Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1995 Dec;63(12):4939–4943. doi: 10.1128/iai.63.12.4939-4943.1995

Antibody-independent binding of complement component C1q by Legionella pneumophila.

C S Mintz 1, P I Arnold 1, W Johnson 1, D R Schultz 1
PMCID: PMC173710  PMID: 7591161

Abstract

Incubation of Legionella pneumophila Philadelphia 1 in normal human serum depleted of either classical-pathway component C1q or alternative-pathway component factor B resulted in activation of the complement system. Experiments focused on the role of the classical pathway in complement activation revealed that legionellae bound C1q independently of antibody. Purified preparations of L. pneumophila major outer membrane protein but not serogroup 1 lipopolysaccharide bound C1q independently of antibody. This suggests that antibody-independent binding of C1q by L. pneumophila can result in activation of the classical pathway in normal human serum and that major outer membrane protein may be a C1q acceptor on the L. pneumophila cell surface.

Full Text

The Full Text of this article is available as a PDF (210.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albertí S., Marqués G., Camprubí S., Merino S., Tomás J. M., Vivanco F., Benedí V. J. C1q binding and activation of the complement classical pathway by Klebsiella pneumoniae outer membrane proteins. Infect Immun. 1993 Mar;61(3):852–860. doi: 10.1128/iai.61.3.852-860.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Albertí S., Rodríquez-Quiñones F., Schirmer T., Rummel G., Tomás J. M., Rosenbusch J. P., Benedí V. J. A porin from Klebsiella pneumoniae: sequence homology, three-dimensional model, and complement binding. Infect Immun. 1995 Mar;63(3):903–910. doi: 10.1128/iai.63.3.903-910.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Alvarez-Dominguez C., Carrasco-Marin E., Leyva-Cobian F. Role of complement component C1q in phagocytosis of Listeria monocytogenes by murine macrophage-like cell lines. Infect Immun. 1993 Sep;61(9):3664–3672. doi: 10.1128/iai.61.9.3664-3672.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bellinger-Kawahara C., Horwitz M. A. Complement component C3 fixes selectively to the major outer membrane protein (MOMP) of Legionella pneumophila and mediates phagocytosis of liposome-MOMP complexes by human monocytes. J Exp Med. 1990 Oct 1;172(4):1201–1210. doi: 10.1084/jem.172.4.1201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dreyfus L. A. Virulence associated ingestion of Legionella pneumophila by HeLa cells. Microb Pathog. 1987 Jul;3(1):45–52. doi: 10.1016/0882-4010(87)90036-2. [DOI] [PubMed] [Google Scholar]
  6. Ehret W., Ruckdeschel G. Membrane proteins of legionellaceae. I. Membrane proteins of different strains and serogroups of Legionella pneumophila. Zentralbl Bakteriol Mikrobiol Hyg A. 1985 Jul;259(4):433–445. doi: 10.1016/s0176-6724(85)80075-4. [DOI] [PubMed] [Google Scholar]
  7. Fields B. S., Barbaree J. M., Shotts E. B., Jr, Feeley J. C., Morrill W. E., Sanden G. N., Dykstra M. J. Comparison of guinea pig and protozoan models for determining virulence of Legionella species. Infect Immun. 1986 Sep;53(3):553–559. doi: 10.1128/iai.53.3.553-559.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Forsgren A., Mclean R. H., Michael A. F., Quie P. G. Studies of the alternate pathway in chelated serum. J Lab Clin Med. 1975 Jun;85(6):904–912. [PubMed] [Google Scholar]
  9. Gabay J. E., Blake M., Niles W. D., Horwitz M. A. Purification of Legionella pneumophila major outer membrane protein and demonstration that it is a porin. J Bacteriol. 1985 Apr;162(1):85–91. doi: 10.1128/jb.162.1.85-91.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Galdiero F., Tufano M. A., Sommese L., Folgore A., Tedesco F. Activation of complement system by porins extracted from Salmonella typhimurium. Infect Immun. 1984 Nov;46(2):559–563. doi: 10.1128/iai.46.2.559-563.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Guan E. N., Burgess W. H., Robinson S. L., Goodman E. B., McTigue K. J., Tenner A. J. Phagocytic cell molecules that bind the collagen-like region of C1q. Involvement in the C1q-mediated enhancement of phagocytosis. J Biol Chem. 1991 Oct 25;266(30):20345–20355. [PubMed] [Google Scholar]
  12. Hoffman P. S., Ripley M., Weeratna R. Cloning and nucleotide sequence of a gene (ompS) encoding the major outer membrane protein of Legionella pneumophila. J Bacteriol. 1992 Feb;174(3):914–920. doi: 10.1128/jb.174.3.914-920.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hoffman P. S., Seyer J. H., Butler C. A. Molecular characterization of the 28- and 31-kilodalton subunits of the Legionella pneumophila major outer membrane protein. J Bacteriol. 1992 Feb;174(3):908–913. doi: 10.1128/jb.174.3.908-913.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Holden E. P., Winkler H. H., Wood D. O., Leinbach E. D. Intracellular growth of Legionella pneumophila within Acanthamoeba castellanii Neff. Infect Immun. 1984 Jul;45(1):18–24. doi: 10.1128/iai.45.1.18-24.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Horwitz M. A., Silverstein S. C. Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest. 1980 Sep;66(3):441–450. doi: 10.1172/JCI109874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Husmann L. K., Johnson W. Adherence of Legionella pneumophila to guinea pig peritoneal macrophages, J774 mouse macrophages, and undifferentiated U937 human monocytes: role of Fc and complement receptors. Infect Immun. 1992 Dec;60(12):5212–5218. doi: 10.1128/iai.60.12.5212-5218.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Joiner K. A., Hawiger A., Gelfand J. A. A study of optimal reaction conditions for an assay of the human alternative complement pathway. Am J Clin Pathol. 1983 Jan;79(1):65–72. doi: 10.1093/ajcp/79.1.65. [DOI] [PubMed] [Google Scholar]
  18. Latsch M., Möllerfeld J., Ringsdorf H., Loos M. Studies on the interaction of C1q, a subcomponent of the first component of complement, with porins from Salmonella minnesota incorporated into artificial membranes. FEBS Lett. 1990 Dec 10;276(1-2):201–204. doi: 10.1016/0014-5793(90)80542-q. [DOI] [PubMed] [Google Scholar]
  19. Loos M., Bitter-Suermann D., Dierich M. Interaction of the first (C1), the second (C2) and the fourth (C4) component of complement with different preparations of bacterial lipopolysaccharides and with lipid A. J Immunol. 1974 Mar;112(3):935–940. [PubMed] [Google Scholar]
  20. Loos M., Clas F. Antibody-independent killing of gram-negative bacteria via the classical pathway of complement. Immunol Lett. 1987 Feb;14(3):203–208. doi: 10.1016/0165-2478(87)90102-7. [DOI] [PubMed] [Google Scholar]
  21. Loos M., Wellek B., Thesen R., Opferkuch W. Antibody-independent interaction of the first component of complement with Gram-negative bacteria. Infect Immun. 1978 Oct;22(1):5–9. doi: 10.1128/iai.22.1.5-9.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MULLER-EBERHARD H. J., KUNKEL H. G. Isolation of a thermolabile serum protein which precipitates gamma-globulin aggregates and participates in immune hemolysis. Proc Soc Exp Biol Med. 1961 Feb;106:291–295. doi: 10.3181/00379727-106-26313. [DOI] [PubMed] [Google Scholar]
  23. Mintz C. S., Schultz D. R., Arnold P. I., Johnson W. Legionella pneumophila lipopolysaccharide activates the classical complement pathway. Infect Immun. 1992 Jul;60(7):2769–2776. doi: 10.1128/iai.60.7.2769-2776.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Newsome A. L., Baker R. L., Miller R. D., Arnold R. R. Interactions between Naegleria fowleri and Legionella pneumophila. Infect Immun. 1985 Nov;50(2):449–452. doi: 10.1128/iai.50.2.449-452.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Payne N. R., Horwitz M. A. Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J Exp Med. 1987 Nov 1;166(5):1377–1389. doi: 10.1084/jem.166.5.1377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pearlman E., Jiwa A. H., Engleberg N. C., Eisenstein B. I. Growth of Legionella pneumophila in a human macrophage-like (U937) cell line. Microb Pathog. 1988 Aug;5(2):87–95. doi: 10.1016/0882-4010(88)90011-3. [DOI] [PubMed] [Google Scholar]
  27. Stemmer F., Loos M. Evidence for direct binding of the first component of complement, C1, to outer membrane proteins from Salmonella minnesota. Curr Top Microbiol Immunol. 1985;121:73–84. doi: 10.1007/978-3-642-45604-6_4. [DOI] [PubMed] [Google Scholar]
  28. Summersgill J. T., Raff M. J., Miller R. D. Interactions of virulent and avirulent Legionella pneumophila with human polymorphonuclear leukocytes. Microb Pathog. 1988 Jul;5(1):41–47. doi: 10.1016/0882-4010(88)90079-4. [DOI] [PubMed] [Google Scholar]
  29. Tenner A. J., Cooper N. R. Analysis of receptor-mediated C1q binding to human peripheral blood mononuclear cells. J Immunol. 1980 Oct;125(4):1658–1664. [PubMed] [Google Scholar]
  30. Verbrugh H. A., Lee D. A., Elliott G. R., Keane W. F., Hoidal J. R., Peterson P. K. Opsonization of Legionella pneumophila in human serum: key roles for specific antibodies and the classical complement pathway. Immunology. 1985 Apr;54(4):643–653. [PMC free article] [PubMed] [Google Scholar]
  31. Vroon D. H., Schultz D. R., Zarco R. M. The separation of nine components and two inactivators of components of complement in humansserum. Immunochemistry. 1970 Jan;7(1):43–61. doi: 10.1016/0019-2791(70)90029-7. [DOI] [PubMed] [Google Scholar]
  32. Zhang S. C., Schultz D. R., Ryan U. S. Receptor-mediated binding of C1q on pulmonary endothelial cells. Tissue Cell. 1986;18(1):13–18. doi: 10.1016/0040-8166(86)90003-0. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES