Functions of the complement components C3 and C5 during sepsis

FASEB Journal

Volumn 22, Issue 10, 2008, Pages 3483-3490

  Flierl, Michael A ^a   Rittirsch, Daniel ^a   Nadeau, Brian A ^a   Day, Danielle E ^a   Zetoune, Firas S ^a   Sarma, J Vidya ^a   Huber Lang, Markus S ^b   Ward, Peter A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ULM MEDICAL SCHOOL   (Germany)

Author keywords

CH 50; Chemokines; Colony forming units; Cytokines; Survival

Indexed keywords

COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5A RECEPTOR; COMPLEMENT MEMBRANE ATTACK COMPLEX; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; CHEMOKINE; COMPLEMENT COMPONENT C5A; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; CONTROLLED STUDY; HEMOLYSIS; INFECTION CONTROL; INFLAMMATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FOLDING; PROTEIN FUNCTION; SEPSIS; SURVIVAL; ANIMAL; BLOOD; COMPLEMENT HEMOLYSIS TEST; DISEASE MODEL; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

ANIMALIA; MUS;

ANIMALS; BACTEREMIA; CHEMOKINES; COMPLEMENT C3; COMPLEMENT C5A; COMPLEMENT HEMOLYTIC ACTIVITY ASSAY; COMPLEMENT MEMBRANE ATTACK COMPLEX; CYTOKINES; DISEASE MODELS, ANIMAL; MICE; MICE, KNOCKOUT;

EID: 54049102451     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.08-110595     Document Type: Article

References (55)

1. Riedemann, N. C., Guo, R. F., and Ward, P. A. (2003) The enigma of sepsis. J. Clin. Investig. 112, 460-467
2. Levy, M. M., Fink, M. P., Marshall, J. C., Abraham, E., Angus, D., Cook, D., Cohen, J., Opal, S. M., Vincent, J. L., and Ramsay, G. (2003) 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit. Care Med. 31, 1250-1256
3. Annane, D., Bellissant, E., and Cavaillon, J. M. (2005) Septic shock. Lancet 365, 63-78
4. Dombrovskiy, V. Y., Martin, A. A., Sunderram, J., and Paz, H. L. (2007) Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: a trend analysis from 1993 to 2003. Crit. Care Med. 35, 1244-1250
5. Kochanek, K. D., and Smith, B. L. (2004) Deaths: preliminary data for 2002. Natl. Vital Stat. Rep. 52, 1-47
6. Guo, R. F., and Ward, P. A. (2005) Role of C5a in inflammatory responses. Annu. Rev. Immunol. 23, 821-852
7. Muller-Eberhard, H. J. (1988) Molecular organization and function of the complement system. Annu. Rev. Biochem. 57, 321-347
8. Reid, K. B., and Porter, R. R. (1981) The proteolytic activation systems of complement. Annu. Rev. Biochem. 50, 433-464
9. Gerard, C. (2003) Complement C5a in the sepsis syndrome - too much of a good thing? N. Engl. J. Med. 348, 167-169
10. Ward, P. A. (2004) The dark side of C5a in sepsis. Nat. Rev. Immunol. 4, 133-142
11. Huber-Lang, M. S., Younkin, E. M., Sarma, J. V., McGuire, S. R., Lu, K. T., Guo, R. F., Padgaonkar, V. A., Curnutte, J. T., Erickson, R., and Ward, P. A. (2002) Complement-induced impairment of innate immunity during sepsis. J. Immunol. 169, 3223-3231
12. Huber-Lang, M., Sarma, V. J., Lu, K. T., McGuire, S. R., Padgaonkar, V. A., Guo, R. F., Younkin, E. M., Kunkel, R. G., Ding, J., Erickson, R., Curnutte, J. T., and Ward, P. A. (2001) Role of C5a in multiorgan failure during sepsis. J. Immunol. 166, 1193-1199
13. Guo, R. F., Huber-Lang, M., Wang, X., Sarma, V., Padgaonkar, V. A., Craig, R. A., Riedemann, N. C., McClintock, S. D., Hlaing, T., Shi, M. M., and Ward, P. A. (2000) Protective effects of anti-C5a in sepsis-induced thymocyte apoptosis. J. Clin. Investig. 106, 1271-1280
14. Riedemann, N. C., Guo, R. F., Laudes, I. J., Keller, K., Sarma, V. J., Padgaonkar, V., Zetoune, F. S., and Ward, P. A. (2002) C5a receptor and thymocyte apoptosis in sepsis. FASEB J. 16, 887-888
15. Laudes, I. J., Chu, J. C., Sikranth, S., Huber-Lang, M., Guo, R. F., Riedemann, N., Sarma, J. V., Schmaier, A. H., and Ward, P. A. (2002) Anti-c5a ameliorates coagulation/fibrinolytic protein changes in a rat model of sepsis. Am. J. Pathol. 160, 1867-1875
16. Nakae, H., Endo, S., Inada, K., Takakuwa, T., Kasai, T., and Yoshida, M. (1994) Serum complement levels and severity of sepsis. Res. Commun. Chem. Pathol. Pharmacol. 84, 189-195
17. Nakae, H., Endo, S., Inada, K., and Yoshida, M. (1996) Chronological changes in the complement system in sepsis. Surg. Today 26, 225-229
18. Stove, S., Welte, T., Wagner, T. O., Kola, A., Klos, A., Bautsch, W., and Kohl, J. (1996) Circulating complement proteins in patients with sepsis or systemic inflammatory response syndrome. Clin. Diagn. Lab. Immunol. 3, 175-183
19. Hack, C. E., Nuijens, J. H., Felt-Bersma, R. J., Schreuder, W. O., Eerenberg-Belmer, A. J., Paardekooper, J., Bronsveld, W., and Thijs, L. G. (1989) Elevated plasma levels of the anaphylatoxins C3a and C4a are associated with a fatal outcome in sepsis. Am. J. Med. 86, 20-26
20. Czermak, B. J., Sarma, V., Pierson, C. L., Warner, R. L., Huber-Lang, M., Bless, N. M., Schmal, H., Friedl, H. P., and Ward, P. A. (1999) Protective effects of C5a blockade in sepsis. Nat. Med. 5, 788-792
21. Huber-Lang, M. S., Riedeman, N. C., Sarma, J. V., Younkin, E. M., McGuire, S. R., Laudes, I. J., Lu, K. T., Guo, R. F., Neff, T. A., Padgaonkar, V. A., Lambris, J. D., Spruce, L., Mastellos, D., Zetoune, F. S., and Ward, P. A. (2002) Protection of innate immunity by C5aR antagonist in septic mice. FASEB J. 16, 1567-1574
22. Huber-Lang, M. S., Sarma, J. V., McGuire, S. R., Lu, K. T., Guo, R. F., Padgaonkar, V. A., Younkin, E. M., Laudes, I. J., Riedemann, N. C., Younger, J. G., and Ward, P. A. (2001) Protective effects of anti-C5a peptide antibodies in experimental sepsis. FASEB J. 15, 568-570
23. Prodeus, A. P., Zhou, X., Maurer, M., Galli, S. J., and Carroll, M. C. (1997) Impaired mast cell-dependent natural immunity in complement C3-deficient mice. Nature 390, 172-175
24. Fischer, M. B., Prodeus, A. P., Nicholson-Weller, A., Ma, M., Murrow, J., Reid, R. R., Warren, H. B., Lage, A. L., Moore, F. D., Jr., Rosen, F. S., and Carroll, M. C. (1997) Increased susceptibility to endotoxin shock in complement C3- and C4-deficient mice is corrected by C1 inhibitor replacement. J. Immunol. 159, 976-982
25. Circolo, A., Garnier, G., Fukuda, W., Wang, X., Hidvegi, T., Szalai, A. J., Briles, D. E., Volanakis, J. E., Wetsel, R. A., and Colten, H. R. (1999) Genetic disruption of the murine complement C3 promoter region generates deficient mice with extrahepatic expression of C3 mRNA. Immunopharmacology 42, 135-149
26. Baker, C. C., Chaudry, I. H., Gaines, H. O., and Baue, A. E. (1983) Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery 94, 331-335
27. Bora, P. S., Sohn, J. H., Cruz, J. M., Jha, P., Nishihori, H., Wang, Y., Kaliappan, S., Kaplan, H. J., and Bora, N. S. (2005) Role of complement and complement membrane attack complex in laser-induced choroidal neovascularization. J. Immunol. 174, 491-497
28. Leinhase, I., Holers, V. M., Thurman, J. M., Harhausen, D., Schmidt, O. I., Pietzcker, M., Taha, M. E., Rittirsch, D., Huber-Lang, M., Smith, W. R., Ward, P. A., and Stahel, P. F. (2006) Reduced neuronal cell death after experimental brain injury in mice lacking a functional alternative pathway of complement activation. BMC Neurosci. 7, 55
29. Leinhase, I., Rozanski, M., Harhausen, D., Thurman, J. M., Schmidt, O. I., Hossini, A. M., Taha, M. E., Rittirsch, D., Ward, P. A., Holers, V. M., Ertel, W., and Stahel, P. F. (2007) Inhibition of the alternative complement activation pathway in traumatic brain injury by a monoclonal anti-factor B antibody: a randomized placebo-controlled study in mice. J. Neuroinflamm. 4, 13
30. Huber-Lang, M., Sarma, J. V., Zetoune, F. S., Rittirsch, D., Neff, T. A., McGuire, S. R., Lambris, J. D., Warner, R. L., Flierl, M. A., Hoesel, L. M., Gebhard, F., Younger, J. G., Drouin, S. M., Wetsel, R. A., and Ward, P. A. (2006) Generation of C5a in the absence of C3: a new complement activation pathway. Nat. Med. 12, 682-687
31. Van Dijk, H., Rademaker, P. M., and Willers, J. M. (1980) Estimation of classical pathway of mouse complement activity by use of sensitized rabbit erythrocytes. J. Immunol. Methods 39, 257-268
32. Rittirsch, D., Flierl, M. A., Nadeau, B. A., Day, D. E., Huber-Lang, M., Mackay, C. R., Zetoune, F. S., Gerard, N. P., Cianflone, K., Koehl, J., Gerard, C., Sarma, J. V., and Ward, P. A.(2008) Functional roles of C5a receptors in sepsis. Nat. Med. 14, 551-557
33. Newman, S. L., and Mikus, L. K. (1985) Deposition of C3b and iC3b onto particulate activators of the human complement system: quantitation with monoclonal antibodies to human C3. J. Exp. Med. 161, 1414-1431
34. Gasque, P. (2004) Complement: a unique innate immune sensor for danger signals. Mol. Immunol. 41, 1089-1098
35. Mollnes, T. E., Brekke, O. L., Fung, M., Fure, H., Christiansen, D., Bergseth, G., Videm, V., Lappegard, K. T., Kohl, J., and Lambris, J. D. (2002) Essential role of the C5a receptor in E coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. Blood 100, 1869-1877
36. Brekke, O. L., Christiansen, D., Fure, H., Fung, M., and Mollnes, T. E. (2007) The role of complement C3 opsonization, C5a receptor, and CD14 in E. coli-induced up-regulation of granulocyte and monocyte CD11b/CD18 (CR3), phagocytosis, and oxidative burst in human whole blood. J. Leukoc. Biol. 81, 1404-1413
37. Buras, J. A., Rice, L., Orlow, D., Pavlides, S., Reenstra, W. R., Ceonzo, K., and Stahl, G. L. (2004) Inhibition of C5 or absence of C6 protects from sepsis mortality. Immunobiology 209, 629-635
38. Rittirsch, D., Hoesel, L. M., and Ward, P. A. (2007) The disconnect between animal models of sepsis and human sepsis. J. Leukoc. Biol. 81, 137-143
39. Ebong, S. J., Call, D. R., Bolgos, G., Newcomb, D. E., Granger, J. I., O'Reilly, M., and Remick, D. G. (1999) Immunopathologic responses to non-lethal sepsis. Shock 12, 118-126
40. Remick, D. G., Newcomb, D. E., Bolgos, G. L., and Call, D. R. (2000) Comparison of the mortality and inflammatory response of two models of sepsis: lipopolysaccharide vs. cecal ligation and puncture. Shock 13, 110-116
41. Remick, D. G., and Ward, P. A. (2005) Evaluation of endotoxin models for the study of sepsis. Shock 24(Suppl. 1), 7-11
42. Alper, C. A., Colten, H. R., Rosen, F. S., Rabson, A. R., Macnab, G. M., and Gear, J. S. (1972) Homozygous deficiency of C3 in a patient with repeated infections. Lancet 2, 1179-1181
43. Alper, C. A., Colten, H. R., Gear, J. S., Rabson, A. R., and Rosen, F. S. (1976) Homozygous human C3 deficiency: the role of C3 in antibody production, C-1s-induced vasopermeability, and cobra venom-induced passive hemolysis. J. Clin. Investig. 57, 222-229
44. Rosenfeld, S. I., Kelly, M. E., and Leddy, J. P. (1976) Hereditary deficiency of the fifth component of complement in man: I. Clinical, immunochemical, and family studies. J. Clin. Investig. 57, 1626-1634
45. Bone, R. C. (1996) Immunologic dissonance: a continuing evolution in our understanding of the systemic inflammatory response syndrome (SIRS) and the multiple organ dysfunction syndrome (MODS). Ann. Intern. Med. 125, 680-687
46. Bone, R. C. (1996) Toward a theory regarding the pathogenesis of the systemic inflammatory response syndrome: what we do and do not know about cytokine regulation. Crit. Care Med. 24, 163-172
47. Remick, D. G. (2003) Cytokine therapeutics for the treatment of sepsis: why has nothing worked? Curr. Pharm. Des. 9, 75-82
48. Gerard, C., Bruyns, C., Marchant, A., Abramowicz, D., Vandenabeele, P., Delvaux, A., Fiers, W., Goldman, M., and Velu, T. (1993) Interleukin 10 reduces the release of tumor necrosis factor and prevents lethality in experimental endotoxemia. J. Exp. Med. 177, 547-550
49. Santucci, L., Fiorucci, S., Chiorean, M., Brunori, P. M., Di Matteo, F. M., Sidoni, A., Migliorati, G., and Morelli, A. (1996) Interleukin 10 reduces lethality and hepatic injury induced by lipopolysaccharide in galactosamine-sensitized mice. Gastroenterology 111, 736-744
50. Berg, D. J., Kuhn, R., Rajewsky, K., Muller, W., Menon, S., Davidson, N., Grunig, G., and Rennick, D. (1995) Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Schwartzmann reaction but not endotoxin tolerance. J. Clin. Investig. 96, 2339-2347
51. Ashare, A., Powers, L. S., Butler, N. S., Doerschug, K. C., Monick, M. M., and Hunninghake, G. W. (2005) Anti-inflammatory response is associated with mortality and severity of infection in sepsis. Am. J. Physiol. Lung Cell Mol. Physiol. 288, L633-L640
52. Wang, Q., Wang, J. J., Fischer, J. E., and Hasselgren, P. O. (1998) Mucosal production of complement C3 and serum amyloid A is differentially regulated in different parts of the gastrointestinal tract during endotoxemia in mice. J. Gastrointest. Surg. 2, 537-546
53. Yang, H., Tuzun, E., Alagappan, D., Yu, X., Scott, B. G., Ischenko, A., and Christadoss, P. (2005) IL-1 receptor antagonist-mediated therapeutic effect in murine myasthenia gravis is associated with suppressed serum proinflammatory cytokines, C3, and anti-acetylcholine receptor IgG1. J. Immunol. 175, 2018-2025
54. Osuchowski, M. F., Welch, K., Yang, H., Siddiqui, J., and Remick, D. G. (2007) Chronic sepsis mortality characterized by an individualized inflammatory response. J. Immunol. 179, 623-630
55. Sprong, T., Brandtzaeg, P., Fung, M., Pharo, A. M., Hoiby, E. A., Michaelsen, T. E., Aase, A., van der Meer, J. W., van Deuren, M., and Mollnes, T. E. (2003) Inhibition of C5a-induced inflammation with preserved C5b-9-mediated bactericidal activity in a human whole blood model of meningococcal sepsis. Blood 102, 3702-3710