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

Atsuo Iida, Kaori Sano, Mayu Inokuchi, Jumpei Nomura, Takayuki Suzuki, Mao Kuriki, Maina Sogabe, Daichi Susaki, Kaoru Tonosaki, Tetsu Kinoshita, Eiichi Hondo

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

Abstract

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.

Original languageEnglish
Article numberjeb242613
JournalJournal of Experimental Biology
Volume224
Issue number13
DOIs
StatePublished - Jul 2021
Externally publishedYes

Keywords

  • Amnionless
  • Cubilin
  • Goodeidae
  • Proteolysis
  • Trophotaenia
  • Viviparity

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