Role of T cell TGFβ signaling and IL-17 in allograft acceptance and fibrosis associated with chronic rejection

Journal of Immunology

Volumn 183, Issue 11, 2009, Pages 7297-7306

  Faust, Susan M ^a   Lu, Guanyi ^a   Marini, Bernard L ^a   Zou, Weiping ^a   Gordon, David ^a   Iwakura, Yoichiro ^b,c   Laouar, Yasmina ^a   Bishop, D Keith ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND MONOCLONAL ANTIBODY; IMMUNOGLOBULIN G; INTERLEUKIN 17; OKT 4; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CHRONIC GRAFT REJECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; GRAFT RECIPIENT; GRAFT SURVIVAL; HEART GRAFT; HEART MUSCLE FIBROSIS; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T CELL DEPLETION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; ALLOTRANSPLANTATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CHRONIC DISEASE; FIBROSIS; FLOW CYTOMETRY; GENETICS; GRAFT REJECTION; HEART TRANSPLANTATION; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CHRONIC DISEASE; FIBROSIS; FLOW CYTOMETRY; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; HUMANS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-17; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION, HOMOLOGOUS;

EID: 73349094069     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902446     Document Type: Article

References (84)

1. Weiss, M. J., J. C. Madsen, B. R. Rosengard, and J. S. Allan. 2008. Mechanisms of chronic rejection in cardiothoracic transplantation. Front Biosci. 13: 2980-2988. (Pubitemid 351606109)
2. Waaga, A. M., M. Gasser, I. Laskowski, and N. L. Tilney. 2000. Mechanisms of chronic rejection. Curr. Opin. Immunol. 12: 517-521.
3. Mannon, R. B. 2006. Therapeutic targets in the treatment of allograft fibrosis. Am. J. Transplant. 6: 867-875. (Pubitemid 44356636)
4. Orosz, C. G., and R. P. Pelletier. 1997. Chronic remodeling pathology in grafts. Curr. Opin. Immunol. 9: 676-680.
5. Womer, K. L., J. P. Vella, and M. H. Sayegh. 2000. Chronic allograft dysfunction: mechanisms and new approaches to therapy. Semin. Nephrol. 20: 126-147.
6. Garrity, E. R., Jr., and M. R. Mehra. 2004. An update on clinical outcomes in heart and lung transplantation. Transplantation 77: S68-S74. (Pubitemid 38668462)
7. Li, M. O., Y. Y. Wan, S. Sanjabi, A. K. Robertson, and R. A. Flavell. 2006. Transforming growth factor-β regulation of immune responses. Annu. Rev. Immunol. 24: 99-146.
8. Shull, M. M., I. Ormsby, A. B. Kier, S. Pawlowski, R. J. Diebold, M. Yin, R. Allen, C. Sidman, G. Proetzel, D. Calvin, et al. 1992. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359: 693-699.
9. Kulkarni, A. B., and S. Karlsson. 1993. Transforming growth factor-β1 knockout mice: a mutation in one cytokine gene causes a dramatic inflammatory disease. Am. J. Pathol. 143: 3-9.
10. Gorelik, L., and R. A. Flavell. 2000. Abrogation of TGFβ signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12: 171-181. (Pubitemid 30398631)
11. Lucas, P. J., S. J. Kim, S. J. Melby, and R. E. Gress. 2000. Disruption of T cell homeostasis in mice expressing a T cell-specific dominant negative transforming growth factor βII receptor. J. Exp. Med. 191: 1187-1196.
12. Rubtsov, Y. P., and A. Y. Rudensky. 2007. TGFβ signalling in control of T-cell-mediated self-reactivity. Nat. Rev. Immunol. 7: 443-453.
13. + regulatory T cells is mediated by cell surface-bound transforming growth factor β. J. Exp. Med. 194: 629-644.
14. Levings, M. K., R. Bacchetta, U. Schulz, and M. G. Roncarolo. 2002. The role of IL-10 and TGFβ in the differentiation and effector function of T regulatory cells. Int. Arch. Allergy Immunol. 129: 263-276.
15. Wood, K. J., and S. Sakaguchi. 2003. Regulatory T cells in transplantation tolerance. Nat. Rev. Immunol. 3: 199-210.
16. Ming, J. E., K. L. Russell, D. M. McDonald-McGinn, and E. H. Zackai. 2005. Autoimmune disorders in Kabuki syndrome. Am. J. Med. Genet. A. 132A: 260-262.
17. + regulatory T cells confer infectious tolerance in a TGFβ-dependent manner. J. Exp. Med. 205: 1975-1981.
18. Marie, J. C., D. Liggitt, and A. Y. Rudensky. 2006. Cellular mechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factor-β receptor. Immunity 25: 441-454.
19. + regulatory T cells by TGFβ induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
20. H17 and regulatory T cells. Nature 441: 235-238.
21. H17 lineage. Nature 441: 231-234.
22. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189. (Pubitemid 43214587)
23. H17 cell differentiation by antagonizing RORγt function. Nature 453: 236-240.
24. Wilson, N. J., K. Boniface, J. R. Chan, B. S. McKenzie, W. M. Blumenschein, J. D. Mattson, B. Basham, K. Smith, T. Chen, F. Morel, et al. 2007. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8: 950-957.
25. Korn, T., M. Oukka, V. Kuchroo, and E. Bettelli. 2007. Th17 cells: effector T cells with inflammatory properties. Semin. Immunol. 19: 362-371. (Pubitemid 351274046)
26. H17 cells. Nature 448: 484-487.
27. H17 cells. Nature 453: 1051-1057.
28. Ouyang, W., J. K. Kolls, and Y. Zheng. 2008. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467. (Pubitemid 351471762)
29. Weaver, C. T., R. D. Hatton, P. R. Mangan, and L. E. Harrington. 2007. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25: 821-852.
30. Pohlers, D., J. Brenmoehl, I. Loffler, C. K. Muller, C. Leipner, S. Schultze-Mosgau, A. Stallmach, R. W. Kinne, and G. Wolf. 2009. TGFβ and fibrosis in different organs-molecular pathway imprints. Biochim. Biophys. Acta 1792: 746-756.
31. Cortez, D. M., M. D. Feldman, S. Mummidi, A. J. Valente, B. Steffensen, M. Vincenti, J. L. Barnes, and B. Chandrasekar. 2007. IL-17 stimulates MMP-1 expression in primary human cardiac fibroblasts via p38 MAPK- and ERK1/2-dependent C/EBP-β, NF-κB, and AP-1 activation. Am. J. Physiol. 293: H3356-H3365.
32. Venkatachalam, K., S. Mummidi, D. M. Cortez, S. D. Prabhu, A. J. Valente, and B. Chandrasekar. 2008. Resveratrol inhibits high glucose-induced PI3K/Akt/ERK-dependent interleukin-17 expression in primary mouse cardiac fibroblasts. Am. J. Physiol. 294: H2078-H2087.
33. Burlingham, W. J., R. B. Love, E. Jankowska-Gan, L. D. Haynes, Q. Xu, J. L. Bobadilla, K. C. Meyer, M. S. Hayney, R. K. Braun, D. S. Greenspan, et al. 2007. IL-17-dependent cellular immunity to collagen type V predisposes to obliterative bronchiolitis in human lung transplants. J. Clin. Invest. 117: 3498-3506.
34. Molet, S., Q. Hamid, F. Davoine, E. Nutku, R. Taha, N. Page, R. Olivenstein, J. Elias, and J. Chakir. 2001. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J. Allergy Clin. Immunol. 108: 430-438. (Pubitemid 32881066)
35. Dubin, P. J., F. McAllister, and J. K. Kolls. 2007. Is cystic fibrosis a TH17 disease? Inflamm. Res. 56: 221-227.
36. Fukami, N., S. Ramachandran, D. Saini, M. Walter, W. Chapman, G. A. Patterson, and T. Mohanakumar. 2009. Antibodies to MHC class I induce autoimmunity: role in the pathogenesis of chronic rejection. J. Immunol. 182: 309-318.
37. Simonian, P. L., C. L. Roark, F. Wehrmann, A. K. Lanham, F. Diaz del Valle, W. K. Born, R. L. O'Brien, and A. P. Fontenot. 2009. Th17-polarized immune response in a murine model of hypersensitivity pneumonitis and lung fibrosis. J. Immunol. 182: 657-665.
38. Walsh, P. T., D. K. Taylor, and L. A. Turka. 2004. Tregs and transplantation tolerance. J. Clin. Invest. 114: 1398-1403.
39. + regulatory T cells in the induction and maintenance of transplantation tolerance. Transpl. Immunol. 17: 120-129.
40. Josien, R., P. Douillard, C. Guillot, M. Muschen, I. Anegon, J. Chetritt, S. Menoret, C. Vignes, J. P. Soulillou, and M. C. Cuturi. 1998. A critical role for transforming growth factor-β in donor transfusion-induced allograft tolerance. J. Clin. Invest. 102: 1920-1926. (Pubitemid 29001837)
41. + T cells or B cells. J. Immunol. 161: 1868-1874.
42. Daley, S. R., J. Ma, E. Adams, S. P. Cobbold, and H. Waldmann. 2007. A key role for TGFβ signaling to T cells in the long-term acceptance of allografts. J. Immunol. 179: 3648-3654.
43. + T cells to transforming growth factor α1. Transplantation 70: 1292-1301.
44. Csencsits, K., S. C. Wood, G. Lu, and D. K. Bishop. 2005. Transforming growth factor-β1 gene transfer is associated with the development of regulatory cells. Am. J. Transplant. 5: 2378-2384. (Pubitemid 43919420)
45. Csencsits, K., S. C. Wood, G. Lu, S. M. Faust, D. Brigstock, E. J. Eichwald, C. G. Orosz, and D. K. Bishop. 2006. Transforming growth factor β-induced connective tissue growth factor and chronic allograft rejection. Am. J. Transplant. 6: 959-966. (Pubitemid 44356645)
46. Nakae, S., Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, I. Homma, K. Sekikawa, M. Asano, and Y. Iwakura. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17: 375-387. (Pubitemid 35279557)
47. Corry, R. J., H. J. Winn, and P. S. Russell. 1973. Primarily vascularized allografts of hearts in mice: the role of H-2D, H-2K, and non-H-2 antigens in rejection. Transplantation 16: 343-350.
48. Bishop, D. K., W. Li, S. Y. Chan, R. D. Ensley, J. Shelby, and E. J. Eichwald. 1994. Helper T lymphocyte unresponsiveness to cardiac allografts following transient depletion of CD4-positive cells: implications for cellular and humoral responses. Transplantation 58: 576-584.
49. Piccotti, J. R., K. Li, S. Y. Chan, E. J. Eichwald, and D. K. Bishop. 1999. Cytokine regulation of chronic cardiac allograft rejection: evidence against a role for Th1 in the disease process. Transplantation 67: 1548-1555.
50. Csencsits, K., B. E. Burrell, G. Lu, E. J. Eichwald, G. L. Stahl, and D. K. Bishop. 2008. The classical complement pathway in transplantation: unanticipated protective effects of C1q and role in inductive antibody therapy. Am. J. Transplant. 8: 1622-1630.
51. Matesic, D., P. V. Lehmann, and P. S. Heeger. 1998. High-resolution characterization of cytokine-producing alloreactivity in naive and allograft-primed mice. Transplantation 65: 906-914. (Pubitemid 28201441)
52. Burrell, B. E., G. Lu, X. C. Li, and D. K. Bishop. 2009. OX40 costimulation prevents allograft acceptance induced by CD40-CD40L blockade. J. Immunol. 182: 379-390.
53. Diaz, J. A., A. J. Booth, G. Lu, S. C. Wood, D. J. Pinsky, and D. K. Bishop. 2009. Critical role for IL-6 in hypertrophy and fibrosis in chronic cardiac allograft rejection. Am J. Transplant. 9: 1773-1783.
54. Wood, S. C., G. Lu, B. E. Burrell, and D. K. Bishop. 2008. Transplant acceptance following anti-CD4 versus anti-CD40L therapy: evidence for differential maintenance of graft-reactive T cells. Am. J. Transplant. 8: 2037-2048.
55. Nathan, M. J., D. Yin, E. J. Eichwald, and D. K. Bishop. 2002. The immunobiology of inductive anti-CD40L therapy in transplantation: allograft acceptance is not dependent upon the deletion of graft-reactive T cells. Am. J. Transplant. 2: 323-332.
56. Branton, M. H., and J. B. Kopp. 1999. TGFβ and fibrosis. Microbes Infect. 1: 1349-1365.
57. Leask, A. 2007. TGFβ, cardiac fibroblasts, and the fibrotic response. Cardiovasc. Res. 74: 207-212. (Pubitemid 46533834)
58. Jain, S., P. N. Furness, and M. L. Nicholson. 2000. The role of transforming growth factor β in chronic renal allograft nephropathy. Transplantation 69: 1759-1766. (Pubitemid 30340326)
59. Colvin, R. B. 2007. Antibody-mediated renal allograft rejection: diagnosis and pathogenesis. J. Am. Soc. Nephrol. 18: 1046-1056. (Pubitemid 46536891)
60. Singh, N., J. Pirsch, and M. Samaniego. 2009. Antibody-mediated rejection: treatment alternatives and outcomes. Transplant Rev. (Orlando) 23: 34-46.
61. Calderhead, D. M., Y. Kosaka, E. M. Manning, and R. J. Noelle. 2000. CD40-CD154 interactions in B-cell signaling. Curr. Top. Microbiol. Immunol. 245: 73-99.
62. Wasowska, B. A., Z. Qian, D. L. Cangello, E. Behrens, K. Van Tran, J. Layton, F. Sanfilippo, and W. M. Baldwin, III. 2001. Passive transfer of alloantibodies restores acute cardiac rejection in IgKO mice. Transplantation 71: 727-736. (Pubitemid 32377270)
63. Baldwin, W. M., 3rd, E. K. Kasper, A. A. Zachary, B. A. Wasowska, and E. R. Rodriguez. 2004. Beyond C4d: other complement-related diagnostic approaches to antibody-mediated rejection. Am. J. Transplant. 4: 311-318.
64. Rodriguez, E. R., D. V. Skojec, C. D. Tan, A. A. Zachary, E. K. Kasper, J. V. Conte, and W. M. Baldwin, III. 2005. Antibody-mediated rejection in human cardiac allografts: evaluation of immunoglobulins and complement activation products C4d and C3d as markers. Am. J. Transplant. 5: 2778-2785. (Pubitemid 43920074)
65. Schubert, L. A., E. Jeffery, Y. Zhang, F. Ramsdell, and S. F. Ziegler. 2001. Scurfin (FOXP3) acts as a repressor of transcription and regulates T cell activation. J. Biol. Chem. 276: 37672-37679. (Pubitemid 37384195)
66. + regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J. Immunol. 172: 6003-6010.
67. - T cells through Foxp3 induction and down-regulation of Smad7. J. Immunol. 172: 5149-5153.
68. Veldhoen, M., and B. Stockinger. 2006. TGFβ1, a "Jack of all trades": the link with pro-inflammatory IL-17-producing T cells. Trends Immunol. 27: 358-361.
69. Waldmann, H., T. C. Chen, L. Graca, E. Adams, S. Daley, S. Cobbold, and P. J. Fairchild. 2006. Regulatory T cells in transplantation. Semin. Immunol. 18: 111-119.
70. Wakashin, H., K. Hirose, Y. Maezawa, S. Kagami, A. Suto, N. Watanabe, Y. Saito, M. Hatano, T. Tokuhisa, Y. Iwakura, et al. 2008. IL-23 and Th17 cells enhance Th2-cell-mediated eosinophilic airway inflammation in mice. Am. J. Respir. Crit. Care Med. 178: 1023-1032.
71. + T-cell subpopulation TH17 in the pathogenesis of systemic scleroderma. Nat. Clin. Pract. Rheumatol. 3: 682-683.
72. Waldmann, H., L. Graca, S. Cobbold, E. Adams, M. Tone, and Y. Tone. 2004. Regulatory T cells and organ transplantation. Semin. Immunol. 16: 119-126.
73. Rahimi, S., Z. Qian, J. Layton, K. Fox-Talbot, W. M. Baldwin, III, and B. A. Wasowska. 2004. Non-complement- and complement-activating antibodies synergize to cause rejection of cardiac allografts. Am. J. Transplant. 4: 326-334.
74. Behr, T. M., H. E. Feucht, K. Richter, C. Reiter, C. H. Spes, D. Pongratz, P. Uberfuhr, B. Meiser, K. Theisen, and C. E. Angermann. 1999. Detection of humoral rejection in human cardiac allografts by assessing the capillary deposition of complement fragment C4d in endomyocardial biopsies. J. Heart Lung Transplant. 18: 904-912.
75. + regulatory T cell recruitment in human renal allograft infiltrates. J. Immunol. 179: 4901-4909.
76. + T regulatory cells mediating allograft tolerance depends on the CCR4 chemokine receptor. J. Exp. Med. 201: 1037-1044.
77. Graca, L., S. P. Cobbold, and H. Waldmann. 2002. Identification of regulatory T cells in tolerated allografts. J. Exp. Med. 195: 1641-1646.
78. + regulatory T cells. J. Exp. Med. 201: 737-746.
79. Chen, D., and J. S. Bromberg. 2006. T regulatory cells and migration. Am. J. Transplant. 6: 1518-1523.
80. Zhang, N., B. Schroppel, G. Lal, C. Jakubzick, X. Mao, D. Chen, N. Yin, R. Jessberger, J. C. Ochando, Y. Ding, and J. S. Bromberg. 2009. Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response. Immunity 30: 458-469.
81. Leask, A., and D. J. Abraham. 2004. TGFβ signaling and the fibrotic response. FASEB J. 18: 816-827.
82. Hirano, T., S. Akira, T. Taga, and T. Kishimoto. 1990. Biological and clinical aspects of interleukin 6. Immunol. Today 11: 443-449.
83. Uitto, J. 2007. IL-6 signaling pathway in keloids: a target for pharmacologic intervention? J. Invest. Dermatol. 127: 6-8.
84. Duncan, M. R., and B. Berman. 1991. Stimulation of collagen and glycosaminoglycan production in cultured human adult dermal fibroblasts by recombinant human interleukin 6. J. Invest. Dermatol. 97: 686-692.