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 Cowan, C.
Right arrow Articles by Straley, S. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Cowan, C.
Right arrow Articles by Straley, S. C.

 Previous Article  |  Next Article 

Infection and Immunity, August 2000, p. 4523-4530, Vol. 68, No. 8
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Invasion of Epithelial Cells by Yersinia pestis: Evidence for a Y. pestis-Specific Invasin

Clarissa Cowan, Heather A. Jones, Yasemin H. Kaya, Robert D. Perry, and Susan C. Straley*

Department of Microbiology and Immunology, Chandler Medical Center, University of Kentucky, Lexington, Kentucky 40536-0298

Received 16 February 2000/Returned for modification 5 April 2000/Accepted 5 May 2000

The causative agent of plague, Yersinia pestis, is regarded as being noninvasive for epithelial cells and lacks the major adhesins and invasins of its enteropathogenic relatives Yersinia enterocolitica and Yersinia pseudotuberculosis. However, there are studies indicating that Y. pestis invades and causes systemic infection from ingestive and aerogenic routes of infection. Accordingly, we developed a gentamicin protection assay and reexamined invasiveness of Y. pestis for HeLa cells. By optimizing this assay, we discovered that Y. pestis is highly invasive. Several factors, including the presence of fetal bovine serum, the configuration of the tissue culture plate, the temperature at which the bacteria are grown, and the presence of the plasminogen activator protease Pla-encoding plasmid pPCP1, were found to influence invasiveness strongly. Suboptimal combinations of these factors may have contributed to negative findings by previous studies attempting to demonstrate invasion by Y. pestis. Invasion of HeLa cells was strongly inhibited by cytochalasin D and modestly inhibited by colchicine, indicating strong and modest respective requirements for microfilaments and microtubules. We found no significant effect of the iron status of yersiniae or of the pigmentation locus on invasion and likewise no significant effect of the Yops regulon. However, an unidentified thermally induced property (possibly the Y. pestis-specific capsular protein Caf1) did inhibit invasiveness significantly, and the plasmid pPCP1, unique to Y. pestis, was essential for highly efficient invasion. pPCP1 encodes an invasion-promoting factor and not just an adhesin, because Y. pestis lacking this plasmid still adhered to HeLa cells. These studies have enlarged our picture of Y. pestis biology and revealed the importance of properties that are unique to Y. pestis.


* Corresponding author. Mailing address: Department of Microbiology and Immunology, Chandler Medical Center, University of Kentucky, Lexington, KY 40536-0298. Phone: (859) 323-6538. Fax: (859) 257-8994. E-mail: scstra01{at}pop.uky.edu.


Infection and Immunity, August 2000, p. 4523-4530, Vol. 68, No. 8
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Haiko, J., Suomalainen, M., Ojala, T., Lahteenmaki, K., Korhonen, T. K. (2009). Invited review: Breaking barriers -- attack on innate immune defences by omptin surface proteases of enterobacterial pathogens. Innate Immunity 15: 67-80 [Abstract]  
  • Felek, S., Krukonis, E. S. (2009). The Yersinia pestis Ail Protein Mediates Binding and Yop Delivery to Host Cells Required for Plague Virulence. Infect. Immun. 77: 825-836 [Abstract] [Full Text]  
  • Lawrenz, M. B., Lenz, J. D., Miller, V. L. (2009). A Novel Autotransporter Adhesin Is Required for Efficient Colonization during Bubonic Plague. Infect. Immun. 77: 317-326 [Abstract] [Full Text]  
  • Zhan, L., Han, Y., Yang, L., Geng, J., Li, Y., Gao, H., Guo, Z., Fan, W., Li, G., Zhang, L., Qin, C., Zhou, D., Yang, R. (2008). The Cyclic AMP Receptor Protein, CRP, Is Required for Both Virulence and Expression of the Minimal CRP Regulon in Yersinia pestis Biovar microtus. Infect. Immun. 76: 5028-5037 [Abstract] [Full Text]  
  • Felek, S., Lawrenz, M. B., Krukonis, E. S. (2008). The Yersinia pestis autotransporter YapC mediates host cell binding, autoaggregation and biofilm formation. Microbiology 154: 1802-1812 [Abstract] [Full Text]  
  • Forman, S., Wulff, C. R., Myers-Morales, T., Cowan, C., Perry, R. D., Straley, S. C. (2008). yadBC of Yersinia pestis, a New Virulence Determinant for Bubonic Plague. Infect. Immun. 76: 578-587 [Abstract] [Full Text]  
  • Kim, T.-J., Chauhan, S., Motin, V. L., Goh, E.-B., Igo, M. M., Young, G. M. (2007). Direct Transcriptional Control of the Plasminogen Activator Gene of Yersinia pestis by the Cyclic AMP Receptor Protein. J. Bacteriol. 189: 8890-8900 [Abstract] [Full Text]  
  • Kolodziejek, A. M., Sinclair, D. J., Seo, K. S., Schnider, D. R., Deobald, C. F., Rohde, H. N., Viall, A. K., Minnich, S. S., Hovde, C. J., Minnich, S. A., Bohach, G. A. (2007). Phenotypic characterization of OmpX, an Ail homologue of Yersinia pestis KIM. Microbiology 153: 2941-2951 [Abstract] [Full Text]  
  • Galvan, E. M., Chen, H., Schifferli, D. M. (2007). The Psa Fimbriae of Yersinia pestis Interact with Phosphatidylcholine on Alveolar Epithelial Cells and Pulmonary Surfactant. Infect. Immun. 75: 1272-1279 [Abstract] [Full Text]  
  • Vishnyakova, T. G., Kurlander, R., Bocharov, A. V., Baranova, I. N., Chen, Z., Abu-Asab, M. S., Tsokos, M., Malide, D., Basso, F., Remaley, A., Csako, G., Eggerman, T. L., Patterson, A. P. (2006). CLA-1 and its splicing variant CLA-2 mediate bacterial adhesion and cytosolic bacterial invasion in mammalian cells. Proc. Natl. Acad. Sci. USA 103: 16888-16893 [Abstract] [Full Text]  
  • Liu, F., Chen, H., Galvan, E. M., Lasaro, M. A., Schifferli, D. M. (2006). Effects of Psa and F1 on the Adhesive and Invasive Interactions of Yersinia pestis with Human Respiratory Tract Epithelial Cells.. Infect. Immun. 74: 5636-5644 [Abstract] [Full Text]  
  • Chain, P. S. G., Hu, P., Malfatti, S. A., Radnedge, L., Larimer, F., Vergez, L. M., Worsham, P., Chu, M. C., Andersen, G. L. (2006). Complete Genome Sequence of Yersinia pestis Strains Antiqua and Nepal516: Evidence of Gene Reduction in an Emerging Pathogen.. J. Bacteriol. 188: 4453-4463 [Abstract] [Full Text]  
  • Chromy, B. A., Choi, M. W., Murphy, G. A., Gonzales, A. D., Corzett, C. H., Chang, B. C., Fitch, J. P., McCutchen-Maloney, S. L. (2005). Proteomic Characterization of Yersinia pestis Virulence. J. Bacteriol. 187: 8172-8180 [Abstract] [Full Text]  
  • Cowan, C., Philipovskiy, A. V., Wulff-Strobel, C. R., Ye, Z., Straley, S. C. (2005). Anti-LcrV Antibody Inhibits Delivery of Yops by Yersinia pestis KIM5 by Directly Promoting Phagocytosis. Infect. Immun. 73: 6127-6137 [Abstract] [Full Text]  
  • Luck, S. N., Bennett-Wood, V., Poon, R., Robins-Browne, R. M., Hartland, E. L. (2005). Invasion of Epithelial Cells by Locus of Enterocyte Effacement-Negative Enterohemorrhagic Escherichia coli. Infect. Immun. 73: 3063-3071 [Abstract] [Full Text]  
  • Philipovskiy, A. V., Cowan, C., Wulff-Strobel, C. R., Burnett, S. H., Kerschen, E. J., Cohen, D. A., Kaplan, A. M., Straley, S. C. (2005). Antibody against V Antigen Prevents Yop-Dependent Growth of Yersinia pestis. Infect. Immun. 73: 1532-1542 [Abstract] [Full Text]  
  • Huang, X.-Z., Lindler, L. E. (2004). The pH 6 Antigen Is an Antiphagocytic Factor Produced by Yersinia pestis Independent of Yersinia Outer Proteins and Capsule Antigen. Infect. Immun. 72: 7212-7219 [Abstract] [Full Text]  
  • Cowell, B. A., Twining, S. S., Hobden, J. A., Kwong, M. S. F., Fleiszig, S. M. J. (2003). Mutation of lasA and lasB reduces Pseudomonas aeruginosa invasion of epithelial cells. Microbiology 149: 2291-2299 [Abstract] [Full Text]  
  • Makoveichuk, E., Cherepanov, P., Lundberg, S., Forsberg, A., Olivecrona, G. (2003). pH6 antigen of Yersinia pestis interacts with plasma lipoproteins and cell membranes. J. Lipid Res. 44: 320-330 [Abstract] [Full Text]  
  • PARKHILL, J., THOMSON, N. (2003). Evolutionary Strategies of Human Pathogens. Cold Spring Harb Symp Quant Biol 68: 151-158 [Abstract]  
  • Du, Y., Rosqvist, R., Forsberg, A. (2002). Role of Fraction 1 Antigen of Yersinia pestis in Inhibition of Phagocytosis. Infect. Immun. 70: 1453-1460 [Abstract] [Full Text]  
  • Prentice, M. B., James, K. D., Parkhill, J., Baker, S. G., Stevens, K., Simmonds, M. N., Mungall, K. L., Churcher, C., Oyston, P. C. F., Titball, R. W., Wren, B. W., Wain, J., Pickard, D., Hien, T. T., Farrar, J. J., Dougan, G. (2001). Yersinia pestis pFra Shows Biovar-Specific Differences and Recent Common Ancestry with a Salmonella enterica Serovar Typhi Plasmid. J. Bacteriol. 183: 2586-2594 [Abstract] [Full Text]