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Cell-type diversity and regionalized gene expression in the planarian intestine.

ABSTRACT: Proper function and repair of the digestive system are vital to most animals. Deciphering the mechanisms involved in these processes requires an atlas of gene expression and cell types. Here, we applied laser-capture microdissection (LCM) and RNA-seq to characterize the intestinal transcriptome of Schmidtea mediterranea, a planarian flatworm that can regenerate all organs, including the gut. We identified hundreds of genes with intestinal expression undetected by previous approaches. Systematic analyses revealed extensive conservation of digestive physiology and cell types with other animals, including humans. Furthermore, spatial LCM enabled us to uncover previously unappreciated regionalization of gene expression in the planarian intestine along the medio-lateral axis, especially among intestinal goblet cells. Finally, we identified two intestine-enriched transcription factors that specifically regulate regeneration (hedgehog signaling effector gli-1) or maintenance (RREB2) of goblet cells. Altogether, this work provides resources for further investigation of mechanisms involved in gastrointestinal function, repair and regeneration.

SUBMITTER: Forsthoefel DJ

PROVIDER: S-EPMC7117911 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Cell-type diversity and regionalized gene expression in the planarian intestine.

Forsthoefel David J DJ Cejda Nicholas I NI Khan Umair W UW Newmark Phillip A PA

eLife 20200402

Proper function and repair of the digestive system are vital to most animals. Deciphering the mechanisms involved in these processes requires an atlas of gene expression and cell types. Here, we applied laser-capture microdissection (LCM) and RNA-seq to characterize the intestinal transcriptome of <i>Schmidtea mediterranea</i>, a planarian flatworm that can regenerate all organs, including the gut. We identified hundreds of genes with intestinal expression undetected by previous approaches. Syst ...[more]

PMID: 32240093

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Project description:BackgroundHigh intakes of fructose are associated with metabolic diseases, including hypertriglyceridemia and intestinal tumor growth. Although small intestinal epithelia consist of many different cell types, express lipogenic genes, and convert dietary fructose to fatty acids, there is no information on the identity of the cell type(s) mediating this conversion and on the effects of fructose on lipogenic gene expression.ObjectivesWe hypothesized that fructose regulates the intestinal expression of genes involved in lipid and apolipoprotein synthesis, that regulation depends on the fructose transporter solute carrier family 2 member a5 [Slc2a5 (glucose transporter 5)] and on ketohexokinase (Khk), and that regulation occurs only in enterocytes.MethodsWe compared lipogenic gene expression among different organs from wild-type adult male C57BL mice consuming a standard vivarium nonpurified diet. We then gavaged twice daily for 2.5 d fructose or glucose solutions (15%, 0.3 mL per mouse) into wild-type, Slc2a5-knockout (KO), and Khk-KO mice with free access to the nonpurified diet and determined expression of representative lipogenic genes. Finally, from mice fed the nonpurified diet, we made organoids highly enriched in enterocyte, goblet, Paneth, or stem cells and then incubated them overnight in 10 mM fructose or glucose.ResultsMost lipogenic genes were significantly expressed in the intestine relative to the kidney, liver, lung, and skeletal muscle. In vivo expression of Srebf1, Acaca, Fasn, Scd1, Dgat1, Gk, Apoa4, and Apob mRNA and of Scd1 protein increased (P < 0.05) by 3- to 20-fold in wild-type, but not in Slc2a5-KO and Khk-KO, mice gavaged with fructose. In vitro, Slc2a5- and Khk-dependent, fructose-induced increases, which ranged from 1.5- to 4-fold (P < 0.05), in mRNA concentrations of all these genes were observed only in organoids enriched in enterocytes.ConclusionsFructose specifically stimulates expression of mouse small intestinal genes for lipid and apolipoprotein synthesis. Secretory and stem cells seem incapable of transport- and metabolism-dependent lipogenesis, occurring only in absorptive enterocytes.

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Cell-type diversity and regionalized gene expression in the planarian intestine.

Publications

Cell-type diversity and regionalized gene expression in the planarian intestine.

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