Identification of novel yolk ferritins unique to planarians: planarians supply aluminum rather than iron to vitellaria in egg capsules

Osamu Kawase, Hisashi Iwaya, Yoshiya Asano, Hiromoto Inoue, Seiya Kudo, Motoki Sasahira, Nobuyuki Azuma, Daisuke Kondoh, Madoka Ichikawa-Seki, Xuenan Xuan, Kimitoshi Sakamoto, Hikaru Okamoto, Hinaki Nakadate, Wataru Inoue, Ikuma Saito, Miyu Narita, Kiyono Sekii, Kazuya Kobayashi

Research output: Contribution to journalArticlepeer-review

Abstract

All animals, other than Platyhelminthes, produce eggs containing yolk, referred to as “entolecithal” eggs. However, only Neoophora, in the phylum Platyhelminthes, produce “ectolecithal” eggs (egg capsules), in which yolk is stored in the vitelline cells surrounding oocytes. Vitelline cells are derived from vitellaria (yolk glands). Vitellaria are important reproductive organs that may be studied to elucidate unique mechanisms that have been evolutionarily conserved within Platyhelminthes. Currently, only limited molecular level information is available on vitellaria. The current study identified major vitellaria-specific proteins in a freshwater planarian, Dugesia ryukyuensis, using peptide mass fingerprinting (PMF) and expression analyses. Amino acid sequence analysis and orthology analysis via OrthoFinder ver.2.3.8 indicated that the identified major vitellaria-specific novel yolk ferritins were conserved in planarians (Tricladida). Because ferritins play an important role in Fe (iron) storage, we examined the metal elements contained in vitellaria and ectolecithal eggs, using non-heme iron histochemistry, elemental analysis based on inductively coupled plasma mass spectrometry and transmission electron microscopy– energy-dispersive X-ray spectroscopy analysis. Interestingly, vitellaria and egg capsules contained large amounts of aluminum (Al), but not Fe. The knockdown of the yolk ferritin genes caused a decrease in the volume of egg capsules, abnormality in juveniles, and increase in Al content in vitellaria. Yolk ferritins of D. ryukyuensis may regulate Al concentration in vitellaria via their pooling function of Al and protect the egg capsule production and normal embryogenesis from Al toxicity.

Original languageEnglish
Pages (from-to)391-413
Number of pages23
JournalCell and Tissue Research
Volume386
Issue number2
DOIs
Publication statusPublished - 2021 Nov
Externally publishedYes

Keywords

  • Aluminum (Al)
  • Egg capsules (ectolecithal eggs, cocoons)
  • Ferritin
  • Planarian
  • Vitellaria (yolk glands)

ASJC Scopus subject areas

  • Pathology and Forensic Medicine
  • Histology
  • Cell Biology

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