Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1994 Oct 15;303(Pt 2):407–411. doi: 10.1042/bj3030407

Binding of surfactant protein A to the lipid A moiety of bacterial lipopolysaccharides.

J F Van Iwaarden 1, J C Pikaar 1, J Storm 1, E Brouwer 1, J Verhoef 1, R S Oosting 1, L M van Golde 1, J A van Strijp 1
PMCID: PMC1137342  PMID: 7980398

Abstract

Surfactant protein A (SP-A) enhances the phagocytosis of opsonized and non-opsonized bacteria by alveolar macrophages, but it is not known with which component of the bacterial surface it associates. We investigated the interaction of SP-A with lipopolysaccharides (LPS), which are important biologically active constituents of the outer membranes of Gram-negative bacteria. Flow cytometry was used to study the binding of fluorescein isothiocyanate-labelled SP-A either to LPS of various chain lengths coupled to magnetic beads or to Gram-negative bacteria. The binding of SP-A to LPS-coated beads was saturable, both time- and concentration-dependent, and required both Ca2+ and Na+. SP-A bound to the lipid A moiety of LPS and to LPS from either the Re-mutant of Salmonella minnesota or the J5-mutant of Escherichia coli. In contrast, it did not bind to O111 LPS of E. coli, suggesting that SP-A binds only to rough LPS. The binding of SP-A to LPS was not affected by mannan and heparin or by deglycosylation of the SP-A, indicating that the carbohydrate-binding domain and the carbohydrate moiety of SP-A are not involved in its interaction with LPS. We also observed saturable and concentration-dependent binding of SP-A to the live J5 mutant of whole E. coli, but not to its O111 mutant. In addition, Re LPS aggregated in the presence of SP-A, Ca2+ and Na+. We conclude that SP-A associates with LPS via the lipid A moiety of rough LPS and may be involved in the anti-bacterial defences of the lung.

Full text

PDF
407

Selected References

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

  1. Baughman R. P., Sternberg R. I., Hull W., Buchsbaum J. A., Whitsett J. Decreased surfactant protein A in patients with bacterial pneumonia. Am Rev Respir Dis. 1993 Mar;147(3):653–657. doi: 10.1164/ajrccm/147.3.653. [DOI] [PubMed] [Google Scholar]
  2. Benson B., Hawgood S., Schilling J., Clements J., Damm D., Cordell B., White R. T. Structure of canine pulmonary surfactant apoprotein: cDNA and complete amino acid sequence. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6379–6383. doi: 10.1073/pnas.82.19.6379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Childs R. A., Wright J. R., Ross G. F., Yuen C. T., Lawson A. M., Chai W., Drickamer K., Feizi T. Specificity of lung surfactant protein SP-A for both the carbohydrate and the lipid moieties of certain neutral glycolipids. J Biol Chem. 1992 May 15;267(14):9972–9979. [PubMed] [Google Scholar]
  4. Chung J., Yu S. H., Whitsett J. A., Harding P. G., Possmayer F. Effect of surfactant-associated protein-A (SP-A) on the activity of lipid extract surfactant. Biochim Biophys Acta. 1989 Apr 26;1002(3):348–358. doi: 10.1016/0005-2760(89)90349-4. [DOI] [PubMed] [Google Scholar]
  5. Drickamer K. Two distinct classes of carbohydrate-recognition domains in animal lectins. J Biol Chem. 1988 Jul 15;263(20):9557–9560. [PubMed] [Google Scholar]
  6. Erich T., Schellekens J., Bouter A., Van Kranen J., Brouwer E., Verhoef J. Binding characteristics and cross-reactivity of three different antilipid A monoclonal antibodies. J Immunol. 1989 Dec 15;143(12):4053–4060. [PubMed] [Google Scholar]
  7. Haagsman H. P., Elfring R. H., van Buel B. L., Voorhout W. F. The lung lectin surfactant protein A aggregates phospholipid vesicles via a novel mechanism. Biochem J. 1991 Apr 1;275(Pt 1):273–276. doi: 10.1042/bj2750273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Haagsman H. P., Hawgood S., Sargeant T., Buckley D., White R. T., Drickamer K., Benson B. J. The major lung surfactant protein, SP 28-36, is a calcium-dependent, carbohydrate-binding protein. J Biol Chem. 1987 Oct 15;262(29):13877–13880. [PubMed] [Google Scholar]
  9. Haagsman H. P., White R. T., Schilling J., Lau K., Benson B. J., Golden J., Hawgood S., Clements J. A. Studies of the structure of lung surfactant protein SP-A. Am J Physiol. 1989 Dec;257(6 Pt 1):L421–L429. doi: 10.1152/ajplung.1989.257.6.L421. [DOI] [PubMed] [Google Scholar]
  10. Hartley C. A., Jackson D. C., Anders E. M. Two distinct serum mannose-binding lectins function as beta inhibitors of influenza virus: identification of bovine serum beta inhibitor as conglutinin. J Virol. 1992 Jul;66(7):4358–4363. doi: 10.1128/jvi.66.7.4358-4363.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hawgood S., Benson B. J., Schilling J., Damm D., Clements J. A., White R. T. Nucleotide and amino acid sequences of pulmonary surfactant protein SP 18 and evidence for cooperation between SP 18 and SP 28-36 in surfactant lipid adsorption. Proc Natl Acad Sci U S A. 1987 Jan;84(1):66–70. doi: 10.1073/pnas.84.1.66. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hawgood S. Pulmonary surfactant apoproteins: a review of protein and genomic structure. Am J Physiol. 1989 Aug;257(2 Pt 1):L13–L22. doi: 10.1152/ajplung.1989.257.2.L13. [DOI] [PubMed] [Google Scholar]
  13. Ikeda K., Sannoh T., Kawasaki N., Kawasaki T., Yamashina I. Serum lectin with known structure activates complement through the classical pathway. J Biol Chem. 1987 Jun 5;262(16):7451–7454. [PubMed] [Google Scholar]
  14. Kawasaki N., Kawasaki T., Yamashina I. A serum lectin (mannan-binding protein) has complement-dependent bactericidal activity. J Biochem. 1989 Sep;106(3):483–489. doi: 10.1093/oxfordjournals.jbchem.a122878. [DOI] [PubMed] [Google Scholar]
  15. King R. J., Simon D., Horowitz P. M. Aspects of secondary and quaternary structure of surfactant protein A from canine lung. Biochim Biophys Acta. 1989 Feb 20;1001(3):294–301. doi: 10.1016/0005-2760(89)90114-8. [DOI] [PubMed] [Google Scholar]
  16. Kuan S. F., Rust K., Crouch E. Interactions of surfactant protein D with bacterial lipopolysaccharides. Surfactant protein D is an Escherichia coli-binding protein in bronchoalveolar lavage. J Clin Invest. 1992 Jul;90(1):97–106. doi: 10.1172/JCI115861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kuhlman M., Joiner K., Ezekowitz R. A. The human mannose-binding protein functions as an opsonin. J Exp Med. 1989 May 1;169(5):1733–1745. doi: 10.1084/jem.169.5.1733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kuroki Y., Akino T. Pulmonary surfactant protein A (SP-A) specifically binds dipalmitoylphosphatidylcholine. J Biol Chem. 1991 Feb 15;266(5):3068–3073. [PubMed] [Google Scholar]
  19. Kuroki Y., Gasa S., Ogasawara Y., Makita A., Akino T. Binding of pulmonary surfactant protein A to galactosylceramide and asialo-GM2. Arch Biochem Biophys. 1992 Dec;299(2):261–267. doi: 10.1016/0003-9861(92)90273-y. [DOI] [PubMed] [Google Scholar]
  20. Kuroki Y., Shiratori M., Ogasawara Y., Tsuzuki A., Akino T. Characterization of pulmonary surfactant protein D: its copurification with lipids. Biochim Biophys Acta. 1991 Nov 5;1086(2):185–190. doi: 10.1016/0005-2760(91)90006-4. [DOI] [PubMed] [Google Scholar]
  21. Lachmann P. J. Conglutinin and immunoconglutinins. Adv Immunol. 1967;6:479–527. doi: 10.1016/s0065-2776(08)60527-1. [DOI] [PubMed] [Google Scholar]
  22. Manz-Keinke H., Plattner H., Schlepper-Schäfer J. Lung surfactant protein A (SP-A) enhances serum-independent phagocytosis of bacteria by alveolar macrophages. Eur J Cell Biol. 1992 Feb;57(1):95–100. [PubMed] [Google Scholar]
  23. Martin T. R., Mathison J. C., Tobias P. S., Letúrcq D. J., Moriarty A. M., Maunder R. J., Ulevitch R. J. Lipopolysaccharide binding protein enhances the responsiveness of alveolar macrophages to bacterial lipopolysaccharide. Implications for cytokine production in normal and injured lungs. J Clin Invest. 1992 Dec;90(6):2209–2219. doi: 10.1172/JCI116106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Phelps D. S., Floros J. Localization of surfactant protein synthesis in human lung by in situ hybridization. Am Rev Respir Dis. 1988 Apr;137(4):939–942. doi: 10.1164/ajrccm/137.4.939. [DOI] [PubMed] [Google Scholar]
  25. Possmayer F. A proposed nomenclature for pulmonary surfactant-associated proteins. Am Rev Respir Dis. 1988 Oct;138(4):990–998. doi: 10.1164/ajrccm/138.4.990. [DOI] [PubMed] [Google Scholar]
  26. Raetz C. R., Ulevitch R. J., Wright S. D., Sibley C. H., Ding A., Nathan C. F. Gram-negative endotoxin: an extraordinary lipid with profound effects on eukaryotic signal transduction. FASEB J. 1991 Sep;5(12):2652–2660. doi: 10.1096/fasebj.5.12.1916089. [DOI] [PubMed] [Google Scholar]
  27. Raponi G., Keller N., Overbeek B. P., Rozenberg-Arska M., van Kessel K. P., Verhoef J. Enhanced phagocytosis of encapsulated Escherichia coli strains after exposure to sub-MICs of antibiotics is correlated to changes of the bacterial cell surface. Antimicrob Agents Chemother. 1990 Feb;34(2):332–336. doi: 10.1128/aac.34.2.332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Suzuki Y., Fujita Y., Kogishi K. Reconstitution of tubular myelin from synthetic lipids and proteins associated with pig pulmonary surfactant. Am Rev Respir Dis. 1989 Jul;140(1):75–81. doi: 10.1164/ajrccm/140.1.75. [DOI] [PubMed] [Google Scholar]
  29. Tenner A. J., Robinson S. L., Borchelt J., Wright J. R. Human pulmonary surfactant protein (SP-A), a protein structurally homologous to C1q, can enhance FcR- and CR1-mediated phagocytosis. J Biol Chem. 1989 Aug 15;264(23):13923–13928. [PubMed] [Google Scholar]
  30. Thiel S. Mannan-binding protein, a complement activating animal lectin. Immunopharmacology. 1992 Sep-Oct;24(2):91–99. doi: 10.1016/0162-3109(92)90015-5. [DOI] [PubMed] [Google Scholar]
  31. Thiel S., Reid K. B. Structures and functions associated with the group of mammalian lectins containing collagen-like sequences. FEBS Lett. 1989 Jun 19;250(1):78–84. doi: 10.1016/0014-5793(89)80689-1. [DOI] [PubMed] [Google Scholar]
  32. Van Iwaarden J. F., Shimizu H., Van Golde P. H., Voelker D. R., Van Golde L. M. Rat surfactant protein D enhances the production of oxygen radicals by rat alveolar macrophages. Biochem J. 1992 Aug 15;286(Pt 1):5–8. doi: 10.1042/bj2860005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Voorhout W. F., Veenendaal T., Kuroki Y., Ogasawara Y., van Golde L. M., Geuze H. J. Immunocytochemical localization of surfactant protein D (SP-D) in type II cells, Clara cells, and alveolar macrophages of rat lung. J Histochem Cytochem. 1992 Oct;40(10):1589–1597. doi: 10.1177/40.10.1527377. [DOI] [PubMed] [Google Scholar]
  34. Voss T., Eistetter H., Schäfer K. P., Engel J. Macromolecular organization of natural and recombinant lung surfactant protein SP 28-36. Structural homology with the complement factor C1q. J Mol Biol. 1988 May 5;201(1):219–227. doi: 10.1016/0022-2836(88)90448-2. [DOI] [PubMed] [Google Scholar]
  35. Wakamiya N., Okuno Y., Sasao F., Ueda S., Yoshimatsu K., Naiki M., Kurimura T. Isolation and characterization of conglutinin as an influenza A virus inhibitor. Biochem Biophys Res Commun. 1992 Sep 30;187(3):1270–1278. doi: 10.1016/0006-291x(92)90440-v. [DOI] [PubMed] [Google Scholar]
  36. Wright J. R., Clements J. A. Metabolism and turnover of lung surfactant. Am Rev Respir Dis. 1987 Aug;136(2):426–444. doi: 10.1164/ajrccm/136.2.426. [DOI] [PubMed] [Google Scholar]
  37. Wright J. R., Wager R. E., Hawgood S., Dobbs L., Clements J. A. Surfactant apoprotein Mr = 26,000-36,000 enhances uptake of liposomes by type II cells. J Biol Chem. 1987 Feb 25;262(6):2888–2894. [PubMed] [Google Scholar]
  38. Wright J. R., Youmans D. C. Pulmonary surfactant protein A stimulates chemotaxis of alveolar macrophage. Am J Physiol. 1993 Apr;264(4 Pt 1):L338–L344. doi: 10.1152/ajplung.1993.264.4.L338. [DOI] [PubMed] [Google Scholar]
  39. van Iwaarden F., Welmers B., Verhoef J., Haagsman H. P., van Golde L. M. Pulmonary surfactant protein A enhances the host-defense mechanism of rat alveolar macrophages. Am J Respir Cell Mol Biol. 1990 Jan;2(1):91–98. doi: 10.1165/ajrcmb/2.1.91. [DOI] [PubMed] [Google Scholar]
  40. van Iwaarden J. F., van Strijp J. A., Ebskamp M. J., Welmers A. C., Verhoef J., van Golde L. M. Surfactant protein A is opsonin in phagocytosis of herpes simplex virus type 1 by rat alveolar macrophages. Am J Physiol. 1991 Aug;261(2 Pt 1):L204–L209. doi: 10.1152/ajplung.1991.261.2.L204. [DOI] [PubMed] [Google Scholar]
  41. van Iwaarden J. F., van Strijp J. A., Visser H., Haagsman H. P., Verhoef J., van Golde L. M. Binding of surfactant protein A (SP-A) to herpes simplex virus type 1-infected cells is mediated by the carbohydrate moiety of SP-A. J Biol Chem. 1992 Dec 15;267(35):25039–25043. [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES