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 Sexton, J. A.
Right arrow Articles by Vogel, J. P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sexton, J. A.
Right arrow Articles by Vogel, J. P.

 Previous Article  |  Next Article 

Infection and Immunity, October 2004, p. 5983-5992, Vol. 72, No. 10
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.10.5983-5992.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Legionella pneumophila DotU and IcmF Are Required for Stability of the Dot/Icm Complex

Jessica A. Sexton,1 Jennifer L. Miller,1 Aki Yoneda,1 Thomas E. Kehl-Fie,2 and Joseph P. Vogel1*

Department of Molecular Microbiology,1 Department of Pediatrics, Washington University School of Medicine, St. Louis, Missouri2

Received 7 April 2004/ Returned for modification 13 May 2004/ Accepted 26 June 2004

Legionella pneumophila utilizes a type IV secretion system (T4SS) encoded by 26 dot/icm genes to replicate inside host cells and cause disease. In contrast to all other L. pneumophila dot/icm genes, dotU and icmF have homologs in a wide variety of gram-negative bacteria, none of which possess a T4SS. Instead, dotU and icmF orthologs are linked to a locus encoding a conserved cluster of proteins designated IcmF-associated homologous proteins, which has been proposed to constitute a novel cell surface structure. We show here that dotU is partially required for L. pneumophila intracellular growth, similar to the known requirement for icmF. In addition, we show that dotU and icmF are necessary for optimal plasmid transfer and sodium sensitivity, two additional phenotypes associated with a functional Dot/Icm complex. We found that these effects are due to the destabilization of the T4SS at the transition into the stationary phase, the point at which L. pneumophila becomes virulent. Specifically, three Dot proteins (DotH, DotG, and DotF) exhibit decreased stability in a {Delta}dotU {Delta}icmF strain. Furthermore, overexpression of just one of these proteins, DotH, is sufficient to suppress the intracellular growth defect of the {Delta}dotU {Delta}icmF mutant. This suggests a model where the DotU and IcmF proteins serve to prevent DotH degradation and therefore function to stabilize the L. pneumophila T4SS. Due to their wide distribution among bacterial species and their genetic linkage to known or predicted cell surface structures, we propose that this function in complex stabilization may be broadly conserved.

* Corresponding author. Mailing address: Department of Molecular Microbiology, Washington University, Campus Box 8230, 660 S. Euclid Ave., St. Louis, MO 63110. Phone: (314) 747-1029. Fax: (314) 362-3203. E-mail: jvogel{at}borcim.wustl.edu.

Editor: J. T. Barbieri

Infection and Immunity, October 2004, p. 5983-5992, Vol. 72, No. 10
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.10.5983-5992.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Ma, L.-S., Lin, J.-S., Lai, E.-M. (2009). An IcmF Family Protein, ImpLM, Is an Integral Inner Membrane Protein Interacting with ImpKL, and Its Walker A Motif Is Required for Type VI Secretion System-Mediated Hcp Secretion in Agrobacterium tumefaciens. J. Bacteriol. 191: 4316-4329 [Abstract] [Full Text]  
  • Leiman, P. G., Basler, M., Ramagopal, U. A., Bonanno, J. B., Sauder, J. M., Pukatzki, S., Burley, S. K., Almo, S. C., Mekalanos, J. J. (2009). From the Cover: Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. USA 106: 4154-4159 [Abstract] [Full Text]  
  • Aschtgen, M.-S., Bernard, C. S., De Bentzmann, S., Lloubes, R., Cascales, E. (2008). SciN Is an Outer Membrane Lipoprotein Required for Type VI Secretion in Enteroaggregative Escherichia coli. J. Bacteriol. 190: 7523-7531 [Abstract] [Full Text]  
  • Filloux, A., Hachani, A., Bleves, S. (2008). The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154: 1570-1583 [Abstract] [Full Text]  
  • Barysheva, O. V., Fujii, J., Takaesu, G., Yoshida, S.-i. (2008). Application of unstable Gfp variants to the kinetic study of Legionella pneumophila icm gene expression during infection. Microbiology 154: 1015-1025 [Abstract] [Full Text]  
  • Shalom, G., Shaw, J. G., Thomas, M. S. (2007). In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages. Microbiology 153: 2689-2699 [Abstract] [Full Text]  
  • Brotcke, A., Weiss, D. S., Kim, C. C., Chain, P., Malfatti, S., Garcia, E., Monack, D. M. (2006). Identification of MglA-Regulated Genes Reveals Novel Virulence Factors in Francisella tularensis. Infect. Immun. 74: 6642-6655 [Abstract] [Full Text]  
  • Vincent, C. D., Buscher, B. A., Friedman, J. R., Williams, L. A., Bardill, P., Vogel, J. P. (2006). Identification of Non-dot/icm Suppressors of the Legionella pneumophila {Delta}dotL Lethality Phenotype. J. Bacteriol. 188: 8231-8243 [Abstract] [Full Text]  
  • Pukatzki, S., Ma, A. T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W. C., Heidelberg, J. F., Mekalanos, J. J. (2006). Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. USA 103: 1528-1533 [Abstract] [Full Text]  
  • Yerushalmi, G., Zusman, T., Segal, G. (2005). Additive Effect on Intracellular Growth by Legionella pneumophila Icm/Dot Proteins Containing a Lipobox Motif. Infect. Immun. 73: 7578-7587 [Abstract] [Full Text]  
  • Parsons, D. A., Heffron, F. (2005). sciS, an icmF Homolog in Salmonella enterica Serovar Typhimurium, Limits Intracellular Replication and Decreases Virulence. Infect. Immun. 73: 4338-4345 [Abstract] [Full Text]  
  • Buscher, B. A., Conover, G. M., Miller, J. L., Vogel, S. A., Meyers, S. N., Isberg, R. R., Vogel, J. P. (2005). The DotL Protein, a Member of the TraG-Coupling Protein Family, Is Essential for Viability of Legionella pneumophila Strain Lp02. J. Bacteriol. 187: 2927-2938 [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»