Abstract
Lung surfactant protein A (SP-A) is the most abundant surfactant-associated protein present in the lung. A receptor for SP-A has been shown to be present on A549 alveolar type II cells and on other cell types, including alveolar macrophage. The SP-A receptor on A549 cells has been identified as the collectin receptor, or C1q receptor, which binds several structurally-related ligands. SP-A contains C-type lectin domains, but the role of carbohydrate binding by SP-A in physiological and pathological phenomena is not yet established. In this paper we report the binding of SP-A to pollen from Populus nigra italica (Lombardy Poplar), Poa pratensis (Kentucky blue grass),Secale cerale (cultivated rye) and Ambrosia elatior (short ragweed). Saturable and concentration dependent binding of SP-A to pollen grains was observed. Interaction of SP-A with pollen grains takes place through waterextractable components, in which the major species present, in Lombardy poplar pollen,are 57 kD and 7 kD (glyco)proteins. The binding of SP-A to pollen grains and their aqueous extracts was calcium ion dependent and was inhibited by mannose, and is therefore mediated by the lectin domain. Binding of SP-A to pollen grains was found to mediate adhesion of pollen grains to A549 cells. The results suggest that pollen grains or other carbohydrate-bearing particles (e. g. microorganisms) could potentially interact with different cell types via the collectin receptor (C1q Receptor) in the presence of SP-A.
References
Arvieux, J., Reboul, A., Bensa, J. C., and Colomb, M. G. (1984) Characterization of the C1q receptor on a human macrophage cell line U937.Biochem. J. 218:547–555.
Cannon, G. J. and Swanson, J. A. (1992) The macrophage capacity for phagocytosis.J. Cell. Sci 101: 907–913.
Cottom, G. P., Moran, D. M., and Standring, R. (1986) Physicochemical and immunochemical characterization of allergic proteins from rye-grass (Lolium perenne) pollen prepared by rapid and efficient purification method.Biochem. J 234:305–310.
Drevets, D. A. and Campbell, P. A. (1991) Macrophage phagocytosis: use of fluorescence microscopy to distinguish between extracellular and intracellular bacteria.J. Immunol. Meth 142:31–38.
Dobbs, L. G., Wright, J. R., Hawgwood, S., Gonzalez, R., Venstrom, K., and Nellenbogen, J. (1987) Pulmonary surfactant and its components inhibit secretion of phosphatidylcholine from cultured rat alveolar type II cells.Proc. Natl. Acad. Sci 84:1010–1014.
Fraker, P. J., and Speck, J. C. Jr. (1978) Protein and cell membrane iodination with sparingly soluble chloroamide, 1,3,4,6-tetra chloro-3a,6a-Diphenylglycoluril.Biochem. Biophys. Res. Commun 80:849–857.
Griffith, I. J., Smith, P. M., Pollack, J., Theerakulpisut, P., Avjioglu, A., Davies, S., Hough, T., Singh, M. B., Simpson, R. J., and Ward, L. D. (1990) Cloning and sequencing of Lol pl, the major allergenic protein of rye-grass pollen.FEBS Lett 279:210–215.
Ghebrehiwet, B. (1989) Functions associated with the C1q receptor.Behring Inst. Mit 84:204–215.
Haagsman, H. S., Hawgood, S.,Sargeant, T., Buckley, D., White, R., Drickamer, K., and Benson B. J. (1987) The major lung surfactant protein, SP 28-36, is a calcium-dependent, carbohydrate-binding protein.J. Biol. Chem 262:13877–13880.
Hawgood, S. (1989) Plumonary surfactant apoprotein: a review of protein and genomic structure.Am. J. Physiol 257:L13-L22.
Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 227:680–685.
Lu, J.,Willis, A. C., and Reid, K. B. M. (1992) Purification, characterization and cDNA cloning of human lung surfactant protein D.Biochem. J 284:795–802.
Malhotra, R. and Sim R. B. (1989) Chemical and hydrodynamic characterization of the human leukocyte receptor for complement subcomponent C1q.Biochem. J. 262:625–631.
Malhotra, R., Theil, S., Reid, K. B. M. and Sim, R. B. (1990) Human leukocyte C1q receptor binds other soluble proteins with collagen domains.J. Exp. Med 172:955–959.
Malhotra, R., Haurum, J., Thiel, S. and Sim, R. B. (1992a) Interaction of C1q receptor with lung surfactant protein A.Eur J. Immunol 22:1437–1445.
Malhotra, R., Lu, J., Theil, S., Jensenius, J.-C. Wills, A. C. and Sim, R. B. (1922b) C1q receptor (Collectin receptor): Primary structure, homology, and interaction with ligands.Immunobiology 184:437–438.
Manz-Keinke, H., Plattner, H. and Schlepper-Schafer, J. (1992) Lung surfactant protein A (SP-A) enhances serum-independent phagocytosis of bacteria by alveolar macrophages.Eur. J. Cell. Biol 57:95–100.
Peerschke, E. I. B., Malhotra, R., Ghebrehiwet, B., Reid, K. B. M., Willis,A. C. and Sim, R. B. (1992) Isolation of a human endothelial cell C1q receptor (C1qR).J. Leukocyte Biol. (in press)
Pison, U., Wright, J. R. and Hawgood, S. (1992) Specific binding of surfactant apoprotein SP-A to rat alveolar macrophages.Am. J. Physiol 262:L412-L417.
Suphioglu, C., Singh, M. B., Taylor, P., Bellomo, R., Holmes, P., Puy, R. and Knox, R. B. (1992) Mechanism of grass-pollen-induced asthma.Lancet 339:569–572.
Tenner, A. J. (1989) C1q interaction with cell surface receptors.Behring Inst. Mitt 84:220–229.
Tenner, A. J., Robinson, S. L., Borchelt, J. and Wright, J. R. (1989) Human pulmonary surfactant protein (SP-A), a protein structurally homologous to C1q, can enhance FcR- and CR1-mediated phagocytosis.J. Biol. Chem 264:13923–13928.
Thiel, S. and Reid, K. B. M. (1989) Structures and functions associated with the group of mammalian lectins containing collagen-like sequences.FEBS Lett 250:78–84.
Van-Iwaarden, F., Welmers, B. Verhoef, J., Haagsman, H. and Van-Golde, L. M. G. (1990) Pulmonary surfactant protein A enhances the host-defense mechanism of rat alveolar macrophages.Am. J. Respir. Cell. Mol. Biol. 2:91–98.
Van-Iwaarden, J. F., Van-Strijp, J. A. G., Ebskamp, M. J. M., Wellmers, A. C., Verhoef, J. and Van-Golde, L. M. G. (1991) Surfactant protein A is an opsonin in phagocytosis of herpes simplex virus type 1 by rat alveolar macrophages.Am. J. Physiol 261:L204-L209.
Wright, J. R., Wager, R. E., Hawgood, S., Dobbs, L. and Clements, J. A. (1987) Surfactant apoprotein Mr=26,000–36,000 enhances uptake of liposomes by type II cells.J. Biol. Chem 262:2888–2894.
Zimmerman, P. E., Voelker, D. R., McCormack, F. X., Paulsrud, J. R. and Martin II, W. J. (1992) 120-kD surface glycoprotein of Pneumocystis carinii is a ligand for surfactant protein A.J. Clin. Invest. 89:143–149.
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Malhotra, R., Haurum, J., Thiel, S. et al. Pollen grains bind to lung alveolar type II cells (A549) via lung surfactant protein A (SP-A). Biosci Rep 13, 79–90 (1993). https://doi.org/10.1007/BF01145960
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DOI: https://doi.org/10.1007/BF01145960