TRF2 functions as a protein hub and regulates telomere maintenance by recognizing specific peptide motifs

Nature Structural and Molecular Biology

Volumn 16, Issue 4, 2009, Pages 372-379

  Kim, Hyeung ^a   Lee, Ok Hee ^a   Xin, Huawei ^a   Chen, Liuh Yow ^a   Qin, Jun ^a   Chae, Heekyung Kate ^a   Lin, Shiaw Yih ^b   Safari, Amin ^a   Liu, Dan ^a   Songyang, Zhou ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CELL CYCLE PROTEIN; PEPTIDE LIBRARY; PHOSPHATASE NUCLEAR TARGETING SUBUNIT; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN MCPH1; TELOMERIC REPEAT BINDING FACTOR 1; TELOMERIC REPEAT BINDING FACTOR 2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA DAMAGE; GENOME ANALYSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTEOMICS; TELOMERE;

CELL CYCLE; CELL LINE; DNA-BINDING PROTEINS; HUMANS; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; RNA-BINDING PROTEINS; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 2;

MAMMALIA;

EID: 64049099444     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1575     Document Type: Article

References (46)

1. Blackburn, E.H. Switching and signaling at the telomere. Cell 106, 661-673 (2001).
2. Hackett, J.A. & Greider, C.W. Balancing instability: dual roles for telomerase and telomere dysfunction in tumorigenesis. Oncogene 21, 619-626 (2002).
3. Granger, M.P., Wright, W.E. & Shay, J.W. Telomerase in cancer and aging. Crit. Rev. Oncol. Hematol. 41, 29-40 (2002).
4. Harrington, L. & Robinson, M.O. Telomere dysfunction: multiple paths to the same end. Oncogene 21, 592-597 (2002).
5. Collins, K. & Mitchell, J.R. Telomerase in the human organism. Oncogene 21, 564-579 (2002).
6. Maser, R.S. & DePinho, R.A. Connecting chromosomes, crisis, and cancer. Science 297, 565-569 (2002).
7. Hahn, W.C. & Weinberg, R.A. Modelling the molecular circuitry of cancer. Nat. Rev. Cancer 2, 331-341 (2002).
8. Blasco, M.A. Mammalian telomeres and telomerase: why they matter for cancer and aging. Eur. J. Cell Biol. 82, 441-446 (2003).
9. Cech, T.R. Beginning to understand the end of the chromosome. Cell 116, 273-279 (2004).
10. Henderson, E., Hardin, C.C., Walk, S.K., Tinoco Jr, I. & Blackburn, E.H. Telomeric DNA oligonucleotides form novel intramolecular structures containing guanine-guanine base pairs. Cell 51, 899-908 (1987).
11. de Lange, T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19, 2100-2110 (2005).
12. Songyang, Z. & Liu, D. Inside the mammalian telomere interactome: regulation and regulatory activities of telomeres. Crit. Rev. Eukaryot. Gene Expr. 16, 103-118 (2006).
13. Broccoli, D., Smogorzewska, A., Chong, L. & de Lange, T. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 17, 231-235 (1997).
14. Bilaud, T. et al. Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet. 17, 236-239 (1997).
15. Verdun, R.E. & Karlseder, J. Replication and protection of telomeres. Nature 447, 924-931 (2007).
16. Iwano, T., Tachibana, M., Reth, M. & Shinkai, Y. Importance of TRF1 for functional telomere structure. J. Biol. Chem. 279, 1442-1448 (2004).
17. Celli, G.B. & de Lange, T. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 7, 712-718 (2005).
18. Takai, H., Smogorzewska, A. & de Lange, T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13, 1549-1556 (2003).
19. Denchi, E.L. & de Lange, T. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448, 1068-1071 (2007).
20. Wang, R.C., Smogorzewska, A. & de Lange, T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119, 355-368 (2004).
21. van Steensel, B., Smogorzewska, A. & de Lange, T. TRF2 protects human telomeres from end-to-end fusions. Cell 92, 401-413 (1998).
22. van Overbeek, M. & de Lange, T. Apollo, an Artemis-related nuclease, interacts with TRF2 and protects human telomeres in S phase. Curr. Biol. 16, 1295-1302 (2006).
23. Lenain, C. et al. The Apollo 5 exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr. Biol. 16, 1303-1310 (2006).
24. Chen, Y. et al. A shared docking motif in TRF1 and TRF2 used for differential recruitment of telomeric proteins. Science 319, 1092-1096 (2008).
25. Songyang, Z. et al. SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767-778 (1993).
26. Songyang, Z. Recognition and regulation of primary-sequence motifs by signaling modular domains. Prog. Biophys. Mol. Biol. 71, 359-372 (1999).
27. Yaffe, M.B. et al. A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat. Biotechnol. 19, 348-353 (2001).
28. d'Adda di Fagagna, F. et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426, 194-198 (2003).
29. Karlseder, J., Broccoli, D., Dai, Y., Hardy, S. & de Lange, T. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283, 1321-1325 (1999).
30. Liu, D., O'Connor, M.S., Qin, J. & Songyang, Z. Telosome, a mammalian telomereassociated complex formed by multiple telomeric proteins. J. Biol. Chem. 279, 51338-51342 (2004).
31. O'Connor, M.S., Safari, A., Liu, D., Qin, J. & Songyang, Z. The human Rap1 protein complex and modulation of telomere length. J. Biol. Chem. 279, 28585-28591 (2004).
32. Hu, C.D. & Kerppola, T.K. Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat. Biotechnol. 21, 539-545 (2003).
33. Chen, L.Y., Liu, D. & Songyang, Z. Telomere maintenance through spatial control of telomeric proteins. Mol. Cell. Biol. 27, 5898-5909 (2007).
34. Allen, P.B., Kwon, Y.G., Nairn, A.C. & Greengard, P. Isolation and characterization of PNUTS, a putative protein phosphatase 1 nuclear targeting subunit. J. Biol. Chem. 273, 4089-4095 (1998).
35. Lin, S.Y., Rai, R., Li, K., Xu, Z.X. & Elledge, S.J. BRIT1/MCPH1 is a DNA damage responsive protein that regulates the Brca1-Chk1 pathway, implicating checkpoint dysfunction in microcephaly. Proc. Natl. Acad. Sci. USA 102, 15105-15109 (2005).
36. Rai, R. et al. BRIT1 regulates early DNA damage response, chromosomal integrity, and cancer. Cancer Cell 10, 145-157 (2006).
37. Alderton, G.K. et al. Regulation of mitotic entry by microcephalin and its overlap with ATR signalling. Nat. Cell Biol. 8, 725-733 (2006).
38. Wood, J.L., Singh, N., Mer, G. & Chen, J. MCPH1 functions in an H2AX-dependent but MDC1-independent pathway in response to DNA damage. J. Biol. Chem. 282, 35416-35423 (2007).
39. O'Connor, M.S., Safari, A., Xin, H., Liu, D. & Songyang, Z. A critical role for TPP1 and TIN2 interaction in high-order telomeric complex assembly. Proc. Natl. Acad. Sci. USA 103, 11874-11879 (2006).
40. Xin, H. et al. TPP1 is a homologue of ciliate TEBP-β and interacts with POT1 to recruit telomerase. Nature 445, 559-562 (2007).
41. Bae, N.S. & Baumann, P.A. RAP1/TRF2 complex inhibits nonhomologous end-joining at human telomeric DNA ends. Mol. Cell 26, 323-334 (2007).
42. Price, C.M. wRAPing up the end to prevent telomere fusions. Mol. Cell 26, 463-464 (2007).
43. Kim, H., Chen, J. & Yu, X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316, 1202-1205 (2007).
44. Songyang, Z. & Cantley, L.C. The use of peptide library for the determination of kinase peptide substrates. Methods Mol. Biol. 87, 87-98 (1998).
45. Liu, D. et al. PTOP interacts with POT1 and regulates its localization to telomeres. Nat. Cell Biol. 6, 673-680 (2004).
46. Mendez, J. & Stillman, B. Chromatin association of human origin recognition complex, Cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20, 8602-8612 (2000).