Analysis of the behavior of mitochondria in the ovaries of the earthworm Dendrobaena veneta Rosa 1839

PLoS One. 2015 Feb 11;10(2):e0117187. doi: 10.1371/journal.pone.0117187. eCollection 2015.

Abstract

We examined six types of cells that form the ovary of the earthworm Dendrobena veneta ogonia, prooocytes, vitellogenic oocytes, trophocytes, fully grown postvitellogenic oocytes and somatic cells of the gonad. The quantitative stereological method revealed a much higher "volume density" of mitochondria in all of the types of germ-line cells except for the somatic cells. Fluorescent vital stain JC-1, however, showed a much higher oxidative activity of mitochondria in the somatic cells than in the germ-line cells. The distribution of active and inactive mitochondria within the studied cells was assessed using the computer program ImageJ. The analysis showed a higher luminosity of inactive mitochondria in all of the types of germ-line cells and a higher luminosity of active mitochondria in somatic cells. The OXPHOS activity was found in somatic cells mitochondria and in the peripheral mitochondria of the vitellogenic oocytes. The detection of reactive oxygen species (ROS) revealed a differentiated distribution of ROS in the different cell types. The amount of ROS substances was lower in somatic cells than in younger germ-line cells. The ROS level was also low in the cytoplasm of fully grown postwitellogenic oocytes. The distribution of the MnSOD enzyme that protects mitochondria against destructive role of ROS substances was high in the oogonia and in prooocytes and it was very high in vitellogenic and postvitellogenic oocytes. However, a much lower level of this protective enzyme was observed in the trophocytes and the lowest level was found in the cytoplasm of somatic cells. The lower mitochondrial activity and higher level of MnSOD activity in germ-line cells when compared to somatic cells testifies to the necessity of the organisms to protect the mitochondria of oocytes against the destructive role of the ROS that are produced during oxidative phosphorylation. The protection of the mitochondria in oocytes is essential for the transfer of healthy organelles to the next generation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Electron Transport Complex IV / metabolism
  • Female
  • Mitochondria / enzymology
  • Mitochondria / metabolism*
  • Oligochaeta / cytology*
  • Oogenesis
  • Ovary / cytology*
  • Reactive Oxygen Species / metabolism
  • Superoxide Dismutase / metabolism

Substances

  • Reactive Oxygen Species
  • Superoxide Dismutase
  • Electron Transport Complex IV

Grants and funding

This research was financed by the Department of Animal Histology and Embryology, University of Silesia, Katowice, Poland. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.