No DDRama at chromosome ends: TRF2 takes centre stage

Trends in Biochemical Sciences

Volumn 40, Issue 5, 2015, Pages 275-285

  Feuerhahn, Sascha ^a,d   Chen, Liuh yow ^b   Luke, Brian ^c,e   Porro, Antonio ^a,d  

^a EPFL   (Switzerland)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e INSTITUTE OF MOLECULAR BIOLOGY IMB   (Germany)

Author keywords

Chromatin; DNA damage response; T loops; Telomeres; TERRA; TRF2

Indexed keywords

ATM PROTEIN; DOUBLE STRANDED DNA; LONG UNTRANSLATED RNA; PROTEIN TERRA; REGULATOR PROTEIN; TELOMERIC REPEAT BINDING FACTOR 2; UNCLASSIFIED DRUG; CHROMATIN;

BINDING SITE; CHROMATIN STRUCTURE; CHROMOSOME STRUCTURE; DNA CONFORMATION; DNA DAMAGE; DNA PROTEIN COMPLEX; DNA STRAND BREAKAGE; EUKARYOTIC CELL; HUMAN; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION; TELOMERE; TRANSCRIPTION REGULATION; ANIMAL; CHROMATIN; CHROMOSOME; DNA REPAIR; GENETICS; METABOLISM; PHYSIOLOGY;

EUKARYOTA;

ANIMALS; CHROMATIN; CHROMOSOMES; DNA DAMAGE; DNA REPAIR; HUMANS; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 84927913032     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2015.03.003     Document Type: Review

References (101)

1. de Lange T. How telomeres solve the end-protection problem. Science 2009, 326:948-952.
2. Makarov V.L., et al. Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 1997, 88:657-666.
3. Wright W.E., et al. Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev. 1997, 11:2801-2809.
4. Stewart S.A., et al. Erosion of the telomeric single-strand overhang at replicative senescence. Nat. Genet. 2003, 33:492-496.
5. Zhao Y., et al. Quantitative telomeric overhang determination using a double-strand specific nuclease. Nucleic Acids Res. 2008, 36:e14.
6. Dai X., et al. Molecular steps of G-overhang generation at human telomeres and its function in chromosome end protection. EMBO J. 2010, 29:2788-2801.
7. Palm W., de Lange T. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 2008, 42:301-334.
8. Sfeir A., et al. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 2009, 138:90-103.
9. Baumann P., Cech T.R. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 2001, 292:1171-1175.
10. Kabir S., et al. TALEN gene knockouts reveal no requirement for the conserved human shelterin protein Rap1 in telomere protection and length regulation. Cell Rep. 2014, 9:1273-1280.
11. d'Adda di Fagagna F., et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003, 426:194-198.
12. Fumagalli M., et al. Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat. Cell Biol. 2012, 14:355-365.
13. Hewitt G., et al. Telomeres are favoured targets of a persistent DNA damage response in ageing and stress-induced senescence. Nat. Commun. 2012, 3:708.
14. Karlseder J., et al. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 1999, 283:1321-1325.
15. Celli G.B., de Lange T. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 2005, 7:712-718.
16. Denchi E.L., de Lange T. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 2007, 448:1068-1071.
17. Takai H., et al. DNA damage foci at dysfunctional telomeres. Curr. Biol. 2003, 13:1549-1556.
18. Celli G.B., et al. Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat. Cell Biol. 2006, 8:885-890.
19. Smogorzewska A., et al. DNA ligase IV-dependent NHEJ of deprotected mammalian telomeres in G1 and G2. Curr. Biol. 2002, 12:1635-1644.
20. Takai K.K., et al. Telomere protection by TPP1/POT1 requires tethering to TIN2. Mol. Cell 2011, 44:647-659.
21. Frescas D., de Lange T. TRF2-tethered TIN2 can mediate telomere protection by TPP1/POT1. Mol. Cell. Biol. 2014, 34:1349-1362.
22. Broccoli D., et al. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 1997, 17:231-235.
23. Bilaud T., et al. Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet. 1997, 17:236-239.
24. Bilaud T., et al. The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res. 1996, 24:1294-1303.
25. Hanaoka S., et al. Comparison between TRF2 and TRF1 of their telomeric DNA-bound structures and DNA-binding activities. Protein Sci. 2005, 14:119-130.
26. Court R., et al. How the human telomeric proteins TRF1 and TRF2 recognize telomeric DNA: a view from high-resolution crystal structures. EMBO Rep. 2005, 6:39-45.
27. Stansel R.M., et al. T-loop assembly in vitro involves binding of TRF2 near the 3' telomeric overhang. EMBO J. 2001, 20:5532-5540.
28. Fouche N., et al. The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats. J. Biol. Chem. 2006, 281:37486-37495.
29. Poulet A., et al. TRF2 promotes, remodels and protects telomeric Holliday junctions. EMBO J. 2009, 28:641-651.
30. Amiard S., et al. A topological mechanism for TRF2-enhanced strand invasion. Nat. Struct. Mol. Biol. 2007, 14:147-154.
31. Ye J., et al. TRF2 and apollo cooperate with topoisomerase 2alpha to protect human telomeres from replicative damage. Cell 2010, 142:230-242.
32. Karlseder J., et al. Senescence induced by altered telomere state, not telomere loss. Science 2002, 295:2446-2449.
33. Fujita K., et al. Positive feedback between p53 and TRF2 during telomere-damage signalling and cellular senescence. Nat. Cell Biol. 2010, 12:1205-1212.
34. Cesare A.J., et al. Spontaneous occurrence of telomeric DNA damage response in the absence of chromosome fusions. Nat. Struct. Mol. Biol. 2009, 16:1244-1251.
35. Kaul Z., et al. Five dysfunctional telomeres predict onset of senescence in human cells. EMBO Rep. 2012, 13:52-59.
36. Cesare A.J., Karlseder J. A three-state model of telomere control over human proliferative boundaries. Curr. Opin. Cell Biol. 2012, 24:731-738.
37. Cesare A.J., et al. The telomere deprotection response is functionally distinct from the genomic DNA damage response. Mol. Cell 2013, 51:141-155.
38. Orthwein A., et al. Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science 2014, 344:189-193.
39. Hayashi M.T., et al. A telomere-dependent DNA damage checkpoint induced by prolonged mitotic arrest. Nat. Struct. Mol. Biol. 2012, 19:387-394.
40. Cesare A.J. Mitosis, double strand break repair, and telomeres: a view from the end: how telomeres and the DNA damage response cooperate during mitosis to maintain genome stability. Bioessays 2014, 36:1054-1061.
41. Okamoto K., et al. A two-step mechanism for TRF2-mediated chromosome-end protection. Nature 2013, 494:502-505.
42. Griffith J.D., et al. Mammalian telomeres end in a large duplex loop. Cell 1999, 97:503-514.
43. Doksani Y., et al. Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation. Cell 2013, 155:345-356.
44. van Overbeek M., de Lange T. Apollo, an Artemis-related nuclease, interacts with TRF2 and protects human telomeres in S phase. Curr. Biol. 2006, 16:1295-1302.
45. Lenain C., et al. The Apollo 5' exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr. Biol. 2006, 16:1303-13s
46. Moshous D., et al. Artemis, a novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 2001, 105:177-186.
47. Wu P., et al. Apollo contributes to G overhang maintenance and protects leading-end telomeres. Mol. Cell 2010, 39:606-617.
48. Wu P., et al. Telomeric 3' overhangs derive from resection by Exo1 and Apollo and fill-in by POT1b-associated CST. Cell 2012, 150:39-52.
49. Sarek G., et al. TRF2 recruits RTEL1 to telomeres in S phase to promote T-loop unwinding. Mol. Cell 2015, 57:622-635.
50. Uringa E.J., et al. RTEL1 contributes to DNA replication and repair and telomere maintenance. Mol. Biol. Cell 2012, 23:2782-2792.
51. Vannier J.B., et al. RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 2012, 149:795-806.
52. Wan B., et al. SLX4 assembles a telomere maintenance toolkit by bridging multiple endonucleases with telomeres. Cell Rep. 2013, 4:861-869.
53. Fekairi S., et al. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 2009, 138:78-89.
54. Kim Y., et al. Regulation of multiple DNA repair pathways by the Fanconi anemia protein SLX4. Blood 2013, 121:54-63.
55. Munoz I.M., et al. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell 2009, 35:116-127.
56. Svendsen J.M., et al. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 2009, 138:63-77.
57. Pickett H.A., et al. Control of telomere length by a trimming mechanism that involves generation of t-circles. EMBO J. 2009, 28:799-809.
58. Saint-Leger A., et al. The basic N-terminal domain of TRF2 limits recombination endonuclease action at human telomeres. Cell Cycle 2014, 13:2469-2474.
59. Wang R.C., et al. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 2004, 119:355-368.
60. Ribes-Zamora A., et al. TRF2 interaction with Ku heterotetramerization interface gives insight into c-NHEJ prevention at human telomeres. Cell Rep. 2013, 5:194-206.
61. Bianchi A., de Lange T. Ku binds telomeric DNA in vitro. J. Biol. Chem. 1999, 274:21223-21227.
62. Bae N.S., Baumann P. A RAP1/TRF2 complex inhibits nonhomologous end-joining at human telomeric DNA ends. Mol. Cell 2007, 26:323-334.
63. Schoeftner S., Blasco M.A. A 'higher order' of telomere regulation: telomere heterochromatin and telomeric RNAs. EMBO J. 2009, 28:2323-2336.
64. Galati A., et al. TRF2 controls telomeric nucleosome organization in a cell cycle phase-dependent manner. PLoS ONE 2012, 7:e34386.
65. Wu P., de Lange T. No overt nucleosome eviction at deprotected telomeres. Mol. Cell. Biol. 2008, 28:5724-5735.
66. Jacobs J.J. Fusing telomeres with RNF8. Nucleus 2012, 3:143-149.
67. Peuscher M.H., Jacobs J.J. DNA-damage response and repair activities at uncapped telomeres depend on RNF8. Nat. Cell Biol. 2011, 13:1139-1145.
68. Dimitrova N., et al. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 2008, 456:524-528.
69. Fradet-Turcotte A., et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 2013, 499:50-54.
70. Bartocci C., et al. Isolation of chromatin from dysfunctional telomeres reveals an important role for Ring1b in NHEJ-mediated chromosome fusions. Cell Rep. 2014, 7:1320-1332.
71. Cao R., et al. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol. Cell 2005, 20:845-854.
72. Stock J.K., et al. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat. Cell Biol. 2007, 9:1428-1435.
73. Azzalin C.M., et al. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007, 318:798-801.
74. Schoeftner S., Blasco M.A. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 2008, 10:228-236.
75. Luke B., Lingner J. TERRA: telomeric repeat-containing RNA. EMBO J. 2009, 28:2503-2510.
76. Deng Z., et al. TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol. Cell 2009, 35:403-413.
77. Porro A., et al. Molecular dissection of telomeric repeat-containing RNA biogenesis unveils the presence of distinct and multiple regulatory pathways. Mol. Cell. Biol. 2010, 30:4808-4817.
78. Porro A., et al. Functional characterization of the TERRA transcriptome at damaged telomeres. Nat. Commun. 2014, 5:5379.
79. Baker A.M., et al. The telomere binding protein TRF2 induces chromatin compaction. PLoS ONE 2011, 6:e19124.
80. Arnoult N., et al. Telomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1alpha. Nat. Struct. Mol. Biol. 2012, 19:948-956.
81. Chiolo I., et al. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 2011, 144:732-744.
82. Miller K.M., et al. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat. Struct. Mol. Biol. 2010, 17:1144-1151.
83. Sun Y., et al. DNA damage-induced acetylation of lysine 3016 of ATM activates ATM kinase activity. Mol. Cell. Biol. 2007, 27:8502-8509.
84. Sun Y., et al. Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat. Cell Biol. 2009, 11:1376-1382.
85. Kaidi A., Jackson S.P. KAT5 tyrosine phosphorylation couples chromatin sensing to ATM signalling. Nature 2013, 498:70-74.
86. Cann K.L., Dellaire G. Heterochromatin and the DNA damage response: the need to relax. Biochem. Cell Biol. 2011, 89:45-60.
87. Porro A., et al. TERRA-reinforced association of LSD1 with MRE11 promotes processing of uncapped telomeres. Cell Rep. 2014, 6:765-776.
88. Shi Y., et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
89. Metzger E., et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005, 437:436-439.
90. Lan F., et al. Mechanisms involved in the regulation of histone lysine demethylases. Curr. Opin. Cell Biol. 2008, 20:316-325.
91. Huang J., et al. p53 is regulated by the lysine demethylase LSD1. Nature 2007, 449:105-108.
92. Cho H.S., et al. Demethylation of RB regulator MYPT1 by histone demethylase LSD1 promotes cell cycle progression in cancer cells. Cancer Res. 2011, 71:655-660.
93. Kontaki H., Talianidis I. Lysine methylation regulates E2F1-induced cell death. Mol. Cell 2010, 39:152-160.
94. van Steensel B., et al. TRF2 protects human telomeres from end-to-end fusions. Cell 1998, 92:401-413.
95. Zhu X.D., et al. ERCC1/XPF removes the 3' overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol. Cell 2003, 12:1489-1498.
96. Attwooll C.L., et al. The mre11 complex and the response to dysfunctional telomeres. Mol. Cell. Biol. 2009, 29:5540-5551.
97. Deng Y., et al. Multiple roles for MRE11 at uncapped telomeres. Nature 2009, 460:914-918.
98. Karlseder J., et al. The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol. 2004, 2:E240.
99. Buscemi G., et al. The shelterin protein TRF2 inhibits Chk2 activity at telomeres in the absence of DNA damage. Curr. Biol. 2009, 19:874-879.
100. Bombarde O., et al. TRF2/RAP1 and DNA-PK mediate a double protection against joining at telomeric ends. EMBO J. 2010, 29:1573-1584.
101. Sfeir A., et al. Loss of Rap1 induces telomere recombination in the absence of NHEJ or a DNA damage signal. Science 2010, 327:1657-1661.