Degradation of the Separase-cleaved Rec8, a Meiotic Cohesin Subunit, by the N-end Rule Pathway

J Biol Chem. 2016 Apr 1;291(14):7426-38. doi: 10.1074/jbc.M116.714964. Epub 2016 Feb 8.

Abstract

The Ate1 arginyltransferase (R-transferase) is a component of the N-end rule pathway, which recognizes proteins containing N-terminal degradation signals called N-degrons, polyubiquitylates these proteins, and thereby causes their degradation by the proteasome. Ate1 arginylates N-terminal Asp, Glu, or (oxidized) Cys. The resulting N-terminal Arg is recognized by ubiquitin ligases of the N-end rule pathway. In the yeastSaccharomyces cerevisiae, the separase-mediated cleavage of the Scc1/Rad21/Mcd1 cohesin subunit generates a C-terminal fragment that bears N-terminal Arg and is destroyed by the N-end rule pathway without a requirement for arginylation. In contrast, the separase-mediated cleavage of Rec8, the mammalian meiotic cohesin subunit, yields a fragment bearing N-terminal Glu, a substrate of the Ate1 R-transferase. Here we constructed and used a germ cell-confinedAte1(-/-)mouse strain to analyze the separase-generated C-terminal fragment of Rec8. We show that this fragment is a short-lived N-end rule substrate, that its degradation requires N-terminal arginylation, and that maleAte1(-/-)mice are nearly infertile, due to massive apoptotic death ofAte1(-/-)spermatocytes during the metaphase of meiosis I. These effects ofAte1ablation are inferred to be caused, at least in part, by the failure to destroy the C-terminal fragment of Rec8 in the absence of N-terminal arginylation.

Keywords: meiosis; protein degradation; proteolysis; spermatogenesis; ubiquitin.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aminoacyltransferases / genetics
  • Aminoacyltransferases / metabolism
  • Animals
  • Apoptosis*
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Male
  • Metaphase*
  • Mice
  • Mice, Knockout
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • Proteolysis*
  • Separase / genetics
  • Separase / metabolism*
  • Spermatocytes / metabolism*

Substances

  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Nuclear Proteins
  • Phosphoproteins
  • Rad21 protein, mouse
  • Rec8 protein, mouse
  • Aminoacyltransferases
  • arginyltransferase
  • Separase