Skip to main content
Log in

Localization of surfactant protein A (SP-A) in alveolar macrophage subpopulations of normal and fibrotic rat lung

  • Original Paper
  • Published:
Histochemistry Aims and scope Submit manuscript

Abstract

The colocalization of surfactant protein A (SP-A) and the alveolar macrophage markers ED1 and RM-1, as well as various lectins of the N-acetyl-galactosamine group [Maclura pomifera lectin (MPA), Dolichos biflorus lectin (DBA), soybean agglutinin (SBA)] and of the mannose group [Canavalia ensiformis lectin (ConA), Galanthus nivalis lectin (GNA)] was studied in normal and fibrotic rat lung tissues. In normal tissue, SP-A was located preferentially in the alveolar macrophage subpopulation lacking specific binding sites for lectins of the N-acetylgalactosamine group (DBA and SBA), although 50% of MPA-binding macrophages contained SP-A. The ED1-positive cells were SP-A-negative, whereas SP-A uptake could be detected among the RM-1 immunoreactive as well as the ConA and GNA binding macrophages. In fibrotic lung tissue, however, a small number of .DBA and SBA binding macrophages contained SP-A and the percentage of GNA and ConA binding alveolar macrophages exhibiting SP-A immunoreactivity was reduced. Additionally, the number of ED1+/SP-A+ macrophages was found to be increased. Immunoelectron microscopy revealed accumulation of SP-A in the extracellular space. The differing SP-A content in different alveolar macrophage subpopulations suggests a more complex mechanism of uptake and degradation of surfactant proteins in normal and pathological conditions, which cannot simply be explained by the glycoconjugate pattern on the surface of alveolar macrophages.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Chandler DB, Fuller WC, Jackson RM, Fulmer JD (1986) Studies of membrane receptors and phagocytosis in subpopulations of rat alveolar macrophages. Am Rev Respir Dis 133:461–467

    Google Scholar 

  • Dijkstra CD, Döpp EA, Joling P, Kraal G (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54:589–599

    Google Scholar 

  • Everson P, Chandler DB (1992) Changes in distribution, morphology, and tumor necrosis factor-α secretion of alveolar macrophage subpopulations during the development of bleomycin-induced pulmonary fibrosis. Am J Pathol 140:503–512

    Google Scholar 

  • Floros J, Phelbs DS, Kourembanas S, Taeusch HW (1986) Primary translation products, biosynthesis, and tissue specificity of the major surfactant protein in rat. J Biol Chem 261:828–831

    Google Scholar 

  • Fujiwara T (1972) Biochemical aspects of pulmonary alveolar surface lining layer. Acta Pathol Jpn 22:805–810

    Google Scholar 

  • Gallagher JE, George G, Brody RA (1987) Sialic acid mediates the initial binding of positively charged inorganic particles to alveolar macrophage membranes. Am Rev Respir Dis 135:1345–1352

    Google Scholar 

  • Haagsman HP, Hawgood S, Sargeant T, Buckley D, White RT, Drickamer K, Benson BJ (1987) The major lung surfactant protein, SP 28–36, is a calcium-dependent, carbohydrate-binding protein. J Biol Chem 262:13877–13880

    Google Scholar 

  • Hance AJ, Douches S, Winchester RJ, Ferrans VJ, Crtystal RG (1985) Characterization of mononuclear phagocyte subpopulations in the human lung by using monoclonal antibodies: changes in alveolar macrophage phenotype associated with pulmonary sarcoidosis. J Immunol 134:284–292

    Google Scholar 

  • Holt PG, Oliver J, McMenamin C, Schon-Hegrad MA (1992) Studies on the surface phenotype and functions of dendritic cells in parenchymal lung tissue of the rat. Immunology 75:582–587

    Google Scholar 

  • Hoogsteeden HC, Hal PTW van, Wilkhuijs JM, Hop W, Hilvering C (1993) Differences in expression of monocyte/macrophage surface antigens in peripheral blood and bronchoalveolar lavage cells in interstitial lung diseases. Lung 171:149–160

    Google Scholar 

  • Kalina M, McCormack FX, Crowley H, Voelker DR, Mason RJ (1993) Internalization of surfactant protein A (SP-A) into lamellar bodies of rat alveolar type II cells in vitro. J Histochem Cytochem 41:57–70

    Google Scholar 

  • Kasper M, Haroske G, Pollack K, Migheli A, Müller M (1993) Heterogeneous Dolichos biflorus lectin binding to a subset of rat alveolar macrophages in normal and fibrotic lung tissue. Acta Histochem 95:1–11

    Google Scholar 

  • Kasper M, Haroske G, Müller M (1994) Species differences in lectin binding to pulmonary cells: soybean agglutinin (SBA) as a marker of type I alveolar epithelial cells and alveolar macrophages in mini pigs. Acta Histochem 96:63–73

    Google Scholar 

  • Kuroki Y, Mason RJ, Voelker DR (1988) Alveolar type II cells express a high-affinity receptor for pulmonary surfactant protein A. Proc Natl Acad Sci USA 85:5566–5570

    Google Scholar 

  • Kuroki Y, Gasa S, Ogasawara Y, Makita A, Akino T (1992) Binding of pulmonary surfactant protein A to galactosylceramide and asialo-G M2 . Arch Biochem Biophys 299:261–267

    Google Scholar 

  • Manz-Keinke H, Egenhofer C, Plattner H, Schlepper-Schäffer J (1991) Specific interaction of lung surfactant protein A (SP-A) with rat alveolar macrophages. Exp Cell Res 192:597–603

    Google Scholar 

  • Migheli A, Attanasio A, Schiffer D (1992) LR gold embedding of nervous tissue for immunoelectron microscopy studies. Histochemistry 97:413–419

    Google Scholar 

  • Murata Y, Kuroki Y, Akino T (1993) Role of the C-terminal domain of pulmonary surfactant protein A in binding to alveolar type II cells and regulation of phospholipid secretion. Biochem J 291:71–76

    Google Scholar 

  • Naimark A (1970) Cellular dynamics and lipid metabolism in the lung. Fed Proc 32:1967–1971

    Google Scholar 

  • Perez-Arellano JL, Losa-Garcia JE, Orfao-Matos A, Gonzalez M, Cruz JL de la, Jimenez A, Castro S de (1993) Comparison of two techniques (flow cytometry and alkaline immunophosphatase) in the evaluation of alveolar macrophage immunophenotype. Diagn Cytopathol 9:259–265

    Google Scholar 

  • Pison U, Wright JR, Hawgood S (1992) Specific binding of surfactant apoprotein SP-A to rat alveolar macrophages. Am J Physiol 262:L412-L417

    Google Scholar 

  • Ryan RM, Morris RE, Rice WR, Ciraolog G, Whitsett JA (1989) Binding and uptake of pulmonary surfactant protein (SP-A) by pulmonary type II epithelial cells. J Histochem Cytochem 37:429–436

    Google Scholar 

  • Sakai K, Kweon MN, Kohri T, Kishino Y (1992a) Effects of pulmonary surfactant and surfactant protein A on phagocytosis of fractionated alveolar macrophages: relationship to starvation. Cell Mol Biol 38:123–130

    Google Scholar 

  • Sakai K, Kohri T, Kawaguchi Y, Kweon MN, Kishino Y (1992b) Heterogeneity of immunohistochemical staining with pulmonary surfactant protein A among fractionated alveolar macrophages which involves metabolism of pulmonary surfactant. Cell Mol Biol 38:853–860

    Google Scholar 

  • Sano K, Fisher J, Mason RJ, Kuroki Y, Schilling J, Benson B, Voelker D (1987) Isolation and sequence of a cDNA clone for the rat surfactant-associated protein (PSP-A). Biochem Biophys Res Commun 144:367–374

    Google Scholar 

  • Saunders GC, Steinkamp JA, Lehnert BE (1987) Flow cytometric analyses of lectin binding to rat alveolar macrophages. Cytometry 8:602–611

    Google Scholar 

  • Schaffer J (1918) Veränderungen an Gewebselementen durch einseitige Wirkung der Fixierungsflüssigkeit und Allgemeines über Fixierung. Anat Anz 51:353–398

    Google Scholar 

  • Schulte BA, Spicer SS (1985) Histochemical methods for characterizing secretory and cell surface sialoglycoconjugates. J Histochem Cytochem 33:427–433

    Google Scholar 

  • Striz I, Wang YM, Svarcova I, Trnka L, Sorg C, Costabel U (1993) The phenotype of alveolar macrophages and its correlation with immune cells in bronchoalveolar lavage. Eur Respir J 6:1287–1294

    Google Scholar 

  • Takeya M, Hsiao L, Shimokawa Y, Takahashi K (1989) Heterogeneity of rat macrophages recognized by monoclonal antibodies: an immunohistochemical and immunoelectron microscopic study. J Histochem Cytochem 37:635–641

    Google Scholar 

  • Tenner AJ, Robinson SL, Borchelt J, Wright JR (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

    Google Scholar 

  • Valberg PA, Blanchard JD (1992) Pulmonary macrophage physiology, origin, motility, endocytosis. In: Parent RA (ed) Comparative biology of the normal lung. CRC Press, Boca Raton Ann Harbor London, pp 681–724

    Google Scholar 

  • Vignaud J-M, Allam M, Martinet N, Pech M, Plenat F, Matinet Y (1991) Presence of platelet derived growth factor in normal and fibrotic lung is specifically associated with interstitial macrophages, while both interstitial macrophages and alveolar epithelial cells express in c-sis protooncogene. Am J Respir Cell Mol Biol 5:531–538

    Google Scholar 

  • Weaver TE (1988) Pulmonary surfactant-associated proteins. Gen Pharmacol 19:361–368

    Google Scholar 

  • Weaver TE, Whittsett JA (1991) Function and regulation of expression of pulmonary surfactant-associated proteins. Biochem J 273:249–264

    Google Scholar 

  • Wintergerst E, Manz-Keinke M, Plattner H, Schlepper-Schäfer S (1989) The interaction of a lung surfactant protein (SP-A) with macrophages is mannose dependent. Eur J Cell Biol 50:291–296

    Google Scholar 

  • Wright JR, Wagner RE, Hawgood S, Dobbs L, Clements JA (1987) Surfactant apoprotein Mr=26000–36000 enhances uptake of liposomes by type II cells. J Biol Chem 262:2888–2894

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kasper, M., Haroske, G., Schuh, D. et al. Localization of surfactant protein A (SP-A) in alveolar macrophage subpopulations of normal and fibrotic rat lung. Histochemistry 102, 345–352 (1994). https://doi.org/10.1007/BF00268905

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00268905

Keywords

Navigation