G-quadruplex formation at the 3′ end of telomere DNA inhibits its extension by telomerase, polymerase and unwinding by helicase

Nucleic Acids Research

Volumn 39, Issue 14, 2011, Pages 6229-6237

  Wang, Quan ^a   Liu, Jia Quan ^b   Chen, Zhao ^b,c   Zheng, Ke Wei ^b   Chen, Chang Yue ^b   Hao, Yu Hua ^a   Tan, Zheng ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b WUHAN UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA POLYMERASE; GUANINE QUADRUPLEX; HELICASE; TELOMERASE;

ARTICLE; CONTROLLED STUDY; DNA FLANKING REGION; ENZYME ACTIVITY; HUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; RNA TRANSCRIPTION; RNA TRANSLATION; TELOMERE;

DNA; DNA POLYMERASE I; G-QUADRUPLEXES; RECQ HELICASES; TELOMERASE; TELOMERE;

EID: 80051762076     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr164     Document Type: Article

References (40)

1. Makarov, V.L., Hirose, Y. and Langmore, J.P. (1997) Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell, 88, 657-666. (Pubitemid 27152408)
2. Wright, W.E., Tesmer, V.M., Huffman, K.E., Levene, S.D. and Shay, J.W. (1997) Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev., 11, 2801-2809. (Pubitemid 27481681)
3. Zhao, Y., Hoshiyama, H., Shay, J.W. and Wright, W.E. (2008) Quantitative telomeric overhang determination using a double-strand specific nuclease. Nucleic Acids Res., 36, e14.
4. Chai, W., Du, Q., Shay, J.W. and Wright, W.E. (2006) Human telomeres have different overhang sizes at leading versus lagging strands. Mol. Cell, 21, 427-435. (Pubitemid 43163537)
5. Olovnikov, A.M. (1973) A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol., 41, 181-190.
6. Morin, G.B. (1997) Telomere control of replicative lifespan. Exp. Gerontol., 32, 375-382. (Pubitemid 27366476)
7. Kim, N.W., Piatyszek, M.A., Prowse, K.R., Harley, C.B., West, M.D., Ho, P.L., Coviello, G.M., Wright, W.E., Weinrich, S.L. and Shay, J.W. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science, 266, 2011-2015.
8. Zahler, A.M., Williamson, J.R., Cech, T.R. and Prescott, D.M. (1991) Inhibition of telomerase by G-quartet DNA structures. Nature, 350, 718-720. (Pubitemid 21912306)
9. Neidle, S. (2010) Human telomeric G-quadruplex: the current status of telomeric G-quadruplexes as therapeutic targets in human cancer. FEBS J., 277, 1118-1125.
10. Tang, J., Kan, Z.Y., Yao, Y., Wang, Q., Hao, Y.H. and Tan, Z. (2008) G-quadruplex preferentially forms at the very 3' end of vertebrate telomeric DNA. Nucleic Acids Res., 36, 1200-1208. (Pubitemid 351330937)
11. Beattie, T.L., Zhou, W., Robinson, M.O. and Harrington, L. (1998) Reconstitution of human telomerase activity in vitro. Curr. Biol., 8, 177-180. (Pubitemid 28091578)
12. Weinrich, S.L., Pruzan, R., Ma, L., Ouellette, M., Tesmer, V.M., Holt, S.E., Bodnar, A.G., Lichtsteiner, S., Kim, N.W., Trager, J.B. et al. (1997) Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat. Genet., 17, 498-502. (Pubitemid 27518407)
13. Gomez, D., Mergny, J.L. and Riou, J.F. (2002) Detection of telomerase inhibitors based on g-quadruplex ligands by a modified telomeric repeat amplification protocol assay. Cancer Res., 62, 3365-3368. (Pubitemid 34651379)
14. Kim, N.W. and Wu, F. (1997) Advances in quantification and characterization of telomerase activity by the telomeric repeat amplification protocol (TRAP). Nucleic Acids Res., 25, 2595-2597. (Pubitemid 27298154)
15. Yao, Y., Wang, Q., Hao, Y.H. and Tan, Z. (2007) An exonuclease I hydrolysis assay for evaluating G-quadruplex stabilization by small molecules. Nucleic Acids Res., 35, e68.
16. Zheng, K.W., Chen, Z., Hao, Y.H. and Tan, Z. (2010) Molecular crowding creates an essential environment for the formation of stable G-quadruplexes in long double-stranded DNA. Nucleic Acids Res., 38, 327-338.
17. 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.
18. Pedroso, I.M., Hayward, W. and Fletcher, T.M. (2009) The effect of the TRF2 N-terminal and TRFH regions on telomeric G-quadruplex structures. Nucleic Acids Res., 37, 1541-1554.
19. Ijdo, J.W., Wells, R.A., Baldini, A. and Reeders, S.T. (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res., 19, 4780.
20. Liu, J.Q., Chen, C.Y., Xue, Y., Hao, Y.H. and Tan, Z. (2010) G-quadruplex hinders translocation of BLM helicase on DNA: a real-time fluorescence spectroscopic unwinding study and comparison with duplex substrates. J. Am. Chem. Soc., 132, 10521-10527.
21. Wang, Q., Ma, L., Hao, Y.H. and Tan, Z. (2010) Folding equilibrium constants of telomere g-quadruplexes in free state or associated with proteins determined by isothermal differential hybridization. Anal. Chem., 82, 9469-9475.
22. Gavory, G., Farrow, M. and Balasubramanian, S. (2002) Minimum length requirement of the alignment domain of human telomerase RNA to sustain catalytic activity in vitro. Nucleic Acids Res., 30, 4470-4480. (Pubitemid 35277257)
23. Yanez, G.H., Khan, S.J., Locovei, A.M., Pedroso, I.M. and Fletcher, T.M. (2005) DNA structure-dependent recruitment of telomeric proteins to single-stranded/double-stranded DNA junctions. Biochem. Biophys. Res. Commun., 328, 49-56. (Pubitemid 40164634)
24. Qi, H., Lin, C.P., Fu, X., Wood, L.M., Liu, A.A., Tsai, Y.C., Chen, Y., Barbieri, C.M., Pilch, D.S. and Liu, L.F. (2006) G-quadruplexes induce apoptosis in tumor cells. Cancer Res., 66, 11808-11816. (Pubitemid 46094192)
25. Morin, G.B. (1991) Recognition of a chromosome truncation site associated with alpha-thalassaemia by human telomerase. Nature, 353, 454-456. (Pubitemid 21912537)
26. Huard, S. and Autexier, C. (2004) Human telomerase catalyzes nucleolytic primer cleavage. Nucleic Acids Res., 32, 2171-2180. (Pubitemid 38854772)
27. Rivera, M.A. and Blackburn, E.H. (2004) Processive utilization of the human telomerase template: lack of a requirement for template switching. J. Biol. Chem., 279, 53770-53781. (Pubitemid 40051886)
28. Henson, J.D., Neumann, A.A., Yeager, T.R. and Reddel, R.R. (2002) Alternative lengthening of telomeres in mammalian cells. Oncogene, 21, 598-610. (Pubitemid 34146260)
29. Drouin, R., Therrien, J.P., Angers, M. and Ouellet, S. (2001) In vivo DNA analysis. Methods Mol. Biol., 148, 175-219.
30. Yuan, B.F., Zhuang, X.Y., Hao, Y.H. and Tan, Z. (2008) Kinetics of base stacking-aided DNA hybridization. Chem. Commun., 6600-6602.
31. Karow, J.K., Chakraverty, R.K. and Hickson, I.D. (1997) The Bloom's syndrome gene product is a 30-50 DNA helicase. J. Biol. Chem., 272, 30611-30614. (Pubitemid 27527490)
32. Sun, H., Karow, J.K., Hickson, I.D. and Maizels, N. (1998) The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem., 273, 27587-27592. (Pubitemid 28500481)
33. Hickson, I.D. (2003) RecQ helicases: caretakers of the genome. Nat. Rev. Cancer, 3, 169-178. (Pubitemid 37328869)
34. Xue, Y., Kan, Z.Y., Wang, Q., Yao, Y., Liu, J., Hao, Y.H. and Tan, Z. (2007) Human telomeric DNA forms parallel-stranded intramolecular G-quadruplex in K+solution under molecular crowding condition. J. Am. Chem. Soc., 129, 11185-11191. (Pubitemid 47435722)
35. Kan, Z.Y., Lin, Y., Wang, F., Zhuang, X.Y., Zhao, Y., Pang, D.W., Hao, Y.H. and Tan, Z. (2007) G-quadruplex formation in human telomeric (TTAGGG) (4) sequence with complementary strand in close vicinity under molecularly crowded condition. Nucleic Acids Res., 35, 3646-3653. (Pubitemid 47244659)
36. Schaffitzel, C., Berger, I., Postberg, J., Hanes, J., Lipps, H.J. and Pluckthun, A. (2001) In vitro generated antibodies specific for telomeric guanine-quadruplex DNA react with Stylonychia lemnae macronuclei. Proc. Natl Acad. Sci. USA, 98, 8572-8577. (Pubitemid 32678069)
37. Paeschke, K., Simonsson, T., Postberg, J., Rhodes, D. and Lipps, H.J. (2005) Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo. Nat. Struct. Mol. Biol., 12, 847-854. (Pubitemid 41486707)
38. Zhang, M.L., Tong, X.J., Fu, X.H., Zhou, B.O., Wang, J., Liao, X.H., Li, Q.J., Shen, N., Ding, J. and Zhou, J.Q. (2010) Yeast telomerase subunit Est1p has guanine quadruplex-promoting activity that is required for telomere elongation. Nat. Struct. Mol. Biol., 17, 202-209.
39. Enokizono, Y., Konishi, Y., Nagata, K., Ouhashi, K., Uesugi, S., Ishikawa, F. and Katahira, M. (2005) Structure of hnRNP D complexed with single-stranded telomere DNA and unfolding of the quadruplex by heterogeneous nuclear ribonucleoprotein D. J. Biol. Chem., 280, 18862-18870. (Pubitemid 41379588)
40. Lipps, H.J. and Rhodes, D. (2009) G-quadruplex structures: in vivo evidence and function. Trends Cell Biol., 19, 414-422.