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A new model for fish ion regulation: identification of ionocytes in freshwater- and seawater-acclimated medaka (Oryzias latipes)

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Abstract

The ion regulation mechanisms of fishes have been recently studied in zebrafish (Danio rerio), a stenohaline species. However, recent advances using this organism are not necessarily applicable to euryhaline fishes. The euryhaline species medaka (Oryzias latipes), which, like zebrafish, is genetically well categorized and amenable to molecular manipulation, was proposed as an alternative model for studying osmoregulation during acclimation to different salinities. To establish its suitability as an alternative, the present study was conducted to (1) identify different types of ionocytes in the embryonic skin and (2) analyze gene expressions of the transporters during seawater acclimation. Double/triple in situ hybridization and/or immunocytochemistry revealed that freshwater (FW) medaka contain three types of ionocyte: (1) Na+/H+ exchanger 3 (NHE3) cells with apical NHE3 and basolateral Na+-K+-2Cl− cotransporter (NKCC), Na+-K+-ATPase (NKA) and anion exchanger (AE); (2) Na+-Cl− cotransporter (NCC) cells with apical NCC and basolateral H+-ATPase; and (3) epithelial Ca2+ channel (ECaC) cells [presumed accessory (AC) cells] with apical ECaC. On the other hand, seawater (SW) medaka has a single predominant ionocyte type, which possesses apical cystic fibrosis transmembrane conductance regulator (CFTR) and NHE3 and basolateral NKCC and NKA and is accompanied by smaller AC cells that express lower levels of basolateral NKA. Reciprocal gene expressions of decreased NHE3, AE, NCC and ECaC and increased CFTR and NKCC in medaka gills during SW were revealed by quantative PCR analysis.

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Acknowledgements

This study was financially supported by grants to P.P.H. from Academia Sinica and the National Science Council, Taiwan, R.O.C. We extend our thanks to Ms. Y.C. Tung for her assistance during the experiments.

Disclosures

The authors declare no conflicts of interest, financial or otherwise.

Author Contributions

Author contributions: H.-H.H., L.-Y.L., Y.-C.T. and J.-L.H. performed experiments; H.-H.H., L.-Y.L., Y.-C.T. and J.-L.H. analyzed data; H.-H.H., L.-Y.L., Y.-C.T., J.-L.H. and P.-P.H. interpreted experimental results; H.-H.H., Y.-C.T., J.-L.H. and P.-P.H. prepared figures; H.-H.H and J.-L.H. drafted the manuscript; L.-Y.L., J.-L.H. and P.-P.H. edited and revised the manuscript; J.-L.H. and P.-P.H. conceived and designed the study; P.-P.H. approved the final version of the manuscript.

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Authors and Affiliations

  1. Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, Taiwan, Republic of China

    Hao-Hsuan Hsu & Pung-Pung Hwang

  2. Department of Life Science, National Taiwan Normal University, Taipei, Taiwan, Republic of China

    Li-Yih Lin & Yung-Che Tseng

  3. Department of Anatomy, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan, Republic of China

    Jiun-Lin Horng

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  1. Hao-Hsuan Hsu
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  2. Li-Yih Lin
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  3. Yung-Che Tseng
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  4. Jiun-Lin Horng
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  5. Pung-Pung Hwang
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Correspondence to Pung-Pung Hwang.

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Pung-Pung Hwang and Jiun-Lin Horng contributed equally to this study.

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Hsu, HH., Lin, LY., Tseng, YC. et al. A new model for fish ion regulation: identification of ionocytes in freshwater- and seawater-acclimated medaka (Oryzias latipes). Cell Tissue Res 357, 225–243 (2014). https://doi.org/10.1007/s00441-014-1883-z

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