Effects of undigested protein-rich ingredients on polarised small intestinal organoid monolayers

Soumya K Kar; Bart van der Hee; Linda M P Loonen; Nico Taverne; Johanna J Taverne-Thiele; Dirkjan Schokker; Mari A Smits; Alfons J M Jansman; Jerry M Wells

doi:10.1186/s40104-020-00443-4

Effects of undigested protein-rich ingredients on polarised small intestinal organoid monolayers

J Anim Sci Biotechnol. 2020 May 18:11:51. doi: 10.1186/s40104-020-00443-4. eCollection 2020.

Authors

Affiliations

¹ 1Host Microbe Interactomics Group, Wageningen University & Research, De Elst 1, 6708 WD Wageningen, The Netherlands.
² 2Laboratory of Microbiology, Wageningen University & Research, Stippeneng 4, 6708 WE Wageningen, The Netherlands.
³ 3Wageningen Livestock Research, Wageningen University & Research, De Elst 1, 6708 WD Wageningen, The Netherlands.

^# Contributed equally.

Abstract

Abstract: Here, we describe the use of monolayers of intestinal epithelial cells derived from intestinal organoids and transcriptomics to investigate the direct effects of dietary protein sources on epithelial function. Mechanically dissociated 3D organoids of mouse duodenum were used to generate a polarized epithelium containing all cell types found in the tissue of origin. The organoid-derived cell monolayers were exposed to 4% (w/v) of 'undigested (non-hydrolysed)-soluble' fraction of protein sources used as feed ingredients [soybean meal (SBM) and casein], or alternative protein sources (spray dried plasma protein, and yellow meal worm), or controls for 6 h prior to RNA isolation and transcriptomics. All protein sources altered expression of unique biological processes in the epithelial cells. Exposure of intestinal organoids to SBM downregulated expression of retinol and retinoid metabolic processes as well as cholesterol and lipid biosynthetic pathways, consistent with the reported hypotriglyceridaemic effect of soy protein in vivo. These findings support the use of intestinal organoids as models to evaluate complex interactions between dietary ingredients and the intestinal epithelium and highlights some unique host effects of alternative protein sources in animal feed and potentially human food.

Graphical abstract: Schematic representation of the study. 3-dimensional organoids were generated from mouse duodenum (1). The organoids were subsequently dissociated into single cells (2) and grown as 2-dimensional polarised monolayers (3). Polarized monolayers of organoid cells were exposed to different protein sources [CAS, SBM, SDPP, YMW, or medium control (MC)] for 6 h (4) and further processed for imaging (5) gene expression (6), and biochemical assays (7), to investigate the effects of undigested protein sources on the duodenal epithelium.

Keywords: Alternative protein sources; Casein; Intestinal organoids; Organoids; Soybean meal; Spray dried plasma protein; Transcriptomics; Yellow meal worm.