Two rheumatoid arthritis-specific autoantigens correlate microbial immunity with autoimmune responses in joints

Journal of Clinical Investigation

Volumn 127, Issue 8, 2017, Pages 2946-2956

  Pianta, Annalisa ^a   Arvikar, Sheila L ^a   Strle, Klemen ^a   Drouin, Elise E ^a,c   Wang, Qi ^b,d   Costello, Catherine E ^b   Steere, Allen C ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Antigenics Inc   (United States)

^d WATERS CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FILAMIN A; GAMMA INTERFERON; HLA DR ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; N ACETYLGLUCOSAMINE 6 SULFATASE; ANTIRHEUMATIC AGENT; AUTOANTIGEN; EPITOPE; FILAMIN; N-ACETYLGLUCOSAMINE-6-SULFATASE; SULFATASE;

ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; COMMENSAL; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE SEVERITY; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; MAJOR CLINICAL STUDY; MICROBIAL IMMUNITY; MUCOSAL IMMUNITY; PARABACTEROIDES; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYARTHRITIS; PREVOTELLA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; SEQUENCE HOMOLOGY; SYNOVIUM; T LYMPHOCYTE; ARTHRITIS, RHEUMATOID; AUTOIMMUNITY; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOLOGY; JOINT; METABOLISM; MONONUCLEAR CELL; PATHOLOGY;

ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; AUTOANTIGENS; AUTOIMMUNITY; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; FILAMINS; GASTROINTESTINAL MICROBIOME; HLA-DR ANTIGENS; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; JOINTS; LEUKOCYTES, MONONUCLEAR; SULFATASES; SYNOVIAL MEMBRANE;

EID: 85026642886     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI93450     Document Type: Article

References (46)

1. Li Y, et al. Deficient activity of the nuclease MRE11A induces T cell aging and promotes arthritogenic effector functions in patients with rheumatoid arthritis. Immunity. 2016;45(4):903-916.
2. Gregersen PK, Silver J, Winchester RJ. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 1987;30(11):1205-1213.
3. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med. 2011;365(23):2205-2219.
4. Nishimura K, et al. Meta-analysis: diagnostic accuracy of anti-cyclic citrullinated peptide antibody and rheumatoid factor for rheumatoid arthritis. Ann Intern Med. 2007;146(11):797-808.
5. 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):273-281.
6. Suzuki K, et al. High diagnostic performance of ELISA detection of antibodies to citrullinated antigens in rheumatoid arthritis. Scand J Rheumatol. 2003;32(4):197-204.
7. del Puente A, Knowler WC, Pettitt DJ, Bennett PH. The incidence of rheumatoid arthritis is predicted by rheumatoid factor titer in a longitudinal population study. Arthritis Rheum. 1988;31(10):1239-1244.
8. Majka DS, et al. Duration of preclinical rheumatoid arthritis-related autoantibody positivity increases in subjects with older age at time of disease diagnosis. Ann Rheum Dis. 2008;67(6):801-807.
9. Nielen MM, et al. Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum. 2004;50(2):380-386.
10. Bachmaier K, Neu N, de la Maza LM, Pal S, Hessel A, Penninger JM. Chlamydia infections and heart disease linked through antigenic mimicry. Science. 1999;283(5406):1335-1339.
11. Miller SD, et al. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat Med. 1997;3(10):1133-1136.
12. Zhao ZS, Granucci F, Yeh L, Schaffer PA, Cantor H. Molecular mimicry by herpes simplex virustype 1: autoimmune disease after viral infection. Science. 1998;279(5355):1344-1347.
13. Scher JU, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202.
14. Zhang X, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21(8):895-905.
15. Maeda Y, et al. Dysbiosis contributes to arthritis development via activation of autoreactive T cells in the intestine. Arthritis Rheumatol. 2016;68(11):2646-2661.
16. Hemmer B, et al. Predictable TCR antigen recognition based on peptide scans leads to the identification of agonist ligands with no sequence homology. J Immunol. 1998;160(8):3631-3636.
17. Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med. 1998;4(7):781-785.
18. Ehl S, et al. Viral and bacterial infections interfere with peripheral tolerance induction and activate CD8+ T cells to cause immunopathology. J Exp Med. 1998;187(5):763-774.
19. Seward RJ, Drouin EE, Steere AC, Costello CE. Peptides presented by HLA-DR molecules in synovia of patients with rheumatoid arthritis or antibiotic-refractory Lyme arthritis. Mol Cell Proteomics. 2011;10(3):M110.002477.
20. Wang Q, et al. Immunogenic HLA-DR-presented self-peptides identified directly from clinical samples of synovial tissue, synovial fluid, or peripheral blood in patients with rheumatoid arthritis or Lyme arthritis. J Proteome Res. 2017;16(1):122-136.
21. Drouin EE, et al. A novel human autoantigen, endothelial cell growth factor, is a target of T and B cell responses in patients with Lyme disease. Arthritis Rheum. 2013;65(1):186-196.
22. Crowley JT, et al. A highly expressed human protein, apolipoprotein B-100, serves as an autoantigen in a subgroup of patients with Lyme disease. J Infect Dis. 2015;212(11):1841-1850.
23. Crowley JT, et al. Matrix metalloproteinase-10 is a target of T and B cell responses that correlate with synovial pathology in patients with antibiotic-refractory Lyme arthritis. J Autoimmun. 2016;69:24-37.
24. Pianta A, et al. Annexin A2 is a target of autoimmune T and B cell responses associated with synovial fibroblast proliferation in patients with antibiotic-refractory Lyme arthritis. Clin Immunol. 2015;160(2):336-341.
25. Pianta A, et al. Evidence for immune relevance of Prevotella copri, a gut microbe, in patients with rheumatoid arthritis. Arthritis Rheumatol. 2017;69(5):964-975.
26. Sturniolo T, et al. Generation of tissue-specific and promiscuous HLA ligand databases using DNA microarrays and virtual HLA class II matrices. Nat Biotechnol. 1999;17(6):555-561.
27. Mikuls TR, et al. Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol. 2014;66(5):1090-1100.
28. Sievers F, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7:539.
29. Yu CS, Lin CJ, Hwang JK. Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci. 2004;13(5):1402-1406.
30. Arvikar SL, et al. Clinical correlations with Porphyromonas gingivalis antibody responses in patients with early rheumatoid arthritis. Arthritis Res Ther. 2013;15(5):R109.
31. Benjdia A, Martens EC, Gordon JI, Berteau O. Sulfatases and a radical S-adenosyl-L-methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron. J Biol Chem. 2011;286(29):25973-25982.
32. Ulmer JE, et al. Characterization of glycosaminoglycan (GAG) sulfatases from the human gut symbiont Bacteroides thetaiotaomicron reveals the first GAG-specific bacterial endosulfatase. J Biol Chem. 2014;289(35):24289-24303.
33. Coutinho A, Kazatchkine MD, Avrameas S. Natural autoantibodies. Curr Opin Immunol. 1995;7(6):812-818.
34. Dighiero G. Natural autoantibodies, tolerance, and autoimmunity. Ann N Y Acad Sci. 1997;815:182-192.
35. Kroese FG, Butcher EC, Stall AM, Lalor PA, Adams S, Herzenberg LA. Many of the IgA producing plasma cells in murine gut are derived from self-replenishing precursors in the peritoneal cavity. Int Immunol. 1989;1(1):75-84.
36. Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science. 2000;288(5474):2222-2226.
37. Suzuki K, Ha SA, Tsuji M, Fagarasan S. Intestinal IgA synthesis: a primitive form of adaptive immunity that regulates microbial communities in the gut. Semin Immunol. 2007;19(2):127-135.
38. Kubinak JL, Round JL. Do antibodies select a healthy microbiota? Nat Rev Immunol. 2016;16(12):767-774.
39. Klareskog L, Rönnelid J, Lundberg K, Padyukov L, Alfredsson L. Immunity to citrullinated proteins in rheumatoid arthritis. Annu Rev Immunol. 2008;26:651-675.
40. Romero V, et al. Immune-mediated poreforming pathways induce cellular hypercitrullination and generate citrullinated autoantigens in rheumatoid arthritis. Sci Transl Med. 2013;5(209):209ra150.
41. Wang JY, Roehrl MH. Glycosaminoglycans are a potential cause of rheumatoid arthritis. Proc Natl Acad Sci U S A. 2002;99(22):14362-14367.
42. Kim H, McCulloch CA. Filamin A mediates interactions between cytoskeletal proteins that control cell adhesion. FEBS Lett. 2011;585(1):18-22.
43. Feng Y, et al. Filamin A (FLNA) is required for cell-cell contact in vascular development and cardiac morphogenesis. Proc Natl Acad Sci U S A. 2006;103(52):19836-19841.
44. Kuriya B, et al. Earlier time to remission predicts sustained clinical remission in early rheumatoid arthritis-results from the Canadian Early Arthritis Cohort (CATCH). J Rheumatol. 2014;41(11):2161-2166.
45. van Nies JA, Tsonaka R, Gaujoux-Viala C, Fautrel B, van der Helm-van Mil AH. Evaluating relationships between symptom duration and persistence of rheumatoid arthritis: does a window of opportunity exist? Results on the Leiden early arthritis clinic and ESPOIR cohorts. Ann Rheum Dis. 2015;74(5):806-812.
46. Aletaha D, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010;62(9):2569-2581.