An RNA-Binding Multimer Specifies Nematode Sperm Fate

Cell Rep. 2018 Jun 26;23(13):3769-3775. doi: 10.1016/j.celrep.2018.05.095.

Abstract

FOG-3 is a master regulator of sperm fate in Caenorhabditis elegans and homologous to Tob/BTG proteins, which in mammals are monomeric adaptors that recruit enzymes to RNA binding proteins. Here, we determine the FOG-3 crystal structure and in vitro demonstrate that FOG-3 forms dimers that can multimerize. The FOG-3 multimeric structure has a basic surface potential, suggestive of binding nucleic acid. Consistent with that prediction, FOG-3 binds directly to nearly 1,000 RNAs in nematode spermatogenic germ cells. Most binding is to the 3' UTR, and most targets (94%) are oogenic mRNAs, even though assayed in spermatogenic cells. When tethered to a reporter mRNA, FOG-3 represses its expression. Together these findings elucidate the molecular mechanism of sperm fate specification and reveal the evolution of a protein from monomeric to multimeric form with acquisition of a distinct mode of mRNA repression.

Keywords: FOG-3; RNA binding protein; Tob/BTG; multimerization; protein evolution; sperm fate.

Publication types

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

MeSH terms

  • 3' Untranslated Regions
  • Animals
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Dimerization
  • Male
  • Protein Binding
  • Protein Multimerization
  • RNA / chemistry
  • RNA / metabolism
  • RNA Processing, Post-Transcriptional
  • Spermatogenesis
  • Spermatozoa / cytology
  • Spermatozoa / metabolism*

Substances

  • 3' Untranslated Regions
  • Caenorhabditis elegans Proteins
  • FOG-3 protein, C elegans
  • RNA