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PMID: 10722588 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro.

Infection and immunity ·Vol. 68 ·No. 4 ·2000-04-00 ·Pages 1953-63

Peiser L, Gough PJ, Kodama T, Gordon S

Abstract

Macrophage class A scavenger receptors (SR-AI and SR-AII) contribute to host defense by binding polyanionic ligands such as lipopolysaccharide and lipoteichoic acid. SR-A knockout (SR-A(-/-)) mice are more susceptible to endotoxic shock and Listeria monocytogenes infection in vivo, possibly due to decreased clearance of lipopolysaccharide and microorganisms, respectively. We have used flow cytometry to analyze the role of SR-A and other scavenger-like receptors in phagocytosis of bacteria in vitro. Chinese hamster ovary cells stably transfected with human SR-A bound Escherichia coli and Staphylococcus aureus but ingested few organisms. Primary human monocyte-derived macrophages (Mphi) bound and ingested E. coli more efficiently, and this was partially but selectively blocked by the general SR inhibitor, poly(I). A specific and selective role for SR-A was shown, since bone marrow culture-derived Mphi from SR-A(-/-) mice ingested fewer E. coli organisms than did wild-type cells, while uptake of antibody-opsonized E. coli was unaffected. SR-A-dependent uptake of E. coli varied with the bacterial strain; ingestion of DH5alpha and K1 by SR-A(-/-) Mphi was reduced by 30 to 60% and 70 to 75%, respectively. Phagocytosis and endocytosis via SR-A were markedly down-modulated when Mphi were plated on serum-coated tissue culture plastic compared to bacteriologic plastic, where cell adhesion is mediated by SR-A and CR3, respectively. This paper demonstrates that SR-A can bind and ingest bacteria directly, consistent with a role in host defense in vivo, and highlights the importance of the source of the Mphi, bacterial strain, and culture conditions on receptor function in vitro.

MeSH Terms
Animals Bacterial Adhesion Bone Marrow Cells/microbiology CHO Cells Cell Line Cells, Cultured Cricetinae Escherichia coli/immunology Flow Cytometry Humans Macrophages/microbiology Mice Mice, Inbred ICR Mice, Knockout Microscopy, Fluorescence Monocytes/cytology,microbiology Phagocytosis/physiology Protein Isoforms Receptors, Immunologic/physiology Receptors, Scavenger Scavenger Receptors, Class A Staphylococcus aureus/metabolism Temperature Time Factors Transfection
Chemicals
MSR1 protein, human Msr1 protein, mouse Protein Isoforms Receptors, Immunologic Receptors, Scavenger Scavenger Receptors, Class A
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Peiser L
Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, United Kingdom. leanne.peiser@path.ox.ac.uk
Gough P J
Kodama T
Gordon S
References (47)
47 references, click to expand
  1. 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):607-21 PMID: 383878
  2. Role for the class A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12456-60 PMID: 8901603
  3. Fibronectin and serum amyloid P component stimulate C3b- and C3bi-mediated phagocytosis in cultured human monocytes.
    J Exp Med. 1983 Oct 1;158(4):1338-43 PMID: 6225825
  4. Optimal conditions for proliferation of bone marrow-derived mouse macrophages in culture: the roles of CSF-1, serum, Ca2+, and adherence.
    J Cell Physiol. 1983 Nov;117(2):189-94 PMID: 6605349
  5. Evaluation of flow cytometry and fluorescence microscopy for the estimation of bovine mononuclear phagocytes.
    J Immunol Methods. 1985 Apr 8;78(1):13-24 PMID: 3981015
  6. A new simple fluorometric assay for phagocytosis.
    J Immunol Methods. 1986 Apr 17;88(2):175-83 PMID: 3514764
  7. Phagocytosis of agarose beads by receptors for C3b (CR1) and iC3b (CR3) on human alveolar macrophages cultured on fibronectin in vitro. A scanning electron microscopic study.
    Scand J Immunol. 1986 Dec;24(6):653-60 PMID: 2948272
  8. Monoclonal antibody to the murine type 3 complement receptor inhibits adhesion of myelomonocytic cells in vitro and inflammatory cell recruitment in vivo.
    J Exp Med. 1987 Dec 1;166(6):1685-701 PMID: 2445894
  9. Purification and characterization of a bovine acetyl low density lipoprotein receptor.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):9238-42 PMID: 3194423
  10. Type I macrophage scavenger receptor contains alpha-helical and collagen-like coiled coils.
    Nature. 1990 Feb 8;343(6258):531-5 PMID: 2300204
  11. Coiled-coil fibrous domains mediate ligand binding by macrophage scavenger receptor type II.
    Nature. 1990 Feb 8;343(6258):570-2 PMID: 2300208
  12. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts.
    Science. 1990 Aug 10;249(4969):641-6 PMID: 2200126
  13. Human macrophage scavenger receptors: primary structure, expression, and localization in atherosclerotic lesions.
    Proc Natl Acad Sci U S A. 1990 Dec;87(23):9133-7 PMID: 2251254
  14. Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells.
    J Exp Med. 1990 Dec 1;172(6):1785-94 PMID: 2258707
  15. Expression of type I and type II bovine scavenger receptors in Chinese hamster ovary cells: lipid droplet accumulation and nonreciprocal cross competition by acetylated and oxidized low density lipoprotein.
    Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4931-5 PMID: 2052575
  16. Recognition and plasma clearance of endotoxin by scavenger receptors.
    Nature. 1991 Jul 25;352(6333):342-4 PMID: 1852209
  17. Structure, organization, and chromosomal mapping of the human macrophage scavenger receptor gene.
    J Biol Chem. 1993 Jan 25;268(3):2120-5 PMID: 8093617
  18. A rapid and simple microfluorometric phagocytosis assay.
    J Immunol Methods. 1993 Jun 4;162(1):1-7 PMID: 8509646
  19. Divalent cation-independent macrophage adhesion inhibited by monoclonal antibody to murine scavenger receptor.
    Nature. 1993 Jul 22;364(6435):343-6 PMID: 8332192
  20. Structures and high and low affinity ligand binding properties of murine type I and type II macrophage scavenger receptors.
    J Lipid Res. 1993 Jun;34(6):983-1000 PMID: 8394868
  21. The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1863-7 PMID: 8127896
  22. The SRCR superfamily: a family reminiscent of the Ig superfamily.
    Trends Biochem Sci. 1994 Jan;19(1):5-8 PMID: 8140623
  23. Macrophage-colony-stimulating factor selectively enhances macrophage scavenger receptor expression and function.
    J Exp Med. 1994 Aug 1;180(2):705-9 PMID: 8046345
  24. Characteristics of Escherichia coli in acute community-acquired cystitis of adult women.
    Scand J Infect Dis. 1993;25(6):705-12 PMID: 7914381
  25. Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP).
    Annu Rev Biochem. 1994;63:601-37 PMID: 7979249
  26. Two distinct regions of FC gamma RI initiate separate signalling pathways involved in endocytosis and phagocytosis.
    EMBO J. 1995 Feb 1;14(3):432-41 PMID: 7859733
  27. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages.
    Cell. 1995 Feb 24;80(4):603-9 PMID: 7867067
  28. Transmembrane association with gamma-chain is required for Fc gamma RI-mediated phagocytosis in transfected COS cells.
    Biochem Soc Trans. 1995 Feb;23(1):121S PMID: 7758683
  29. Ligand binding and phagocytosis by CD16 (Fc gamma receptor III) isoforms. Phagocytic signaling by associated zeta and gamma subunits in Chinese hamster ovary cells.
    J Biol Chem. 1995 Oct 27;270(43):25762-70 PMID: 7592758
  30. Fluorescence labeling of bacteria for studies of intracellular pathogenesis.
    J Immunol Methods. 1995 Nov 16;187(1):69-79 PMID: 7490459
  31. Regulation of monocyte CD36 and thrombospondin-1 expression by soluble mediators.
    Arterioscler Thromb Vasc Biol. 1996 Aug;16(8):1019-25 PMID: 8696941
  32. Scavenger receptors in innate immunity.
    Curr Opin Immunol. 1996 Feb;8(1):20-8 PMID: 8729442
  33. Structures of class A macrophage scavenger receptors. Electron microscopic study of flexible, multidomain, fibrous proteins and determination of the disulfide bond pattern of the scavenger receptor cysteine-rich domain.
    J Biol Chem. 1996 Oct 25;271(43):26924-30 PMID: 8900177
  34. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection.
    Nature. 1997 Mar 20;386(6622):292-6 PMID: 9069289
  35. The other side of scavenger receptors: pattern recognition for host defense.
    Curr Opin Lipidol. 1997 Oct;8(5):275-80 PMID: 9335951
  36. Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo.
    J Immunol. 1999 Jan 15;162(2):939-47 PMID: 9916718
  37. Analysis of macrophage scavenger receptor (SR-A) expression in human aortic atherosclerotic lesions.
    Arterioscler Thromb Vasc Biol. 1999 Mar;19(3):461-71 PMID: 10073945
  38. Mechanisms of phagocytosis in macrophages.
    Annu Rev Immunol. 1999;17:593-623 PMID: 10358769
  39. The macrophage scavenger receptor type A is expressed by activated macrophages and protects the host against lethal endotoxic shock.
    J Exp Med. 1997 Nov 3;186(9):1431-9 PMID: 9348300
  40. Insulin enhances macrophage scavenger receptor-mediated endocytic uptake of advanced glycation end products.
    J Biol Chem. 1998 Apr 10;273(15):8630-7 PMID: 9535837
  41. A naturally occurring isoform of the human macrophage scavenger receptor (SR-A) gene generated by alternative splicing blocks modified LDL uptake.
    J Lipid Res. 1998 Mar;39(3):531-43 PMID: 9548586
  42. The multiple roles of macrophage scavenger receptors (MSR) in vivo: resistance to atherosclerosis and susceptibility to infection in MSR knockout mice.
    J Atheroscler Thromb. 1997;4(1):1-11 PMID: 9583348
  43. Recent progress in defining the role of scavenger receptors in lipid transport, atherosclerosis and host defence.
    Curr Opin Lipidol. 1998 Oct;9(5):425-32 PMID: 9812196
  44. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases.
    Science. 1998 Nov 27;282(5394):1717-21 PMID: 9831565
  45. Complementary roles for scavenger receptor A and CD36 of human monocyte-derived macrophages in adhesion to surfaces coated with oxidized low-density lipoproteins and in secretion of H2O2.
    J Exp Med. 1998 Dec 21;188(12):2257-65 PMID: 9858512
  46. Monocytes can phagocytose Gram-negative bacteria by a CD14-dependent mechanism.
    J Immunol. 1996 Nov 1;157(9):4119-25 PMID: 8892647
  47. Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis.
    Annu Rev Biochem. 1983;52:223-61 PMID: 6311077
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2000-04-00
Pages
1953-63
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC97372
Subset
IM
Grants
Wellcome Trust · United Kingdom
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