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Microbial colonization induces dynamic temporal and spatial patterns of NF-?B activation in the zebrafish digestive tract.

ABSTRACT: The nuclear factor ?-light-chain enhancer of activated B cells (NF-?B) transcription factor pathway is activated in response to diverse microbial stimuli to regulate expression of genes involved in immune responses and tissue homeostasis. However, the temporal and spatial activation of NF-?B in response to microbial signals have not been determined in whole living organisms, and the molecular and cellular details of these responses are not well understood. We used in vivo imaging and molecular approaches to analyze NF-?B activation in response to the commensal microbiota in transparent gnotobiotic zebrafish.We used DNA microarrays, in situ hybridization, and quantitative reverse transcription polymerase chain reaction analyses to study the effects of the commensal microbiota on gene expression in gnotobiotic zebrafish. Zebrafish PAC2 and ZFL cells were used to study the NF-?B signaling pathway in response to bacterial stimuli. We generated transgenic zebrafish that express enhanced green fluorescent protein under transcriptional control of NF-?B, and used them to study patterns of NF-?B activation during development and microbial colonization.Bacterial stimulation induced canonical activation of the NF-?B pathway in zebrafish cells. Colonization of germ-free transgenic zebrafish with a commensal microbiota activated NF-?B and led to up-regulation of its target genes in intestinal and extraintestinal tissues of the digestive tract. Colonization with the bacterium Pseudomonas aeruginosa was sufficient to activate NF-?B, and this activation required a functional flagellar apparatus.In zebrafish, transcriptional activity of NF-?B is spatially and temporally regulated by specific microbial factors. The observed patterns of NF-?B-dependent responses to microbial colonization indicate that cells in the gastrointestinal tract respond robustly to the microbial environment.

SUBMITTER: Kanther M

PROVIDER: S-EPMC3164861 | biostudies-literature | 2011 Jul

REPOSITORIES: biostudies-literature

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Microbial colonization induces dynamic temporal and spatial patterns of NF-κB activation in the zebrafish digestive tract.

Kanther Michelle M Sun Xiaolun X Mühlbauer Marcus M Mackey Lantz C LC Flynn Edward J EJ Bagnat Michel M Jobin Christian C Rawls John F JF

Gastroenterology 20110324 1

<h4>Background & aims</h4>The nuclear factor κ-light-chain enhancer of activated B cells (NF-κB) transcription factor pathway is activated in response to diverse microbial stimuli to regulate expression of genes involved in immune responses and tissue homeostasis. However, the temporal and spatial activation of NF-κB in response to microbial signals have not been determined in whole living organisms, and the molecular and cellular details of these responses are not well understood. We used in vi ...[more]

PMID: 21439961

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Project description:Diversity and composition of microbial communities was compared across the 13 major sections of the digestive tract (esophagus, reticulum, rumen, omasum, abomasum, duodenum, jejunum, ileum, cecum, ascending colon, transverse colon, descending colon, and rectum) in two captive populations of American bison (Bison bison), one of which was finished on forage, the other on grain.Microbial diversity fell to its lowest levels in the small intestine, with Bacteroidetes reaching their lowest relative abundance in that region, while Firmicutes and Euryarchaeota attained their highest relative abundances there. Gammaproteobacteria were most abundant in the esophagus, small intestine, and colon. The forage-finished bison population exhibited higher overall levels of diversity, as well as a higher relative abundance of Bacteroidetes in most gut sections. The grain-finished bison population exhibited elevated levels of Firmicutes and Gammaproteobacteria. Within each population, different sections of the digestive tract exhibited divergent microbial community composition, although it was essentially the same among sections within a given region of the digestive tract. Shannon diversity was lowest in the midgut. For each section of the digestive tract, the two bison populations differed significantly in microbial community composition.Similarities among sections indicate that the esophagus, reticulum, rumen, omasum, and abomasum may all be considered to house the foregut microbiota; the duodenum, jejunum, and ileum may all be considered to house the small intestine or midgut microbiota; and the cecum, ascending colon, transverse colon, descending colon, and rectum may all be considered to house the hindgut microbiota. Acid from the stomach, bile from the gall bladder, digestive enzymes from the pancreas, and the relatively low retention time of the small intestine may have caused the midgut's low microbial diversity. Differences in microbial community composition between populations may have been most strongly influenced by differences in diet (forage or grain). The clinical condition of the animals used in the present study was not evaluated, so further research is needed to establish whether the microbial profiles of some bison in this study are indeed indicative of dysbiosis, a predisposing factor to ruminal acidosis and its sequelae.

Dataset Information

Microbial colonization induces dynamic temporal and spatial patterns of NF-?B activation in the zebrafish digestive tract.

Publications

Microbial colonization induces dynamic temporal and spatial patterns of NF-κB activation in the zebrafish digestive tract.

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