Systemic inflammation and remote organ injury following trauma require HMGB1

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 293, Issue 4, 2007, Pages

  Levy, Ryan M ^a   Mollen, Kevin P ^a   Prince, Jose M ^a   Kaczorowski, David J ^a   Vallabhaneni, Raghuveer ^a   Liu, Shiguang ^b   Tracey, Kevin J ^c   Lotze, Michael T ^a   Hackam, David J ^a   Fink, Mitchell P ^a,b   Vodovotz, Yoram ^a,d   Billiar, Timothy R ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Damage associated molecular pattern molecule; Danger signal; Femur fracture; Pattern recognition receptor; Tissue injury

Indexed keywords

ALANINE AMINOTRANSFERASE; DNA; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 6; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; FEMUR FRACTURE; LIVER INJURY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

ANIMALS; ANTIBODIES; BIOLOGICAL MARKERS; FRACTURES, BONE; HMGB1 PROTEIN; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C3H; NF-KAPPA B; TOLL-LIKE RECEPTOR 4; WOUNDS AND INJURIES;

EID: 35148861150     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00272.2007     Document Type: Article

References (50)

1. Abreu MT, Arnold ET, Thomas LS, Gonsky R, Zhou Y, Hu B, Arditi M. TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J Biol Chem 277: 20431-20437, 2002.
2. Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, Janson A, Kokkola R, Zhang M, Yang H, Tracey KJ. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 192: 565-570, 2000.
3. Barsness KA, Arcaroli J, Harken AH, Abraham E, Banerjee A, Reznikov L, McIntyre RC. Hemorrhage-induced acute lung injury is TLR-4 dependent. Am J Physiol Regul Integr Comp Physiol 287: R592-R599, 2004.
4. Cetin S, Ford HR, Sysko LR, Agarwal C, Wang J, Neal MD, Baty C, Apodaca G, Hackam DJ. Endotoxin inhibits intestinal epithelial restitution through activation of Rho-GTPase and increased focal adhesions. J Biol Chem 279: 24592-24600, 2004.
5. Cinat ME, Waxman K, Granger GA, Pearce W, Annas C, Daughters K. Trauma causes sustained elevation of soluble tumor necrosis factor receptors. J Am Coll Surg 179: 529-537, 1994.
6. Demarco RA, Fink MP, Lotze MT. Monocytes promote natural killer cell interferon gamma production in response to the endogenous danger signal HMGB1. Mol Immunol 42: 433-444, 2005.
7. Faist E, Baue AE, Dittmer H, Heberer G. Multiple organ failure in polytrauma patients. J Trauma 23: 775-787, 1983.
8. Guo W, Ding J, Huang Q, Jerrells T, Deitch EA. Alterations in intestinal bacterial flora modulate the systemic cytokine response to hemorrhagic shock. Am J Physiol Gastrointest Liver Physiol 269: G827-G832, 1995.
9. Hauser CJ, Zhou X, Joshi P, Cuchens MA, Kregor P, Devidas M, Kennedy RJ, Poole GV, Hughes JL. The immune microenvironment of human fracture/soft-tissue hematomas and its relationship to systemic immunity. J Trauma 42: 895-903, 1997.
10. Hensler T, Sauerland S, Bouillon B, Raum M, Rixen D, Helling HJ, Andermahr J, Neugebauer EA. Association between injury pattern of patients with multiple injuries and circulating levels of soluble tumor necrosis factor receptors, interleukin-6 and interleukin-10, and polymor-phonuclear neutrophil elastase. J Trauma 52: 962-970, 2002.
11. Hoyert DL, Heron MP, Murphy SL, Kung HC. Deaths: final data for 2003. Natl Vital Stat Rep 54: 1-120, 2006.
12. Ito N, DeMarco RA, Mailliard RB, Han J, Rabinowich H, Kalinski P, Stolz DB, Zeh HJ 3rd, Lotze MT. Cytolytic cells induce HMGB1 release from melanoma cell lines. J Leukoc Biol 81: 75-83, 2006.
13. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 5: 987-995, 2004.
14. Johnson GB, Brunn GJ, Kodaira Y, Platt JL. Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J Immunol 168: 5233-5239, 2002.
15. Keel M, Trentz O. Pathophysiology of polytrauma. Injury 36: 691-709, 2005.
16. Kim JY, Park JS, Strassheim D, Douglas I, Diaz del Valle F, Asehnoune K, Mitra S, Kwak SH, Yamada S, Maruyama I, Ishizaka A, Abraham E. HMGB1 contributes to the development of acute lung injury after hemorrhage. Am J Physiol Lung Cell Mol Physiol 288: L958-L965, 2005.
17. Lamphier MS, Sirois CM, Verma A, Golenbock DT, Latz E. TLR9 and the recognition of self and non-self nucleic acids. Ann NY Acad Sci 1082: 31-43, 2006.
18. Levy RM, Prince JM, Yang R, Mollen KP, Liao H, Watson GA, Fink MP, Vodovotz Y, Billiar TR. Systemic inflammation and remote organ damage following bilateral femur fracture requires Toll-like receptor 4. Am J Physiol Regul Integr Comp Physiol 291: R970-R976, 2006.
19. Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 5: 331-342, 2005.
20. Martin C, Boisson C, Haccoun M, Thomachot L, Mege JL. Patterns of cytokine evolution (tumor necrosis factor-α and interleukin-6) after septic shock, hemorrhagic shock, and severe trauma. Crit Care Med 25: 1813-1819, 1997.
21. Mollen KP, Anand RJ, Tsung A, Prince JM, Levy RM, Billiar TR. Emerging paradigm: toll-like receptor 4-sentinel for the detection of tissue damage. Shock 26: 430-437, 2006.
22. Moore EE. Synergy of bone fractures, soft tissue disruption, and hemorrhagic shock in the genesis of postinjury immunochaos: the pathway to multiple organ failure. Crit Care Med 26: 1305-1306, 1998.
23. Napolitano LM, Ferrer T, McCarter RJ Jr, Scalea TM. Systemic inflammatory response syndrome score at admission independently predicts mortality and length of stay in trauma patients. J Trauma 49: 647-652, 2000.
24. Neal MD, Leaphart C, Levy R, Prince J, Billiar TR, Watkins S, Li J, Cetin S, Ford H, Schreiber A, Hackam DJ. Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J Immunol 176: 3070-3079, 2006.
25. Neidhardt R, Keel M, Steckholzer U, Safret A, Ungethuem U, Trentz O, Ertel W. Relationship of interleukin-10 plasma levels to severity of injury and clinical outcome in injured patients. J Trauma 42: 863-870, 1997.
26. Ogawa EN, Ishizaka A, Tasaka S, Koh H, Ueno H, Amaya F, Ebina M, Yamada S, Funakoshi Y, Soejima J, Moriyama K, Kotani T, Hashimoto S, Morisaki H, Abraham E, Takeda J. Contribution of high-mobility group box-1 to the development of ventilator-induced lung injury. Am J Respir Crit Care Med 174: 400-407, 2006.
27. Ohashi K, Burkart V, Flohe S, Kolb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J Immunol 164: 558-561, 2000.
28. Oyama J, Blais C Jr, Liu X, Pu M, Kobzik L, Kelly RA, Bourcier T. Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation 109: 784-789, 2004.
29. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim JY, Strassheim D, Sohn JW, Yamada S, Maruyama I, Banerjee A, Ishizaka A, Abraham E. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 290: C917-C924, 2006.
30. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, Ishizaka A, Abraham E. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 279: 7370-7377, 2004.
31. Partrick DA, Moore EE, Moore FA, Biffl WL, Barnett CC Jr. Release of anti-inflammatory mediators after major torso trauma correlates with the development of postinjury multiple organ failure. Am J Surg 178: 564-569, 1999.
32. Peitzman AB, Udekwu AO, Ochoa J, Smith S. Bacterial translocation in trauma patients. J Trauma 31: 1083-1086, 1991.
33. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088, 1998.
34. Prince JM, Levy RM, Yang R, Mollen KP, Fink MP, Vodovotz Y, Billiar TR. Toll-like receptor-4 signaling mediates hepatic injury and systemic inflammation in hemorrhagic shock. J Am Coll Surg 202: 407-417, 2006.
35. Prinz M, Garbe F, Schmidt H, Mildner A, Gutcher I, Wolter K, Piesche M, Schroers R, Weiss E, Kirschning CJ, Rochford CD, Bruck W, Becher B. Innate immunity mediated by TLR9 modulates pathogenicity in an animal model of multiple sclerosis. J Clin Invest 116: 456-464, 2006.
36. Rose S, Marzi I. Mediators in polytrauma-pathophysiological significance and clinical relevance. Langenbecks Arch Surg 383: 199-208, 1998.
37. Rouhiainen A, Tumova S, Valmu L, Kalkkinen N, Rauvala H. Pivotal advance: analysis of proinflammatory activity of highly purified eukaryotic recombinant HMGB1 (amphoterin). J Leukoc Biol 81: 49-58, 2007.
38. Roumen RM, Hendriks T, van der Ven-Jongekrijg J, Nieuwenhuijzen GA, Sauerwein RW, van der Meer JW, Goris RJ. Cytokine patterns in patients after major vascular surgery, hemorrhagic shock, and severe blunt trauma. Relation with subsequent adult respiratory distress syndrome and multiple organ failure. Ann Surg 218: 769-776, 1993.
39. Schnare M, Barton GM, Holt AC, Takeda K, Akira S, Medzhitov R. Toll-like receptors control activation of adaptive immune responses. Nat Immunol 2: 947-950, 2001.
40. Sherry RM, Cue JI, Goddard JK, Parramore JB, DiPiro JT. Interleukin-10 is associated with the development of sepsis in trauma patients. J Trauma 40: 613-616, 1996.
41. Strecker W, Gebhard F, Rager J, Bruckner UB, Steinbach G, Kinzl L. Early biochemical characterization of soft-tissue trauma and fracture trauma. J Trauma 47: 358-364, 1999.
42. Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, Billiar TR. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 201: 1135-1143, 2005.
43. Tsung A, Zheng N, Jeyabalan G, Izuishi K, Klune JR, Geller DA, Lotze MT, Lu L, Billiar TR. Increasing numbers of hepatic dendritic cells promote HMGB1-mediated ischemia-reperfusion injury. J Leukoc Biol 81: 119-128, 2007.
44. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, Abraham E, Andersson J, Andersson U, Molina PE, Abumrad NN, Sama A, Tracey KJ. HMG-1 as a late mediator of endotoxin lethality in mice. Science 285: 248-251, 1999.
45. Wolfs TG, Buurman WA, van Schadewijk A, de Vries B, Daemen MA, Hiemstra PS, van 't Veer C. In vivo expression of Toll-like receptor 2 and 4 by renal epithelial cells: IFN-γ and TNF-α mediated up-regulation during inflammation. J Immunol 168: 1286-1293, 2002.
46. Yang H, Ochani M, Li J, Qiang X, Tanovic M, Harris HE, Susarla SM, Ulloa L, Wang H, DiRaimo R, Czura CJ, Wang H, Roth J, Warren HS, Fink MP, Fenton MJ, Andersson U, Tracey KJ. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci USA 101: 296-301, 2004.
47. Yang R, Gallo DJ, Baust JJ, Watkins SK, Delude RL, Fink MP. Effect of hemorrhagic shock on gut barrier function and expression of stress-related genes in normal and gnotobiotic mice. Am J Physiol Regul Integr Comp Physiol 283: R1263-R1274, 2002.
48. Yang R, Harada T, Mollen KP, Prince JM, Levy RM, Englert JA, Gallowitsch-Puerta M, Yang L, Yang H, Tracey KJ, Harbrecht BG, Billiar TR, Fink MP. Anti-HMGB1 neutralizing antibody ameliorates gut barrier dysfunction and improves survival after hemorrhagic shock. Mol Med 12: 105-114, 2006.
49. Yao YM, Redl H, Bahrami S, Schlag G. The inflammatory basis of trauma/shock-associated multiple organ failure. Inflamm Res 47: 201-210, 1998.
50. Yu M, Wang H, Ding A, Golenbock DT, Latz E, Czura CJ, Fenton MJ, Tracey KJ, Yang H. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 26: 174-179, 2006.