TGFβ neutralization within cardiac allografts by decorin gene transfer attenuates chronic rejection

Journal of Immunology

Volumn 183, Issue 11, 2009, Pages 7307-7313

  Faust, Susan M ^a   Lu, Guanyi ^a   Wood, Sherri C ^a   Bishop, D Keith ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; DECORIN; OKT 4; TRANSFORMING GROWTH FACTOR BETA; PROTEOGLYCAN; SCLEROPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CARDIAC ALLOGRAFT; CARDIAC GRAFT REJECTION; CHRONIC GRAFT REJECTION; CONTROLLED STUDY; FIBROSING ALVEOLITIS; GENE EXPRESSION; GENE TRANSFER; GRAFT SURVIVAL; HEART GRAFT; HEART VENTRICLE HYPERTROPHY; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T CELL DEPLETION; T LYMPHOCYTE; ALLOTRANSPLANTATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CHRONIC DISEASE; DRUG ANTAGONISM; FIBROSIS; GENETIC TRANSDUCTION; GENETICS; GRAFT REJECTION; HEART TRANSPLANTATION; IMMUNOLOGY; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; B-LYMPHOCYTES; CHRONIC DISEASE; EXTRACELLULAR MATRIX PROTEINS; FIBROSIS; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PROTEOGLYCANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION, HOMOLOGOUS;

EID: 73349119965     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902736     Document Type: Article

References (72)

1. Al-khaldi, A., and R. C. Robbins. 2006. New directions in cardiac transplantation. Annu. Rev. Med. 57: 455-471.
2. Hayry, P., H. Isoniemi, S. Yilmaz, A. Mennander, K. Lemstrom, A. Raisanen-Sokolowski, P. Koskinen, J. Ustinov, I. Lautenschlager, E. Taskinen, et al. 1993. Chronic allograft rejection. Immunol. Rev. 134: 33-81.
3. 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.
4. Libby, P., and J. S. Pober. 2001. Chronic rejection. Immunity 14: 387-397.
5. Orosz, C. G., and R. P. Pelletier. 1997. Chronic remodeling pathology in grafts. Curr. Opin. Immunol. 9: 676-680.
6. Weis, M., and W. von Scheidt. 1997. Cardiac allograft vasculopathy: a review. Circulation 96: 2069-2077.
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-β 1 gene results in multifocal inflammatory disease. Nature 359: 693-699.
9. Kulkarni, A. B., J. M. Ward, L. Yaswen, C. L. Mackall, S. R. Bauer, C. G. Huh, R. E. Gress, and S. Karlsson. 1995. Transforming growth factor-β 1 null mice: an animal model for inflammatory disorders. Am. J. Pathol. 146: 264-275.
10. Rubtsov, Y. P., and A. Y. Rudensky. 2007. TGFβ signalling in control of T-cellmediated self-reactivity. Nat. Rev. Immunol. 7: 443-453.
11. Lebman, D. A., and J. S. Edmiston. 1999. The role of TGF-β in growth, differentiation, and maturation of B lymphocytes. Microbes Infect. 1: 1297-1304.
12. + regulatory T cells is mediated by cell surfacebound transforming growth factor β. J. Exp. Med. 194: 629-644.
13. Levings, M. K., R. Bacchetta, U. Schulz, and M. G. Roncarolo. 2002. The role of IL-10 and TGF-β in the differentiation and effector function of T regulatory cells. Int. Arch. Allergy Immunol. 129: 263-276.
14. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
15. 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.
16. Branton, M. H., and J. B. Kopp. 1999. TGF-β and fibrosis. Microbes Infect. 1: 1349-1365.
17. Leask, A., and D. J. Abraham. 2004. TGF-β signaling and the fibrotic response. FASEB J. 18: 816-827.
18. Kang, H. R., S. J. Cho, C. G. Lee, R. J. Homer, and J. A. Elias. 2007. Transforming growth factor (TGF)-β1 stimulates pulmonary fibrosis and inflammation via a Bax-dependent, bid-activated pathway that involves matrix metalloproteinase- 12. J. Biol. Chem. 282: 7723-7732.
19. Yamamoto, T., N. A. Noble, A. H. Cohen, C. C. Nast, A. Hishida, L. I. Gold, and W. A. Border. 1996. Expression of transforming growth factor-β isoforms in human glomerular diseases. Kidney Int. 49: 461-469. (Pubitemid 26050323)
20. Denton, C. P., and D. J. Abraham. 2001. Transforming growth factor-β and connective tissue growth factor: key cytokines in scleroderma pathogenesis. Curr. Opin. Rheumatol. 13: 505-511. (Pubitemid 33070969)
21. 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)
22. Leask, A. 2007. TGFβ, cardiac fibroblasts, and the fibrotic response. Cardiovasc. Res. 74: 207-212. (Pubitemid 46533834)
23. Stander, M., U. Naumann, W. Wick, and M. Weller. 1999. Transforming growth factor-β and p-21: multiple molecular targets of decorin-mediated suppression of neoplastic growth. Cell Tissue Res. 296: 221-227. (Pubitemid 29219174)
24. Yamaguchi, Y., D. M. Mann, and E. Ruoslahti. 1990. Negative regulation of transforming growth factor-β by the proteoglycan decorin. Nature 346: 281-284. (Pubitemid 20227409)
25. Border, W. A., N. A. Noble, T. Yamamoto, J. R. Harper, Y. Yamaguchi, M. D. Pierschbacher, and E. Ruoslahti. 1992. Natural inhibitor of transforming growth factor-β protects against scarring in experimental kidney disease. Nature 360: 361-364.
26. Isaka, Y., D. K. Brees, K. Ikegaya, Y. Kaneda, E. Imai, N. A. Noble, and W. A. Border. 1996. Gene therapy by skeletal muscle expression of decorin prevents fibrotic disease in rat kidney. Nat. Med. 2: 418-423. (Pubitemid 26191913)
27. 2+-dependent phosphorylation of Smad2 at serine-240. Biochem J. 362: 643-649.
28. Kolb, M., P. J. Margetts, P. J. Sime, and J. Gauldie. 2001. Proteoglycans decorin and biglycan differentially modulate TGF-β-mediated fibrotic responses in the lung. Am. J. Physiol. 280: L1327-L1334.
29. 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.
30. Daley, S. R., J. Ma, E. Adams, S. P. Cobbold, and H. Waldmann. 2007. A key role for TGF-β signaling to T cells in the long-term acceptance of allografts. J. Immunol. 179: 3648-3654.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. Chan, S. Y., K. Li, J. R. Piccotti, M. C. Louie, T. A. Judge, L. A. Turka, E. J. Eichwald, and D. K. Bishop. 1999. Tissue-specific consequences of the anti-adenoviral immune response: implications for cardiac transplants. Nat. Med. 5: 1143-1149.
38. + T cells to transforming growth factor β1. Transplantation 70: 1292-1301.
39. 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.
40. Cutroneo, K. R. 2007. TGF-β-induced fibrosis and SMAD signaling: oligo decoys as natural therapeutics for inhibition of tissue fibrosis and scarring. Wound Repair Regen. 15 Suppl. 1: S54-S60.
41. Walsh, P. T., D. K. Taylor, and L. A. Turka. 2004. Tregs and transplantation tolerance. J. Clin. Invest. 114: 1398-1403.
42. + regulatory T cells in the induction and maintenance of transplantation tolerance. Transpl. Immunol. 17: 120-129.
43. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
44. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-β induces development of the TH17 lineage. Nature 441: 231-234.
45. Zhou, L., J. E. Lopes, M. M. Chong, I. I. Ivanov, R. Min, G. D. Victora, Y. Shen, J. Du, Y. P. Rubtsov, A. Y. Rudensky, et al. 2008. TGF-β-induced Foxp3 inhibits TH17 cell differentiation by antagonizing RORγt function. Nature 453: 236-240. 46. Chen, D., and J. S. Bromberg. 2006. T regulatory cells and migration. Am. J. Transplant. 6: 1518-1523.
46. Marian, A. J. 2008. Genetic determinants of cardiac hypertrophy. Curr. Opin. Cardiol. 23: 199-205.
47. Schneider, M. D. 2002. Serial killer: angiotensin drives cardiac hypertrophy via TGF-β1. J. Clin. Invest. 109: 715-716.
48. Raichlin, E., H. R. Villarraga, K. Chandrasekaran, A. L. Clavell, R. P. Frantz, S. S. Kushwaha, R. J. Rodeheffer, C. G. McGregor, R. C. Daly, S. J. Park, et al. 2009. Cardiac allograft remodeling after heart transplantation is associated with increased graft vasculopathy and mortality. Am. J. Transplant. 9: 132-139.
49. Torre-Amione, G. 2009. Cardiac allograft hypertrophy: a new target for therapy, a surrogate marker for survival? Am. J. Transplant. 9: 7-8.
50. Mannon, R. B. 2006. Therapeutic targets in the treatment of allograft fibrosis. Am. J. Transplant. 6: 867-875.
51. 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)
52. Wood, K. J., and S. Sakaguchi. 2003. Regulatory T cells in transplantation tolerance. Nat. Rev. Immunol. 3: 199-210.
53. + regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J. Immunol. 172: 6003-6010.
54. + regulatory T cell recruitment in human renal allograft infiltrates. J. Immunol. 179: 4901-4909.
55. + T regulatory cells mediating allograft tolerance depends on the CCR4 chemokine receptor. J. Exp. Med. 201: 1037-1044.
56. Josefowicz, S. Z., and A. Rudensky. 2009. Control of regulatory T cell lineage commitment and maintenance. Immunity 30: 616-625.
57. Liston, A., and A. Y. Rudensky. 2007. Thymic development and peripheral homeostasis of regulatory T cells. Curr. Opin. Immunol. 19: 176-185. (Pubitemid 46356966)
58. 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.
59. Petrov, V. V., R. H. Fagard, and P. J. Lijnen. 2002. Stimulation of collagen production by transforming growth factor-β1 during differentiation of cardiac fibroblasts to myofibroblasts. Hypertension 39: 258-263.
60. Weber, K. T., C. G. Brilla, S. E. Campbell, G. Zhou, L. Matsubara, and E. Guarda. 1992. Pathologic hypertrophy with fibrosis: the structural basis for myocardial failure. Blood 1: 75-85.
61. Jahanyar, J., D. L. Joyce, R. E. Southard, M. Loebe, G. P. Noon, M. M. Koerner, G. Torre-Amione, and K. A. Youker. 2007. Decorin-mediated transforming growth factor-β inhibition ameliorates adverse cardiac remodeling. J. Heart Lung Transplant. 26: 34-40. (Pubitemid 46096736)
62. Bettelli, E., T. Korn, M. Oukka, and V. K. Kuchroo. 2008. Induction and effector functions of TH17 cells. Nature 453: 1051-1057. (Pubitemid 351871737)
63. 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)
64. 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.
65. 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.
66. 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.
67. 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)
68. Dubin, P. J., F. McAllister, and J. K. Kolls. 2007. Is cystic fibrosis a TH17 disease? Inflamm. Res. 56: 221-227.
69. 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.
70. Groeneveld, T. W., M. Oroszlan, R. T. Owens, M. C. Faber-Krol, A. C. Bakker, G. J. Arlaud, D. J. McQuillan, U. Kishore, M. R. Daha, and A. Roos. 2005. Interactions of the extracellular matrix proteoglycans decorin and biglycan with C1q and collectins. J. Immunol. 175: 4715-4723.
71. Wehner, J., C. N. Morrell, T. Reynolds, E. R. Rodriguez, and W. M. Baldwin, 3rd. 2007. Antibody and complement in transplant vasculopathy. Circ. Res. 100: 191-203.
72. Faust, S. M., G. Lu, B. L. Marini, W. Zou, D. Gordon, Y. Iwakura, Y. Laouar, and D. K. Bishop. 2009. Role of T cell TGFβ signaling and IL-17 in allograft acceptance and fibrosis associated with chronic rejection. J. Immunol. 183: 7297-7306.