Complement factor 3 deficiency attenuates hemorrhagic shock-related hepatic injury and systemic inflammatory response syndrome

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 5, 2010, Pages

  Cai, Changchun ^a,b   Gill, Roop ^a   Eum, Hyun Ae ^a   Cao, Zongxian ^a   Loughran, Patricia A ^a   Darwiche, Sophie ^a   Edmonds, Rebecca D ^a   Menzel, Christoph L ^a   Billiar, Timothy R ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b QINGDAO UNIVERSITY   (China)

Author keywords

Double strand DNA; Heme oxygenase 1; High mobility group box 1; Single strand DNA; Systemic inflammatory response syndrome

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; COMPLEMENT COMPONENT C3; DOUBLE STRANDED DNA; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 6; SINGLE STRANDED DNA; SNAKE VENOM;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; COMPLEMENT ACTIVATION; COMPLEMENT DEFICIENCY; CONTROLLED STUDY; CYTOKINE RELEASE; FEMUR FRACTURE; HEMORRHAGIC SHOCK; LIVER INJURY; MALE; MOUSE; MULTIPLE ORGAN FAILURE; NONHUMAN; PRIORITY JOURNAL; RESUSCITATION; SOFT TISSUE INJURY; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; BIOLOGICAL MARKERS; COBRA VENOMS; COMPLEMENT ACTIVATION; COMPLEMENT C3; DISEASE MODELS, ANIMAL; DNA, SINGLE-STRANDED; FEMORAL FRACTURES; HEME OXYGENASE (DECYCLIZING); HMGB1 PROTEIN; INJECTIONS, INTRAPERITONEAL; INTERLEUKIN-10; INTERLEUKIN-6; LIVER; LIVER DISEASES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SHOCK, HEMORRHAGIC; SOFT TISSUE INJURIES; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; TIME FACTORS;

EID: 78149481862     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00282.2010     Document Type: Article

References (43)

1. Alper CA, Balavitch D. Cobra venom factor: evidence for its being altered cobra C3 (the third component of complement). Science 191: 1275-1276, 1976.
2. 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.
3. Cardon LR, Burge C, Clayton DA, Karlin S. Pervasive CpG suppression in animal mitochondrial genomes. Proc Natl Acad Sci USA 91: 3799-3803, 1994.
4. Chou CC, Fang HY, Chen YL, Wu CY, Siao FY, Chou MJ. Plasma nuclear DNA and mitochondrial DNA as prognostic markers in corrosive injury patients. Dig Surg 25: 300-304, 2008.
5. Collard CD, Agah A, Stahl GL. Complement activation following reoxygenation of hypoxic human endothelial cells: role of intracellular reactive oxygen species, NF-kappaB and new protein synthesis. Immunopharmacology 39: 39-50, 1998.
6. Diepenhorst GM, van Gulik TM, Hack CE. Complement-mediated ischemia-reperfusion injury: lessons learned from animal and clinical studies. Ann Surg 249: 889-899, 2009.
7. Fruchterman TM, Spain DA, Wilson MA, Harris PD, Garrison RN. Complement inhibition prevents gut ischemia and endothelial cell dysfunction after hemorrhage/resuscitation. Surgery 124: 782-791, 1998.
8. Gebhard F, Pfetsch H, Steinbach G, Strecker W, Kinzl L, Bruckner UB. Is interleukin 6 an early marker of injury severity following major trauma in humans? Arch Surg 135: 291-295, 2000.
9. He S, Atkinson C, Qiao F, Cianflone K, Chen X, Tomlinson S. A complement-dependent balance between hepatic ischemia/reperfusion injury and liver regeneration in mice. J Clin Invest 119: 2304-2316, 2009.
10. Hecke F, Schmidt U, Kola A, Bautsch W, Klos A, Köhl J. Circulating complement proteins in multiple trauma patients: correlation with injury severity, development of sepsis, and outcome. Crit Care Med 25: 2015-2024, 1997.
11. Huber-Lang M, Sarma JV, Zetoune FS, Rittirsch D, Neff TA, McGuire SR, Lambris JD, Warner RL, Flierl MA, Hoesel LM, Gebhard F, Younger JG, Drouin SM, Wetsel RA, Ward PA. Generation of C5a in the absence of C3: a new complement activation pathway. Nat Med 12: 682-687, 2006.
12. Ishii KJ, Coban C, Kato H, Takahashi K, Torii Y, Takeshita F, Ludwig H, Sutter G, Suzuki K, Hemmi H, Sato S, Yamamoto M, Uematsu S, Kawai T, Takeuchi O, Akira S. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol 7: 40-44, 2005.
13. Kauvar DS, Lefering R, Wade CE. Impact of hemorrhage on trauma outcome: an overview of epidemiology, clinical presentations, and therapeutic considerations. J Trauma 60: S3-S11, 2006.
14. 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.
15. Kung HC, Hoyert DL, Xu J, Murphy SL. Deaths: final data for 2005. Natl Vital Stat Rep 56: 1-120, 2008.
16. Lam NY, Rainer TH, Chan LY, Joynt GM, Lo YM. Time course of early and late changes in plasma DNA in trauma patients. Clin Chem 49: 1286-1291, 2003.
17. Lesavre PH, Hugli TE, Esser AF, Müller-Eberhard HJ. The alternative pathway C3/C5 convertase: chemical basis of factor B activation. J Immunol 123: 529-534, 1979. (Pubitemid 9203384)
18. Levy RM, Mollen KP, Prince JM, Kaczorowski DJ, Vallabhaneni R, Liu S, Tracey KJ, Lotze MT, Hackam DJ, Fink MP, Vodovotz Y, Billiar TR. Systemic inflammation and remote organ injury following trauma require HMGB-1. Am J Physiol Regul Integr Comp Physiol 293: R1538-R1544, 2007.
19. Müller-Eberhard HJ, Fjellström K. Isolation of the anticomplementary protein from cobra venom and its mode of action on C3. J Immunol 107: 1666-1672, 1971.
20. 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.
21. Okabe Y, Kawane K, Akira S, Taniguchi T, Nagata S. Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J Exp Med 202: 1333-1339, 2005.
22. Ombrellino M, Wang H, Ajemian MS, Talhouk A, Scher LA, Friedman SG, Tracey KJ. Increased serum concentrations of high-mobility-group protein 1 in haemorrhagic shock. Lancet 354: 1446-1447, 1999.
23. Pepys MB. Studies in vivo of cobra factor and murine C3. Immunology 28: 369-377, 1975.
24. 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. (Pubitemid 43356214)
25. 2-mediated complement activation and cytokines-mediated fibroblasts superoxide generation on skin inflammation. Dermatologica 179: S107-S112, 1989.
26. Stensballe J, Christiansen M, Tønnesen E, Espersen K, Lippert FK, Rasmussen LS. The early IL-6 and IL-10 response in trauma is correlated with injury severity and mortality. Acta Anaesthesiol Scand 53: 515-521, 2009.
27. Sunden-Cullberg J, Norrby-Teglund A, Rouhiainen A, Rauvala H, Herman G, Tracey KJ, Lee ML, Andersson J, Tokics L, Treutiger CJ. Persistent elevation of high mobility group box-1 protein (HMGB1) in patients with severe sepsis and septic shock. Crit Care Med 33: 564-573, 2005.
28. Takahashi T, Shimizu H, Morimatsu H, Maeshima K, Inoue K, Akagi R, Matsumi M, Katayama H, Morita K. Heme oxygenase-1 is an essential cytoprotective component in oxidative tissue injury induced by hemorrhagic shock. J Clin Biochem Nutr 44, 28-40, 2009.
29. 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.
30. Vallabhaneni R, Kaczorowski DJ, Yaakovian MD, Rao J, Zuckerbraun BS. Heme oxygenase 1 protects against hepatic hypoxia and injury from hemorrhage via regulation of cellular respiration. Shock 33: 274-281, 2010.
31. von Zabern WV, Hesse D, Nolte R, Haller Y. Generation of an activated form of human C5 (C5b-like C5) by oxygen radicals. Immunol Lett 14: 209-215, 1987.
32. 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.
33. Weiser MR, Williams JP, Moore FD Jr, Kobzik L, Ma M, Hechtman HB, Carroll MC. Reperfusion injury of ischemic skeletal muscle is mediated by natural antibody and complement. J Exp Med 183: 2343-2348, 1996. (Pubitemid 26158925)
34. Williams JP, Pechet TT, Weiser MR, Reid R, Kobzik L, Moore FD Jr, Carroll MC, Hechtman HB. Intestinal reperfusion injury is mediated by IgM and complement. J Appl Physiol 86: 938-942, 1999.
35. 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.
36. 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.
37. Yang S, Nakamura T, Hua Y, Keep RF, Younger JG, He Y, Hoff JT, Xi G. The role of complement C3 in intracerebral hemorrhage-induced brain injury. J Cereb Blood Flow Metab 26: 1490-1495, 2006. (Pubitemid 44809078)
38. Yasuda K, Yu P, Kirschning CJ, Schlatter B, Schmitz F, Heit A, Bauer S, Hochrein H, Wagner H. Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways. J Immunol 174: 6129-6136, 2005.
39. Younger JG, Sasaki N, Waite MD, Murray HN, Saleh EF, Ravage ZB, Hirschl RB, Ward PA, Till GO. Detrimental effects of complement activation in hemorrhagic shock. J Appl Physiol 90: 441-446, 2001.
40. Zhang Q, Itagaki K, Hauser CJ. Mitochondrial DNA is released by shock and activates neutrophils via p38 MAP-kinase. Shock 34: 55-59, 2010.
41. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464: 104-107, 2010.
42. Zhou W, Farrar CA, Abe K, Pratt JR, Marsh JE, Wang Y, Stahl GL, Sacks SH. Predominant role for C5b-9 in renal ischemia/reperfusion injury. J Clin Invest 105: 1363-1371, 2000. (Pubitemid 30322402)
43. Zuckerbraun BS, McCloskey CA, Gallo D, Liu F, Ifedigbo E, Otterbein LE, Billiar TR. Carbon monoxide prevents multiple organ injury in a model of hemorrhagic shock and resuscitation. Shock 23: 527-532, 2005.