IL-6 promotes cardiac graft rejection mediated by CD4 + cells

Journal of Immunology

Volumn 187, Issue 11, 2011, Pages 5764-5771

  Booth, Adam Jared ^a   Grabauskiene, Svetlana ^b   Wood, Sherri Chan ^b   Lu, Guanyi ^b   Burrell, Bryna E ^c   Bishop, D Keith ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIBODY; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; MONOCYTE CHEMOTACTIC PROTEIN 1;

ACUTE GRAFT REJECTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; CARDIAC GRAFT REJECTION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LINEAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GRAFT SURVIVAL; HEART TRANSPLANTATION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL TIME; TH1 CELL; TH2 CELL;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL LINEAGE; FEMALE; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; INTERLEUKIN-6; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSPLANTATION, HOMOLOGOUS;

EID: 82755189261     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100766     Document Type: Article

References (70)

1. Bishop, D. K., J. Shelby, and E. J. Eichwald. 1992. Mobilization of T lymphocytes following cardiac transplantation: evidence that CD4-positive cells are required for cytotoxic T lymphocyte activation, inflammatory endothelial development, graft infiltration, and acute allograft rejection. Transplantation 53: 849-857.
2. Shizuru, J. A., K. B. Seydel, T. F. Flavin, A. P. Wu, C. C. Kong, E. G. Hoyt, N. Fujimoto, M. E. Billingham, V. A. Starnes, and C. G. Fathman. 1990. Induction of donor-specific unresponsiveness to cardiac allografts in rats by pretransplant anti-CD4 monoclonal antibody therapy. Transplantation 50: 366-373. (Pubitemid 20309852)
3. + cells are essential for allorejection. J. Exp. Med. 184: 2013-2018.
4. 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 TGFb signaling and IL-17 in allograft acceptance and fibrosis associated with chronic rejection. J. Immunol. 183: 7297-7306.
5. Dodge, I. L., M. W. Carr, M. Cernadas, and M. B. Brenner. 2003. IL-6 production by pulmonary dendritic cells impedes Th1 immune responses. J. Immunol. 170: 4457-4464. (Pubitemid 36519950)
6. Diehl, S., J. Anguita, A. Hoffmeyer, T. Zapton, J. N. Ihle, E. Fikrig, and M. Rincón. 2000. Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity 13: 805-815. (Pubitemid 32041803)
7. Rincón, M., J. Anguita, T. Nakamura, E. Fikrig, and R. A. Flavell. 1997. Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J. Exp. Med. 185: 461-469. (Pubitemid 27078364)
8. 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.
9. Kimura, A., T. Naka, and T. Kishimoto. 2007. IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc. Natl. Acad. Sci. USA 104: 12099-12104. (Pubitemid 47185636)
10. Yamamoto, M., K. Yoshizaki, T. Kishimoto, and H. Ito. 2000. IL-6 is required for the development of Th1 cell-mediated murine colitis. J. Immunol. 164: 4878-4882. (Pubitemid 30238092)
11. Joseph, S. B., K. T. Miner, and M. Croft. 1998. Augmentation of naive, Th1 and Th2 effector CD4 responses by IL-6, IL-1 and TNF. Eur. J. Immunol. 28: 277-289. (Pubitemid 28048298)
12. +CD25 T cells. J. Immunol. 179: 2041-2045.
13. Samanta, A., B. Li, X. Song, K. Bembas, G. Zhang, M. Katsumata, S. J. Saouaf, Q. Wang, W. W. Hancock, Y. Shen, and M. I. Greene. 2008. TGF-β and IL-6 signals modulate chromatin binding and promoter occupancy by acetylated FOXP3. Proc. Natl. Acad. Sci. USA 105: 14023-14027.
14. + T cell regulatory functions. J. Immunol. 178: 271-279.
15. Zhao, X. M., T. K. Yeoh, M. Hiebert, W. H. Frist, and G. G. Miller. 1993. The expression of acidic fibroblast growth factor (heparin-binding growth factor-1) and cytokine genes in human cardiac allografts and T cells. Transplantation 56: 1177-1182. (Pubitemid 23348697)
16. Zhao, X. M., W. H. Frist, T. K. Yeoh, and G. G. Miller. 1993. Expression of cytokine genes in human cardiac allografts: correlation of IL-6 and transforming growth factor-beta (TGF-β) with histological rejection. Clin. Exp. Immunol. 93: 448-451.
17. Liang, Y., K. Christopher, P. W. Finn, Y. L. Colson, and D. L. Perkins. 2007. Graft produced interleukin-6 functions as a danger signal and promotes rejection after transplantation. Transplantation 84: 771-777. (Pubitemid 47480663)
18. Booth, A. J., K. Csencsits-Smith, S. C. Wood, G. Lu, K. E. Lipson, and D. K. Bishop. 2010. Connective tissue growth factor promotes fibrosis downstream of TGFβ and IL-6 in chronic cardiac allograft rejection. Am. J. Transplant. 10: 220-230.
19. 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.
20. Chen, L., E. Ahmed, T. Wang, Y. Wang, J. Ochando, A. S. Chong, and M. L. Alegre. 2009. TLR signals promote IL-6/IL-17-dependent transplant rejection. J. Immunol. 182: 6217-6225.
21. Burrell, B. E., and D. K. Bishop. 2010. Th17 cells and transplant acceptance. Transplantation 90: 945-948.
22. + Th17 mediate costimulation blockade-resistant allograft rejection in T-bet-deficient mice. J. Immunol. 181: 3906-3914.
23. Booth, A. J., and D. K. Bishop. 2010. TGF-β, IL-6, IL-17 and CTGF direct multiple pathologies of chronic cardiac allograft rejection. Immunotherapy 2: 511-520.
24. + T cells results in Th2 cytokine production and alternate mechanisms of allograft rejection. Transplantation 59: 1155-1161.
25. Piccotti, J. R., S. Y. Chan, A. M. VanBuskirk, E. J. Eichwald, and D. K. Bishop. 1997. Are Th2 helper T lymphocytes beneficial, deleterious, or irrelevant in promoting allograft survival? Transplantation 63: 619-624. (Pubitemid 27132189)
26. Piccotti, J. R., S. Y. Chan, R. E. Goodman, J. Magram, E. J. Eichwald, and D. K. Bishop. 1996. IL-12 antagonism induces T helper 2 responses, yet exacerbates cardiac allograft rejection: evidence against a dominant protective role for T helper 2 cytokines in alloimmunity. J. Immunol. 157: 1951-1957. (Pubitemid 126449668)
27. 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.
28. 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)
29. 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. (Pubitemid 24289849)
30. Bishop, D. K., S. Chan, W. Li, R. D. Ensley, S. Xu, and E. J. Eichwald. 1993. CD4-positive helper T lymphocytes mediate mouse cardiac allograft rejection independent of donor alloantigen specific cytotoxic T lymphocytes. Transplantation 56: 892-897. (Pubitemid 23321525)
31. + cells and CD40-CD40 ligand interactions. J. Immunol. 166: 3248-3255.
32. Spörri, B., K. M. Müller, U. Wiesmann, and M. Bickel. 1999. Soluble IL-6 receptor induces calcium flux and selectively modulates chemokine expression in human dermal fibroblasts. Int. Immunol. 11: 1053-1058. (Pubitemid 29338746)
33. Tieu, B. C., C. Lee, H. Sun, W. Lejeune, A. Recinos, III, X. Ju, H. Spratt, D. C. Guo, D. Milewicz, R. G. Tilton, and A. R. Brasier. 2009. An adventitial IL- 6/MCP1 amplification loop accelerates macrophage-mediated vascular inflammation leading to aortic dissection in mice. J. Clin. Invest. 119: 3637-3651.
34. Hurst, S. M., T. S. Wilkinson, R. M. McLoughlin, S. Jones, S. Horiuchi, N. Yamamoto, S. Rose-John, G. M. Fuller, N. Topley, and S. A. Jones. 2001. Il-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 14: 705-714. (Pubitemid 32592418)
35. Takatsuki, F., A. Okano, C. Suzuki, R. Chieda, Y. Takahara, T. Hirano, T. Kishimoto, J. Hamuro, and Y. Akiyama. 1988. Human recombinant IL-6/ B cell stimulatory factor 2 augments murine antigen-specific antibody responses in vitro and in vivo. J. Immunol. 141: 3072-3077.
36. Goldman, M., A. Le Moine, M. Braun, V. Flamand, and D. Abramowicz. 2001. A role for eosinophils in transplant rejection. Trends Immunol. 22: 247-251. (Pubitemid 32667511)
37. Martinez, O. M., N. L. Ascher, L. Ferrell, J. Villanueva, J. Lake, J. P. Roberts, and S. M. Krams. 1993. Evidence for a nonclassical pathway of graft rejection involving interleukin 5 and eosinophils. Transplantation 55: 909-918. (Pubitemid 23122070)
38. Reed, E. F., A. J. Demetris, E. Hammond, S. Itescu, J. A. Kobashigawa, N. L. Reinsmoen, E. R. Rodriguez, M. Rose, S. Stewart, N. Suciu-Foca, et al. International Society for Heart and Lung Transplantation. 2006. Acute antibody-mediated rejection of cardiac transplants. J. Heart Lung Transplant. 25: 153-159. (Pubitemid 43156365)
39. Colvin, R. B., and R. N. Smith. 2005. Antibody-mediated organ-allograft rejection. Nat. Rev. Immunol. 5: 807-817. (Pubitemid 41400854)
40. 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.
41. Atreya, R., J. Mudter, S. Finotto, J. Müllberg, T. Jostock, S. Wirtz, M. Schütz, B. Bartsch, M. Holtmann, C. Becker, et al. 2000. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat. Med. 6: 583-588. (Pubitemid 30305911)
42. DiCosmo, B. F., G. P. Geba, D. Picarella, J. A. Elias, J. A. Rankin, B. R. Stripp, J. A. Whitsett, and R. A. Flavell. 1994. Airway epithelial cell expression of interleukin-6 in transgenic mice: uncoupling of airway inflammation and bronchial hyperreactivity. J. Clin. Invest. 94: 2028-2035.
43. Vanden Bush, T. J., C. M. Buchta, J. Claudio, and G. A. Bishop. 2009. Cutting edge: importance of IL-6 and cooperation between innate and adaptive immune receptors in cellular vaccination with B lymphocytes. J. Immunol. 183: 4833-4837.
44. Ming, J. E., R. M. Steinman, and A. Granelli-Piperno. 1992. IL-6 enhances the generation of cytolytic T lymphocytes in the allogeneic mixed leucocyte reaction. Clin. Exp. Immunol. 89: 148-153.
45. Renauld, J. C., A. Vink, and J. Van Snick. 1989. Accessory signals in murine cytolytic T cell responses: dual requirement for IL-1 and IL-6. J. Immunol. 143: 1894-1898. (Pubitemid 19241204)
46. Kishimoto, H., and J. Sprent. 1999. Strong TCR ligation without costimulation causes rapid onset of Fas-dependent apoptosis of naive murine CD4+ T cells. J. Immunol. 163: 1817-1826. (Pubitemid 29382180)
47. Teague, T. K., B. C. Schaefer, D. Hildeman, J. Bender, T. Mitchell, J.W. Kappler, and P. Marrack. 2000. Activation-induced inhibition of interleukin 6-mediated T cell survival and signal transducer and activator of transcription 1 signaling. J. Exp. Med. 191: 915-926.
48. Teague, T. K., P. Marrack, J. W. Kappler, and A. T. Vella. 1997. IL-6 rescues resting mouse T cells from apoptosis. J. Immunol. 158: 5791-5796. (Pubitemid 127483985)
49. Russell, M. E., D. H. Adams, L. R. Wyner, Y. Yamashita, N. J. Halnon, and M. J. Karnovsky. 1993. Early and persistent induction of monocyte chemo-attractant protein 1 in rat cardiac allografts. Proc. Natl. Acad. Sci. USA 90: 6086-6090. (Pubitemid 23191459)
50. Fleury, S., J. Li, E. Simeoni, E. Fiorini, L. K. von Segesser, L. Kappenberger, and G. Vassalli. 2006. Gene transfer of RANTES and MCP-1 chemokine antagonists prolongs cardiac allograft survival. Gene Ther. 13: 1104-1109.
51. Wehner, J. R., C. N. Morrell, E. R. Rodriguez, R. L. Fairchild, and W. M. Baldwin, III. 2009. Immunological challenges of cardiac transplantation: the need for better animal models to answer current clinical questions. J. Clin. Immunol. 29: 722-729.
52. + T cells. J. Exp. Med. 206: 69-78.
53. Nurieva, R. I., and C. Dong. 2009. (IL-)12 and 21: a new kind of help in the follicles. Immunol. Cell Biol. 87: 577-578.
54. Leonard, W. J., and R. Spolski. 2005. Interleukin-21: a modulator of lymphoid proliferation, apoptosis and differentiation. Nat. Rev. Immunol. 5: 688-698. (Pubitemid 43086171)
55. Nadeau, W. J., T. G. Pistole, and B. A. McCormick. 2002. Polymorphonuclear leukocyte migration across model intestinal epithelia enhances Salmonella typhimurium killing via the epithelial derived cytokine, IL-6. Microbes Infect. 4: 1379-1387. (Pubitemid 35435355)
56. Romano, M., M. Sironi, C. Toniatti, N. Polentarutti, P. Fruscella, P. Ghezzi, R. Faggioni, W. Luini, V. van Hinsbergh, S. Sozzani, et al. 1997. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 6: 315-325. (Pubitemid 27148598)
57. McLoughlin, R. M., B. J. Jenkins, D. Grail, A. S. Williams, C. A. Fielding, C. R. Parker, M. Ernst, N. Topley, and S. A. Jones. 2005. IL-6 trans-signaling via STAT3 directs T cell infiltration in acute inflammation. Proc. Natl. Acad. Sci. USA 102: 9589-9594. (Pubitemid 40981725)
58. Leal, I. S., B. Smedegârd, P. Andersen, and R. Appelberg. 1999. Interleukin-6 and interleukin-12 participate in induction of a type 1 protective T-cell response during vaccination with a tuberculosis subunit vaccine. Infect. Immun. 67: 5747-5754. (Pubitemid 29508094)
59. Wu, W., L. Weigand, and S. Mendez. 2009. The IL-6-deficient mouse exhibits impaired lymphocytic responses to a vaccine combining live Leishmania major and CpG oligodeoxynucleotides. Can. J. Microbiol. 55: 705-713.
60. Ladel, C. H., C. Blum, A. Dreher, K. Reifenberg, M. Kopf, and S. H. Kaufmann. 1997. Lethal tuberculosis in interleukin-6-deficient mutant mice. Infect. Immun. 65: 4843-4849. (Pubitemid 27463266)
61. Ehrchen, J. M., K. Roebrock, D. Foell, N. Nippe, E. von Stebut, J. M. Weiss, N. A. Münck, D. Viemann, G. Varga, C. Müller-Tidow, et al. 2010. Keratinocytes determine Th1 immunity during early experimental leishmaniasis. PLoS Pathog. 6: e1000871.
62. La Flamme, A. C., and E. J. Pearce. 1999. The absence of IL-6 does not affect Th2 cell development in vivo, but does lead to impaired proliferation, IL-2 receptor expression, and B cell responses. J. Immunol. 162: 5829-5837. (Pubitemid 29314935)
63. Nickerson, P., W. Steurer, J. Steiger, X. Zheng, A. W. Steele, and T. B. Strom. 1994. Cytokines and the Th1/Th2 paradigm in transplantation. Curr. Opin. Immunol. 6: 757-764. (Pubitemid 24312145)
64. Dallman, M. J. 1995. Cytokines and transplantation: Th1/Th2 regulation of the immune response to solid organ transplants in the adult. Curr. Opin. Immunol. 7: 632-638.
65. Waaga, A. M., M. Gasser, J. E. Kist-van Holthe, N. Najafian, A. Müller, J. P. Vella, K. L. Womer, A. Chandraker, S. J. Khoury, and M. H. Sayegh. 2001. Regulatory functions of self-restricted MHC class II allopeptide-specific Th2 clones in vivo. J. Clin. Invest. 107: 909-916. (Pubitemid 32274044)
66. Black, S. M., M. E. Schott, B. H. Batdorf, B. A. Benson, M. S. Rutherford, B. K. Levay-Young, and A. P. Dalmasso. 2010. IL-4 induces protection of vascular endothelial cells against killing by complement and melittin through lipid biosynthesis. Eur. J. Immunol. 40: 803-812.
67. Grehan, J. F., B. K. Levay-Young, J. L. Fogelson, V. François- Bongarçon, B. A. Benson, and A. P. Dalmasso. 2005. IL-4 and IL-13 induce protection of porcine endothelial cells from killing by human complement and from apoptosis through activation of a phosphatidylinositide 3-kinase/Akt pathway. J. Immunol. 175: 1903-1910. (Pubitemid 41023097)
68. + T cell-mediated suppression by dendritic cells. Science 299: 1033-1036.
69. Pasare, C., and R. Medzhitov. 2004. Toll-dependent control mechanisms of CD4 T cell activation. Immunity 21: 733-741. (Pubitemid 39487894)
70. Yang, Y., C. T. Huang, X. Huang, and D. M. Pardoll. 2004. Persistent Toll-like receptor signals are required for reversal of regulatory T cell-mediated CD8 tolerance. Nat. Immunol. 5: 508-515. (Pubitemid 38660463)