Iida Atsuo, Sano Kaori, Inokuchi Mayu, Nomura Jumpei, Suzuki Takayuki, Kuriki Mao, Sogabe Maina, Susaki Daichi, Tonosaki Kaoru, Kinoshita Tetsu, Hondo Eiichi
Department of Animal Sciences, Graduate School of Bioagricultural Sciences, Nagoya University, Tokai National Higher Education and Research System, Nagoya 464-8601, Aichi, Japan.
Department of Chemistry, Faculty of Science, Josai University, Sakado 350-0295, Saitama, Japan.
J Exp Biol. 2021 Jul 1;224(13). doi: 10.1242/jeb.242613. Epub 2021 Jul 2.
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.
在胎生动物中，营养物质从母体向胚胎的转移对繁殖至关重要。在胎生硬骨鱼艾氏异丽鱼（古氏鱼科）中，卵巢内的胚胎通过带状滋养层摄取分泌到卵巢液中的母体成分。我们之前的研究报道，带状滋养层的上皮层细胞通过囊泡运输摄取一种母体蛋白。然而，负责吸收的分子仍然不清楚。在这里，我们聚焦于作为参与吸收的受体的Cubam（立方蛋白-无载脂蛋白）以及作为囊泡中功能性蛋白酶的组织蛋白酶L。我们的结果表明，Cubam受体分布在带状滋养层上皮的顶端表面，然后被摄入细胞内囊泡。带状滋养层在上皮层细胞中具有酸性细胞器和组织蛋白酶L依赖性蛋白水解活性。这一证据与我们的假设并不矛盾，即受体介导的内吞作用和蛋白水解在胎生硬骨鱼通过带状滋养层吸收母体大分子中发挥作用。这种涉及内吞作用的营养吸收并非胎生鱼类的特有特征。在卵生鱼类的幼体阶段或胎生哺乳动物的哺乳阶段也报道过类似过程。我们的研究结果表明，胎生硬骨鱼基于带状滋养层的胎生方式是从脊椎动物常见的肠道吸收系统的一种改变演化而来。这是一项理解脊椎动物生殖系统策略性变化的基础研究。
