COP9 signalosome component CSN-5 stabilizes PUF proteins FBF-1 and FBF-2 in Caenorhabditis elegans germline stem and progenitor cells

Genetics. 2024 May 7;227(1):iyae033. doi: 10.1093/genetics/iyae033.

Abstract

RNA-binding proteins FBF-1 and FBF-2 (FBFs) are required for germline stem cell maintenance and the sperm/oocyte switch in Caenorhabditis elegans, although the mechanisms controlling FBF protein levels remain unknown. We identified an interaction between both FBFs and CSN-5), a component of the constitutive photomorphogenesis 9 (COP9) signalosome best known for its role in regulating protein degradation. Here, we find that the Mpr1/Pad1 N-terminal metalloprotease domain of CSN-5 interacts with the Pumilio and FBF RNA-binding domain of FBFs and the interaction is conserved for human homologs CSN5 and PUM1. The interaction between FBF-2 and CSN-5 can be detected in vivo by proximity ligation. csn-5 mutation results in the destabilization of FBF proteins, which may explain previously observed decrease in the numbers of germline stem and progenitor cells, and disruption of oogenesis. The loss of csn-5 does not decrease the levels of a related PUF protein PUF-3, and csn-5(lf) phenotype is not enhanced by fbf-1/2 knockdown, suggesting that the effect is specific to FBFs. The effect of csn-5 on oogenesis is largely independent of the COP9 signalosome and is cell autonomous. Surprisingly, the regulation of FBF protein levels involves a combination of COP9-dependent and COP9-independent mechanisms differentially affecting FBF-1 and FBF-2. This work supports a previously unappreciated role for CSN-5 in the stabilization of germline stem cell regulatory proteins FBF-1 and FBF-2.

Keywords: COP9 signalosome; COPS5; CSN-2; CSN-6; PUM1; germline; oocyte development.

Publication types

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

MeSH terms

  • Animals
  • COP9 Signalosome Complex* / genetics
  • COP9 Signalosome Complex* / metabolism
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Caenorhabditis elegans* / cytology
  • Caenorhabditis elegans* / genetics
  • Caenorhabditis elegans* / metabolism
  • Germ Cells / metabolism
  • Oogenesis / genetics
  • Protein Stability
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Stem Cells / cytology
  • Stem Cells / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • COP9 Signalosome Complex
  • fem-3-binding protein, C elegans
  • RNA-Binding Proteins
  • CSN-5 protein, C elegans