Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2015, Article ID 631384, 12 pages
http://dx.doi.org/10.1155/2015/631384
Research Article

IL-1 Receptor Blockade Alleviates Graft-versus-Host Disease through Downregulation of an Interleukin-1-Dependent Glycolytic Pathway in Th17 Cells

1The Rheumatism Research Center, Catholic Research Institute of Medical Sciences, The Catholic University of Korea, Seoul, Republic of Korea
2Division of Hepatology, Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of Korea, 505 Banpo-Dong, Seocho-Ku, Seoul 137-040, Republic of Korea
3Division of Rheumatology, Department of Internal Medicine, The Catholic University of Korea, Seoul 137-040, Republic of Korea

Received 30 July 2015; Revised 27 October 2015; Accepted 4 November 2015

Academic Editor: Mirella Giovarelli

Copyright © 2015 Min-Jung Park et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Gabay, C. Lamacchia, and G. Palmer, “IL-1 pathways in inflammation and human diseases,” Nature Reviews Rheumatology, vol. 6, no. 4, pp. 232–241, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. E. V. Acosta-Rodriguez, G. Napolitani, A. Lanzavecchia, and F. Sallusto, “Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells,” Nature Immunology, vol. 8, no. 9, pp. 942–949, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. C. A. Dinarello, “Interleukin-1 in the pathogenesis and treatment of inflammatory diseases,” Blood, vol. 117, no. 14, pp. 3720–3732, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. I. Ben-Shlomo, S. Kol, L. M. Roeder et al., “Interleukin (IL)-1β increases glucose uptake and induces glycolysis in aerobically cultured rat ovarian cells: evidence that IL-1β may mediate the gonadotropin-induced midcycle metabolic shift,” Endocrinology, vol. 138, no. 7, pp. 2680–2688, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. D. J. Taylor, E. B. Faragher, and J. M. Evanson, “Inflammatory cytokines stimulate glucose uptake and glycolysis but reduce glucose oxidation in human dermal fibroblasts in vitro,” Circulatory Shock, vol. 37, no. 2, pp. 105–110, 1992. View at Google Scholar · View at Scopus
  6. R. Korngold and J. Sprent, “Lethal graft-versus-host disease after bone marrow transplantation across minor histocompatibility barriers in mice. Prevention by removing mature T cells from marrow,” Journal of Experimental Medicine, vol. 148, no. 6, pp. 1687–1698, 1978. View at Publisher · View at Google Scholar · View at Scopus
  7. F. Malard, C. Bossard, E. Brissot et al., “Increased Th17/Treg ratio in chronic liver GVHD,” Bone Marrow Transplantation, vol. 49, no. 4, pp. 539–544, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Ruggeri, M. Capanni, E. Urbani et al., “Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants,” Science, vol. 295, no. 5562, pp. 2097–2100, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. W. D. Shlomchik, M. S. Couzens, C. B. Tang et al., “Prevention of graft versus host disease by inactivation of host antigen-presenting cells,” Science, vol. 285, no. 5426, pp. 412–415, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. T. Teshima, P. Reddy, K. P. Lowler et al., “Flt3 ligand therapy for recipients of allogeneic bone marrow transplants expands host CD8α+ dendritic cells and reduces experimental acute graft-versus-host disease,” Blood, vol. 99, no. 5, pp. 1825–1832, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Cooke, “Th17 cells in inflammatory conditions,” The Review of Diabetic Studies, vol. 3, no. 2, pp. 72–75, 2006. View at Publisher · View at Google Scholar
  12. M. S. Maddur, P. Miossec, S. V. Kaveri, and J. Bayry, “Th17 cells: biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies,” The American Journal of Pathology, vol. 181, no. 1, pp. 8–18, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Z. Shi, R. Wang, G. Huang et al., “HIF1α-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells,” The Journal of Experimental Medicine, vol. 208, no. 7, pp. 1367–1376, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. E. V. Dang, J. Barbi, H.-Y. Yang et al., “Control of TH17/Treg balance by hypoxia-inducible factor 1,” Cell, vol. 146, no. 5, pp. 772–784, 2011. View at Publisher · View at Google Scholar
  15. C. A. Dinarello, A. Simon, and J. W. M. van der Meer, “Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases,” Nature Reviews Drug Discovery, vol. 11, no. 8, pp. 633–652, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. C. A. Dinarello, “Blocking IL-1 in systemic inflammation,” The Journal of Experimental Medicine, vol. 201, no. 9, pp. 1355–1359, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Goldbach-Mansky, “Blocking interleukin-1 in rheumatic diseases: its initial disappointments and recent successes in the treatment of autoinflammatory diseases,” Annals of the New York Academy of Sciences, vol. 1182, pp. 111–123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. J. H. Antin, D. Weisdorf, D. Neuberg et al., “Interleukin-1 blockade does not prevent acute graft-versus-host disease: results of a randomized, double-blind, placebo-controlled trial of interleukin-1 receptor antagonist in allogeneic bone marrow transplantation,” Blood, vol. 100, no. 10, pp. 3479–3482, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. P. L. McCarthy Jr., S. Abhyankar, S. Neben et al., “Inhibition of interleukin-1 by an interleukin-1 receptor antagonist prevents graft-versus-host disease,” Blood, vol. 78, no. 8, pp. 1915–1918, 1991. View at Google Scholar · View at Scopus
  20. J. Fukui, M. Inaba, Y. Ueda et al., “Prevention of graft-versus-host disease by intra-bone marrow injection of donor T cells,” STEM CELLS, vol. 25, no. 6, pp. 1595–1601, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. I. Devic, M. Shi, M. M. Schubert et al., “Proteomic analysis of saliva from patients with oral chronic graft-versus-host disease,” Biology of Blood and Marrow Transplantation, vol. 20, no. 7, pp. 1048–1055, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Jankovic, J. Ganesan, M. Bscheider et al., “The Nlrp3 inflammasome regulates acute graft-versus-host disease,” The Journal of Experimental Medicine, vol. 210, no. 10, pp. 1899–1910, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Liang, S. Ma, Y. Zhang et al., “IL-1β and TLR4 signaling are involved in the aggravated murine acute graft-versus-host disease caused by delayed bortezomib administration,” Journal of Immunology, vol. 192, no. 3, pp. 1277–1285, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Zhu, H. Yamane, and W. E. Paul, “Differentiation of effector CD4 T cell populations,” Annual Review of Immunology, vol. 28, pp. 445–489, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Ratajczak, A. Janin, R. P. De Latour et al., “Th17/Treg ratio in human graft-versus-host disease,” Blood, vol. 116, no. 7, pp. 1165–1171, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Yen, J. Cheung, H. Scheerens et al., “IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6,” The Journal of Clinical Investigation, vol. 116, no. 5, pp. 1310–1316, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. J. S. Serody and G. R. Hill, “The IL-17 differentiation pathway and its role in transplant outcome,” Biology of Blood and Marrow Transplantation, vol. 18, supplement 1, pp. S56–S61, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Weiss, N. Haeffner-Cavaillon, M. Laude, J.-M. Cavaillon, and M. D. Kazatchkine, “Human T cells and interleukin 4 inhibit the release of interleukin 1 induced by lipopolysaccharide in serum-free cultures of autologous monocytes,” European Journal of Immunology, vol. 19, no. 7, pp. 1347–1350, 1989. View at Publisher · View at Google Scholar · View at Scopus
  29. E. Vannier, L. C. Miller, and C. A. Dinarello, “Coordinated antiinflammatory effects of interleukin 4: interleukin 4 suppresses interleukin 1 production but up-regulates gene expression and synthesis of interleukin 1 receptor antagonist,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 9, pp. 4076–4080, 1992. View at Publisher · View at Google Scholar · View at Scopus
  30. V. Ratanatharathorn, R. A. Nash, D. Przepiorka et al., “Phase III study comparing methotrexate and tacrolimus (prograf, FK506) with methotrexate and cyclosporine for graft-versus-host disease prophylaxis after HLA-identical sibling bone marrow transplantation,” Blood, vol. 92, no. 7, pp. 2303–2314, 1998. View at Google Scholar · View at Scopus
  31. D. A. Jacobsohn, J. Margolis, J. Doherty, V. Anders, and G. B. Vogelsang, “Weight loss and malnutrition in patients with chronic graft-versus-host disease,” Bone Marrow Transplantation, vol. 29, no. 3, pp. 231–236, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Pintar, R. Zorc-Pleskovič, M. Alessiani, A. Milutinović, and A. Pleskovič, “Prognostic value of skin histology in GVHD after intestinal transplantation,” European Journal of Pediatric Surgery, vol. 17, no. 6, pp. 412–415, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Socié and B. R. Blazar, “Acute graft-versus-host disease: from the bench to the bedside,” Blood, vol. 114, no. 20, pp. 4327–4336, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. E. Gatza, D. R. Wahl, A. W. Opipari et al., “Manipulating the bioenergetics of alloreactive T cells causes their selective apoptosis and arrests graft-versus-host disease,” Science Translational Medicine, vol. 3, no. 67, Article ID 67ra8, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. C. J. Fox, P. S. Hammerman, and C. B. Thompson, “Fuel feeds function: energy metabolism and the T-cell response,” Nature Reviews Immunology, vol. 5, no. 11, pp. 844–852, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. M. G. V. Heiden, L. C. Cantley, and C. B. Thompson, “Understanding the warburg effect: the metabolic requirements of cell proliferation,” Science, vol. 324, no. 5930, pp. 1029–1033, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. K. A. Frauwirth, J. L. Riley, M. H. Harris et al., “The CD28 signaling pathway regulates glucose metabolism,” Immunity, vol. 16, no. 6, pp. 769–777, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. N. J. Maciver, S. R. Jacobs, H. L. Wieman, J. A. Wofford, J. L. Coloff, and J. C. Rathmell, “Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival,” Journal of Leukocyte Biology, vol. 84, no. 4, pp. 949–957, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. L. V. Sinclair, J. Rolf, E. Emslie, Y.-B. Shi, P. M. Taylor, and D. A. Cantrell, “Control of amino-acid transport by antigen receptors coordinates the metabolic reprogramming essential for T cell differentiation,” Nature Immunology, vol. 14, no. 5, pp. 500–508, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Wang, C. P. Dillon, L. Z. Shi et al., “The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation,” Immunity, vol. 35, no. 6, pp. 871–882, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. R. D. Michalek, V. A. Gerriets, S. R. Jacobs et al., “Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets,” Journal of Immunology, vol. 186, no. 6, pp. 3299–3303, 2011. View at Publisher · View at Google Scholar · View at Scopus