Oxazolone-Induced Enterocolitis in Zebrafish Depends on the Composition of the Intestinal Microbiota

Brugman, Sylvia; Liu, Kit–Yeng; Lindenbergh-Kortleve, Dicky J.; Samsom, Janneke N.; Furuta, Glenn T.; Renshaw, Stephen A.; Willemsen, Rob; Nieuwenhuis, Edward E.S.

doi:10.1053/j.gastro.2009.07.069

Cited by 119 publications

(147 citation statements)

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“…However, the mortality observed in the TNBS-treated zebrafish in the present study was slightly lower than previously reported by Geiger et al [10], studying a comparable zebrafish model. Brugman et al [6] did not note reduced survival rates in adult zebrafish exposed to a low concentration (0.2%) oxazolone which is lower that the concentration (0.6%) used in this study.…”

Section: Discussionmentioning

confidence: 79%

“…Depletion of these mucus-containing cells and has been reported in intestines of patients with ulcerative colitis and in oxazolone-exposed rodent models; in contrast, Crohn's disease patients and the associated animal models usually exhibit a differentiation of the goblet cell population [13] [21] [32]. A distinct emptying of goblet cells in intestines of oxazolone-exposed adult zebrafish has been reported [6] whereas both an increase in goblet cell density [7] [11] and an unaffected goblet cell population [9] [10] have been observed in models using TNBS and larval/adult zebrafish. Goblet cells in fish have been shown to release mucins as a response to environmental factors, such as formalin [34] and ectoparasites [35], but the effect on skin goblet cells in the present study may be mediated by systemic factors such as cytokines produced in intestinal cells.…”

Section: Discussionmentioning

confidence: 99%

“…The zebrafish (Danio rerio) is an emerging animal model in the field of human disease studies due to its many advantageous traits [5]. The majority of immune molecules relevant to IBD pathogenesis are also found in zebrafish and several colitis-studies have been performed using adult and larval zebrafish [6]- [12]. From these studies it is known that an inflammatory state relevant to the human condition can be engineered in zebrafish, but the role of underlying activators-e.g.…”

Section: Introductionmentioning

confidence: 99%

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Comparison of Two Chemically-Induced Colitis-Models in Adult Zebrafish, Using Optical Projection Tomography and Novel Transcriptional Markers

Haarder¹,

Kania²,

Holm³

et al. 2016

OJI

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Crohn's disease and ulcerative colitis-inflammatory bowel diseases (IBD)-are chronic conditions with an inadequately understood pathogenesis. Employing a set of novel molecular markers in a gene expression assay (qPCR), we have used adult zebrafish to investigate two acute inflammatory models, induced by the haptenizing agents oxazolone and TNBS. In addition, goblet cell dynamics in the scales and intestine and 5-HT (serotonin) in intestinal tissues were investigated through optical projection tomography. Gene expression studies revealed a distinct and significant upregulation of proinflammatory cytokines, acute-phase reactants and metalloprotease 9 in both chemical models, primarily after 72 hours. In comparison, transcription factors and cytokines associated with Th1 and Th17 (Crohn's) and Th2 (ulcerative colitis) were mainly not affected in this acute setting. However, elevated transcript levels were detected in Foxp3, IL-10 and T-bet, which are linked with tolerance and Tregs in mammals. Goblet cells in scales were depleted in both chemical models and in the intestine of oxazolone-treated fish. A marked 5-HT signal was noted in intestinal tissue of some chemically treated zebrafish. In conclusion, a distinct acute inflammatory reaction was induced in both chemical models. Further, oxazolone and TNBS did not result in clear-cut Th2 and Th1/Th17 pathway signaling at this early timepoint, but the applied molecular tools may provide further insight to the IBD pathogenesis and translational value of the IBD zebrafish model. How to cite this paper:

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Section: Discussionmentioning

confidence: 79%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Comparison of Two Chemically-Induced Colitis-Models in Adult Zebrafish, Using Optical Projection Tomography and Novel Transcriptional Markers

Haarder¹,

Kania²,

Holm³

et al. 2016

OJI

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“…Inflammatory bowel disease can be modeled in zebrafish using a chemical called oxazolone, which induces intestinal inflammation (Brugman et al 2009). By treating zebrafish with the antibiotic vancomycin, Fusobacteria became the dominant phyla in the gut microbiota, and the inflammatory response observed in response to oxazolone was markedly decreased.…”

Section: Zebrafishmentioning

confidence: 99%

Exploring host–microbiota interactions in animal models and humans

2013

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The animal and bacterial kingdoms have coevolved and coadapted in response to environmental selective pressures over hundreds of millions of years. The meta'omics revolution in both sequencing and its analytic pipelines is fostering an explosion of interest in how the gut microbiome impacts physiology and propensity to disease. Gut microbiome studies are inherently interdisciplinary, drawing on approaches and technical skill sets from the biomedical sciences, ecology, and computational biology. Central to unraveling the complex biology of environment, genetics, and microbiome interaction in human health and disease is a deeper understanding of the symbiosis between animals and bacteria. Experimental model systems, including mice, fish, insects, and the Hawaiian bobtail squid, continue to provide critical insight into how host-microbiota homeostasis is constructed and maintained. Here we consider how model systems are influencing current understanding of host-microbiota interactions and explore recent human microbiome studies.The distinctive body plans of animals offer many niches for members of the archaeal and bacterial kingdoms. While the lumen of the human distal gut is one of the most densely populated ecosystems on our planet, humans and other animals harbor several microbiomes on and within their body surfaces such as the respiratory and urogenital tracts and the skin. As the gut has evolved from the relatively simple tube of the ancient cyclostomatida to the more highly compartmentalized gastrointestinal tracts of mammalian species, the diversity and complexity of the microbial inhabitants of those spaces has increased as well (Fig.

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“…We have developed gnotobiotic husbandry methods for the zebrafish, and used them to reveal host responses to the gut microbiota including effects on innate immunity, nutrient metabolism, and intestinal epithelial differentiation and renewal (Rawls et al, 2004(Rawls et al, , 2006Bates et al, 2006Bates et al, , 2007Cheesman and Guillemin, 2007;Cheesman et al, 2011;Kanther and Rawls, 2010). Preliminary insights into the membership of the zebrafish gut microbiota have been provided by sequencing libraries of bacterial 16S rRNA genes amplified from pooled intestinal samples from zebrafish reared in laboratory aquaculture facilities (Rawls et al, 2004(Rawls et al, , 2006Bates et al, 2006;Brugman et al, 2009). These results indicate that the zebrafish gut microbiota is numerically dominated at all stages of the zebrafish life cycle by members of the bacterial phylum Proteobacteria, with the phyla Firmicutes and Fusobacteria also prevalent during larval and adult stages respectively.…”

Section: Introductionmentioning

confidence: 99%

Evidence for a core gut microbiota in the zebrafish

et al. 2011

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Experimental analysis of gut microbial communities and their interactions with vertebrate hosts is conducted predominantly in domesticated animals that have been maintained in laboratory facilities for many generations. These animal models are useful for studying coevolved relationships between host and microbiota only if the microbial communities that occur in animals in lab facilities are representative of those that occur in nature. We performed 16S rRNA gene sequence-based comparisons of gut bacterial communities in zebrafish collected recently from their natural habitat and those reared for generations in lab facilities in different geographic locations. Patterns of gut microbiota structure in domesticated zebrafish varied across different lab facilities in correlation with historical connections between those facilities. However, gut microbiota membership in domesticated and recently caught zebrafish was strikingly similar, with a shared core gut microbiota. The zebrafish intestinal habitat therefore selects for specific bacterial taxa despite radical differences in host provenance and domestication status.

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Oxazolone-Induced Enterocolitis in Zebrafish Depends on the Composition of the Intestinal Microbiota

Cited by 119 publications

References 52 publications

Comparison of Two Chemically-Induced Colitis-Models in Adult Zebrafish, Using Optical Projection Tomography and Novel Transcriptional Markers

Comparison of Two Chemically-Induced Colitis-Models in Adult Zebrafish, Using Optical Projection Tomography and Novel Transcriptional Markers

Exploring host–microbiota interactions in animal models and humans

Evidence for a core gut microbiota in the zebrafish

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