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Multi-regional expression of pancreas-related digestive enzyme genes in the intestinal chamber of the ascidian Ciona intestinalis type A

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Abstract

Bilateria share sequential steps in their digestive systems, and digestion occurs in a pre-absorption step within a chamber-like structure. Previous studies on the ascidian Ciona intestinalis type A, an evolutionary research model of vertebrate organs, revealed that Ciona homologs of pancreas-related exocrine digestive enzymes (XDEs) are exclusively expressed in the chamber-like bulging stomach. In the development of the gastrointestinal tract, genes for the pancreas-related transcription factors, namely Ptf1a, Nr5a2, and Pdx, are expressed near the stomach. Recent organ/tissue RNA-seq studies on two Ciona species reported that transcripts of the XDE homologs exist in the intestinal regions, as well as in the stomach. In the present study, we investigated the spatial gene expression of XDE homologs in the gastrointestinal region of the C. intestinalis type A. Whole-mount in situ hybridization using adult and juvenile specimens revealed apparent expression signals of XDE homologs in a small number of gastrointestinal epithelial cells. Furthermore, two pancreas-related transcription factor genes, Nr5a2 and Pdx, exhibited multi-regional expression along the Ciona juvenile intestines. These results imply that ascidians may form multiple digestive regions corresponding to the vertebrate pancreas.

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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 Miss Kanon Kojo 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 K.U. performed ISH and histochemical analyses. S.N. and Y.S. performed gene expression assays using GFP. 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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The authors declare no competing interests.

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Iguchi, R., Usui, K., Nakayama, S. et al. Multi-regional expression of pancreas-related digestive enzyme genes in the intestinal chamber of the ascidian Ciona intestinalis type A. Cell Tissue Res 394, 423–430 (2023). https://doi.org/10.1007/s00441-023-03839-6

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  • DOI: https://doi.org/10.1007/s00441-023-03839-6

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