Identification of a novel iron regulated staphylococcal surface protein with haptoglobin-haemoglobin binding activity

Molecular Microbiology

Volumn 49, Issue 1, 2003, Pages 37-53

  Dryla, Agnieszka ^a   Gelbmann, Dieter ^a   Von Gabain, Alexander ^a   Nagy, Eszter ^a  

^a INTERCELL AG   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; BIOTIN; FUR PROTEIN; GLYCINE; HAPTOGLOBIN; HEMOGLOBIN; IRON; LEUCINE; LIGAND; PLASMA PROTEIN; PROLINE; RECEPTOR; RECOMBINANT PROTEIN; REGULATOR PROTEIN; STAPHYLOCOCCUS HAPTOGLOBIN RECEPTOR A; STAPHYLOCOCCUS SURFACE PROTEIN; THREONINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BINDING AFFINITY; BINDING ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; GENE DELETION; HUMAN; IMMUNOGENICITY; IN VITRO STUDY; ISOTOPE LABELING; LIGAND BINDING; NONHUMAN; NUTRIENT UPTAKE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; RECEPTOR AFFINITY; REGULATORY MECHANISM; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION REGULATION; TWO DIMENSIONAL ELECTROPHORESIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CELL DIVISION; CELL WALL; HAPTOGLOBINS; HEMOGLOBINS; HUMANS; IRON; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); HARA; NEGIBACTERIA; POSIBACTERIA; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 0038385189     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03542.x     Document Type: Article

References (54)

1. Andrade, M.A., Ciccarelli, F.D., Perez-Iratxeta, C., and Bork, P. (2002) NEAT: a domain duplicated in genes near the components of a putative Fe3+ siderophore transporter from Gram-positive pathogenic bacteria. Genome Biol 3: research0047.1-0047.5.
2. Arvidson, S., and Tegmark, K. (2001) Regulation of virulence determinants in Staphylococcus aureus. Int J Med Microbiol 291: 159-170.
3. Baichoo, N., and Helmann, J.D. (2002) Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 184: 5826-5832.
4. Berkova, N., Gilbert, C., Goupil, S., Yan, J., Korobko, V., and Naccache, P.H. (1999)TNF-induced haptoglobin release from human neutrophils: pivotal role of the TNF p55 receptor. J Immunol 162: 6226-6232.
5. Borezee, E., Msadek, T., Durant, L., and Berche, P. (2000) Identification in Listeria monocytogenes of MecA, a homologue of the Bacillus subtilis competence regulatory protein. J Bacteriol 182: 5931-5934.
6. Bracken, C.S., Baer, M.T., Abdur-Rashid, A., Helms, W., and Stojiljkovic, I. (1999) Use of heme-protein complexes by the Yersinia enterocolitica HemR receptor: histidine residues are essential for receptor function. J Bacteriol 181: 6063-6072.
7. Braun, V. (2001) Iron uptake mechanisms and their regulation in pathogenic bacteria. Int J Med Microbiol 291: 67-79.
8. Brown, J., and Holden, D. (2002) Iron acquisition by Gram-positive bacterial pathogens. Microbes Infect 4: 1149-1156.
9. Brown, J.S., Gilliland, S.M., and Holden, D.W. (2001) A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol Microbiol 40: 572-585.
10. Calderwood, S.B., and Mekalanos, J.J. (1987) Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J Bacteriol 169: 4759-4764.
11. Chakraborty, T., Leimeister-Wachter, M., Domann, E., Hartl, M., Goebel, W., Nichterlein, T., and Notermans, S. (1992) Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J Bacteriol 174: 568-574.
12. Cockayne, A., Hill, P.J., Powell, N.B., Bishop, K., Sims, C., and Williams, P. (1998) Molecular cloning of a 32-kilodalton lipoprotein component of a novel iron-regulated Staphylococcus epidermidis ABC transporter. Infect Immun 66: 3767-3774.
13. Cornelissen, C.N., and Sparling, P.F. (1994) Iron piracy: acquisition of transferrin-bound iron by bacterial pathogens. Mol Microbiol 14: 843-850.
14. Crosa, J.H. (1997) Signal transduction and transcriptional and post-transcriptional control of iron-regulated genes in bacteria. Microbiol Mol Biol Rev 61: 319-336.
15. El Ghmati, S.M, Van Hoeyveld, E.M., Van Strijp, J.G., Ceuppens, J.L., and Stevens, E.A. (1996) Identification of haptoglobin as an alternative ligand for CD11b/CD18. J Immunol 1996 (156): 2542-2552.
16. Escolar, L., Perez-Martin, J., and de Lorenzo, V. (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181: 6223-6229.
17. Etz, H., Minh, D.B., Henics, T., Dryla, A., Winkler, B., Triska, C., et al. (2002) Identification of in vivo expressed vaccine candidate antigens from Staphylococcus aureus. Proc Natl Acad Sci USA 99: 6573-6578.
18. Foster, T.J., and Hook, M. (1998) Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6: 484-488.
19. Genco, C.A., and Dixon, D.W. (2001) Emerging strategies in microbial haem capture. Mol Microbiol 39: 1-11.
20. Guerout-Fleury, A.M., Shazand, K., Frandsen, N., and Stragier, P. (1995) Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167: 335-336.
21. Hammerschmidt, S., Bethe, G., Remane, P.H., and Chhatwal, G.S. (1999) Identification of pneumococcal surface protein A as a lactoferrin-binding protein of Streptococcus pneumoniae. Infect Immun 67: 1683-1687.
22. Hochstrasser, D.F., Harrington, MG., Hochstrasser, A.C., Miller, M.J., and Merril, C.R. (1988) Methods for increasing the resolution of two-dimensional protein electrophoresis. Anal Biochem 173: 424-435.
23. Hornef, M.W., Wick, M.J., Rhen, M., and Normark, S. (2002) Bacterial strategies for overcoming host innate and adaptive immune responses. Nat Immunol 3: 1033-1040.
24. Horsburgh, M.J., Ingham, E., and Foster, S.J. (2001) Staphylococcus aureus, fur is an interactive regulator with perr, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J Bacteriol 183: 468-475.
25. Jin, H., Ren, Z., Pozsgay, J.M., Elkins, C., Whitby, P.W., Morton, D.J., and Stull, T.L. (1996) Cloning of a DNA fragment encoding a heme-repressible haemoglobin-binding outer membrane protein from Haemophilus influenzae. Infect Immun 64: 3134-3141.
26. Kahler, C.M., Blum, E., Miller, Y.K., Ryan, D., Popovic, T., and Stephens, D.S. (2001) exl, an exchangeable genetic island in Neisseria meningitides. Infect Immun 69: 1687-1696.
27. Kreiswirth, B.N., Lofdahl, S., Bentley, M.J., O'Reilly, M., Schlievert, P.M., Bergdoll, M.S., and Novick, R.P. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 680-685.
28. Kristiansen, M., Graversen, J.H., Jacobsen, C., Sonne, O., Hoffman, H.J., Law, S.K., and Moestrup, S.K. (2001) Identification of the haemoglobin scavenger receptor. Nature 409: 198-201.
29. Kuroda, M, Ohta, T., Uchiyama, I., Baba, T., Yuzawa, H., Kobayashi, I., et al. (2001) Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357: 1225-1240.
30. Lei, B., DeLeo, F.R., Hoe, N.P., Graham, M.R., Mackie, S.M., Cole, R.L., et al. (2001) Evasion of human innate and acquired immunity by a bacterial homolog of CD11b that inhibits opsonophagocytosis. Nat Med 7: 1298-1305.
31. Lewis, L.A., Gray, E., Wang, Y.P., Roe, B.A., and Dyer, D.W. (1997) Molecular characterization of hpuAB, the haemoglobin-haptoglobin-utilization operon of Neisseria meningitidis. Mol Microbiol 3: 737-749.
32. de Lorenzo, V., Giovannini, F., Herrero, M., and Neilands, J.B. (1988) Metal ion regulation of gene expression. Fur repressor-operator interaction at the promoter region of the aerobactin system of pCoIV-K30. J Mol Biol 203: 875-884.
33. Mazmanian, S.K., Liu, G., Ton-That, H., and Schneewind, O. (1999) Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285: 760-763.
34. Mazmanian, S.K., Ton-That, H., Su, K., and Schneewind, O. (2002) An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc Natl Acad Sci USA 99: 2293-2298.
35. Mazmanian, S.K., Skaar, E.P., Gaspar, A.H., Humayun, M., Gornicki, P., Jelenska, J., et al. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
36. McDevitt, D., Francois, P., Vaudaux, P., and Foster, T.J. (1994) Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol Microbiol 11: 237-248.
37. Modun, B., and Williams, P. (1999) The staphylococcal transferrin-binding protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase. Infect Immun 67: 1086-1092.
38. Morrissey, J.A., Cockayne, A., Hammacott, J., Bishop, K., Denman-Johnson, A., Hill, P.J., and Williams, P. (2002) Conservation, surface exposure, and in vivo expression of the Frp family of iron-regulated cell wall proteins in Staphylococcus aureus. Infect Immun 70: 2399-2407.
39. Novick, R.P. (1967) Properties of a cryptic high-frequency transducing phage in Staphyloccus aureus. Virology 33: 155-166.
40. Oh, S.K., Pavlotsky, N., and Tauber, A.I. (1990) Specific binding of haptoglobin to human neutrophils and its functional consequences. J Leukoc Biol 47: 142-148.
41. Park, P.W., Rosenbloom, J., Abrams, W.R., Rosenbloom, J., and Mecham, R.P. (1996) Molecular cloning and expression of the gene for elastin-binding protein (ebpS) in Staphylococcus aureus. J Biol Chem 271: 15803-15809.
42. Ratledge, C., and Dover, L.G. (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54: 881-941.
43. Ren, Z., Jin, H., Morton, D.J., and Stull, T.L. (1998) hgpB, a gene encoding a second Haemophilus influenzae hemoglobin- and hemoglobin-haptoglobin-binding protein. Infect Immun 66: 4733-4741.
44. Ripio, M.T., Dominguez-Bernal, G., Suarez, M., Brehm, K., Berche, P., and Vazquez-Boland, J.A. (1996) Transcriptional activation of virulence genes in wild-type strains of Listeria monocytogenes, response to a change in the extracellular medium composition. Res Microbiol 147: 371-384.
45. Ross, G.D. (2000) Regulation of the adhesion versus cytotoxic functions of the Mac-1/CR3/alphaMbeta2-integrin glycoprotein. Crit Rev Immunol 20: 197-222.
46. Rossbacher, J., Wagner, L., and Pasternack, M.S. (1999) Inhibitory effect of haptoglobin on granulocyte chemotaxis, phagocytosis and bactericidal activity. Scand J Immunol 50: 399-404.
47. Schryvers, A.B., and Stojiljkovic, I. (1999) Iron acquisition systems in the pathogenic Neisseria. Mol Microbiol 32: 1117-1123.
48. Shafer, W.M., and Iandolo, J.J. (1979) Genetics of staphylococcal enterotoxin B in methicillin-resistant isolates of Staphylococcus aureus. Infect Immun 25: 902-911.
49. Simpson, W., Olczak, T., and Genco, C.A. (2000) Characterization and expression of HmuR, a TonB-dependent hemoglobin receptor of Porphyromonas gingivalis. J Bacteriol 182: 5737-5748.
50. Stojiljkovic, I., Larson, J., Hwa, V., Anic, S., and So, M. (1996) HmbR outer membrane receptors of pathogenic Neisseria spp. iron-regulated, hemoglobin-binding proteins with a high level of primary structure conservation. J Bacteriol 178: 4670-4678.
51. Taylor, J.M., and Heinrichs, D.E. (2002) Transferrin binding in Staphylococcus aureus: involvement of a cell wall-anchored protein. Mol Microbiol 43: 1603-1614.
52. Wagner, L., Gessl, A., Parzer, S.B., Base, W., Waldhausl, W., and Pasternack, M.S. (1996) Haptoglobin phenotyping by newly developed monoclonal antibodies. Demonstration of haptoglobin uptake into peripheral blood neutrophils and monocytes. J Immunol 156: 1989-1996.
53. Wassell, J. (2000) Haptoglobin: function and polymorphism. Clin Laboratory 46: 547-552.
54. Xiong, A., Singh, V.K., Cabrera, G., and Jayaswal, R.K. (2000) Molecular characterization of the ferric-uptake regulator, Fur, from Staphylococcus aureus. Microbiology 146: 659-668.