IL-1α and IL-1β are endogenous mediators linking cell injury to the adaptive alloimmune response

Journal of Immunology

Volumn 179, Issue 10, 2007, Pages 6536-6546

  Rao, Deepak A ^a   Tracey, Kevin J ^b   Pober, Jordan S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; HLA DR ANTIGEN; INTERLEUKIN 1; INTERLEUKIN 1BETA; CD14 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; RECOMBINANT PROTEIN; TLR4 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ALLOIMMUNITY; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOTHELIUM CELL; GRAFT FAILURE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOADSORPTION; PRIORITY JOURNAL; ALLOTRANSPLANTATION; ARTERIOSCLEROSIS; CD4+ T LYMPHOCYTE; DRUG EFFECT; GRAFT REJECTION; IMMUNOLOGY; ISCHEMIA; LYMPHOCYTE ACTIVATION; MONOCYTE; ORGAN TRANSPLANTATION; PATHOLOGY;

ANTIGENS, CD14; ARTERIOSCLEROSIS; CD4-POSITIVE T-LYMPHOCYTES; ENDOTHELIAL CELLS; GRAFT REJECTION; HMGB1 PROTEIN; HUMANS; INTERFERON TYPE II; INTERLEUKIN-17; INTERLEUKIN-1ALPHA; INTERLEUKIN-1BETA; ISCHEMIA; LYMPHOCYTE ACTIVATION; MONOCYTES; ORGAN TRANSPLANTATION; RECEPTORS, INTERLEUKIN-1; RECOMBINANT PROTEINS; TOLL-LIKE RECEPTOR 4; TRANSPLANTATION, HOMOLOGOUS;

EID: 38449101266     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.10.6536     Document Type: Article

References (84)

1. Libby, P., and J. S. Pober. 2001. Chronic rejection. Immunity 14: 387-397.
2. Tullius, S. G., and N. L. Tilney. 1995. Both alloantigen-dependent and -independent factors influence chronic allograft rejection. Transplantation 59: 313-318.
3. Choi, J., D. R. Enis, K. P. Koh, S. L. Shiao, and J. S. Pober. 2004. T lymphocyte-endothelial cell interactions. Annu. Rev. Immunol. 22: 683-709.
4. + T cell-mediated cardiac allograft rejection. J. Immunol. 167: 5457-5463.
5. Nagano, H., R. N. Mitchell, M. K. Taylor, S. Hasegawa, N. L. Tilney, and P. Libby. 1997. Interferon-γ deficiency prevents coronary arteriosclerosis but not myocardial rejection in transplanted mouse hearts. J. Clin. Invest. 100: 550-557.
6. Tellides, G., D. A. Tereb, N. C. Kirkiles-Smith, R. W. Kim, J. H. Wilson, J. S. Schechner, M. I. Lorber, and J. S. Pober. 2000. Interferon-γ elicits arteriosclerosis in the absence of leukocytes. Nature 403: 207-211.
7. Wang, Y., W. R. Burns, P. C. Tang, T. Yi, J. S. Schechner, H. G. Zerwes, W. C. Sessa, M. I. Lorber, J. S. Pober, and G. Tellides. 2004. Interferon-γ plays a nonredundant role in mediating T cell-dependent outward vascular remodeling of allogeneic human coronary arteries. FASEB J. 18: 606-608.
8. Antonysamy, M. A., W. C. Fanslow, F. Fu, W. Li, S. Qian, A. B. Troutt, and A. W. Thomson. 1999. Evidence for a role of IL-17 in organ allograft rejection: IL-17 promotes the functional differentiation of dendritic cell progenitors. J. Immunol. 162: 577-584.
9. Tang, J. L., V. M. Subbotin, M. A. Antonysamy, A. B. Troutt, A. S. Rao, and A. W. Thomson. 2001. Interleukin-17 antagonism inhibits acute but not chronic vascular rejection. Transplantation 72: 348-350.
10. Terasaki, P. I., J. M. Cecka, D. W. Gjertson, and S. Takemoto. 1995. High survival rates of kidney transplants from spousal and living unrelated donors. N. Engl. J. Med. 333: 333-336.
11. Salahudeen, A. K., N. Haider, and W. May. 2004. Cold ischemia and the reduced long-term survival of cadaveric renal allografts. Kidney Int. 65: 713-718.
12. Perico, N., D. Cattaneo, M. H. Sayegh, and G. Remuzzi. 2004. Delayed graft function in kidney transplantation. Lancet 364: 1814-1827.
13. Weis, M., and W. von Scheidt. 1997. Cardiac allograft vasculopathy: a review. Circulation 96: 2069-2077.
14. Lietz, K., and L. W. Miller. 2004. Current understanding and management of allograft vasculopathy. Semin Thorac Cardiovasc Surg. 16: 386-394.
15. Halloran, P. F., J. Homik, N. Goes, S. L. Lui, J. Urmson, V. Ramassar, and S. M. Cockfield. 1997. The "injury response": a concept linking nonspecific injury, acute rejection, and long-term transplant outcomes. Transplant Proc. 29: 79-81.
16. Chalasani, G., Q. Li, B. T. Konieczny, L. Smith-Diggs, B. Wrobel, Z. Dai, D. L. Perkins, F. K. Baddoura, and F. G. Lakkis. 2004. The allograft defines the type of rejection (acute versus chronic) in the face of an established effector immune response. J. Immunol. 172: 7813-7820.
17. Dinarello, C. A. 1996. Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147.
18. Tesar, B. M., D. Jiang, J. Liang, S. M. Palmer, P. W. Noble, and D. R. Goldstein. 2006. The role of hyaluronan degradation products as innate alloimmune agonists. Am. J. Transplant. 6: 2622-2635.
19. Andrade, C. F., T. K. Waddell, S. Keshavjee, and M. Liu. 2005. Innate immunity and organ transplantation: the potential role of toll-like receptors. Am. J. Transplant. 5: 969-975.
20. Rock, K. L., A. Hearn, C. J. Chen, and Y. Shi. 2005. Natural endogenous adjuvants. Springer Semin. Immunopathol. 26: 231-246.
21. Zeh, H. J., III, and M. T. Lotze. 2005. Addicted to death: invasive cancer and the immune response to unscheduled cell death. J. Immunother. 28: 1-9.
22. Shi, Y., J. E. Evans, and K. L. Rock. 2003. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425: 516-521.
23. Rifkin, I. R., E. A. Leadbetter, L. Busconi, G. Viglianti, and A. Marshak-Rothstein. 2005. Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol. Rev. 204: 27-42.
24. Land, W. G. 2005. The role of postischemic reperfusion injury and other non-antigen-dependent inflammatory pathways in transplantation. Transplantation 79: 505-514.
25. Chen, C. J., H. Kono, D. Golenbock, G. Reed, S. Akira, and K. L. Rock. 2007. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat. Med. 13: 851-856.
26. Chen, C. J., Y. Shi, A. Hearn, K. Fitzgerald, D. Golenbock, G. Reed, S. Akira, and K. L. Rock. 2006. MyD88-dependent IL-1 receptor signaling is essential for gouty inflammation stimulated by monosodium urate crystals. J. Clin. Invest. 116: 2262-2271.
27. Scaffidi, P., T. Misteli, and M. E. Bianchi. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
28. Dumitriu, I. E., P. Baruah, A. A. Manfredi, M. E. Bianchi, and P. Rovere-Querini. 2005. HMGB1: guiding immunity from within. Trends Immunol. 26: 381-387.
29. Andersson, U., H. Wang, K. Palmblad, A. C. Aveberger, O. Bloom, H. Erlandsson-Harris, A. Janson, R. Kokkola, M. Zhang, H. Yang, and K. J. Tracey. 2000. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J. Exp. Med. 192: 565-570.
30. Park, J. S., J. Arcaroli, H. K. Yum, H. Yang, H. Wang, K. Y. Yang, K. H. Choe, D. Strassheim, T. M. Pitts, K. J. Tracey, and E. Abraham. 2003. Activation of gene expression in human neutrophils by high mobility group box 1 protein. Am. J. Physiol. 284: C870-C879.
31. Messmer, D., H. Yang, G. Telusma, F. Knoll, J. Li, B. Messmer, K. J. Tracey, and N. Chiorazzi. 2004. High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J. Immunol. 173: 307-313.
32. Yu, M., H. Wang, A. Ding, D. T. Golenbock, E. Latz, C. J. Czura, M. J. Fenton, K. J. Tracey, and H. Yang. 2006. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 26: 174-179.
33. Dumitriu, I. E., P. Baruah, B. Valentinis, R. E. Voll, M. Herrmann, P. P. Nawroth, B. Arnold, M. E. Bianchi, A. A. Manfredi, and P. Rovere-Querini. 2005. Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J. Immunol. 174: 7506-7515.
34. Huang, Y., H. Yin, J. Han, B. Huang, J. Xu, F. Zheng, Z. Tan, M. Fang, L. Rui, D. Chen, et al. 2007. Extracellular hmgb1 functions as an innate immune-mediator implicated in murine cardiac allograft acute rejection. Am. J. Transplant. 7: 799-808.
35. Kurt-Jones, E. A., W. Fiers, and J. S. Pober. 1987. Membrane interleukin 1 induction on human endothelial cells and dermal fibroblasts. J. Immunol. 139: 2317-2324.
36. Libby, P., J. M. Ordovas, K. R. Auger, A. H. Robbins, L. K. Birinyi, and C. A. Dinarello. 1986. Endotoxin and tumor necrosis factor induce interleukin-1 gene expression in adult human vascular endothelial cells. Am. J. Pathol. 124: 179-185.
37. Libby, P., J. M. Ordovas, L. K. Birinyi, K. R. Auger, and C. A. Dinarello. 1986. Inducible interleukin-1 gene expression in human vascular smooth muscle cells. J. Clin. Invest. 78: 1432-1438.
38. Mosley, B., D. L. Urdal, K. S. Prickett, A. Larsen, D. Cosman, P. J. Conlon, S. Gillis, and S. K. Dower. 1987. The interleukin-1 receptor binds the human interleukin-1 alpha precursor but not the interleukin-1β precursor. J. Biol. Chem. 262: 2941-2944.
39. Loppnow, H., and P. Libby. 1992. Functional significance of human vascular smooth muscle cell-derived interleukin 1 in paracrine and autocrine regulation pathways. Exp. Cell Res. 198: 283-290.
40. Kurt-Jones, E. A., S. Hamberg, J. Ohara, W. E. Paul, and A. K. Abbas. 1987. Heterogeneity of helper/inducer T lymphocytes. I. Lymphokine production and lymphokine responsiveness. J. Exp. Med. 166: 1774-1787.
41. + T cells. Eur. J. Immunol. 22: 95-100.
42. Lichtman, A. H., J. Chin, J. A. Schmidt, and A. K. Abbas. 1988. Role of interleukin 1 in the activation of T lymphocytes. Proc. Natl. Acad. Sci. USA 85: 9699-9703.
43. + effector T cells. J. Immunol. 176: 7278-7287.
44. Sutton, C., C. Brereton, B. Keogh, K. H. Mills, and E. C. Lavelle. 2006. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J. Exp. Med. 203: 1685-1691.
45. 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.
46. Acosta-Rodriguez, E. V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8: 942-949.
47. Li, J., H. Wang, J. M. Mason, J. Levine, M. Yu, L. Ulloa, C. J. Czura, K. J. Tracey, and H. Yang. 2004. Recombinant HMGB1 with cytokine-stimulating activity. J. Immunol. Methods 289: 211-223.
48. Pober, J. S., M. P. Bevilacqua, D. L. Mendrick, L. A. Lapierre, W. Fiers, and M. A. Gimbrone, Jr. 1986. Two distinct monokines, interleukin 1 and tumor necrosis factor, each independently induce biosynthesis and transient expression of the same antigen on the surface of cultured human vascular endothelial cells. J. Immunol. 136: 1680-1687.
49. + T cells. J. Immunol. 178: 3237-3243.
50. Mahboubi, K., and J. S. Pober. 2002. Activation of signal transducer and activator of transcription 1 (STAT1) is not sufficient for the induction of STAT1-dependent genes in endothelial cells: comparison of interferon-θ and oncostatin M. J. Biol. Chem. 277: 8012-8021.
51. Mahboubi, K., N. C. Kirkiles-Smith, J. Karras, and J. S. Pober. 2003. Desensitization of signaling by oncostatin M in human vascular cells involves cytoplasmic Tyr residue 759 in gp130 but is not mediated by either Src homology 2 domain-containing tyrosine phosphatase 2 or suppressor of cytokine signaling 3. J. Biol. Chem. 278: 25014-25023.
52. Valantine, H. A. 2003. Cardiac allograft vasculopathy: central role of endothelial injury leading to transplant "atheroma". Transplantation 76: 891-899.
53. Fiuza, C., M. Bustin, S. Talwar, M. Tropea, E. Gerstenberger, J. H. Shelhamer, and A. F. Suffredini. 2003. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 101: 2652-2660.
54. Treutiger, C. J., G. E. Mullins, A. S. Johansson, A. Rouhiainen, H. M. Rauvala, H. Erlandsson-Harris, U. Andersson, H. Yang, K. J. Tracey, J. Andersson, and J. E. Palmblad. 2003. High mobility group 1 B-box mediates activation of human endothelium. J. Intern. Med. 254: 375-385.
55. Wautier, J. L., and A. M. Schmidt. 2004. Protein glycation: a firm link to endothelial cell dysfunction. Circ. Res. 95: 233-238.
56. Dauphinee, S. M., and A. Karsan. 2006. Lipopolysaccharide signaling in endothelial cells. Lab. Invest. 86: 9-22.
57. Xu, H., K. K. Dhanireddy, and A. D. Kirk. 2006. Human monocytes as intermediaries between allogeneic endothelial cells and allospecific T cells: a role for direct scavenger receptor-mediated endothelial membrane uptake in the initiation of alloimmunity. J. Immunol. 176: 750-761.
58. Dong, C. 2006. Diversification of T-helper-cell lineages: finding the family root of IL-17-producing cells. Nat. Rev. Immunol. 6: 329-333.
59. Acosta-Rodriguez, E. V., L. Rivino, J. Geginat, D. Jarrossay, M. Gattorno, A. Lanzavecchia, F. Sallusto, and G. Napolitani. 2007. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8: 639-646.
60. + allogeneic vascular endothelium: identification of accessory interactions. Transplantation 56: 128-134.
61. + direct allorecognition in graft rejection. J. Immunol. 173: 3027-3034.
62. Shiao, S. L., J. M. McNiff, and J. S. Pober. 2005. Memory T cells and their costimulators in human allograft injury. J. Immunol. 175: 4886-4896.
63. Lombardi, G., S. Sidhu, M. Daly, J. R. Batchelor, W. Makgoba, and R. I. Lechler. 1990. Are primary alloresponses truly primary? Int. Immunol. 2: 9-13.
64. Valujskikh, A. 2006. The challenge of inhibiting alloreactive T-cell memory. Am. J. Transplant 6: 647-651.
65. Durum, S. K., J. A. Schmidt, and J. J. Oppenheim. 1985. Interleukin 1: an immunological perspective. Annu. Rev. Immunol. 3: 263-287.
66. Staruch, M. J., and D. D. Wood. 1983. The adjuvanticity of interleukin 1 in vivo. J. Immunol. 130: 2191-2194.
67. + T cell help for induction of in vivo type 1 and type 2 antipolysaccharide and antiprotein Ig isotype responses to intact Streptococcus pneumoniae, but not to a soluble pneumococcal conjugate vaccine. J. Immunol. 177: 6044-6051.
68. Tominaga, K., T. Yoshimoto, K. Torigoe, M. Kurimoto, K. Matsui, T. Hada, H. Okamura, and K. Nakanishi. 2000. IL-12 synergizes with IL-18 or IL-1β for IFN-γ production from human T cells. Int. Immunol. 12: 151-160.
69. Cooper, A. L., and D. Beasley. 1999. Hypoxia stimulates proliferation and interleukin-1alpha production in human vascular smooth muscle cells. Am. J. Physiol. 277: H1326-H1337.
70. Shreeniwas, R., S. Koga, M. Karakurum, D. Pinsky, E. Kaiser, J. Brett, B. A. Wolitzky, C. Norton, J. Plocinski, W. Benjamin, et al. 1992. Hypoxia-mediated induction of endothelial cell interleukin-1 alpha: an autocrine mechanism promoting expression of leukocyte adhesion molecules on the vessel surface. J. Clin. Invest. 90: 2333-2339.
71. Saadi, S., R. A. Holzknecht, C. P. Patte, D. M. Stern, and J. L. Platt. 1995. Complement-mediated regulation of tissue factor activity in endothelium. J. Exp. Med. 182: 1807-1814.
72. Saadi, S., R. A. Holzknecht, C. P. Patte, and J. L. Platt. 2000. Endothelial cell activation by pore-forming structures: pivotal role for interleukin-1α. Circulation 101: 1867-1873.
73. Hamilton, K. K., R. Hattori, C. T. Esmon, and P. J. Sims. 1990. Complement proteins C5b-9 induce vesiculation of the endothelial plasma membrane and expose catalytic surface for assembly of the prothrombinase enzyme complex. J. Biol. Chem. 265: 3809-3814.
74. Thomas, J. O., and A. A. Travers. 2001. HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem. Sci. 26: 167-174.
75. Werman, A., R. Werman-Venkert, R. White, J. K. Lee, B. Werman, Y. Krelin, E. Voronov, C. A. Dinarello, and R. N. Apte. 2004. The precursor form of IL-1α is an intracrine proinflammatory activator of transcription. Proc. Natl. Acad. Sci. USA 101: 2434-2439.
76. Watson, C. A., L. Camera-Benson, R. Palmer-Crocker, and J. S. Pober. 1995. Variability among human umbilical vein endothelial cultures. Science 268: 447-448.
77. Taniguchi, N., K. Kawahara, K. Yone, T. Hashiguchi, M. Yamakuchi, M. Goto, K. Inoue, S. Yamada, K. Ijiri, S. Matsunaga, et al. 2003. High mobility group box chromosomal protein 1 plays a role in the pathogenesis of rheumatoid arthritis as a novel cytokine. Arthritis Rheum. 48: 971-981.
78. Park, J. S., F. Gamboni-Robertson, Q. He, D. Svetkauskaite, J. Y. Kim, D. Strassheim, J. W. Sohn, S. Yamada, I. Maruyama, A. Banerjee, et al. 2006. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am. J. Physiol. 290: C917-C924.
79. Tsung, A., R. Sahai, H. Tanaka, A. Nakao, M. P. Fink, M. T. Lotze, H. Yang, J. Li, K. J. Tracey, D. A. Geller, and T. R. Billiar. 2005. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J. Exp. Med. 201: 1135-1143.
80. Gao, B., Y. Wang, and M. F. Tsan. 2006. The heat sensitivity of cytokine-inducing effect of lipopolysaccharide. J. Leukocyte Biol. 80: 359-366.
81. Mariathasan, S., D. S. Weiss, K. Newton, J. McBride, K. O'Rourke, M. Roose-Girma, W. P. Lee, Y. Weinrauch, D. M. Monack, and V. M. Dixit. 2006. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232.
82. Martinon, F., V. Petrilli, A. Mayor, A. Tardivel, and J. Tschopp. 2006. Goutassociated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241.
83. H2 lymphocytes. Nat. Immunol. 4: 78-86.
84. Jirik, F. R., T. J. Podor, T. Hirano, T. Kishimoto, D. J. Loskutoff, D. A. Carson, and M. Lotz. 1989. Bacterial lipopolysaccharide and inflammatory mediators augment IL-6 secretion by human endothelial cells. J. Immunol. 142: 144-147.