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Repetitive and zonal expression profiles of absorption-related genes in the gastrointestinal tract of ascidian Ciona intestinalis type A

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Abstract

Intestinal absorption is essential for heterotrophic bilaterians with a tubular gut. Although the fundamental features of the digestive system were shared among chordates with evolution, the gut morphologies of vertebrates diverged and adapted to different food habitats. The ascidian Ciona intestinalis type A, a genome-wide research model of basal chordates, is used to examine the functional morphology of the intestines because of its transparent juvenile body. In the present study, the characteristic gene expression patterns (GEP) of Ciona absorptive proteins, e.g., brush border membrane enzymes for terminal digestion (lactase, maltase, APA, and APN) and transporters (SGLT1, GLUT5, PEPT1, and B0AT1), were investigated in juveniles and young adults, with a special reference to the absorption of other nutrients by pinocytosis- and phagocytosis-related proteins (megalin, cubilin, amnionless, Dab2, Rab7, LAMP, cathepsins, and MRC1). Whole-mount in situ hybridization revealed that these GEP showed multi-regional and repetitive features along the Ciona gastrointestinal tract, mainly in the stomach and several regions of the intestines. In young adults, many absorption-related genes, including pinocytosis-/phagocytosis-related genes, were also expressed between the stomach and mid-intestine. In the gastrointestinal epithelium, absorption-related genes showed zonal GEP along the epithelial structure. Comparisons of GEP, including other intestinal functions, such as nutrient digestion and intestinal protection, indicated the repetitive assignment of a well-coordinated set of intestinal GEP in the Ciona gastrointestinal tract.

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Acknowledgements

We thank Dr. Nori Satoh and Dr. Yutaka Satou for providing the Ciona cDNA clones. We are grateful to Manabu Yoshida, Yutaka Satou, all members of the Laboratory of Developmental Genomics, Department of Zoology of Kyoto University; the Misaki Marine Biological Station of the University of Tokyo; the Maizuru Fishery Research Station of Kyoto University; and the National BioResource Project (NBRP) for the cultivation and provision of Ciona adults and experimental materials. We thank Mr. Minoru Hayashibe, Kanae Usui, Masayuki Yamagishi, and the laboratory members of our group for their assistance with ISH analyses and laboratory cultures of Ciona juveniles.

Funding

This work was supported by a Grant-in-Aid for Scientific Research (KAKENHI) from JSPS and MEXT Japan to M.O. (Grant Number 20K07221), Y.S. (Grant Number 19H03262), and S.N. (Grant Number JP17J06306). This work was partly supported by the cooperative research program of the Institute of Nature and Environmental Technology, Kanazawa University, Acceptance No. 18040 and 19048 to S.N. and T.S.

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M.O., Y.S., and T.S. designed the experiments. R.I. and S.N. performed ISH and histochemical analyses. M.O. and all coauthors wrote the manuscript.

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Correspondence to Michio Ogasawara.

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This article does not contain any studies with human participants performed by any of the authors. Animals were maintained and used in accordance with the regulations on animal experimentation at the University of Tsukuba and Chiba University.

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Iguchi, R., Nakayama, S., Sasakura, Y. et al. Repetitive and zonal expression profiles of absorption-related genes in the gastrointestinal tract of ascidian Ciona intestinalis type A. Cell Tissue Res 394, 343–360 (2023). https://doi.org/10.1007/s00441-023-03828-9

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  • DOI: https://doi.org/10.1007/s00441-023-03828-9

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