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 Sauer, J.-D.
Right arrow Articles by Heinzen, R. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sauer, J.-D.
Right arrow Articles by Heinzen, R. A.

 Previous Article  |  Next Article 

Infection and Immunity, August 2005, p. 4494-4504, Vol. 73, No. 8
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.8.4494-4504.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Specificity of Legionella pneumophila and Coxiella burnetii Vacuoles and Versatility of Legionella pneumophila Revealed by Coinfection

John-Demian Sauer,1,2 Jeffrey G. Shannon,1 Dale Howe,1 Stanley F. Hayes,1 Michele S. Swanson,2 and Robert A. Heinzen1*

Coxiella Pathogenesis Section, Laboratory of Intracellular Parasites, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, 903 S. 4th St., Hamilton, Montana 59840,1 Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan 481092

Received 18 January 2005/ Accepted 11 March 2005

Legionella pneumophila and Coxiella burnetii are phylogenetically related intracellular bacteria that cause aerosol-transmitted lung infections. In host cells both pathogens proliferate in vacuoles whose biogenesis displays some common features. To test the functional similarity of their respective intracellular niches, African green monkey kidney epithelial (Vero) cells, A/J mouse bone marrow-derived macrophages, human macrophages, and human dendritic cells (DC) containing mature C. burnetii replication vacuoles were superinfected with L. pneumophila, and then the acidity, lysosome-associated membrane protein (LAMP) content, and cohabitation of mature replication vacuoles was assessed. In all cell types, wild-type L. pneumophila occupied distinct vacuoles in close association with acidic, LAMP-positive C. burnetii replication vacuoles. In murine macrophages, but not primate macrophages, DC, or epithelial cells, L. pneumophila replication vacuoles were acidic and LAMP positive. Unlike wild-type L. pneumophila, type IV secretion-deficient dotA mutants trafficked to lysosome-like C. burnetii vacuoles in Vero cells where they survived but failed to replicate. In primate macrophages, DC, or epithelial cells, growth of L. pneumophila was as robust in superinfected cell cultures as in those singly infected. Thus, despite their noted similarities, L. pneumophila and C. burnetii are exquisitely adapted for replication in unique replication vacuoles, and factors that maintain the C. burnetii replication vacuole do not alter biogenesis of an adjacent L. pneumophila replication vacuole. Moreover, L. pneumophila can replicate efficiently in either lysosomal vacuoles of A/J mouse cells or in nonlysosomal vacuoles of primate cells.

* Corresponding author. Mailing address: Laboratory of Intracellular Parasites, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, 903 S. 4th St., Hamilton, MT 59840. Phone: (406) 375-9695. Fax: (307) 363-9380. E-mail: rheinzen{at}niaid.nih.gov.

Editor: A. D. O'Brien

Infection and Immunity, August 2005, p. 4494-4504, Vol. 73, No. 8
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.8.4494-4504.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Chong, A., Lima, C. A., Allan, D. S., Nasrallah, G. K., Garduno, R. A. (2009). The Purified and Recombinant Legionella pneumophila Chaperonin Alters Mitochondrial Trafficking and Microfilament Organization. Infect. Immun. 77: 4724-4739 [Abstract] [Full Text]  
  • Voth, D. E., Howe, D., Beare, P. A., Vogel, J. P., Unsworth, N., Samuel, J. E., Heinzen, R. A. (2009). The Coxiella burnetii Ankyrin Repeat Domain-Containing Protein Family Is Heterogeneous, with C-Terminal Truncations That Influence Dot/Icm-Mediated Secretion. J. Bacteriol. 191: 4232-4242 [Abstract] [Full Text]  
  • Beare, P. A., Unsworth, N., Andoh, M., Voth, D. E., Omsland, A., Gilk, S. D., Williams, K. P., Sobral, B. W., Kupko, J. J. III, Porcella, S. F., Samuel, J. E., Heinzen, R. A. (2009). Comparative Genomics Reveal Extensive Transposon-Mediated Genomic Plasticity and Diversity among Potential Effector Proteins within the Genus Coxiella. Infect. Immun. 77: 642-656 [Abstract] [Full Text]  
  • Chen, D. E., Podell, S., Sauer, J.-D., Swanson, M. S., Saier, M. H. (2008). The phagosomal nutrient transporter (Pht) family. Microbiology 154: 42-53 [Abstract] [Full Text]  
  • Chatfield, C. H., Cianciotto, N. P. (2007). The Secreted Pyomelanin Pigment of Legionella pneumophila Confers Ferric Reductase Activity. Infect. Immun. 75: 4062-4070 [Abstract] [Full Text]  
  • Rogers, J., Hakki, A., Perkins, I., Newton, C., Widen, R., Burdash, N., Klein, T., Friedman, H. (2007). Legionella pneumophila Infection Up-Regulates Dendritic Cell Toll-Like Receptor 2 (TLR2)/TLR4 Expression and Key Maturation Markers. Infect. Immun. 75: 3205-3208 [Abstract] [Full Text]  
  • Santic, M., Asare, R., Doric, M., Abu Kwaik, Y. (2007). Host-Dependent Trigger of Caspases and Apoptosis by Legionella pneumophila. Infect. Immun. 75: 2903-2913 [Abstract] [Full Text]  
  • LeBlanc, J. J., Davidson, R. J., Hoffman, P. S. (2006). Compensatory Functions of Two Alkyl Hydroperoxide Reductases in the Oxidative Defense System of Legionella pneumophila.. J. Bacteriol. 188: 6235-6244 [Abstract] [Full Text]  
  • Fernandez-Moreira, E., Helbig, J. H., Swanson, M. S. (2006). Membrane Vesicles Shed by Legionella pneumophila Inhibit Fusion of Phagosomes with Lysosomes.. Infect. Immun. 74: 3285-3295 [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»