Nucleic acid-stimulated antigen-presenting cells trigger T cells to induce disease in a rat transfer model of inflammatory arthritis

Journal of Autoimmunity

Volumn 36, Issue 3-4, 2011, Pages 288-300

  Hoffmann, Markus H ^a   Skriner, Karl ^b   Herman, Sonja ^a   Baumann, Christoph ^c   Steiner, Carl Walter ^a   Ospelt, Caroline ^d   Meyer, Brigitte ^a   Gleiss, Andreas ^a   Pfatschbacher, Jürgen ^a   Niederreiter, Birgit ^a   Tuncel, Jonatan ^e   Zanoni, Gerald ^f   Steiner, Guenter ^a,g  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b HUMBOLDT UNIVERSITY   (Germany)

^c ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^e KAROLINSKA INSTITUTE   (Sweden)

^f FEDERAL RESEARCH AND TRAINING CENTRE FOR FORESTS   (Austria)

^g Ludwig Boltzmann Cluster for Cardiovascular Research   (Austria)

Author keywords

Arthritis; Autoantigen; Damage associated molecular pattern; Innate immunity; Toll like receptors

Indexed keywords

DNA; NUCLEIC ACID; OLIGONUCLEOTIDE; PRISTANE; RNA; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CONTROLLED STUDY; DNA BINDING; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; RAT; RHEUMATOID ARTHRITIS; RNA BINDING; SPLEEN CELL; T LYMPHOCYTE;

ANIMALS; ANTIGEN-PRESENTING CELLS; ARTHRITIS, RHEUMATOID; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; RATS; T-LYMPHOCYTES; TERPENES; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 9;

EID: 79954847184     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2011.02.007     Document Type: Article

References (60)

1. Choy E.H., Panayi G.S. Cytokine pathways and joint inflammation in rheumatoid arthritis. New England Journal of Medicine 2001, 344:907-916.
2. Foell D., Wittkowski H., Roth J. Mechanisms of disease: a 'DAMP' view of inflammatory arthritis. Nature Clinical Practice Rheumatology 2007, 3:382-390.
3. Brentano F., Schorr O., Gay R.E., Gay S., Kyburz D. RNA released from necrotic synovial fluid cells activates rheumatoid arthritis synovial fibroblasts via Toll-like receptor 3. Arthritis & Rheumatism 2005, 52:2656-2665.
4. Iwahashi M., Yamamura M., Aita T., Okamoto A., Ueno A., Ogawa N., et al. Expression of Toll-like receptor 2 on CD16+ blood monocytes and synovial tissue macrophages in rheumatoid arthritis. Arthritis & Rheumatism 2004, 50:1457-1467.
5. Radstake T.R., Roelofs M.F., Jenniskens Y.M., Oppers-Walgreen B., van Riel P.L., Barrera P., et al. Expression of toll-like receptors 2 and 4 in rheumatoid synovial tissue and regulation by proinflammatory cytokines interleukin-12 and interleukin-18 via interferon-gamma. Arthritis & Rheumatism 2004, 50:3856-3865.
6. Seibl R., Birchler T., Loeliger S., Hossle J.P., Gay R.E., Saurenmann T., et al. Expression and regulation of toll-like receptor 2 in rheumatoid arthritis synovium. American Journal of Pathology 2003, 162:1221-1227.
7. Mayeda A., Munroe S.H., Caceres J.F., Krainer A.R. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO Journal 1994, 13:5483-5495.
8. Steiner G., Hartmuth K., Skriner K., Maurer Fogy I., Sinski A., Thalmann E., et al. Purification and partial sequencing of the nuclear autoantigen RA33 shows that it is indistinguishable from the A2 p.otein of the heterogeneous nuclear ribonucleoprotein complex. Journal of Clinical Investigation 1992, 90:1061-1066.
9. Greidinger E.L., Gazitt T., Jaimes K.F., Hoffmann R.W. Human T cell clones specific for heterogeneous nuclear ribonucleoprotein A2 autoantigen from connective tissue disease patients assist in autoantibody production. Arthritis & Rheumatism 2004, 50:2216-2222.
10. Fritsch R., Eselbock D., Skriner K., Jahn-Schmid B., Scheinecker C., Bohle B., et al. Characterization of autoreactive T cells to the autoantigens heterogeneous nuclear ribonucleoprotein A2 (RA33) and filaggrin in patients with rheumatoid arthritis. Journal of Immunology 2002, 169:1068-1076.
11. Fritsch-Stork R., Mullegger D., Skriner K., Jahn-Schmid B., Smolen J.S., Steiner G. The spliceosomal autoantigen heterogeneous nuclear ribonucleoprotein A2 (hnRNP-A2) is a major T cell autoantigen in patients with systemic lupus erythematosus. Arthritis Research & Therapy 2006, 8:R118.
12. Steiner G., Skriner K., Smolen J.S. Autoantibodies to the A/B proteins of the heterogeneous nuclear ribonucleoprotein complex: novel tools for the diagnosis of rheumatic diseases. International Archives of Allergy & Immunology 1996, 111:314-319.
13. Trembleau S., Hoffmann M., Meyer B., Nell V., Radner H., Zauner W., et al. Immunodominant T-cell epitopes of hnRNP-A2 associated with disease activity in patients with rheumatoid arthritis. European Journal of Immunology 2010, 40:1795-1808.
14. Skriner K., Sommergruber W.H., Tremmel V., Fischer I., Barta A., Smolen J.S., et al. Anti-A2/RA33 autoantibodies are directed to the RNA binding region of the A2 p.otein of the heterogeneous nuclear ribonucleoprotein complex. Differential epitope recognition in rheumatoid arthritis, systemic lupus erythematosus, and mixed connective tissue disease. Journal of Clinical Investigation 1997, 100:127-135.
15. Schett G., Dumortier H., Hoefler E., Muller S., Steiner G. B cell epitopes of the heterogeneous nuclear ribonucleoprotein A2: identification of a new specific antibody marker for active lupus disease. Annals of the Rheumatic Diseases 2009, 68:729-735.
16. Vingsbo C., Sahlstrand P., Brun J.G., Jonsson R., Saxne T., Holmdahl R. Pristane-induced arthritis in rats: a new model for rheumatoid arthritis with a chronic disease course influenced by both major histocompatibility complex and non-major histocompatibility complex genes. American Journal of Pathology 1996, 149:1675-1683.
17. Hoffmann M.H., Tuncel J., Skriner K., Tohidast-Akrad M., Turk B., Pinol-Roma S., et al. The rheumatoid arthritis-associated autoantigen hnRNP-A2 (RA33) is a major stimulator of autoimmunity in rats with pristane-induced arthritis. Journal of Immunology 2007, 179:7568-7576.
18. Hoffmann M.H., Hayer S., Steiner G. Immmunopathogenesis of rheumatoid arthritis. Induction of arthritogenic autoimmune responses by proinflammatory stimuli. Annals of the New York Academy of Sciences 2009, 1173:391-400.
19. Ospelt C., Brentano F., Rengel Y., Stanczyk J., Kolling C., Tak P.P., et al. Overexpression of toll-like receptors 3 and 4 in synovial tissue from patients with early rheumatoid arthritis: toll-like receptor expression in early and longstanding arthritis. Arthritis & Rheumatism 2008, 58:3684-3692.
20. Arnett F.C., Edworthy S.M., Bloch D.A., McShane D.J., Fries J.F., Cooper N.S., et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis & Rheumatism 1988, 31:315-324.
21. Hoffmann M.H., Hopf R., Niederreiter B., Redl H., Smolen J.S., Steiner G. Gait changes precede overt arthritis and strongly correlate with symptoms and histopathological events in pristane-induced arthritis. Arthritis Research & Therapy 2010, 12:R41.
22. Holmberg J., Tuncel J., Yamada H., Lu S., Olofsson P., Holmdahl R. Pristane, a non-antigenic adjuvant, induces MHC class II-restricted, arthritogenic T cells in the rat. Journal of Immunology 2006, 176:1172-1179.
23. Lau C.M., Broughton C., Tabor A.S., Akira S., Flavell R.A., Mamula M.J., et al. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. Journal of Experimental Medicine 2005, 202:1171-1177.
24. Vollmer J., Tluk S., Schmitz C., Hamm S., Jurk M., Forsbach A., et al. Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. Journal of Experimental Medicine 2005, 202:1575-1585.
25. Brooks S.A., Rigby W.F. Characterization of the mRNA ligands bound by the RNA binding protein hnRNP A2 utilizing a novel in vivo technique. Nucleic Acids Research 2000, 28:E49.
26. He Y., Smith R. Nuclear functions of heterogeneous nuclear ribonucleoproteins A/B. Cellular & Molecular Life Sciences 2009, 66:1239-1256.
27. Haas T., Metzger J., Schmitz F., Heit A., Muller T., Latz E., et al. The DNA sugar backbone 2' deoxyribose determines toll-like receptor 9 activation. Immunity 2008, 28:315-323.
28. Liu J., Xu C., Hsu L.C., Luo Y., Xiang R., Chuang T.H. A five-amino-acid motif in the undefined region of the TLR8 ectodomain is required for species-specific ligand recognition. Molecular Immunology 2010, 47:1083-1090.
29. Sun S., Rao N.L., Venable J., Thurmond R., Karlsson L. TLR7/9 antagonists as therapeutics for immune-mediated inflammatory disorders. Inflammation & Allergy Drug Targets 2007, 6:223-235.
30. Baechler E.C., Batliwalla F.M., Karypis G., Gaffney P.M., Ortmann W.A., Espe K.J., et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:2610-2615.
31. Farkas L., Beiske K., Lund-Johansen F., Brandtzaeg P., Jahnsen F.L. Plasmacytoid dendritic cells (natural interferon- alpha/beta-producing cells) accumulate in cutaneous lupus erythematosus lesions. American Journal of Pathology 2001, 159:237-243.
32. Nacionales D.C., Kelly K.M., Lee P.Y., Zhuang H., Li Y., Weinstein J.S., et al. Type I Interferon production by tertiary lymphoid tissue developing in response to 2,6,10,14-tetramethyl-pentadecane (pristane). American Journal of Pathology 2006, 168:1227-1240.
33. Nacionales D.C., Kelly-Scumpia K.M., Lee P.Y., Weinstein J.S., Lyons R., Sobel E., et al. Deficiency of the type I interferon receptor protects mice from experimental lupus. Arthritis & Rheumatism 2007, 56:3770-3783.
34. Ganguly D., Chamilos G., Lande R., Gregorio J., Meller S., Facchinetti V., et al. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. Journal of Experimental Medicine 2009, 206:1983-1994.
35. Lande R., Gregorio J., Facchinetti V., Chatterjee B., Wang Y.H., Homey B., et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007, 449:564-569.
36. Roelofs M.F., Joosten L.A., Abdollahi-Roodsaz S., van Lieshout A.W., Sprong T., van den Hoogen F.H., et al. The expression of toll-like receptors 3 and 7 in rheumatoid arthritis synovium is increased and costimulation of toll-like receptors 3, 4, and 7/8 results in synergistic cytokine production by dendritic cells. Arthritis & Rheumatism 2005, 52:2313-2322.
37. van der Pouw Kraan T.C., Wijbrandts C.A., van Baarsen L.G., Voskuyl A.E., Rustenburg F., Baggen J.M., et al. Rheumatoid arthritis subtypes identified by genomic profiling of peripheral blood cells: assignment of a type I interferon signature in a subpopulation of patients. Annals of the Rheumatic Diseases 2007, 66:1008-1014.
38. Isnardi I., Ng Y.S., Srdanovic I., Motaghedi R., Rudchenko S., von Bernuth H., et al. IRAK-4- and MyD88-dependent pathways are essential for the removal of developing autoreactive B cells in humans. Immunity 2008, 29:746-757.
39. Tabeta K., Hoebe K., Janssen E.M., Du X., Georgel P., Crozat K., et al. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nature Immunology 2006, 7:156-164.
40. Samuels J., Ng Y.S., Coupillaud C., Paget D., Meffre E. Impaired early B cell tolerance in patients with rheumatoid arthritis. Journal of Experimental Medicine 2005, 201:1659-1667.
41. Hoffmann M.H., Steiner G. A Common pathway for all autoimmune diseases? The unholy alliance of environment, cell death and nucleic acids. Current Immunology Reviews 2009, 5:69-88.
42. Sverdrup B., Kallberg H., Bengtsson C., Lundberg I., Padyukov L., Alfredsson L., et al. Association between occupational exposure to mineral oil and rheumatoid arthritis: results from the Swedish EIRA case-control study. Arthritis Research & Therapy 2005, 7:R1296-R1303.
43. Dedera D.A., Urashima M., Chauhan D., LeBrun D.P., Bronson R.T., Anderson K.C. Interleukin-6 is required for pristane-induced plasma cell hyperplasia in mice. British Journal of Haematology 1996, 94:53-61.
44. Lee P.Y., Kumagai Y., Li Y., Takeuchi O., Yoshida H., Weinstein J.S., et al. TLR7-dependent and FcgammaR-independent production of type I interferon in experimental mouse lupus. Journal of Experimental Medicine 2008, 205:2995-3006.
45. Janz S., Shacter E. A new method for delivering alkanes to mammalian cells: preparation and preliminary characterization of an inclusion complex between beta-cyclodextrin and pristane (2,6,10,14-tetramethylpentadecane). Toxicology 1991, 69:301-315.
46. Calvani N., Caricchio R., Tucci M., Sobel E.S., Silvestris F., Tartaglia P., et al. Induction of apoptosis by the hydrocarbon oil pristane: implications for pristane-induced lupus. Journal of Immunology 2005, 175:4777-4782.
47. Holmdahl R., Lorentzen J.C., Lu S., Olofsson P., Wester L., Holmberg J., et al. Arthritis induced in rats with non-immunogenic adjuvants as models for rheumatoid arthritis. Immunological Reviews 2001, 184:184-202.
48. Kinne R.W., Brauer R., Stuhlmuller B., Palombo-Kinne E., Burmester G.R. Macrophages in rheumatoid arthritis. Arthritis Research 2000, 2:189-202.
49. Mulherin D., Fitzgerald O., Bresnihan B. Synovial tissue macrophage populations and articular damage in rheumatoid arthritis. Arthritis & Rheumatism 1996, 39:115-124.
50. Gibbons L.J., Hyrich K.L. Biologic therapy for rheumatoid arthritis: clinical efficacy and predictors of response. BioDrugs 2009, 23:111-124.
51. Moran-Jones K., Wayman L., Kennedy D.D., Reddel R.R., Sara S., Snee M.J., et al. hnRNP A2, a potential ssDNA/RNA molecular adapter at the telomere. Nucleic Acids Research 2005, 33:486-496.
52. Gantier M.P., Tong S., Behlke M.A., Xu D., Phipps S., Foster P.S., et al. TLR7 is involved in sequence-specific sensing of single-stranded RNAs in human macrophages. Journal of Immunology 2008, 180:2117-2124.
53. Ito T., Yang M., Wang Y.H., Lande R., Gregorio J., Perng O.A., et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatorycells by inducible costimulator ligand. Journal of Experimental Medicine 2007, 204:105-115.
54. Jongbloed S.L., Benson R.A., Nickdel M.B., Garside P., McInnes I.B., Brewer J.M. Plasmacytoid dendritic cells regulate breach of selftolerance in autoimmune arthritis. Journal of Immunology 2009, 182:963-968.
55. 1 regulatory T cells. Journal of Immunology 2004, 173:4433-4442.
56. Ochando J.C., Homma C., Yang Y., Hidalgo A., Garin A., Tacke F., et al. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nature Immunology 2006, 7:652-662.
57. Cella M., Facchetti F., Lanzavecchia A., Colonna M. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 p.larization. Nature Immunology 2000, 1:305-310.
58. Barrat F.J., Meeker T., Gregorio J., Chan J.H., Uematsu S., Akira S., et al. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. Journal of Experimental Medicine 2005, 202:1131-1139.
59. Means T.K., Latz E., Hayashi F., Murali M.R., Golenbock D.T., Luster A.D. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. Journal of Clinical Investigation 2005, 115:407-417.
60. Blanco P., Palucka A.K., Gill M., Pascual V., Banchereau J. Induction of dendritic cell differentiation by IFN-α in systemic lupus erythematosus. Science 2001, 294:1540-1543.