CBD-1 scaffolds two independent complexes required for eggshell vitelline layer formation and egg activation in C. elegans

Delfina P. González, Helen V. Lamb, Diana Partida, Zachary T. Wilson, Marie Claire Harrison, Julián A. Prieto, James J. Moresco, Jolene K. Diedrich, John R. Yates, Sara K. Olson

Research output: Contribution to journalArticlepeer-review

Abstract

Metazoan eggs have a specialized coat of extracellular matrix that aids in sperm-egg recognition. The coat is rapidly remodeled after fertilization to prevent polyspermy and establish a more permanent barrier to protect the developing embryo. In nematodes, this coat is called the vitelline layer, which is remodeled into the outermost layer of a rigid and impermeable eggshell. We have identified three key components of the vitelline layer structural scaffold – PERM-2, PERM-4 and CBD-1, the first such proteins to be described in the nematode C. elegans. CBD-1 recruited PERM-2 and PERM-4 to the nascent vitelline layer via two N-terminal chitin-binding domains. After fertilization, all three proteins redistributed from the zygote surface to the outer eggshell. Depletion of PERM-2 and PERM-4 from the scaffold led to a porous vitelline layer that permitted soluble factors to leak through the eggshell and resulted in embryonic death. In addition to its role in vitelline layer assembly, CBD-1 is also known to scaffold a protein complex required for fertilization and egg activation (EGG-1-5/CHS-1/MBK-2). We found the PERM complex and EGG complex to be structurally and functionally independent, and regulated through distinct domains of CBD-1. CBD-1 is thus a multifaceted regulator that promotes distinct aspects of vitelline layer assembly and egg activation. In sum, our findings identify the first vitelline layer components in nematodes, and provide a foundation through which to explore both conserved and species-specific strategies used by animals to build protective barriers following fertilization.

Original languageEnglish (US)
JournalUnknown Journal
DOIs
StatePublished - Jul 14 2018
Externally publishedYes

Keywords

  • C. elegans eggshell
  • CBD-1
  • fertilization
  • PERM-2 and PERM-4
  • vitelline layer
  • zona pellucida

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • Immunology and Microbiology(all)
  • Neuroscience(all)
  • Pharmacology, Toxicology and Pharmaceutics(all)

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