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Regional Mucosa-Associated Microbiota Determine Physiological Expression of TLR2 and TLR4 in Murine Colon

Journal Article · · PLoS ONE
 [1];  [2];  [2];  [2];  [2];  [3];  [2];  [2]
  1. University of Chicago, IL (United States); DOE/OSTI
  2. University of Chicago, IL (United States)
  3. University of Chicago, IL (United States); Argonne National Laboratory (ANL), Argonne, IL (United States)
+ Show Author Affiliations
Many colonic mucosal genes that are highly regulated by microbial signals are differentially expressed along the rostralcaudal axis. This would suggest that differences in regional microbiota exist, particularly mucosa-associated microbes that are less likely to be transient. We therefore explored this possibility by examining the bacterial populations associated with the normal proximal and distal colonic mucosa in context of host Toll-like receptors (TLR) expression in C57BL/6J mice housed in specific pathogen-free (SPF) and germ-free (GF) environments. 16S rRNA gene-based terminal restriction fragment length polymorphism (T-RFLP) and clone library analysis revealed significant differences in the community structure and diversity of the mucosa-associated microbiota located in the distal colon compared to proximal colon and stool, the latter two clustering closely. Differential expression of colonic TLR2 and TLR4 along the proximal-distal axis was also found in SPF mice, but not in GF mice, suggesting that enteric microbes are essential in maintaining the regional expression of these TLRs. TLR2 is more highly expressed in proximal colon and decreases in a gradient to distal while TLR4 expression is highest in distal colon and a gradient of decreased expression to proximal colon is observed. After transfaunation in GF mice, both regional colonization of mucosa-associated microbes and expression of TLRs in the mouse colon were reestablished. In addition, exposure of the distal colon to cecal (proximal) microbiota induced TLR2 expression. These results demonstrate that regional colonic mucosa-associated microbiota determine the region-specific expression of TLR2 and TLR4. Conversely, region-specific host assembly rules are essential in determining the structure and function of mucosa-associated microbial populations. We believe this type of host-microbial mutualism is pivotal to the maintenance of intestinal and immune homeostasis.
Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); University of Chicago; Crohns and Colitis Foundation of America
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1627434
Journal Information:
PLoS ONE, Journal Name: PLoS ONE Journal Issue: 10 Vol. 5; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (26)

Bacterial colonization leads to the colonic secretion of RELMβ/FIZZ2, a novel goblet cell-specific protein journal November 2003
Multifaceted transcriptional regulation of the murine intestinal mucus layer by endogenous microbiota journal January 2008
16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis journal April 2009
Regulation of dextran sodium sulfate induced colitis by leukocyte beta 2 integrins journal April 2006
Innate immunity and intestinal microbiota in the development of Type 1 diabetes journal September 2008
Obesity alters gut microbial ecology journal July 2005
The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy journal January 2003
Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes journal May 2006
Gut flora, Toll-like receptors and nuclear receptors: a tripartite communication that tunes innate immunity in large intestine journal May 2008
Reversing Bacteria-induced Vitamin D Receptor Dysfunction Is Key to Autoimmune Disease journal September 2009
Commensal Host-Bacterial Relationships in the Gut journal May 2001
Host-Bacterial Mutualism in the Human Intestine journal March 2005
Diversity of the Human Intestinal Microbial Flora journal June 2005
Molecular Analysis of Commensal Host-Microbial Relationships in the Intestine journal February 2001
Mucosa-Associated Bacteria in the Human Gastrointestinal Tract Are Uniformly Distributed along the Colon and Differ from the Community Recovered from Feces journal July 2002
Aggregating Phenotype in Lactobacillus crispatus Determines Intestinal Colonization and TLR2 and TLR4 Modulation in Murine Colonic Mucosa journal September 2007
H OW H OST -M ICROBIAL I NTERACTIONS S HAPE THE N UTRIENT E NVIRONMENT OF THE M AMMALIAN I NTESTINE journal July 2002
Inflammation-induced, 3′UTR-dependent translational inhibition of Hsp70 mRNA impairs intestinal homeostasis journal May 2009
PECAM-1 (CD 31) mediates transendothelial leukocyte migration in experimental colitis journal August 2007
Luminal bacterial flora determines physiological expression of intestinal epithelial cytoprotective heat shock proteins 25 and 72 journal April 2005
Novel role of the vitamin D receptor in maintaining the integrity of the intestinal mucosal barrier journal January 2008
Differential expression, distribution, and function of PPAR-γ in the proximal and distal colon journal August 2007
Smad3 Deficiency Promotes Tumorigenesis in the Distal Colon of ApcMin/+ Mice journal September 2006
Toll-Like Receptor 2 (TLR2) Plays a Major Role in Innate Resistance in the Lung against Murine Mycoplasma journal May 2010
Enteroendocrine cells express functional Toll-like receptors text January 2007
Strategic Compartmentalization of Toll-Like Receptor 4 in the Mouse Gut journal April 2003

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  • Sharbafi, Mohammad Hossein; Assadiasl, Sara; Pour‐reza‐gholi, Fatemeh
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Taxonomic Identification of Commensal Bacteria Associated with the Mucosa and Digesta throughout the Gastrointestinal Tracts of Preweaned Calves journal March 2014
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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
bacteria
colon
epithelial cells
gene expression
gut bacteria
polymerase chain reaction
ribosomal RNA
toll-like receptors