A topological mechanism for TRF2-enhanced strand invasion

Nature Structural and Molecular Biology

Volumn 14, Issue 2, 2007, Pages 147-154

  Amiard, Simon ^a,b   Doudeau, Michel ^b   Pinte, Sébastien ^a   Poulet, Anaïs ^a,c   Lenain, Christelle ^a   Faivre Moskalenko, Cendrine ^c,d   Angelov, Dimitar ^a,c   Hug, Nele ^e   Vindigni, Alessandro ^f   Bouvet, Philippe ^a,c   Paoletti, Jacques ^b   Gilson, Eric ^a   Giraud Panis, Marie Josèphe ^a,c  

^a Univ Claude Bernard   (France)

^b CENTRE DE BIOPHYSIQUE MOLÉCULAIRE   (France)

^c Laboratoire Joliot Curie   (France)

^d Laboratoire de Physique UMR CNRS ENSL   (France)

^e SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

^f INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MUTANT PROTEIN; TELOMERIC REPEAT BINDING FACTOR 2;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CORRELATION ANALYSIS; DNA BINDING; DNA STRAND; HUMAN; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SEQUENCE HOMOLOGY;

EID: 33846969882     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1192     Document Type: Article

References (47)

1. Chan, S.R. & Blackburn, E.H. Telomeres and telomerase. Phil. Trans. R. Soc. Lond. B 359, 109-121 (2004).
2. Smogorzewska, A. & De Lange, T. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73, 177-208 (2004).
3. Wenz, C. et al. Human telomerase contains two cooperating telomerase RNA molecules. EMBO J. 20, 3526-3534 (2001).
4. Wang, Y. & Patel, D.J. Guanine residues in d(T2AG3) and d(T2G4) form parallel-stranded potassium cation stabilized G-quadruplexes with anti glycosidic torsion angles in solution. Biochemistry 31, 8112-8119 (1992).
5. Griffith, J.D. et al. Mammalian telomeres end in a large duplex loop. Cell 97, 503-514 (1999).
6. 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. 20, 5532-5540 (2001).
7. Ancelin, K. et al. Targeting assay to study the cis functions of human telomeric proteins: evidence for inhibition of telomerase by TRF1 and for activation of telomere degradation by TRF2. Mol. Cell. Biol. 22, 3474-3487 (2002).
8. Wang, R.C., Smogorzewska, A. & de Lange, T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119, 355-368 (2004).
9. Dunham, M.A., Neumann, A.A., Fasching, C.L. & Reddel, R.R. Telomere maintenance by recombination in human cells. Nat. Genet. 26, 447-450 (2000).
10. Bauman, P. & Cech, T.R. Pot1, the putative telomere end binding protein in fission yeast and humans. Science 292, 1171-1175 (2001).
11. Chong, L. et al. A human telomeric protein. Science 270, 1663-1667 (1995).
12. Bilaud, T. et al. Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet. 17, 236-239 (1997).
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. Holloman, W.K., Wiegand, R., Hoessli, C. & Radding, C.M. Uptake of homologous single-stranded fragments by superhelical DNA: a possible mechanism for initiation of genetic recombination. Proc. Natl. Acad. Sci. USA 72, 2394-2398 (1975).
15. Voloshin, O.N. et al. An eclectic DNA structure adopted by human telomeric sequence under superhelical stress and low pH. J. Biomol. Struct. Dyn. 9, 643-652 (1992).
16. Henderson, E. et al. Structure, synthesis, and regulation of telomeres. Cancer Cells 6, 453-461 (1988).
17. Okabe, J., Eguchi, A., Masago, A., Hayakawa, T. & Nakanishi, M. TRF1 is a critical trans-acting factor required for de novo telomere formation in human cells. Hum. Mol. Genet. 9, 2639-2650 (2000).
18. Cox, M.M. The bacterial RecA protein as a motor protein. Annu. Rev. Microbiol. 57, 551-577 (2003).
19. Verdun, R.E. & Karlseder, J. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127, 709-720 (2006).
20. 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. 6, 39-45 (2005).
21. Fouche, N. et al. The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats. J. Biol. Chem. 281, 37486-37495 (2006).
22. Dantzer, F. et al. Functional interaction between poly(ADP-Ribose) polymerase 2 (PARP-2) and TRF2: PARP activity negatively regulates TRF2. Mol. Cell. Biol. 24, 1595-1607 (2004).
23. Li, B., Oestreich, S. & de Lange, T. Identification of human Rap1: implications for telomere evolution. Cell 101, 471-483 (2000).
24. Opresko, P.L. et al. Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem. 277, 41110-41119 (2002).
25. Shure, M., Pulleyblank, D.E. & Vinograd, J. The problems of eukaryotic and prokaryotic DNA packaging and in vivo conformation posed by superhelix density heterogeneity. Nucleic Acids Res. 4, 1183-1205 (1977).
26. Waldmann, T., Eckerich, C., Baack, M. & Gruss, C. The ubiquitous chromatin protein DEK alters the structure of DNA by introducing positive supercoils. J. Biol. Chem. 277, 24988-24994 (2002).
27. Musgrave, D.R., Sandman, K.M. & Reeve, J.N. DNA binding by the archaeal histone HMf results in positive supercoiling. Proc. Natl. Acad. Sci. USA 88, 10397-10401 (1991).
28. Klungsoyr, H.K. & Skarstad, K. Positive supercoiling is generated in the presence of Escherichia coli SeqA protein. Mol. Microbiol. 54, 123-131 (2004).
29. Rau, D.C., Gellert, M., Thoma, F. & Maxwell, A. Structure of the DNA gyrase-DNA complex as revealed by transient electric dichroism. J. Mol. Biol. 193, 555-569 (1987).
30. Yoshimura, S.H., Maruyama, H., Ishikawa, F., Ohki, R. & Takeyasu, K. Molecular mechanisms of DNA end-loop formation by TRF2. Genes Cells 9, 205-218 (2004).
31. Rivetti, C., Guthold, M. & Bustamante, C. Wrapping of DNA around the E. coli RNA polymerase open promoter complex. EMBO J. 18, 4464-4475 (1999).
32. Shin, M. et al. DNA looping-mediated repression by histone-like protein H-NS: specific requirement of Es70 as a cofactor for looping. Genes Dev. 19, 2388-2398 (2005).
33. Belotserkovskii, B.P., Krasilnikova, M.M., Veselkov, A.G. & Frank-Kamenetskii, M.D. Kinetic trapping of H-DNA by oligonucleotide binding. Nucleic Acids Res. 20, 1903-1908 (1992).
34. Budarf, M. & Blackburn, E. S1 nuclease sensitivity of a double-stranded telomeric DNA sequence. Nucleic Acids Res. 15, 6273-6292 (1987).
35. Gilson, E., Muller, T., Sogo, J., Laroche, T. & Gasser, S.M. RAP1 stimulates single- to double-strand association of yeast telomeric DNA: implications for telomere-telomere interactions. Nucleic Acids Res. 22, 5310-5320 (1994).
36. Huertas, D., Lipps, H. & Azorin, F. Characterization of the structural conformation adopted by (TTAGGG)n telomeric DNA repeats of different length in closed circular DNA. J. Biomol. Struct. Dyn. 12, 79-90 (1994).
37. Lyamichev, V.I. et al. An unusual DNA structure detected in a telomeric sequence under superhelical stress and at low pH. Nature 339, 634-637 (1989).
38. Brunori, M. et al. TRF2 inhibition promotes anchorage-independent growth of telomerase-positive human fibroblasts. Oncogene 25, 990-997 (2006).
39. van Steensel, B., Smogorzewska, A. & de Lange, T. TRF2 protects human telomeres from end-to-end fusions. Cell 92, 401-413 (1998).
40. Zhu, X.D., Kuster, B., Mann, M., Petrini, J.H. & de Lange, T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25, 347-352 (2000).
41. Griffith, J., Bianchi, A. & de Lange, T. TRF1 promotes parallel pairing of telomeric tracts in vitro. J. Mol. Biol. 278, 79-88 (1998).
42. Miller, K.M. & Cooper, J.P. The telomere protein Taz1 is required to prevent and repair genomic DNA breaks. Mol. Cell 11, 303-313 (2003).
43. Kelleher, C., Kurth, I. & Lingner, J. Human protection of telomeres 1 (POT1) is a negative regulator of telomerase activity in vitro. Mol. Cell. Biol. 25, 808-818 (2005).
44. Henricksen, L.A., Umbricht, C.B. & Wold, M.S. Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem. 269, 11121-11132 (1994).
45. Angelov, D., Novakov, E., Khochbin, S. & Dimitrov, S. Ultraviolet laser footprinting of histone H1(0)-four-way junction DNA complexes. Biochemistry 38, 11333-11339 (1999).
46. Spassky, A. & Angelov, D. Influence of the local helical conformation on the guanine modifications generated from one-electron DNA oxidation. Biochemistry 36, 6571-6576 (1997).
47. Lyubchenko, Y.L., Oden, P.I., Lampner, D., Lindsay, S.M. & Dunker, K.A. Atomic force microscopy of DNA and bacteriophage in air, water and propanol: the role of adhesion forces. Nucleic Acids Res. 21, 1117-1123 (1993).