Egg multivesicular bodies elicit an LC3-associated phagocytosis-like pathway to degrade paternal mitochondria after fertilization

Sharon Ben-Hur, Shoshana Sernik, Sara Afar, Alina Kolpakova, Yoav Politi, Liron Gal, Anat Florentin, Ofra Golani, Ehud Sivan, Nili Dezorella, David Morgenstern, Shmuel Pietrokovski, Eyal Schejter, Keren Yacobi-Sharon and Eli Arama ()
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Sharon Ben-Hur: Weizmann Institute of Science
Shoshana Sernik: Weizmann Institute of Science
Sara Afar: Weizmann Institute of Science
Alina Kolpakova: Weizmann Institute of Science
Yoav Politi: Weizmann Institute of Science
Liron Gal: Weizmann Institute of Science
Anat Florentin: Weizmann Institute of Science
Ofra Golani: Weizmann Institute of Science
Ehud Sivan: Weizmann Institute of Science
Nili Dezorella: Weizmann Institute of Science
David Morgenstern: Weizmann Institute of Science
Shmuel Pietrokovski: Weizmann Institute of Science
Eyal Schejter: Weizmann Institute of Science
Keren Yacobi-Sharon: Weizmann Institute of Science
Eli Arama: Weizmann Institute of Science

Nature Communications, 2024, vol. 15, issue 1, 1-25

Abstract: Abstract Mitochondria are maternally inherited, but the mechanisms underlying paternal mitochondrial elimination after fertilization are far less clear. Using Drosophila, we show that special egg-derived multivesicular body vesicles promote paternal mitochondrial elimination by activating an LC3-associated phagocytosis-like pathway, a cellular defense pathway commonly employed against invading microbes. Upon fertilization, these egg-derived vesicles form extended vesicular sheaths around the sperm flagellum, promoting degradation of the sperm mitochondrial derivative and plasma membrane. LC3-associated phagocytosis cascade of events, including recruitment of a Rubicon-based class III PI(3)K complex to the flagellum vesicular sheaths, its activation, and consequent recruitment of Atg8/LC3, are all required for paternal mitochondrial elimination. Finally, lysosomes fuse with strings of large vesicles derived from the flagellum vesicular sheaths and contain degrading fragments of the paternal mitochondrial derivative. Given reports showing that in some mammals, the paternal mitochondria are also decorated with Atg8/LC3 and surrounded by multivesicular bodies upon fertilization, our findings suggest that a similar pathway also mediates paternal mitochondrial elimination in other flagellated sperm-producing organisms.

Date: 2024
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DOI: 10.1038/s41467-024-50041-5

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