The NBS1-Treacle complex controls ribosomal RNA transcription in response to DNA damage

Nature Cell Biology

Volumn 16, Issue 8, 2014, Pages 792-803

  Larsen, Dorthe H ^a,b   Hari, Flurina ^a   Clapperton, Julie A ^c   Gwerder, Myriam ^a   Gutsche, Katrin ^a   Altmeyer, Matthias ^b   Jungmichel, Stephanie ^b   Toledo, Luis I ^b   Fink, Daniel ^a   Rask, Maj Britt ^b   Grøfte, Merete ^b   Lukas, Claudia ^b   Nielsen, Michael L ^b   Smerdon, Stephen J ^c   Lukas, Jiri ^b   Stucki, Manuel ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b University of Copenhagen   (Denmark)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; NIBRIN; NUCLEAR FACTOR; NUCLEOLAR FACTOR TREACLE; TRANSCRIPTION FACTOR POL I; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DNA DIRECTED RNA POLYMERASE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MULTIPROTEIN COMPLEX; NBN PROTEIN, HUMAN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; RIBOSOME RNA; TCOF1 PROTEIN, HUMAN;

ARTICLE; BIOACCUMULATION; BIOGENESIS; CHROMOSOME BREAKAGE; CONTROLLED STUDY; DNA DAMAGE; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MANDIBULOFACIAL DYSOSTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CELL LINE; CHEMISTRY; DOUBLE STRANDED DNA BREAK; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; MOLECULAR GENETICS; NUCLEOLUS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CELL LINE; CELL NUCLEOLUS; CONSERVED SEQUENCE; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; GENE SILENCING; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT FUSION PROTEINS; RNA POLYMERASE I; RNA, RIBOSOMAL; TRANSCRIPTION, GENETIC;

EID: 84905510594     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3007     Document Type: Article

References (33)

1. Harper, J. W. & Elledge, S. J. The DNA damage response: ten years after. Mol. Cell 28, 739-745 (2007).
2. Shiloh, Y. & Ziv, Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 14, 197-210 (2013).
3. Difilippantonio, S. & Nussenzweig, A. The NBS1-ATM connection revisited. Cell Cycle 6, 2366-2370 (2007).
4. Chrzanowska, K. H., Gregorek, H., Dembowska-Bagi nska, B., Kalina, M. A. & Digweed, M. Nijmegen breakage syndrome (NBS). Orphanet J. Rare Dis. 7, 13 (2012).
5. Stucki, M. & Jackson, S. P. H2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair 5, 534-543 (2006).
6. Spycher, C. et al. Constitutive phosphorylation of MDC1 physically links the MRE11- RAD50-NBS1 complex to damaged chromatin. J. Cell Biol. 181, 227-240 (2008).
7. Melander, F. et al. Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J. Cell Biol. 181, 213-226 (2008).
8. Chapman, J. R. & Jackson, S. P. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. 9, 795-801 (2008).
9. Wu, L., Luo, K., Lou, Z. & Chen, J. MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc. Natl Acad. Sci. USA 105, 11200-11205 (2008).
10. Lloyd, J. et al. A supramodular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Cell 139, 100-111 (2009).
11. Williams, R. S. et al. Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 139, 87-99 (2009).
12. Shanbhag, N. M., Rafalska-Metcalf, I. U., Balane-Bolivar, C., Janicki, S. M. & Greenberg, R. A. ATM-dependent chromatin changes silence transcription In cis to DNA double-strand breaks. Cell 141, 970-981 (2010).
13. Kruhlak, M. J. et al. The ATM repair pathway inhibits RNA polymerase I transcription in response to chromosome breaks. Nature 447, 730-734 (2007).
14. Lukas, C., Bartek, J. & Lukas, J. Imaging of protein movement induced by chromosomal breakage: tiny 'local' lesions pose great 'global' challenges. Chromosoma 114, 146-154 (2005).
15. Goldberg, M. et al. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421, 952-956 (2003).
16. Lukas, C. et al. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23, 2674-2683 (2004).
17. Sakai, D. & Trainor, P. A. Treacher Collins syndrome: unmasking the role of Tcof1/treacle. Int. J. Biochem. Cell Biol. 41, 1229-1232 (2009).
18. Wise, C. A. et al. TCOF1 gene encodes a putative nucleolar phosphoprotein that exhibits mutations in Treacher Collins Syndrome throughout its coding region. Proc. Natl Acad. Sci. USA 94, 3110-3115 (1997).
19. Isaac, C. et al. Characterization of the nucleolar gene product, treacle, in Treacher Collins syndrome. Mol. Biol. Cell 11, 3061-3071 (2000).
20. Meier, U. T. & Blobel, G. Nopp140 shuttles on tracks between nucleolus and cytoplasm. Cell 70, 127-138 (1992).
21. Valdez, B. C., Henning, D., So, R. B., Dixon, J. & Dixon, M. J. The Treacher Collins syndrome (TCOF1) gene product is involved in ribosomal DNA gene transcription by interacting with upstream binding factor. Proc. Natl Acad. Sci. USA 101, 10709-10714 (2004).
22. Dixon, J. et al. Tcof1/Treacle is required for neural crest cell formation and proliferation deficiencies that cause craniofacial abnormalities. Proc. Natl Acad. Sci. USA 103, 13403-13408 (2006).
23. Pankotai, T., Bonhomme, C., Chen, D. & Soutoglou, E. DNAPKcs-dependent arrest of RNA polymerase II transcription in the presence of DNA breaks. Nat. Struct. Mol. Biol. 19, 276-282 (2012).
24. Matsuoka, S. et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (2007).
25. Jones, N. C. et al. Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat. Med. 14, 125-133 (2008).
26. Dauwerse, J. G. et al. Mutations in genes encoding subunits of RNA polymerases I and III cause Treacher Collins syndrome. Nat. Genet. 43, 20-22 (2010).
27. Ide, S., Miyazaki, T., Maki, H. & Kobayashi, T. Abundance of ribosomal RNA gene copies maintains genome integrity. Science 327, 693-696 (2010).
28. Lukas, C., Falck, J., Bartkova, J., Bartek, J. & Lukas, J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5, 255-260 (2003).
29. Gudjonsson, T. et al. TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 150, 697-709 (2012).
30. Nielsen, M. L. et al. Iodoacetamide-induced artifact mimics ubiquitination in mass spectrometry. Nat. Methods 5, 459-460 (2008).
31. Kelstrup, C. D., Young, C., Lavallee, R., Nielsen, M. L. & Olsen, J. V. Optimized fast and sensitive acquisition methods for shotgun proteomics on a quadrupole orbitrap mass spectrometer. J. Proteome Res. 11, 3487-3497 (2012).
32. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008).
33. Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805 (2011).