Elimination of paternal mitochondria through the lysosomal degradation pathway in C. elegans

Cell Res. 2011 Dec;21(12):1662-9. doi: 10.1038/cr.2011.182. Epub 2011 Nov 22.

Abstract

In mammals, the inheritance of mitochondrion and its DNA (mtDNA) is strictly maternal, despite the fact that a sperm can inject up to 100 functional mitochondria into the oocyte during fertilization. The mechanisms responsible for the elimination of the paternal mitochondria remain largely unknown. We report here that this paternal mitochondrial elimination process is conserved in Caenorhabditis elegans, and that the lysosomal pathway actively participates in this process. Molecular and cell biological analyses indicate that in wild-type animals paternal mitochondria and mtDNA are destroyed within two hours after fertilization. In animals with compromised lysosomes, paternal mitochondria persist until late embryonic stages. Therefore, the lysosomal pathway plays an important role in degrading paternal mitochondria introduced into the oocyte during fertilization. Our study indicates that C. elegans is an excellent animal model for understanding and dissecting this conserved biological process critical for animal development and reproduction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans Proteins / antagonists & inhibitors
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • DNA, Mitochondrial / metabolism
  • Embryo, Nonmammalian / metabolism
  • Lysosomes / metabolism*
  • Male
  • Mitochondria / metabolism*
  • RNA Interference
  • Receptors, Cytoplasmic and Nuclear / antagonists & inhibitors
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Time Factors
  • Ubiquitin / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • DNA, Mitochondrial
  • RPN-10 protein, C elegans
  • Rad-23 protein, C elegans
  • Receptors, Cytoplasmic and Nuclear
  • Ubiquitin