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Dev Biol. 2018 Oct 15;442(2):288-300. doi: 10.1016/j.ydbio.2018.08.005. Epub 2018 Aug 16.

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

Author information

1
Department of Biology and Program in Molecular Biology, Pomona College, Claremont, CA 91711, USA.
2
Department of Molecular Medicine, The Scripps Research Institute, La Jolla, CA 92037, USA.
3
Department of Biology and Program in Molecular Biology, Pomona College, Claremont, CA 91711, USA. Electronic address: sara.olson@pomona.edu.

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 tethered 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 anchor 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 functionally independent, and structurally organized 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 characterize 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.

KEYWORDS:

C. elegans eggshell; CBD-1; Fertilization; PERM-2 and PERM-4; Vitelline layer; Zona pellucida

PMID:
30120927
PMCID:
PMC6143425
[Available on 2019-10-15]
DOI:
10.1016/j.ydbio.2018.08.005
[Indexed for MEDLINE]
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