The ERM-1 membrane-binding domain directs erm-1 mRNA localization to the plasma membrane in the C. elegans embryo

Development. 2022 Nov 15;149(22):dev200930. doi: 10.1242/dev.200930. Epub 2022 Nov 18.

Abstract

mRNA localization and transport are integral in regulating gene expression. In Caenorhabditis elegans embryos, the maternally inherited mRNA erm-1 (Ezrin/Radixin/Moesin) becomes concentrated in anterior blastomeres. erm-1 mRNA localizes within those blastomeres to the plasma membrane where the essential ERM-1 protein, a membrane-actin linker, is also found. We demonstrate that the localization of erm-1 mRNA to the plasma membrane is translation dependent and requires its encoded N-terminal, membrane-binding (FERM) domain. By perturbing translation through multiple methods, we found that erm-1 mRNA localization at the plasma membrane persisted only if the nascent peptide remained in complex with the translating mRNA. Indeed, re-coding the erm-1 mRNA coding sequence while preserving the encoded amino acid sequence did not disrupt erm-1 mRNA localization, corroborating that the information directing mRNA localization resides within its membrane-binding protein domain. A single-molecule inexpensive fluorescence in situ hybridization screen of 17 genes encoding similar membrane-binding domains identified three plasma membrane-localized mRNAs in the early embryo. Ten additional transcripts showed potential membrane localization later in development. These findings point to a translation-dependent pathway for localization of mRNAs encoding membrane-associated proteins.

Keywords: C. elegans; erm-1; FERM domain; Plasma membrane; Translation; mRNA localization.

Publication types

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

MeSH terms

  • Actins / metabolism
  • Animals
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Caenorhabditis elegans* / genetics
  • Caenorhabditis elegans* / metabolism
  • Cell Membrane / metabolism
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism
  • In Situ Hybridization, Fluorescence
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism

Substances

  • RNA, Messenger
  • Actins
  • ERM-1 protein, C elegans
  • Cytoskeletal Proteins
  • Caenorhabditis elegans Proteins