Antigen presentation by dendritic cells in rheumatoid arthritis

Current Topics in Medicinal Chemistry

Volumn 13, Issue 6, 2013, Pages 712-719

  Rodríguez Fernández, José Luis ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Adaptive immune response; Citrullination; Immunological synapse; Shared epitope

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CD72 ANTIGEN; CD86 ANTIGEN; CITRULLINE; CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; EPITOPE; HLA DRB1 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 6; METALLOPROTEINASE; RHEUMATOID FACTOR; SECONDARY LYMPHOID TISSUE CHEMOKINE; TUMOR NECROSIS FACTOR ALPHA;

ALLELE; ANTIGEN PRESENTATION; ARTHRITIS; ARTICLE; CD4+ T LYMPHOCYTE; CHEMICAL STRUCTURE; DENDRITIC CELL; GENETIC SUSCEPTIBILITY; HLA SYSTEM; HUMAN; IMMUNE RESPONSE; INFLAMMATORY DISEASE; LYMPHOID TISSUE; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; SIDE EFFECT; STIMULATION; SYNOVIUM;

ANIMALS; ANTIGEN PRESENTATION; ARTHRITIS, RHEUMATOID; DENDRITIC CELLS; HUMANS;

EID: 84878809006     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/1568026611313060004     Document Type: Article

References (99)

1. Scott, D. L.; Wolfe, F.; Huizinga, T. W., Rheumatoid arthritis. Lancet 2010, 376(10) 1094-1108.
2. Klareskog, L.; Catrina, A.; Paget, S., Rheumatoid arthritis Lancet 2009, 373(9664) 659-672.
3. Steinman, R. M., Dendritic cells: versatile controllers of the immune system. Nat. Med. 2007, 13(10) 1155-1159.
4. Jones, E. Y.; Fugger, L.; Strominger, J. L.; Siebold, C., MHC class II proteins and disease: a structural perspective. Nat. Rev. Immunol. 2006, 6(4) 271-282.
5. Cope, A. P., T cells in rheumatoid arthritis. Arthritis Res Ther. 2008, 10 (Suppl 1), S1.
6. Devereux, D.; RE, O. H.; McGuire, J.; van Schooten, W. C.; Lamb, J. R., HLA-DR4Dw4-restricted T cell recognition of self antigen(s) in the rheumatoid synovial compartment. Int. Immunol. 1990, 3(7) 635-640.
7. Gaston, J. S.; Solovera, J.; Strober, S., Recognition of self class II major histocompatibility complex antigens by CD8 T cell clones derived from rheumatoid arthritis synovial membrane. Autoimmunity 1990, 8(2) 115-123.
8. Goronzy, J. J.; Bartz-Bazzanella, P.; Hu, W.; Jendro, M. C.; Walser-Kuntz, D. R.; Weyand, C. M., Dominant clonotypes in the repertoire of CD4 T cells in rheumatoid arthritis. J. Clin. Invest. 1994, 94(5) 2068-2076.
9. Waase, I.; Kayser, C.; Carlson, P. J.; Goronzy, J. J.; Weyand, C. M., Oligoclonal T cell proliferation in patients with rheumatoid arthritis and their unaffected siblings. Arthr. Rheum. 1996, 39(6) 904-913.
10. Moder, K. G.; Luthra, H. S.; Kubo, R.; Griffiths, M.; David, C. S., Prevention of collagen induced arthritis in mice by treatment with an antibody directed against the T cell receptor alpha beta framework. Autoimmunity 1992, 11(4) 219-224.
11. Moder, K. G.; Luthra, H. S.; Griffiths, M.; David, C. S., Prevention of collagen induced arthritis in mice by deletion of T cell receptor V beta 8 bearing T cells with monoclonal antibodies. Br J Rheumatol. 1993, 32(1) 26-30.
12. Hemler M. E.; Glass, D.; Coblyn, J. S.; Jacobson, J. G., Very late activation antigens on rheumatoid synovial fluid T lymphocytes. Association with stages of T cell activation. J. Clin. Invest. 1986, 78(3) 696-702.
13. Salmon, M.; Gaston, J. S., The role of T-lymphocytes in rheumatoid arthritis. Br. Med. Bull. 1995, 51(2) 332-345.
14. Brennan, F. M.; Chantry, D.; Jackson, A.; Maini, R.; Feldmann, M., Inhibitory effect of TNF alpha antibodies on synovial cell interleukin-1 production in rheumatoid arthritis. Lancet 1989, 2(8657) 244-247.
15. Burger, D.; Dayer, J. M.; Palmer, G.; Gabay, C., Is IL-1 a good therapeutic target in the treatment of arthritis? Best Pract Res Clin Rheumatol 2006, 20(5) 879-896.
16. Nishimoto, N.; Kishimoto, T., Interleukin 6: from bench to bedside. Nat Clin Pract Rheumatol. 2006, 2(11) 619-626.
17. Moreland, L. W.; Schiff, M. H.; Baumgartner, S. W.; Tindall, E. A.; Fleischmann, R. M.; Bulpitt, K. J.; Weaver, A. L.; Keystone, E. C.; Furst, D. E.; Mease, P. J.; Ruderman, E. M.; Horwitz, D. A.; Arkfeld, D. G.; Garrison, L.; Burge, D. J.; Blosch, C. M.; Lange, M. L.; McDonnell, N. D.; Weinblatt, M. E., Etanercept therapy in rheumatoid arthritis. A randomized, controlled trial. Ann. Intern. Med. 1999, 130(6) 478-486.
18. Jiang, Y.; Genant, H. K.; Watt, I.; Cobby, M.; Bresnihan, B.; Aitchison, R.; McCabe, D., A multicenter, double-blind, dose-ranging, randomized, placebo-controlled study of recombinant human interleukin-1 receptor antagonist in patients with rheumatoid arthritis: radiologic progression and correlation of Genant and Larsen scores. Arthritis Rheum. 2000, 43(5) 1001-1009.
19. Nishimoto N; Yoshizaki K; Miyasaka N; Yamamoto K; Kawai S; Takeuchi T; Hashimoto J; Azuma J T K., Treatment of rheumatoid arthritis with humanized anti-interleukin-6 receptor antibody: a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum. 2004, 50(6) 1761-1769.
20. Brennan, F. M.; McInnes, I. B., Evidence that cytokines play a role in rheumatoid arthritis. J. Clin. Invest. 2008, 118(11) 3537-3545.
21. Boissier, M.-C., Cell and cytokine imbalances in rheumatoid synovitis. Joint Bone Spine 2011, 78(3) 230-234.
22. Hofbauer, L. C.; Lacey, D. L.; Dunstan, C. R.; Spelsberg, T. C.; Riggs, B. L.; Khosla, S., Interleukin-1-beta and tumor necrosis factor-alpha, but not interleukin-6, stimulate osteoprotegerin ligand gene expression in human osteoblastic cells. Bone 1999, 25(3) 255-259.
23. Abeles, A. M.; Pillinger, M. H., The role of the synovial fibroblast in rheumatoid arthritis: cartilage destruction and the regulation of matrix metalloproteinases. Bull. NYU Hosp. Jt. Dis. 2006, 64(1-2) 20-24.
24. Shen, H.; Goodall, J. C.; Gaston, J. S., Frequency and phenotype of T helper 17 cells in peripheral blood and synovial fluid of patients with reactive arthritis. J Rheumatol. 2010, 37(10) 2096-2099.
25. Lubberts, E., Th17 cytokines and arthritis. Semin Immunopathol. 2010, 32(1) 43-53.
26. Nielen, M. M.; van Scha ardenburg, D.; Reesink, H. W.; van de Stadt, R. J.; van der Horst-Bruinsma, I. E.; de Koning, M. H.; Habibuw, M. R.; Vandenbroucke, J. P.; Dijkmans, B. A., Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum. 2004, 50(2) 380-386.
27. Snir, O.; Widhe, M.; Hermansson, M.; von Spee, C.; Lindberg, J.; Hensen, S.; Lundberg, K.; Engström, A.; Venables, P. J.; Toes, R. E.; Holmdahl, R.; Klareskog, L.; Malmström, V., Antibodies to several citrullinated antigens are enriched in the joints of rheumatoid arthritis patients. Arthritis Rheum. 2010, 62(1) 44-52.
28. Wegner, N.; Lundberg, K.; Kinloch, A.; Fisher, B.; Malmström, V.; Feldmann, M.; Venables, P. J., Autoimmunity to specific citrullinated proteins gives the first clues to the etiology of rheumatoid arthritis. Immunol Rev. 2010, 233(1) 34-54.
29. Doyle, H. A.; Mamula, M. J., Autoantigenesis: the evolution of protein modifications in autoimmune disease. Curr Opin Immunol. 2012, 24(1) 112-118.
30. Vossenaar, E. R.; Radstake, T. R.; van der Heijden, A.; van Mansum, M. A.; Dieteren, C.; de Rooij, D. J.; Barrera, P.; Zendman, A. J.; van Venrooij, W. J., Expression and activity of citrullinating peptidylarginine deiminase enzymes in monocytes and macro-phages. Ann Rheum Dis. 2004, 63(4) 373-381.
31. Foulquier, C.; Sebbag, M.; Clavel, C.; Chapuy-Regaud, S.; Al Badine, R.; Méchin, M. C.; Vincent, C.; Nachat, R.; Yamada, M.; Takahara, H.; Simon, M.; Guerrin, M.; Serre, G., Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation Arthritis Rheum. 2007, 56(11) 3541-3553.
32. Kinloch, A.; Lundberg, K.; Wait, R.; Wegner, N.; Lim, N. H.; Zendman, A. J.; Saxne, T.; Malmström, V.; Venables, P. J., Synovial fluid is a site of citrullination of autoantigens in inflammatory arthritis. Arthritis Rheum. 2008, 58(8) 2287-2295.
33. Lundberg, K.; Kinloch, A.; Fisher, B. A.; Wegner, N.; Wait, R.; Charles, P.; Mikuls, T. R.; Venables, P. J., Antibodies to citrullinated alpha-enolase peptide 1 are specific for rheumatoid arthritis and cross-react with bacterial enolase. Arthritis Rheum. 2008, 58(10) 3009-3019.
34. Makrygiannakis, D.; Hermansson, M.; Ulfgren, A. K.; Nicholas, A. P.; Zendman, A. J.; Eklund, A.; Grunewald, J.; Skold, C. M.; Klareskog, L.; Catrina, A. I., Smoking increases peptidylarginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann Rheum Dis. 2008, 67(10) 1488-1492.
35. De Pablo, P.; Chapple, I. L.; Buckley, C. D.; Dietrich, T., Periodontitis in systemic rheumatic diseases. Nat Rev Rheumatol 2009, 5(4) 218-224.
36. Wegner, N.; Wait, R.; Sroka, A.; Eick, S.; Nguyen, K. A.; Lundberg, K.; Kinloch, A.; Culshaw, S.; Potempa, J.; Venables, P. J., Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum. 2010, 62(9) 2662-2672.
37. Shi, J.; Knevel, R.; Suwannalai, P.; van der Linden, M. P.; Janssen, G. M.; van Veelen, P. A.; Levarht, N. E.; van der Helm-van Mil, A. H.; Cerami, A.; Huizinga, T. W.; Toes, R. E.; Trouw, L. A., Autoantibodies recognizing carbamylated proteins are present in sera of patients with rheumatoid arthritis and predict joint damage. Proc Natl Acad Sci U S A. 2011, 108(42) 17372-17377.
38. Huizinga, T. W.; Amos, C. I.; van der Helm-van Mil, A. H.; Chen, W.; van Gaalen, F. A.; Jawaheer, D.; Schreuder, G. M.; Wener, M.; Breedveld, F. C.; Ahmad, N.; Lum, R. F.; de Vries, R. R.; Gregersen, P. K.; Toes, R. E.; Criswell, L. A., Refining the complex rheumatoid arthritis phenotype based on specificity of the HLA-DRB1 shared epitope for antibodies to citrullinated proteins. Arthritis Rheum. 2005, 52(11) 3433-3438.
39. Vencovsk, J.; Machácek, S.; Sedová, L.; Kafková, J.; Gatterová, J.; Pesáková, V.; R zicková, S., Autoantibodies can be prognostic markers of an erosive disease in early rheumatoid arthritis. Ann Rheum Dis. 2003, 62(5) 427-430.
40. Kuhn, K. A.; Kulik, L.; Tomooka, B.; Braschler, K. J.; Arend, W. P.; Robinson, W. H.; Holers, V. M., Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis J. Clin. Invest. 2006, 116(4) 961-973.
41. Klareskog, L.; Rönnelid, J.; Lundberg, K.; Padyukov, L.; Alfredsson, L., Immunity to citrullinated proteins in rheumatoid arthritis. Annu. Rev. Immunol. 2008, 26, 651-675.
42. van Gaalen, F. A.; van Aken, J.; Huizinga, T. W.; Schreuder, G. M.; Breedveld, F. C.; Zanelli, E.; van Venrooij, W. J.; Verweij, C. L.; Toes, R. E.; de Vries, R. R., Association between HLA class II genes and autoantibodies to cyclic citrullinated peptides (CCPs) influences the severity of rheumatoid arthritis. Arthritis Rheum 2004, 50(7) 2113-2121.
43. Hoffman, I.; Peene, I.; Cebecauer, L.; Isenberg, D.; Huizinga, T. W.; Union, A.; Meheus, L.; De Bosschere, K.; Hulstaert, F.; Veys, E. M.; De Keyser, F., Presence of rheumatoid factor and antibodies to citrullinated peptides in systemic lupus erythematosus. Ann Rheum Dis. 2005, 64(2) 330-332.
44. Schellekens, G. A.; Visser, H.; de Jong, B. A.; van den Hoogen, F. H.; Hazes, J. M.; Breedveld, F. C.; van Venrooij, W. J., The diagnostic properties of rheumatoid arthritis antibodies recognizing a cyclic citrullinated peptide. Arthritis Rheum. 2000, 43(1) 155-163
45. Zanelli, E.; Breedveld, F. C.; de Vries, R. R., HLA class II association with rheumatoid arthritis: facts and interpretations. Hum Immunol. 2000, 61(12) 1254-1261.
46. Fugger, L.; Rothbard, J. B.; Sonderstrup-McDevitt, G., Specificity of an HLA-DRB1*0401-restricted T cell response to type II collagen. Eur. J. Immunol. 1996, 26(4) 928-933.
47. Rosloniec, E. F.; Brand, D. D.; Myers, L. K.; Whittington, K. B.; Gumanovskaya, M.; Zaller, D. M.; Woods, A.; Altmann, D. M.; Stuart, J. M.; Kang, A. H., An HLA-DR1 transgene confers susceptibility to collagen-induced arthritis elicited with human type II collagen. J. Exp. Med. 1997, 185(6) 1113-1122.
48. Rosloniec, E. F.; Brand, D. D.; Myers, L. K.; Esaki, Y.; Whittington, K. B.; Zaller, D. M.; Woods, A.; Stuart, J. M.; Kang, A. H., Induction of autoimmune arthritis in HLA-DR4 (DRB1*0401) transgenic mice by immunization with human and bovine type II collagen. J. Immunol. 1998, 160(6) 2573-2578.
49. Andersson, E. C.; Hansen, B. E.; Jacobsen, H.; Madsen, L. S.; Andersen, C. B.; Engberg, J.; Rothbard, J. B.; McDevitt, G. S.; Malmstrom, V.; Holmdahl, R.; Fugger, L., Definition of MHC and T cell receptor contacts in the HLA-DR4 restricted immunodominant epitope in type II collagen and characterization of collagen-induced arthritis in HLA-DR4 and human CD4 transgenic mice. Proc. Natl. Acad. Sci. USA 1998, 95(13) 7574-7579.
50. Gregersen, P. K.; Silver, J.; Winchester, R. J., The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 1987, 30(11) 1205-1213.
51. Wucherpfennig, K. W.; Strominger, J. L., Selective binding of self peptides to disease-associated major histocompatibility complex (MHC) molecules: a mechanism for MHC-linked susceptibility to human autoimmune diseases. J Exp Med. 1995, 181(5) 1597-601.
52. Dessen, A.; Lawrence, C. M.; Cupo, S.; Zaller, D. M.; Wiley, D. C., X-ray crystal s tructure of HLA-DR4 (DRA*0101, DRB1*0401) complexed with a peptide from human collagen II. Immunity 1997, 7(4) 473-481.
53. Hammer, J.; Gallazzi, F.; Bono, E.; Karr, R. W.; Guenot, J.; Valsasnini, P.; Nagy, Z. A.; Sinigaglia, F., Peptide binding specificity of HLADR4 molecules: correlation with rheumatoid arthritis association. J. Exp. Med. 1995, 181(5) 1847-1855.
54. Hill, J. A.; Southwood, S.; Sette, A.; Jevnikar, A. M.; Bell, D. A.; Cairns, E., The conversion of arginine to citrulline allows for high-affinity peptide interaction with the rheumatoid arthritis associated HLA-DRB1P0401 MHC Class II molecule. J. Immunol. 2003, 171(2) 538-541.
55. Hill, J. A.; Bell, D. A.; Brintnell, W.; Yue, D.; Wehrli, B.; Jevnikar, A. M.; Lee, D. M.; Hueber, W.; Robinson, W. H.; Cairns, E., Arthritis induced by posttranslationally (citrullinated) fibrinogen in DR4-IE transgenic mice. J. Exp. Med. 2003, 205(4) 967-979.
56. van der Helm-van Mil, A. H.; Verpoort, K. N.; Breedveld, F. C.; Huizinga, T. W.; Toes, R. E.; de Vries, R. R., The HLA-DRB1 shared epitope alleles are primarily a risk factor for anti-cyclic citrullinated peptide antibodies and are not an independent risk factor for development of rheumatoid arthritis. Arthritis Rheum. 2006, 54(4) 1117-1121.
57. Bennett, C. L.; Chakraverty, R., Dendritic cells in tissues: in situ stimulation of immunity and immunopathology. Trends Immunol. 2012, 33(1) 8-13.
58. Matzinger, P., An innate sense of danger. Ann. NY Acad. Sci. 2002, 961, 341-342.
59. Sallusto, F.; Cella, M.; Danieli, C.; Lanzavecchia, A., Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: Downregulation by cytokines and bacterial products. J. Exp. Med. 1995, 182(2) 389-400.
60. Sánchez-Sánchez, N.; Riol-Blanco, L.; Rodríguez-Fernández, J. L., The multiple personalities of the chemokine receptor CCR7 in dendritic cells. J. Immunol. 2006, 176(9) 5153-5159.
61. Delgado-Martín, C.; Escribano, C.; Pablos, J. L.; Riol-Blanco, L.; Rodríguez-Fernández, J. L., Chemokine CXCL12 uses CXCR4 and a signaling core formed by bifunctional Akt, extracellular signal-regulated kinase (ERK)1/2, and mammalian target of rapamycin complex 1 (mTORC1) proteins to control chemotaxis and survival simultaneously in mature dendritic cells. J. Biol. Chem. 2011, 286(43) 37222-37236.
62. L.; Delgado-Martín, C.; Sánchez-Sánchez, N.; Alonso -C. L. M.; Gutiérrez-López, M. D.; Del Hoyo, G. M.; Navarro, J.; Sánchez-Madrid, F.; Cabañas, C.; Sánchez-Mateos, P.; Rodríguez-Fernández, J. L., Immunological synapse formation inhibits, via NF-kappaB and FOXO1, the apoptosis of dendritic cells. Nature Immunol. 2009, 10(7) 753-760.
63. Rodríguez-Fernández, J. L.; Riol-Blanco, L.; Delgado-Martín, C., What is an immunological synapse?. Microbes Infect. 2010, 12(6) 438-445.
64. Rodríguez-Fernández, J. L.; Riol-Blanco, L.; Delgado-Martín, C., What is the function of the dendritic cell side of the immunological synapse?. Sci. Signal. 2010, 3(105) re2.
65. Thomas, R.; Quinn, C., Functional differentiation of dendritic cells in rheumatoid arthritis: role of CD86 in the synovium. J Immunol. 1996, 156(8) 3074-3086.
66. Lebre, M. C.; Jongbloed, S. L.; Tas, S. W.; Smeets, T. J.; McInnes, I. B.; Tak, P. P., Rheumatoid arthritis synovium contains two subsets of CD83-DC-LAMP-dendritic cells with distinct cytokine profiles. Am J Pathol. 2008, 172(4) 940-950.
67. Thomas, R.; Davis, L. S.; Lipsky, P. E., Rheumatoid synovium is enriched in mature antigen-presenting cells. J. Immunol. 1994, 152(5) 2613-2623.
68. Summers, K. L.; Daniel, P.; O'Donnell, J. L.; Hart, D. N. J., Dendritic cells in synovial fluid of chronic inflammatory arthritis lack CD80 surface expression. Clin Exp Immunol 1995, 100(1) 81-89.
69. Summers, K. L.; O'Donnell, J. L.; Williams, L. A.; Hart, D. N. J., Expression and function of CD80 and CD86 costimulator molecules on synovial dendritic cells in chronic arthritis. Arthritis Rheum. 1996, 39(8) 1287-1291.
70. Haringman, J. J.; Ludikhuize, J.; Tak, P. P., Chemokines in joint disease: the key to inflammation?. Ann Rheum Dis. 2004, 63(10) 1186-1194.
71. Pettit, A. R.; Thomas, R., Dendritic cells: the driving force behind autoimmunity in rheumatoid arthritis?. Immunol Cell Biol 1999, 77(5) 420-427.
72. Leung, B. P.; Conacher, M.; Hunter, D.; McInnes, I. B.; Liew, F. Y.; Brewer, J. M., A novel dendritic cell-induced model of erosive inflammatory arthritis: distinct roles for dendritic cells in T cell activation and induction of local inflammation. J Immunol. 2002, 169(12) 7071-7077.
73. Tsark, E. C.; Wang, W.; Teng, Y. C.; Arkfeld, D. G.; Dodge, G. R.; Kovats, S., Differential MHC class II-mediated presentation of rheumatoid arthritis autoantigens by human dendritic cells and macrophages. J. Immunol. 2002, 169(11) 6625-6633.
74. Thomas, R.; MacDonald, K. P. A.; Pettit, A. R.; Cavanagh, L. L.; Padmanabha, J.; Zehntner, S., Dendritic cells and the pathogenesis of rheumatoid arthritis. J. Leukoc. Biol. 1999, 66(2) 286-292.
75. MacDonald KPA; Nishioka, N.; Lipky, P. E.; Thomas, R., Functional CD40-ligand is expressed by T cells in rheumatoid arthritis J. Clin. Invest. 1997, 100(9) 2404-2414.
76. Randen, I.; Mellbye, O. J.; Forre, O.; Natvig, J. B., The identification of germinal centres and follicular dendritic cell networks in rheumatoid synovial tissue. Scand J Immunol 1995, 41(5) 481-486.
77. Thomas, R.; Lipsky, P. E., Could endogenous self-peptides presented by dendritic cells initiate rheumatoid arthritis?. Immunol. Today 1996, 17(12) 559-564.
78. Page, G.; Lebecque, S.; Miossec, P., Anatomic localization of immature and mature dendritic cells in an ectopic lymphoid organ: correlation with selective chemokine expression in rheumatoid synovium. J Immunol 2000, 168(10) 5333-5341.
79. Takemura, S.; Braun, A.; Crowson, C.; Kurtin, P. J.; Cofield, R. H.; O'Fallon, W. M.; Goronzy, J. J.; Weyand, C. M., Lymphoid neogenesis in rheumatoid synovitis. J Immunol. 2001, 167(2) 1072-1080
80. Weyand, C. M.; Goronzy, J. J., Ectopic germinal center formation in rheumatoid synovitis. Ann N Y Acad Sci 2003, 987, 140-149.
81. Wengner, A. M.; Höpken, U. E.; Petrow, P. K.; Hartmann, S.; Schurigt, U.; Bräuer, R.; Lipp, M., CXCR5-and CCR7-dependent lymphoid neogenesis in a murine model of chronic antigen-induced arthritis. Arthritis Rheum. 2007, 56(10) 3271-3283.
82. Taneja, V.; David, C. S., Role of HLA clas II genes in susceptibility/ resistance to inflammatory arthritis: studies with humanized mice. Immunology Reviews 2009, 233(1) 62-78.
83. Rose, H. M.; Ragan, C., Differential agglutination of normal and sensitized sheep erythrocytes by sera of patients with rheumatoid arthritis. Proc Soc. Exper. Biol Med 1948, 68(1) 1-6.
84. Crotty, S., Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 2011, 29, 621-663.
85. Yanaba, K.; Hamaguchi, Y.; Venturi, G. M.; Steeber, D. A.; St Clair, E. W.; Tedder, T. F., B cell depletion delays collageninduced arthritis in mice: arthritis induction requires synergy between humoral and cell-mediated immunity. J. Immunol. 2007, 179(2) 1369-1380.
86. Taneja, V.; Krco, C. J.; Behrens, M. D.; Luthra, H. S.; Griffiths, M. M.; David, C. S., B cells are important as antigen presenting cells for induction of MHC-restricted arthritis in transgenic mice. Mol Immunol. 2007, 44(11) 2988-2996.
87. Wooley, P. H.; Luthra, H. S.; Singh, S. K.; Huse, A. R.; Stuart, J. M.; David, C. S., Passive transfer of arthritis to mice by injection of human anti-type II collagen antibody. Mayo Clin. Proc. 1984, 59(11) 737-743.
88. Kavanaugh, A. F.; Nichols, L. A.; Lipsky, P. E., Treatment of refractory rheumatoid arthritis with an anti-CD54 (intercellular adhesion molecule-1, ICAM-1) monoclonal antibody. Arthr. Rheumatism. 1992, 37(7), 992-999.
89. Durie, F. H.; Fava, R. A.; Foy, T. M.; Aruffo, A.; Ledbetter, J. A.; Noelle, R. J., Preventio of collagen-induced arthritis with an antibody to gp39, the ligand of CD40. Science 1993, 261(5126) 1328-1330.
90. Barney-Knoerzer, D.; Karr, R. W.; Schwartz, B. D.; Mengle-Gaw, L. J., Collagen induce arthritis in the BB rat: prevention of disease by treatment with CTLA4-Ig. J. Clin. Invest. 1995, 96(2) 987-993.
91. Bullard, D. C.; Hurley, L. A.; Lorenzo, I.; Sly, L. M.; Beaudet, A. L.; Staite, N. D., Reduced susceptibility to collagen-induced arthritis in mice deficient in intercellular adhesion molecule-1. J. Immunol. 1996, 157(7) 3153-3158.
92. Hahn, M.; Nicholson, M. J.; Pyrdol, J.; Wucherpfennig, K. W., Unconventional topology of self peptide-major histocompatibility complex binding by a human autoimmune T cell receptor. Nature Immunol. 2005, 6(5) 490-496.
93. Nicholson, M. J.; Hahn, M.; Wucherpfennig, K. W., Unusual features of self-peptide/MHC binding by autoimmune T cell receptors. Immunity 2005, 23(4) 351-360.
94. Reinherz, E. L.; Tan, K.; Tang, L.; Kern, P.; Liu, J.; Xiong, Y.; Hussey, R. E.; Smolyar, A.; Hare, B.; Zhang, R.; Joachimiak, A.; Chang, H. C.; Wagner, G.; Wang, J., The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 1999, 286(5445) 1913-1921.
95. van der Merwe, P. A.; Davis, S. J., Molecular interactions mediating T cell antigen recognition Annu. Rev. Immunol. 2003, 21, 659-684.
96. Deng, L.; Mariuzza, R. A., Recognition of self-peptide-MHC complexes by autoimmune T-cell receptors. Trends Biochem Sci 2007, 32(11) 500-508.
97. Bridgeman, J. S.; Sewell, A. K.; Miles, J. J.; Price, D. A.; Cole, D. K., Structural and biophysical determinants of alphabeta T-cell antigen recognition. Immunology 2011, 135(1) 9-18.
98. Schubert, D. A.; Gordo, S.; Sabatino Jr., J. J.; Vadhana, S.; Gagnon, E.; Sethi, D. K.; Seth, N. P.; Choudhuri, K.; Reijonen, H.; Nepom, G. T.; Evavold, B. D.; Dustin, M. L.; Wucherpfenning, K. W., Self-reactive CD4 T cell clones form unusual immunological synapses. J. Exp. Med. 2012, 209(2) 335-352.
99. Weyand, C. M.; Goronzy, J. J., Pathomechanisms in rheumatoid arthritis--time for a string theory? J. Clin. Invest. 2006, 116(4) 869-871.