Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission.
In sexual reproduction of most animals, the spermatozoon provides DNA and centrioles, together with some cytoplasm and organelles, to the oocyte that is being fertilized. Paternal mitochondria and their genomes are generally eliminated in the embryo by an unknown degradation mechanism. We show that, upon fertilization, a Caenorhabditis elegans spermatozoon triggers the recruitment of autophagosomes within minutes and subsequent paternal mitochondria degradation. Whereas the nematode-specific sperm membranous organelles are ubiquitinated before autophagosome formation, the mitochondria are not. The degradation of both paternal structures and mitochondrial DNA requires an LC3-dependent autophagy. Analysis of fertilized mouse embryos shows the localization of autophagy markers, which suggests that this autophagy event is evolutionarily conserved to prevent both the transmission of paternal mitochondrial DNA to the offspring and the establishment of heteroplasmy.
Université Pierre et Marie Curie-Paris VI, UMR7622-Biologie du Développement, 9 Quai St. Bernard, Paris, France.
Sara
S
Al Rawi
Sophie
S
Louvet-Vallée
Abderazak
A
Djeddi
Martin
M
Sachse
Emmanuel
E
Culetto
Connie
C
Hajjar
Lynn
L
Boyd
Renaud
R
Legouis
Vincent
V
Galy
D000818:Animals; D001343:Autophagy; D017173:Caenorhabditis elegans / Q000196:embryology* / Q000502:physiology; D029742:Caenorhabditis elegans Proteins / Q000032:analysis; D004272:DNA, Mitochondrial / Q000032:analysis / Q000235:genetics* / Q000378:metabolism; D004625:Embryo, Nonmammalian / Q000502:physiology*; D047108:Embryonic Development; D005260:Female; D005306:Fertilization; D057850:Hermaphroditic Organisms; D008247:Lysosomes / Q000378:metabolism; D008297:Male; D051379:Mice; D008928:Mitochondria / Q000378:metabolism*; D009865:Oocytes / Q000502:physiology; D015388:Organelles / Q000378:metabolism; D010588:Phagosomes / Q000378:metabolism; D013094:Spermatozoa / Q000737:chemistry / Q000502:physiology / Q000648:ultrastructure*; D054875:Ubiquitination
D029742:Caenorhabditis elegans Proteins; D004272:DNA, Mitochondrial