Disruption of the C5a receptor gene increases resistance to acute Gram-negative bacteremia and endotoxic shock: Opposing roles of C3a and C5a

Molecular Immunology

Volumn 45, Issue 7, 2008, Pages 1907-1915

  Hollmann, Travis J ^a,b   Mueller Ortiz, Stacey L ^a   Braun, Michael C ^a   Wetsel, Rick A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Anaphylatoxins; Complement; Knock out Mice; Sepsis; Shock

Indexed keywords

ANTIHISTAMINIC AGENT; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A RECEPTOR; DIPHENHYDRAMINE; ESCHERICHIA COLI ENDOTOXIN; TRIPROLIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOPHIL; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; ESCHERICHIA COLI; FEMALE; GENE DISRUPTION; GRAM NEGATIVE SEPSIS; HEMOCONCENTRATION; HISTAMINE RELEASE; HOST RESISTANCE; MALE; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR GENE; SEPTIC SHOCK; THROMBOCYTOPENIA;

ACUTE DISEASE; ANIMALS; BACTEREMIA; COMPLEMENT C3A; COMPLEMENT C5A; DISEASE SUSCEPTIBILITY; FLOW CYTOMETRY; GENE TARGETING; GRAM-NEGATIVE BACTERIA; HEMATOCRIT; HISTAMINE ANTAGONISTS; IMMUNITY, NATURAL; MACROPHAGES, PERITONEAL; MAST CELLS; MICE; PLATELET COUNT; RECEPTOR, ANAPHYLATOXIN C5A; SHOCK, SEPTIC;

ANIMALIA; ESCHERICHIA COLI; MURINAE; MUS; NEGIBACTERIA;

EID: 39149091052     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2007.10.037     Document Type: Article

References (45)

1. Bao L., Gerard N.P., Eddy Jr. R.L., Shows T.B., and Gerard C. Mapping of genes for the human C5a receptor (C5AR), human FMLP receptor (FPR), and two FMLP receptor homologue orphan receptors (FPRH1, FPRH2) to chromosome 19. Genomics 13 (1992) 437-440
2. Bygrave A.E., Rose K.L., Cortes-Hernandez J., Warren J., Rigby R.J., Cook H.T., Walport M.J., Vyse T.J., and Botto M. Spontaneous autoimmunity in 129 and C57BL/6 mice-implications for autoimmunity described in gene-targeted mice. PLoS Biol. 2 (2004) E243
3. Cole L., Bellomo R., Hart G., Journois D., Davenport P., Tipping P., and Ronco C. A phase II randomized, controlled trial of continuous hemofiltration in sepsis. Crit. Care Med. 30 (2002) 100-106
4. Drouin S.M., Kildsgaard J., Haviland J., Zabner J., Jia H.P., McCray Jr. P.B., Tack B.F., and Wetsel R.A. Expression of the complement anaphylatoxin C3a and C5a receptors on bronchial epithelial and smooth muscle cells in models of sepsis and asthma. J. Immunol. 166 (2001) 2025-2032
5. Ember J.A., Jagels M.A., and Hugli T.E. In: Frank M., and Volanakis J.E. (Eds). Human Complement System in Health and Disease (1998), Marcel Dekker, Inc, New York 241-284
6. Ewart S.L., Kuperman D., Schadt E., Tankersley C., Grupe A., Shubitowski D.M., Peltz G., and Wills-Karp M. Quantitative trait loci controlling allergen-induced airway hyperresponsiveness in inbred mice. Am. J. Respir. Cell Mol. Biol. 23 (2000) 537-545
7. Fischer W.H., and Hugli T.E. Regulation of B cell functions by C3a and C3a(desArg): suppression of TNF-alpha, IL-6, and the polyclonal immune response. J. Immunol. 159 (1997) 4279-4286
8. Friedberger E. Weitere untersuchungen uber eisissanaphylaxie: IV. Mitteilung. Immunitaetaforsch. Exp. Ther. 4 (1910) 636-690
9. Groeneveld A.B., Tacx A.N., Bossink A.W., van Mierlo G.J., and Hack C.E. Circulating inflammatory mediators predict shock and mortality in febrile patients with microbial infection. Clin. Immunol. 106 (2003) 106-115
10. Gulbins E., Siow Y., and Vitale G.C. Complement 5a induces in vivo synthesis of cysteinyl leukotrienes in rats. Prostaglandins Leukot. Essent. Fatty Acids 48 (1993) 331-334
11. Guo R.F., Riedemann N.C., Laudes I.J., Sarma V.J., Kunkel R.G., Dilley K.A., Paulauskis J.D., and Ward P.A. Altered neutrophil trafficking during sepsis. J. Immunol. 169 (2002) 307-314
12. Guo R.F., Riedemann N.C., and Ward P.A. Role of C5a-C5aR interaction in sepsis. Shock 21 (2004) 1-7
13. 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. Elevated plasma levels of the anaphylatoxins C3a and C4a are associated with a fatal outcome in sepsis. Am. J. Med. 86 (1989) 20-26
14. Hecke F., Schmidt U., Kola A., Bautsch W., Klos A., and Kohl J. Circulating complement proteins in multiple trauma patients-correlation with injury severity, development of sepsis, and outcome. Crit. Care Med. 25 (1997) 2015-2024
15. Hopken U.E., Lu B., Gerard N.P., and Gerard C. The C5a chemoattractant receptor mediates mucosal defence to infection. Nature 383 (1996) 86-89
16. Hug B.A., Wesselschmidt R.L., Fiering S., Bender M.A., Epner E., Groudine M., and Ley T.J. Analysis of mice containing a targeted deletion of beta-globin locus control region 5′ hypersensitive site 3. Mol. Cell Biol. 16 (1996) 2906-2912
17. Hugli T.E., and Muller-Eberhard H.J. Anaphylatoxins: C3a and C5a. Adv. Immunol. 26 (1978) 1-53
18. Humbles A.A., Lu B., Nilsson C.A., Lilly C., Israel E., Fujiwara Y., Gerard N.P., and Gerard C. A role for the C3a anaphylatoxin receptor in the effector phase of asthma. Nature 406 (2000) 998-1001
19. Joiner K.A., Brown E.J., and Frank M.M. Complement and bacteria: chemistry and biology in host defense. Annu. Rev. Immunol. 2 (1984) 461-491
20. Joiner K.A., Goldman R., Schmetz M., Berger M., Hammer C.H., Frank M.M., and Leive L. A quantitative analysis of C3 binding to O-antigen capsule, lipopolysaccharide, and outer membrane protein of E. coli 0111B4. J. Immunol. 132 (1984) 369-375
21. Kildsgaard J., Hollmann T.J., Matthews K.W., Bian K., Murad F., and Wetsel R.A. Cutting edge: targeted disruption of the C3a receptor gene demonstrates a novel protective anti-inflammatory role for C3a in endotoxin-shock. J. Immunol. 165 (2000) 5406-5409
22. Kong P.L., Morel L., Croker B.P., and Craft J. The centromeric region of chromosome 7 from MRL mice (Lmb3) is an epistatic modifier of Fas for autoimmune disease expression. J. Immunol. 172 (2004) 2785-2794
23. Li P., Allen H., Banerjee S., Franklin S., Herzog L., Johnston C., McDowell J., Paskind M., Rodman L., Salfeld J., et al. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80 (1995) 401-411
24. Lundberg C., Marceau F., and Hugli T.E. C5a-induced hemodynamic and hematologic changes in the rabbit. Role of cyclooxygenase products and polymorphonuclear leukocytes. Am. J. Pathol. 128 (1987) 471-483
25. Matthews K.W., Mueller-Ortiz S.L., and Wetsel R.A. Carboxypeptidase N: a pleiotropic regulator of inflammation. Mol. Immunol. 40 (2004) 785-793
26. Michell B.B. Preparation of mouse cell suspensions. In: Shiigi B.B.M.a.S.M. (Ed). Selected Methods in Cellular Immunology (1980), W.H. Freeman and Company, San Francisco 3-13
27. Mohan C., Yu Y., Morel L., Yang P., and Wakeland E.K. Genetic dissection of Sle pathogenesis: Sle3 on murine chromosome 7 impacts T cell activation, differentiation, and cell death. J. Immunol. 162 (1999) 6492-6502
28. Mohr M., Hopken U., Oppermann M., Mathes C., Goldmann K., Siever S., Gotze O., and Burchardi H. Effects of anti-C5a monoclonal antibodies on oxygen use in a porcine model of severe sepsis. Eur. J. Clin. Invest. 28 (1998) 227-234
29. Morrison D.C., and Ulevitch R.J. The effects of bacterial endotoxins on host mediation systems. A review. Am. J. Pathol. 93 (1978) 526-617
30. Nakae H., Endo S., Inada K., and Yoshida M. Chronological changes in the complement system in sepsis. Surg. Today 26 (1996) 225-229
31. Ober C., Cox N.J., Abney M., Di Rienzo A., Lander E.S., Changyaleket B., Gidley H., Kurtz B., Lee J., Nance M., Pettersson A., Prescott J., Richardson A., Schlenker E., Summerhill E., Willadsen S., and Parry R. Genome-wide search for asthma susceptibility loci in a founder population. The Collaborative Study on the Genetics of Asthma. Hum. Mol. Genet. 7 (1998) 1393-1398
32. Pangburn M.K., Morrison D.C., Schreiber R.D., and Muller-Eberhard H.J. Activation of the alternative complement pathway: recognition of surface structures on activators by bound C3b. J. Immunol. 124 (1980) 977-982
33. Pavek K., Piper P.J., and Smedegard G. Anaphylatoxin-induced shock and two patterns of anaphylactic shock: hemodynamics and mediators. Acta Physiol. Scand. 105 (1979) 393-403
34. Reid R.R., Prodeus A.P., Khan W., Hsu T., Rosen F.S., and Carroll M.C. Endotoxin shock in antibody-deficient mice: unraveling the role of natural antibody and complement in the clearance of lipopolysaccharide. J. Immunol. 159 (1997) 970-975
35. Riedemann N.C., Guo R.F., Bernacki K.D., Reuben J.S., Laudes I.J., Neff T.A., Gao H., Speyer C., Sarma V.J., Zetoune F.S., and Ward P.A. Regulation by C5a of neutrophil activation during sepsis. Immunity 19 (2003) 193-202
36. Riedemann N.C., Guo R.F., Neff T.A., Laudes I.J., Keller K.A., Sarma V.J., Markiewski M.M., Mastellos D., Strey C.W., Pierson C.L., Lambris J.D., Zetoune F.S., and Ward P.A. Increased C5a receptor expression in sepsis. J. Clin. Invest. 110 (2002) 101-108
37. Selberg O., Hecker H., Martin M., Klos A., Bautsch W., and Kohl J. Discrimination of sepsis and systemic inflammatory response syndrome by determination of circulating plasma concentrations of procalcitonin, protein complement 3a, and interleukin-6. Crit. Care Med. 28 (2000) 2793-2798
38. Smedegard G., Cui L.X., and Hugli T.E. Endotoxin-induced shock in the rat. A role for C5a. Am. J. Pathol. 135 (1989) 489-497
39. Stevens J.H., O'Hanley P., Shapiro J.M., Mihm F.G., Satoh P.S., Collins J.A., and Raffin T.A. Effects of anti-C5a antibodies on the adult respiratory distress syndrome in septic primates. J. Clin. Invest. 77 (1986) 1812-1816
40. Stove S., Welte T., Wagner T.O., Kola A., Klos A., Bautsch W., and Kohl J. Circulating complement proteins in patients with sepsis or systemic inflammatory response syndrome. Clin. Diagn. Lab. Immunol. 3 (1996) 175-183
41. Takabayashi T., Vannier E., Burke J.F., Tompkins R.G., Gelfand J.A., and Clark B.D. Both C3a and C3a(desArg) regulate interleukin-6 synthesis in human peripheral blood mononuclear cells. J. Infect. Dis. 177 (1998) 1622-1628
42. Takabayashi T., Vannier E., Clark B.D., Margolis N.H., Dinarello C.A., Burke J.F., and Gelfand J.A. A new biologic role for C3a and C3a desArg: regulation of TNF-alpha and IL-1 beta synthesis. J. Immunol. 156 (1996) 3455-3460
43. Vogt W. Anaphylatoxins: possible roles in disease. Complement 3 (1986) 177-188
44. Wetsel R.A., Kildsgaard J., and Haviland D.L. Complement anaphylatoxins (C3a,C4a, and C5a) and their receptors (C3aR, C5aR/CD88) as therapeutic targets in inflammation. In: Lambris J.D., and Holers V.M. (Eds). Therapeutic Interventions in the Complement System (2000), Humana Press, Totowa, New Jersey 113-153
45. Zhao L., Ohtaki Y., Yamaguchi K., Matsushita M., Fujita T., Yokochi T., Takada H., and Endo Y. LPS-induced platelet response and rapid shock in mice: contribution of O-antigen region of LPS and involvement of the lectin pathway of the complement system. Blood 100 (2002) 3233-3239