CBD-1 organizes 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 journalArticle

2 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)288-300
Number of pages13
JournalDevelopmental Biology
Volume442
Issue number2
DOIs
StatePublished - Oct 15 2018
Externally publishedYes

Fingerprint

Egg Shell
Ovum
Fertilization
Proteins
Chitin
Zygote
Eggs
Extracellular Matrix
Spermatozoa
Embryonic Structures

Keywords

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

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

Cite this

González, D. P., Lamb, H. V., Partida, D., Wilson, Z. T., Harrison, M. C., Prieto, J. A., ... Olson, S. K. (2018). CBD-1 organizes two independent complexes required for eggshell vitelline layer formation and egg activation in C. elegans. Developmental Biology, 442(2), 288-300. https://doi.org/10.1016/j.ydbio.2018.08.005

CBD-1 organizes two independent complexes required for eggshell vitelline layer formation and egg activation in C. elegans. / González, Delfina P.; Lamb, Helen V.; Partida, Diana; Wilson, Zachary T.; Harrison, Marie Claire; Prieto, Julián A.; Moresco, James J.; Diedrich, Jolene K.; Yates, John R.; Olson, Sara K.

In: Developmental Biology, Vol. 442, No. 2, 15.10.2018, p. 288-300.

Research output: Contribution to journalArticle

González, DP, Lamb, HV, Partida, D, Wilson, ZT, Harrison, MC, Prieto, JA, Moresco, JJ, Diedrich, JK, Yates, JR & Olson, SK 2018, 'CBD-1 organizes two independent complexes required for eggshell vitelline layer formation and egg activation in C. elegans', Developmental Biology, vol. 442, no. 2, pp. 288-300. https://doi.org/10.1016/j.ydbio.2018.08.005
González, Delfina P. ; Lamb, Helen V. ; Partida, Diana ; Wilson, Zachary T. ; Harrison, Marie Claire ; Prieto, Julián A. ; Moresco, James J. ; Diedrich, Jolene K. ; Yates, John R. ; Olson, Sara K. / CBD-1 organizes two independent complexes required for eggshell vitelline layer formation and egg activation in C. elegans. In: Developmental Biology. 2018 ; Vol. 442, No. 2. pp. 288-300.
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AU - Harrison, Marie Claire

AU - Prieto, Julián A.

AU - Moresco, James J.

AU - Diedrich, Jolene K.

AU - Yates, John R.

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