A porcine ligated loop model reveals new insight into the host immune response against Campylobacter jejuni
Abstract
The symptoms of infectious diarrheal disease are mediated by a combination of a pathogen’s 39 virulence factors and the host immune system. Campylobacter jejuni is the leading bacterial 40 cause of diarrhea worldwide due to its near-ubiquitous zoonotic association with poultry. One of 41 the outstanding questions is to what extent the bacteria are responsible for the diarrheal 42 symptoms via intestinal cell necrosis versus immune cell initiated tissue damage. To determine 43 the stepwise process of inflammation that leads to diarrhea, we used a piglet ligated intestinal 44 loop model to study the intestinal response to C. jejuni. Pigs were chosen due to the anatomical 45 similarity between the porcine and the human intestine. We found that the abundance of 46 neutrophil related proteins increased in the intestinal lumen during C. jejuni infection, including 47 proteins related to neutrophil migration (neutrophil elastase and MMP9), actin reorganization 48 (Arp2/3), and antimicrobial proteins (lipocalin-2, myeloperoxidase, S100A8, and S100A9). The 49 appearance of neutrophil proteins also corresponded with increases of the inflammatory 50 cytokines IL-8 and TNF-a. Compared to infection with the C. jejuni wild-type strain, infection with 51 the noninvasive C. jejuni ΔciaD mutant resulted in a blunted inflammatory response, withmore »
- Authors:
-
[1];
[2];
[3];
[2];
[2];
[1]
- Washington State Univ., Pullman, WA (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- US Dept. of Agriculture (USDA), Albany, CA (United States). Agricultural Research Service
- US Dept. of Agriculture (USDA), Pullman, WA (United States). Agricultural Research Service; Washington State Univ., Pullman, WA (United States)
- US Dept. of Agriculture (USDA), Ames, IA (United States). Agricultural Research Service
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
- Sponsoring Org.:
- National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA; Agricultural Research Service (ARS)
- OSTI Identifier:
- 1671036
- Report Number(s):
- PNNL-SA-152772
Journal ID: ISSN 1949-0976
- Grant/Contract Number:
- AC05-76RL01830; R01AI125356; R21AI124144; GM094623; 5T32AI007025; R01AI083387
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Gut Microbes
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 1949-0976
- Publisher:
- Taylor & Francis
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; disease model; innate immunity; proteomics; intestinal disease; pathogenesis
Citation Formats
Negretti, Nicholas M., Ye, Yinyin, Malavasi, Lais M., Pokharel, Swechha M., Huynh, Steven, Noh, Susan, Klima, Cassidy, Gourley, Christopher R., Ragle, Claude A., Bose, Santanu, Looft, Torey, Parker, Craig T., Clair, Geremy C. D., Adkins, Joshua N., and Konkel, Michael E. A porcine ligated loop model reveals new insight into the host immune response against Campylobacter jejuni. United States: N. p., 2020.
Web. doi:10.1080/19490976.2020.1814121.
Negretti, Nicholas M., Ye, Yinyin, Malavasi, Lais M., Pokharel, Swechha M., Huynh, Steven, Noh, Susan, Klima, Cassidy, Gourley, Christopher R., Ragle, Claude A., Bose, Santanu, Looft, Torey, Parker, Craig T., Clair, Geremy C. D., Adkins, Joshua N., & Konkel, Michael E. A porcine ligated loop model reveals new insight into the host immune response against Campylobacter jejuni. United States. https://doi.org/10.1080/19490976.2020.1814121
Negretti, Nicholas M., Ye, Yinyin, Malavasi, Lais M., Pokharel, Swechha M., Huynh, Steven, Noh, Susan, Klima, Cassidy, Gourley, Christopher R., Ragle, Claude A., Bose, Santanu, Looft, Torey, Parker, Craig T., Clair, Geremy C. D., Adkins, Joshua N., and Konkel, Michael E. Fri .
"A porcine ligated loop model reveals new insight into the host immune response against Campylobacter jejuni". United States. https://doi.org/10.1080/19490976.2020.1814121. https://www.osti.gov/servlets/purl/1671036.
@article{osti_1671036,
title = {A porcine ligated loop model reveals new insight into the host immune response against Campylobacter jejuni},
author = {Negretti, Nicholas M. and Ye, Yinyin and Malavasi, Lais M. and Pokharel, Swechha M. and Huynh, Steven and Noh, Susan and Klima, Cassidy and Gourley, Christopher R. and Ragle, Claude A. and Bose, Santanu and Looft, Torey and Parker, Craig T. and Clair, Geremy C. D. and Adkins, Joshua N. and Konkel, Michael E.},
abstractNote = {The symptoms of infectious diarrheal disease are mediated by a combination of a pathogen’s 39 virulence factors and the host immune system. Campylobacter jejuni is the leading bacterial 40 cause of diarrhea worldwide due to its near-ubiquitous zoonotic association with poultry. One of 41 the outstanding questions is to what extent the bacteria are responsible for the diarrheal 42 symptoms via intestinal cell necrosis versus immune cell initiated tissue damage. To determine 43 the stepwise process of inflammation that leads to diarrhea, we used a piglet ligated intestinal 44 loop model to study the intestinal response to C. jejuni. Pigs were chosen due to the anatomical 45 similarity between the porcine and the human intestine. We found that the abundance of 46 neutrophil related proteins increased in the intestinal lumen during C. jejuni infection, including 47 proteins related to neutrophil migration (neutrophil elastase and MMP9), actin reorganization 48 (Arp2/3), and antimicrobial proteins (lipocalin-2, myeloperoxidase, S100A8, and S100A9). The 49 appearance of neutrophil proteins also corresponded with increases of the inflammatory 50 cytokines IL-8 and TNF-a. Compared to infection with the C. jejuni wild-type strain, infection with 51 the noninvasive C. jejuni ΔciaD mutant resulted in a blunted inflammatory response, with less 52 inflammatory cytokines and neutrophil markers. Overall, these findings indicate that intestinal 53 inflammation is driven by C. jejuni virulence and that neutrophils are the predominant cell type 54 responding to C. jejuni infection. We propose that this model can be used as a platform to study 55 the early immune events during infection with intestinal pathogens.},
doi = {10.1080/19490976.2020.1814121},
journal = {Gut Microbes},
number = 1,
volume = 12,
place = {United States},
year = {Fri Sep 04 00:00:00 EDT 2020},
month = {Fri Sep 04 00:00:00 EDT 2020}
}
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Figure 1: Schematic of the ligated loop creation and representative image of tissue removed from the pig. Panels A: Schematic representation of the intestinal pig loops, beginning at the ileocecal junction at the left, and ascending into the small intestine to the right. Loops in red were inoculated with C.more », and loops in black are control loops. ‘I’ indicates an infected loop, and ‘C’ indicates a control loop. B: Representative tissue removed from the pig at 30 hours post-infection, oriented in the same direction as in Panel A. Arrows indicate the location of the double ligation between each individual intestinal loop.
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