Soluble CD163 promotes recognition, phagocytosis and killing of Staphylococcus aureus via binding of specific fibronectin peptides

Cellular Microbiology

Volumn 14, Issue 6, 2012, Pages 914-936

  Kneidl, Jessica ^a   Löffler, Bettina ^a   Erat, Michele C ^b   Kalinka, Julia ^a   Peters, Georg ^a   Roth, Johannes ^a   Barczyk, Katarzyna ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM10 ENDOPEPTIDASE; ADAM17 PROTEIN; CD163 ANTIGEN; FIBRONECTIN; METALLOPROTEINASE; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; ENDOTHELIUM CELL; HOST; HUMAN; HUMAN CELL; IMMUNE ADHERENCE; IMMUNE RESPONSE; MONOCYTE; NEUTROPHIL; PARACRINE SIGNALING; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BACTERIAL OUTER MEMBRANE PROTEINS; CELLS, CULTURED; EXTRACELLULAR MATRIX PROTEINS; FIBRONECTINS; HOST-PATHOGEN INTERACTIONS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNITY, INNATE; MEMBRANE PROTEINS; MICROBIAL VIABILITY; PEPTIDE FRAGMENTS; PHAGOCYTES; PHAGOCYTOSIS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, CELL SURFACE; SEQUENCE DELETION; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 84861186812     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01766.x     Document Type: Article

References (77)

1. de Assis, M.C., Da Costa, A.O., Barja-Fidalgo, T.C., and Plotkowski, M.C. (2000) Human endothelial cells are activated by interferon-gamma plus tumour necrosis factor-alpha to kill intracellular Pseudomonas aeruginosa. Immunology 101: 271-278.
2. Bingham, R.J., Rudino-Pinera, E., Meenan, N.A., Schwarz-Linek, U., Turkenburg, J.P., Höök, M., etal. (2008) Crystal structures of fibronectin-binding sites from Staphylococcus aureus FnBPA in complex with fibronectin domains. Proc Natl Acad Sci USA 105: 12254-12258.
3. Bover, L.C., Cardo-Vila, M., Kuniyasu, A., Sun, J., Rangel, R., Takeya, M., etal. (2007) A previously unrecognized protein-protein interaction between TWEAK and CD163: potential biological implications. J Immunol 178: 8183-8194.
4. Czuprynski, C.J., Brown, J.F., Maroushek, N., Wagner, R.D., and Steinberg, H. (1994) Administration of anti-granulocyte mAb RB6-8C5 impairs the resistance of mice to Listeria monocytogenes infection. J Immunol 152: 1836-1846.
5. Droste, A., Sorg, C., and Högger, P. (1999) Shedding of CD163, a novel regulatory mechanism for a member of the scavenger receptor cysteine-rich family. Biochem Biophys Res Commun 256: 110-113.
6. Eberhard, T., Virkola, R., Korhonen, T., Kronvall, G., and Ullberg, M. (1998) Binding to human extracellular matrix by Neisseria meningitidis. Infect Immun 66: 1791-1794.
7. Ehrchen, J., Steinmuller, L., Barczyk, K., Tenbrock, K., Nacken, W., Eisenacher, M., etal. (2007) Glucocorticoids induce differentiation of a specifically activated, anti-inflammatory subtype of human monocytes. Blood 109: 1265-1274.
8. Erat, M.C., Schwarz-Linek, U., Pickford, A.R., Farndale, R.W., Campbell, I.D., and Vakonakis, I. (2010) Implications for collagen binding from the crystallographic structure of fibronectin 6FnI1-2FnII7FnI. J Biol Chem 285: 33764-33770.
9. Etzerodt, A., Maniecki, M.B., Möller, K., Möller, H.J., and Moestrup, S.K. (2010) Tumor necrosis factor {alpha}-converting enzyme (TACE/ADAM17) mediates ectodomain shedding of the scavenger receptor CD163. J Leukoc Biol 88: 1201-1205.
10. Fabriek, B.O., Polfliet, M.M., Vloet, R.P., van der Schors, R.C., Ligtenberg, A.J., Weaver, L.K., etal. (2007) The macrophage CD163 surface glycoprotein is an erythroblast adhesion receptor. Blood 109: 5223-5229.
11. Fabriek, B.O., van Bruggen, R., Deng, D.M., Ligtenberg, A.J., Nazmi, K., Schornagel, K., etal. (2009) The macrophage scavenger receptor CD163 functions as an innate immune sensor for bacteria. Blood 113: 887-892.
12. Foster, T.J., and Höök, M. (1998) Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6: 484-488.
13. Fournier, B., and Philpott, D.J. (2005) Recognition of Staphylococcus aureus by the innate immune system. Clin Microbiol Rev 18: 521-540.
14. Fowler, T., Wann, E.R., Joh, D., Johansson, S., Foster, T.J., and Höök, M. (2000) Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell beta1 integrins. Eur J Cell Biol 79: 672-679.
15. Gaini, S., Koldkjaer, O.G., Pedersen, S.S., Pedersen, C., Moestrup, S.K., and Möller, H.J. (2006) Soluble haemoglobin scavenger receptor (sCD163) in patients with suspected community-acquired infections. APMIS 114: 103-111.
16. Gaini, S., Pedersen, S.S., Koldkaer, O.G., Pedersen, C., Moestrup, S.K., and Möller, H.J. (2008) New immunological serum markers in bacteraemia: anti-inflammatory soluble CD163, but not proinflammatory high mobility group-box 1 protein, is related to prognosis. Clin Exp Immunol 151: 423-431.
17. Garzoni, C., and Kelley, W.L. (2009) Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol 17: 59-65.
18. Gordon, S. (2001) Homeostasis: a scavenger receptor for haemoglobin. Curr Biol 11: R399-R401.
19. Gotz, F., Ahrne, S., and Lindberg, M. (1981) Plasmid transfer and genetic recombination by protoplast fusion in staphylococci. J Bacteriol 145: 74-81.
20. Grundmeier, M., Hussain, M., Becker, P., Heilmann, C., Peters, G., and Sinha, B. (2004) Truncation of fibronectin-binding proteins in Staphylococcus aureus strain Newman leads to deficient adherence and host cell invasion due to loss of the cell wall anchor function. Infect Immun 72: 7155-7163.
21. Grundmeier, M., Tuchscherr, L., Bruck, M., Viemann, D., Roth, J., Willscher, E., etal. (2010a) Staphylococcal strains vary greatly in their ability to induce an inflammatory response in endothelial cells. J Infect Dis 201: 871-880.
22. Grundmeier, M., Tuchscherr, L., Bruck, M., Viemann, D., Roth, J., Willscher, E., etal. (2010b) Staphylococcal strains vary greatly in their ability to induce an inflammatory response in endothelial cells. J Infect Dis 201: 871-880.
23. Högger, P., Dreier, J., Droste, A., Buck, F., and Sorg, C. (1998) Identification of the integral membrane protein RM3/1 on human monocytes as a glucocorticoid-inducible member of the scavenger receptor cysteine-rich family (CD163). J Immunol 161: 1883-1890.
24. Horsburgh, M.J., Aish, J.L., White, I.J., Shaw, L., Lithgow, J.K., and Foster, S.J. (2002) sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184: 5457-5467.
25. Hull, J.R., Tamura, G.S., and Castner, D.G. (2008) Interactions of the streptococcal C5a peptidase with human fibronectin. Acta Biomater 4: 504-513.
26. Hussain, M., Becker, K., von Eiff, C., Schrenzel, J., Peters, G., and Herrmann, M. (2001) Identification and characterization of a novel 38.5-kilodalton cell surface protein of Staphylococcus aureus with extended-spectrum binding activity for extracellular matrix and plasma proteins. J Bacteriol 183: 6778-6786.
27. Hussain, M., Haggar, A., Heilmann, C., Peters, G., Flock, J.I., and Herrmann, M. (2002) Insertional inactivation of Eap in Staphylococcus aureus strain Newman confers reduced staphylococcal binding to fibroblasts. Infect Immun 70: 2933-2940.
28. Ingham, K.C., Brew, S.A., and Isaacs, B.S. (1988) Interaction of fibronectin and its gelatin-binding domains with fluorescent-labeled chains of type I collagen. J Biol Chem 263: 4624-4628.
29. Ingham, K.C., Brew, S.A., and Migliorini, M.M. (1989) Further localization of the gelatin-binding determinants within fibronectin. Active fragments devoid of type II homologous repeat modules. J Biol Chem 264: 16977-16980.
30. Jönsson, K., Signas, C., Muller, H.P., and Lindberg, M. (1991) Two different genes encode fibronectin binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of the second gene. Eur J Biochem 202: 1041-1048.
31. Kristiansen, M., Graversen, J.H., Jacobsen, C., Sonne, O., Hoffman, H.J., Law, S.K., etal. (2001) Identification of the haemoglobin scavenger receptor. Nature 409: 198-201.
32. Lowy, F.D. (1998) Staphylococcus aureus infections. N Engl J Med 339: 520-532.
33. Ludwig, A., Hundhausen, C., Lambert, M.H., Broadway, N., Andrews, R.C., Bickett, D.M., etal. (2005) Metalloproteinase inhibitors for the disintegrin-like metalloproteinases ADAM10 and ADAM17 that differentially block constitutive and phorbol ester-inducible shedding of cell surface molecules. Comb Chem High Throughput Screen 8: 161-171.
34. Mao, Y., and Schwarzbauer, J.E. (2005) Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol 24: 389-399.
35. Marjenberg, Z.R., Ellis, I.R., Hagan, R.M., Prabhakaran, S., Höök, M., Talay, S.R., etal. (2011) Cooperative binding and activation of fibronectin by a bacterial surface protein. J Biol Chem 286: 1884-1894.
36. Massey, R.C., Kantzanou, M.N., Fowler, T., Day, N.P., Schofield, K., Wann, E.R., etal. (2001) Fibronectin-binding protein A of Staphylococcus aureus has multiple, substituting, binding regions that mediate adherence to fibronectin and invasion of endothelial cells. Cell Microbiol 3: 839-851.
37. Meenan, N.A., Visai, L., Valtulina, V., Schwarz-Linek, U., Norris, N.C., Gurusiddappa, S., etal. (2007) The tandem beta-zipper model defines high affinity fibronectin-binding repeats within Staphylococcus aureus FnBPA. J Biol Chem 282: 25893-25902.
38. Menzies, B.E. (2003) The role of fibronectin binding proteins in the pathogenesis of Staphylococcus aureus infections. Curr Opin Infect Dis 16: 225-229.
39. Meszaros, A.J., Reichner, J.S., and Albina, J.E. (1999) Macrophage phagocytosis of wound neutrophils. J Leukoc Biol 65: 35-42.
40. Millard, C.J., Campbell, I.D., and Pickford, A.R. (2005) Gelatin binding to the 8F19F1 module pair of human fibronectin requires site-specific N-glycosylation. FEBS Lett 579: 4529-4534.
41. Möller, H.J., Moestrup, S.K., Weis, N., Wejse, C., Nielsen, H., Pedersen, S.S., etal. (2006) Macrophage serum markers in pneumococcal bacteremia: prediction of survival by soluble CD163. Crit Care Med 34: 2561-2566.
42. Newgreen, D. (1984) Spreading of explants of embryonic chick mesenchymes and epithelia on fibronectin and laminin. Cell Tissue Res 236: 265-277.
43. Okumura, Y., Kamikubo, Y., Curriden, S.A., Wang, J., Kiwada, T., Futaki, S., etal. (2002) Kinetic analysis of the interaction between vitronectin and the urokinase receptor. J Biol Chem 277: 9395-9404.
44. Owen, C.A., Campbell, E.J., and Stockley, R.A. (1992) Monocyte adherence to fibronectin: role of CD11/CD18 integrins and relationship to other monocyte functions. J Leukoc Biol 51: 400-408.
45. Peterson, P.K., Verhoef, J., Schmeling, D., and Quie, P.G. (1977) Kinetics of phagocytosis and bacterial killing by human polymorphonuclear leukocytes and monocytes. J Infect Dis 136: 502-509.
46. Potts, J.R., and Campbell, I.D. (1996) Structure and function of fibronectin modules. Matrix Biol 15: 313-320.
47. Pruessmeyer, J., Martin, C., Hess, F.M., Schwarz, N., Schmidt, S., Kogel, T., etal. (2010) A disintegrin and metalloproteinase 17 (ADAM17) mediates inflammation-induced shedding of syndecan-1 and -4 by lung epithelial cells. J Biol Chem 285: 555-564.
48. van Putten, J.P., Duensing, T.D., and Cole, R.L. (1998) Entry of OpaA+ gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol Microbiol 29: 369-379.
49. Roche, F.M., Downer, R., Keane, F., Speziale, P., Park, P.W., and Foster, T.J. (2004) The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J Biol Chem 279: 38433-38440.
50. Sa E Cunha, C., Griffiths, N.J., and Virji, M. (2010) Neisseria meningitidis Opc invasin binds to the sulphated tyrosines of activated vitronectin to attach to and invade human brain endothelial cells. PLoS Pathog 6: e1000911.
51. Sarrias, M.R., Gronlund, J., Padilla, O., Madsen, J., Holmskov, U., and Lozano, F. (2004) The Scavenger Receptor Cysteine-Rich (SRCR) domain: an ancient and highly conserved protein module of the innate immune system. Crit Rev Immunol 24: 1-37.
52. Schroder, A., Kland, R., Peschel, A., von Eiff, C., and Aepfelbacher, M. (2006) Live cell imaging of phagosome maturation in Staphylococcus aureus infected human endothelial cells: small colony variants are able to survive in lysosomes. Med Microbiol Immunol 195: 185-194.
53. Schutze, S., Machleidt, T., Adam, D., Schwandner, R., Wiegmann, K., Kruse, M.L., etal. (1999) Inhibition of receptor internalization by monodansylcadaverine selectively blocks p55 tumor necrosis factor receptor death domain signaling. J Biol Chem 274: 10203-10212.
54. Schwarz-Linek, U., Werner, J.M., Pickford, A.R., Gurusiddappa, S., Kim, J.H., Pilka, E.S., etal. (2003) Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423: 177-181.
55. Schwarz-Linek, U., Pilka, E.S., Pickford, A.R., Kim, J.H., Höök, M., Campbell, I.D., etal. (2004) High affinity streptococcal binding to human fibronectin requires specific recognition of sequential F1 modules. J Biol Chem 279: 39017-39025.
56. Schwarz-Linek, U., Höök, M., and Potts, J.R. (2006) Fibronectin-binding proteins of gram-positive cocci. Microbes Infect 8: 2291-2298.
57. Sendi, P., and Proctor, R.A. (2009) Staphylococcus aureus as an intracellular pathogen: the role of small colony variants. Trends Microbiol 17: 54-58.
58. Sinha, B., and Herrmann, M. (2005) Mechanism and consequences of invasion of endothelial cells by Staphylococcus aureus. Thromb Haemost 94: 266-277.
59. Sinha, B., Francois, P.P., Nusse, O., Foti, M., Hartford, O.M., Vaudaux, P., etal. (1999) Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol 1: 101-117.
60. Sinha, B., Francois, P., Que, Y.A., Hussain, M., Heilmann, C., Moreillon, P., etal. (2000) Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect Immun 68: 6871-6878.
61. Sjostedt, A., Conlan, J.W., and North, R.J. (1994) Neutrophils are critical for host defense against primary infection with the facultative intracellular bacterium Francisella tularensis in mice and participate in defense against reinfection. Infect Immun 62: 2779-2783.
62. Tamura, G.S., and Rubens, C.E. (1995) Group B streptococci adhere to a variant of fibronectin attached to a solid phase. Mol Microbiol 15: 581-589.
63. Tuchscherr, L., Medina, E., Hussain, M., Volker, W., Heitmann, V., Niemann, S., etal. (2011) Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol Med 3: 129-141.
64. Unkmeir, A., Latsch, K., Dietrich, G., Wintermeyer, E., Schinke, B., Schwender, S., etal. (2002) Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol Microbiol 46: 933-946.
65. Vakonakis, I., Langenhan, T., Promel, S., Russ, A., and Campbell, I.D. (2008) Solution structure and sugar-binding mechanism of mouse latrophilin-1 RBL: a 7TM receptor-attached lectin-like domain. Structure 16: 944-953.
66. Vakonakis, I., Staunton, D., Ellis, I.R., Sarkies, P., Flanagan, A., Schor, A.M., etal. (2009) Motogenic sites in human fibronectin are masked by long range interactions. J Biol Chem 284: 15668-15675.
67. Van Gorp, H., Delputte, P.L., and Nauwynck, H.J. (2010) Scavenger receptor CD163, a Jack-of-all-trades and potential target for cell-directed therapy. Mol Immunol 47: 1650-1660.
68. Viemann, D., Goebeler, M., Schmid, S., Nordhues, U., Klimmek, K., Sorg, C., etal. (2006) TNF induces distinct gene expression programs in microvascular and macrovascular human endothelial cells. J Leukoc Biol 80: 174-185.
69. Virji, M., Makepeace, K., and Moxon, E.R. (1994) Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells; the role of integrins in apical interactions. Mol Microbiol 14: 173-184.
70. Virji, M., Makepeace, K., Peak, I.R., Ferguson, D.J., Jennings, M.P., and Moxon, E.R. (1995) Opc- and pilus-dependent interactions of meningococci with human endothelial cells: molecular mechanisms and modulation by surface polysaccharides. Mol Microbiol 18: 741-754.
71. Wann, E.R., Gurusiddappa, S., and Höök, M. (2000) The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem 275: 13863-13871.
72. Weaver, L.K., Hintz-Goldstein, K.A., Pioli, P.A., Wardwell, K., Qureshi, N., Vogel, S.N., etal. (2006) Pivotal advance: activation of cell surface Toll-like receptors causes shedding of the hemoglobin scavenger receptor CD163. J Leukoc Biol 80: 26-35.
73. Weaver, L.K., Pioli, P.A., Wardwell, K., Vogel, S.N., and Guyre, P.M. (2007) Up-regulation of human monocyte CD163 upon activation of cell-surface Toll-like receptors. J Leukoc Biol 81: 663-671.
74. Wenzel, I., Roth, J., and Sorg, C. (1996) Identification of a novel surface molecule, RM3/1, that contributes to the adhesion of glucocorticoid-induced human monocytes to endothelial cells. Eur J Immunol 26: 2758-2763.
75. Williams, R.J., Henderson, B., Sharp, L.J., and Nair, S.P. (2002) Identification of a fibronectin-binding protein from Staphylococcus epidermidis. Infect Immun 70: 6805-6810.
76. Zwadlo, G., Brocker, E.B., von Bassewitz, D.B., Feige, U., and Sorg, C. (1985) A monoclonal antibody to a differentiation antigen present on mature human macrophages and absent from monocytes. J Immunol 134: 1487-1492.
77. Zwadlo, G., Voegeli, R., Osthoff, K.S., and Sorg, C. (1987) A monoclonal antibody to a novel differentiation antigen on human macrophages associated with the down-regulatory phase of the inflammatory process. Exp Cell Biol 55: 295-304.