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 Rossier, O.
Right arrow Articles by Cianciotto, N. P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Rossier, O.
Right arrow Articles by Cianciotto, N. P.

 Previous Article  |  Next Article 

Infection and Immunity, January 2004, p. 310-321, Vol. 72, No. 1
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.1.310-321.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Legionella pneumophila Type II Protein Secretion Promotes Virulence in the A/J Mouse Model of Legionnaires' Disease Pneumonia

Ombeline Rossier, Shawn R. Starkenburg, and Nicholas P. Cianciotto*

Department of Microbiology and Immunology, Northwestern University Medical School, Chicago, Illinois 60611

Received 2 September 2003/ Returned for modification 3 October 2003/ Accepted 7 October 2003

Legionella pneumophila, the gram-negative agent of Legionnaires' disease, possesses type IV pili and a type II protein secretion (Lsp) system, both of which are dependent upon the PilD prepilin peptidase. By analyzing multiple pilD mutants and various types of Lsp mutants as well as performing trans-complementation of these mutants, we have confirmed that PilD and type II secretion genes are required for L. pneumophila infection of both amoebae and human macrophages. Based upon a complete analysis of lspDE, lspF, and lspG mutants, we found that the type II system controls the secretion of protease, RNase, lipase, phospholipase A, phospholipase C, lysophospholipase A, and tartrate-sensitive and tartrate-resistant acid phosphatase activities and influences the appearance of colonies. Examination of the developing L. pneumophila genome database indicated that the organism has two other loci (lspC and lspLM) that are predicted to promote secretion and thus a set of genes that is comparable to the type II secretion genes in other gram-negative bacteria. In contrast to lsp mutants, L. pneumophila pilus mutants lacking either the PilQ secretin, the PspA pseudopilin, or pilin were not defective for colonial growth, secreted activities, or intracellular replication. L. pneumophila dot/icm mutants were also not impaired for type II-dependent exoenzymes. Upon intratracheal inoculation into A/J mice, lspDE, lspF, and pilD mutants, but not pilus mutants, exhibited a reduced ability to grow in the lung, as measured by competition assays. The lspF mutant was also defective in an in vivo kinetic assay. Examination of infected mouse sera revealed that type II secreted proteins are expressed in vivo. Thus, the L. pneumophila Lsp system is a virulence factor and the only type II secretion system linked to intracellular infection.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, Northwestern University Medical School, 320 East Superior St., Chicago, IL 60611. Phone: (312) 503-0385. Fax: (312) 503-1339. E-mail: n-cianciotto{at}northwestern.edu.

Editor: D. L Burns

Infection and Immunity, January 2004, p. 310-321, Vol. 72, No. 1
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.1.310-321.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Allard, K. A., Dao, J., Sanjeevaiah, P., McCoy-Simandle, K., Chatfield, C. H., Crumrine, D. S., Castignetti, D., Cianciotto, N. P. (2009). Purification of Legiobactin and Importance of This Siderophore in Lung Infection by Legionella pneumophila. Infect. Immun. 77: 2887-2895 [Abstract] [Full Text]  
  • Rossier, O., Dao, J., Cianciotto, N. P. (2009). A type II secreted RNase of Legionella pneumophila facilitates optimal intracellular infection of Hartmannella vermiformis. Microbiology 155: 882-890 [Abstract] [Full Text]  
  • Stewart, C. R., Rossier, O., Cianciotto, N. P. (2009). Surface Translocation by Legionella pneumophila: a Form of Sliding Motility That Is Dependent upon Type II Protein Secretion. J. Bacteriol. 191: 1537-1546 [Abstract] [Full Text]  
  • Soderberg, M. A., Dao, J., Starkenburg, S. R., Cianciotto, N. P. (2008). Importance of Type II Secretion for Survival of Legionella pneumophila in Tap Water and in Amoebae at Low Temperatures. Appl. Environ. Microbiol. 74: 5583-5588 [Abstract] [Full Text]  
  • Newton, H. J., Sansom, F. M., Dao, J., Cazalet, C., Bruggemann, H., Albert-Weissenberger, C., Buchrieser, C., Cianciotto, N. P., Hartland, E. L. (2008). Significant Role for ladC in Initiation of Legionella pneumophila Infection. Infect. Immun. 76: 3075-3085 [Abstract] [Full Text]  
  • Sansom, F. M., Riedmaier, P., Newton, H. J., Dunstone, M. A., Muller, C. E., Stephan, H., Byres, E., Beddoe, T., Rossjohn, J., Cowan, P. J., d'Apice, A. J. F., Robson, S. C., Hartland, E. L. (2008). Enzymatic Properties of an Ecto-nucleoside Triphosphate Diphosphohydrolase from Legionella pneumophila: SUBSTRATE SPECIFICITY AND REQUIREMENT FOR VIRULENCE. J. Biol. Chem. 283: 12909-12918 [Abstract] [Full Text]  
  • Galka, F., Wai, S. N., Kusch, H., Engelmann, S., Hecker, M., Schmeck, B., Hippenstiel, S., Uhlin, B. E., Steinert, M. (2008). Proteomic Characterization of the Whole Secretome of Legionella pneumophila and Functional Analysis of Outer Membrane Vesicles. Infect. Immun. 76: 1825-1836 [Abstract] [Full Text]  
  • Soderberg, M. A., Cianciotto, N. P. (2008). A Legionella pneumophila Peptidyl-Prolyl cis-trans Isomerase Present in Culture Supernatants Is Necessary for Optimal Growth at Low Temperatures. Appl. Environ. Microbiol. 74: 1634-1638 [Abstract] [Full Text]  
  • Rossier, O., Dao, J., Cianciotto, N. P. (2008). The Type II Secretion System of Legionella pneumophila Elaborates Two Aminopeptidases, as Well as a Metalloprotease That Contributes to Differential Infection among Protozoan Hosts. Appl. Environ. Microbiol. 74: 753-761 [Abstract] [Full Text]  
  • De Buck, E., Anne, J., Lammertyn, E. (2007). The role of protein secretion systems in the virulence of the intracellular pathogen Legionella pneumophila. Microbiology 153: 3948-3953 [Abstract] [Full Text]  
  • Newton, H. J., Sansom, F. M., Dao, J., McAlister, A. D., Sloan, J., Cianciotto, N. P., Hartland, E. L. (2007). Sel1 Repeat Protein LpnE Is a Legionella pneumophila Virulence Determinant That Influences Vacuolar Trafficking. Infect. Immun. 75: 5575-5585 [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]  
  • Molmeret, M., Santic', M., Asare, R., Carabeo, R. A., Kwaik, Y. A. (2007). Rapid Escape of the dot/icm Mutants of Legionella pneumophila into the Cytosol of Mammalian and Protozoan Cells. Infect. Immun. 75: 3290-3304 [Abstract] [Full Text]  
  • DebRoy, S., Dao, J., Soderberg, M., Rossier, O., Cianciotto, N. P. (2006). Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc. Natl. Acad. Sci. USA 103: 19146-19151 [Abstract] [Full Text]  
  • DebRoy, S., Aragon, V., Kurtz, S., Cianciotto, N. P. (2006). Legionella pneumophila Mip, a Surface-Exposed Peptidylproline cis-trans-Isomerase, Promotes the Presence of Phospholipase C-Like Activity in Culture Supernatants. Infect. Immun. 74: 5152-5160 [Abstract] [Full Text]  
  • Huang, B., Yuan, Z., Heron, B. A., Gray, B. R., Eglezos, S., Bates, J. R., Savill, J. (2006). Distribution of 19 major virulence genes in Legionella pneumophila serogroup 1 isolates from patients and water in Queensland, Australia.. J Med Microbiol 55: 993-997 [Abstract] [Full Text]  
  • Newton, H. J., Sansom, F. M., Bennett-Wood, V., Hartland, E. L. (2006). Identification of Legionella pneumophila-Specific Genes by Genomic Subtractive Hybridization with Legionella micdadei and Identification of lpnE, a Gene Required for Efficient Host Cell Entry. Infect. Immun. 74: 1683-1691 [Abstract] [Full Text]  
  • Broich, M., Rydzewski, K., McNealy, T. L., Marre, R., Flieger, A. (2006). The Global Regulatory Proteins LetA and RpoS Control Phospholipase A, Lysophospholipase A, Acyltransferase, and Other Hydrolytic Activities of Legionella pneumophila JR32. J. Bacteriol. 188: 1218-1226 [Abstract] [Full Text]  
  • Allard, K. A., Viswanathan, V. K., Cianciotto, N. P. (2006). lbtA and lbtB Are Required for Production of the Legionella pneumophila Siderophore Legiobactin. J. Bacteriol. 188: 1351-1363 [Abstract] [Full Text]  
  • Miyake, M., Watanabe, T., Koike, H., Molmeret, M., Imai, Y., Abu Kwaik, Y. (2005). Characterization of Legionella pneumophila pmiA, a Gene Essential for Infectivity of Protozoa and Macrophages. Infect. Immun. 73: 6272-6282 [Abstract] [Full Text]  
  • Edelstein, P. H., Hu, B., Shinzato, T., Edelstein, M. A. C., Xu, W., Bessman, M. J. (2005). Legionella pneumophila NudA Is a Nudix Hydrolase and Virulence Factor. Infect. Immun. 73: 6567-6576 [Abstract] [Full Text]  
  • Banerji, S., Bewersdorff, M., Hermes, B., Cianciotto, N. P., Flieger, A. (2005). Characterization of the Major Secreted Zinc Metalloprotease- Dependent Glycerophospholipid:Cholesterol Acyltransferase, PlaC, of Legionella pneumophila. Infect. Immun. 73: 2899-2909 [Abstract] [Full Text]  
  • Rossier, O., Cianciotto, N. P. (2005). The Legionella pneumophila tatB Gene Facilitates Secretion of Phospholipase C, Growth under Iron-Limiting Conditions, and Intracellular Infection. Infect. Immun. 73: 2020-2032 [Abstract] [Full Text]  
  • Neild, A., Murata, T., Roy, C. R. (2005). Processing and Major Histocompatibility Complex Class II Presentation of Legionella pneumophila Antigens by Infected Macrophages. Infect. Immun. 73: 2336-2343 [Abstract] [Full Text]  
  • McNealy, T. L, Forsbach-Birk, V., Shi, C., Marre, R. (2005). The Hfq Homolog in Legionella pneumophila Demonstrates Regulation by LetA and RpoS and Interacts with the Global Regulator CsrA. J. Bacteriol. 187: 1527-1532 [Abstract] [Full Text]  
  • Soderberg, M. A., Rossier, O., Cianciotto, N. P. (2004). The Type II Protein Secretion System of Legionella pneumophila Promotes Growth at Low Temperatures. J. Bacteriol. 186: 3712-3720 [Abstract] [Full Text]  
  • Lammertyn, E., Van Mellaert, L., Meyen, E., Lebeau, I., De Buck, E., Anne, J., Geukens, N. (2004). Molecular and functional characterization of type I signal peptidase from Legionella pneumophila. Microbiology 150: 1475-1483 [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»