Iron-regulated surface determinant B (IsdB) promotes Staphylococcus aureus adherence to and internalization by non-phagocytic human cells

Cellular Microbiology

Volumn 15, Issue 6, 2013, Pages 1026-1041

  Zapotoczna, Marta ^a   Jevnikar, Zala ^b   Miajlovic, Helen ^a   Kos, Janko ^b   Foster, Timothy J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2BBETA3 INTEGRIN; BACTERIAL PROTEIN; FIBRONECTIN; FIBRONECTIN BINDING PROTEIN; INTEGRIN; IRON REGULATED SURFACE DETERMINANT B PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIUM ADHERENCE; CELL ADHESION; CELL INVASION; CHO CELL; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAPHYLOCOCCUS AUREUS; THROMBOCYTE;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BLOOD PLATELETS; CATION TRANSPORT PROTEINS; CELLS, CULTURED; FIBRONECTINS; HEK293 CELLS; HELA CELLS; HEMOGLOBINS; HUMANS; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN BINDING; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); MAMMALIA; STAPHYLOCOCCUS AUREUS;

EID: 84877794313     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12097     Document Type: Article

References (58)

1. Agerer, F., Lux, S., Michel, A., Rohde, M., Ohlsen, K., and Hauck, C.R. (2005) Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J Cell Sci 118 (Part 10): 2189-2200.
2. Allard, M., Moisan, H., Brouillette, E., Gervais, A.L., Jacques, M., Lacasse, P., etal. (2006) Transcriptional modulation of some Staphylococcus aureus iron-regulated genes during growth in vitro and in a tissue cage model in vivo. Microbes Infect 8: 1679-1690.
3. Bae, T., and Schneewind, O. (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63.
4. van Belkum, A., Verkaik, N.J., de Vogel, C.P., Boelens, H.A., Verveer, J., Nouwen, J.L., etal. (2009) Reclassification of Staphylococcus aureus nasal carriage types. J Infect Dis 199: 1820-1826.
5. Brouillette, E., Grondin, G., Shkreta, L., Lacasse, P., and Talbot, B.G. (2003) In vivo and in vitro demonstration that Staphylococcus aureus is an intracellular pathogen in the presence or absence of fibronectin-binding proteins. Microb Pathog 35: 159-168.
6. Cheng, A.G., Kim, H.K., Burts, M.L., Krausz, T., Schneewind, O., and Missiakas, D.M. (2009) Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J 23: 3393-3404.
7. Clarke, S.R., and Foster, S.J. (2008) IsdA protects Staphylococcus aureus against the bactericidal protease activity of apolactoferrin. Infect Immun 76: 1518-1526.
8. Clarke, S.R., Wiltshire, M.D., and Foster, S.J. (2004) IsdA of Staphylococcus aureus is a broad spectrum, iron-regulated adhesin. Mol Microbiol 51: 1509-1519.
9. Clarke, S.R., Mohamed, R., Bian, L., Routh, A.F., Kokai-Kun, J.F., Mond, J.J., etal. (2007) The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin. Cell Host Microbe 1: 199-212.
10. Clarke, S.R., Andre, G., Walsh, E.J., Dufrene, Y.F., Foster, T.J., and Foster, S.J. (2009) Iron-regulated surface determinant protein A mediates adhesion of Staphylococcus aureus to human corneocyte envelope proteins. Infect Immun 77: 2408-2416.
11. Claro, T., Widaa, A., O'Seaghdha, M., Miajlovic, H., Foster, T.J., O'Brien, F.J., etal. (2011) Staphylococcus aureus protein A binds to osteoblasts and triggers signals that weaken bone in osteomyelitis. PLoS ONE 6: e18748.
12. Corrigan, R.M., and Foster, T.J. (2009) An improved tetracycline-inducible expression vector for Staphylococcus aureus. Plasmid 61: 126-129.
13. Corrigan, R.M., Miajlovic, H., and Foster, T.J. (2009) Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells. BMC Microbiol 9: 22.
14. Coutinho, A., Garcia, C., Gonzalez-Rodriguez, J., and Lillo, M.P. (2007) Conformational changes in human integrin alphaIIbbeta3 after platelet activation, monitored by FRET. Biophys Chem 130: 76-87.
15. Dryla, A., Hoffmann, B., Gelbmann, D., Giefing, C., Hanner, M., Meinke, A., etal. (2007) High-affinity binding of the staphylococcal HarA protein to haptoglobin and hemoglobin involves a domain with an antiparallel eight-stranded beta-barrel fold. J Bacteriol 189: 254-264.
16. Edwards, A.M., Potts, J.R., Josefsson, E., and Massey, R.C. (2010) Staphylococcus aureus host cell invasion and virulence in sepsis is facilitated by the multiple repeats within FnBPA. PLoS Pathog 6: e1000964.
17. von Eiff, C., Becker, K., Metze, D., Lubritz, G., Hockmann, J., Schwarz, T., etal. (2001) Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with Darier's disease. Clin Infect Dis 32: 1643-1647.
18. Ellington, J.K., Reilly, S.S., Ramp, W.K., Smeltzer, M.S., Kellam, J.F., and Hudson, M.C. (1999) Mechanisms of Staphylococcus aureus invasion of cultured osteoblasts. Microb Pathog 26: 317-323.
19. Garzoni, C., and Kelley, W.L. (2009) Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol 17: 59-65.
20. Grigg, J.C., Ukpabi, G., Gaudin, C.F., and Murphy, M.E. (2010) Structural biology of heme binding in the Staphylococcus aureus Isd system. J Inorg Biochem 104: 341-348.
21. Grigg, J.C., Mao, C.X., and Murphy, M.E. (2011) Iron-coordinating tyrosine is a key determinant of NEAT domain heme transfer. J Mol Biol 413: 684-698.
22. 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.
23. Haggar, A., Hussain, M., Lonnies, H., Herrmann, M., Norrby-Teglund, A., and Flock, J.I. (2003) Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells. Infect Immun 71: 2310-2317.
24. Harburger, D.S., and Calderwood, D.A. (2009) Integrin signalling at a glance. J Cell Sci 122 (Part 2): 159-163.
25. Hauck, C.R., Agerer, F., Muenzner, P., and Schmitter, T. (2006) Cellular adhesion molecules as targets for bacterial infection. Eur J Cell Biol 85: 235-242.
26. Hirschhausen, N., Schlesier, T., Schmidt, M.A., Gotz, F., Peters, G., and Heilmann, C. (2010) A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell Microbiol 12: 1746-1764.
27. 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.
28. Kim, H.K., DeDent, A., Cheng, A.G., McAdow, M., Bagnoli, F., Missiakas, D.M., etal. (2010) IsdA and IsdB antibodies protect mice against Staphylococcus aureus abscess formation and lethal challenge. Vaccine 28: 6382-6392.
29. Krishna Kumar, K., Jacques, D.A., Pishchany, G., Caradoc-Davies, T., Spirig, T., Malmirchegini, G.R., etal. (2011) Structural basis for hemoglobin capture by Staphylococcus aureus cell-surface protein, IsdH. J Biol Chem 286: 38439-38447.
30. Kuipers, O.P., de Ruyter, P.G.G.A., Kleerebezem, M., and de Vos, W.M. (1998) Quorum-sensing controlled gene expression in lactic acid bacteria. J Biotechnol 64: 15-21.
31. Levinson, A.I., Dziarski, A., Zweiman, B., and Dziarski, R. (1983) Staphylococcal peptidoglycan: T-cell-dependent mitogen and relatively T-cell-independent polyclonal B-cell activator of human lymphocytes. Infect Immun 39: 290-296.
32. Lofblom, J., Kronqvist, N., Uhlen, M., Stahl, S., and Wernerus, H. (2007) Optimization of electroporation-mediated transformation: Staphylococcus carnosus as model organism. J Appl Microbiol 102: 736-747.
33. Lowy, F.D. (1998) Staphylococcus aureus infections. N Engl J Med 339: 520-532.
34. Luo, B.H., Springer, T.A., and Takagi, J. (2003) Stabilizing the open conformation of the integrin headpiece with a glycan wedge increases affinity for ligand. Proc Natl Acad Sci USA 100: 2403-2408.
35. Luo, B.H., Takagi, J., and Springer, T.A. (2004) Locking the beta3 integrin I-like domain into high and low affinity conformations with disulfides. J Biol Chem 279: 10215-10221.
36. Ma, Y.Q., Qin, J., and Plow, E.F. (2007) Platelet integrin alpha(IIb)beta(3): activation mechanisms. J Thromb Haemost 5: 1345-1352.
37. 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.
38. Mazmanian, S.K., Skaar, E.P., Gaspar, A.H., Humayun, M., Gornicki, P., Jelenska, J., etal. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
39. Miajlovic, H., Fallon, P.G., Irvine, A.D., and Foster, T.J. (2010a) Effect of filaggrin breakdown products on growth of and protein expression by Staphylococcus aureus. J Allergy Clin Immunol 126: 1184-1190 e1183.
40. Miajlovic, H., Zapotoczna, M., Geoghegan, J.A., Kerrigan, S.W., Speziale, P., and Foster, T.J. (2010b) Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 156 (Part 3): 920-928.
41. Monk, I.R., Shah, I.M., Xu, M., Tan, M.W., and Foster, T.J. (2012) Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. MBio 3: e00277-11. doi: 10.1128/mBio.00277-11.
42. Moore, G.E., and Glick, J.L. (1967) Perspective of human cell culture. Surg Clin North Am 47: 1315-1324.
43. 2+-dependent inhibitory site. J Biol Chem 273: 6821-6829.
44. O'Neill, E., Humphreys, H., and O'Gara, J.P. (2009) Carriage of both the fnbA and fnbB genes and growth at 37 degrees C promote FnBP-mediated biofilm development in meticillin-resistant Staphylococcus aureus clinical isolates. J Med Microbiol 58 (Part 4): 399-402.
45. Otto, B.R., Verweij-van Vught, A.M., and MacLaren, D.M. (1992a) Blood substitutes and infection. Nature 358: 23-24.
46. Otto, B.R., Verweij-van Vught, A.M., and MacLaren, D.M. (1992b) Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit Rev Microbiol 18: 217-233.
47. Pishchany, G., McCoy, A.L., Torres, V.J., Krause, J.C., Crowe, J.E., Jr, Fabry, M.E., etal. (2010) Specificity for human hemoglobin enhances Staphylococcus aureus infection. Cell Host Microbe 8: 544-550.
48. Que, Y.A., Haefliger, J.A., Piroth, L., Francois, P., Widmer, E., Entenza, J.M., etal. (2005) Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J Exp Med 201: 1627-1635.
49. de Ruyter, P.G.G.A., Kuipers, O.P., and de Vos, W.M. (1996) Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62: 3662-3667.
50. Schleifer, K.H., and Fischer, U. (1982) Description of a New Species of the Genus Staphylococcus: Staphylococcus carnosus. Int J Syst Bacteriol 32: 153-156.
51. Schroder, A., Schroder, B., Roppenser, B., Linder, S., Sinha, B., Fassler, R., etal. (2006) Staphylococcus aureus fibronectin binding protein-A induces motile attachment sites and complex actin remodeling in living endothelial cells. Mol Biol Cell 17: 5198-5210.
52. Sinha, B., and Herrmann, M. (2005) Mechanism and consequences of invasion of endothelial cells by Staphylococcus aureus. Thromb Haemost 94: 266-277.
53. 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.
54. Smith, E.J., Visai, L., Kerrigan, S.W., Speziale, P., and Foster, T.J. (2011) The Sbi protein is a multifunctional immune evasion factor of Staphylococcus aureus. Infect Immun 79: 3801-3809.
55. Speziale, P., Pietrocola, G., Rindi, S., Provenzano, M., Provenza, G., Di Poto, A., etal. (2009) Structural and functional role of Staphylococcus aureus surface components recognizing adhesive matrix molecules of the host. Future Microbiol 4: 1337-1352.
56. Torres, V.J., Pishchany, G., Humayun, M., Schneewind, O., and Skaar, E.P. (2006) Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. J Bacteriol 188: 8421-8429.
57. Visai, L., Yanagisawa, N., Josefsson, E., Tarkowski, A., Pezzali, I., Rooijakkers, S.H., etal. (2009) Immune evasion by Staphylococcus aureus conferred by iron-regulated surface determinant protein IsdH. Microbiology 155 (Part 3): 667-679.
58. Yuan, X.M., Brunk, U.T., and Olsson, A.G. (1995) Effects of iron- and hemoglobin-loaded human monocyte-derived macrophages on oxidation and uptake of LDL. Arterioscler Thromb Vasc Biol 15: 1345-1351.