Glycolytic enzymes localize to ribonucleoprotein granules in Drosophila germ cells, bind Tudor and protect from transposable elements

EMBO Rep. 2015 Mar;16(3):379-86. doi: 10.15252/embr.201439694. Epub 2015 Jan 18.

Abstract

Germ cells give rise to all cell lineages in the next-generation and are responsible for the continuity of life. In a variety of organisms, germ cells and stem cells contain large ribonucleoprotein granules. Although these particles were discovered more than 100 years ago, their assembly and functions are not well understood. Here we report that glycolytic enzymes are components of these granules in Drosophila germ cells and both their mRNAs and the enzymes themselves are enriched in germ cells. We show that these enzymes are specifically required for germ cell development and that they protect their genomes from transposable elements, providing the first link between metabolism and transposon silencing. We further demonstrate that in the granules, glycolytic enzymes associate with the evolutionarily conserved Tudor protein. Our biochemical and single-particle EM structural analyses of purified Tudor show a flexible molecule and suggest a mechanism for the recruitment of glycolytic enzymes to the granules. Our data indicate that germ cells, similarly to stem cells and tumor cells, might prefer to produce energy through the glycolytic pathway, thus linking a particular metabolism to pluripotency.

Keywords: Tudor domain; germ cells; glycolysis; stem cells; transposable elements.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Base Sequence
  • Cytoplasmic Granules / metabolism*
  • DNA Transposable Elements / physiology*
  • Drosophila / enzymology*
  • Drosophila / physiology
  • Drosophila Proteins / metabolism*
  • Germ Cells / physiology*
  • Glycolysis
  • Membrane Transport Proteins / metabolism*
  • MicroRNAs / genetics
  • Molecular Sequence Data
  • Ribonucleoproteins / metabolism*
  • Sequence Analysis, DNA

Substances

  • DNA Transposable Elements
  • Drosophila Proteins
  • Membrane Transport Proteins
  • MicroRNAs
  • Ribonucleoproteins
  • tud protein, Drosophila