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 Coburn, B.
Right arrow Articles by Finlay, B. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Coburn, B.
Right arrow Articles by Finlay, B. B.

 Previous Article  |  Next Article 

Infection and Immunity, June 2005, p. 3219-3227, Vol. 73, No. 6
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.6.3219-3227.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Salmonella enterica Serovar Typhimurium Pathogenicity Island 2 Is Necessary for Complete Virulence in a Mouse Model of Infectious Enterocolitis

Bryan Coburn,1 Yuling Li,1 David Owen,2 Bruce A. Vallance,3 and B. Brett Finlay1,4*

Michael Smith Laboratories and Department of Microbiology and Immunology,1 Department of Biochemistry and Molecular Biology, University of British Columbia, Vancouver, Canada,4 Department of Anatomical Pathology, Vancouver General Hospital, Vancouver, Canada,2 BC Research Institute, BC Children's and Women's Hospital, Vancouver, Canada3

Received 9 December 2004/ Returned for modification 21 January 2005/ Accepted 8 February 2005

Salmonella species cause a wide range of disease in multiple hosts. Salmonella enterica serovar Typhimurium causes self-limited intestinal disease in humans and systemic typhoid-like illness in susceptible mice. The prevailing dogma in murine S. enterica serovar Typhimurium pathogenesis is that distinct virulence mechanisms—Salmonella pathogenicity islands 1 and 2 (SPI1 and SPI2)—perform distinct roles in pathogenesis, the former being important for invasion and intestinal disease and the latter important for intracellular survival and systemic persistence and disease. Although evidence from bovine infections has suggested that SPI2 has a role in ileal disease, there is no evidence that SPI2 is important for inflammation in a disease that more closely recapitulates human colitis. Using S. enterica serovar Typhimurium strains that lack functional type III secretion systems, we demonstrate that SPI2 is essential for complete virulence in murine infectious enterocolitis. Using a recently characterized murine model (M. Barthel,S. Hapfelmeier, L. Quintanilla-Martinez, M. Kremer, M. Rohde, M. Hogardt, K. Pfeffer, H. Russmann, and W. D. Hardt, Infect. Immun. 71:2839-2858, 2003), we demonstrate that SPI1 mutants are unable to cause intestinal disease 48 h after infection and that SPI2-deficient bacteria also cause significantly attenuated typhlitis. We show that at the peak of inflammation in the cecum, SPI2 mutants induce diminished intercellular adhesion molecule 1 expression and neutrophil recruitment but that wild-type and mutant Salmonella are similarly distributed in the lumen of the infected organ. Finally, we demonstrate that attenuation of intestinal inflammation is accompanied by resolution of typhlitis in the mutant, but not wild-type, infections. Collectively, these results indicate that SPI2 is needed for enterocolitis, as well as for systemic disease.

* Corresponding author. Mailing address: Michael Smith Laboratories, University of British Columbia, 2185 East Mall, Vancouver, British Columbia V6T 1Z4, Canada. Phone: (604) 822-2493. Fax: (604) 822-9830. E-mail: bfinlay{at}interchange.ubc.ca.

Editor: D. L. Burns

Infection and Immunity, June 2005, p. 3219-3227, Vol. 73, No. 6
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.6.3219-3227.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Suar, M., Periaswamy, B., Songhet, P., Misselwitz, B., Muller, A., Kappeli, R., Kremer, M., Heikenwalder, M., Hardt, W.-D. (2009). Accelerated Type III Secretion System 2-Dependent Enteropathogenesis by a Salmonella enterica Serovar Enteritidis PT4/6 Strain. Infect. Immun. 77: 3569-3577 [Abstract] [Full Text]  
  • Desin, T. S., Lam, P.-K. S., Koch, B., Mickael, C., Berberov, E., Wisner, A. L. S., Townsend, H. G. G., Potter, A. A., Koster, W. (2009). Salmonella enterica Serovar Enteritidis Pathogenicity Island 1 Is Not Essential for but Facilitates Rapid Systemic Spread in Chickens. Infect. Immun. 77: 2866-2875 [Abstract] [Full Text]  
  • Haneda, T., Winter, S. E., Butler, B. P., Wilson, R. P., Tukel, C., Winter, M. G., Godinez, I., Tsolis, R. M., Baumler, A. J. (2009). The Capsule-Encoding viaB Locus Reduces Intestinal Inflammation by a Salmonella Pathogenicity Island 1-Independent Mechanism. Infect. Immun. 77: 2932-2942 [Abstract] [Full Text]  
  • Kum, W. W. S., Lee, S., Grassl, G. A., Bidshahri, R., Hsu, K., Ziltener, H. J., Finlay, B. B. (2009). Lack of Functional P-Selectin Ligand Exacerbates Salmonella Serovar Typhimurium Infection. J. Immunol. 182: 6550-6561 [Abstract] [Full Text]  
  • Bhagwat, A. A., Jun, W., Liu, L., Kannan, P., Dharne, M., Pheh, B., Tall, B. D., Kothary, M. H., Gross, K. C., Angle, S., Meng, J., Smith, A. (2009). Osmoregulated periplasmic glucans of Salmonella enterica serovar Typhimurium are required for optimal virulence in mice. Microbiology 155: 229-237 [Abstract] [Full Text]  
  • Ashkar, A. A., Reid, S., Verdu, E. F., Zhang, K., Coombes, B. K. (2009). Interleukin-15 and NK1.1+ Cells Provide Innate Protection against Acute Salmonella enterica Serovar Typhimurium Infection in the Gut and in Systemic Tissues. Infect. Immun. 77: 214-222 [Abstract] [Full Text]  
  • Papp-Wallace, K. M., Nartea, M., Kehres, D. G., Porwollik, S., McClelland, M., Libby, S. J., Fang, F. C., Maguire, M. E. (2008). The CorA Mg2+ Channel Is Required for the Virulence of Salmonella enterica Serovar Typhimurium. J. Bacteriol. 190: 6517-6523 [Abstract] [Full Text]  
  • Sekirov, I., Tam, N. M., Jogova, M., Robertson, M. L., Li, Y., Lupp, C., Finlay, B. B. (2008). Antibiotic-Induced Perturbations of the Intestinal Microbiota Alter Host Susceptibility to Enteric Infection. Infect. Immun. 76: 4726-4736 [Abstract] [Full Text]  
  • Bustamante, V. H., Martinez, L. C., Santana, F. J., Knodler, L. A., Steele-Mortimer, O., Puente, J. L. (2008). HilD-mediated transcriptional cross-talk between SPI-1 and SPI-2. Proc. Natl. Acad. Sci. USA 105: 14591-14596 [Abstract] [Full Text]  
  • Le Negrate, G., Faustin, B., Welsh, K., Loeffler, M., Krajewska, M., Hasegawa, P., Mukherjee, S., Orth, K., Krajewski, S., Godzik, A., Guiney, D. G., Reed, J. C. (2008). Salmonella Secreted Factor L Deubiquitinase of Salmonella typhimurium Inhibits NF-{kappa}B, Suppresses I{kappa}B{alpha} Ubiquitination and Modulates Innate Immune Responses. J. Immunol. 180: 5045-5056 [Abstract] [Full Text]  
  • Hapfelmeier, S., Muller, A. J., Stecher, B., Kaiser, P., Barthel, M., Endt, K., Eberhard, M., Robbiani, R., Jacobi, C. A., Heikenwalder, M., Kirschning, C., Jung, S., Stallmach, T., Kremer, M., Hardt, W.-D. (2008). Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent stepin {Delta}invG S. Typhimurium colitis. JEM 205: 437-450 [Abstract] [Full Text]  
  • Coburn, B., Sekirov, I., Finlay, B. B. (2007). Type III Secretion Systems and Disease. Clin. Microbiol. Rev. 20: 535-549 [Abstract] [Full Text]  
  • Raffatellu, M., Santos, R. L., Chessa, D., Wilson, R. P., Winter, S. E., Rossetti, C. A., Lawhon, S. D., Chu, H., Lau, T., Bevins, C. L., Adams, L. G., Baumler, A. J. (2007). The Capsule Encoding the viaB Locus Reduces Interleukin-17 Expression and Mucosal Innate Responses in the Bovine Intestinal Mucosa during Infection with Salmonella enterica Serotype Typhi. Infect. Immun. 75: 4342-4350 [Abstract] [Full Text]  
  • Giacomodonato, M. N., Uzzau, S., Bacciu, D., Caccuri, R., Sarnacki, S. H., Rubino, S., Cerquetti, M. C. (2007). SipA, SopA, SopB, SopD and SopE2 effector proteins of Salmonella enterica serovar Typhimurium are synthesized at late stages of infection in mice. Microbiology 153: 1221-1228 [Abstract] [Full Text]  
  • Steiner, T. S. (2007). How Flagellin and Toll-Like Receptor 5 Contribute to Enteric Infection. Infect. Immun. 75: 545-552 [Full Text]  
  • Coombes, B. K., Lowden, M. J., Bishop, J. L., Wickham, M. E., Brown, N. F., Duong, N., Osborne, S., Gal-Mor, O., Finlay, B. B. (2007). SseL Is a Salmonella-Specific Translocated Effector Integrated into the SsrB-Controlled Salmonella Pathogenicity Island 2 Type III Secretion System. Infect. Immun. 75: 574-580 [Abstract] [Full Text]  
  • Stecher, B., Paesold, G., Barthel, M., Kremer, M., Jantsch, J., Stallmach, T., Heikenwalder, M., Hardt, W.-D. (2006). Chronic Salmonella enterica Serovar Typhimurium-Induced Colitis and Cholangitis in Streptomycin-Pretreated Nramp1+/+ Mice. Infect. Immun. 74: 5047-5057 [Abstract] [Full Text]  
  • Rollenhagen, C., Bumann, D. (2006). Salmonella enterica Highly Expressed Genes Are Disease Specific. Infect. Immun. 74: 1649-1660 [Abstract] [Full Text]  
  • Raffatellu, M., Chessa, D., Wilson, R. P., Tukel, C., Akcelik, M., Baumler, A. J. (2006). Capsule-Mediated Immune Evasion: a New Hypothesis Explaining Aspects of Typhoid Fever Pathogenesis. Infect. Immun. 74: 19-27 [Full Text]  
  • Suar, M., Jantsch, J., Hapfelmeier, S., Kremer, M., Stallmach, T., Barrow, P. A., Hardt, W.-D. (2006). Virulence of Broad- and Narrow-Host-Range Salmonella enterica Serovars in the Streptomycin-Pretreated Mouse Model. Infect. Immun. 74: 632-644 [Abstract] [Full Text]  
  • Coombes, B. K., Coburn, B. A., Potter, A. A., Gomis, S., Mirakhur, K., Li, Y., Finlay, B. B. (2005). Analysis of the Contribution of Salmonella Pathogenicity Islands 1 and 2 to Enteric Disease Progression Using a Novel Bovine Ileal Loop Model and a Murine Model of Infectious Enterocolitis. Infect. Immun. 73: 7161-7169 [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»