P300-mediated acetylation of TRF2 is required for maintaining functional telomeres

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages 2267-2283

  Her, Yoon Ra ^a   Chung, In Kwon ^a  

^a Yonsei University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; TELOMERIC REPEAT BINDING FACTOR 2;

ACETYLATION; ARTICLE; BINDING AFFINITY; CELL AGING; CELL GROWTH; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TELOMERE;

ACETYLATION; AMINO ACID SUBSTITUTION; CELL LINE; CELL PROLIFERATION; DNA DAMAGE; HUMANS; P300-CBP TRANSCRIPTION FACTORS; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 2; UBIQUITIN;

EID: 84876394163     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1354     Document Type: Article

References (59)

1. Blackburn, E.H. (2001) Switching and signaling at the telomere. Cell, 106, 661-673.
2. Smogorzewska, A. and de Lange, T. (2004) Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem., 73, 177-208.
3. Greider, C.W. (1999) Telomeres do d-Loop-t-loop. Cell, 97, 419-422.
4. Griffith, J.D., Comeau, L., Rosenfield, S., Stansel, R.M., Bianchi, A., Moss, H. and de Lange, T. (1999) Mammalian telomeres end in a large duplex loop. Cell, 97, 503-514.
5. Liu, D., O'Connor, M.S., Qin, J. and Songyang, Z. (2004) Telosome, a mammalian telomere-Associated complex formed by multiple telomeric proteins. J. Biol. Chem., 279, 51338-51342.
6. Palm, W. and de Lange, T. (2008) How shelterin protects mammalian telomeres. Annu. Rev. Genet., 42, 301-334.
7. Sfeir, A. and de Lange, T. (2012) Removal of shelterin reveals the telomere end-protection problem. Science, 336, 593-597.
8. van Steensel, B. and de Lange, T. (1997) Control of telomere length by the human telomeric protein TRF1. Nature, 385, 740-743.
9. Broccoli, D., Smogorzewska, A., Chong, L. and de Lange, T. (1997) Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet., 17, 231-235.
10. Baumann, P. and Cech, T.R. (2001) Pot1, the putative telomere end-binding protein in fission yeast and humans. Science, 292, 1171-1175.
11. Li, B., Oestreich, S. and de Lange, T. (2000) Identification of human Rap1: implications for telomere evolution. Cell, 101, 471-483.
12. O'Connor, M.S., Safari, A., Xin, H., Liu, D. and Songyang, Z. (2006) A critical role for TPP1 and TIN2 interaction in high-order telomeric complex assembly. Proc. Natl Acad. Sci. USA, 103, 11874-11879.
13. Xin, H., Liu, D., Wan, M., Safari, A., Kim, H., Sun, W., O'Connor, M.S. and Songyang, Z. (2007) TPP1 is a homologue of ciliate TEBP-beta and interacts with POT1 to recruit telomerase. Nature, 445, 559-562.
14. de Lange, T. (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev., 19, 2100-2110.
15. Hsu, H.L., Gilley, D., Galande, S.A., Hande, M.P., Allen, B., Kim, S.H., Li, G.C., Campisi, J., Kohwi-Shigematsu, T. and Chen, D.J. (2000) Ku acts in a unique way at the mammalian telomere to prevent end joining. Genes Dev., 14, 2807-2812.
16. Tarsounas, M., Munoz, P., Claas, A., Smiraldo, P.G., Pittman, D.L., Blasco, M.A. and West, S.C. (2004) Telomere maintenance requires the RAD51D recombination/repair protein. Cell, 117, 337-347.
17. Francia, S., Weiss, R.S., Hande, M.P., Freire, R. and d'Adda di Fagagna, F. (2006) Telomere and telomerase modulation by the mammalian Rad9/Rad1/Hus1 DNA-damage-checkpoint complex. Curr. Biol., 16, 1551-1558.
18. Garcia-Cao, M., O'Sullivan, R., Peters, A.H., Jenuwein, T. and Blasco, M.A. (2004) Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat. Genet., 36, 94-99.
19. Stansel, R.M., de Lange, T. and Griffith, J.D. (2001) T-loop assembly in vitro involves binding of TRF2 near the 3' telomeric overhang. EMBO J., 20, 5532-5540.
20. Verdun, R.E. and Karlseder, J. (2007) Replication and protection of telomeres. Nature, 447, 924-931.
21. Takai, H., Smogorzewska, A. and de Lange, T. (2003) DNA damage foci at dysfunctional telomeres. Curr. Biol., 13, 1549-1556.
22. d'Adda di Fagagna, F., Reaper, P.M., Clay-Farrace, L., Fiegler, H., Carr, P., Von Zglinicki, T., Saretzki, G., Carter, N.P. and Jackson, S.P. (2003) A DNA damage checkpoint response in telomere-initiated senescence. Nature, 426, 194-198.
23. Guo, X., Deng, Y., Lin, Y., Cosme-Blanco, W., Chan, S., He, H., Yuan, G., Brown, E.J. and Chang, S. (2007) Dysfunctional telomeres activate an ATM-ATR-dependent DNA damage response to suppress tumorigenesis. EMBO J., 26, 4709-4719.
24. Karlseder, J., Broccoli, D., Dai, Y., Hardy, S. and de Lange, T. (1999) p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science, 283, 1321-1325.
25. Denchi, E.L. and de Lange, T. (2007) Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature, 448, 1068-1071.
26. Karlseder, J., Hoke, K., Mirzoeva, O.K., Bakkenist, C., Kastan, M.B., Petrini, J.H. and de Lange, T. (2004) The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol., 2, E240.
27. Lenain, C., Bauwens, S., Amiard, S., Brunori, M., Giraud-Panis, M.J. and Gilson, E. (2006) The Apollo 50 exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr. Biol., 16, 1303-1310.
28. van Overbeek, M. and de Lange, T. (2006) Apollo, an Artemis-related nuclease, interacts with TRF2 and protects human telomeres in S phase. Curr. Biol., 16, 1295-1302.
29. Kim, H., Lee, O.H., Xin, H., Chen, L.Y., Qin, J., Chae, H.K., Lin, S.Y., Safari, A., Liu, D. and Songyang, Z. (2009) TRF2 functions as a protein hub and regulates telomere maintenance by recognizing specific peptide motifs. Nat. Struct. Mol. Biol., 16, 372-379.
30. Yoo, H.H. and Chung, I.K. (2011) Requirement of DDX39 DEAD box RNA helicase for genome integrity and telomere protection. Aging Cell, 10, 557-571.
31. Walker, J.R. and Zhu, X.D. (2012) Post-translational modifications of TRF1 and TRF2 and their roles in telomere maintenance. Mech. Ageing Dev., 133, 421-434.
32. Tanaka, H., Mendonca, M.S., Bradshaw, P.S., Hoelz, D.J., Malkas, L.H., Meyn, M.S. and Gilley, D. (2005) DNA damageinduced phosphorylation of the human telomere-Associated protein TRF2. Proc. Natl Acad. Sci. USA, 102, 15539-15544.
33. Huda, N., Tanaka, H., Mendonca, M.S. and Gilley, D. (2009) DNA damage-induced phosphorylation of TRF2 is required for the fast pathway of DNA double-strand break repair. Mol. Cell. Biol., 29, 3597-3604.
34. Fujita, K., Horikawa, I., Mondal, A.M., Jenkins, L.M., Appella, E., Vojtesek, B., Bourdon, J.C., Lane, D.P. and Harris, C.C. (2010) Positive feedback between p53 and TRF2 during telomere-damage signaling and cellular senescence. Nat. Cell Biol., 12, 1205-1212.
35. Potts, P.R. and Yu, H. (2007) The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat. Struct. Mol. Biol., 14, 581-590.
36. Yeager, T.R., Neumann, A.A., Englezou, A., Huschtscha, L.I., Noble, J.R. and Reddel, R.R. (1999) Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res., 59, 4175-4179.
37. Mitchell, T.R., Glenfield, K., Jeyanthan, K. and Zhu, X.D. (2009) Arginine methylation regulates telomere length and stability. Mol. Cell. Biol., 29, 4918-4934.
38. Dantzer, F., Giraud-Panis, M.J., Jaco, I., Ame, J.C., Schultz, I., Blasco, M., Koering, C.E., Gilson, E., Menissier-de Murcia, J. et al. (2004) Functional interaction between poly(ADP-Ribose) polymerase 2 (PARP-2) and TRF2: PARP activity negatively regulates TRF2. Mol. Cell. Biol., 24, 1595-1607.
39. Gomez, M., Wu, J., Schreiber, V., Dunlap, J., Dantzer, F., Wang, Y. and Liu, Y. (2006) PARP1 Is a TRF2-Associated poly(ADP-ribose)polymerase and protects eroded telomeres. Mol. Biol. Cell, 17, 1686-1696.
40. Lee, G.E., Yu, E.Y., Cho, C.H., Lee, J., Muller, M.T. and Chung, I.K. (2004) DNA-protein kinase catalytic subunitinteracting protein KIP binds telomerase by interacting with human telomerase reverse transcriptase. J. Biol. Chem., 279, 34750-34755.
41. Loayza, D. and de lange, T. (2003) POT1 as a terminal transducer of TRF1 telomere length control. Nature, 423, 1013-1018.
42. van Steensel, B., Smogorzewska, A. and de Lange, T. (1998) TRF2 protects human telomeres from end-to-end fusions. Cell, 92, 401-413.
43. Liu, L., Scolnick, D.M., Trievel, R.C., Zhang, H.B., Marmorstein, R., Halazonetis, T.D. and Berger, S.L. (1999) p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol. Cell. Biol., 19, 1202-1209.
44. Avantaggiati, M.L., Ogryzko, V., Gardner, K., Giordano, A., Levine, A.S. and Kelly, K. (1997) Recruitment of p300/CBP in p53-dependent signal pathways. Cell, 89, 1175-1184.
45. Kwon, C. and Chung, I.K. (2004) Interaction of an Arabidopsis RNA-binding protein with plant single-stranded telomeric DNA modulates telomerase activity. J. Biol. Chem., 279, 12812-12818.
46. Yuan, W., Condorelli, G., Caruso, M., Felsani, A. and Giordano, A. (1996) Human p300 protein is a coactivator for the transcription factor MyoD. J. Biol. Chem., 271, 9009-9013.
47. Ye, J.Z., Donigian, J.R., van Overbeek, M., Loayza, D., Luo, Y., Krutchinsky, A.N., Chait, B.T. and de Lange, T. (2004) TIN2 binds TRF1 and TRF2 simultaneously and stabilizes the TRF2 complex on telomeres. J. Biol. Chem., 279, 47264-47271.
48. Bhanot, M. and Smith, S. (2012) TIN2 stability is regulated by the E3 ligase Siah2. Mol. Cell. Biol., 32, 376-384.
49. Minucci, S. and Pelicci, P.G. (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer, 6, 38-35.
50. DiTullio, R.A., Mochan, T.A., Venere, M., Bartkova, J., Sehested, M., Bartek, J. and Halazonetis, T.D. (2002) 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol., 4, 998-1002.
51. Bakkenist, C.J. and Kastan, M.B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature, 421, 499-506.
52. Herbig, U., Jobling, W.A., Chen, B.P., Chen, D.J. and Sedivy, J.M. (2004) Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53 and p21CIP1, but not p16INK4a. Mol. Cell, 14, 501-513.
53. Lechel, A., Lechel, A., Satyanarayana, A., Ju, Z., Plentz, R.R., Schaetzlein, S., Rudolph, C., Wilkens, L., Wiemann, S.U., Saretzki, G. et al. (2005) The cellular level of telomere dysfunction determines induction of senescence or apoptosis in vivo. EMBO Rep., 6, 275-281.
54. Stagno D'Alcontres, M., Mendez-Bermudez, A., Foxon, J.L., Royle, N.J. and Salomoni, P. (2007) Lack of TRF2 in ALT cells causes PML-dependent p53 activation and loss of telomeric DNA. J. Cell Biol., 179, 855-867.
55. Wagner, S.A., Beli, P., Weinert, B.T., Nielsen, M.L., Cox, J., Mann, M. and Choudhary, C. (2011) A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell. Proteomics, 10, M111.013284.
56. Chang, W., Dynek, J.N. and Smith, S. (2003) TRF1 is degraded by ubiquitin-mediated proteolysis after release from telomeres. Genes Dev., 17, 1328-1333.
57. Kim, M.K., Kang, M.R., Nam, H.W., Bae, Y.S., Kim, Y.S. and Chung, I.K. (2008) Regulation of telomeric repeat binding factor 1 binding to telomeres by casein kinase 2-mediated phosphorylation. J. Biol. Chem., 283, 14144-14152.
58. Bodnar, A.G., Ouellette, M., Frolkis, M., Holt, S.E., Chiu, C.P., Morin, G.B., Harley, C.B., Shay, J.W., Lichtsteiner, S. and Wright, W.E. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science, 279, 349-352.
59. Campisi, J. and d'Adda di Fagagna, F. (2007) Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell. Biol., 8, 729-740