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Journal of Immunology Research
Volume 2015, Article ID 712490, 10 pages
http://dx.doi.org/10.1155/2015/712490
Review Article

The Role of Posttranslational Protein Modifications in Rheumatological Diseases: Focus on Rheumatoid Arthritis

Reumatologia, Dipartimento di Medicina Interna e Specialità Mediche, Sapienza Università di Roma, Italy

Received 22 September 2014; Revised 16 January 2015; Accepted 5 February 2015

Academic Editor: David Kaplan

Copyright © 2015 Andrea Mastrangelo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Y. Zhao and O. N. Jensen, “Modification-specific proteomics: strategies for characterization of post-translational modifications using enrichment techniques,” Proteomics, vol. 9, no. 20, pp. 4632–4641, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Walsh, Posttranslational Modification of Proteins: Expanding Nature's Inventory, Roberts and Co., 2006.
  3. R. D. Emes, A. J. Pocklington, C. N. G. Anderson et al., “Evolutionary expansion and anatomical specialization of synapse proteome complexity,” Nature Neuroscience, vol. 11, no. 7, pp. 799–806, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. D. L. Scott, F. Wolfe, and T. W. J. Huizinga, “Rheumatoid arthritis,” The Lancet, vol. 376, no. 9746, pp. 1094–1108, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Varki, H. Freeze, and P. Gagneux, Essentials of Glycobiology, Cold Spring Harbor Laboratory Press, 2nd edition, 2008.
  6. J. S. Haurum, I. B. Høier, G. Arsequell et al., “Presentation of cytosolic glycosylated peptides by human class I major histocompatibility complex molecules in vivo,” Journal of Experimental Medicine, vol. 190, no. 1, pp. 145–150, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. J. W. Bullen, J. L. Balsbaugh, D. Chanda et al., “Cross-talk between two essential nutrient-sensitive enzymes: O-GlcNAc transferase (OGT) and AMP-activated protein kinase (AMPK),” Journal of Biological Chemistry, vol. 289, no. 15, pp. 10592–10606, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. N. E. Zachara, N. O'Donnell, W. D. Cheung, J. J. Mercer, J. D. Marth, and G. W. Hart, “Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress: a survival response of mammalian cells,” The Journal of Biological Chemistry, vol. 279, no. 29, pp. 30133–30142, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. A. W. Purcell, I. R. van Driel, and P. A. Gleeson, “Impact of glycans on T-cell tolerance to glycosylated self-antigens,” Immunology and Cell Biology, vol. 86, no. 7, pp. 574–579, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. B. A. Cobb and D. L. Kasper, “Coming of age: carbohydrates and immunity,” European Journal of Immunology, vol. 35, no. 2, pp. 352–356, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Michaëlsson, M. Andersson, Å. Engström, and R. Holmdahl, “Identification of an immunodominant type-II collagen peptide recognized by T cells in H-2q mice: self tolerance at the level of determinant selection,” European Journal of Immunology, vol. 22, no. 7, pp. 1819–1825, 1992. View at Publisher · View at Google Scholar · View at Scopus
  12. B.-Y. Diab, N. C. Lambert, F.-E. L'Faqihi, P. Loubet-Lescoulié, C. De Préval, and H. Coppin, “Human collagen II peptide 256-271 preferentially binds to HLA-DR molecules associated with susceptibility to rheumatoid arthritis,” Immunogenetics, vol. 49, no. 1, pp. 36–44, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Corthay, J. Bäcklund, J. Broddefalk et al., “Epitope glycosylation plays a critical role for T cell recognition of type II collagen in collagen-induced arthritis,” European Journal of Immunology, vol. 28, no. 8, pp. 2580–2590, 1998. View at Publisher · View at Google Scholar
  14. B. Dzhambazov, K. S. Nandakumar, J. Kihlberg, L. Fugger, R. Holmdahl, and M. Vestberg, “Therapeutic vaccination of active arthritis with a glycosylated collagen type II peptide in complex with MHC class II molecules,” The Journal of Immunology, vol. 176, no. 3, pp. 1525–1533, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Batsalova, I. Lindh, J. Bäcklund, B. Dzhambazov, and R. Holmdahl, “Comparative analysis of collagen type II-specific immune responses during development of collagen-induced arthritis in two B10 mouse strains,” Arthritis Research & Therapy, vol. 14, no. 6, article R237, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Dzhambazov, M. Holmdahl, H. Yamada et al., “The major T cell epitope on type II collagen is glycosylated in normal cartilage but modified by arthritis in both rats and humans,” European Journal of Immunology, vol. 35, no. 2, pp. 357–366, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Bläss, C. Meier, H. W. Vohr, M. Schwochau, C. Specker, and G. R. Burmester, “The p68 autoantigen characteristic of rheumatoid arthritis is reactive with carbohydrate epitope specific autoantibodies,” Annals of the Rheumatic Diseases, vol. 57, no. 4, pp. 220–225, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. O. Y. Goodwin, M. S. Thomasson, A. J. Lin, M. M. Sweeney, and M. A. Macnaughtan, “E. coli sabotages the in vivo production of O-linked β-N-acetylglucosamine-modified proteins,” Journal of Biotechnology, vol. 168, no. 4, pp. 315–323, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Yang, F.-G. Li, X.-S. Xie, S.-Q. Wang, and J.-M. Fan, “CagA, a major virulence factor of Helicobacter pylori, promotes the production and underglycosylation of IgA1 in DAKIKI cells,” Biochemical and Biophysical Research Communications, vol. 444, no. 2, pp. 276–281, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. J. C. Nolz and J. T. Harty, “IL-15 regulates memory CD8+ T cell O-glycan synthesis and affects trafficking,” The Journal of Clinical Investigation, vol. 124, no. 3, pp. 1013–1026, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. P. Delmotte, S. Degroote, J.-J. Lafitte, G. Lamblin, J.-M. Perini, and P. Roussel, “Tumor necrosis factor α increases the expression of glycosyltransferases and sulfotransferases responsible for the biosynthesis of sialylated and/or sulfated Lewis x epitopes in the human bronchial mucosa,” Journal of Biological Chemistry, vol. 277, no. 1, pp. 424–431, 2002. View at Google Scholar · View at Scopus
  22. R. Jefferis, J. Lund, and M. Goodall, “Recognition sites on human IgG for Fcγ receptors: the role of glycosylation,” Immunology Letters, vol. 44, no. 2-3, pp. 111–117, 1995. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Goulabchand, T. Vincent, F. Batteux, J. F. Eliaou, and P. Guilpain, “Impact of autoantibody glycosylation in autoimmune diseases,” Autoimmunity Reviews, vol. 13, no. 7, pp. 742–750, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. W. Louthrenoo, N. Kasitanon, R. Wichainun et al., “Anti-agalactosyl IgG antibodies in Thai patients with rheumatoid arthritis, systemic lupus erythematosus, and systemic sclerosis,” Clinical Rheumatology, vol. 29, no. 3, pp. 241–246, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Böhm, I. Schwab, A. Lux, and F. Nimmerjahn, “The role of sialic acid as a modulator of the anti-inflammatory activity of IgG,” Seminars in Immunopathology, vol. 34, no. 3, pp. 443–453, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Kaneko, F. Nimmerjahn, and J. V. Ravetch, “Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation,” Science, vol. 313, no. 5787, pp. 670–673, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. X. Yu, S. Vasiljevic, D. A. Mitchell, M. Crispin, and C. N. Scanlan, “Dissecting the molecular mechanism of IVIg therapy: the interaction between serum IgG and DC-SIGN is independent of antibody glycoform or Fc domain,” Journal of Molecular Biology, vol. 425, no. 8, pp. 1253–1258, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. I. K. Campbell, S. Miescher, D. R. Branch et al., “Therapeutic effect of IVIG on inflammatory arthritis in mice is dependent on the Fc portion and independent of sialylation or basophils,” The Journal of Immunology, vol. 192, no. 11, pp. 5031–5038, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. R. M. Anthony and J. V. Ravetch, “A novel role for the IgG Fc glycan: the anti-inflammatory activity of sialylated IgG Fcs,” Journal of Clinical Immunology, vol. 30, supplement 1, pp. S9–S14, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Wang, C. I. A. Balog, K. Stavenhagen et al., “Fc-glycosylation of IgG1 is modulated by B-cell stimuli,” Molecular & Cellular Proteomics, vol. 10, no. 5, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Hess, A. Winkler, A. K. Lorenz et al., “T cell-independent B cell activation induces immunosuppressive sialylated IgG antibodies,” The Journal of Clinical Investigation, vol. 123, no. 9, pp. 3788–3796, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Albrecht, L. Unwin, M. Muniyappa, and P. M. Rudd, “Glycosylation as a marker for inflammatory arthritis,” Cancer Biomarkers, vol. 14, no. 1, pp. 17–28, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. H. U. Scherer, J. Wang, R. E. M. Toes et al., “Immunoglobulin 1 (IgG1) Fc-glycosylation profiling of anti-citrullinated peptide antibodies from human serum,” PROTEOMICS—Clinical Applications, vol. 3, no. 1, pp. 106–115, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Matsumoto, K. Shikata, F. Takeuchi, N. Kojima, and T. Mizuochi, “Autoantibody activity of IgG rheumatoid factor increases with decreasing levels of galactosylation and sialylation,” Journal of Biochemistry, vol. 128, no. 4, pp. 621–628, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Rombouts, E. Ewing, L. A. van de Stadt et al., “Anti-citrullinated protein antibodies acquire a pro-inflammatory Fc glycosylation phenotype prior to the onset of rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 74, no. 1, pp. 234–241, 2015. View at Google Scholar
  36. F. E. van de Geijn, M. Wuhrer, M. H. J. Selman et al., “Immunoglobulin G galactosylation and sialylation are associated with pregnancy-induced improvement of rheumatoid arthritis and the postpartum flare: results from a large prospective cohort study,” Arthritis Research and Therapy, vol. 11, no. 6, article R193, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Bondt, M. H. J. Selman, A. M. Deelder et al., “Association between galactosylation of immunoglobulin G and improvement of rheumatoid arthritis during pregnancy is independent of sialylation,” Journal of Proteome Research, vol. 12, no. 10, pp. 4522–4531, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Saroha, S. Kumar, B. P. Chatterjee, and H. R. Das, “Jacalin bound plasma O-glycoproteome and reduced sialylation of alpha 2-HS glycoprotein (A2HSG) in rheumatoid arthritis patients,” PLoS ONE, vol. 7, no. 10, Article ID e46374, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. S. A. Flowers, L. Ali, C. S. Lane, M. Olin, and N. G. Karlsson, “Selected reaction monitoring to differentiate and relatively quantitate isomers of sulfated and unsulfated core 1 O-glycans from salivary MUC7 protein in rheumatoid arthritis,” Molecular and Cellular Proteomics, vol. 12, no. 4, pp. 921–931, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Jin, A.-K. H. Ekwall, J. Bylund et al., “Human synovial lubricin expresses sialyl Lewis x determinant and has L-selectin ligand activity,” The Journal of Biological Chemistry, vol. 287, no. 43, pp. 35922–35933, 2012. View at Google Scholar · View at Scopus
  41. A. Croce, O. Firuzi, F. Altieri et al., “Effect of infliximab on the glycosylation of IgG of patients with rheumatoid arthritis,” Journal of Clinical Laboratory Analysis, vol. 21, no. 5, pp. 303–314, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. K. S. Nandakumar, M. Collin, K. E. Happonen et al., “Dominant suppression of inflammation by glycan-hydrolyzed IgG,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 25, pp. 10252–10257, 2013. View at Google Scholar · View at Scopus
  43. I. Schwab, S. Mihai, M. Seeling, M. Kasperkiewicz, R. J. Ludwig, and F. Nimmerjahn, “Broad requirement for terminal sialic acid residues and FcγRIIB for the preventive and therapeutic activity of intravenous immunoglobulins in vivo,” European Journal of Immunology, vol. 44, no. 5, pp. 1444–1453, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Guhr, J. Bloem, N. I. L. Derksen et al., “Enrichment of sialylated IgG by lectin fractionation does not enhance the efficacy of immunoglobulin G in a murine model of immune thrombocytopenia,” PLoS ONE, vol. 6, no. 6, Article ID e21246, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. W. J. van Venrooij and G. J. M. Pruijn, “Citrullination: a small change for a protein with great consequences for rheumatoid arthritis,” Arthritis Research, vol. 2, no. 4, pp. 249–251, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. E. R. Vossenaar, A. J. W. Zendman, W. J. van Venrooij, and G. J. M. Pruijn, “PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease,” BioEssays, vol. 25, no. 11, pp. 1106–1118, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. Baka, B. György, P. Géher, E. I. Buzás, A. Falus, and G. Nagy, “Citrullination under physiological and pathological conditions,” Joint Bone Spine, vol. 79, no. 5, pp. 431–436, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. E. R. Vossenaar, T. R. D. Radstake, A. van Der Heijden et al., “Expression and activity of citrullinating peptidylarginine deiminase enzymes in monocytes and macrophages,” Annals of the Rheumatic Diseases, vol. 63, no. 4, pp. 373–381, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Yamada, A. Suzuki, X. Chang, and K. Yamamoto, “Citrullinated proteins in rheumatoid arthritis,” Frontiers in Bioscience, vol. 10, no. 1, pp. 54–64, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Aggarwal, K. Liao, R. Nair, S. Ringold, and K. H. Costenbader, “Anti-citrullinated peptide antibody assays and their role in the diagnosis of rheumatoid arthritis,” Arthritis Care & Research, vol. 61, no. 11, pp. 1472–1483, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. L. A. van de Stadt, M. H. M. T. de Koning, R. J. van De Stadt et al., “Development of the anti-citrullinated protein antibody repertoire prior to the onset of rheumatoid arthritis,” Arthritis & Rheumatism, vol. 63, no. 11, pp. 3226–3233, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. K. Forslind, M. Ahlmén, K. Eberhardt, I. Hafström, and B. Svensson, “Prediction of radiological outcome in early rheumatoid arthritis in clinical practice: role of antibodies to citrullinated peptides (anti-CCP),” Annals of the Rheumatic Diseases, vol. 63, no. 9, pp. 1090–1095, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Alessandri, M. Bombardieri, N. Papa et al., “Decrease of anti-cyclic citrullinated peptide antibodies and rheumatoid factor following anti-TNFalpha therapy (infliximab) in rheumatoid arthritis is associated with clinical improvement,” Annals of the Rheumatic Diseases, vol. 63, no. 10, pp. 1218–1221, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. J. J. B. C. van Beers, C. M. Schwarte, J. Stammen-Vogelzangs, E. Oosterink, B. Božič, and G. J. M. Pruijn, “The rheumatoid arthritis synovial fluid citrullinome reveals novel citrullinated epitopes in apolipoprotein E, myeloid nuclear differentiation antigen, and β-actin,” Arthritis & Rheumatism, vol. 65, no. 1, pp. 69–80, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. S. W. Scally, J. Petersen, S. C. Law et al., “A molecular basis for the association of the HLA-DRB1 locus, citrullination, and rheumatoid arthritis,” The Journal of Experimental Medicine, vol. 210, no. 12, pp. 2569–2582, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. R. R. P. de Vries, D. van der Woude, J. J. Houwing, and R. E. M. Toes, “Genetics of ACPA-positive rheumatoid arthritis: the beginning of the end?” Annals of the Rheumatic Diseases, vol. 70, no. 1, pp. i51–i54, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. Q. Remijsen, T. W. Kuijpers, E. Wirawan, S. Lippens, P. Vandenabeele, and T. Vanden Berghe, “Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality,” Cell Death and Differentiation, vol. 18, no. 4, pp. 581–588, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Leshner, S. Wang, C. Lewis et al., “PAD4 mediated histone hypercitrullination induces heterochromatin decondensation and chromatin unfolding to form neutrophil extracellular trap-like structures,” Frontiers in Immunology, vol. 3, article 307, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. N. Branzk and V. Papayannopoulos, “Molecular mechanisms regulating NETosis in infection and disease,” Seminars in Immunopathology, vol. 35, no. 4, pp. 513–530, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. R. Khandpur, C. Carmona-Rivera, A. Vivekanandan-Giri et al., “NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis,” Science Translational Medicine, vol. 5, no. 178, Article ID 178ra40, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Spengler, B. Lugonja, A. Creese et al., “Synovial fluid neutrophils undergoing NETosis contribute to joint inflammation by producing citrullinated autoantigens,” Annals of the Rheumatic Diseases, vol. 72, supplement 1, article A10, 2013. View at Google Scholar
  62. A. L. Griffen, M. R. Becker, S. R. Lyons, M. L. Moeschberger, and E. J. Leys, “Prevalence of Porphyromonas gingivalis and periodontal health status,” Journal of Clinical Microbiology, vol. 36, no. 11, pp. 3239–3242, 1998. View at Google Scholar · View at Scopus
  63. P. I. Eke, B. A. Dye, L. Wei, G. O. Thornton-Evans, and R. J. Genco, “Prevalence of periodontitis in adults in the united states: 2009 and 2010,” Journal of Dental Research, vol. 91, no. 10, pp. 914–920, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. T. R. Mikuls, J. B. Payne, F. Yu et al., “Periodontitis and porphyromonas gingivalis in patients with rheumatoid arthritis,” Arthritis & Rheumatology, vol. 66, no. 5, pp. 1090–1100, 2014. View at Publisher · View at Google Scholar · View at Scopus
  65. N. Wegner, R. Wait, A. Sroka et al., “Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: implications for autoimmunity in rheumatoid Arthritis,” Arthritis & Rheumatism, vol. 62, no. 9, pp. 2662–2672, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. W. Nesse, J. Westra, J. E. van der Wal et al., “The periodontium of periodontitis patients contains citrullinated proteins which may play a role in ACPA (anti-citrullinated protein antibody) formation,” Journal of Clinical Periodontology, vol. 39, no. 7, pp. 599–607, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Arandjelovic, K. R. McKenney, S. S. Leming, and K. A. Mowen, “ATP induces protein arginine deiminase 2-dependent citrullination in mast cells through the P2X7 purinergic receptor,” The Journal of Immunology, vol. 189, no. 8, pp. 4112–4122, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. L. Klareskog, V. Malmström, K. Lundberg, L. Padyukov, and L. Alfredsson, “Smoking, citrullination and genetic variability in the immunopathogenesis of rheumatoid arthritis,” Seminars in Immunology, vol. 23, no. 2, pp. 92–98, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. B. M. Mohamed, N. K. Verma, A. M. Davies et al., “Citrullination of proteins: a common post-translational modification pathway induced by different nanoparticles in vitro and in vivo,” Nanomedicine, vol. 7, no. 8, pp. 1181–1195, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. D. Makrygiannakis, M. Hermansson, A.-K. Ulfgren et al., “Smoking increases peptidylarginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells,” Annals of the Rheumatic Diseases, vol. 67, no. 10, pp. 1488–1492, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. V. Romero, J. Fert-Bober, P. A. Nigrovic et al., “Immune-mediated pore-forming pathways induce cellular hypercitrullination and generate citrullinated autoantigens in rheumatoid arthritis,” Science Translational Medicine, vol. 5, no. 209, Article ID 209ra150, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. D. Glick, S. Barth, and K. F. Macleod, “Autophagy: cellular and molecular mechanisms,” The Journal of Pathology, vol. 221, no. 1, pp. 3–12, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. P. Jiang and N. Mizushima, “Autophagy and human diseases,” Cell Research, vol. 24, no. 1, pp. 69–79, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. J. M. Ireland and E. R. Unanue, “Autophagy in antigen-presenting cells results in presentation of citrullinated peptides to CD4 T cells,” The Journal of Experimental Medicine, vol. 208, no. 13, pp. 2625–2632, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. T. Bongartz, T. Cantaert, S. R. Atkins et al., “Citrullination in extra-articular manifestations of rheumatoid arthritis,” Rheumatology, vol. 46, no. 1, pp. 70–75, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. V. C. Willis, A. M. Gizinski, N. K. Banda 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,” The Journal of Immunology, vol. 186, no. 7, pp. 4396–4404, 2011. View at Publisher · View at Google Scholar · View at Scopus
  77. Y. Wang, P. Li, S. Wang et al., “Anticancer peptidylarginine deiminase (PAD) inhibitors regulate the autophagy flux and the mammalian target of rapamycin complex 1 activity,” The Journal of Biological Chemistry, vol. 287, no. 31, pp. 25941–25953, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. G. R. Stark, W. H. Stein, and S. Moore, “Reactions of the cyanate present in aqueous urea with amino acids and proteins,” The Journal of Biological Chemistry, vol. 235, no. 11, pp. 3177–3181, 1960. View at Google Scholar
  79. G. R. Stark, “On the reversible reaction of cyanate with sulfhydryl groups and the determination of NH2-terminal cysteine and cystine in proteins,” The Journal of Biological Chemistry, vol. 239, no. 5, pp. 1411–1414, 1964. View at Google Scholar · View at Scopus
  80. A. Willemze, R. E. M. Toes, T. W. J. Huizinga, and L. A. Trouw, “New biomarkers in rheumatoid arthritis,” The Netherlands Journal of Medicine, vol. 70, no. 9, pp. 392–399, 2012. View at Google Scholar · View at Scopus
  81. P. Hagel, J. J. T. Gerding, W. Fieggen, and H. Bloemendal, “Cyanate formation in solutions of urea. I. Calculation of cyanate concentrations at different temperature and pH,” Biochimica et Biophysica Acta, vol. 243, no. 3, pp. 366–373, 1971. View at Publisher · View at Google Scholar · View at Scopus
  82. J. S. Claxton, P. C. Sandoval, G. Liu, C.-L. Chou, J. D. Hoffert, and M. A. Knepper, “Endogenous carbamylation of renal medullary proteins,” PLoS ONE, vol. 8, no. 12, Article ID e82655, 2013. View at Publisher · View at Google Scholar · View at Scopus
  83. J. M. Roberts, P. R. Veres, A. K. Cochran et al., “Isocyanic acid in the atmosphere and its possible link to smoke-related health effects,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 22, pp. 8966–8971, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. R. C. Baldwin, A. Pasi, J. T. MacGregor, and C. H. Hine, “The rates of radical formation from the dipyridylium herbicides paraquat, diquat, and morfamquat in homogenates of rat lung, kidney, and liver: an inhibitory effect of carbon monoxide,” Toxicology and Applied Pharmacology, vol. 32, no. 2, pp. 298–304, 1975. View at Publisher · View at Google Scholar · View at Scopus
  85. C. A. Sanchez, B. C. Blount, L. Valentin-Blasini, and R. I. Krieger, “Perchlorate, thiocyanate, and nitrate in edible cole crops (Brassica sp.) produced in the lower Colorado River region,” Bulletin of Environmental Contamination and Toxicology, vol. 79, no. 6, pp. 655–659, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. J. Chung and J. L. Wood, “Oxidation of thiocyanate to cyanide and sulfate by the lactoperoxidase-hydrogen peroxide system,” Archives of Biochemistry and Biophysics, vol. 141, no. 1, pp. 73–78, 1970. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Jaisson, C. Pietrement, and P. Gillery, “Carbamylation-derived products: bioactive compounds and potential biomarkers in chronic renal failure and atherosclerosis,” Clinical Chemistry, vol. 57, no. 11, pp. 1499–1505, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. I. Koshiishi and T. Imanari, “State analysis of endogenous cyanate ion in human plasma,” Journal of Pharmacobio-Dynamics, vol. 13, no. 4, pp. 254–258, 1990. View at Publisher · View at Google Scholar · View at Scopus
  89. C. M. Balion, T. F. Draisey, and R. J. Thibert, “Carbamylated hemoglobin and carbamylated plasma protein in hemodialyzed patients,” Kidney International, vol. 53, no. 2, pp. 488–495, 1998. View at Publisher · View at Google Scholar · View at Scopus
  90. J. Shi, R. Knevel, P. Suwannalai et al., “Autoantibodies recognizing carbamylated proteins are present in sera of patients with rheumatoid arthritis and predict joint damage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 42, pp. 17372–17377, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. P. Mydel, Z. Wang, M. Brisslert et al., “Carbamylation-dependent activation of T cells: a novel mechanism in the pathogenesis of autoimmune arthritis,” Journal of Immunology, vol. 184, no. 12, pp. 6882–6890, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. J. Shi, L. A. van de Stadt, E. W. N. Levarht et al., “Anti-carbamylated protein antibodies are present in arthralgia patients and predict the development of rheumatoid arthritis,” Arthritis & Rheumatism, vol. 65, no. 4, pp. 911–915, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. J. Shi, L. A. van de Stadt, E. W. N. Levarht et al., “Anti-carbamylated protein (anti-CarP) antibodies precede the onset of rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 73, no. 4, pp. 780–783, 2014. View at Publisher · View at Google Scholar