Enteric infection coupled with chronic Notch pathway inhibition alters colonic mucus composition leading to dysbiosis, barrier disruption and colitis
Abstract
Intestinal mucus layer disruption and gut microflora modification in conjunction with tight junction (TJ) changes can increase colonic permeability that allows bacterial dissemination and intestinal and systemic disease. In a previous study, we showed that Citrobacter rodentium (CR)-induced colonic crypt hyperplasia and/or colitis is regulated by a functional cross-talk between the Notch and Wnt/β-catenin pathways. In the current study, mucus analysis in the colons of CR-infected (108 CFUs) and Notch blocker Dibenzazepine (DBZ, i.p.; 10μmol/Kg b.w.)-treated mice revealed significant alterations in the composition of trace O-glycans and complex type and hybrid N-glycans, compared to CR-infected mice alone that preceded/ accompanied alterations in 16S rDNA microbial community structure and elevated EUB338 staining. While mucin-degrading bacterium, Akkermansia muciniphila (A. muciniphila) along with Enterobacteriaceae belonging to Proteobacteria phyla increased in the feces, antimi- crobial peptides Angiogenin-4, Intelectin-1 and Intelectin-2, and ISC marker Dclk1, exhibited dramatic decreases in the colons of CR-infected/DBZ-treated mice. Also evident was a loss of TJ and adherens junction protein immuno-staining within the colonic crypts that negatively impacted paracellular barrier. These changes coincided with the loss of Notch signaling and exacerbation of mucosal injury. In response to a cocktail of antibiotics (Metro- nidazole/ciprofloxacin) for 10 days, there was increased survivalmore »
- Authors:
-
[1];
- Univ. of Kansas Medical Center, Kansas City, KS (United States). Dept. of Surgery
- Univ. of Kansas, Lawrence, KS (United States). Dept. of Molecular Biosciences
- Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Division
- Univ. of Oklahoma Health Sciences Center, Oklahoma City, OK (United States). Oklahoma Medical Research Foundation
- Children's Mercy Hospital, Kansas City, MO (United States). Division of Neonatology
- Cincinnati Children's Hospital Medical Center, Cincinnati, OH (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- University of Kansas Medical Center, Kansas City, KS (United States); National Institutes of Health (NIH)
- OSTI Identifier:
- 1569278
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 13; Journal Issue: 11; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 70 PLASMA PHYSICS AND FUSION TECHNOLOGY
Citation Formats
Ahmed, Ishfaq, Roy, Badal C., Raach, Rita-Marie T., Owens, Sarah M., Xia, Lijun, Anant, Shrikant, Sampath, Venkatesh, Umar, Shahid, and Han, Xiaonan. Enteric infection coupled with chronic Notch pathway inhibition alters colonic mucus composition leading to dysbiosis, barrier disruption and colitis. United States: N. p., 2018.
Web. doi:10.1371/journal.pone.0206701.
Ahmed, Ishfaq, Roy, Badal C., Raach, Rita-Marie T., Owens, Sarah M., Xia, Lijun, Anant, Shrikant, Sampath, Venkatesh, Umar, Shahid, & Han, Xiaonan. Enteric infection coupled with chronic Notch pathway inhibition alters colonic mucus composition leading to dysbiosis, barrier disruption and colitis. United States. https://doi.org/10.1371/journal.pone.0206701
Ahmed, Ishfaq, Roy, Badal C., Raach, Rita-Marie T., Owens, Sarah M., Xia, Lijun, Anant, Shrikant, Sampath, Venkatesh, Umar, Shahid, and Han, Xiaonan. Thu .
"Enteric infection coupled with chronic Notch pathway inhibition alters colonic mucus composition leading to dysbiosis, barrier disruption and colitis". United States. https://doi.org/10.1371/journal.pone.0206701. https://www.osti.gov/servlets/purl/1569278.
@article{osti_1569278,
title = {Enteric infection coupled with chronic Notch pathway inhibition alters colonic mucus composition leading to dysbiosis, barrier disruption and colitis},
author = {Ahmed, Ishfaq and Roy, Badal C. and Raach, Rita-Marie T. and Owens, Sarah M. and Xia, Lijun and Anant, Shrikant and Sampath, Venkatesh and Umar, Shahid and Han, Xiaonan},
abstractNote = {Intestinal mucus layer disruption and gut microflora modification in conjunction with tight junction (TJ) changes can increase colonic permeability that allows bacterial dissemination and intestinal and systemic disease. In a previous study, we showed that Citrobacter rodentium (CR)-induced colonic crypt hyperplasia and/or colitis is regulated by a functional cross-talk between the Notch and Wnt/β-catenin pathways. In the current study, mucus analysis in the colons of CR-infected (108 CFUs) and Notch blocker Dibenzazepine (DBZ, i.p.; 10μmol/Kg b.w.)-treated mice revealed significant alterations in the composition of trace O-glycans and complex type and hybrid N-glycans, compared to CR-infected mice alone that preceded/ accompanied alterations in 16S rDNA microbial community structure and elevated EUB338 staining. While mucin-degrading bacterium, Akkermansia muciniphila (A. muciniphila) along with Enterobacteriaceae belonging to Proteobacteria phyla increased in the feces, antimi- crobial peptides Angiogenin-4, Intelectin-1 and Intelectin-2, and ISC marker Dclk1, exhibited dramatic decreases in the colons of CR-infected/DBZ-treated mice. Also evident was a loss of TJ and adherens junction protein immuno-staining within the colonic crypts that negatively impacted paracellular barrier. These changes coincided with the loss of Notch signaling and exacerbation of mucosal injury. In response to a cocktail of antibiotics (Metro- nidazole/ciprofloxacin) for 10 days, there was increased survival that coincided with: i) decreased levels of Proteobacteria, ii) elevated Dclk1 levels in the crypt and, iii) reduced paracellular permeability. Thus, enteric infections that interfere with Notch activity may pro- mote mucosal dysbiosis that is preceded by changes in mucus composition. Controlled use of antibiotics seems to alleviate gut dysbiosis but may be insufficient to promote colonic crypt regeneration.},
doi = {10.1371/journal.pone.0206701},
journal = {PLoS ONE},
number = 11,
volume = 13,
place = {United States},
year = {Thu Nov 01 00:00:00 EDT 2018},
month = {Thu Nov 01 00:00:00 EDT 2018}
}
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Figures / Tables:
Fig 1: Analysis of colon mucus samples for N-type glycosylation. A. FTMS m/z 800–1800 of mucus samples. Processing of mucus samples from uninfected (Normal), CR-infected (CR) and CR+DBZ-treated (CR+DBZ) mouse colons included removal of lipids and precipitation of proteins into a protein-rich powder that was subsequently treated with trypsin, purified,more »
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