Autoimmune disease in Lyn-deficient mice is dependent on an inflammatory environment established by IL-6

Journal of Immunology

Volumn 184, Issue 3, 2010, Pages 1348-1360

  Tsantikos, Evelyn ^a,b   Oracki, Sarah A ^b   Quilici, Cathy ^a   Anderson, Gary P ^b   Tarlinton, David M ^b   Hibbs, Margaret L ^a  

^a ROYAL MELBOURNE HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; PROTEIN KINASE LYN; AUTACOID; AUTOANTIBODY; LYN PROTEIN-TYROSINE KINASE; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL EXPANSION; CELL LINEAGE; CELL MATURATION; CELL THERAPY; COMPREHENSION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENVIRONMENT; ENZYME DEFICIENCY; EXTRAMEDULLARY HEMATOPOIESIS; GENE DELETION; IMMUNOCOMPETENT CELL; INFLAMMATORY DISEASE; LEUKOCYTE; MOUSE; MYELOPOIESIS; NONHUMAN; PHENOTYPE; PLASMA CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; SPLENOMEGALY; T LYMPHOCYTE ACTIVATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DISEASE COURSE; DRUG ANTAGONISM; ENZYMOLOGY; GENE REARRANGEMENT; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE;

ANIMALS; AUTOANTIBODIES; B-LYMPHOCYTES; DISEASE PROGRESSION; IMMUNOGLOBULIN CLASS SWITCHING; INFLAMMATION MEDIATORS; INTERLEUKIN-6; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MYELOPOIESIS; SPLENOMEGALY; SRC-FAMILY KINASES; T-LYMPHOCYTES;

EID: 77949322552     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901878     Document Type: Article

References (73)

1. Bach, J. F. 2005. A Toll-like trigger for autoimmune disease. Nat. Med. 11: 120-121.
2. Lang, K. S., M. Recher, T. Junt, A. A. Navarini, N. L. Harris, S. Freigang, B. Odermatt, C. Conrad, L. M. Ittner, S. Bauer, et al. 2005. Toll-like receptor engagement converts T-cell autoreactivity into overt autoimmune disease. Nat. Med. 11: 138-145.
3. Crow, M. K., and K. A. Kirou. 2004. Interferon-a in systemic lupus erythematosus. Curr. Opin. Rheumatol. 16: 541-547.
4. Bach, J. F. 2005. Infections and autoimmune diseases. J. Autoimmun. 25(Suppl): 74-80.
5. Dale, J. B., and E. H. Beachey. 1985. Epitopes of streptococcal M proteins shared with cardiac myosin. J. Exp. Med. 162: 583-591.
6. Fujinami, R. S., and M. B. Oldstone. 1985. Amino acid homology between the encephalitogenic site of myelin basic protein and virus: mechanism for autoimmunity. Science 230: 1043-1045.
7. Oldstone, M. B. 1998. Molecular mimicry and immune-mediated diseases. FASEB J. 12: 1255-1265.
8. Fujinami, R. S., M. G. von Herrath, U. Christen, and J. L. Whitton. 2006. Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin. Microbiol. Rev. 19: 80-94.
9. McCoy, L., I. Tsunoda, and R. S. Fujinami. 2006. Multiple sclerosis and virus induced immune responses: autoimmunity can be primed by molecular mimicry and augmented by bystander activation. Autoimmunity 39: 9-19. (Pubitemid 43878516)
10. Miller, S. D., C. L. Vanderlugt, W. S. Begolka, W. Pao, R. L. Yauch, K. L. Neville, Y. Katz-Levy, A. Carrizosa, and B. S. Kim. 1997. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat. Med. 3: 1133-1136.
11. Horwitz, M. S., L. M. Bradley, J. Harbertson, T. Krahl, J. Lee, and N. Sarvetnick. 1998. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat. Med. 4: 781-785.
12. Goodnow, C. C., J. G. Cyster, S. B. Hartley, S. E. Bell, M. P. Cooke, J. I. Healy, S. Akkaraju, J. C. Rathmell, S. L. Pogue, and K. P. Shokat. 1995. Self-tolerance checkpoints in B lymphocyte development. Adv. Immunol. 59: 279-368.
13. Tsubata, T. 2005. B cell abnormality and autoimmune disorders. Autoimmunity 38: 331-337.
14. Kono, D. H., and A. N. Theofilopoulos. 2006. Genetics of SLE in mice. Springer Semin. Immunopathol. 28: 83-96.
15. Hibbs, M. L., D. M. Tarlinton, J. Armes, D. Grail, G. Hodgson, R. Maglitto, S. A. Stacker, and A. R. Dunn. 1995. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 83: 301-311.
16. Nishizumi, H., I. Taniuchi, Y. Yamanashi, D. Kitamura, D. Ilic, S. Mori, T. Watanabe, and T. Yamamoto. 1995. Impaired proliferation of peripheral B cells and indication of autoimmune disease in lyn-deficient mice. Immunity 3: 549-560.
17. Chan, V. W., F. Meng, P. Soriano, A. L. DeFranco, and C. A. Lowell. 1997. Characterization of the B lymphocyte populations in Lyn-deficient mice and the role of Lyn in signal initiation and down-regulation. Immunity 7: 69-81.
18. Chan, V. W., C. A. Lowell, and A. L. DeFranco. 1998. Defective negative regulation of antigen receptor signaling in Lyn-deficient B lymphocytes. Curr. Biol. 8: 545-553.
19. Cornall, R. J., J. G. Cyster, M. L. Hibbs, A. R. Dunn, K. L. Otipoby, E. A. Clark, and C. C. Goodnow. 1998. Polygenic autoimmune traits: Lyn, CD22, and SHP-1 are limiting elements of a biochemical pathway regulating BCR signaling and selection. Immunity 8: 497-508.
20. Nishizumi, H., K. Horikawa, I. Mlinaric-Rascan, and T. Yamamoto. 1998. A double-edged kinase Lyn: a positive and negative regulator for antigen receptor-mediated signals. J. Exp. Med. 187: 1343-1348.
21. Smith, K. G., D. M. Tarlinton, G. M. Doody, M. L. Hibbs, and D. T. Fearon. 1998. Inhibition of the B cell by CD22: a requirement for Lyn. J. Exp. Med. 187: 807-811.
22. Xu, Y., K. W. Harder, N. D. Huntington, M. L. Hibbs, and D. M. Tarlinton. 2005. Lyn tyrosine kinase: accentuating the positive and the negative.Immunity 22: 9-18.
23. Harder, K. W., C. Quilici, E. Naik, M. Inglese, N. Kountouri, A. Turner, K. Zlatic, D. M. Tarlinton, and M. L. Hibbs. 2004. Perturbed myelo/erythropoiesis in Lyn-deficient mice is similar to that in mice lacking the inhibitory phosphatases SHP-1 and SHIP-1. Blood 104: 3901-3910.
24. Satterthwaite, A. B., C. A. Lowell, W. N. Khan, P. Sideras, F. W. Alt, and O. N. Witte. 1998. Independent and opposing roles for Btk and lyn in B and myeloid signaling pathways. J. Exp. Med. 188: 833-844.
25. Takeshita, H., I. Taniuchi, J. Kato, and T. Watanabe. 1998. Abrogation of autoimmune disease in Lyn-deficient mice by the mutation of the Btk gene. Int. Immunol. 10: 435-444.
26. Hasegawa, M., M. Fujimoto, J. C. Poe, D. A. Steeber, C. A. Lowell, and T. F. Tedder. 2001. A CD19-dependent signaling pathway regulates autoimmunity in Lyn-deficient mice. J. Immunol. 167: 2469-2478. (Pubitemid 32768872)
27. Silver, K. L., T. L. Crockford, T. Bouriez-Jones, S. Milling, T. Lambe, and R. J. Cornall. 2007. MyD88-dependent autoimmune disease in Lyn-deficient mice. Eur. J. Immunol. 37: 2734-2743.
28. Beavitt, S. J., K. W. Harder, J. M. Kemp, J. Jones, C. Quilici, F. Casagranda, E. Lam, D. Turner, S. Brennan, P. D. Sly, et al. 2005. Lyn-deficient mice develop severe, persistent asthma: Lyn is a critical negative regulator of Th2 immunity. J. Immunol. 175: 1867-1875.
29. Chu, C. L., and C. A. Lowell. 2005. The Lyn tyrosine kinase differentially regulates dendritic cell generation and maturation. J. Immunol. 175: 2880-2889.
30. Kopf, M., H. Baumann, G. Freer, M. Freudenberg, M. Lamers, T. Kishimoto, R. Zinkernagel, H. Bluethmann, and G. Köhler. 1994. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368: 339-342. (Pubitemid 24104268)
31. Kitamura, D., and K. Rajewsky. 1992. Targeted disruption of m chain membrane exon causes loss of heavy-chain allelic exclusion. Nature 356: 154-156.
32. Harder, K. W., L. M. Parsons, J. Armes, N. Evans, N. Kountouri, R. Clark, C. Quilici, D. Grail, G. S. Hodgson, A. R. Dunn, and M. L. Hibbs. 2001. Gain-and loss-of-function Lyn mutant mice define a critical inhibitory role for Lyn in the myeloid lineage. Immunity 15: 603-615.
33. Meade, J., C. Fernandez, and M. Turner. 2002. The tyrosine kinase Lyn is required for B cell development beyond the T1 stage in the spleen: rescue by overexpression of Bcl-2. Eur. J. Immunol. 32: 1029-1034.
34. Yamanashi, Y., S. Mori, M. Yoshida, T. Kishimoto, K. Inoue, T. Yamamoto, and K. Toyoshima. 1989. Selective expression of a protein-tyrosine kinase, p56lyn, in hematopoietic cells and association with production of human T-cell lymphotropic virus type I. Proc. Natl. Acad. Sci. USA 86: 6538-6542.
35. Flores-Borja, F., P. S. Kabouridis, E. C. Jury, D. A. Isenberg, and R. A. Mageed. 2005. Decreased Lyn expression and translocation to lipid raft signaling domains in B lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum. 52: 3955-3965.
36. Gabay, C., P. Roux-Lombard, P. de Moerloose, J. M. Dayer, T. Vischer, and P. A. Guerne. 1993. Absence of correlation between interleukin 6 and C-reactive protein blood levels in systemic lupus erythematosus compared with rheumatoid arthritis. J. Rheumatol. 20: 815-821. (Pubitemid 23158475)
37. Nagafuchi, H., N. Suzuki, Y. Mizushima, and T. Sakane. 1993. Constitutive expression of IL-6 receptors and their role in the excessive B cell function in patients with systemic lupus erythematosus. J. Immunol. 151: 6525-6534. (Pubitemid 23340399)
38. Alonzi, T., E. Fattori, D. Lazzaro, P. Costa, L. Probert, G. Kollias, F. De Benedetti, V. Poli, and G. Ciliberto. 1998. Interleukin 6 is required for the development of collagen-induced arthritis. J. Exp. Med. 187: 461-468.
39. Gabay, C. 2006. Interleukin-6 and chronic inflammation. Arthritis Res. Ther. 8 (Suppl 2): S3.
40. Kopf, M., A. Ramsay, F. Brombacher, H. Baumann, G. Freer, C. Galanos, J. C. Gutierrez-Ramos, and G. Köhler. 1995. Pleiotropic defects of IL-6-deficient mice including early hematopoiesis, T and B cell function, and acute phase responses. Ann. N. Y. Acad. Sci. 762: 308-318.
41. Markine-Goriaynoff, D., T. D. Nguyen, G. Bigaignon, J. Van Snick, and J. P. Coutelier. 2001. Distinct requirements for IL-6 in polyclonal and specific Ig production induced by microorganisms. Int. Immunol. 13: 1185-1192.
42. Uchiumi, F., K. Semba, Y. Yamanashi, J. Fujisawa, M. Yoshida, K. Inoue, K. Toyoshima, and T. Yamamoto. 1992. Characterization of the promoter region of the src family gene lyn and its trans activation by human T-cell leukemia virus type I-encoded p40tax. Mol. Cell. Biol. 12: 3784-3795.
43. Kishimoto, T. 2006. Interleukin-6: discovery of a pleiotropic cytokine. Arthritis Res. Ther. 8(Suppl 2): S2.
44. Fattori, E., M. Cappelletti, P. Costa, C. Sellitto, L. Cantoni, M. Carelli, R. Faggioni, G. Fantuzzi, P. Ghezzi, and V. Poli. 1994. Defective inflammatory response in interleukin 6-deficient mice. J. Exp. Med. 180: 1243-1250.
45. Fattori, E., C. Della Rocca, P. Costa, M. Giorgio, B. Dente, L. Pozzi, and G. Ciliberto. 1994. Development of progressive kidney damage and myeloma kidney in interleukin-6 transgenic mice. Blood 83: 2570-2579. (Pubitemid 24135849)
46. Linker-Israeli, M., R. J. Deans, D. J. Wallace, J. Prehn, T. Ozeri-Chen, and J. R. Klinenberg. 1991. Elevated levels of endogenous IL-6 in systemic lupus erythematosus. A putative role in pathogenesis. J. Immunol. 147: 117-123.
47. Kitani, A., M. Hara, T. Hirose, M. Harigai, K. Suzuki, M. Kawakami, Y. Kawaguchi, T. Hidaka, M. Kawagoe, and H. Nakamura. 1992. Autostimulatory effects of IL-6 on excessive B cell differentiation in patients with systemic lupus erythematosus: analysis of IL-6 production and IL-6R expression. Clin. Exp. Immunol. 88: 75-83.
48. Stuart, R. A., A. J. Littlewood, P. J. Maddison, and N. D. Hall. 1995. Elevated serum interleukin-6 levels associated with active disease in systemic connective tissue disorders. Clin. Exp. Rheumatol. 13: 17-22.
49. Cross, J. T., and H. P. Benton. 1999. The roles of interleukin-6 and interleukin-10 in B cell hyperactivity in systemic lupus erythematosus. Inflamm. Res. 48: 255-261.
50. Finck, B. K., B. Chan, and D. Wofsy. 1994. Interleukin 6 promotes murine lupus in NZB/NZW F1 mice. J. Clin. Invest. 94: 585-591.
51. Mihara, M., N. Takagi, Y. Takeda, and Y. Ohsugi. 1998. IL-6 receptor blockage inhibits the onset of autoimmune kidney disease in NZB/W F1 mice. Clin. Exp. Immunol. 112: 397-402.
52. Liang, B., D. B. Gardner, D. E. Griswold, P. J. Bugelski, and X. Y. Song. 2006. Anti-interleukin-6 monoclonal antibody inhibits autoimmune responses in a murine model of systemic lupus erythematosus. Immunology 119: 296-305. (Pubitemid 44571047)
53. Nishimoto, N., K. Yoshizaki, K. Maeda, T. Kuritani, H. Deguchi, B. Sato, N. Imai, M. Suemura, T. Kakehi, N. Takagi, and T. Kishimoto. 2003. Toxicity, pharmacokinetics, and dose-finding study of repetitive treatment with the humanized anti-interleukin 6 receptor antibody MRA in rheumatoid arthritis. Phase I/II clinical study. J. Rheumatol. 30: 1426-1435.
54. Nishimoto, N., K. Yoshizaki, N. Miyasaka, K. Yamamoto, S. Kawai, T. Takeuchi, J. Hashimoto, J.Azuma, and T. Kishimoto. 2004. Treatment of rheumatoid arthritis with humanized anti-interleukin-6 receptor antibody: a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum. 50: 1761-1769. (Pubitemid 38725087)
55. Woo, P., N. Wilkinson, A. M. Prieur, T. Southwood, V. Leone, P. Livermore, H. Wythe, D. Thomson, and T. Kishimoto. 2005. Open label phase II trial of single, ascending doses of MRA in Caucasian children with severe systemic juvenile idiopathic arthritis: proof of principle of the efficacy of IL-6 receptor blockade in this type of arthritis and demonstration of prolonged clinical improvement. Arthritis Res. Ther. 7: R1281-R1288.
56. Edwards, J. C., L. Szczepanski, J. Szechinski, A. Filipowicz-Sosnowska, P. Emery, D. R. Close, R. M. Stevens, and T. Shaw. 2004. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350: 2572-2581.
57. Emery, P., R. Fleischmann, A. Filipowicz-Sosnowska, J. Schechtman, L. Szczepanski, A. Kavanaugh, A. J. Racewicz, R. F. van Vollenhoven, N. F. Li, S. Agarwal, et al; DANCER Study Group. 2006. The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, dose-ranging trial. Arthritis Rheum. 54: 1390-1400.
58. Cohen, S. B., P. Emery, M. W. Greenwald, M. Dougados, R. A. Furie, M. C. Genovese, E. C. Keystone, J. E. Loveless, G. R. Burmester, M. W. Cravets, et al; REFLEX Trial Group. 2006. Rituximab for rheumatoid arthritis refractory to anti-tumor necrosis factor therapy: Results of a multicenter, randomized, double-blind, placebo-controlled, phase III trial evaluating primary efficacy and safety at twenty-four weeks. Arthritis Rheum. 54: 2793-2806.
59. Looney, R. J., J. H. Anolik, D. Campbell, R. E. Felgar, F. Young, L. J. Arend, J. A. Sloand, J. Rosenblatt, and I. Sanz. 2004. B cell depletion as a novel treatment for systemic lupus erythematosus: a phase I/II dose-escalation trial of rituximab. Arthritis Rheum. 50: 2580-2589.
60. Leandro, M. J., G. Cambridge, J. C. Edwards, M. R. Ehrenstein, and D. A. Isenberg. 2005. B-cell depletion in the treatment of patients with systemic lupus erythematosus: a longitudinal analysis of 24 patients. Rheumatology (Oxford) 44: 1542-1545. (Pubitemid 41742472)
61. Smith, K. G., R. B. Jones, S. M. Burns, and D. R. Jayne. 2006. Long-term comparison of rituximab treatment for refractory systemic lupus erythematosus and vasculitis: Remission, relapse, and re-treatment. Arthritis Rheum. 54: 2970-2982.
62. 2008. Genentech and Biogen Idec: Phase II/III Study Of Rituxan Fails To Meet Endpoints. FierceBiotech.
63. Hawley, R. G., A. Z. Fong, B. F. Burns, and T. S. Hawley. 1992. Transplantable myeloproliferative disease induced in mice by an interleukin 6 retrovirus. J. Exp. Med. 176: 1149-1163.
64. Ikebuchi, K., G. G. Wong, S. C. Clark, J. N. Ihle, Y. Hirai, and M. Ogawa. 1987. Interleukin 6 enhancement of interleukin 3-dependent proliferation of multipotential hemopoietic progenitors. Proc. Natl. Acad. Sci. USA 84: 9035-9039.
65. Tsuji, K., S. D. Lyman, T. Sudo, S. C. Clark, and M. Ogawa. 1992. Enhancement of murine hematopoiesis by synergistic interactions between steel factor (ligand for c-kit), interleukin-11, and other early acting factors in culture. Blood 79: 2855-2860.
66. Walker, F., H. H. Zhang, V. Matthews, J. Weinstock, E. C. Nice, M. Ernst, S. Rose-John, and A. W. Burgess. 2008. IL6/sIL6R complex contributes to emergency granulopoietic responses in G-CSF- and GM-CSF-deficient mice. Blood 111: 3978-3985.
67. Bernad, A., M. Kopf, R. Kulbacki, N. Weich, G. Koehler, and J. C. Gutierrez-Ramos. 1994. Interleukin-6 is required in vivo for the regulation of stem cells and committed progenitors of the hematopoietic system. Immunity 1: 725-731.
68. Urashima, M., D. Chauhan, M. Hatziyanni, A. Ogata, D. Hollenbaugh, A. Aruffo, and K. C. Anderson. 1996. CD40 ligand triggers interleukin-6 mediated B cell differentiation. Leuk. Res. 20: 507-515.
69. Hilbert, D. M., M. P. Cancro, P. A. Scherle, R. P. Nordan, J. Van Snick, W. Gerhard, and S. Rudikoff. 1989. T cell derived IL-6 is differentially required for antigen-specific antibody secretion by primary and secondary B cells. J. Immunol. 143: 4019-4024.
70. Bergui, L., M. Schena, G. Gaidano, M. Riva, and F. Caligaris-Cappio. 1989. Interleukin 3 and interleukin 6 synergistically promote the proliferation and differentiation of malignant plasma cell precursors in multiple myeloma. J. Exp. Med. 170: 613-618.
71. Kopf, M., S. Herren, M. V. Wiles, M. B. Pepys, and M. H. Kosco-Vilbois. 1998. Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component. J. Exp. Med. 188: 1895-1906.
72. Nurieva, R. I., Y. Chung, D. Hwang, X. O. Yang, H. S. Kang, L. Ma, Y. H. Wang, S. S. Watowich, A. M. Jetten, Q. Tian, and C. Dong. 2008. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29: 138-149.
73. Hsu, H. C., P. Yang, J. Wang, Q. Wu, R. Myers, J. Chen, J. Yi, T. Guentert, A. Tousson, A. L. Stanus, et al. 2008. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat. Immunol. 9: 166-175.