Biphasic adaptation to osmotic stress in the C. elegans germ line

Am J Physiol Cell Physiol. 2017 Jun 1;312(6):C741-C748. doi: 10.1152/ajpcell.00364.2016. Epub 2017 Apr 5.

Abstract

Cells respond to environmental stress in multiple ways. In the germ line, heat shock and nutritive stress trigger the assembly of large ribonucleoprotein (RNP) granules via liquid-liquid phase separation (LLPS). The RNP granules are hypothesized to maintain the quality of oocytes during stress. The goal of this study was to investigate the cellular response to glucose in the germ line and determine if it is an osmotic stress response. We found that exposure to 500 mM glucose induces the assembly of RNP granules in the germ line within 1 h. Interestingly, the RNP granules are maintained for up to 3 h; however, they dissociate after longer periods of stress. The RNP granules include processing body and stress granule proteins, suggesting shared functions. Based on several lines of evidence, the germ line response to glucose largely appears to be an osmotic stress response, thus identifying osmotic stress as a trigger of LLPS. Although RNP granules are not maintained beyond 3 h of osmotic stress, the quality of oocytes does not appear to decrease after longer periods of stress, suggesting a secondary adaptation in the germ line. We used an indirect marker of glycerol and observed high levels after 5 and 20 h of glucose exposure. Moreover, in gpdh-1;gpdh-2 germ lines, glycerol levels are reduced concomitant with RNP granules being maintained for an extended period. We speculate that increased glycerol levels may function as a secondary osmoregulatory adaptive response in the germ line, following a primary response of RNP granule assembly.

Keywords: C. elegans; RNP granules; germ line; glucose; osmotic stress.

MeSH terms

  • Adaptation, Physiological*
  • Animals
  • Caenorhabditis elegans / drug effects*
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Cell Survival / drug effects
  • Cytoplasmic Granules / drug effects*
  • Cytoplasmic Granules / metabolism
  • Cytoplasmic Granules / ultrastructure
  • Disorders of Sex Development / genetics
  • Disorders of Sex Development / metabolism
  • Dose-Response Relationship, Drug
  • Gene Expression Regulation
  • Genes, Reporter
  • Glucose / pharmacology*
  • Glycerol / metabolism
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Oocytes / cytology
  • Oocytes / drug effects*
  • Oocytes / metabolism
  • Osmotic Pressure
  • RNA Nucleotidyltransferases / genetics
  • RNA Nucleotidyltransferases / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Ribonucleoproteins / agonists
  • Ribonucleoproteins / genetics*
  • Ribonucleoproteins / metabolism
  • Stress, Physiological

Substances

  • Caenorhabditis elegans Proteins
  • Car-1 protein, C elegans
  • RNA-Binding Proteins
  • Ribonucleoproteins
  • Green Fluorescent Proteins
  • RNA Nucleotidyltransferases
  • cgh-1 protein, C elegans
  • Glucose
  • Glycerol