Cited by 119Systemic Lupus Erythematosus ResearchRedox biology and oxidative stressNeutrophil, Myeloperoxidase and Oxidative Mechanisms

Oxidative post-translational modifications and their involvement in the pathogenesis of autoimmune diseases

Open access
Ryan, Brent J., Nissim, Ahuva, Winyard, Paul G.·2014·Redox Biology

Abstract

Tissue inflammation results in the production of numerous reactive oxygen, nitrogen and chlorine species, in addition to the products of lipid and sugar oxidation. Some of these products are capable of chemically modifying amino acids. This in turn results in changes to the structure and function of proteins. Increasing evidence demonstrates that such oxidative post-translational modifications result in the generation of neo-epitopes capable of eliciting both innate and adaptive immune responses. In this paper, we focus on how free radicals and related chemical species generated in inflammatory environments modulate the antigenicity of self-proteins, resulting in immune responses which involve the generation of autoantibodies against key autoantigens in autoimmune diseases. As examples, we will focus on Ro-60 and C1q in systemic lupus erythematosus, along with type-II collagen in rheumatoid arthritis. This review also covers some of the emerging literature which demonstrates that neo-epitopes generated by oxidation are conserved, as exemplified by the evolutionarily conserved pathogen-associated molecular patterns (PAMPs). We discuss how these observations relate to the pathogenesis of both human autoimmune diseases and inflammatory disease, such as atherosclerosis. The potential for these neo-epitopes and the immune responses against them to act as biomarkers or therapeutic targets is also discussed.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.redox.2014.05.004

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Sulfur-containing moieties such as the sulfhydryl group of cysteine and the thioether group of methionine are targeted by oxidative stress and form a plethora of posttranslational protein modifications.

    “Sulfur-containing moieties such as the sulfhydryl group of cysteine and the thioether group of methionine are targeted by oxidative stress and a plethora of posttranslational protein modifications is formed (Fig. 1) [15].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 107 · Cited by 119

Research works printed but not linked: 103

  1. [1]Bashir S. Oxidative DNA damage and cellular sensitivity to oxidative stress in human autoimmune diseases Annals of the Rheumatic Diseases 52 9 1993 659 666 8239761 8239761 PMC1005143
  2. [2]Pattison D.J. Winyard P.G. Dietary antioxidants in inflammatory arthritis: do they have any role in etiology or therapy? Nature Clinical Practice: Rheumatology 4 11 2008 590 596 18825134 18825134
  3. [3]Szabó-Taylor K.É. Oxidative stress in rheumatoid arthritis Alcaraz M.J. Gualillo O. Sánchez-Pernaute O. Studies on Arthritis and Joint Disorders 2013 Springer New York 145 167
  4. [4]Winyard P.G. Measurement and meaning of markers of reactive species of oxygen, nitrogen and sulfur in healthy human subjects and patients with inflammatory joint disease Biochemical Society Transactions 39 5 2011 1226 1232 21936794 21936794
  5. [5]Burska A.N. Autoantibodies to posttranslational modifications in rheumatoid arthritis Mediators of Inflammation 2014 2014 492873 24782594 24782594 PMC3981057
  6. [6]Morgan P.E. Sturgess A.D. Davies M.J. Increased levels of serum protein oxidation and correlation with disease activity in systemic lupus erythematosus Arthritis and Rheumatism 52 7 2005 2069 2079 15986354 15986354
  7. [7]Khan F. Siddiqui A.A. Ali R. Measurement and significance of 3-nitrotyrosine in systemic lupus erythematosus Scandinavian Journal of immunology 64 5 2006 507 514 17032243 17032243
  8. [8]Kirkham P.A. Barnes P.J. Oxidative stress in COPD Chest 144 1 2013 266 273 23880677 23880677
  9. [9]Binder C.J. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL Nature Medicine 9 6 2003 736 743 12740573 12740573
  10. [10]Kalluri R. Reactive oxygen species expose cryptic epitopes associated with autoimmune Goodpasture syndrome Journal of Biological Chemistry 275 26 2000 20027 20032 10748075 10748075
  11. [11]Scofield R.H. Modification of lupus-associated 60-kDa Ro protein with the lipid oxidation product 4-hydroxy-2-nonenal increases antigenicity and facilitates epitope spreading Free Radical Biology and Medicine 38 6 2005 719 728 15721982 15721982
  12. [12]Matzinger P. Tolerance, danger, and the extended family Annual Review of Immunology 12 1994 991 1045 8011301 8011301
  13. [13]Matzinger P. The danger model: arenewed sense of self Science (New York, N.Y.) 296 5566 2002 301 305 11951032 11951032
  14. [14]Lichtman A.H. Adaptive immunity in atherogenesis: new insights and therapeutic approaches Journal of Clinical investigation 123 1 2013 27 36 23281407 23281407 PMC3533280
  15. [15]Stavnezer J. Guikema J.E.J. Schrader C.E. Mechanism and regulation of class switch recombination Annual Review of Immunology 26 1 2008 261 292 18370922 PMC2707252 18370922
  16. [16]Bajénoff M. Wurtz O. Guerder S. Repeated antigen exposure is necessary for the differentiation, but not the initial proliferation, of naive CD4+ T cells Journal of Immunology (Baltimore, Md.: 1950) 168 4 2002 1723 1729 11823503 11823503
  17. [17]Tongren J.E. Target antigen, age, and duration of antigen exposure independently regulate immunoglobulin G subclass switching in malaria Infection and Immunity 74 1 2006 257 264 16368979 16368979 PMC1346665
  18. [18]Aalberse R.C. van der Gaag R. van Leeuwen J. Serologic aspects of IgG4 antibodies. I. Prolonged immunization results in an IgG4-restricted response Journal of Immunology (Baltimore, Md.: 1950) 130 2 1983 722 726 6600252 6600252
  19. [19]Casciola-Rosen L. Cleavage by granzyme B is strongly predictive of autoantigen status: implications for initiation of autoimmunity Journal of Experimental Medicine 190 6 1999 815 826 10499920 10499920 PMC2195625
  20. [20]Aletaha D. Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League against rheumatism collaborative initiative Arthritis and Rheumatism 62 9 2010 2569 2581 20872595 20872595
  21. [21]Schellekens G.A. Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies Journal of Clinical Investigation 101 1 1998 273 281 9421490 9421490 PMC508564
  22. [22]Brahms H. The C-terminal RG dipeptide repeats of the spliceosomal Sm proteins D1 and D3 contain symmetrical dimethylarginines, which form a major B-cell epitope for anti-Sm autoantibodies Journal of Biological Chemistry 275 22 2000 17122 17129 10747894 10747894
  23. [23]Molberg O. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease Nature Medicine 4 6 1998 713 717 9623982 9623982
  24. [24]Anderton S.M. Post-translational modifications of self antigens: implications for autoimmunity Current Opinion in Immunology 16 6 2004 753 758 15511669 15511669
  25. [25]Chou M.Y. Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans Journal of Clinical Investigation 119 5 2009 1335 1349 19363291 19363291 PMC2673862
  26. [26]Eggleton P. Detection and isolation of human serum autoantibodies that recognize oxidatively modified autoantigens Free Radical Biology and Medicine 57 2013 79 91 23246567 23246567
  27. [27]Ryan B.J. Eggleton P. Detection and characterization of autoantibodies against modified self-proteins in SLE sera after exposure to reactive oxygen and nitrogen species Methods in Molecular Biology (Clifton, N.J.) 1134 2014 163 171 24497361 24497361
  28. [28]Harman L.S. Mottley C. Mason R.P. Free radical metabolites of l-cysteine oxidation Journal of Biological Chemistry 259 9 1984 5606 5611 6325443 6325443
  29. [29]Wood Z.A. Structure, mechanism and regulation of peroxiredoxins Trends in Biochemical Sciences 28 1 2003 32 40 12517450 12517450
  30. [30]Stadtman E.R. Levine R.L. Protein oxidation Annals of the New York Academy of Sciences 899 1 2000 191 208 10863540
  31. [31]Simat T.J. Steinhart H. Oxidation of Free tryptophan and tryptophan residues in peptides and proteins Journal of Agricultural and Food Chemistry 46 2 1998 490 498 10554268 10554268
  32. [32]Heinecke J.W. Tyrosyl radical generated by myeloperoxidase catalyzes the oxidative cross-linking of proteins Journal of Clinical Investigation 91 6 1993 2866 2872 8390491 8390491 PMC443356
  33. [33]Ischiropoulos H. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase Archives of Biochemistry and Biophysics 298 2 1992 431 437 1416974 1416974
  34. [34]Alvarez B. Peroxynitrite-dependent tryptophan nitration Chemical Research in Toxicology 9 2 1996 390 396 8839040 8839040
  35. [35]Hazen S.L. Heinecke J.W. 3-Chlorotyrosine, a specific marker of myeloperoxidase-catalyzed oxidation, is markedly elevated in low density lipoprotein isolated from human atherosclerotic intima Journal of Clinical Investigation 99 9 1997 2075 2081 9151778 9151778 PMC508036
  36. [36]Pattison D.I. Davies M.J. Kinetic analysis of the role of histidine chloramines in hypochlorous acid mediated protein oxidation Biochemistry 44 19 2005 7378 7387 15882077 15882077
  37. [37]Chapman A.L.P. Chlorination of bacterial and neutrophil proteins during phagocytosis and killing of Staphylococcus aureus Journal of Biological Chemistry 277 12 2002 9757 9762 11733505 11733505
  38. [38]Uchida K. Stadtman E.R. Modification of histidine residues in proteins by reaction with 4-hydroxynonenal Proceedings of the National Academy of Sciences of the United States of America 89 10 1992 4544 4548 1584790 1584790 PMC49119
  39. [39]Bruenner B.A. Jones A.D. German J.B. Direct characterization of protein adducts of the lipid peroxidation product 4-hydroxy-2-nonenal using electrospray mass spectrometry Chemical Research in Toxicology 8 4 1995 552 559 7548735 7548735
  40. [40]Miyata T. Increased pentosidine, an advanced glycation end product, in plasma and synovial fluid from patients with rheumatoid arthritis and its relation with inflammatory markers Biochemical and Biophysical Research Communications 244 1 1998 45 49 9514872 9514872
  41. [41]Vitek M.P. Advanced glycation end products contribute to amyloidosis in Alzheimer disease Proceedings of the National Academy of Sciences of the United States of America 91 11 1994 4766 4770 8197133 8197133 PMC43869
  42. [42]Rodriguez-Garcia J. Requena J.R. Rodriguez-Segade S. Increased concentrations of serum pentosidine in rheumatoid arthritis Clinical Chemistry 44 2 1998 250 255 9474020 9474020
  43. [43]Casciola-Rosen L.A. Anhalt G. Rosen A. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes Journal of Experimental Medicine 179 4 1994 1317 1330 7511686 7511686 PMC2191465
  44. [44]Blanco P. Increase in activated CD8+ T lymphocytes expressing perforin and granzyme B correlates with disease activity in patients with systemic lupus erythematosus Arthritis and Rheumatism 52 1 2005 201 211 15641052 15641052
  45. [45]Herrmann M. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus Arthritis and Rheumatism 41 7 1998 1241 1250 9663482 9663482
  46. [46]Donnelly S. Impaired recognition of apoptotic neutrophils by the C1q/calreticulin and CD91 pathway in systemic lupus erythematosus Arthritis and Rheumatism 54 5 2006 1543 1556 16645988 16645988
  47. [47]Miller Y.I. Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity Circulation Research 108 2 2011 235 248 21252151 21252151 PMC3075542
  48. [48]Friggeri A. Participation of the receptor for advanced glycation end products in efferocytosis Journal of Immunology (Baltimore, Md.: 1950) 186 11 2011 6191 6198 21502377 PMC3955180 21502377
  49. [50]Wang G. Markers of oxidative and nitrosative stress in systemic lupus erythematosus: correlation with disease activity Arthritis and Rheumatism 62 7 2010 2064 2072 20201076 20201076 PMC2935652
  50. [51]de Leeuw K. Accumulation of advanced glycation endproducts in patients with systemic lupus erythematosus Rheumatology (Oxford, England) 46 10 2007 1551 1556 17848401 17848401
  51. [52]Otaki N. Identification of a lipid peroxidation product as the source of oxidation-specific epitopes recognized by anti-DNA autoantibodies Journal of Biological Chemistry 285 44 2010 33834 33842 20736172 20736172 PMC2962483
  52. [53]Arbuckle M.R. Development of autoantibodies before the clinical onset of systemic lupus erythematosus New England Journal of Medicine 349 16 2003 1526 1533 14561795 14561795
  53. [54]Kurien B.T. Degree of modification of Ro60 by the lipid peroxidation by-product 4-hydroxy-2-nonenal may differentially induce Sjögren syndrome or systemic lupus erythematosus in BALB/c mice Free Radical Biology and Medicine 50 10 2011 1222 1233 20946951 20946951 PMC3591494
  54. [55]Kurien B.T. Immunization with 60 kD Ro peptide produces different stages of preclinical autoimmunity in a Sjögren's syndrome model among multiple strains of inbred mice Clinical and Experimental Immunology 173 1 2013 67 75 23607771 PMC3694536
  55. [56]Korb L.C. Ahearn J.M. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited Journal of Immunology (Baltimore, Md.: 1950) 158 10 1997 4525 4528 9144462 9144462
  56. [57]Botto M. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies Nature Genetics 19 1 1998 56 59 9590289 9590289
  57. [58]Siegert C.E. Predictive value of IgG autoantibodies against C1q for nephritis in systemic lupus erythematosus Annals of the Rheumatic Diseases 52 12 1993 851 856 8311534 8311534 PMC1005214
  58. [59]Trendelenburg M. High prevalence of anti-C1q antibodies in biopsy-proven active lupus nephritis Nephrology, Dialysis, Transplantation: Official Publication of the European Dialysis and Transplant Association– European Renal Association 21 11 2006 3115 3121 16877491 16877491
  59. [60]Yin Y. Diagnostic value of serum anti-C1q antibodies in patients with lupus nephritis: a meta-analysis Lupus 21 10 2012 1088 1097 22777943 22777943
  60. [61]Trinder P.K. Altered (oxidized) C1q induces a rheumatoid arthritis-like destructive and chronic inflammation in joint structures in arthritis-susceptible rats Clinical Immunology and Immunopathology 82 2 1997 149 156 9000483 9000483
  61. [62]Ryan, B.J., The Effect of Oxidative Post-translational Modifications to C1q on its Antigenicity and Function, in Relation to the Pathogenesis of Systemic Lupus Erythematosus (Ph.D. thesis), Peninsula College of Medicine and Dentistry, Plymouth, UK, 2011.
  62. [64]Amara A. Autoantibodies to malondialdehyde-modified epitope in connective tissue diseases and vasculitides Clinical and Experimental Immunology 101 2 1995 233 238 7544246 7544246 PMC1553266
  63. [65]Svenungsson E. Risk factors for cardiovascular disease in systemic lupus erythematosus Circulation 104 16 2001 1887 1893 11602489 11602489
  64. [66]Frostegard J. Lipid peroxidation is enhanced in patients with systemic lupus erythematosus and is associated with arterial and renal disease manifestations Arthritis and Rheumatism 52 1 2005 192 200 15641060 15641060
  65. [67]Chen C. Stenzel-Poore M.P. Rittenberg M.B. Natural auto- and polyreactive antibodies differing from antigen-induced antibodies in the H chain CDR3 Journal of Immunology (Baltimore, Md.: 1950) 147 7 1991 2359 2367 1918968 1918968
  66. [68]Mannoor K. Expression of natural autoantibodies in MRL-lpr mice protects from lupus nephritis and improves survival Journal of Immunology (Baltimore, Md.: 1950) 188 8 2012 3628 3638 22407922 22407922
  67. [69]Schellekens G.A. The diagnostic properties of rheumatoid arthritis antibodies recognizing a cyclic citrullinated peptide Arthritis and Rheumatism 43 1 2000 155 163 10643712 10643712
  68. [70]Wang Z. Protein carbamylation links inflammation, smoking, uremia and atherogenesis Nature Medicine 13 10 2007 1176 1184 17828273 17828273
  69. [71]Jaisson S. Carbamylated albumin is a potent inhibitor of polymorphonuclear neutrophil respiratory burst FEBS Letters 581 7 2007 1509 1513 17376441 17376441
  70. [72]Garnotel R. Enhanced activation of and increased production of matrix metalloproteinase-9 by human blood monocytes upon adhering to carbamylated collagen FEBS Letters 563 1–3 2004 13 16 15063715 15063715
  71. [73]Scinocca M. Antihomocitrullinated fibrinogen antibodies are specific to rheumatoid arthritis and frequently bind citrullinated proteins/peptides Journal of Rheumatology 41 2 2014 270 279 24429169 24429169
  72. [74]Shi J. 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 108 42 2011 17372 17377 21987802 21987802 PMC3198314
  73. [75]Ligier S. Fortin P.R. Newkirk M.M. A new antibody in rheumatoid arthritis targeting glycated IgG: IgM anti-IgG-AGE British Journal of Rheumatology 37 12 1998 1307 1314 9973155 9973155
  74. [76]Griffiths H.R. Lunec J. Effect of polymorph derived oxidants on IgG in relation to rheumatoid factor binding Scandinavian Journal of Rheumatology. Supplement 75 1988 148 156 2853449 2853449
  75. [77]Margiloff L. Metal-catalyzed oxidation of immunoglobulin G impairs Fc receptor-mediated binding to macrophages Free Radical Biology and Medicine 25 7 1998 780 785 9823543 9823543
  76. [78]Griffiths H.R. Lunec J. The C1q binding activity of IgG is modified in vitro by reactive oxygen species: implications for rheumatoid arthritis FEBS Letters 388 2–3 1996 161 164 8690077 8690077
  77. [79]Uesugi M. Yoshida K. Jasin H.E. Inflammatory properties of IgG modified by oxygen radicals and peroxynitrite Journal of Immunology (Baltimore, Md.: 1950) 165 11 2000 6532 6537 11086095 11086095
  78. [80]Al-Shobaili H.A. Hydroxyl radical modification of immunoglobulin G generated cross-reactive antibodies: its potential role in systemic lupus erythematosus Clinical Medicine Insights: Arthritis and Musculoskeletal Disorders 4 2011 11 19 21487454 21487454 PMC3072208
  79. [81]Nissim A. Generation of neoantigenic epitopes after posttranslational modification of type II collagen by factors present within the inflamed joint Arthritis and Rheumatism 52 12 2005 3829 3838 16329077 16329077
  80. [82]Strollo R. Autoantibodies to posttranslationally modified type II collagen as potential biomarkers for rheumatoid arthritis Arthritis and Rheumatism 65 7 2013 1702 1712 23575908 23575908
  81. [83]Trigwell S.M. Islet glutamic acid decarboxylase modified by reactive oxygen species is recognized by antibodies from patients with type 1 diabetes mellitus Clinical and Experimental Immunology 126 2 2001 242 249 11703367 11703367 PMC1906190
  82. [84]Strollo R. HLA-dependent autoantibodies against post-translationally modified collagen type II in type 1 diabetes mellitus Diabetologia 56 3 2013 563 572 23160643 23160643
  83. [85]Feghali-Bostwick C.A. Autoantibodies in patients with chronic obstructive pulmonary disease American Journal of Respiratory and Critical Care Medicine 177 2 2008 156 163 17975205 17975205 PMC2204079
  84. [86]Kirkham P.A. Oxidative stress-induced antibodies to carbonyl-modified protein correlate with severity of chronic obstructive pulmonary disease American Journal of Respiratory and Critical Care Medicine 184 7 2011 796 802 21965015 21965015 PMC3398415
  85. [87]Bronte V. Boosting antitumor responses of T lymphocytes infiltrating human prostate cancers Journal of Experimental Medicine 201 8 2005 1257 1268 15824085 15824085 PMC2213151
  86. [88]De Sanctis F. The emerging immunological role of post-translational modifications by reactive nitrogen species in cancer microenvironment Frontiers in Immunology 5 2014 69 24605112 24605112 PMC3932549
  87. [89]Brändlein S. Natural IgM antibodies and immunosurveillance mechanisms against epithelial cancer cells in humans Cancer Research 63 22 2003 7995 8005 14633732 14633732
  88. [90]Brändlein S. Human monoclonal IgM antibodies with apoptotic activity isolated from cancer patients Human Antibodies 11 4 2002 107 119 12775891 12775891
  89. [91]bVollmers H.P. Brändlein S. Nature's Best weapons to fight cancer. Revival of human monoclonal IgM antibodies Human Antibodies 11 4 2002 131 142 12775893 12775893
  90. [92]Peters M.J. Relations between autoantibodies against oxidized low-density lipoprotein, inflammation, subclinical atherosclerosis, and cardiovascular disease in rheumatoid arthritis Journal of Rheumatology 35 8 2008 1495 1499 18597411 18597411
  91. [93]Skaggs B.J. Hahn B.H. McMahon M. Accelerated atherosclerosis in patients with SLE: mechanisms and management Nature Reviews: Rheumatology 8 4 2012 214 223 22331061 22331061 PMC3765069
  92. [94]Mok M.Y. Systemic sclerosis is an independent risk factor for increased coronary artery calcium deposition Arthritis and Rheumatism 63 5 2011 1387 1395 21538320 21538320
  93. [95]Dorman J.S. The Pittsburgh insulin-dependent diabetes mellitus (IDDM) morbidity and mortality study. Mortality results Diabetes 33 3 1984 271 276 6698317 6698317
  94. [96]Tsimikas S. Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events Journal of Lipid Research 48 2 2007 425 433 17093289 17093289
  95. [97]Horkko S. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid–protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins Journal of Clinical Investigation 103 1 1999 117 128 9884341 9884341 PMC407862
  96. [98]Shaw P.X. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity Journal of Clinical Investigation 105 12 2000 1731 1740 10862788 10862788 PMC378505
  97. [100]Huang Y. An abundant dysfunctional apolipoprotein A1 in human atheroma Nature Medicine 20 2 2014 193 203 24464187 PMC3923163 24464187
  98. [101]Tsimikas S. Human oxidation-specific antibodies reduce foam cell formation and atherosclerosis progression Journal of the American College of Cardiology 58 16 2011 1715 1727 21982317 21982317 PMC3230644
  99. [102]Tangye S.G. To B1 or not to B1: that really is still the question! Blood 121 26 2013 5109 5110 23813936 23813936
  100. [103]Welling G.W. Prediction of sequential antigenic regions in proteins FEBS Letters 188 2 1985 215 218 2411595 2411595
  101. [104]Winter J. Bleach activates a redox-regulated chaperone by oxidative protein unfolding Cell 135 4 2008 691 701 19013278 19013278 PMC2606091
  102. [105]Herold M. Anti-CCP: history and its usefulness Clinical and Developmental Immunology 12 2 2005 131 135 16050144 16050144 PMC2270729
  103. [106]Briley-Saebo K.C. Targeted molecular probes for imaging atherosclerotic lesions with magnetic resonance using antibodies that recognize oxidation-specific epitopes Circulation 117 25 2008 3206 3215 18541740 18541740 PMC4492476

Authors
Ryan, B. J., Nissim, A., & Winyard, P. G.
Affiliations
  • University of Oxford (GB)
  • Queen Mary University of London (GB)
  • University of Exeter (GB)
Corresponding author
Winyard, Paul G.
Venue
Redox Biology
Publisher
Elsevier BV
Published
2014
Volume
2
Pages
715-724
ISSN
2213-2317 (ISSN-L)
OpenAlex
W1987053691
Cited by
119
References
107
Citations by year
2026: 13 · 2025: 6 · 2024: 7 · 2023: 7 · 2022: 8 · 2021: 17 · 2020: 11 · 2019: 10 · 2018: 12 · 2017: 11 · 2016: 4 · 2015: 12 · 2014: 1
FWCI
1.53
Type
journal article
Language
en
Open access
Locations
  • Redox Biology (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Figshare (submittedVersion)
  • Open Research Exeter (University of Exeter) (submittedVersion, cc-by-nc-nd)
Funders
  • Versus Arthritis
  • Medical Research Council (MR/J002747/1)
Topics
  • Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
  • Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Keywords
oxidative post-translational modifications, autoimmune disease, neoantigens, autoantibodies, autoantigens, reactive oxygen species, free radicals, systemic lupus erythematosus, C1q, rheumatoid arthritis, type II collagen, pathogen-associated molecular patterns, atherosclerosis, inflammation, biomarkers, therapeutic target
MeSH terms
Arthritis, Rheumatoid, Autoantibodies, Autoantigens, Autoimmune Diseases, Chlorine, Humans, Lupus Erythematosus, Systemic, Protein Processing, Post-Translational, Glycation End Products, Advanced, Reactive Oxygen Species, Reactive Nitrogen Species

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review