This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hussain, M. Articles by Herrmann, M. Search for Related Content PubMed PubMed Citation Articles by Hussain, M. Articles by Herrmann, M.

Journal of Bacteriology, December 2001, p. 6778-6786, Vol. 183, No. 23
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.23.6778-6786.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

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

Muzaffar Hussain,^1,* Karsten Becker,¹ Christof von Eiff,¹ Jacques Schrenzel,² Georg Peters,¹ and Mathias Herrmann^1,

Institute of Medical Microbiology, University Hospital of Muenster, Muenster, Germany,¹ and Institute of Medical Microbiology and Hygiene and Division of Infectious Diseases, University Hospital, Geneva, Switzerland²

Received 1 July 2001/Accepted 5 September 2001

The ability to attach to host ligands is a well-established pathogenic factor in invasive Staphylococcus aureus disease. In addition to the family of adhesive proteins bound to the cell wall via the sortase A (srtA) mechanism, secreted proteins such as the fibrinogen-binding protein Efb, the extracellular adhesion protein Eap, or coagulase have been found to interact with various extracellular host molecules. Here we describe a novel protein, the extracellular matrix protein-binding protein (Emp) initially identified in Western ligand blots as a 40-kDa protein due to its broad-spectrum recognition of fibronectin, fibrinogen, collagen, and vitronectin. Emp is expressed in the stationary growth phase and is closely associated with the cell surface and yet is extractable by sodium dodecyl sulfate. The conferring gene emp (1,023 nucleotides) encodes a signal peptide of 26 amino acids and a mature protein of a calculated molecular mass of 35.5 kDa. Using PCR, emp was demonstrated in all 240 S. aureus isolates of a defined clinical strain collection as well as in 6 S. aureus laboratory strains, whereas it is lacking in all 10 S. epidermidis strains tested. Construction of an allelic replacement mutant (mEmp50) revealed the absence of Emp in mEmp50, a significantly decreased adhesion of mEmp50 to immobilized fibronectin and fibrinogen, and restoration of these characteristics upon complementation of mEmp50. Emp expression was also demonstrable upon heterologous complementation of S. carnosus. rEmp expressed in Escherichia coli interacted with fibronectin, fibrinogen, and vitronectin in surface plasmon resonance experiments at a K_d of 21 nM, 91 nM, and 122 pM, respectively. In conclusion, the biologic characterization of Emp suggests that it is a member of the group of secreted S. aureus molecules that interact with an extended spectrum of host ligands and thereby contribute to S. aureus pathogenicity.

---

^* Corresponding author. Mailing address: Institute of Medical Microbiology, University Hospital, Domagkstr. 10, 48129 Muenster, Germany. Phone: 49-251-835-5357. Fax: 49-251-835-5350. E-mail: muzaffa{at}uni-muenster.de.

Present address: Institute of Medical Microbiology and Hygiene, University of Saarland Hospital, Homburg 66421, Germany.

---

Journal of Bacteriology, December 2001, p. 6778-6786, Vol. 183, No. 23
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.23.6778-6786.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

This article has been cited by other articles:

• Piroth, L., Que, Y.-A., Widmer, E., Panchaud, A., Piu, S., Entenza, J. M., Moreillon, P. (2008). The Fibrinogen- and Fibronectin-Binding Domains of Staphylococcus aureus Fibronectin-Binding Protein A Synergistically Promote Endothelial Invasion and Experimental Endocarditis. Infect. Immun. 76: 3824-3831 [Abstract] [Full Text]  
• Johnson, M., Cockayne, A., Morrissey, J. A. (2008). Iron-Regulated Biofilm Formation in Staphylococcus aureus Newman Requires ica and the Secreted Protein Emp. Infect. Immun. 76: 1756-1765 [Abstract] [Full Text]  
• Ventura, C. L., Higdon, R., Kolker, E., Skerrett, S. J., Rubens, C. E. (2008). Host Airway Proteins Interact with Staphylococcus aureus during Early Pneumonia. Infect. Immun. 76: 888-898 [Abstract] [Full Text]  
• Chatterjee, I., Kriegeskorte, A., Fischer, A., Deiwick, S., Theimann, N., Proctor, R. A., Peters, G., Herrmann, M., Kahl, B. C. (2008). In Vivo Mutations of Thymidylate Synthase (Encoded by thyA) Are Responsible for Thymidine Dependency in Clinical Small-Colony Variants of Staphylococcus aureus. J. Bacteriol. 190: 834-842 [Abstract] [Full Text]  
• Hussain, M., von Eiff, C., Sinha, B., Joost, I., Herrmann, M., Peters, G., Becker, K. (2008). eap Gene as Novel Target for Specific Identification of Staphylococcus aureus. J. Clin. Microbiol. 46: 470-476 [Abstract] [Full Text]  
• Harraghy, N., Homerova, D., Herrmann, M., Kormanec, J. (2008). Mapping the Transcription Start Points of the Staphylococcus aureus eap, emp, and vwb Promoters Reveals a Conserved Octanucleotide Sequence That Is Essential for Expression of These Genes. J. Bacteriol. 190: 447-451 [Abstract] [Full Text]  
• Arrecubieta, C., Lee, M.-H., Macey, A., Foster, T. J., Lowy, F. D. (2007). SdrF, a Staphylococcus epidermidis Surface Protein, Binds Type I Collagen. J. Biol. Chem. 282: 18767-18776 [Abstract] [Full Text]  
• Boisset, S., Geissmann, T., Huntzinger, E., Fechter, P., Bendridi, N., Possedko, M., Chevalier, C., Helfer, A. C., Benito, Y., Jacquier, A., Gaspin, C., Vandenesch, F., Romby, P. (2007). Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev. 21: 1353-1366 [Abstract] [Full Text]  
• Sobke, A. C. S., Selimovic, D., Orlova, V., Hassan, M., Chavakis, T., Athanasopoulos, A. N., Schubert, U., Hussain, M., Thiel, G., Preissner, K. T., Herrmann, M. (2006). The extracellular adherence protein from Staphylococcus aureus abrogates angiogenic responses of endothelial cells by blocking Ras activation. FASEB J. 20: 2621-2623 [Abstract] [Full Text]  
• Michel, A., Agerer, F., Hauck, C. R., Herrmann, M., Ullrich, J., Hacker, J., Ohlsen, K. (2006). Global Regulatory Impact of ClpP Protease of Staphylococcus aureus on Regulons Involved in Virulence, Oxidative Stress Response, Autolysis, and DNA Repair.. J. Bacteriol. 188: 5783-5796 [Abstract] [Full Text]  
• Hallstrom, T., Trajkovska, E., Forsgren, A., Riesbeck, K. (2006). Haemophilus influenzae Surface Fibrils Contribute to Serum Resistance by Interacting with Vitronectin. J. Immunol. 177: 430-436 [Abstract] [Full Text]  
• Blickwede, M., Goethe, R., Wolz, C., Valentin-Weigand, P., Schwarz, S. (2005). Molecular basis of florfenicol-induced increase in adherence of Staphylococcus aureus strain Newman. J Antimicrob Chemother 56: 315-323 [Abstract] [Full Text]  
• Chatterjee, I., Becker, P., Grundmeier, M., Bischoff, M., Somerville, G. A., Peters, G., Sinha, B., Harraghy, N., Proctor, R. A., Herrmann, M. (2005). Staphylococcus aureus ClpC Is Required for Stress Resistance, Aconitase Activity, Growth Recovery, and Death. J. Bacteriol. 187: 4488-4496 [Abstract] [Full Text]  
• Harraghy, N., Kormanec, J., Wolz, C., Homerova, D., Goerke, C., Ohlsen, K., Qazi, S., Hill, P., Herrmann, M. (2005). sae is essential for expression of the staphylococcal adhesins Eap and Emp. Microbiology 151: 1789-1800 [Abstract] [Full Text]  
• Grundmeier, M., Hussain, M., Becker, P., Heilmann, C., Peters, G., 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 [Abstract] [Full Text]  
• Kostakioti, M., Stathopoulos, C. (2004). Functional Analysis of the Tsh Autotransporter from an Avian Pathogenic Escherichia coli Strain. Infect. Immun. 72: 5548-5554 [Abstract] [Full Text]  
• Xiong, Y.-Q., Bayer, A. S., Yeaman, M. R., van Wamel, W., Manna, A. C., Cheung, A. L. (2004). Impacts of sarA and agr in Staphylococcus aureus Strain Newman on Fibronectin-Binding Protein A Gene Expression and Fibronectin Adherence Capacity In Vitro and in Experimental Infective Endocarditis. Infect. Immun. 72: 1832-1836 [Abstract] [Full Text]  
• Heilmann, C., Thumm, G., Chhatwal, G. S., Hartleib, J., Uekotter, A., Peters, G. (2003). Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis. Microbiology 149: 2769-2778 [Abstract] [Full Text]  
• Haggar, A., Hussain, M., Lonnies, H., Herrmann, M., Norrby-Teglund, A., Flock, J.-I. (2003). Extracellular Adherence Protein from Staphylococcus aureus Enhances Internalization into Eukaryotic Cells. Infect. Immun. 71: 2310-2317 [Abstract] [Full Text]  
• Clarke, S. R., Harris, L. G., Richards, R. G., Foster, S. J. (2002). Analysis of Ebh, a 1.1-Megadalton Cell Wall-Associated Fibronectin-Binding Protein of Staphylococcus aureus. Infect. Immun. 70: 6680-6687 [Abstract] [Full Text]  
• Fink, D. L., Green, B. A., St. Geme III, J. W. (2002). The Haemophilus influenzae Hap Autotransporter Binds to Fibronectin, Laminin, and Collagen IV. Infect. Immun. 70: 4902-4907 [Abstract] [Full Text]  
• Bjerketorp, J., Nilsson, M., Ljungh, A., Flock, J.-I., Jacobsson, K., Frykberg, L. (2002). A novel von Willebrand factor binding protein expressed by Staphylococcus aureus. Microbiology 148: 2037-2044 [Abstract] [Full Text]