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Paracrine and endocrine pathways of natriuretic peptides assessed by ligand-receptor map** in the Japanese eel brain

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Abstract

The natriuretic peptide (NP) family consists of cardiac NPs (ANP, BNP, and VNP) and brain NPs (CNPs) in teleosts. In addition to CNP1-4, a paralogue of CNP4 (named CNP4b) was recently discovered in basal teleosts including Japanese eel. Mammals have lost most Cnps during the evolution, but teleost cnps were conserved and diversified, suggesting that CNPs are important hormones for maintaining brain functions in teleost. The present study evaluated the potency of each Japanese eel CNP to their NP receptors (NPR-A, NPR-B, NPR-C, and NPR-D) overexpressed in CHO cells. A comprehensive brain map of cnps- and nprs-expressing neurons in Japanese eel was constructed by integrating the localization results obtained by in situ hybridization. The result showed that CHO cells expressing NPR-A and NPR-B induced strong cGMP productions after stimulation by cardiac and brain NPs, respectively. Regarding brain distribution of cnps, cnp1 is engaged in the ventral telencephalic area and periventricular area including the parvocellular preoptic nucleus (Pp), anterior/posterior tuberal nuclei, and periventricular gray zone of the optic tectum. cnp3 is found in the habenular nucleus and prolactin cells in the pituitary. cnp4 is expressed in the ventral telencephalic area, while cnp4b is expressed in the motoneurons in the medullary area. Such CNP isoform-specific localizations suggest that function of each CNP has diverged in the eel brain. Furthermore, the Pp lacking the blood-brain barrier expressed both npra and nprb, suggesting that endocrine and paracrine NPs interplay for regulating the Pp functions in Japanese eels.

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Acknowledgements

We thank Dr. Christopher A. Loretz of the State University of New York at Buffalo for critical reading of the manuscript and Dr. Naoyuki Yamamoto of Nagoya University for valuable advice on the fish brain anatomy.

Funding

This work was supported in part by JSPS KAKENHI Grants (nos. 20K06242 to TT, 20K15604 to YK, and 22K06291 to MW) and the Toyo Suisan Foundation.

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Authors and Affiliations

  1. Department of Biomolecular Science, Toho University, 2-2-1 Miyama, Funabashi, Chiba, 274-8510, Japan

    Tomoki Izumi, Ami Saito, Yukitoshi Katayama, Marty Kwok-Shing Wong & Takehiro Tsukada

  2. Department of Bioactive Peptides, Frontier Science Research Center, University of Miyazaki, 5200, Kihara, Kiyotake, Miyazaki, Miyazaki, 889-1692, Japan

    Takanori Ida

  3. Department of Anatomy, Faculty of Medicine, Tottori University, 86 Nishicho, Yonago, Tottori, 683-8503, Japan

    Takao Mukuda

  4. Center for Earth Surface System Dynamics, Atmosphere and Ocean Research Institute, the University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8564, Japan

    Marty Kwok-Shing Wong

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  1. Tomoki Izumi
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Correspondence to Takehiro Tsukada.

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Izumi, T., Saito, A., Ida, T. et al. Paracrine and endocrine pathways of natriuretic peptides assessed by ligand-receptor map** in the Japanese eel brain. Cell Tissue Res 396, 197–212 (2024). https://doi.org/10.1007/s00441-024-03873-y

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