Translational Repression of G3BP in Cancer and Germ Cells Suppresses Stress Granules and Enhances Stress Tolerance

Mol Cell. 2020 Aug 20;79(4):645-659.e9. doi: 10.1016/j.molcel.2020.06.037. Epub 2020 Jul 20.

Abstract

Stress granules (SGs) are membrane-less ribonucleoprotein condensates that form in response to various stress stimuli via phase separation. SGs act as a protective mechanism to cope with acute stress, but persistent SGs have cytotoxic effects that are associated with several age-related diseases. Here, we demonstrate that the testis-specific protein, MAGE-B2, increases cellular stress tolerance by suppressing SG formation through translational inhibition of the key SG nucleator G3BP. MAGE-B2 reduces G3BP protein levels below the critical concentration for phase separation and suppresses SG initiation. Knockout of the MAGE-B2 mouse ortholog or overexpression of G3BP1 confers hypersensitivity of the male germline to heat stress in vivo. Thus, MAGE-B2 provides cytoprotection to maintain mammalian spermatogenesis, a highly thermosensitive process that must be preserved throughout reproductive life. These results demonstrate a mechanism that allows for tissue-specific resistance against stress and could aid in the development of male fertility therapies.

Keywords: DDX5; G3BP; MAGE-B2; RNA binding protein; cancer; cancer-testis antigen; spermatogonial stem cells; stress granule; testis; translation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5' Untranslated Regions
  • Animals
  • Antigens, Neoplasm / genetics
  • Antigens, Neoplasm / metabolism
  • Cytoplasmic Granules / genetics*
  • Cytoplasmic Granules / metabolism
  • Cytoplasmic Granules / pathology
  • DEAD-box RNA Helicases / genetics
  • DEAD-box RNA Helicases / metabolism
  • DNA Helicases / genetics*
  • DNA Helicases / metabolism
  • Female
  • HCT116 Cells
  • HeLa Cells
  • Humans
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism
  • Poly-ADP-Ribose Binding Proteins / genetics*
  • Poly-ADP-Ribose Binding Proteins / metabolism
  • Protein Biosynthesis*
  • RNA Helicases / genetics*
  • RNA Helicases / metabolism
  • RNA Recognition Motif Proteins / genetics*
  • RNA Recognition Motif Proteins / metabolism
  • Spermatogonia / cytology
  • Spermatogonia / pathology
  • Stress, Physiological / genetics*
  • Testis / cytology
  • Testis / metabolism

Substances

  • 5' Untranslated Regions
  • Antigens, Neoplasm
  • Mageb2 protein, mouse
  • Mageb4 protein, mouse
  • Neoplasm Proteins
  • Poly-ADP-Ribose Binding Proteins
  • RNA Recognition Motif Proteins
  • Ddx5 protein, human
  • DNA Helicases
  • G3BP1 protein, human
  • DEAD-box RNA Helicases
  • RNA Helicases