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

Journal of Immunology Research

Volumn 2015, Issue , 2015, Pages

  Mastrangelo, Andrea ^a   Colasanti, Tania ^a   Barbati, Cristiana ^a   Pecani, Arbi ^a   Sabatinelli, Danilo ^a   Pendolino, Monica ^a   Truglia, Simona ^a   Massaro, Laura ^a   Mancini, Riccardo ^a   Miranda, Francesca ^a   Spinelli, Francesca Romana ^a   Conti, Fabrizio ^a   Alessandri, Cristiano ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN; ANTIBODY; ANTIGEN;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CARBAMOYLATION; CELL SURVIVAL; EXTRACELLULAR TRAP; FOLLOW UP; HLA SYSTEM; HUMAN; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; RHEUMATOID ARTHRITIS; ANIMAL; GLYCOSYLATION; IMMUNOLOGY;

ANIMALS; ANTIBODIES; ANTIGENS; ARTHRITIS, RHEUMATOID; GLYCOSYLATION; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84930959229     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2015/712490     Document Type: Review

References (93)

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.
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.
4. D. L. Scott, F. Wolfe, and T. W. J. Huizinga, "Rheumatoid arthritis," The Lancet, vol. 376, no. 9746, pp. 1094-1108, 2010.
5. nd 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.
7. J. W. Bullen, J. L. Balsbaugh, D. Chanda et al., "Crosstalk 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
20. 8+ T cell O-glycan synthesis and affects trafficking," The Journal of Clinical Investigation, vol. 124, no. 3, pp. 1013-1026, 2014.
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.
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.
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.
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.
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.
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.
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 glycoformor Fc domain," Journal of Molecular Biology, vol. 425, no. 8, pp. 1253-1258, 2013.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
53. C. Alessandri, M. Bombardieri, N. Papa et al., "Decrease of anticyclic 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
73. P. Jiang and N. Mizushima, "Autophagy and human diseases," Cell Research, vol. 24, no. 1, pp. 69-79, 2014.
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.
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.
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 ofmurine collagen-induced arthritis," The Journal of Immunology, vol. 186, no. 7, pp. 4396-4404, 2011.
77. Y. Wang, P. Li, S. Wang et al., "Anticancer peptidylarginine deiminase (PAD) inhibitors regulate the autophagy flux and the mammalian target of rapamycincomplex 1 activity," The Journal of Biological Chemistry, vol. 287, no. 31, pp. 25941-25953, 2012.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.