Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention

EMBO J. 2004 Jul 7;23(13):2674-83. doi: 10.1038/sj.emboj.7600269. Epub 2004 Jun 17.

Abstract

Mdc1/NFBD1 controls cellular responses to DNA damage, in part via interacting with the Mre11-Rad50-Nbs1 complex that is involved in the recognition, signalling, and repair of DNA double-strand breaks (DSBs). Here, we show that in live human cells, the transient interaction of Nbs1 with DSBs and its phosphorylation by ATM are Mdc1-independent. However, ablation of Mdc1 by siRNA or mutation of the Nbs1's FHA domain required for Mdc1 binding reduced the affinity of Nbs1 for DSB-flanking chromatin and caused aberrant pan-nuclear dispersal of Nbs1. This occurred despite normal phosphorylation of H2AX, indicating that lack of Mdc1 does not impair this DSB-induced chromatin change, but rather precludes the sustained engagement of Nbs1 with these regions. Mdc1 (but not Nbs1) became partially immobilized to chromatin after DSB generation, and siRNA-mediated depletion of H2AX prevented such relocalization of Mdc1 and uncoupled Nbs1 from DSB-flanking chromatin. Our data suggest that Mdc1 functions as an H2AX-dependent interaction platform enabling a switch from transient, Mdc1-independent recruitment of Nbs1 to DSBs towards sustained, Mdc1-dependent interactions with the surrounding chromosomal microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Antibodies, Monoclonal / metabolism
  • Cell Cycle Proteins / chemistry
  • Cell Cycle Proteins / metabolism*
  • Cell Line, Tumor
  • Cell Nucleus / metabolism
  • Chromatin / metabolism*
  • DNA Damage*
  • DNA-Binding Proteins / metabolism*
  • Fluorescent Antibody Technique
  • Fluorescent Dyes
  • Histones / metabolism*
  • Humans
  • Hydrazines
  • Microscopy, Confocal
  • Nuclear Proteins / chemistry
  • Nuclear Proteins / metabolism*
  • Osteosarcoma / pathology
  • Phosphoproteins / metabolism
  • Protein Structure, Tertiary
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Trans-Activators / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Alexa 488 hydrazide
  • Antibodies, Monoclonal
  • Cell Cycle Proteins
  • Chromatin
  • DNA-Binding Proteins
  • Fluorescent Dyes
  • H2AX protein, human
  • Histones
  • Hydrazines
  • MDC1 protein, human
  • NBN protein, human
  • Nuclear Proteins
  • Phosphoproteins
  • RNA, Small Interfering
  • Trans-Activators