Loss of PGL-1 and PGL-3, members of a family of constitutive germ-granule components, promotes germline apoptosis in C. elegans

J Cell Sci. 2016 Jan 15;129(2):341-53. doi: 10.1242/jcs.174201. Epub 2015 Nov 23.

Abstract

In Caenorhabditis elegans, the mechanisms regulating germline apoptosis remain largely unknown, except for the core machinery. Here, we found that mutants of pgl-1 and pgl-3, encoding members of a family of constitutive protein components of germline-specific P granules, showed increased germline apoptosis under both physiological and DNA-damaged conditions. We also found that the number of germ cells that lost PGL proteins increased significantly following UV irradiation, and that only those PGL-absent germ cells were selectively engulfed by gonadal sheath cells in adult hermaphrodite gonads. We further revealed that CEP-1, the p53 homolog, and the caspase CED-3 promoted elimination of PGL-1 from germ cells following UV irradiation. Furthermore, protein levels of CED-4, the Apaf-1 homolog, and cytoplasmic translocation of SIR-2.1, a Sirtuin homolog, significantly increased in pgl mutants and increased even more following UV irradiation. CED-4 and SIR-2.1 were essential for high levels of germline apoptosis in pgl mutants. We conclude that PGL proteins suppress excessive germline apoptosis by repressing both the protein levels of CED-4 and the cytoplasmic translocation of SIR-2.1. Our study has revealed new roles for PGL-1 and PGL-3 in the control of germline apoptosis.

Keywords: Caenorhabditis elegans; Germline apoptosis; P granules; PGL-1; PGL-3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis*
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans Proteins / genetics*
  • Caenorhabditis elegans Proteins / metabolism
  • Caspases / metabolism
  • Epistasis, Genetic
  • Hermaphroditic Organisms / cytology
  • Hermaphroditic Organisms / genetics
  • Male
  • Protein Transport
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism
  • Spermatozoa / cytology
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • CEP-1 protein, C elegans
  • Caenorhabditis elegans Proteins
  • PGL-1 protein, C elegans
  • PGL-3 protein, C elegans
  • RNA-Binding Proteins
  • Tumor Suppressor Protein p53
  • Caspases
  • ced-3 protein, C elegans