Chicken intestinal organoids: a novel method to measure the mode of action of feed additives

Author(s)Mitchell, Jordan
Author(s)Sutton, Kate
Author(s)Elango, Jeyashree Nathan
Author(s)Borowska, Dominika
Author(s)Perry, Famatta
Author(s)Lahaye, Ludovic
Author(s)Santin, Elizabeth
Author(s)Arsenault, Ryan J.
Author(s)Vervelde, Lonneke
Date Accessioned2024-05-21T19:45:07Z
Date Available2024-05-21T19:45:07Z
Publication Date2024-05-20
DescriptionThis article was originally published in Frontiers in Immunology. The version of record is available at: https://doi.org/10.3389/fimmu.2024.1368545. © 2024 Mitchell, Sutton, Elango, Borowska, Perry, Lahaye, Santin, Arsenault and Vervelde. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
AbstractThere is a rapidly growing interest in how the avian intestine is affected by dietary components and feed additives. The paucity of physiologically relevant models has limited research in this field of poultry gut health and led to an over-reliance on the use of live birds for experiments. The development of complex 3D intestinal organoids or “mini-guts” has created ample opportunities for poultry research in this field. A major advantage of the floating chicken intestinal organoids is the combination of a complex cell system with an easily accessible apical-out orientation grown in a simple culture medium without an extracellular matrix. The objective was to investigate the impact of a commercial proprietary blend of organic acids and essential oils (OA+EO) on the innate immune responses and kinome of chicken intestinal organoids in a Salmonella challenge model. To mimic the in vivo prolonged exposure of the intestine to the product, the intestinal organoids were treated for 2 days with 0.5 or 0.25 mg/mL OA+EO and either uninfected or infected with Salmonella and bacterial load in the organoids was quantified at 3 hours post infection. The bacteria were also treated with OA+EO for 1 day prior to challenge of the organoids to mimic intestinal exposure. The treatment of the organoids with OA+EO resulted in a significant decrease in the bacterial load compared to untreated infected organoids. The expression of 88 innate immune genes was investigated using a high throughput qPCR array, measuring the expression of 88 innate immune genes. Salmonella invasion of the untreated intestinal organoids resulted in a significant increase in the expression of inflammatory cytokine and chemokines as well as genes involved in intracellular signaling. In contrast, when the organoids were treated with OA+EO and challenged with Salmonella, the inflammatory responses were significantly downregulated. The kinome array data suggested decreased phosphorylation elicited by the OA+EO with Salmonella in agreement with the gene expression data sets. This study demonstrates that the in vitro chicken intestinal organoids are a new tool to measure the effect of the feed additives in a bacterial challenge model by measuring innate immune and protein kinases responses.
SponsorThe author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by Jefo Nutrition Inc., the Biotechnology and Biological Sciences Research Council Institute Strategic Program Grant funding (BBS/E/D/10002073 and BBS/E/D/20002174), and University of Delaware internal support funds.
CitationMitchell J, Sutton K, Elango JN, Borowska D, Perry F, Lahaye L, Santin E, Arsenault RJ and Vervelde L (2024) Chicken intestinal organoids: a novel method to measure the mode of action of feed additives. Front. Immunol. 15:1368545. doi: 10.3389/fimmu.2024.1368545
ISSN1664-3224
URLhttps://udspace.udel.edu/handle/19716/34423
Languageen_US
PublisherFrontiers in Immunology
dc.rightsAttribution 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/
Keywordsorganoid
Keywordschicken
Keywordsfeed additives
Keywordsin vitro
Keywordsinnate immunity
Keywordsimmunometabolomics
KeywordsSalmonella
TitleChicken intestinal organoids: a novel method to measure the mode of action of feed additives
TypeArticle
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