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

 Previous Article  |  Next Article 

Journal of Bacteriology, February 2001, p. 951-958, Vol. 183, No. 3
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.3.951-958.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Periplasmic Transit and Disulfide Bond Formation of the Autotransported Shigella Protein IcsA

Lauren D. Brandon and Marcia B. Goldberg*

Infectious Disease Division, Massachusetts General Hospital, Boston, Massachusetts 02114

Received 15 August 2000/Accepted 9 November 2000

The Shigella outer membrane protein IcsA belongs to the family of type V secreted (autotransported) virulence factors. Members of this family mediate their own translocation across the bacterial outer membrane: the carboxy-terminal beta  domain forms a beta  barrel channel in the outer membrane through which the amino-terminal alpha  domain passes. IcsA, which is localized at one pole of the bacterium, mediates actin assembly by Shigella, which is essential for bacterial intracellular movement and intercellular dissemination. Here, we characterize the transit of IcsA across the periplasm during its secretion. We show that an insertion in the dsbB gene, whose gene product mediates disulfide bond formation of many periplasmic intermediates, does not affect the surface expression or unipolar targeting of IcsA. However, IcsA forms one disulfide bond in the periplasm in a DsbA/DsbB-dependent fashion. Furthermore, cellular fractionation studies reveal that IcsA has a transient soluble periplasmic intermediate. Our data also suggest that IcsA is folded in a proteinase K-resistant state in the periplasm. From these data, we propose a novel model for the secretion of IcsA that may be applicable to other autotransported proteins.

* Corresponding author. Mailing address: Infectious Disease Division, Massachusetts General Hospital, 55 Fruit St., GRJ504, Boston, MA 02114. Phone: (617) 726-3812. Fax: (617) 726-7416. E-mail: mgoldberg1{at}partners.org.

Journal of Bacteriology, February 2001, p. 951-958, Vol. 183, No. 3
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.3.951-958.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Ieva, R., Bernstein, H. D. (2009). Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. USA 106: 19120-19125 [Abstract] [Full Text]  
  • Ruiz-Perez, F., Henderson, I. R., Leyton, D. L., Rossiter, A. E., Zhang, Y., Nataro, J. P. (2009). Roles of Periplasmic Chaperone Proteins in the Biogenesis of Serine Protease Autotransporters of Enterobacteriaceae. J. Bacteriol. 191: 6571-6583 [Abstract] [Full Text]  
  • Janakiraman, A., Fixen, K. R., Gray, A. N., Niki, H., Goldberg, M. B. (2009). A Genome-Scale Proteomic Screen Identifies a Role for DnaK in Chaperoning of Polar Autotransporters in Shigella. J. Bacteriol. 191: 6300-6311 [Abstract] [Full Text]  
  • Bodelon, G., Marin, E., Fernandez, L. A. (2009). Role of Periplasmic Chaperones and BamA (YaeT/Omp85) in Folding and Secretion of Intimin from Enteropathogenic Escherichia coli Strains. J. Bacteriol. 191: 5169-5179 [Abstract] [Full Text]  
  • Wagner, J. K., Heindl, J. E., Gray, A. N., Jain, S., Goldberg, M. B. (2009). Contribution of the Periplasmic Chaperone Skp to Efficient Presentation of the Autotransporter IcsA on the Surface of Shigella flexneri. J. Bacteriol. 191: 815-821 [Abstract] [Full Text]  
  • May, K. L., Morona, R. (2008). Mutagenesis of the Shigella flexneri Autotransporter IcsA Reveals Novel Functional Regions Involved in IcsA Biogenesis and Recruitment of Host Neural Wiscott-Aldrich Syndrome Protein. J. Bacteriol. 190: 4666-4676 [Abstract] [Full Text]  
  • Purdy, G. E., Fisher, C. R., Payne, S. M. (2007). IcsA Surface Presentation in Shigella flexneri Requires the Periplasmic Chaperones DegP, Skp, and SurA. J. Bacteriol. 189: 5566-5573 [Abstract] [Full Text]  
  • Jain, S., Goldberg, M. B. (2007). Requirement for YaeT in the Outer Membrane Assembly of Autotransporter Proteins. J. Bacteriol. 189: 5393-5398 [Abstract] [Full Text]  
  • Kostakioti, M., Stathopoulos, C. (2006). Role of the {alpha}-Helical Linker of the C-Terminal Translocator in the Biogenesis of the Serine Protease Subfamily of Autotransporters. Infect. Immun. 74: 4961-4969 [Abstract] [Full Text]  
  • Rutherford, N., Charbonneau, M.-E., Berthiaume, F., Betton, J.-M., Mourez, M. (2006). The Periplasmic Folding of a Cysteineless Autotransporter Passenger Domain Interferes with Its Outer Membrane Translocation. J. Bacteriol. 188: 4111-4116 [Abstract] [Full Text]  
  • Junker, M., Schuster, C. C., McDonnell, A. V., Sorg, K. A., Finn, M. C., Berger, B., Clark, P. L. (2006). Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl. Acad. Sci. USA 103: 4918-4923 [Abstract] [Full Text]  
  • Litwin, C. M., Johnson, J. M. (2005). Identification, Cloning, and Expression of the CAMP-Like Factor Autotransporter Gene (cfa) of Bartonella henselae. Infect. Immun. 73: 4205-4213 [Abstract] [Full Text]  
  • Adams, T. M., Wentzel, A., Kolmar, H. (2005). Intimin-Mediated Export of Passenger Proteins Requires Maintenance of a Translocation-Competent Conformation. J. Bacteriol. 187: 522-533 [Abstract] [Full Text]  
  • Henderson, I. R., Navarro-Garcia, F., Desvaux, M., Fernandez, R. C., Ala'Aldeen, D. (2004). Type V Protein Secretion Pathway: the Autotransporter Story. Microbiol. Mol. Biol. Rev. 68: 692-744 [Abstract] [Full Text]  
  • Yang, T. H., Pan, J. G., Seo, Y. S., Rhee, J. S. (2004). Use of Pseudomonas putida EstA as an Anchoring Motif for Display of a Periplasmic Enzyme on the Surface of Escherichia coli. Appl. Environ. Microbiol. 70: 6968-6976 [Abstract] [Full Text]  
  • Velarde, J. J., Nataro, J. P. (2004). Hydrophobic Residues of the Autotransporter EspP Linker Domain Are Important for Outer Membrane Translocation of Its Passenger. J. Biol. Chem. 279: 31495-31504 [Abstract] [Full Text]  
  • Surana, N. K., Cutter, D., Barenkamp, S. J., St. Geme, J. W. III (2004). The Haemophilus influenzae Hia Autotransporter Contains an Unusually Short Trimeric Translocator Domain. J. Biol. Chem. 279: 14679-14685 [Abstract] [Full Text]  
  • Veiga, E., de Lorenzo, V., Fernandez, L. A. (2003). Neutralization of Enteric Coronaviruses with Escherichia coli Cells Expressing Single-Chain Fv-Autotransporter Fusions. J. Virol. 77: 13396-13398 [Abstract] [Full Text]  
  • Nikaido, H. (2003). Molecular Basis of Bacterial Outer Membrane Permeability Revisited. Microbiol. Mol. Biol. Rev. 67: 593-656 [Abstract] [Full Text]  
  • Purdy, G. E., Hong, M., Payne, S. M. (2002). Shigella flexneri DegP Facilitates IcsA Surface Expression and Is Required for Efficient Intercellular Spread. Infect. Immun. 70: 6355-6364 [Abstract] [Full Text]  
  • Charles, M., Perez, M., Kobil, J. H., Goldberg, M. B. (2001). Polar targeting of Shigella virulence factor IcsA in Enterobacteriacae and Vibrio. Proc. Natl. Acad. Sci. USA 10.1073/pnas.171310498v1 [Abstract] [Full Text]  
  • Charles, M., Perez, M., Kobil, J. H., Goldberg, M. B. (2001). Polar targeting of Shigella virulence factor IcsA in Enterobacteriacae and Vibrio. Proc. Natl. Acad. Sci. USA 98: 9871-9876 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»