A higher-order entity formed by the flexible assembly of RAP1 with TRF2

Nucleic Acids Research

Volumn 44, Issue 4, 2015, Pages 1962-1976

  Gaullier, Guillaume ^a   Miron, Simona ^a   Pisano, Sabrina ^b   Buisson, Rémi ^b,g   Le Bihan, Yann Vaï ^a,h   Tellier Lebègue, Carine ^a   Messaoud, Wala ^a   Roblin, Pierre ^c,d   Guimarães, Beatriz G ^c   Thai, Robert ^e   Giraud Panis, Marie Josèphe ^b   Gilson, Eric ^b,f   Le Du, Marie Hélène ^a  

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

^b UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^c SYNCHROTRON SOLEIL   (France)

^d INRA   (France)

^e SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^f UNIVERSITY HOSPITAL OF NICE   (France)

^g HARVARD MEDICAL SCHOOL   (United States)

^h INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RAP1 PROTEIN; TELOMERIC REPEAT BINDING FACTOR 2; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN BINDING; SHELTERIN, HUMAN; TELOMERE BINDING PROTEIN; TERF2 PROTEIN, HUMAN; TERF2IP PROTEIN, HUMAN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOCHEMISTRY; BIOPHYSICS; CONTROLLED STUDY; DIMERIZATION; DNA BINDING; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; TELOMERE HOMEOSTASIS; X RAY DIFFRACTION; CHEMISTRY; DNA DAMAGE; GENETICS; GENOMIC INSTABILITY; METABOLISM; TELOMERE;

DNA DAMAGE; DNA-BINDING PROTEINS; GENOMIC INSTABILITY; HUMANS; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; TELOMERE; TELOMERE-BINDING PROTEINS; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 84960491018     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1531     Document Type: Article

References (55)

1. 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.
2. de Lange, T. (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev., 19, 2100-2110.
3. Songyang, Z. and Liu, D. (2006) Inside the mammalian telomere interactome: regulation and regulatory activities of telomeres. Crit. Rev. Eukaryot. Gene Expr., 16, 103-118.
4. Giraud-Panis, M.-J., Pisano, S., Benarroch-Popivker, D., Pei, B., Le Du, M.-H. and Gilson, E. (2013) One identity or more for telomeres? Front. Oncol., 3, 48.
5. Luo, Z., Dai, Z., Xie, X., Feng, X., Liu, D., Songyang, Z. and Xiong, Y. (2015) TeloPIN: a database of telomeric proteins interaction network in mammalian cells. Database (Oxford), bav018.
6. Qin, J. and Gronenborn, A.M. (2014) Weak protein complexes: challenging to study but essential for life. FEBS J., 281, 1948-1949.
7. Gilson, E. and Géli, V. (2007) How telomeres are replicated. Nat. Rev. Mol. Cell Biol., 8, 825-838.
8. Verdun, R.E. and Karlseder, J. (2007) Replication and protection of telomeres. Nature, 447, 924-931.
9. Ye, J., Lenain, C., Bauwens, S., Rizzo, A., Saint-Léger, A., Poulet, A., Benarroch, D., Magdinier, F., Morere, J., Amiard, S. et al. (2010) TRF2 and Apollo cooperate with topoisomerase 2alpha to protect human telomeres from replicative damage. Cell, 142, 230-242.
10. Biroccio, A., Cherfils-Vicini, J., Augereau, A., Pinte, S., Bauwens, S., Ye, J., Simonet, T., Horard, B., Jamet, K., Cervera, L. et al. (2013) TRF2 inhibits a cell-extrinsic pathway through which natural killer cells eliminate cancer cells. Nat. Cell Biol., 15, 818-828.
11. Ye, J., Renault, V.M., Jamet, K. and Gilson, E. (2014) Transcriptional outcome of telomere signalling. Nat. Rev. Genet., 15, 491-503.
12. Lenain, C., Bauwens, S., Amiard, S., Brunori, M., Giraud-Panis, M.-J. and Gilson, E. (2006) The Apollo 5' exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr. Biol., 16, 1303-1310.
13. 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.
14. Fairall, L., Chapman, L., Moss, H., de Lange, T. and Rhodes, D. (2001) Structure of the TRFH dimerization domain of the human telomeric proteins TRF1 and TRF2. Mol. Cell, 8, 351-361.
15. Chen, Y., Yang, Y., van Overbeek, M., Donigian, J.R., Baciu, P., de Lange, T. and Lei, M. (2008) A shared docking motif in TRF1 and TRF2 used for differential recruitment of telomeric proteins. Science, 319, 1092-1096.
16. Wan, B., Yin, J., Horvath, K., Sarkar, J., Chen, Y., Wu, J., Wan, K., Lu, J., Gu, P., Yu, E.Y. et al. (2013) SLX4 assembles a telomere maintenance toolkit by bridging multiple endonucleases with telomeres. Cell Rep., 4, 861-869.
17. 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.
18. Sarek, G., Vannier, J.B., Panier, S., Petrini, J.H. and Boulton, S.J. (2015) TRF2 recruits RTEL1 to telomeres in S phase to promote T-loop unwinding. Mol. Cell, 57, 622-635.
19. 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. (2012) The N-terminal domains of TRF1 and TRF2 regulate their ability to condense telomeric DNA. Nucleic Acids Res., 40, 2566-2576.
20. Okamoto, K., Bartocci, C., Ouzounov, I., Diedrich, J.K., Yates, J.R. 3rd and Denchi, E.L. (2013) A two-step mechanism for TRF2-mediated chromosome-end protection. Nature, 494, 502-505.
21. Bilaud, T., Brun, C., Ancelin, K., Koering, C.E., Laroche, T. and Gilson, E. (1997) Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet., 17, 236-239.
22. Court, R., Chapman, L., Fairall, L. and Rhodes, D. (2005) How the human telomeric proteins TRF1 and TRF2 recognize telomeric DNA: a view from high-resolution crystal structures. EMBO Rep., 6, 39-45.
23. Palm, W. and de Lange, T. (2008) How shelterin protects mammalian telomeres. Annu. Rev. Genet., 42, 301-334.
24. Fouche, N., Cesare, A.J., Willcox, S., Ozgur, S., Compton, S.A. and Griffith, J.D. (2006) The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats. J. Biol. Chem., 281, 37486-37495.
25. Poulet, A., Buisson, R., Faivre-Moskalenko, C., Koelblen, M., Amiard, S., Montel, F., Cuesta-Lopez, S., Bornet, O., Guerlesquin, F., Godet, T. et al. (2009) TRF2 promotes, remodels and protects telomeric Holliday junctions. EMBO J., 28, 641-651.
26. Deng, Z., Norseen, J., Wiedmer, A., Riethman, H. and Lieberman, P.M. (2009) TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol. Cell, 35, 403-413.
27. Baker, A.M., Fu, Q., Hayward, W., Victoria, S., Pedroso, I.M., Lindsay, S.M. and Fletcher, T.M. (2011) The telomere binding protein TRF2 induces chromatin compaction. PLoS One, 6, e19124.
28. Chen, Y., Rai, R., Zhou, Z.-R., Kanoh, J., Ribeyre, C., Yang, Y., Zheng, H., Damay, P., Wang, F., Tsujii, H. et al. (2011) A conserved motif within RAP1 has diversified roles in telomere protection and regulation in different organisms. Nat. Struct. Mol. Biol., 18, 213-221.
29. Li, B., Oestreich, S. and de Lange, T. (2000) Identification of human Rap1: implications for telomere evolution. Cell, 101, 471-483.
30. Bae, N.S. and Baumann, P. (2007) A RAP1/TRF2 complex inhibits nonhomologous end-joining at human telomeric DNA ends. Mol. Cell, 26, 323-334.
31. Kabir, S., Sfeir, A. and de Lange, T. (2010) Taking apart Rap1: an adaptor protein with telomeric and non-telomeric functions. Cell Cycle Georget. Tex, 9, 4061-4067.
32. Kabir, S., Hockemeyer, D. and de Lange, T. (2014) TALEN gene knockouts reveal no requirement for the conserved human shelterin protein Rap1 in telomere protection and length regulation. Cell Rep., 9, 1273-1280.
33. Martinez, P., Thanasoula, M., Carlos, A.R., Gó;mez-Ló;pez, G., Tejera, A.M., Schoeftner, S., Dominguez, O., Pisano, D.G., Tarsounas, M. and Blasco, M.A. (2010) Mammalian Rap1 controls telomere function and gene expression through binding to telomeric and extratelomeric sites. Nat. Cell Biol., 12, 768-780.
34. Yang, D., Xiong, Y., Kim, H., He, Q., Li, Y., Chen, R. and Songyang, Z. (2011) Human telomeric proteins occupy selective interstitial sites. Cell Res., 21, 1013-1027.
35. Teo, H., Ghosh, S., Luesch, H., Ghosh, A., Wong, E.T., Malik, N., Orth, A., de Jesus, P., Perry, A.S., Oliver, J.D. et al. (2010) Telomere-independent Rap1 is an IKK adaptor and regulates NF-kappaB-dependent gene expression. Nat. Cell Biol., 12, 758-767.
36. Takai, K.K., Hooper, S., Blackwood, S., Gandhi, R. and de Lange, T. (2010) In vivo stoichiometry of shelterin components. J. Biol. Chem., 285, 1457-1467.
37. Janoušková;, E., Nečasová;, I., Pavloušková;, J., Zimmermann, M., Hluchý;, M., Marini, V., Nová;ková;, M. and Hofr, C. (2015) Human Rap1 modulates TRF2 attraction to telomeric DNA. Nucleic Acids Res., 43, 2691-2700.
38. Amiard, S., Doudeau, M., Pinte, S., Poulet, A., Lenain, C., Faivre-Moskalenko, C., Angelov, D., Hug, N., Vindigni, A., Bouvet, P. et al. (2007) A topological mechanism for TRF2-enhanced strand invasion. Nat. Struct. Mol. Biol., 14, 147-154.
39. David, G. and Pérez, J. (2009) Combined sampler robot and high-performance liquid chromatography: a fully automated system for biological small-angle X-ray scattering experiments at the Synchrotron SOLEIL SWING beamline. J. Appl. Crystallogr., 42, 892-900.
40. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr., 66, 125-132.
41. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr., 40, 658-674.
42. Bricogne, G., Blanc, E., Brandl, M., Flensburg, C., Keller, P., Paciorek, W., Roversi, P., Smart, O.S., Vonrhein, C. and Womack, T.O. (2011) BUSTER, version 2.8.0. Camb. U. K. Glob. Phasing Ltd.
43. Abmayr, S.M., Yao, T., Parmely, T. and Workman, J.L. (2006) Preparation of nuclear and cytoplasmic extracts from mammalian cells. In: Current Protocols in Molecular Biology. Vol. 75, 12.1, 12.1.1-12.1.10. John Wiley & Sons, Inc.
44. Eswar, N., Eramian, D., Webb, B., Shen, M.-Y. and Sali, A. (2008) Protein structure modeling with MODELLER. Methods Mol. Biol. Clifton N.J., 426, 145-159.
45. Zhang, W., Zhang, J., Zhang, X., Xu, C. and Tu, X. (2011) Solution structure of Rap1 BRCT domain from Saccharomyces cerevisiae reveals a novel fold. Biochem. Biophys. Res. Commun., 404, 1055-1059.
46. Hanaoka, S., Nagadoi, A., Yoshimura, S., Aimoto, S., Li, B., de Lange, T. and Nishimura, Y. (2001) NMR structure of the hRap1 Myb motif reveals a canonical three-helix bundle lacking the positive surface charge typical of Myb DNA-binding domains. J. Mol. Biol., 312, 167-175.
47. Schrödinger LLC (2010) The PyMOL Molecular Graphics System, Version 1.7.4
48. Ashkenazy, H., Erez, E., Martz, E., Pupko, T. and Ben-Tal, N. (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res., 38, W529-W533.
49. Arat, Ö.N. and Griffith, J.D. (2012) Human Rap1 interacts directly with telomeric DNA and regulates TRF2 localization at the telomere. J. Biol. Chem., 287, 41583-41594.
50. Rambo, R.P. and Tainer, J.A. (2010) Bridging the solution divide: comprehensive structural analyses of dynamic RNA, DNA, and protein assemblies by small-angle X-ray scattering. Curr. Opin. Struct. Biol., 20, 128-137.
51. Durand, D., Vivès, C., Cannella, D., Pérez, J., Pebay-Peyroula, E., Vachette, P. and Fieschi, F. (2010) NADPH oxidase activator p67phox behaves in solution as a multidomain protein with semi-flexible linkers. J. Struct. Biol., 169, 45-53.
52. Carson, M., Johnson, D.H., McDonald, H., Brouillette, C. and DeLucas, L. (2007) His-tag impact on structure. Acta Cryst., D63, 295-301.
53. Sabaty, M., Grosse, S., Adryanczyk, G., Boiry, S., Biaso, F., Arnous, P. and Pignol, D. (2013) Detrimental effect of the 6 His C-terminal tag on YedY enzymatic activity and influence of the TAT signal sequence on YedY synthesis. BMC Biochem., 14, 28.
54. Noirclerc-Savoye, M., Flayhan, A., Pereira, C., Gallet, B., Gans, P., Ebel, C. and Breyton, C. (2015) Tail proteins of phage T5: investigation of the effect of the His6-tag position, from expression to crystallisation. Protein Expr. Purif., 109, 70-78.
55. Gerloff, D.L., Woods, N.T., Farago, A.A. and Monteiro, A.N.A. (2012) BRCT domains: a little more than kin, and less than kind. FEBS Lett., 586, 2711-2716.