NKT cell-derived urokinase-type plasminogen activator promotes peripheral tolerance associated with eye

Journal of Immunology

Volumn 179, Issue 4, 2007, Pages 2215-2222

  Sonoda, Koh Hei ^a,b   Nakamura, Takahiko ^b   Young, Howard A ^c   Hart, David ^d   Carmeliet, Peter ^e   Stein Streilein, Joan ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b KYUSHU UNIVERSITY   (Japan)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF CALGARY   (Canada)

^e UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; INTERLEUKIN 10; PLASMIN; T LYMPHOCYTE RECEPTOR; UROKINASE; CD1 ANTIGEN; CELL SURFACE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; PLASMINOGEN; PLASMINOGEN ACTIVATOR, UROKINASE RECEPTORS; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR EYE CHAMBER; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DELAYED HYPERSENSITIVITY; ENZYME DEFICIENCY; FEMALE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE; ANIMAL; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MOUSE MUTANT; NATURAL KILLER CELL; SPLEEN;

ADOPTIVE TRANSFER; ANIMALS; ANTERIOR CHAMBER; ANTIGENS, CD1; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; IMMUNE TOLERANCE; INTERLEUKIN-10; KILLER CELLS, NATURAL; MICE; MICE, KNOCKOUT; PLASMIN; PLASMINOGEN; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, CELL SURFACE; SPLEEN; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA; URINARY PLASMINOGEN ACTIVATOR;

EID: 34848881592     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.4.2215     Document Type: Article

References (58)

1. Streilein, J. W. 1993. Immune privilege as the result of local tissue barriers and immunosuppressive microenvironments. Curr. Opin. Immunol. 5: 428-432.
2. Griffith, T. S., T. Brunner, S. M. Fletcher, D. R. Green, and T. A. Ferguson. 1995. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science 270: 1189-1192.
3. Taylor, A. W., J. W. Streilein, and S. W. Cousins. 1994. Immunoreactive vasoactive intestinal peptide contributes to the immunosuppressive activity of normal aqueous humor. J. Immunol. 153: 1080-1086.
4. Streilein, J. W. 2003. Ocular immune privilege: therapeutic opportunities from an experiment of nature. Nat. Rev. Immunol. 3: 878-889.
5. Streilein, J. W., and D. Bradley. 1991. Analysis of immunosuppressive properties of iris and ciliary body cells and their secretory products. Invest. Ophthalmol. Vis. Sci. 32: 2700-2710.
6. Wilbanks, G. A., and J. W. Streilein. 1990. Distinctive humoral immune responses following anterior chamber and intravenous administration of soluble antigen: evidence for active suppression of IgG2-secreting B lymphocytes. Immunology 71: 566-572.
7. Wilbanks, G. A., and J. W. Streilein. 1992. Macrophages capable of inducing anterior chamber associated immune deviation demonstrate spleen-seeking migratory properties. Reg. Immunol. 4: 130-137.
8. Streilein, J. W., and J. Y. Niederkorn. 1985. Characterization of the suppressor cell(s) responsible for anterior chamber-associated immune deviation (ACAID) induced in BALB/c mice by P815 cells. J. Immunol. 134: 1381-1387.
9. Katagiri, K., J. Zhang-Hoover, J. S. Mo, J. Stein-Streilein, and J. W. Streilein. 2002. Using tolerance induced via the anterior chamber of the eye to inhibit Th2-dependent pulmonary pathology. J. Immunol. 169: 84-89.
10. Zhang-Hoover, J., P. Finn, and J. Stein-Streilein. 2005. Modulation of ovalbumin-induced airway inflammation and hyperreactivity by tolerogenic APC. J. Immunol. 175: 7117-7124.
11. Sonoda, K.-H., M. Exley, S. Snapper, S. Balk, and J. Stein-Streilein. 1999. CD1 reactive NKT cells are required for development of systemic tolerance through an immune privileged site. J. Exp. Med. 190: 1215-1225.
12. Lin, H. H., D. E. Faunce, M. Stacey, A. Terajewicz, T. Nakamura, J. Zhang-Hoover, M. Kerley, M. L. Mucenski, S. Gordon, and J. Stein-Streilein. 2005. The macrophage F4/80 receptor is required for the induction of antigen-specific efferent regulatory T cells in peripheral tolerance. J. Exp. Med. 201: 1615-1625.
13. Wilbanks, G. A., and J. W. Streilein. 1991. Studies on the induction of anterior chamber-associated immune deviation (ACAID). 1. Evidence that an antigen-specific, ACAID-inducing, cell-associated signal exists in the peripheral blood. J. Immunol. 146: 2610-2617.
14. Wilbanks, G. A., and J. W. Streilein. 1990. Characterization of suppressor cells in anterior chamber-associated immune deviation (ACAID) induced by soluble antigen: evidence of two functionally and phenotypically distinct T-suppressor cell populations. Immunology 71: 383-389.
15. Keino, H., S. Masli, S. Sasaki, J. W. Streilein, and J. Stein-Streilein. 2006. CD8* T regulatory cells use a novel genetic program that includes CD103 to suppress Th1 immunity in eye-derived tolerance. Invest. Ophthalmol. Vis. Sci. 47: 1533-1543.
16. + T regulatory cells. Invest. Ophthalmol. Vis. Sci. 47: 1047-1055.
17. Bendelac, A., M. N. Rivera, S. H. Park, and J. H. Roark. 1997. Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu. Rev. Immunol. 15: 535-562.
18. Taniguchi, M., M. Harada, S. Koyo, T. Nakayama, and H. Wakao. 2003. The regulatory role of Va14 NKT cells in innate and acquired immune response. Annu. Rev. Immunol. 21: 483-513.
19. + T cell populations. Int. Immunol. 7: 1157-1161.
20. Cui, J., T. Shin, T. Kawano, H. Sato, E. Kondo, I. Toura, Y. Kaneko, H. Koseki, M. Kanno, and M. Taniguchi. 1997. Requirement for Va14 NKT cells in IL-12-mediated rejection of tumors. Science 278: 1623-1626.
21. + T cells. Eur. J. Immunol. 27: 1576-1579.
22. Exley, M. A., N. J. Bigley, O. Cheng, S. M. A. Tahir, S. T. Smiley, Q. L. Carter, H. F. Stils, M. J. Gusby, Y. Koezuka, M. Taniguchi, and S. P. Balk. 2001. CD1d-reactive T-cell activation leads to amelioration of disease caused by diabetogenic encephalomyocarditis virus. J. Leukocyte Biol. 69: 713-718.
23. + T lymphocytes. Science 268: 863-865.
24. + T cell development and early IL-4 production in CD1-deficient mice. Immunity 6: 459-467.
25. Mendiratta, S. K., W. D. Martin, S. Hong, A. Boesteanu, S. Joyce, and L. Van Kaer. 1997. CD1d1 mutant mice are deficient in natural T cells that promptly produce IL-4. Immunity 6: 469-477.
26. Smiley, S. T., M. H. Kaplan, and M. J. Grusby. 1997. Immunoglobulin E production in the absence of interleukin-4-secreting CD1-dependent cells. Science 275: 977-979.
27. Faunce, D. E., K.-H. Sonoda, and J. Stein-Streilein. 2001. MIP-2 recruits NKT cells to the spleen during tolerance induction. J. Immunol. 166: 313-321.
28. + T cells to the spleen during the generation of regulatory T cells in tolerance. J. Immunol. 169: 31-38.
29. D'Orazio, T. J., and J. Y. Niederkorn. 1998. Splenic B cells are required for tolerogenic antigen presentation in the induction of anterior chamber-associated immune deviation (ACAID). Immunology 95: 47-55.
30. Sonoda, K. H., and J. Stein-Streilein. 2002. CD1d on antigen-transporting APC and splenic marginal zone B cells promotes NKT cell-dependent tolerance. Eur. J. Immunol. 32: 848-857.
31. Sonoda, K.-H., D. E. Faunce, M. Taniguchi, M. Exley, S. Balk, and J. Stein-Streilein. 2001. NKT cell-derived IL-10 is essential for the differentiation of antigen-specific T regulatory cells in systemic tolerance. J. Immunol. 166: 42-50.
32. Saksela, O., and D. B. Rifkin. 1988. Cell-associated plasminogen activation: regulation and physiological functions. Annu. Rev. Cell Biol. 4: 93-126.
33. Mondino, A., and F. Blasi. 2004. uPA and uPAR in fibrinolysis, immunity and pathology. Trends Immunol. 25: 450-455.
34. Dano, K., P. A. Andreasen, J. Grondahl-Hansen, P. Kristensen, L. S. Nielsen, and L. Skriver. 1985. Plasminogen activators, tissue degradation, and cancer. Adv. Cancer Res. 44: 139-266.
35. Ny, T., X. R. Peng, and M. Ohlsson. 1993. Hormonal regulation of the fibrinolytic components in the ovary. Thromb. Res. 71: 1-45.
36. Romer, J., T. H. Bugge, C. Pyke, L. R. Lund, M. J. Flick, J. L. Degen, and K. Dano. 1996. Impaired wound healing in mice with a disrupted plasminogen gene. Nat. Med. 2: 287-292.
37. Pepper, M. S., A. P. Sappino, R. Stocklin, R. Montesano, L. Orci, and J. D. Vassalli. 1993. Upregulation of urokinase receptor expression on migrating endothelial cells. J. Cell Biol. 122: 673-684.
38. Dewerchin, M., A. V. Nuffelen, G. Wallays, A. Bouche, L. Moons, P. Carmeliet, R. C. Mulligan, and D. Collen. 1996. Generation and characterization of urokinase receptor-deficient mice. J. Clin. Invest. 97: 870-878.
39. Vassalli, J. D., A. P. Sappino, and D. Belin. 1991. The plasminogen activator/ plasmin system. J. Clin. Invest. 88: 1067-1072.
40. Plesner, T., M. Ploug, V. Ellis, E. Ronne, G. Hoyer-Hansen, M. Wittrup, T. L. Pedersen, T. Tscherning, K. Dano, and N. E. Hansen. 1994. The receptor for urokinase-type plasminogen activator and urokinase is translocated from two distinct intracellular compartments to the plasma membrane on stimulation of human neutrophils. Blood 83: 808-815.
41. Bianchi, E., E. Ferrero, F. Fazioli, F. Mangili, J. Wang, J. R. Bender, F. Blasi, and R. Pardi. 1996. Integrin-dependent induction of functional urokinase receptors in primary T lymphocytes. J. Clin. Invest. 98: 1133-1141.
42. Gyetko, M. R., G.-H. Chen, R. A. McDonald, R. Goodman, G. B. Huffnagle, C. C. Wilkinson, J. A. Fuller, and G. B. Toews. 1996. Urokinase is required for the pulmonary inflammatory response to Cryptococcus neoformans. J. Clin. Invest. 97: 1818-1826.
43. Chapman, H. A. 1997. Plasminogen activators, integrins, and the coordinated regulation of cell adhesion and migration. Curr. Opin. Cell Biol. 9: 714-724.
44. Lyons, R. M., L. E. Gentry, A. F. Purchio, and H. L. Moses. 1990. Mechanism of activation of latent recombinant transforming growth factor β1 by plasmin. J. Cell Biol. 110: 1361-1367.
45. Miyazono, K., A. Olofsson, P. Colosetti, and C. H. Heldin. 1991. A role of the latent TGF-β1-binding protein in the assembly and secretion of TGF-β1. EMBO J. 10: 1091-1101.
46. Bickerstaff, A. A., D. Xia, R. P. Pelletier, and C. G. Orosz. 2000. Mechanisms of graft acceptance: evidence that plasminogen activator controls donor-reactive delayed-type hypersensitivity responses in cardiac allograft acceptor mice. J. Immunol. 164: 5132-5139.
47. Chen, Y., V. K. Kuchroo, J.-I. Inobe, D. A. Hafler, and H. L. Weiner. 1994. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyeilits. Science 265: 1237-1240.
48. Wilbanks, G. A., M. Mammolenti, and J. W. Streilein. 1992. Studies on the induction of anterior chamber-associated immune deviation (ACAID). III. Induction of ACAID depends upon intraocular transforming growth factor-β. Eur. J. Immunol. 22: 165-173.
49. + T regulatory cells following antigen inoculation in an immune privileged site. J. Immunol. 171: 1266-1271.
50. Faunce, D. E., K. H. Sonoda, and J. Stein-Streilein. 2001. MIP-2 recruits NKT cells to the spleen during tolerance induction. J. Immunol. 166: 313-321.
51. Ashour, H. M., and J. Y. Niederkorn. 2006. Peripheral tolerance via the anterior chamber of the eye: role of B cells in MHC class I and II antigen presentation. J. Immunol. 176: 5950-5957.
52. Sonoda, K. H., and J. Stein-Streilein. 2002. CD1d on antigen-transporting APC and splenic marginal zone B cells promotes NKT cell-dependent tolerance. Eur. J. Immunol. 32: 848-857.
53. 2 integrins in vivo. J. Exp. Med. 188: 1029-1037.
54. Hara, Y., R. R. Caspi, B. Wiggert, C. C. Chan, G. A. Wilbanks, and J. W. Streilein. 1992. Suppression of experimental autoimmune uveitis in mice by induction of anterior chamber-associated immune deviation with interphotoreceptor retinoid-binding protein. J. Immunol. 148: 1685-1692.
55. Sumida, T., A. Sakamoto, H. Murata, Y. Makino, H. Takahashi, S. Yoshida, K. Nishioka, I. Iwamoto, and M. Taniguchi. 1995. Selective reduction of T cells bearing invariant Va24JaQ antigen receptor in patients with systemic sclerosis. J. Exp. Med. 182: 1163-1168.
56. Wilson, S. B., S. C. Kent, K. T. Patton, T. Orban, R. A. Jackson, M. Exley, S. Porcelli, D. A. Schatz, M. A. Atkinson, S. P. Balk, et al. 1998. Extreme Th1 bias of invariant Va24JaQ T cells in type 1 diabetes. [Published erratum appears in 1999 Nature 399: 84.] Nature 391: 177-181.
57. + T regulatory cells that can suppress ongoing experimental autoimmune encephalomyelitis. J. Immunol. 172: 1991-1995.
58. + T regulatory cells that modulate pulmonary interstitial fibrosis. J. Immunol. 172: 178-185.