Distinct roles of two eIF4E isoforms in the germline of Caenorhabditis elegans

J Cell Sci. 2020 Mar 30;133(6):jcs237990. doi: 10.1242/jcs.237990.

Abstract

Germ cells use both positive and negative mRNA translational control to regulate gene expression that drives their differentiation into gametes. mRNA translational control is mediated by RNA-binding proteins, miRNAs and translation initiation factors. We have uncovered the discrete roles of two translation initiation factor eIF4E isoforms (IFE-1, IFE-3) that bind 7-methylguanosine (m7G) mRNA caps during Caenorhabditiselegans germline development. IFE-3 plays important roles in germline sex determination (GSD), where it promotes oocyte cell fate and is dispensable for spermatogenesis. IFE-3 is expressed throughout the germline and localizes to germ granules, but is distinct from IFE-1 and PGL-1, and facilitates oocyte growth and viability. This contrasts with the robust expression in spermatocytes of IFE-1, the isoform that resides within P granules in spermatocytes and oocytes, and promotes late spermatogenesis. Each eIF4E is localized by its cognate eIF4E-binding protein (IFE-1:PGL-1 and IFE-3:IFET-1). IFE-3 and IFET-1 regulate translation of several GSD mRNAs, but not those under control of IFE-1. Distinct mutant phenotypes, in vivo localization and differential mRNA translation suggest independent dormant and active periods for each eIF4E isoform in the germline.

Keywords: 4EBP; Gametogenesis; Germline sex determination; Polysomes; eIF4E; mRNA translational control.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Caenorhabditis elegans* / genetics
  • Caenorhabditis elegans* / metabolism
  • Eukaryotic Initiation Factor-4E / genetics
  • Male
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • RNA, Messenger
  • RNA-Binding Proteins

Substances

  • Caenorhabditis elegans Proteins
  • Eukaryotic Initiation Factor-4E
  • PGL-1 protein, C elegans
  • Protein Isoforms
  • RNA, Messenger
  • RNA-Binding Proteins