Cubam receptor-mediated endocytosis in hindgut-derived pseudoplacenta of a viviparous teleost (Xenotoca eiseni).


Journal

The Journal of experimental biology
ISSN: 1477-9145
Titre abrégé: J Exp Biol
Pays: England
ID NLM: 0243705

Informations de publication

Date de publication:
01 07 2021
Historique:
received: 22 03 2021
accepted: 01 06 2021
pubmed: 26 6 2021
medline: 30 7 2021
entrez: 25 6 2021
Statut: ppublish

Résumé

Nutrient transfer from mother to embryo is essential for reproduction in viviparous animals. In the viviparous teleost Xenotoca eiseni (family Goodeidae), the intraovarian embryo intakes the maternal component secreted into the ovarian fluid via the trophotaenia. Our previous study reported that the epithelial layer cells of the trophotaenia incorporate a maternal protein via vesicle trafficking. However, the molecules responsible for the absorption were still elusive. Here, we focused on Cubam (Cubilin-Amnionless) as a receptor involved in the absorption, and cathepsin L as a functional protease in the vesicles. Our results indicated that the Cubam receptor is distributed in the apical surface of the trophotaenia epithelium and then is taken into the intracellular vesicles. The trophotaenia possesses acidic organelles in epithelial layer cells and cathepsin L-dependent proteolysis activity. This evidence does not conflict with our hypothesis that receptor-mediated endocytosis and proteolysis play roles in maternal macromolecule absorption via the trophotaenia in viviparous teleosts. Such nutrient absorption involving endocytosis is not a specific trait in viviparous fish. Similar processes have been reported in the larval stage of oviparous fish or the suckling stage of viviparous mammals. Our findings suggest that the viviparous teleost acquired trophotaenia-based viviparity from a modification of the intestinal absorption system common in vertebrates. This is a fundamental study to understand the strategic variation of the reproductive system in vertebrates.

Identifiants

pubmed: 34170318
pii: 269277
doi: 10.1242/jeb.242613
pmc: PMC8278012
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2021. Published by The Company of Biologists Ltd.

Déclaration de conflit d'intérêts

Competing interests The authors declare no competing or financial interests.

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Auteurs

Atsuo Iida (A)

Department of Animal Sciences, Graduate School of Bioagricultural Sciences, Nagoya University, Tokai National Higher Education and Research System, Nagoya 464-8601, Aichi, Japan.

Kaori Sano (K)

Department of Chemistry, Faculty of Science, Josai University, Sakado 350-0295, Saitama, Japan.

Mayu Inokuchi (M)

Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo, Tokyo 113-8657, Japan.

Jumpei Nomura (J)

Department of Animal Sciences, Graduate School of Bioagricultural Sciences, Nagoya University, Tokai National Higher Education and Research System, Nagoya 464-8601, Aichi, Japan.

Takayuki Suzuki (T)

Department of Animal Sciences, Graduate School of Bioagricultural Sciences, Nagoya University, Tokai National Higher Education and Research System, Nagoya 464-8601, Aichi, Japan.

Mao Kuriki (M)

Department of Regeneration Science and Engineering, Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto, Kyoto 606-8507, Japan.

Maina Sogabe (M)

Department of Regeneration Science and Engineering, Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto, Kyoto 606-8507, Japan.

Daichi Susaki (D)

Kihara Institute for Biological Research, Yokohama City University, Yokohama 244-0813, Kanagawa, Japan.

Kaoru Tonosaki (K)

Kihara Institute for Biological Research, Yokohama City University, Yokohama 244-0813, Kanagawa, Japan.

Tetsu Kinoshita (T)

Kihara Institute for Biological Research, Yokohama City University, Yokohama 244-0813, Kanagawa, Japan.

Eiichi Hondo (E)

Department of Animal Sciences, Graduate School of Bioagricultural Sciences, Nagoya University, Tokai National Higher Education and Research System, Nagoya 464-8601, Aichi, Japan.

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Classifications MeSH