NuRD-ZNF827 recruitment to telomeres creates a molecular scaffold for homologous recombination

Nature Structural and Molecular Biology

Volumn 21, Issue 9, 2014, Pages 760-770

  Conomos, Dimitri ^a,b   Reddel, Roger R ^a,b   Pickett, Hilda A ^a,b  

^a CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 2; HISTONE; LEUCINE RICH REPEAT KINASE 2; MOLECULAR SCAFFOLD; NUCLEAR RECEPTOR TR2; NUCLEAR RECEPTOR TR4; PROMYELOCYTIC LEUKEMIA PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN ZNF827; DNA BINDING PROTEIN; HISTONE DEACETYLASE; ZNF827 PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL INTERACTION; CELL PROLIFERATION; CELL VIABILITY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DEACETYLATION; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HISTONE DEACETYLATION; HISTONE MODIFICATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SISTER CHROMATID; SISTER CHROMATID EXCHANGE; TELOMERE; APOPTOSIS; CELL CYCLE; CELL LINE; CHEMISTRY; GENE SILENCING; GENETICS; METABOLISM;

MAMMALIA;

APOPTOSIS; CELL CYCLE; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; GENE KNOCKDOWN TECHNIQUES; HOMOLOGOUS RECOMBINATION; HUMANS; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; TELOMERE;

EID: 84921969781     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2877     Document Type: Article

References (59)

1. Moyzis, R.K. Et al. A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc. Natl. Acad. Sci. USA 85, 6622-6626 (1988).
2. van Steensel, B., Smogorzewska, A. & de Lange, T. TRF2 protects human telomeres from end-to-end fusions. Cell 92, 401-413 (1998).
3. d'Adda di Fagagna, F. Et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426, 194-198 (2003).
4. Wang, R.C., Smogorzewska, A. & de Lange, T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119, 355-368 (2004).
5. Hockemeyer, D., Sfeir, A.J., Shay, J.W., Wright, W.E. & de Lange, T. POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end. EMBO J. 24, 2667-2678 (2005).
6. Celli, G.B., Denchi, E.L. & de Lange, T. Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat. Cell Biol. 8, 885-890 (2006).
7. Sfeir, A., Kabir, S., van Overbeek, M., Celli, G.B. & de Lange, T. Loss of Rap1 induces telomere recombination in the absence of NHEJ or a DNA damage signal. Science 327, 1657-1661 (2010).
8. Shay, J.W. & Bacchetti, S. A survey of telomerase activity in human cancer. Eur. J. Cancer 33, 787-791 (1997).
9. Dunham, M.A., Neumann, A.A., Fasching, C.L. & Reddel, R.R. Telomere maintenance by recombination in human cells. Nat. Genet. 26, 447-450 (2000).
10. Déjardin, J. & Kingston, R.E. Purification of proteins associated with specific genomic loci. Cell 136, 175-186 (2009).
11. Conomos, D. Et al. Variant repeats are interspersed throughout the telomeres and recruit nuclear receptors in ALT cells. J. Cell Biol. 199, 893-906 (2012).
12. Lee, M. Et al. Telomere extension by telomerase and ALT generates variant repeats by mechanistically distinct processes. Nucleic Acids Res. 42, 1733-1746 (2014).
13. Heaphy, C.M. Et al. Altered telomeres in tumors with ATRX and DAXX mutations. Science 333, 425 (2011).
14. Schwartzentruber, J. Et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482, 226-231 (2012).
15. Lovejoy, C.A. Et al. Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway. PLoS Genet. 8, e1002772 (2012).
16. Bower, K. Et al. Loss of wild-type ATRX expression in somatic cell hybrids segregates with activation of alternative lengthening of telomeres. PLoS ONE 7, e50062 (2012).
17. O'Sullivan, R.J. Et al. Rapid induction of alternative lengthening of telomeres by depletion of the histone chaperone ASF1. Nat. Struct. Mol. Biol. 21, 167-174 (2014).
18. Lai, A.Y. & Wade, P.A. Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat. Rev. Cancer 11, 588-596 (2011).
19. Conomos, D., Pickett, H.A. & Reddel, R.R. Alternative lengthening of telomeres: remodeling the telomere architecture. Front. Oncol. 3, 27 (2013).
20. Cui, S. Et al. Nuclear receptors TR2 and TR4 recruit multiple epigenetic transcriptional corepressors that associate specifically with the embryonic β-type globin promoters in differentiated adult erythroid cells. Mol. Cell. Biol. 31, 3298-3311 (2011).
21. Pickett, H.A., Cesare, A.J., Johnstone, R.L., Neumann, A.A. & Reddel, R.R. Control of telomere length by a trimming mechanism that involves generation of t-circles. EMBO J. 28, 799-809 (2009).
22. Hong, W. Et al. FOG-1 recruits the NuRD repressor complex to mediate transcriptional repression by GATA-1. EMBO J. 24, 2367-2378 (2005).
23. Lauberth, S.M. & Rauchman, M. A conserved 12-amino acid motif in Sall1 recruits the nucleosome remodeling and deacetylase corepressor complex. J. Biol. Chem. 281, 23922-23931 (2006).
24. Cismasiu, V.B. Et al. BCL11B functionally associates with the NuRD complex in T lymphocytes to repress targeted promoter. Oncogene 24, 6753-6764 (2005).
25. Topark-Ngarm, A. Et al. CTIP2 associates with the NuRD complex on the promoter of p57KIP2, a newly identified CTIP2 target gene. J. Biol. Chem. 281, 32272-32283 (2006).
26. Wang, Y. Et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138, 660-672 (2009).
27. Porro, A., Feuerhahn, S. & Lingner, J. TERRA-reinforced association of LSD1 with MRE11 promotes processing of uncapped telomeres. Cell Reports 6, 765-776 (2014).
28. Yeager, T.R. Et al. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59, 4175-4179 (1999).
29. Henson, J.D. Et al. DNA C-circles are specific and quantifiable markers of alternative-lengthening-of-telomeres activity. Nat. Biotechnol. 27, 1181-1185 (2009).
30. Londoño-Vallejo, J.A., Der-Sarkissian, H., Cazes, L., Bacchetti, S. & Reddel, R.R. Alternative lengthening of telomeres is characterized by high rates of telomeric exchange. Cancer Res. 64, 2324-2327 (2004).
31. Bechter, O.E., Zou, Y., Walker, W., Wright, W.E. & Shay, J.W. Telomeric recombination in mismatch repair deficient human colon cancer cells after telomerase inhibition. Cancer Res. 64, 3444-3451 (2004).
32. Cesare, A.J. Et al. Spontaneous occurrence of telomeric DNA damage response in the absence of chromosome fusions. Nat. Struct. Mol. Biol. 16, 1244-1251 (2009).
33. Cesare, A.J. & Reddel, R.R. Alternative lengthening of telomeres: models, mechanisms and implications. Nat. Rev. Genet. 11, 319-330 (2010).
34. Pan, M.R. Et al. Chromodomain helicase DNA-binding protein 4 (CHD4) regulates homologous recombination DNA repair, and its deficiency sensitizes cells to poly(ADP-ribose) polymerase (PARP) inhibitor treatment. J. Biol. Chem. 287, 6764-6772 (2012).
35. Lin, S.Y., Liang, Y. & Li, K. Multiple roles of BRIT1/MCPH1 in DNA damage response, DNA repair, and cancer suppression. Yonsei Med. J. 51, 295-301 (2010).
36. Wu, G., Jiang, X., Lee, W.H. & Chen, P.L. Assembly of functional ALT-associated promyelocytic leukemia bodies requires Nijmegen breakage syndrome 1. Cancer Res. 63, 2589-2595 (2003).
37. Draskovic, I. Et al. Probing PML body function in ALT cells reveals spatiotemporal requirements for telomere recombination. Proc. Natl. Acad. Sci. USA 106, 15726-15731 (2009).
38. Smeenk, G. Et al. The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J. Cell Biol. 190, 741-749 (2010).
39. Lejon, S. Et al. Insights into association of the NuRD complex with FOG-1 from the crystal structure of an RbAp48.FOG-1 complex. J. Biol. Chem. 286, 1196-1203 (2011).
40. Muntoni, A., Neumann, A.A., Hills, M. & Reddel, R.R. Telomere elongation involves intra-molecular DNA replication in cells utilizing alternative lengthening of telomeres. Hum. Mol. Genet. 18, 1017-1027 (2009).
41. Chan, K.L., North, P.S. & Hickson, I.D. BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J. 26, 3397-3409 (2007).
42. Barefield, C. & Karlseder, J. The BLM helicase contributes to telomere maintenance through processing of late-replicating intermediate structures. Nucleic Acids Res. 40, 7358-7367 (2012).
43. Park, S.W. Et al. SUMOylation of Tr2 orphan receptor involves Pml and fine-tunes Oct4 expression in stem cells. Nat. Struct. Mol. Biol. 14, 68-75 (2007).
44. Polo, S.E., Kaidi, A., Baskcomb, L., Galanty, Y. & Jackson, S.P. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J. 29, 3130-3139 (2010).
45. Sims, J.K. & Wade, P.A. Mi-2/NuRD complex function is required for normal S phase progression and assembly of pericentric heterochromatin. Mol. Biol. Cell 22, 3094-3102 (2011).
46. Chou, D.M. Et al. A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc. Natl. Acad. Sci. USA 107, 18475-18480 (2010).
47. Doksani, Y., Wu, J.Y., de Lange, T. & Zhuang, X. Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation. Cell 155, 345-356 (2013).
48. Sfeir, A. Et al. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138, 90-103 (2009).
49. Martínez, P. Et al. Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes Dev. 23, 2060-2075 (2009).
50. Episkopou, H. Et al. Alternative lengthening of telomeres is characterized by reduced compaction of telomeric chromatin. Nucleic Acids Res. 42, 4391-4405 (2014).
51. Benetti, R. Et al. Suv4-20h deficiency results in telomere elongation and derepression of telomere recombination. J. Cell Biol. 178, 925-936 (2007).
52. Gonzalo, S. Et al. DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat. Cell Biol. 8, 416-424 (2006).
53. Benetti, R., Garcia-Cao, M. & Blasco, M.A. Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat. Genet. 39, 243-250 (2007).
54. Stern, J.L., Zyner, K.G., Pickett, H.A., Cohen, S.B. & Bryan, T.M. Telomerase recruitment requires both TCAB1 and Cajal bodies independently. Mol. Cell. Biol. 32, 2384-2395 (2012).
55. Cohen, S.B. & Reddel, R.R. A sensitive direct human telomerase activity assay. Nat. Methods 5, 355-360 (2008).
56. Conomos, D. Et al. Variant repeats are interspersed throughout the telomeres and recruit nuclear receptors in ALT cells. J. Cell Biol. 199, 893-906 (2012).
57. Pickett, H.A., Cesare, A.J., Johnstone, R.L., Neumann, A.A. & Reddel, R.R. Control of telomere length by a trimming mechanism that involves generation of t-circles. EMBO J. 28, 799-809 (2009).
58. Smyth, C.M., Helmer, M.A., Dalla-Pozza, L. & Rowe, P.B. Flow cytometric DNA analyses of frozen samples from children's solid tumors. Pathology 25, 388-393 (1993).
59. Henson, J.D. Et al. DNA C-circles are specific and quantifiable markers of alternative-lengthening-of-telomeres activity. Nat. Biotechnol. 27, 1181-1185 (2009).