Role of SPI-1 Secreted Effectors in Acute Bovine Response to Salmonella enterica Serovar Typhimurium: A Systems Biology Analysis Approach
Abstract
Salmonella enterica Serovar Typhimurium (S. Typhimurium) causes enterocolitis with diarrhea and polymorphonuclear cell (PMN) influx into the intestinal mucosa in humans and calves. The Salmonella Type III Secretion System (T3SS) encoded at Pathogenicity Island I translocates Salmonella effector proteins SipA, SopA, SopB, SopD, and SopE2 into epithelial cells and is required for induction of diarrhea. These effector proteins act together to induce intestinal fluid secretion and transcription of C-X-C chemokines, recruiting PMNs to the infection site. While individual molecular interactions of the effectors with cultured host cells have been characterized, their combined role in intestinal fluid secretion and inflammation is less understood. We hypothesized that comparison of the bovine intestinal mucosal response to wild type Salmonella and a SipA, SopABDE2 effector mutant relative to uninfected bovine ileum would reveal heretofore unidentified diarrheaassociated host cellular pathways. To determine the coordinated effects of these virulence factors, a bovine ligated ileal loop model was used to measure responses to wild type S. Typhimurium (WT) and a ΔsipA, sopABDE2 mutant (MUT) across 12 hours of infection using a bovine microarray. Data were analyzed using standard microarray analysis and a dynamic Bayesian network modeling approach (DBN). Both analytical methods confirmed increased expression of immune responsemore »
- Authors:
-
- Texas A & M University, College Station, TX (United States)
- University of Illinois at Urbana-Champaign, IL (United States)
- University of Texas Southwestern Medical Center, Dallas, TX (United States)
- Sandia National Laboratory (SNL-NM), Albuquerque, NM (United States)
- Serologix, LLC, Austin, TX (United States)
- University of California, Davis, CA (United States)
- Publication Date:
- Research Org.:
- Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institute of Allergy and Infectious Disease; Public Health Service Grant
- OSTI Identifier:
- 1627481
- Grant/Contract Number:
- NA0003525; 1 R01 A144170-01-A1; 1 R01 AI076246 01-A2; USDA 2002-35204-12247; AI060933
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 11; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; salmonella typhimurium; gene expression; salmonellosis; gastrointestinal tract; salmonella; microarrays; wnt signaling cascade; chemokines
Citation Formats
Lawhon, Sara D., Khare, Sangeeta, Rossetti, Carlos A., Everts, Robin E., Galindo, Cristi L., Luciano, Sarah A., Figueiredo, Josely F., Nunes, Jairo E. S., Gull, Tamara, Davidson, George S., Drake, Kenneth L., Garner, Harold R., Lewin, Harris A., Bäumler, Andreas J., and Adams, Leslie Garry. Role of SPI-1 Secreted Effectors in Acute Bovine Response to Salmonella enterica Serovar Typhimurium: A Systems Biology Analysis Approach. United States: N. p., 2011.
Web. doi:10.1371/journal.pone.0026869.
Lawhon, Sara D., Khare, Sangeeta, Rossetti, Carlos A., Everts, Robin E., Galindo, Cristi L., Luciano, Sarah A., Figueiredo, Josely F., Nunes, Jairo E. S., Gull, Tamara, Davidson, George S., Drake, Kenneth L., Garner, Harold R., Lewin, Harris A., Bäumler, Andreas J., & Adams, Leslie Garry. Role of SPI-1 Secreted Effectors in Acute Bovine Response to Salmonella enterica Serovar Typhimurium: A Systems Biology Analysis Approach. United States. https://doi.org/10.1371/journal.pone.0026869
Lawhon, Sara D., Khare, Sangeeta, Rossetti, Carlos A., Everts, Robin E., Galindo, Cristi L., Luciano, Sarah A., Figueiredo, Josely F., Nunes, Jairo E. S., Gull, Tamara, Davidson, George S., Drake, Kenneth L., Garner, Harold R., Lewin, Harris A., Bäumler, Andreas J., and Adams, Leslie Garry. Fri .
"Role of SPI-1 Secreted Effectors in Acute Bovine Response to Salmonella enterica Serovar Typhimurium: A Systems Biology Analysis Approach". United States. https://doi.org/10.1371/journal.pone.0026869. https://www.osti.gov/servlets/purl/1627481.
@article{osti_1627481,
title = {Role of SPI-1 Secreted Effectors in Acute Bovine Response to Salmonella enterica Serovar Typhimurium: A Systems Biology Analysis Approach},
author = {Lawhon, Sara D. and Khare, Sangeeta and Rossetti, Carlos A. and Everts, Robin E. and Galindo, Cristi L. and Luciano, Sarah A. and Figueiredo, Josely F. and Nunes, Jairo E. S. and Gull, Tamara and Davidson, George S. and Drake, Kenneth L. and Garner, Harold R. and Lewin, Harris A. and Bäumler, Andreas J. and Adams, Leslie Garry},
abstractNote = {Salmonella enterica Serovar Typhimurium (S. Typhimurium) causes enterocolitis with diarrhea and polymorphonuclear cell (PMN) influx into the intestinal mucosa in humans and calves. The Salmonella Type III Secretion System (T3SS) encoded at Pathogenicity Island I translocates Salmonella effector proteins SipA, SopA, SopB, SopD, and SopE2 into epithelial cells and is required for induction of diarrhea. These effector proteins act together to induce intestinal fluid secretion and transcription of C-X-C chemokines, recruiting PMNs to the infection site. While individual molecular interactions of the effectors with cultured host cells have been characterized, their combined role in intestinal fluid secretion and inflammation is less understood. We hypothesized that comparison of the bovine intestinal mucosal response to wild type Salmonella and a SipA, SopABDE2 effector mutant relative to uninfected bovine ileum would reveal heretofore unidentified diarrheaassociated host cellular pathways. To determine the coordinated effects of these virulence factors, a bovine ligated ileal loop model was used to measure responses to wild type S. Typhimurium (WT) and a ΔsipA, sopABDE2 mutant (MUT) across 12 hours of infection using a bovine microarray. Data were analyzed using standard microarray analysis and a dynamic Bayesian network modeling approach (DBN). Both analytical methods confirmed increased expression of immune response genes to Salmonella infection and novel gene expression. Gene expression changes mapped to 219 molecular interaction pathways and 1620 gene ontology groups. Bayesian network modeling identified effects of infection on several interrelated signaling pathways including MAPK, Phosphatidylinositol, mTOR, Calcium, Toll-like Receptor, CCR3, Wnt, TGF-β, and Regulation of Actin Cytoskeleton and Apoptosis that were used to model of host-pathogen interactions. Comparison of WT and MUT demonstrated significantly different patterns of host response at early time points of infection (15 minutes, 30 minutes and one hour) within phosphatidylinositol, CCR3, Wnt, and TGF-β signaling pathways and the regulation of actin cytoskeleton pathway.},
doi = {10.1371/journal.pone.0026869},
journal = {PLoS ONE},
number = 11,
volume = 6,
place = {United States},
year = {Fri Nov 11 00:00:00 EST 2011},
month = {Fri Nov 11 00:00:00 EST 2011}
}
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