Assembly of RNP granules in stressed and aging oocytes requires nucleoporins and is coordinated with nuclear membrane blebbing

Dev Biol. 2011 May 15;353(2):173-85. doi: 10.1016/j.ydbio.2011.02.028. Epub 2011 Mar 5.

Abstract

Protective cellular responses to stress and aging in the germline are essential for perpetuation of a species; however, relatively few studies have focused on how germ cells respond to stress and aging. We have previously shown that large ribonucleoprotein (RNP) complexes assemble in oocytes of Caenorhabditis during extended meiotic arrest or after environmental stress. Here we explore the regulation of these dynamic RNPs and demonstrate their assembly is coordinated with dramatic, nuclear membrane blebbing in oocytes. Our ultrastructural analyses reveal distinct changes in the endoplasmic reticulum, and the first evidence for the assembly of stacked annulate lamellae in Caenorhabditis. We further show several nucleoporins are required for the complete assembly of RNP granules, and a disruption in RNP granule assembly coupled with a low frequency of nuclear blebbing in arrested oocytes negatively impacts embryonic viability. Our observations support a model where nuclear membrane blebbing is required to increase the trafficking of nucleoporins to the cell cortex in stressed or meiotically arrested cells and to facilitate the recruitment of RNA and protein components of RNPs into large complexes. These new insights may have general implications for better understanding how germ cells preserve their integrity when fertilization is delayed and how cells respond to stress.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus
  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis / cytology*
  • Caenorhabditis / genetics
  • Caenorhabditis / metabolism*
  • Cellular Senescence
  • Female
  • Heat-Shock Response
  • Helminth Proteins / metabolism*
  • Male
  • Microscopy, Electron, Transmission
  • Models, Biological
  • Nuclear Envelope / metabolism
  • Nuclear Envelope / ultrastructure
  • Nuclear Pore Complex Proteins / metabolism*
  • Oocytes / cytology
  • Oocytes / metabolism*
  • Ribonucleoproteins / metabolism*
  • Stress, Physiological

Substances

  • Helminth Proteins
  • Nuclear Pore Complex Proteins
  • Ribonucleoproteins