DNA damage checkpoint triggers autophagy to regulate the initiation of anaphase

Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):E41-9. doi: 10.1073/pnas.1218065109. Epub 2012 Nov 19.

Abstract

Budding yeast cells suffering a single unrepaired double-strand break (DSB) trigger the Mec1 (ATR)-dependent DNA damage response that causes them to arrest before anaphase for 12-15 h. Here we find that hyperactivation of the cytoplasm-to-vacuole (CVT) autophagy pathway causes the permanent G2/M arrest of cells with a single DSB that is reflected in the nuclear exclusion of both Esp1 and Pds1. Transient relocalization of Pds1 is also seen in wild-type cells lacking vacuolar protease activity after induction of a DSB. Arrest persists even as the DNA damage-dependent phosphorylation of Rad53 diminishes. Permanent arrest can be overcome by blocking autophagy, by deleting the vacuolar protease Prb1, or by driving Esp1 into the nucleus with a SV40 nuclear localization signal. Autophagy in response to DNA damage can be induced in three different ways: by deleting the Golgi-associated retrograde protein complex (GARP), by adding rapamycin, or by overexpression of a dominant ATG13-8SA mutation.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus / physiology
  • Adaptor Proteins, Signal Transducing / genetics
  • Anaphase / physiology*
  • Autophagy / drug effects
  • Autophagy / physiology*
  • Autophagy-Related Proteins
  • Blotting, Western
  • Cell Cycle Checkpoints / physiology*
  • Cell Cycle Proteins / metabolism
  • DNA Breaks, Double-Stranded*
  • Endopeptidases / metabolism
  • Green Fluorescent Proteins
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Nuclear Proteins / metabolism
  • Protein Serine-Threonine Kinases / metabolism*
  • Saccharomyces cerevisiae
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Saccharomycetales
  • Securin
  • Separase
  • Sirolimus / pharmacology

Substances

  • ATG13 protein, S cerevisiae
  • Adaptor Proteins, Signal Transducing
  • Autophagy-Related Proteins
  • Cell Cycle Proteins
  • Intracellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • PDS1 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Securin
  • Green Fluorescent Proteins
  • MEC1 protein, S cerevisiae
  • Protein Serine-Threonine Kinases
  • Endopeptidases
  • ESP1 protein, S cerevisiae
  • Separase
  • Sirolimus