TRF2-Mediated Control of Telomere DNA Topology as a Mechanism for Chromosome-End Protection

Molecular Cell

Volumn 61, Issue 2, 2016, Pages 274-286

  Benarroch Popivker, Delphine ^a   Pisano, Sabrina ^a   Mendez Bermudez, Aaron ^a,b   Lototska, Liudmyla ^a   Kaur, Parminder ^c   Bauwens, Serge ^a   Djerbi, Nadir ^a   Latrick, Chrysa M ^a,j   Fraisier, Vincent ^d   Pei, Bei ^a   Gay, Alexandre ^a,i   Jaune, Emilie ^a   Foucher, Kevin ^a   Cherfils Vicini, Julien ^a   Aeby, Eric ^e,l,m   Miron, Simona ^f,k   Londoño Vallejo, Arturo ^g   Ye, Jing ^b   Le Du, Marie Hélène ^f   Wang, Hong ^c   Gilson, Eric ^a,b,h   Giraud Panis, Marie Josèphe ^a   more..

^a UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d INSTITUT CURIE   (France)

^e EPFL   (Switzerland)

^f INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^g INSTITUT CURIE   (France)

^h UNIVERSITY HOSPITAL OF NICE   (France)

ⁱ INSERM   (France)

^j UNIVERSITÉ DE STRASBOURG   (France)

^k INSTITUTE OF BIOCHEMISTRY OF THE ROMANIAN ACADEMY   (Romania)

^l MASSACHUSETTS GENERAL HOSPITAL   (United States)

^m HARVARD MEDICAL SCHOOL   (United States)

more..

Author keywords

DNA topology; DNA wrapping; RAP1; Telomere; TRF2

Indexed keywords

ARGININE; DIMER; DNA FRAGMENT; GENOMIC DNA; LYSINE; NAKED DNA; RAP1 PROTEIN; TELOMERIC REPEAT BINDING FACTOR 2; ATM PROTEIN; DNA; TELOMERE BINDING PROTEIN; TERF2IP PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME; DNA DAMAGE CHECKPOINT; DNA END JOINING REPAIR; DNA STRAND; FEMALE; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN FOOTPRINTING; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; TELOMERE; BASE PAIRING; CHEMISTRY; CONFORMATION; DNA DAMAGE; HELA CELL LINE; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; BASE PAIRING; DNA; DNA DAMAGE; DNA END-JOINING REPAIR; HELA CELLS; HUMANS; LYSINE; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; TELOMERE; TELOMERE-BINDING PROTEINS; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 84957428149     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.12.009     Document Type: Article

References (65)

1. Amiard S., Doudeau M., Pinte S., Poulet A., Lenain C., Faivre-Moskalenko C., Angelov D., Hug N., Vindigni A., Bouvet P., et al. A topological mechanism for TRF2-enhanced strand invasion. Nat. Struct. Mol. Biol. 2007, 14:147-154.
2. Bae N.S., Baumann P. A RAP1/TRF2 complex inhibits nonhomologous end-joining at human telomeric DNA ends. Mol. Cell 2007, 26:323-334.
3. Baker A.M., Fu Q., Hayward W., Lindsay S.M., Fletcher T.M. The Myb/SANT domain of the telomere-binding protein TRF2 alters chromatin structure. Nucleic Acids Res. 2009, 37:5019-5031.
4. Baker A.M., Fu Q., Hayward W., Victoria S., Pedroso I.M., Lindsay S.M., Fletcher T.M. The telomere binding protein TRF2 induces chromatin compaction. PLoS ONE 2011, 6:e19124.
5. Bankhead T., Kobryn K., Chaconas G. Unexpected twist: harnessing the energy in positive supercoils to control telomere resolution. Mol. Microbiol. 2006, 62:895-905.
6. Bao K., Cohen S.N. Reverse transcriptase activity innate to DNA polymerase I and DNA topoisomerase I proteins of Streptomyces telomere complex. Proc. Natl. Acad. Sci. USA 2004, 101:14361-14366.
7. Benetti R., Schoeftner S., Muñoz P., Blasco M.A. Role of TRF2 in the assembly of telomeric chromatin. Cell Cycle 2008, 7:3461-3468.
8. Bermejo R., Capra T., Jossen R., Colosio A., Frattini C., Carotenuto W., Cocito A., Doksani Y., Klein H., Gómez-González B., et al. The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores. Cell 2011, 146:233-246.
9. Bilaud T., Koering C.E., Binet-Brasselet E., Ancelin K., Pollice A., Gasser S.M., Gilson E. The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res. 1996, 24:1294-1303.
10. Bilaud T., Brun C., Ancelin K., Koering C.E., Laroche T., Gilson E. Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet. 1997, 17:236-239.
11. Biroccio A., Porru M., Rizzo A., Salvati E., D'Angelo C., Orlandi A., Passeri D., Franceschin M., Stevens M.F., Gilson E., et al. DNA damage persistence as determinant of tumor sensitivity to the combination of Topo I inhibitors and telomere-targeting agents. Clin Cancer Res 2011, 17:2227-2236.
12. 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.
13. Cesare A.J., Karlseder J. A three-state model of telomere control over human proliferative boundaries. Curr. Opin. Cell Biol. 2012, 24:731-738.
14. Cesare A.J., Kaul Z., Cohen S.B., Napier C.E., Pickett H.A., Neumann A.A., Reddel R.R. Spontaneous occurrence of telomeric DNA damage response in the absence of chromosome fusions. Nat. Struct. Mol. Biol. 2009, 16:1244-1251.
15. Cesare A.J., Hayashi M.T., Crabbe L., Karlseder J. The telomere deprotection response is functionally distinct from the genomic DNA damage response. Mol. Cell 2013, 51:141-155.
16. Chaconas G., Kobryn K. Structure, function, and evolution of linear replicons in Borrelia. Annu. Rev. Microbiol. 2010, 64:185-202.
17. Chen Y., Yang Y., van Overbeek M., Donigian J.R., Baciu P., de Lange T., Lei M. A shared docking motif in TRF1 and TRF2 used for differential recruitment of telomeric proteins. Science 2008, 319:1092-1096.
18. Chen L., Zhu X., Zou Y., Xing J., Gilson E., Lu Y., Ye J. The topoisomerase II catalytic inhibitor ICRF-193 preferentially targets telomeres that are capped by TRF2. Am. J. Physiol. Cell Physiol. 2015, 308:C372-C377.
19. Court R., Chapman L., Fairall L., Rhodes D. How the human telomeric proteins TRF1 and TRF2 recognize telomeric DNA: a view from high-resolution crystal structures. EMBO Rep. 2005, 6:39-45.
20. Cristofari G., Lingner J. Telomere length homeostasis requires that telomerase levels are limiting. EMBO J. 2006, 25:565-574.
21. d'Alcontres M.S., Palacios J.A., Mejias D., Blasco M.A. TopoIIα prevents telomere fragility and formation of ultra thin DNA bridges during mitosis through TRF1-dependent binding to telomeres. Cell Cycle 2014, 13:1463-1481.
22. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005, 19:2100-2110.
23. 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.
24. Doksani Y., Wu J.Y., de Lange T., Zhuang X. Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation. Cell 2013, 155:345-356.
25. Fairall L., Chapman L., Moss H., de Lange T., Rhodes D. Structure of the TRFH dimerization domain of the human telomeric proteins TRF1 and TRF2. Mol. Cell 2001, 8:351-361.
26. Feuerhahn S., Chen L.Y., Luke B., Porro A. No DDRama at chromosome ends: TRF2 takes centre stage. Trends Biochem. Sci. 2015, 40:275-285.
27. Fouché N., Cesare A.J., Willcox S., Ozgür S., Compton S.A., Griffith J.D. The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats. J. Biol. Chem. 2006, 281:37486-37495.
28. Galati A., Magdinier F., Colasanti V., Bauwens S., Pinte S., Ricordy R., Giraud-Panis M.J., Pusch M.C., Savino M., Cacchione S., Gilson E. TRF2 controls telomeric nucleosome organization in a cell cycle phase-dependent manner. PLoS ONE 2012, 7:e34386.
29. Germe T., Miller K., Cooper J.P. A non-canonical function of topoisomerase II in disentangling dysfunctional telomeres. EMBO J. 2009, 28:2803-2811.
30. Gilson E., Géli V. How telomeres are replicated. Nat. Rev. Mol. Cell Biol. 2007, 8:825-838.
31. Giraud-Panis M.J., Pisano S., Benarroch-Popivker D., Pei B., Le Du M.H., Gilson E. One identity or more for telomeres?. Front. Oncol. 2013, 3:48.
32. Griffith J.D., Comeau L., Rosenfield S., Stansel R.M., Bianchi A., Moss H., de Lange T. Mammalian telomeres end in a large duplex loop. Cell 1999, 97:503-514.
33. Grolimund L., Aeby E., Hamelin R., Armand F., Chiappe D., Moniatte M., Lingner J. A quantitative telomeric chromatin isolation protocol identifies different telomeric states. Nat. Commun. 2013, 4:2848-2859.
34. Hayashi M.T., Cesare A.J., Fitzpatrick J.A., Lazzerini-Denchi E., Karlseder J. A telomere-dependent DNA damage checkpoint induced by prolonged mitotic arrest. Nat. Struct. Mol. Biol. 2012, 19:387-394.
35. Hsieh M.H., Tsai C.H., Lin C.C., Li T.K., Hung T.W., Chang L.T., Hsin L.W., Teng S.C. Topoisomerase II inhibition suppresses the proliferation of telomerase-negative cancers. Cell. Mol. Life Sci. 2015, 72:1825-1837.
36. Kabir S., Hockemeyer D., de Lange T. 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.
37. Kaul Z., Cesare A.J., Huschtscha L.I., Neumann A.A., Reddel R.R. Five dysfunctional telomeres predict onset of senescence in human cells. EMBO Rep. 2012, 13:52-59.
38. Kim H., Lee O.H., Xin H., Chen L.Y., Qin J., Chae H.K., Lin S.Y., Safari A., Liu D., Songyang Z. TRF2 functions as a protein hub and regulates telomere maintenance by recognizing specific peptide motifs. Nat. Struct. Mol. Biol. 2009, 16:372-379.
39. Kouzine F., Gupta A., Baranello L., Wojtowicz D., Ben-Aissa K., Liu J., Przytycka T.M., Levens D. Transcription-dependent dynamic supercoiling is a short-range genomic force. Nat. Struct. Mol. Biol. 2013, 20:396-403.
40. Leonetti C., Scarsella M., Riggio G., Rizzo A., Salvati E., D'Incalci M., Staszewsky L., Frapolli R., Stevens M.F., Stoppacciaro A., et al. G-quadruplex ligand RHPS4 potentiates the antitumor activity of camptothecins in preclinical models of solid tumors. Clin Cancer Res 2008, 14:7284-7291.
41. Mendoza V.L., Vachet R.W. Probing protein structure by amino acid-specific covalent labeling and mass spectrometry. Mass Spectrom. Rev. 2009, 28:785-815.
42. Mirabella A., Gartenberg M.R. Yeast telomeric sequences function as chromosomal anchorage points in vivo. EMBO J. 1997, 16:523-533.
43. Muraki K., Nabetani A., Nishiyama A., Ishikawa F. Essential roles of Xenopus TRF2 in telomere end protection and replication. Genes Cells 2011, 16:728-739.
44. Okamoto K., Bartocci C., Ouzounov I., Diedrich J.K., Yates J.R., Denchi E.L. A two-step mechanism for TRF2-mediated chromosome-end protection. Nature 2013, 494:502-505.
45. Porro A., Feuerhahn S., Delafontaine J., Riethman H., Rougemont J., Lingner J. Functional characterization of the TERRA transcriptome at damaged telomeres. Nat. Commun. 2014, 5:5379-5391.
46. Porro A., Feuerhahn S., Lingner J. TERRA-reinforced association of LSD1 with MRE11 promotes processing of uncapped telomeres. Cell Rep. 2014, 6:765-776.
47. Poulet A., Buisson R., Faivre-Moskalenko C., Koelblen M., Amiard S., Montel F., Cuesta-Lopez S., Bornet O., Guerlesquin F., Godet T., et al. TRF2 promotes, remodels and protects telomeric Holliday junctions. EMBO J. 2009, 28:641-651.
48. Poulet A., Pisano S., Faivre-Moskalenko C., Pei B., Tauran Y., Haftek-Terreau Z., Brunet F., Le Bihan Y.V., Ledu M.H., Montel F., et al. The N-terminal domains of TRF1 and TRF2 regulate their ability to condense telomeric DNA. Nucleic Acids Res. 2012, 40:2566-2576.
49. Saint-Léger A., Koelblen M., Civitelli L., Bah A., Djerbi N., Giraud-Panis M.J., Londoño-Vallejo A., Ascenzioni F., Gilson E. The basic N-terminal domain of TRF2 limits recombination endonuclease action at human telomeres. Cell Cycle 2014, 13:2469-2474.
50. Sarek G., Vannier J.B., Panier S., Petrini J.H., Boulton S.J. TRF2 recruits RTEL1 to telomeres in S phase to promote t-loop unwinding. Mol. Cell 2015, 57:622-635.
51. Sarthy J., Bae N.S., Scrafford J., Baumann P. Human RAP1 inhibits non-homologous end joining at telomeres. EMBO J. 2009, 28:3390-3399.
52. Stansel R.M., de Lange T., Griffith J.D. T-loop assembly in vitro involves binding of TRF2 near the 3' telomeric overhang. EMBO J. 2001, 20:5532-5540.
53. Takai H., Smogorzewska A., de Lange T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 2003, 13:1549-1556.
54. Takai K.K., Kibe T., Donigian J.R., Frescas D., de Lange T. Telomere protection by TPP1/POT1 requires tethering to TIN2. Mol. Cell 2011, 44:647-659.
55. Temime-Smaali N., Guittat L., Wenner T., Bayart E., Douarre C., Gomez D., Giraud-Panis M.J., Londono-Vallejo A., Gilson E., Amor-Guéret M., Riou J.F. Topoisomerase IIIalpha is required for normal proliferation and telomere stability in alternative lengthening of telomeres. EMBO J. 2008, 27:1513-1524.
56. Thanasoula M., Escandell J.M., Martinez P., Badie S., Muñoz P., Blasco M.A., Tarsounas M. p53 prevents entry into mitosis with uncapped telomeres. Curr. Biol. 2010, 20:521-526.
57. Tsai H.H., Huang C.H., Tessmer I., Erie D.A., Chen C.W. Linear Streptomyces plasmids form superhelical circles through interactions between their terminal proteins. Nucleic Acids Res. 2011, 39:2165-2174.
58. van Steensel B., Smogorzewska A., de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell 1998, 92:401-413.
59. Verdun R.E., Karlseder J. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 2006, 127:709-720.
60. Vos S.M., Tretter E.M., Schmidt B.H., Berger J.M. All tangled up: how cells direct, manage and exploit topoisomerase function. Nat. Rev. Mol. Cell Biol. 2011, 12:827-841.
61. Wan B., Yin J., Horvath K., Sarkar J., Chen Y., Wu J., Wan K., Lu J., Gu P., Yu E.Y., et al. SLX4 assembles a telomere maintenance toolkit by bridging multiple endonucleases with telomeres. Cell Rep. 2013, 4:861-869.
62. Wilson J.S., Tejera A.M., Castor D., Toth R., Blasco M.A., Rouse J. Localization-dependent and -independent roles of SLX4 in regulating telomeres. Cell Rep. 2013, 4:853-860.
63. Wu D., Kaur P., Wang H., Erie D.A. Visualizing the path of DNA through proteins using DREEM imaging. Mol. Cell 2016, 61:315-323. this issue.
64. Ye J., Lenain C., Bauwens S., Rizzo A., Saint-Léger A., Poulet A., Benarroch D., Magdinier F., Morere J., Amiard S., et al. TRF2 and apollo cooperate with topoisomerase 2alpha to protect human telomeres from replicative damage. Cell 2010, 142:230-242.
65. Yeeles J.T., Poli J., Marians K.J., Pasero P. Rescuing stalled or damaged replication forks. Cold Spring Harb. Perspect. Biol. 2013, 5:a012815.