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Transport of maternal transthyretin to the fetus in the viviparous teleost Neoditrema ransonnetii (Perciformes, Embiotocidae)

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Abstract

The molecular basis of viviparity in non-mammalian species has not been widely studied. Neoditrema ransonnetii, a surfperch, is a matrotrophic teleost whose fetuses grow by ovarian cavity fluid (OCF) ingestion and by nutrient absorption via their enlarged hindgut. We performed a proteomics analysis of N. ransonnetii plasma protein and found proteins specific to pregnant females; one of these was identified as transthyretin (TTR), a thyroid hormone distributor protein. We synthesized recombinant protein rNrTTR and raised an antibody, anti-rNrTTR, against it. Semi-quantitative analysis by western blotting using the antibody demonstrated that plasma TTR levels were significantly greater in pregnant fish than in non-pregnant fish. OCF and fetal plasma also contained high TTR levels. Immunohistochemical staining showed that large amounts of maternal TTR were taken up by fetal intestinal epithelial cells. These results indicate that maternal TTR is secreted into OCF and taken up by fetal enterocytes, presumably to deliver thyroid hormones to developing fetuses.

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Authors and Affiliations

  1. School of Marine Biosciences, Kitasato University, 1-15-1, Kitasato, Minami-ku, Sagamihara, Kanagawa, 252-0373, Japan

    Osamu Nakamura, Rintaro Suzuki, Kotaro Asai, Harunobu Kaji, Takuya Kaneko, Yo Takahashi, Ayaka Takahagi & Shigeyuki Tsutsui

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  1. Osamu Nakamura
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  2. Rintaro Suzuki
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  3. Kotaro Asai
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  4. Harunobu Kaji
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  5. Takuya Kaneko
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  6. Yo Takahashi
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  7. Ayaka Takahagi
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  8. Shigeyuki Tsutsui
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by RS, KA, HK, TK, YT, and AT. The first draft of the manuscript was written by ON and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Osamu Nakamura.

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Communicated by B. Pelster.

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Supplementary file1. Fig. A1. cDNA sequences of NrTTR and its predicted amino acid sequence (DOCX 26 kb)

360_2020_1261_MOESM2_ESM.tif

Supplementary file2. Fig. A2. Preparation of rTTR. Insoluble fraction of the transformed bacteria was solubilized with urea-containing buffer and subjected to affinity chromatography with Ni-Sepharose column. SDS-PAGE gel stained with CBB. Lane M: marker; Lane 1: insoluble fraction; Lane 2–9: eluted fractions (TIF 2209 kb)

360_2020_1261_MOESM3_ESM.tif

Supplementary file3. Fig. A3. Western blotting with anti-rNrTTR. Pregnant fetal plasma (diluted 1:100) was electrophoresed. M marker (TIF 411 kb)

Supplementary file4 (DOCX 12 kb)

Supplementary file5 (DOCX 15 kb)

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Nakamura, O., Suzuki, R., Asai, K. et al. Transport of maternal transthyretin to the fetus in the viviparous teleost Neoditrema ransonnetii (Perciformes, Embiotocidae). J Comp Physiol B 190, 231–241 (2020). https://doi.org/10.1007/s00360-020-01261-w

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  • DOI: https://doi.org/10.1007/s00360-020-01261-w

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