Mitoguardin-1 and -2 promote maturation and the developmental potential of mouse oocytes by maintaining mitochondrial dynamics and functions

Oncotarget. 2016 Jan 12;7(2):1155-67. doi: 10.18632/oncotarget.6713.

Abstract

Mitochondrial dynamics change mitochondrial morphological features and numbers as a part of adaptive cellular metabolism, which is vital for most eukaryotic cells and organisms. A disease or even death of an animal can occur if these dynamics are disrupted. Using large-scale genetic screening in fruit flies, we previously found the gene mitoguardin (Miga), which encodes a mitochondrial outer-membrane protein and promotes mitochondrial fusion. Knockout mouse strains were generated for the mammalian Miga homologs Miga1 and Miga2. Miga1/2-/- females show greatly reduced quality of oocytes and early embryos and are subfertile. Mitochondria became clustered in the cytoplasm of oocytes from the germinal-vesicle stage to meiosis II; production of reactive oxygen species increased in mitochondria and caused damage to mitochondrial ultrastructures. Additionally, reduced ATP production, a decreased mitochondrial-DNA copy number, and lower mitochondrial membrane potential were detected in Miga1/2-/- oocytes during meiotic maturation. These changes resulted in low rates of polar-body extrusion during oocyte maturation, reduced developmental potential of the resulting early embryos, and consequently female subfertility. We provide direct evidence that MIGA1/2-regulated mitochondrial dynamics is crucial for mitochondrial functions, ensure oocyte maturation, and maintain the developmental potential.

Keywords: Pathology Section; ROS; female infertility; mitochondrion; mtDNA copy number; oocyte meiosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Blastocyst / cytology
  • Blastocyst / drug effects
  • Blastocyst / metabolism
  • Blotting, Western
  • Carbonyl Cyanide m-Chlorophenyl Hydrazone / pharmacology
  • Cells, Cultured
  • DNA, Mitochondrial / genetics
  • DNA, Mitochondrial / metabolism
  • Female
  • Male
  • Membrane Potential, Mitochondrial / drug effects
  • Membrane Potential, Mitochondrial / genetics
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Microscopy, Confocal
  • Microscopy, Electron, Transmission
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mitochondria / ultrastructure
  • Mitochondrial Dynamics*
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Oocytes / drug effects
  • Oocytes / growth & development
  • Oocytes / metabolism*
  • Proton Ionophores / pharmacology
  • Reactive Oxygen Species / metabolism

Substances

  • DNA, Mitochondrial
  • Membrane Proteins
  • Mitochondrial Proteins
  • Proton Ionophores
  • Reactive Oxygen Species
  • mitoguardin-1 protein, mouse
  • mitoguardin-2 protein, mouse
  • Carbonyl Cyanide m-Chlorophenyl Hydrazone
  • Adenosine Triphosphate