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 Pilgrim, S.
Right arrow Articles by Kuhn, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pilgrim, S.
Right arrow Articles by Kuhn, M.

 Previous Article  |  Next Article 

Infection and Immunity, June 2003, p. 3473-3484, Vol. 71, No. 6
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.6.3473-3484.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Deletion of the Gene Encoding p60 in Listeria monocytogenes Leads to Abnormal Cell Division and Loss of Actin-Based Motility

Sabine Pilgrim, Annette Kolb-Mäurer, Ivaylo Gentschev, Werner Goebel,* and Michael Kuhn

Lehrstuhl für Mikrobiologie der Universität Würzburg, Theodor-Boveri-Institut für Biowissenschaften, Am Hubland, D-97074 Würzburg, Germany

Received 24 July 2002/ Returned for modification 24 September 2002/ Accepted 24 February 2003

Protein p60 encoded by the iap gene is regarded as an essential gene product of Listeria monocytogenes. Here we report, however, the successful construction of a viable iap deletion mutant of L. monocytogenes EGD. The mutant, which produces no p60, shows abnormal septum formation and tends to form short filaments and hooked forms during logarithmic growth. These abnormal bacterial cells break into almost normal sized single bacteria in the late-stationary-growth phase. The iap mutant is strongly attenuated in a mouse model after intravenous injection, demonstrating the importance of p60 during infection, and the invasiveness of the {Delta}iap mutant for 3T6 fibroblasts and Caco-2 epithelial cells is slightly reduced. Upon uptake by epithelial cells and macrophages, the iap mutant escapes from the phagosome into the cytosol with the same efficiency as the wild-type strain, and the mutant bacteria also grow intracellularly at a rate similar to that of the wild-type strain. Intracellular movement and cell-to-cell spread are drastically reduced in various cell lines, since the iap-negative bacteria fail to induce the formation of actin tails. However, the bacteria are covered with actin filaments. Most intracellular bacteria show a nonpolar and uneven distribution of ActA around the cell, in contrast to that for the wild-type strain, where ActA is concentrated at the old pole. In an iap+ revertant strain that produces wild-type levels of p60, intracellular movement, cell-to-cell spread, and polar distribution of ActA are fully restored. In vitro analysis of ActA distribution on the filaments of the {Delta}iap strain shows that the loss of bacterial septum formation leads to ActA accumulation at the presumed division sites. In the light of data presented here and elswhere, we propose to rename iap (invasion-associated protein) cwhA (cell wall hydrolase A).

* Corresponding author. Mailing address. Lehrstuhl für Mikrobiologie, Theodor-Boveri Institut für Biowissenschaften der Universität Würzburg, Am Hubland, 97074 Würzburg, Germany. Phone: (49) 931-8884401. Fax: (49) 931-8884402. E-mail: goebel{at}biozentrum.uni-wuerzburg.de.

Editor: S. H. E. Kaufmann

Infection and Immunity, June 2003, p. 3473-3484, Vol. 71, No. 6
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.6.3473-3484.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Tsuge, Y., Ogino, H., Teramoto, H., Inui, M., Yukawa, H. (2008). Deletion of cgR_1596 and cgR_2070, Encoding NlpC/P60 Proteins, Causes a Defect in Cell Separation in Corynebacterium glutamicum R. J. Bacteriol. 190: 8204-8214 [Abstract] [Full Text]  
  • Wang, L., Lin, M. (2008). A novel cell wall-anchored peptidoglycan hydrolase (autolysin), IspC, essential for Listeria monocytogenes virulence: genetic and proteomic analysis. Microbiology 154: 1900-1913 [Abstract] [Full Text]  
  • Monk, I. R., Gahan, C. G. M., Hill, C. (2008). Tools for Functional Postgenomic Analysis of Listeria monocytogenes. Appl. Environ. Microbiol. 74: 3921-3934 [Abstract] [Full Text]  
  • Hett, E. C., Rubin, E. J. (2008). Bacterial Growth and Cell Division: a Mycobacterial Perspective. Microbiol. Mol. Biol. Rev. 72: 126-156 [Abstract] [Full Text]  
  • Bierne, H., Cossart, P. (2007). Listeria monocytogenes Surface Proteins: from Genome Predictions to Function. Microbiol. Mol. Biol. Rev. 71: 377-397 [Abstract] [Full Text]  
  • Young, K. D. (2006). The Selective Value of Bacterial Shape. Microbiol. Mol. Biol. Rev. 70: 660-703 [Abstract] [Full Text]  
  • Gao, L.-Y., Pak, M., Kish, R., Kajihara, K., Brown, E. J. (2006). A Mycobacterial Operon Essential for Virulence In Vivo and Invasion and Intracellular Persistence in Macrophages. Infect. Immun. 74: 1757-1767 [Abstract] [Full Text]  
  • Machata, S., Hain, T., Rohde, M., Chakraborty, T. (2005). Simultaneous Deficiency of both MurA and p60 Proteins Generates a Rough Phenotype in Listeria monocytogenes. J. Bacteriol. 187: 8385-8394 [Abstract] [Full Text]  
  • Heilmann, C., Hartleib, J., Hussain, M. S., Peters, G. (2005). The Multifunctional Staphylococcus aureus Autolysin Aaa Mediates Adherence to Immobilized Fibrinogen and Fibronectin. Infect. Immun. 73: 4793-4802 [Abstract] [Full Text]  
  • Stritzker, J., Schoen, C., Goebel, W. (2005). Enhanced Synthesis of Internalin A in aro Mutants of Listeria monocytogenes Indicates Posttranscriptional Control of the inlAB mRNA. J. Bacteriol. 187: 2836-2845 [Abstract] [Full Text]  
  • Monk, I. R., Cook, G. M., Monk, B. C., Bremer, P. J. (2004). Morphotypic Conversion in Listeria monocytogenes Biofilm Formation: Biological Significance of Rough Colony Isolates. Appl. Environ. Microbiol. 70: 6686-6694 [Abstract] [Full Text]  
  • Johnson, J., Jinneman, K., Stelma, G., Smith, B. G., Lye, D., Messer, J., Ulaszek, J., Evsen, L., Gendel, S., Bennett, R. W., Swaminathan, B., Pruckler, J., Steigerwalt, A., Kathariou, S., Yildirim, S., Volokhov, D., Rasooly, A., Chizhikov, V., Wiedmann, M., Fortes, E., Duvall, R. E., Hitchins, A. D. (2004). Natural Atypical Listeria innocua Strains with Listeria monocytogenes Pathogenicity Island 1 Genes. Appl. Environ. Microbiol. 70: 4256-4266 [Abstract] [Full Text]  
  • Lenz, L. L., Mohammadi, S., Geissler, A., Portnoy, D. A. (2003). SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc. Natl. Acad. Sci. USA 100: 12432-12437 [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»