Peptidylarginine deiminase 4 contributes to tumor necrosis factor α-induced inflammatory arthritis

Arthritis and Rheumatology

Volumn 66, Issue 6, 2014, Pages 1482-1491

  Shelef, Miriam A ^a   Sokolove, Jeremy ^b   Lahey, Lauren J ^b   Wagner, Catriona A ^b   Sackmann, Eric K ^c   Warner, Thomas F ^c   Wang, Yanming ^d   Beebe, David J ^c   Robinson, William H ^b   Huttenlocher, Anna ^c  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CITRULLINATED ANTIGEN; CYCLIC CITRULLINATED PEPTIDE ANTIBODY; IMMUNOGLOBULIN G; PEPTIDYLARGININE DEIMINASE 4; PROTEIN ARGININE DEIMINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DISEASE EXACERBATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE OVEREXPRESSION; HISTOPATHOLOGY; IMMUNOGLOBULIN BLOOD LEVEL; MICROFLUIDIC ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RHEUMATOID ARTHRITIS; T LYMPHOCYTE ACTIVATION;

ANIMALS; ARTHRITIS, EXPERIMENTAL; AUTOANTIBODIES; B-LYMPHOCYTES; CITRULLINE; DISEASE MODELS, ANIMAL; HYDROLASES; IMMUNOGLOBULIN G; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84901640926     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38393     Document Type: Article

References (39)

1. Courvoisier N, Dougados M, Cantagrel A, Goupille P, Meyer O, Sibilia J, et al. Prognostic factors of 10-year radiographic outcome in early rheumatoid arthritis: a prospective study. Arthritis Res Ther 2008; 10: R106.
2. Quirke AM, Fisher BA, Kinloch AJ, Venables PJ,. Citrullination of autoantigens: upstream of TNFα in the pathogenesis of rheumatoid arthritis. FEBS Lett 2011; 585: 3681-8.
3. Klareskog L, Malmstrom V, Lundberg K, Padyukov L, Alfredsson L,. Smoking, citrullination and genetic variability in the immunopathogenesis of rheumatoid arthritis. Semin Immunol 2011; 23: 92-8.
4. Klareskog L, Stolt P, Lundberg K, Kallberg H, Bengtsson C, Grunewald J, et al, and the Epidemiological Investigation of Rheumatoid Arthritis Study Group. A new model for an etiology of rheumatoid arthritis: smoking may trigger HLA-DR (shared epitope)-restricted immune reactions to autoantigens modified by citrullination. Arthritis Rheum 2006; 54: 38-46.
5. Liao F, Li Z, Wang Y, Shi B, Gong Z, Cheng X,. Porphyromonas gingivalis may play an important role in the pathogenesis of periodontitis-associated rheumatoid arthritis. Med Hypotheses 2009; 72: 732-5.
6. Chang X, Yamada R, Suzuki A, Sawada T, Yoshino S, Tokuhiro S, et al. Localization of peptidylarginine deiminase 4 (PADI4) and citrullinated protein in synovial tissue of rheumatoid arthritis. Rheumatology (Oxford) 2005; 44: 40-50.
7. Willis VC, Gizinski AM, Banda NK, Causey CP, Knuckley B, Cordova KN, et al. N-α-benzoyl-N5-(2-chloro-1-iminoethyl)-L-ornithine amide, a protein arginine deiminase inhibitor, reduces the severity of murine collagen-induced arthritis. J Immunol 2011; 186: 4396-404.
8. Foulquier C, Sebbag M, Clavel C, Chapuy-Regaud S, Al Badine R, Mechin MC, et al. Peptidyl arginine deiminase type 2 (PAD-2) and PAD4 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.
9. Kurko J, Besenyei T, Laki J, Glant TT, Mikecz K, Szekanecz Z,. Genetics of rheumatoid arthritis-a comprehensive review. Clin Rev Allergy Immunol 2013; 45: 170-9.
10. Li P, Li M, Lindberg MR, Kennett MJ, Xiong N, Wang Y,. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med 2010; 207: 1853-62.
11. Khandpur R, Carmona-Rivera C, Vivekanandan-Giri A, Gizinski A, Yalavarthi S, Knight JS, et al. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med 2013; 5: 178ra40.
12. Rohrbach AS, Hemmers S, Arandjelovic S, Corr M, Mowen KA,. PAD4 is not essential for disease in the K/BxN murine autoantibody-mediated model of arthritis. Arthritis Res Ther 2012; 14: R104.
13. Wipke BT, Allen PM,. Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol 2001; 167: 1601-8.
14. Jones JE, Slack JL, Fang P, Zhang X, Subramanian V, Causey CP, et al. Synthesis and screening of a haloacetamidine containing library to identify PAD4 selective inhibitors. ACS Chem Biol 2012; 7: 160-5.
15. Makrygiannakis D, af Klint E, Lundberg IE, Lofberg R, Ulfgren AK, Klareskog L, et al. Citrullination is an inflammationdependent process. Ann Rheum Dis 2006; 65: 1219-22.
16. Makrygiannakis D, Revu S, Engstrom M, af Klint E, Nicholas AP, Pruijn GJ, et al. Local administration of glucocorticoids decreases synovial citrullination in rheumatoid arthritis. Arthritis Res Ther 2012; 14: R20.
17. Mastronardi FG, Wood DD, Mei J, Raijmakers R, Tseveleki V, Dosch HM, et al. Increased citrullination of histone H3 in multiple sclerosis brain and animal models of demyelination: a role for tumor necrosis factor-induced peptidylarginine deiminase 4 translocation. J Neurosci 2006; 26: 11387-96.
18. Neeli I, Khan SN, Radic M,. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 2008; 180: 1895-902.
19. Keshari RS, Jyoti A, Dubey M, Kothari N, Kohli M, Bogra J, et al. Cytokines induced neutrophil extracellular traps formation: implication for the inflammatory disease condition. PLoS One 2012; 7: e48111.
20. Boussiotis VA, Nadler LM, Strominger JL, Goldfeld AE,. Tumor necrosis factor α is an autocrine growth factor for normal human B cells. Proc Natl Acad Sci U S A 1994; 91: 7007-11.
21. Kobie JJ, Zheng B, Bryk P, Barnes M, Ritchlin CT, Tabechian DA, et al. Decreased influenza-specific B cell responses in rheumatoid arthritis patients treated with anti-tumor necrosis factor. Arthritis Res Ther 2011; 13: R209.
22. Sokolove J, Bromberg R, Deane KD, Lahey LJ, Derber LA, Chandra PE, et al. Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS One 2012; 7: e35296.
23. Sokolove J, Zhao X, Chandra PE, Robinson WH,. Immune complexes containing citrullinated fibrinogen costimulate macrophages via Toll-like receptor 4 and Fcγ receptor. Arthritis Rheum 2011; 63: 53-62.
24. Douni E, Akassoglou K, Alexopoulou L, Georgopoulos S, Haralambous S, Hill S, et al. Transgenic and knockout analyses of the role of TNF in immune regulation and disease pathogenesis. J Inflamm 1995; 47: 27-38.
25. Sokolove J, Lindstrom TM, Robinson WH,. Development and deployment of antigen arrays for investigation of B-cell fine specificity in autoimmune disease. Front Biosci (Elite Ed) 2012; 4: 320-30.
26. Knipp M, Vasak M,. A colorimetric 96-well microtiter plate assay for the determination of enzymatically formed citrulline. Anal Biochem 2000; 286: 257-64.
27. Sackmann EK, Berthier E, Young EW, Shelef MA, Wernimont SA, Huttenlocher A, et al. Microfluidic kit-on-a-lid: a versatile platform for neutrophil chemotaxis assays. Blood 2012; 120: e45-53.
28. Li P, Schwarz EM,. The TNF-α transgenic mouse model of inflammatory arthritis. Springer Semin Immunopathol 2003; 25: 19-33.
29. Hoffmann M, Hayer S, Steiner G,. Immmunopathogenesis of rheumatoid arthritis: induction of arthritogenic autoimmune responses by proinflammatory stimuli. Ann N Y Acad Sci 2009; 1173: 391-400.
30. Schellekens GA, de Jong BA, van den Hoogen FH, van de Putte LB, van Venrooij WJ,. Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies. J Clin Invest 1998; 101: 273-81.
31. Cantaert T, Teitsma C, Tak PP, Baeten D,. Presence and role of anti-citrullinated protein antibodies in experimental arthritis models. Arthritis Rheum 2013; 65: 939-48.
32. Arandjelovic S, McKenney KR, Leming SS, Mowen KA,. ATP induces protein arginine deiminase 2-dependent citrullination in mast cells through the P2X7 purinergic receptor. J Immunol 2012; 189: 4112-22.
33. Mohanan S, Horibata S, McElwee JL, Dannenberg AJ, Coonrod SA,. Identification of macrophage extracellular trap-like structures in mammary gland adipose tissue: a preliminary study. Front Immunol 2013; 4: 67.
34. Suzuki T, Ikari K, Yano K, Inoue E, Toyama Y, Taniguchi A, et al. PADI4 and HLA-DRB1 are genetic risks for radiographic progression in RA patients, independent of ACPA status: results from the IORRA Cohort Study. PloS One 2013; 8: e61045.
35. Shelef MA, Tauzin S, Huttenlocher A,. Neutrophil migration: moving from zebrafish models to human autoimmunity. Immunol Rev 2013; 256: 269-81.
36. Chumanevich AA, Causey CP, Knuckley BA, Jones JE, Poudyal D, Chumanevich AP, et al. Suppression of colitis in mice by Cl-amidine: a novel peptidylarginine deiminase inhibitor. Am J Physiol Gastrointest Liver Physiol 2011; 300: G929-38.
37. Li P, Wang D, Yao H, Doret P, Hao G, Shen Q, et al. Coordination of PAD4 and HDAC2 in the regulation of p53-target gene expression. Oncogene 2010; 29: 3153-62.
38. Vossenaar ER, Radstake TR, van der Heijden A, van Mansum MA, Dieteren C, de Rooij DJ, et al. Expression and activity of citrullinating peptidylarginine deiminase enzymes in monocytes and macrophages. Ann Rheum Dis 2004; 63: 373-81.
39. Davignon JL, Hayder M, Baron M, Boyer JF, Constantin A, Apparailly F, et al. Targeting monocytes/macrophages in the treatment of rheumatoid arthritis. Rheumatology (Oxford) 2013; 52: 590-8.