Paternal mitochondrial destruction after fertilization is mediated by a common endocytic and autophagic pathway in Drosophila.
Almost all animals contain mitochondria of maternal origin only, but the exact mechanisms underlying this phenomenon are still vague. We investigated the fate of Drosophila paternal mitochondria after fertilization. We demonstrate that the sperm mitochondrial derivative (MD) is rapidly eliminated in a stereotypical process dubbed paternal mitochondrial destruction (PMD). PMD is initiated by a network of vesicles resembling multivesicular bodies and displaying common features of the endocytic and autophagic pathways. These vesicles associate with the sperm tail and mediate the disintegration of its plasma membrane. Subsequently, the MD separates from the axoneme and breaks into smaller fragments, which are then sequestered by autophagosomes for degradation in lysosomes. We further provide evidence for the involvement of the ubiquitin pathway and the autophagy receptor p62 in this process. Finally, we show that the ubiquitin ligase Parkin is not involved in PMD, implying a divergence from the autophagic pathway of damaged mitochondria.
Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100, Israel.
Yoav
Y
Politi
Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100, Israel.
Liron
L
Gal
Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100, Israel.
Yossi
Y
Kalifa
Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100, Israel.
Liat
L
Ravid
Department of Biological Chemistry, Weizmann Institute of Science, Rehovot 76100, Israel.
Zvulun
Z
Elazar
Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100, Israel. Electronic address: eli.arama@weizmann.ac.il.
Eli
E
Arama
D000818:Animals; D001343:Autophagy / Q000502:physiology*; D004272:DNA, Mitochondrial / Q000378:metabolism; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000378:metabolism*; D004705:Endocytosis / Q000502:physiology*; D005306:Fertilization / Q000502:physiology; D040582:Inheritance Patterns / Q000235:genetics / Q000502:physiology*; D008297:Male; D008928:Mitochondria / Q000378:metabolism*; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism*; D013094:Spermatozoa / Q000166:cytology; D025801:Ubiquitin / Q000378:metabolism; D044767:Ubiquitin-Protein Ligases / Q000378:metabolism; D054875:Ubiquitination
C527373:Atg8a protein, Drosophila; D004272:DNA, Mitochondrial; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D009687:Nuclear Proteins; D025801:Ubiquitin; C080596:ref(2)P protein, Drosophila; D044767:Ubiquitin-Protein Ligases; C487430:park protein, Drosophila