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Mediators of Inflammation
Volume 2012, Article ID 315941, 10 pages
http://dx.doi.org/10.1155/2012/315941
Review Article

Danger Signals Activating the Immune Response after Trauma

Division of Trauma Surgery, Department of Surgery, University Hospital Zurich, 8091 Zurich, Switzerland

Received 8 January 2012; Revised 23 March 2012; Accepted 26 March 2012

Academic Editor: Mohamed Lamkanfi

Copyright © 2012 Stefanie Hirsiger 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. D. E. Fry, L. Pearlstein, R. L. Fulton, and H. C. Polk Jr., “Multiple system organ failure. The role of uncontrolled infection,” Archives of Surgery, vol. 115, no. 2, pp. 136–140, 1980. View at Google Scholar · View at Scopus
  2. G. A. Wanner, M. Keel, U. Steckholzer, W. Beier, R. Stocker, and W. Ertel, “Relationship between procalcitonin plasma levels and severity of injury, sepsis, organ failure, and mortality in injured patients,” Critical Care Medicine, vol. 28, no. 4, pp. 950–957, 2000. View at Google Scholar · View at Scopus
  3. H. C. Pape, T. Tsukamoto, P. Kobbe, I. Tarkin, S. Katsoulis, and A. Peitzman, “Assessment of the clinical course with inflammatory parameters,” Injury, vol. 38, no. 12, pp. 1358–1364, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Matzinger, “Tolerance, danger, and the extended family,” Annual Review of Immunology, vol. 12, pp. 991–1045, 1994. View at Google Scholar · View at Scopus
  5. P. F. Hwang, N. Porterfield, D. Pannell, T. A. Davis, and E. A. Elster, “Trauma is danger,” Journal of Translational Medicine, vol. 9, no. 1, article 92, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. M. E. Bianchi, “DAMPs, PAMPs and alarmins: all we need to know about danger,” Journal of Leukocyte Biology, vol. 81, no. 1, pp. 1–5, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. H. E. Harris and A. Raucci, “Alarmin(g) news about danger: workshop on innate danger signals and HMGB1,” EMBO Reports, vol. 7, no. 8, pp. 774–778, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. A. D. Garg, D. V. Krysko, T. Verfaillie, A. Kaczmarek, and G. B. Ferreira, “A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death,” The EMBO Journal, vol. 31, pp. 1062–1079, 2012. View at Google Scholar
  9. T. Panaretakis, O. Kepp, U. Brockmeier et al., “Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death,” EMBO Journal, vol. 28, no. 5, pp. 578–590, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Obeid, A. Tesniere, F. Ghiringhelli et al., “Calreticulin exposure dictates the immunogenicity of cancer cell death,” Nature Medicine, vol. 13, no. 1, pp. 54–61, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. C. A. Janeway Jr. and R. Medzhitov, “Innate immune recognition,” Annual Review of Immunology, vol. 20, pp. 197–216, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Aderem and R. J. Ulevitch, “Toll-like receptors in the induction of the innate immune response,” Nature, vol. 406, no. 6797, pp. 782–787, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. A. P. West, G. S. Shadel, and S. Ghosh, “Mitochondria in innate immune responses,” Nature Reviews Immunology, vol. 11, no. 6, pp. 389–402, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. P. Matzinger, “An innate sense of danger,” Seminars in Immunology, vol. 10, no. 5, pp. 399–415, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Y. Seong and P. Matzinger, “Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses,” Nature Reviews Immunology, vol. 4, no. 6, pp. 469–478, 2004. View at Google Scholar · View at Scopus
  16. S. Muller, P. Scaffidi, B. Degryse, T. Bonaldi, and L. Ronfani, “New EMBO members' review: the double life of HMGB1 chromatin protein: architectural factor and extracellular signal,” The EMBO Journal, vol. 20, pp. 4337–4340, 2001. View at Google Scholar
  17. H. Wang, O. Bloom, M. Zhang et al., “HMG-1 as a late mediator of endotoxin lethality in mice,” Science, vol. 285, no. 5425, pp. 248–251, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Tsung, R. Sahai, H. Tanaka et al., “The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion,” Journal of Experimental Medicine, vol. 201, no. 7, pp. 1135–1143, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. M. T. Lotze and K. J. Tracey, “High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal,” Nature Reviews Immunology, vol. 5, no. 4, pp. 331–342, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Rittirsch, M. A. Flierl, B. A. Nadeau et al., “Functional roles for C5a receptors in sepsis,” Nature Medicine, vol. 14, no. 5, pp. 551–557, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. M. J. Cohen, K. Brohi, C. S. Calfee et al., “Early release of high mobility group box nuclear protein 1 after severe trauma in humans: role of injury severity and tissue hypoperfusion,” Critical Care, vol. 13, no. 6, article R174, 2009. View at Google Scholar · View at Scopus
  22. H. Wang, H. Liao, M. Ochani et al., “Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis,” Nature Medicine, vol. 10, no. 11, pp. 1216–1221, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. J. M. Huston, H. Wang, M. Ochani et al., “Splenectomy protects against sepsis lethality and reduces serum HMGB1 levels,” Journal of Immunology, vol. 181, no. 5, pp. 3535–3539, 2008. View at Google Scholar · View at Scopus
  24. M. Rosas-Ballina, M. Ochani, W. R. Parrish et al., “Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 31, pp. 11008–11013, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. H. E. Harris, U. Andersson, and D. S. Pisetsky, “HMGB1: a multifunctional alarmin driving autoimmune and inflammatory disease,” Nature Reviews Rheumatology, vol. 8, no. 4, pp. 195–202, 2012. View at Google Scholar
  26. I. Ito, J. Fukazawa, and M. Yoshida, “Post-translational methylation of high mobility group box 1 (HMGB1) causes its cytoplasmic localization in neutrophils,” Journal of Biological Chemistry, vol. 282, no. 22, pp. 16336–16344, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. J. Oh, J. H. Youn, Y. Ji et al., “HMGB1 is phosphorylated by classical protein kinase C and is secreted by a calcium-dependent mechanism,” Journal of Immunology, vol. 182, no. 9, pp. 5800–5809, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Yang, P. Lundback, L. Ottosson, H. Erlandsson-Harris, and E. Venereau, “Redox modification of cysteine residues regulates the cytokine activity of HMGB1,” Molecular Medicine, vol. 18, no. 3, pp. 250–259, 2012. View at Google Scholar
  29. A. Castiglioni, V. Canti, P. Rovere-Querini, and A. A. Manfredi, “High-mobility group box 1 (HMGB1) as a master regulator of innate immunity,” Cell and Tissue Research, vol. 343, no. 1, pp. 189–199, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Tang, R. Kang, H. J. Zeh III, and M. T. Lotze, “High-mobility group box 1, oxidative stress, and disease,” Antioxidants and Redox Signaling, vol. 14, no. 7, pp. 1315–1335, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Carta, P. Castellani, L. Delfino, S. Tassi, R. Venè, and A. Rubartelli, “DAMPs and inflammatory processes: the role of redox in the different outcomes,” Journal of Leukocyte Biology, vol. 86, no. 3, pp. 549–555, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Wang, H. Yang, and K. J. Tracey, “Extracellular role of HMGB1 in inflammation and sepsis,” Journal of Internal Medicine, vol. 255, no. 3, pp. 320–331, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. K. J. Tracey, “Understanding immunity requires more than immunology,” Nature Immunology, vol. 11, no. 7, pp. 561–564, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. J. R. Klune, R. Dhupar, J. Cardinal, T. R. Billiar, and A. Tsung, “HMGB1: endogenous danger signaling,” Molecular Medicine, vol. 14, no. 7-8, pp. 476–484, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. E. Abraham, “Unraveling the role of high mobility group box protein 1 in severe trauma,” Critical Care, vol. 13, no. 6, p. 1004, 2009. View at Google Scholar · View at Scopus
  36. Y. Sha, J. Zmijewski, Z. Xu, and E. Abraham, “HMGB1 develops enhanced proinflammatory activity by binding to cytokines,” Journal of Immunology, vol. 180, no. 4, pp. 2531–2537, 2008. View at Google Scholar · View at Scopus
  37. H. S. Hreggvidsdottir, A. M. Lundberg, A. C. Aveberger, L. Klevenvall, and U. Andersson, “HMGB1-partner molecule complexes enhance cytokine production by signaling through the partner molecule receptor,” Molecular Medicine, vol. 18, no. 1, pp. 224–230, 2012. View at Google Scholar
  38. S. P. Jong, F. Gamboni-Robertson, Q. He et al., “High mobility group box 1 protein interacts with multiple Toll-like receptors,” American Journal of Physiology, vol. 290, no. 3, pp. C917–C924, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Yang, H. S. Hreggvidsdottir, K. Palmblad et al., “A critical cysteine is required for HMGB1 binding to toll-like receptor 4 and activation of macrophage cytokine release,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 26, pp. 11942–11947, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Yu, H. Wang, A. Ding et al., “HMGB1 signals through toll-like receptor (TLR) 4 and TLR2,” Shock, vol. 26, no. 2, pp. 174–179, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. O. Hori, J. Brett, T. Slattery et al., “The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of RAGE and amphoterin in the developing nervous system,” Journal of Biological Chemistry, vol. 270, no. 43, pp. 25752–25761, 1995. View at Publisher · View at Google Scholar · View at Scopus
  42. M. A. Hofmann, S. Drury, C. Fu et al., “RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides,” Cell, vol. 97, no. 7, pp. 889–901, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. M. J. Cohen, M. Carles, K. Brohi et al., “Early release of soluble receptor for advanced glycation endproducts after severe trauma in humans,” Journal of Trauma, vol. 68, no. 6, pp. 1273–1278, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Z. Kalea, A. M. Schmidt, and B. I. Hudson, “RAGE: a novel biological and genetic marker for vascular disease,” Clinical Science, vol. 116, no. 8, pp. 621–637, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Abeyama, D. M. Stern, Y. Ito et al., “The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism,” Journal of Clinical Investigation, vol. 115, no. 5, pp. 1267–1274, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Ito, K. Kawahara, T. Nakamura et al., “High-mobility group box 1 protein promotes development of microvascular thrombosis in rats,” Journal of Thrombosis and Haemostasis, vol. 5, no. 1, pp. 109–116, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Yang, M. Ochani, J. Li et al., “Reversing established sepsis with antagonists of endogenous high-mobility group box 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 1, pp. 296–301, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Wang, S. Zhu, R. Zhou, W. Li, and A. E. Sama, “Therapeutic potential of HMGB1-targeting agents in sepsis,” Expert Reviews in Molecular Medicine, vol. 10, article e32, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. E. D. Peltz, E. E. Moore, P. C. Eckels et al., “HMGB1 is markedly elevated within 6 hours of mechanical trauma in humans,” Shock, vol. 32, no. 1, pp. 17–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Sundén-Cullberg, A. Norrby-Teglund, A. Rouhiainen et al., “Persistent elevation of high mobility group box-1 protein (HMGB1) in patients with severe sepsis and septic shock,” Critical Care Medicine, vol. 33, no. 3, pp. 564–573, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. C. A. Dinarello, “Immunological and inflammatory functions of the interleukin-1 family,” Annual Review of Immunology, vol. 27, pp. 519–550, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. C. A. Dinarello, “Interleukin-1 and interleukin-1 antagonism,” Blood, vol. 77, no. 8, pp. 1627–1652, 1991. View at Google Scholar · View at Scopus
  53. C. A. Dinarello, “A clinical perspective of IL-1β as the gatekeeper of inflammation,” European Journal of Immunology, vol. 41, no. 5, pp. 1203–1217, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. J. A. Singh, R. Christensen, G. A. Wells et al., “Biologics for rheumatoid arthritis: an overview of Cochrane reviews,” Cochrane Database of Systematic Reviews, no. 4, Article ID CD007848, 2009. View at Google Scholar · View at Scopus
  55. I. Cohen, P. Rider, Y. Carmi et al., “Differential release of chromatin-bound IL-1α discriminates between necrotic and apoptotic cell death by the ability to induce sterile inflammation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 6, pp. 2574–2579, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. G. Kaplanski, C. Farnarier, S. Kaplanski et al., “Interleukin-1 induces interleukin-8 secretion from endothelial cells by a juxtacrine mechanism,” Blood, vol. 84, no. 12, pp. 4242–4248, 1994. View at Google Scholar · View at Scopus
  57. C. Hauser, J. H. Saurat, A. Schmitt, F. Jaunin, and J. M. Dayer, “Interleukin 1 is present in normal human epidermis,” The Journal of Immunology, vol. 136, pp. 3317–3323, 1986. View at Google Scholar
  58. M. Hacham, S. Argov, R. M. White, S. Segal, and R. N. Apte, “Different patterns of interleukin-1α and interleukin-1β expression in organs of normal young and old mice,” European Cytokine Network, vol. 13, no. 1, pp. 55–65, 2002. View at Google Scholar · View at Scopus
  59. N. Watanabe and Y. Kobayashi, “Selective release of a processed form of interleukin 1α,” Cytokine, vol. 6, no. 6, pp. 597–601, 1994. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Lee, S. Temple, S. Roberts, and P. Price, “Complex effects of IL1A polymorphism and calpain inhibitors on interleukin 1α (IL-1α) mRNA levels and secretion of IL-1α protein,” Tissue Antigens, vol. 72, no. 1, pp. 67–71, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. G. Kaplanski, C. Farnarier, A. M. Benoliel, C. Foa, S. Kaplanski, and P. Bongrand, “A novel role for E- and P-selectins: shape control of endothelial cell monolayers,” Journal of Cell Science, vol. 107, no. 9, pp. 2449–2457, 1994. View at Google Scholar · View at Scopus
  62. M. Buryskova, M. Pospisek, A. Grothey, T. Simmet, and L. Burysek, “Intracellular interleukin-1α functionally interacts with histone acetyltransferase complexes,” Journal of Biological Chemistry, vol. 279, no. 6, pp. 4017–4026, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Werman, R. Werman-Venkert, R. White et al., “The precursor form of IL-1α is an intracrine proinflammatory activator of transcription,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 8, pp. 2434–2439, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. C. Hammerberg, W. P. Arend, G. J. Fisher et al., “Interleukin-1 receptor antagonist in normal and psoriatic epidermis,” Journal of Clinical Investigation, vol. 90, no. 2, pp. 571–583, 1992. View at Google Scholar · View at Scopus
  65. S. Nakae, M. Asano, R. Horai, and Y. Iwakura, “Interleukin-1β, but not interleukin-1α, is required for T-cell-dependent antibody production,” Immunology, vol. 104, no. 4, pp. 402–409, 2001. View at Publisher · View at Google Scholar · View at Scopus
  66. C. J. Chen, H. Kono, D. Golenbock, G. Reed, S. Akira, and K. L. Rock, “Identification of a key pathway required for the sterile inflammatory response triggered by dying cells,” Nature Medicine, vol. 13, no. 7, pp. 851–856, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. V. Hurgin, D. Novick, A. Werman, C. A. Dinarello, and M. Rubinstein, “Antiviral and immunoregulatory activities of IFN-γ depend on constitutively expressed IL-1α,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 12, pp. 5044–5049, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. B. Moser, I. Clark-Lewis, R. Zwahlen, and M. Baggiolini, “Neutrophil-activating properties of the melanoma growth-stimulatory activity,” Journal of Experimental Medicine, vol. 171, no. 5, pp. 1797–1802, 1990. View at Publisher · View at Google Scholar · View at Scopus
  69. T. Eigenbrod, J. H. Park, J. Harder, Y. Iwakura, and G. Nunez, “Cutting edge: critical role for mesothelial cells in necrosis-induced inflammation through the recognition of IL-1 alpha released from dying cells,” The Journal of Immunology, vol. 181, pp. 8194–8198, 2008. View at Google Scholar
  70. H. Kono, D. Karmarkar, Y. Iwakura, and K. L. Rock, “Identification of the cellular sensor that stimulates the inflammatory response to sterile cell death,” Journal of Immunology, vol. 184, no. 8, pp. 4470–4478, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. R. C. Hoch, R. Rodriguez, T. Manning et al., “Effects of accidental trauma on cytokine and endotoxin production,” Critical Care Medicine, vol. 21, no. 6, pp. 839–845, 1993. View at Google Scholar · View at Scopus
  72. C. A. Dinarello, “Anti-cytokine therapies in response to systemic infection,” Journal of Investigative Dermatology Symposium Proceedings, vol. 6, no. 3, pp. 244–250, 2001. View at Google Scholar · View at Scopus
  73. C. Moussion, N. Ortega, and J. P. Girard, “The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel “Alarmin”?” PLoS ONE, vol. 3, no. 10, Article ID e3331, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Schmitz, A. Owyang, E. Oldham et al., “IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines,” Immunity, vol. 23, no. 5, pp. 479–490, 2005. View at Publisher · View at Google Scholar · View at Scopus
  75. V. Carriere, L. Roussel, N. Ortega et al., “IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 1, pp. 282–287, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. T. Ohno, K. Oboki, N. Kajiwara et al., “Caspase-1, caspase-8, and calpain are dispensable for IL-33 release by macrophages,” Journal of Immunology, vol. 183, no. 12, pp. 7890–7897, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Cayrol and J. P. Girard, “The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 22, pp. 9021–9026, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. A. U. Lüthi, S. P. Cullen, E. A. McNeela et al., “Suppression of interleukin-33 bioactivity through proteolysis by apoptotic caspases,” Immunity, vol. 31, no. 1, pp. 84–98, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. F. Y. Liew, N. I. Pitman, and I. B. McInnes, “Disease-associated functions of IL-33: the new kid in the IL-1 family,” Nature Reviews Immunology, vol. 10, no. 2, pp. 103–110, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. D. Talabot-Ayer, C. Lamacchia, C. Gabay, and G. Palmer, “Interleukin-33 is biologically active independently of caspase-1 cleavage,” Journal of Biological Chemistry, vol. 284, no. 29, pp. 19420–19426, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Hong, S. Bae, H. Jhun et al., “Identification of constitutively active interleukin 33 (IL-33) splice variant,” Journal of Biological Chemistry, vol. 286, no. 22, pp. 20078–20086, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. P. Kunes, Z. Holubcova, M. Kolackova, and J. Krejsek, “Interleukin-33, a novel member of the IL-1/IL-18 cytokine family, in cardiology and cardiac surgery,” Thoracic and Cardiovascular Surgeon, vol. 58, no. 8, pp. 443–449, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. A. A. Chackerian, E. R. Oldham, E. E. Murphy, J. Schmitz, S. Pflanz, and R. A. Kastelein, “IL-1 receptor accessory protein and ST2 comprise the IL-33 receptor complex,” Journal of Immunology, vol. 179, no. 4, pp. 2551–2555, 2007. View at Google Scholar · View at Scopus
  84. M. Kurowska-Stolarska, P. Kewin, G. Murphy et al., “IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4,” Journal of Immunology, vol. 181, no. 7, pp. 4780–4790, 2008. View at Google Scholar · View at Scopus
  85. M. Komai-Koma, D. Xu, Y. Li, A. N. J. McKenzie, I. B. McInnes, and F. Y. Liew, “IL-33 is a chemoattractant for human Th2 cells,” European Journal of Immunology, vol. 37, no. 10, pp. 2779–2786, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Ali, M. Huber, C. Kollewe, S. C. Bischoff, W. Falk, and M. U. Martin, “IL-1 receptor accessory protein is essential for IL-33-induced activation of T lymphocytes and mast cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 47, pp. 18660–18665, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. D. Moulin, O. Donzé, D. Talabot-Ayer, F. Mézin, G. Palmer, and C. Gabay, “Interleukin (IL)-33 induces the release of pro-inflammatory mediators by mast cells,” Cytokine, vol. 40, no. 3, pp. 216–225, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. P. N. Pushparaj, K. T. Hwee, C. H. Shiau et al., “The cytokine interleukin-33 mediates anaphylactic shock,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 24, pp. 9773–9778, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Kurowska-Stolarska, B. Stolarski, P. Kewin et al., “IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation,” Journal of Immunology, vol. 183, no. 10, pp. 6469–6477, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. Q. Espinassous, E. Garcia-de-Paco, I. Garcia-Verdugo et al., “IL-33 enhances lipopolysaccharide-induced inflammatory cytokine production from mouse macrophages by regulating lipopolysaccharide receptor complex,” Journal of Immunology, vol. 183, no. 2, pp. 1446–1455, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. H. Iwahana, K. Yanagisawa, A. Ito-Kosaka et al., “Different promoter usage and multiple transcription initiation sites of the interleukin-1 receptor-related human ST2 gene in UT-7 and TM12 cells,” European Journal of Biochemistry, vol. 264, no. 2, pp. 397–406, 1999. View at Publisher · View at Google Scholar · View at Scopus
  92. J. J. Hoogerwerf, M. W. T. Tanck, M. A. D. Van Zoelen, X. Wittebole, P. F. Laterre, and T. Van Der Poll, “Soluble ST2 plasma concentrations predict mortality in severe sepsis,” Intensive Care Medicine, vol. 36, no. 4, pp. 630–637, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. K. Kuroiwa, T. Arai, H. Okazaki, S. Minota, and S. I. Tominaga, “Identification of human ST2 protein in the sera of patients with autoimmune diseases,” Biochemical and Biophysical Research Communications, vol. 284, no. 5, pp. 1104–1108, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. K. Oshikawa, K. Kuroiwa, K. Tago et al., “Elevated soluble ST2 protein levels in sera of patients with asthma with an acute exacerbation,” American Journal of Respiratory and Critical Care Medicine, vol. 164, no. 2, pp. 277–281, 2001. View at Google Scholar · View at Scopus
  95. M. Shimpo, D. A. Morrow, E. O. Weinberg et al., “Serum levels of the interleukin-1 receptor family member ST2 predict mortality and clinical outcome in acute myocardial infarction,” Circulation, vol. 109, no. 18, pp. 2186–2190, 2004. View at Publisher · View at Google Scholar · View at Scopus
  96. J. C. Alves-Filho, F. Snego, F. O. Souto et al., “Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection,” Nature Medicine, vol. 16, no. 6, pp. 708–712, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. E. Faist and M. W. Wichmann, “Immunology in the severely injured,” Chirurg, vol. 68, no. 11, pp. 1066–1070, 1997. View at Google Scholar · View at Scopus
  98. A. Lenz, G. A. Franklin, and W. G. Cheadle, “Systemic inflammation after trauma,” Injury, vol. 38, no. 12, pp. 1336–1345, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. Y. M. Yao, H. Redl, S. Bahrami, and G. Schlag, “The inflammatory basis of trauma/shock-associated multiple organ failure,” Inflammation Research, vol. 47, no. 5, pp. 201–210, 1998. View at Publisher · View at Google Scholar · View at Scopus
  100. I. E. Wallin, “A note on the morphology of bacteria symbiotic in the tissues of higher organisms,” Journal of Bacteriology, vol. 7, pp. 471–474, 1922. View at Google Scholar
  101. Q. Zhang, M. Raoof, Y. Chen et al., “Circulating mitochondrial DAMPs cause inflammatory responses to injury,” Nature, vol. 464, no. 7285, pp. 104–107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  102. J. W. Taanman, “The mitochondrial genome: structure, transcription, translation and replication,” Biochimica et Biophysica Acta, vol. 1410, pp. 103–123, 1999. View at Google Scholar
  103. A. P. West, A. A. Koblansky, and S. Ghosh, “Recognition and signaling by toll-like receptors,” Annual Review of Cell and Developmental Biology, vol. 22, pp. 409–437, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. Q. Zhang, K. Itagaki, and C. J. Hauser, “Mitochondrial DNA is released by shock and activates neutrophils via P38 map kinase,” Shock, vol. 34, no. 1, pp. 55–59, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. L. V. Collins, S. Hajizadeh, E. Holme, I. M. Jonsson, and A. Tarkowski, “Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses,” Journal of Leukocyte Biology, vol. 75, no. 6, pp. 995–1000, 2004. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Raoof, Q. Zhang, K. Itagaki, and C. J. Hauser, “Mitochondrial peptides are potent immune activators that activate human neutrophils via FPR-1,” Journal of Trauma, vol. 68, no. 6, pp. 1328–1332, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. C. J. Hauser, T. Sursal, E. K. Rodriguez, P. T. Appleton, Q. Zhang, and K. Itagaki, “Mitochondrial damage associated molecular patterns from femoral reamings activate neutrophils through formyl peptide receptors and P44/42 MAP kinase,” Journal of Orthopaedic Trauma, vol. 24, no. 9, pp. 534–538, 2010. View at Publisher · View at Google Scholar · View at Scopus
  108. E. Schiffmann, B. A. Corcoran, and S. M. Wahl, “N formylmethionyl peptides as chemoattractants for leucocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 72, no. 3, pp. 1059–1062, 1975. View at Google Scholar · View at Scopus
  109. M. J. Rabiet, E. Huet, and F. Boulay, “Human mitochondria-derived N-formylated peptides are novel agonists equally active on FPR and FPRL1, while Listeria monocytogenes-derived peptides preferentially activate FPR,” European Journal of Immunology, vol. 35, no. 8, pp. 2486–2495, 2005. View at Publisher · View at Google Scholar · View at Scopus
  110. N. Chiang, I. M. Fierro, K. Gronert, and C. N. Serhan, “Activation of lipoxin A4 receptors by aspirin-triggered lipoxins and select peptides evokes ligand-specific responses in inflammation,” Journal of Experimental Medicine, vol. 191, no. 7, pp. 1197–1207, 2000. View at Publisher · View at Google Scholar · View at Scopus
  111. R. Selvatici, S. Falzarano, A. Mollica, and S. Spisani, “Signal transduction pathways triggered by selective formylpeptide analogues in human neutrophils,” European Journal of Pharmacology, vol. 534, no. 1–3, pp. 1–11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  112. Y. Le, P. M. Murphy, and J. M. Wang, “Formyl-peptide receptors revisited,” Trends in Immunology, vol. 23, no. 11, pp. 541–548, 2002. View at Publisher · View at Google Scholar · View at Scopus
  113. I. Migeotte, D. Communi, and M. Parmentier, “Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses,” Cytokine and Growth Factor Reviews, vol. 17, no. 6, pp. 501–519, 2006. View at Publisher · View at Google Scholar · View at Scopus
  114. M. J. Rabiet, E. Huet, and F. Boulay, “The N-formyl peptide receptors and the anaphylatoxin C5a receptors: an overview,” Biochimie, vol. 89, no. 9, pp. 1089–1106, 2007. View at Publisher · View at Google Scholar · View at Scopus
  115. B. McDonald, K. Pittman, G. B. Menezes et al., “Intravascular danger signals guide neutrophils to sites of sterile inflammation,” Science, vol. 330, no. 6002, pp. 362–366, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. E. D. Crouser, G. Shao, M. W. Julian et al., “Monocyte activation by necrotic cells is promoted by mitochondrial proteins and formyl peptide receptors,” Critical Care Medicine, vol. 37, no. 6, pp. 2000–2009, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. W. J. Hubbard, K. I. Bland, and I. H. Chaudry, “The role of the mitochondrion in trauma and shock,” Shock, vol. 22, no. 5, pp. 395–402, 2004. View at Publisher · View at Google Scholar · View at Scopus
  118. C. Power, N. Fanning, and H. P. Redmond, “Cellular apoptosis and organ injury in sepsis: a review,” Shock, vol. 18, no. 3, pp. 197–211, 2002. View at Google Scholar · View at Scopus
  119. L. Duprez, N. Takahashi, F. van Hauwermeiren, B. Vandendriessche, and V. Goossens, “RIP kinase-dependent necrosis drives lethal systemic inflammatory response syndrome,” Immunity, vol. 35, pp. 908–918, 2011. View at Google Scholar
  120. P. Vandenabeele, L. Galluzzi, T. Vanden Berghe, and G. Kroemer, “Molecular mechanisms of necroptosis: an ordered cellular explosion,” Nature Reviews Molecular Cell Biology, vol. 11, no. 10, pp. 700–714, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. N. D. Bonawitz, D. A. Clayton, and G. S. Shadel, “Initiation and beyond: multiple functions of the human mitochondrial transcription machinery,” Molecular Cell, vol. 24, no. 6, pp. 813–825, 2006. View at Publisher · View at Google Scholar · View at Scopus