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MARC-3, a membrane-associated ubiquitin ligase, is required for fast polyspermy block in Caenorhabditis elegans

Author

Listed:
  • Ichiro Kawasaki

    (Gunma University)

  • Kenta Sugiura

    (Gunma University)

  • Taeko Sasaki

    (Gunma University)

  • Noriyuki Matsuda

    (Tokyo Medical and Dental University)

  • Miyuki Sato

    (Gunma University)

  • Ken Sato

    (Gunma University)

Abstract

In many sexually reproducing organisms, oocytes are fundamentally fertilized with one sperm. In Caenorhabditis elegans, chitin layer formation after fertilization by the EGG complex is one of the mechanisms of polyspermy block, but other mechanisms remain unknown. Here, we demonstrate that MARC-3, a membrane-associated RING-CH-type ubiquitin ligase that localizes to the plasma membrane and cortical puncta in oocytes, is involved in fast polyspermy block. During polyspermy, the second sperm entry occurs within approximately 10 s after fertilization in MARC-3-deficient zygotes, whereas it occurs approximately 200 s after fertilization in egg-3 mutant zygotes defective in the chitin layer formation. MARC-3 also functions in the selective degradation of maternal plasma membrane proteins and the transient accumulation of endosomal lysine 63-linked polyubiquitin after fertilization. The RING-finger domain of MARC-3 is required for its in vitro ubiquitination activity and polyspermy block, suggesting that a ubiquitination-mediated mechanism sequentially regulates fast polyspermy block and maternal membrane protein degradation during the oocyte-to-embryo transition.

Suggested Citation

  • Ichiro Kawasaki & Kenta Sugiura & Taeko Sasaki & Noriyuki Matsuda & Miyuki Sato & Ken Sato, 2024. "MARC-3, a membrane-associated ubiquitin ligase, is required for fast polyspermy block in Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44928-6
    DOI: 10.1038/s41467-024-44928-6
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    1. Ravi S. Kamath & Andrew G. Fraser & Yan Dong & Gino Poulin & Richard Durbin & Monica Gotta & Alexander Kanapin & Nathalie Le Bot & Sergio Moreno & Marc Sohrmann & David P. Welchman & Peder Zipperlen &, 2003. "Systematic functional analysis of the Caenorhabditis elegans genome using RNAi," Nature, Nature, vol. 421(6920), pages 231-237, January.
    2. Cynthia DeRenzo & Kimberly J. Reese & Geraldine Seydoux, 2003. "Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation," Nature, Nature, vol. 424(6949), pages 685-689, August.
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