Decreased severity of experimental autoimmune arthritis in peptidylarginine deiminase type 4 knockout mice

BMC Musculoskeletal Disorders

Volumn 17, Issue 1, 2016, Pages

  Suzuki, Akari ^a   Kochi, Yuta ^a   Shoda, Hirofumi ^b   Seri, Yu ^c   Fujio, Keishi ^c   Sawada, Tetsuji ^d   Yamada, Ryo ^a   Yamamoto, Kazuhiko ^a,c  

^a Institute of Physical and Chemical Research   (Japan)

^b the University   (Japan)

^c TOKYO MEDICAL UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

Citrullination; Collagen induced arthritis mice; Peptidylarginine deiminase type 4; Rheumatoid arthritis; TNF

Indexed keywords

COLLAGEN TYPE 2; CYTOKINE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; PROTEIN ARGININE DEIMINASE; PROTEIN PAD2; PROTEIN PADI2; PROTEIN PADI4; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; AUTOANTIBODY; CITRULLINE; HYDROLASE; PEPTIDYLARGININE DEIMINASE 4, MOUSE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ASSAY; CONTROLLED STUDY; DBA 1 MOUSE; DISEASE COURSE; DISEASE SEVERITY; ENZYME BLOOD LEVEL; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LOCALIZATION; EXPERIMENTAL ARTHRITIS; EXPERIMENTAL AUTOIMMUNE ARTHRITIS; EXPERIMENTAL AUTOIMMUNE DISEASE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; WILD TYPE MOUSE; ANIMAL; AUTOIMMUNE DISEASE; BLOOD; C57BL MOUSE; DISEASE EXACERBATION; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HUMAN; IMMUNOLOGY; METABOLISM; SEVERITY OF ILLNESS INDEX;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; AUTOIMMUNE DISEASES; CITRULLINE; COLLAGEN TYPE II; CYTOKINES; DISEASE PROGRESSION; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; HYDROLASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SEVERITY OF ILLNESS INDEX; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84969758604     PISSN: None     EISSN: 14712474     Source Type: Journal    
DOI: 10.1186/s12891-016-1055-2     Document Type: Article

References (70)

1. Suzuki A, Yamada R, Chang X, Tokuhiro S, Sawada T, Suzuki M, et al. Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginine deiminase 4, are associated with rheumatoid arthritis. Nat Genet. 2003;34(4):395-402.
2. Gibofsky A. Epidemiology, pathophysiology, and diagnosis of rheumatoid arthritis: A Synopsis. Am J Manag Care. 2014;20(7 Suppl):S128-135.
3. Barton A, Bowes J, Eyre S, Spreckley K, Hinks A, John S, et al. A functional haplotype of the PADI4 gene associated with rheumatoid arthritis in a Japanese population is not associated in a United Kingdom population. Arthritis Rheum. 2004;50(4):1117-21.
4. Caponi L, Petit-Teixeira E, Sebbag M, Bongiorni F, Moscato S, Pratesi F, et al. A family based study shows no association between rheumatoid arthritis and the PADI4 gene in a white French population. Ann Rheum Dis. 2005;64(4):587-93.
5. Kang CP, Lee HS, Ju H, Cho H, Kang C, Bae SC. A functional haplotype of the PADI4 gene associated with increased rheumatoid arthritis susceptibility in Koreans. Arthritis Rheum. 2006;54(1):90-6.
6. Ikari K, Kuwahara M, Nakamura T, Momohara S, Hara M, Yamanaka H, et al. Association between PADI4 and rheumatoid arthritis: a replication study. Arthritis Rheum. 2005;52(10):3054-7.
7. Martinez A, Valdivia A, Pascual-Salcedo D, Lamas JR, Fernandez-Arquero M, Balsa A, et al. PADI4 polymorphisms are not associated with rheumatoid arthritis in the Spanish population. Rheumatology (Oxford). 2005;44(10):1263-6.
8. Okada Y, Terao C, Ikari K, Kochi Y, Ohmura K, Suzuki A, et al. Meta-analysis identifies nine new loci associated with rheumatoid arthritis in the Japanese population. Nat Genet. 2012;44(5):511-6.
9. Kurreeman FA, Stahl EA, Okada Y, Liao K, Diogo D, Raychaudhuri S, et al. Use of a multiethnic approach to identify rheumatoid- arthritis-susceptibility loci, 1p36 and 17q12. Am J Hum Genet. 2012;90(3):524-32.
10. Stahl EA, Raychaudhuri S, Remmers EF, Xie G, Eyre S, Thomson BP, et al. Genome-wide association study meta-analysis identifies seven new rheumatoid arthritis risk loci. Nat Genet. 2010;42(6):508-14.
11. Plenge RM, Padyukov L, Remmers EF, Purcell S, Lee AT, Karlson EW, et al. 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. 2005;77(6):1044-60.
12. Lettre G, Rioux JD. Autoimmune diseases: insights from genome-wide association studies. Hum Mol Genet. 2008;17(R2):R116-121.
13. Baranzini SE. The genetics of autoimmune diseases: a networked perspective. Curr Opin Immunol. 2009;21(6):596-605.
14. van Gaalen FA, van Aken J, Huizinga TW, Schreuder GM, Breedveld FC, Zanelli E, et al. Association between HLA class II genes and autoantibodies to cyclic citrullinated peptides (CCPs) influences the severity of rheumatoid arthritis. Arthritis Rheum. 2004;50(7):2113-21.
15. Ding B, Padyukov L, Lundstrom E, Seielstad M, Plenge RM, Oksenberg JR, et al. Different patterns of associations with anti-citrullinated protein antibody-positive and anti-citrullinated protein antibody-negative rheumatoid arthritis in the extended major histocompatibility complex region. Arthritis Rheum. 2009;60(1):30-8.
16. Kochi Y, Suzuki A, Yamada R, Yamamoto K. Ethnogenetic heterogeneity of rheumatoid arthritis-implications for pathogenesis. Nat Rev Rheumatol. 2010;6(5):290-5.
17. Kochi Y, Thabet MM, Suzuki A, Okada Y, Daha NA, Toes RE, et al. PADI4 polymorphism predisposes male smokers to rheumatoid arthritis. Ann Rheum Dis. 2011;70(3):512-5.
18. Baka Z, Buzas E, Nagy G. Rheumatoid arthritis and smoking: putting the pieces together. Arthritis Res Ther. 2009;11(4):238.
19. Bang SY, Lee KH, Cho SK, Lee HS, Lee KW, Bae SC. Smoking increases rheumatoid arthritis susceptibility in individuals carrying the HLA-DRB1 shared epitope, regardless of rheumatoid factor or anti-cyclic citrullinated peptide antibody status. Arthritis Rheum. 2010;62(2):369-77.
20. Masdottir B, Jonsson T, Manfredsdottir V, Vikingsson A, Brekkan A, Valdimarsson H. Smoking, rheumatoid factor isotypes and severity of rheumatoid arthritis. Rheumatology (Oxford). 2000;39(11):1202-5.
21. 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(4):e61045.
22. Masson-Bessiere C, Sebbag M, Girbal-Neuhauser E, Nogueira L, Vincent C, Senshu T, et al. The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the alpha- and beta-chains of fibrin. J Immunol. 2001;166(6):4177-84.
23. Nakayama-Hamada M, Suzuki A, Furukawa H, Yamada R, Yamamoto K. Citrullinated fibrinogen inhibits thrombin-catalysed fibrin polymerization. J Biochem. 2008;144(3):393-8.
24. Rubin B, Sonderstrup G. Citrullination of self-proteins and autoimmunity. Scand J Immunol. 2004;60(1-2):112-20.
25. Auger I, Sebbag M, Vincent C, Balandraud N, Guis S, Nogueira L, et al. Influence of HLA-DR genes on the production of rheumatoid arthritis-specific autoantibodies to citrullinated fibrinogen. Arthritis Rheum. 2005;52(11):3424-32.
26. Baeten D, Peene I, Union A, Meheus L, Sebbag M, Serre G, et al. Specific presence of intracellular citrullinated proteins in rheumatoid arthritis synovium: relevance to antifilaggrin autoantibodies. Arthritis Rheum. 2001;44(10):2255-62.
27. Girbal-Neuhauser E, Durieux JJ, Arnaud M, Dalbon P, Sebbag M, Vincent C, et al. The epitopes targeted by the rheumatoid arthritis-associated antifilaggrin autoantibodies are posttranslationally generated on various sites of (pro)filaggrin by deimination of arginine residues. J Immunol. 1999;162(1):585-94.
28. Gomes-Daudrix V, Sebbag M, Girbal E, Vincent C, Simon M, Rakotoarivony J, et al. Immunoblotting detection of so-called 'antikeratin antibodies': a new assay for the diagnosis of rheumatoid arthritis. Ann Rheum Dis. 1994;53(11):735-42.
29. Senshu T, Kan S, Ogawa H, Manabe M, Asaga H. Preferential deimination of keratin K1 and filaggrin during the terminal differentiation of human epidermis. Biochem Biophys Res Commun. 1996;225(3):712-9.
30. Simon M, Girbal E, Sebbag M, Gomes-Daudrix V, Vincent C, Salama G, et al. The cytokeratin filament-aggregating protein filaggrin is the target of the so-called "antikeratin antibodies," autoantibodies specific for rheumatoid arthritis. J Clin Invest. 1993;92(3):1387-93.
31. Utz PJ, Anderson P. Posttranslational protein modifications, apoptosis, and the bypass of tolerance to autoantigens. Arthritis Rheum. 1998;41(7):1152-60.
32. 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(1):40-50.
33. Giles JT, Fert-Bober J, Park JK, Bingham 3rd CO, Andrade F, Fox-Talbot K, et al. Myocardial citrullination in rheumatoid arthritis: a correlative histopathologic study. Arthritis Res Ther. 2012;14(1):R39.
34. Cuthbert GL, Daujat S, Snowden AW, Erdjument-Bromage H, Hagiwara T, Yamada M et al: Histone Deimination Antagonizes Arginine Methylation. In: Cell: 2004/9/3 2004; 2004: 545-553.
35. Wang Y, Wysocka J, Sayegh J, Lee Y-H, Perlin JR, Leonelli L, et al. Human PAD4 Regulates Histone Arginine Methylation Levels via Demethylimination. 2004.
36. Tanikawa C, Espinosa M, Suzuki A, Masuda K, Yamamoto K, Tsuchiya E, et al. Regulation of histone modification and chromatin structure by the p53-PADI4 pathway. Nat Commun. 2012;3:676.
37. Zhang X, Gamble MJ, Stadler S, Cherrington BD, Causey CP, Thompson PR, et al. Genome-wide analysis reveals PADI4 cooperates with Elk-1 to activate c-Fos expression in breast cancer cells. PLoS Genet. 2011;7(6), e1002112.
38. Lee HJ, Joo M, Abdolrasulnia R, Young DG, Choi I, Ware LB, et al. Peptidylarginine deiminase 2 suppresses inhibitory {kappa}B kinase activity in lipopolysaccharide-stimulated RAW 264.7 macrophages. J Biol Chem. 2010;285(51):39655-62.
39. Luo Y, Arita K, Bhatia M, Knuckley B, Lee YH, Stallcup MR, et al. Inhibitors and inactivators of protein arginine deiminase 4: functional and structural characterization. Biochemistry. 2006;45(39):11727-36.
40. Willis VC, Gizinski AM, Banda NK, Causey CP, Knuckley B, Cordova KN, et al. 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. 2011;186(7):4396-404.
41. McElwee JL, Mohanan S, Griffith OL, Breuer HC, Anguish LJ, Cherrington BD, et al. Identification of PADI2 as a potential breast cancer biomarker and therapeutic target. BMC Cancer. 2012;12:500.
42. Trentham DE, Townes AS, Kang AH. Autoimmunity to type II collagen an experimental model of arthritis. J Exp Med. 1977;146(3):857-68.
43. Kuhn KA, Kulik L, Tomooka B, Braschler KJ, Arend WP, Robinson WH, et al. Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis. J Clin Invest. 2006;116(4):961-73.
44. Stanley ER. Murine bone marrow-derived macrophages. Methods Mol Biol. 1990;5:299-302.
45. Zack MD, Melton MA, Stock JL, Storer CE, Barve RA, Minnerly JC, et al. Reduced incidence and severity of experimental autoimmune arthritis in mice expressing catalytically inactive A disintegrin and metalloproteinase 8 (ADAM8). Clin Exp Immunol. 2009;158(2):246-56.
46. 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(4):373-81.
47. Nakashima K, Hagiwara T, Yamada M. Nuclear localization of peptidylarginine deiminase v and histone deimination in granulocytes. J Biol Chem. 2002;277(51):49562-8.
48. Vossenaar ER, Nijenhuis S, Helsen MM, van der Heijden A, Senshu T, van den Berg WB, et al. Citrullination of synovial proteins in murine models of rheumatoid arthritis. Arthritis Rheum. 2003;48(9):2489-500.
49. McInnes IB, Schett G. Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol. 2007;7(6):429-42.
50. 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(1):273-81.
51. Fan L, Wang Q, Liu R, Zong M, He D, Zhang H, et al. Citrullinated fibronectin inhibits apoptosis and promotes the secretion of pro-inflammatory cytokines in fibroblast-like synoviocytes in rheumatoid arthritis. Arthritis Res Ther. 2012;14(6):R266.
52. Okada Y, Shimane K, Kochi Y, Tahira T, Suzuki A, Higasa K, et al. A genome-wide association study identified AFF1 as a susceptibility locus for systemic lupus eyrthematosus in Japanese. PLoS Genet. 2012;8(1), e1002455.
53. Orozco G, Eyre S, Hinks A, Ke X, Wilson AG, Bax DE, et al. Association of CD40 with rheumatoid arthritis confirmed in a large UK case-control study. Ann Rheum Dis. 2009;69(5):813-6.
54. Hugill A, Shimomura K, Ashcroft FM, Cox RD. A mutation in KCNJ11 causing human hyperinsulinism (Y12X) results in a glucose-intolerant phenotype in the mouse. Diabetologia. 2010;53(11):2352-6.
55. Dai X, James RG, Habib T, Singh S, Jackson S, Khim S, et al. A disease-associated PTPN22 variant promotes systemic autoimmunity in murine models. J Clin Invest. 2013;123(5):2024-36.
56. 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(3):R104.
57. He Y, Li J, Zhuang W, Yin L, Chen C, Chi F, et al. The inhibitory effect against collagen-induced arthritis by Schistosoma japonicum infection is infection stage-dependent. BMC Immunol. 2010;11:28.
58. Hoppe B, Haupl T, Gruber R, Kiesewetter H, Burmester GR, Salama A, et al. Detailed analysis of the variability of peptidylarginine deiminase type 4 in German patients with rheumatoid arthritis: a case-control study. Arthritis Res Ther. 2006;8(2):R34.
59. Uysal H, Bockermann R, Nandakumar KS, Sehnert B, Bajtner E, Engstrom A, et al. Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis. J Exp Med. 2009;206(2):449-62.
60. Sebbag M, Chapuy-Regaud S, Auger I, Petit-Texeira E, Clavel C, Nogueira L, et al. Clinical and pathophysiological significance of the autoimmune response to citrullinated proteins in rheumatoid arthritis. Joint Bone Spine. 2004;71(6):493-502.
61. Wysocka J, Allis CD, Coonrod S. Histone arginine methylation and its dynamic regulation. Front Biosci. 2006;11:344-55.
62. McQualter JL, Darwiche R, Ewing C, Onuki M, Kay TW, Hamilton JA, et al. Granulocyte macrophage colony-stimulating factor: a new putative therapeutic target in multiple sclerosis. J Exp Med. 2001;194(7):873-82.
63. Rantapaa-Dahlqvist S, de Jong BA, Berglin E, Hallmans G, Wadell G, Stenlund H, et al. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum. 2003;48(10):2741-9.
64. Lundberg K, Nijenhuis S, Vossenaar ER, Palmblad K, van Venrooij WJ, Klareskog L, et al. Citrullinated proteins have increased immunogenicity and arthritogenicity and their presence in arthritic joints correlates with disease severity. Arthritis Res Ther. 2005;7(3):R458-467.
65. Mrozek K, Karakousis CP, Bloomfield CD. Chromosome 12 breakpoints are cytogenetically different in benign and malignant lipogenic tumors: localization of breakpoints in lipoma to 12q15 and in myxoid liposarcoma to 12q13.3. Cancer Res. 1993;53(7):1670-5.
66. Reid R, de Silva MV, Paterson L, Ryan E, Fisher C. Low-grade fibromyxoid sarcoma and hyalinizing spindle cell tumor with giant rosettes share a common t(7;16)(q34;p11) translocation. Am J Surg Pathol. 2003;27(9):1229-36.
67. Ishigami A, Ohsawa T, Hiratsuka M, Taguchi H, Kobayashi S, Saito Y, et al. Abnormal accumulation of citrullinated proteins catalyzed by peptidylarginine deiminase in hippocampal extracts from patients with Alzheimer's disease. J Neurosci Res. 2005;80(1):120-8.
68. Moscarello MA, Mastronardi FG, Wood DD. The role of citrullinated proteins suggests a novel mechanism in the pathogenesis of multiple sclerosis. Neurochem Res. 2007;32(2):251-6.
69. 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(6):G929-938.
70. Shelef MA, Sokolove J, Lahey LJ, Wagner CA, Sackmann EK, Warner TF, et al. Peptidylarginine deiminase 4 contributes to tumor necrosis factor alpha-induced inflammatory arthritis. Arthritis & rheumatology. 2014;66(6):1482-91.