species-mediated activation of ERK1/2 is required for apoptosis of human neutrophils induced by Entamoeba histolytica. J Immunol 2005;174:4279–88.
   PubMed Web of Science ®Google Scholar
• Ohno Y, Gallin JI. Diffusion of extracellular hydrogen peroxide into intracellular compartments of human neutrophils. Studies utilizing the inactivation of myeloperoxidase by hydrogen peroxide and azide. J Biol Chem 1985;260:8438–46.
   PubMed Web of Science ®Google Scholar
• DeChatelet LR, Shirley PS, Johnston RB, Jr. Effect of phorbol myristate acetate on the oxidative metabolism of human polymorphonuclear leukocytes. Blood 1976;47:545–54.
   PubMed Web of Science ®Google Scholar
• Koren K, Jensen PO, Kuhl M. Development of a rechargeable optical hydrogen peroxide sensor – sensor design and biological application. Analyst 2016;141:4332–9.
   PubMed Web of Science ®Google Scholar
• Test ST, Weiss SJ. Quantitative and temporal characterization of the extracellular H2O2 pool generated by human neutrophils. J Biol Chem 1984;259:399–405.
   PubMed Web of Science ®Google Scholar
• Konig MF, Abusleme L, Reinholdt J, et al. Aggregatibacter actinomycetemcomitans-induced hypercitrullination links periodontal infection to autoimmunity in rheumatoid arthritis. Sci Transl Med 2016;8:369ra176.
   PubMed Web of Science ®Google Scholar
• Stoiber W, Obermayer A, Steinbacher P, Krautgartner WD. The role of reactive oxygen species (ROS) in the formation of extracellular traps (ETs) in humans. Biomolecules 2015;5:702–23.
   PubMed Web of Science ®Google Scholar
• Halliwell B, Clement MV, Long LH. Hydrogen peroxide in the human body. FEBS Lett 2000;486:10–13.
   PubMed Web of Science ®Google Scholar
• Forman HJ, Bernardo A, Davies KJ. What is the concentration of hydrogen peroxide in blood and plasma? Arch Biochem Biophys 2016;603:48–53.
   PubMed Web of Science ®Google Scholar
• Winterbourn CC, Hampton MB, Livesey JH, Kettle AJ. Modeling the reactions of superoxide and myeloperoxidase in the neutrophil phagosome: implications for microbial killing. J Biol Chem 2006;281:39860–9.
   PubMed Web of Science ®Google Scholar
• Neeli I, Radic M. Opposition between PKC isoforms regulates histone deimination and neutrophil extracellular chromatin release. Front Immunol 2013;4:38.
   PubMed Web of Science ®Google Scholar
• Konig MF, Andrade F. A critical reappraisal of neutrophil extracellular traps and NETosis mimics based on differential requirements for protein citrullination. Front Immunol 2016;7:461.
   PubMed Web of Science ®Google Scholar
• Gorlach A, Bertram K, Hudecova S, Krizanova O. Calcium and ROS: a mutual interplay. Redox Biol 2015;6:260–71.
   PubMed Web of Science ®Google Scholar
• Mazars C, Thuleau P, Lamotte O, Bourque S. Cross-talk between ROS and calcium in regulation of nuclear activities. Mol Plant 2010;3:706–18.
   PubMed Web of Science ®Google Scholar
• Sredzinska K, Galicka A, Porowska H, et al. Glutathione reductase activity correlates with concentration of extracellular matrix degradation products in synovial fluid from patients with joint diseases. Acta Biochim Pol 2009;56:635–40.
   PubMed Web of Science ®Google Scholar
• Yoshida S, Katoh T, Tetsuka T, et al. Involvement of thioredoxin in rheumatoid arthritis: its costimulatory roles in the TNF-alpha-induced production of IL-6 and IL-8 from cultured synovial fibroblasts. J Immunol 1999;163:351–8.
   PubMed Web of Science ®Google Scholar
• Sato H, Takahashi T, Ide H, et al. Antioxidant activity of synovial fluid, hyaluronic acid, and two subcomponents of hyaluronic acid. Synovial fluid scavenging effect is enhanced in rheumatoid arthritis patients. Arthritis Rheum 1988;31:63–71.
   PubMed Web of Science ®Google Scholar
• Ediz L, Hiz O, Ozkol H, et al. Relationship between anti-CCP antibodies and oxidant and anti-oxidant activity in patients with rheumatoid arthritis. Int J Med Sci 2011;8:139–47.
   PubMed Web of Science ®Google Scholar
• McGovern NN, Cowburn AS, Porter L, et al. Hypoxia selectively inhibits respiratory burst activity and killing of Staphylococcus aureus in human neutrophils. J Immunol 2011;186:453–63.
   PubMed Web of Science ®Google Scholar
• Nisimoto Y, Diebold BA, Cosentino-Gomes D, Lambeth JD. Nox4: a hydrogen peroxide-generating oxygen sensor. Biochemistry 2014;53:5111–20.
   PubMed Web of Science ®Google Scholar
• Lund-Olesen K. Oxygen tension in synovial fluids. Arthritis Rheum 1970;13:769–76.
   PubMed Web of Science ®Google Scholar
• Ng CT, Biniecka M, Kennedy A, et al. Synovial tissue hypoxia and inflammation in vivo. Ann Rheum Dis 2010;69:1389–95.
   PubMed Web of Science ®Google Scholar
• Fairhurst AM, Wallace PK, Jawad AS, Goulding NJ. Rheumatoid peripheral blood phagocytes are primed for activation but have impaired Fc-mediated generation of reactive oxygen species. Arthritis Res Ther 2007;9:R29.
   PubMed Web of Science ®Google Scholar
• Bayley R, Kite KA, McGettrick HM, et al. The autoimmune-associated genetic variant PTPN22 R620W enhances neutrophil activation and function in patients with rheumatoid arthritis and healthy individuals. Ann Rheum Dis 2015;74:1588–95.
   PubMed Web of Science ®Google Scholar
• Kinloch A, Lundberg K, Wait R, et al. Synovial fluid is a site of citrullination of autoantigens in inflammatory arthritis. Arthritis Rheum 2008;58:2287–95.
   PubMed Web of Science ®Google Scholar