Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1986 Dec 1;164(6):1876–1888. doi: 10.1084/jem.164.6.1876

Adhesion-promoting receptors on human macrophages recognize Escherichia coli by binding to lipopolysaccharide

PMCID: PMC2188477  PMID: 3537192

Abstract

We report here that human macrophages bind Escherichia coli by recognizing bacterial lipopolysaccharide (LPS). Purified LPS was inserted into erythrocyte membranes, and the resulting LPS-coated red cells were bound by macrophages with the same temperature and cation dependence as observed for E. coli. When receptors for LPS were withdrawn from the plasma membrane by spreading the macrophages on LPS- coated surfaces, the binding of E. coli was blocked. We have also identified the receptors on macrophages that recognize LPS. Macrophages express three structurally homologous cell surface proteins, CR3, lymphocyte function-associated antigen (LFA-1), and p150,95. We used surface-bound monoclonal antireceptor antibodies to selectively remove these proteins from the apical surface of macrophages. We found that each of these proteins mediated the binding of E. coli to macrophages.

Full Text

The Full Text of this article is available as a PDF (789.8 KB).

Selected References

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

  1. Anderson D. C., Schmalstieg F. C., Arnaout M. A., Kohl S., Tosi M. F., Dana N., Buffone G. J., Hughes B. J., Brinkley B. R., Dickey W. D. Abnormalities of polymorphonuclear leukocyte function associated with a heritable deficiency of high molecular weight surface glycoproteins (GP138): common relationship to diminished cell adherence. J Clin Invest. 1984 Aug;74(2):536–551. doi: 10.1172/JCI111451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson D. C., Schmalstieg F. C., Shearer W., Becker-Freeman K., Kohl S., Smith C. W., Tosi M. F., Springer T. Leukocyte LFA-1, OKM1, p150,95 deficiency syndrome: functional and biosynthetic studies of three kindreds. Fed Proc. 1985 Jul;44(10):2671–2677. [PubMed] [Google Scholar]
  3. Andersson J., Coutinho A., Lernhardt W., Melchers F. Clonal growth and maturation to immunoglobulin secretion in vitro of every growth-inducible B lymphocyte. Cell. 1977 Jan;10(1):27–34. doi: 10.1016/0092-8674(77)90136-2. [DOI] [PubMed] [Google Scholar]
  4. Beutler B., Mahoney J., Le Trang N., Pekala P., Cerami A. Purification of cachectin, a lipoprotein lipase-suppressing hormone secreted by endotoxin-induced RAW 264.7 cells. J Exp Med. 1985 May 1;161(5):984–995. doi: 10.1084/jem.161.5.984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blackwell J. M., Ezekowitz R. A., Roberts M. B., Channon J. Y., Sim R. B., Gordon S. Macrophage complement and lectin-like receptors bind Leishmania in the absence of serum. J Exp Med. 1985 Jul 1;162(1):324–331. doi: 10.1084/jem.162.1.324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Czop J. K., Austen K. F. A beta-glucan inhibitable receptor on human monocytes: its identity with the phagocytic receptor for particulate activators of the alternative complement pathway. J Immunol. 1985 Apr;134(4):2588–2593. [PubMed] [Google Scholar]
  7. DULBECCO R., VOGT M. Plaque formation and isolation of pure lines with poliomyelitis viruses. J Exp Med. 1954 Feb;99(2):167–182. doi: 10.1084/jem.99.2.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Durum S. K., Schmidt J. A., Oppenheim J. J. Interleukin 1: an immunological perspective. Annu Rev Immunol. 1985;3:263–287. doi: 10.1146/annurev.iy.03.040185.001403. [DOI] [PubMed] [Google Scholar]
  9. English D., Andersen B. R. Single-step separation of red blood cells. Granulocytes and mononuclear leukocytes on discontinuous density gradients of Ficoll-Hypaque. J Immunol Methods. 1974 Aug;5(3):249–252. doi: 10.1016/0022-1759(74)90109-4. [DOI] [PubMed] [Google Scholar]
  10. Euteneuer B., Störkel S., Loos M. Contributions of C1q, bacterial lipopolysaccharide, and porins during attachment and ingestion phases of phagocytosis by murine macrophages. Infect Immun. 1986 Mar;51(3):807–815. doi: 10.1128/iai.51.3.807-815.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ezekowitz R. A., Sim R. B., Hill M., Gordon S. Local opsonization by secreted macrophage complement components. Role of receptors for complement in uptake of zymosan. J Exp Med. 1984 Jan 1;159(1):244–260. doi: 10.1084/jem.159.1.244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fleit H. B., Wright S. D., Unkeless J. C. Human neutrophil Fc gamma receptor distribution and structure. Proc Natl Acad Sci U S A. 1982 May;79(10):3275–3279. doi: 10.1073/pnas.79.10.3275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldman R. C., Joiner K., Leive L. Serum-resistant mutants of Escherichia coli O111 contain increased lipopolysaccharide, lack an O antigen-containing capsule, and cover more of their lipid A core with O antigen. J Bacteriol. 1984 Sep;159(3):877–882. doi: 10.1128/jb.159.3.877-882.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Guthrie L. A., McPhail L. C., Henson P. M., Johnston R. B., Jr Priming of neutrophils for enhanced release of oxygen metabolites by bacterial lipopolysaccharide. Evidence for increased activity of the superoxide-producing enzyme. J Exp Med. 1984 Dec 1;160(6):1656–1671. doi: 10.1084/jem.160.6.1656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lanier L. L., Arnaout M. A., Schwarting R., Warner N. L., Ross G. D. p150/95, Third member of the LFA-1/CR3 polypeptide family identified by anti-Leu M5 monoclonal antibody. Eur J Immunol. 1985 Jul;15(7):713–718. doi: 10.1002/eji.1830150714. [DOI] [PubMed] [Google Scholar]
  16. Mangan D. F., Snyder I. S. Mannose-sensitive interaction of Escherichia coli with human peripheral leukocytes in vitro. Infect Immun. 1979 Nov;26(2):520–527. doi: 10.1128/iai.26.2.520-527.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Medearis D. N., Jr, Camitta B. M., Heath E. C. Cell wall composition and virulence in Escherichia coli. J Exp Med. 1968 Sep 1;128(3):399–414. doi: 10.1084/jem.128.3.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Michl J., Pieczonka M. M., Unkeless J. C., Bell G. I., Silverstein S. C. Fc receptor modulation in mononuclear phagocytes maintained on immobilized immune complexes occurs by diffusion of the receptor molecule. J Exp Med. 1983 Jun 1;157(6):2121–2139. doi: 10.1084/jem.157.6.2121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Michl J., Pieczonka M. M., Unkeless J. C., Silverstein S. C. Effects of immobilized immune complexes on Fc- and complement-receptor function in resident and thioglycollate-elicited mouse peritoneal macrophages. J Exp Med. 1979 Sep 19;150(3):607–621. doi: 10.1084/jem.150.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pangburn M. K., Morrison D. C., Schreiber R. D., Müller-Eberhard H. J. Activation of the alternative complement pathway: recognition of surface structures on activators by bound C3b. J Immunol. 1980 Feb;124(2):977–982. [PubMed] [Google Scholar]
  21. Raetz C. R., Purcell S., Meyer M. V., Qureshi N., Takayama K. Isolation and characterization of eight lipid A precursors from a 3-deoxy-D-manno-octylosonic acid-deficient mutant of Salmonella typhimurium. J Biol Chem. 1985 Dec 25;260(30):16080–16088. [PubMed] [Google Scholar]
  22. Ross G. D., Cain J. A., Lachmann P. J. Membrane complement receptor type three (CR3) has lectin-like properties analogous to bovine conglutinin as functions as a receptor for zymosan and rabbit erythrocytes as well as a receptor for iC3b. J Immunol. 1985 May;134(5):3307–3315. [PubMed] [Google Scholar]
  23. Sanchez-Madrid F., Krensky A. M., Ware C. F., Robbins E., Strominger J. L., Burakoff S. J., Springer T. A. Three distinct antigens associated with human T-lymphocyte-mediated cytolysis: LFA-1, LFA-2, and LFA-3. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7489–7493. doi: 10.1073/pnas.79.23.7489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sanchez-Madrid F., Nagy J. A., Robbins E., Simon P., Springer T. A. A human leukocyte differentiation antigen family with distinct alpha-subunits and a common beta-subunit: the lymphocyte function-associated antigen (LFA-1), the C3bi complement receptor (OKM1/Mac-1), and the p150,95 molecule. J Exp Med. 1983 Dec 1;158(6):1785–1803. doi: 10.1084/jem.158.6.1785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sheetz M. P., Singer S. J. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4457–4461. doi: 10.1073/pnas.71.11.4457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Silverblatt F. J., Dreyer J. S., Schauer S. Effect of pili on susceptibility of Escherichia coli to phagocytosis. Infect Immun. 1979 Apr;24(1):218–223. doi: 10.1128/iai.24.1.218-223.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Speert D. P., Eftekhar F., Puterman M. L. Nonopsonic phagocytosis of strains of Pseudomonas aeruginosa from cystic fibrosis patients. Infect Immun. 1984 Mar;43(3):1006–1011. doi: 10.1128/iai.43.3.1006-1011.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Springer T. A., Thompson W. S., Miller L. J., Schmalstieg F. C., Anderson D. C. Inherited deficiency of the Mac-1, LFA-1, p150,95 glycoprotein family and its molecular basis. J Exp Med. 1984 Dec 1;160(6):1901–1918. doi: 10.1084/jem.160.6.1901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sung S. S., Nelson R. S., Silverstein S. C. Yeast mannans inhibit binding and phagocytosis of zymosan by mouse peritoneal macrophages. J Cell Biol. 1983 Jan;96(1):160–166. doi: 10.1083/jcb.96.1.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tomita T., Blumenstock E., Kanegasaki S. Phagocytic and chemiluminescent responses of mouse peritoneal macrophages to living and killed Salmonella typhimurium and other bacteria. Infect Immun. 1981 Jun;32(3):1242–1248. doi: 10.1128/iai.32.3.1242-1248.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wright S. D., Detmers P. A., Jong M. T., Meyer B. C. Interferon-gamma depresses binding of ligand by C3b and C3bi receptors on cultured human monocytes, an effect reversed by fibronectin. J Exp Med. 1986 May 1;163(5):1245–1259. doi: 10.1084/jem.163.5.1245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wright S. D., Levine R. P. How complement kills E. coli. I. Location of the lethal lesion. J Immunol. 1981 Sep;127(3):1146–1151. [PubMed] [Google Scholar]
  33. Wright S. D., Rao P. E., Van Voorhis W. C., Craigmyle L. S., Iida K., Talle M. A., Westberg E. F., Goldstein G., Silverstein S. C. Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5699–5703. doi: 10.1073/pnas.80.18.5699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wright S. D., Silverstein S. C. Tumor-promoting phorbol esters stimulate C3b and C3b' receptor-mediated phagocytosis in cultured human monocytes. J Exp Med. 1982 Oct 1;156(4):1149–1164. doi: 10.1084/jem.156.4.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES