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Science 7 February 2003: Vol. 299. no. 5608, pp. 906 - 909 DOI: 10.1126/science.1081147
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Reports
Passage of Heme-Iron Across the Envelope of Staphylococcus aureus
Sarkis K. Mazmanian,12*
Eric P. Skaar,12*
Andrew H. Gaspar,12
Munir Humayun,3
Piotr Gornicki,2
Joanna Jelenska,2
Andrzej Joachmiak,4
Dominique M. Missiakas,15
Olaf Schneewind12
The cell wall envelope of Gram-positive pathogens
functions as a scaffold for the attachment of virulence factors and as
a sieve that prevents diffusion of molecules. Here the isd
genes (iron-regulated surface determinant) of Staphylococcus
aureus were found to encode factors responsible for hemoglobin
binding and passage of heme-iron to the cytoplasm, where it acts as an essential nutrient. Heme-iron passage required two sortases that tether
Isd proteins to unique locations within the cell wall. Thus, Isd
appears to act as an import apparatus that uses cell wall-anchored
proteins to relay heme-iron across the bacterial envelope.
1 Committee on Microbiology,
2 Department of Molecular Genetics and Cell Biology,
3 Department of Geophysical Sciences,
5 Department of Biochemistry and Molecular Biology,
University of Chicago, 920 East 58th Street, Chicago, IL 60637, USA.
4 Bioscience Division, Structural Biology Center,
Argonne National Laboratory, 9700 South Cass Avenue, Argonne, IL 60439, USA.
*
These authors contributed equally to this work.
To whom correspondence should be addressed. E-mail:
oschnee{at}delphi.bsd.uchicago.edu
Read the Full Text
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| Full Text »
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| Abstract »
| Full Text »
| PDF »
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| Abstract »
| Full Text »
| PDF »
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151, 3749-3757
| Abstract »
| Full Text »
| PDF »
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| Abstract »
| Full Text »
| PDF »
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| Abstract »
| Full Text »
| PDF »
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- A. H. Gaspar, L. A. Marraffini, E. M. Glass, K. L. DeBord, H. Ton-That, and O. Schneewind (2005)
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187, 4646-4655
| Abstract »
| Full Text »
| PDF »
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- L. A. Marraffini and O. Schneewind (2005)
J. Biol. Chem.
280, 16263-16271
| Abstract »
| Full Text »
| PDF »
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- A. Dryla, S. Prustomersky, D. Gelbmann, M. Hanner, E. Bettinger, B. Kocsis, T. Kustos, T. Henics, A. Meinke, and E. Nagy (2005)
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12, 387-398
| Abstract »
| Full Text »
| PDF »
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- R. Wu, E. P. Skaar, R. Zhang, G. Joachimiak, P. Gornicki, O. Schneewind, and A. Joachimiak (2005)
J. Biol. Chem.
280, 2840-2846
| Abstract »
| Full Text »
| PDF »
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- G. R. Aronoff (2004)
J. Am. Soc. Nephrol.
15, S99-S106
| Full Text »
| PDF »
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- E. P. Skaar, M. Humayun, T. Bae, K. L. DeBord, and O. Schneewind (2004)
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305, 1626-1628
| Abstract »
| Full Text »
| PDF »
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- Y. Zong, T. W. Bice, H. Ton-That, O. Schneewind, and S. V. L. Narayana (2004)
J. Biol. Chem.
279, 31383-31389
| Abstract »
| Full Text »
| PDF »
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- D. Comfort and R. T. Clubb (2004)
Infect. Immun.
72, 2710-2722
| Abstract »
| Full Text »
| PDF »
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- H. Bierne, C. Garandeau, M. G. Pucciarelli, C. Sabet, S. Newton, F. Garcia-del Portillo, P. Cossart, and A. Charbit (2004)
J. Bacteriol.
186, 1972-1982
| Abstract »
| Full Text »
| PDF »
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- S. Znaidi, B. Pelletier, Y. Mukai, and S. Labbe (2004)
J. Biol. Chem.
279, 9462-9474
| Abstract »
| Full Text »
| PDF »
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- R. B. Rea, C. G. M. Gahan, and C. Hill (2004)
Infect. Immun.
72, 717-727
| Abstract »
| Full Text »
| PDF »
- IsdG and IsdI, Heme-degrading Enzymes in the Cytoplasm of Staphylococcus aureus.
- E. P. Skaar, A. H. Gaspar, and O. Schneewind (2004)
J. Biol. Chem.
279, 436-443
| Abstract »
| Full Text »
| PDF »
- Role of Siderophore Biosynthesis in Virulence of Staphylococcus aureus: Identification and Characterization of Genes Involved in Production of a Siderophore.
- S. E. Dale, A. Doherty-Kirby, G. Lajoie, and D. E. Heinrichs (2004)
Infect. Immun.
72, 29-37
| Abstract »
| Full Text »
| PDF »
- Identification and Characterization of HtsA, a Second Heme-Binding Protein Made by Streptococcus pyogenes.
- B. Lei, M. Liu, J. M. Voyich, C. I. Prater, S. V. Kala, F. R. DeLeo, and J. M. Musser (2003)
Infect. Immun.
71, 5962-5969
| Abstract »
| Full Text »
| PDF »
- Fep1 represses expression of the fission yeast Schizosaccharomyces pombe siderophore-iron transport system.
- B. Pelletier, J. Beaudoin, C. C. Philpott, and S. Labbe (2003)
Nucleic Acids Res.
31, 4332-4344
| Abstract »
| Full Text »
| PDF »
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