Telomerase recruitment by the telomere end binding protein-β facilitates G-quadruplex DNA unfolding in ciliates

Nature Structural and Molecular Biology

Volumn 15, Issue 6, 2008, Pages 598-604

  Paeschke, Katrin ^a   Juranek, Stefan ^a   Simonsson, Tomas ^b   Hempel, Anne ^c   Rhodes, Daniela ^c   Lipps, Hans Joachim ^a  

^a UNIVERSITY OF WITTEN HERDECKE   (Germany)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; TELOMERASE; TELOMERE BINDING PROTEIN; TELOMERE END BINDING PROTEIN BETA;

ANIMAL CELL; ARTICLE; CELL CYCLE REGULATION; CILIATE; DNA STRUCTURE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; G QUADRUPLEX DNA UNFOLDING; GENE SYNTHESIS; IN VIVO CULTURE; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; STYLONYCHIA LEMNAE; TELOMERE;

ANIMALS; CELL CYCLE; CILIOPHORA; G-QUADRUPLEXES; NUCLEIC ACID CONFORMATION; PHOSPHORYLATION; PROTEIN TRANSPORT; TELOMERASE; TELOMERE; TELOMERE-BINDING PROTEINS;

CILIOPHORA; STYLONYCHIA LEMNAE;

EID: 44849095213     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1422     Document Type: Article

References (58)

1. de Lange, T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19, 2100-2110 (2005).
2. Klobutcher, L.A., Swanton, M.T., Donini, P. & Prescott, D.M. All gene-sized DNA molecules in four species of hypotrichs have the same terminal sequence and an unusual 3′ terminus. Proc. Natl. Acad. Sci. USA 78, 3015-3019 (1981).
3. Makarov, V.L., Hirose, Y. & Langmore, J.P. Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 88, 657-666 (1997).
4. Gottschling, D.E. & Zakian, V.A. Telomere proteins: specific recognition and protection of the natural termini of Oxytricha macronuclear DNA. Cell 47, 195-205 (1986).
5. Price, C.M. & Cech, T.R. Telomeric DNA-protein interactions of Oxytricha macronuclear DNA. Genes Dev. 1, 783-793 (1987).
6. Jonsson, F. & Lipps, H.J. The biology of telomeres in hypotrichous ciliates. in Telomerases, Telomeres and Cancer. (ed. Krupp, G. & Parwaresch, R.) 205-222 (Kluwer Academic/Plenum, Georgetown, 2002).
7. Gray, J.T., Celander, D.W., Price, C.M. & Cech, T.R. Cloning and expression of genes for the Oxytricha telomere-binding protein: specific subunit interactions in the telomeric complex. Cell 67, 807-814 (1991).
8. Fang, G., Gray, J.T. & Cech, T.R. Oxytricha telomere-binding protein: separable DNA-binding and dimerization domains of the α-subunit. Genes Dev. 7, 870-882 (1993).
9. Simonsson, T. A substrate for telomerase. Trends Biochem. Sci. 28, 632-638 (2003).
10. Theobald, D.L. & Wuttke, D.S. Prediction of multiple tandem OB-fold domains in telomere end-binding proteins Pot1 and Cdc13. Structure 12, 1877-1879 (2004).
11. Baumann, P. & Cech, T.R. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292, 1171-1175 (2001).
12. Lei, M., Podell, E.R. & Cech, T.R. Structure of human POT1 bound to telomeric single-stranded DNA provides a model for chromosome end-protection. Nat. Struct. Mol. Biol. 11, 1223-1229 (2004).
13. Ye, J.Z. et al. POT1-interacting protein PIP1: a telomere length regulator that recruits POT1 to the TIN2/TRF1 complex. Genes Dev. 18, 1649-1654 (2004).
14. Liu, D. et al. PTOP interacts with POT1 and regulates its localization to telomeres. Nat. Cell Biol. 6, 673-680 (2004).
15. Wang, F. et al. The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 445, 506-510 (2007).
16. Xin, H. et al. TPP1 is a homologue of ciliate TEBP-β and interacts with POT1 to recruit telomerase. Nature 445, 559-562 (2007).
17. Griffith, J.D. et al. Mammalian telomeres end in a large duplex loop. Cell 97, 503-514 (1999).
18. de Lange, T. T-loops and the origin of telomeres. Nat. Rev. Mol. Cell Biol. 5, 323-329 (2004).
19. Gilson, E. & Geli, V. How telomeres are replicated. Nat. Rev. Mol. Cell Biol. 8, 825-838 (2007).
20. Schaffitzel, C. et al. In vitro generated antibodies specific for telomeric guaninequadruplex DNA react with Stylonychia lemnae macronuclei. Proc. Natl. Acad. Sci. USA 98, 8572-8577 (2001).
21. Paeschke, K., Simonsson, T., Postberg, J., Rhodes, D. & Lipps, H.J. Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo. Nat. Struct. Mol. Biol. 12, 847-854 (2005).
22. Rhodes, D. Telomere structure. in Telomeres Vol. 45 (eds. De Lange, T., Lundblad, V. & Blackburn, E.) (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2006).
23. Maizels, N. Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nat. Struct. Mol. Biol. 13, 1055-1059 (2006).
24. Fang, G. & Cech, T.R. The β subunit of Oxytricha telomere-binding protein promotes G- quartet formation by telomeric DNA. Cell 74, 875-885 (1993).
25. Hicke, B. et al. Phosphorylation of the Oxytricha telomere protein: possible cell cycle regulation. Nucleic Acids Res. 23, 1887-1893 (1995).
26. Postberg, J. et al. Association of the telomere-telomere binding protein-complex of hypotrichous ciliates with the nuclear matrix and dissociation during replication. J. Cell Sci. 114, 1861-1866 (2001).
27. Postberg, J., Alexandrova, O., Cremer, T. & Lipps, H.J. Exploiting nuclear duality of ciliates to analyse topological requirements for DNA replication and transcription. J. Cell Sci. 118, 3973-3983 (2005).
28. McCarroll, R.M. & Fangman, W.L. Time of replication of yeast centromeres and telomeres. Cell 54, 505-513 (1988).
29. Marcand, S., Brevet, V., Mann, C. & Gilson, E. Cell cycle restriction of telomere elongation. Curr. Biol. 10, 487-490 (2000).
30. Wellinger, R.J., Wolf, A.J. & Zakian, V.A. Saccharomyces telomeres acquire single-strand TG1-3 tails late in S phase. Cell 72, 51-60 (1993).
31. Cristofari, G. & Lingner, J. The Telomerase Ribonucleoprotein Particle. in Telomeres Vol. 45 (ed. De Lange, T., Lundblad, V. & Blackburn, E.) (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2006).
32. Oganesian, L., Moon, I.K., Bryan, T.M. & Jarstfer, M.B. Extension of G-quadruplex DNA by ciliate telomerase. EMBO J. 25, 1148-1159 (2006).
33. Zahler, A.M., Williamson, J.R., Cech, T.R. & Prescott, D.M. Inhibition of telomerase by G-quartet DNA structures. Nature 350, 718-720 (1991).
34. Lei, M., Podell, E.R., Baumann, P. & Cech, T.R. DNA self-recognition in the structure of Pot1 bound to telomeric single-stranded DNA. Nature 426, 198-203 (2003).
35. Zaug, A.J., Podell, E.R. & Cech, T.R. Human POT1 disrupts telomeric G-quadruplexes allowing telomerase extension in vitro. Proc. Natl. Acad. Sci. USA 102, 10864-10869 (2005).
36. Lei, M., Zaug, A.J., Podell, E.R. & Cech, T.R. Switching human telomerase on and off with hPOT1 protein in vitro. J. Biol. Chem. 280, 20449-20456 (2005).
37. Torigoe, H. Fission yeast telomeric DNA binding protein Pot1 has the ability to unfold tetraplex structure of telomeric DNA. Nucleosides Nucleotides Nucleic Acids 26, 1255-1260 (2007).
38. Jackson, D.A. Features of nuclear architecture that influence gene expression in higher eukaryotes: confronting the enigma of epigenetics. J. Cell Biochem. Suppl. 35, 69-77 (2000).
39. Froelich-Ammon, S.J., Dickinson, B.A., Bevilacqua, J.M., Schultz, S.C. & Cech, T.R. Modulation of telomerase activity by telomere DNA-binding proteins in Oxytricha. Genes Dev. 12, 1504-1514 (1998).
40. Paschka, A.G. et al. The use of RNAi to analyze gene function in spirotrichous ciliates. Eur. J. Protistol. 39, 449-454 (2003).
41. Indiani, C. & O'Donnell, M. The replication clamp-loading machine at work in the three domains of life. Nat. Rev. Mol. Cell Biol. 7, 751-761 (2006).
42. Kitagawa, M. et al. Butyrolactone I, a selective inhibitor of cdk2 and cdc2 kinase. Oncogene 8, 2425-2432 (1993).
43. Colgin, L.M., Baran, K., Baumann, P., Cech, T.R. & Reddel, R.R. Human POT1 facilitates telomere elongation by telomerase. Curr. Biol. 13, 942-946 (2003).
44. Armbruster, B.N. et al. Rescue of an hTERT mutant defective in telomere elongation by fusion with hPot1. Mol. Cell. Biol. 24, 3552-3561 (2004).
45. Loayza, D. & De Lange, T. POT1 as a terminal transducer of TRF1 telomere length control. Nature 423, 1013-1018 (2003).
46. 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).
47. Taggart, A.K., Teng, S.C. & Zakian, V.A. Est1p as a cell cycle-regulated activator of telomere-bound telomerase. Science 297, 1023-1026 (2002).
48. Pennock, E., Buckley, K. & Lundblad, V. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104, 387-396 (2001).
49. Tseng, S.F., Lin, J.J. & Teng, S.C. The telomerase-recruitment domain of the telomere binding protein Cdc13 is regulated by Mec1p/Tel1p-dependent phosphorylation. Nucleic Acids Res. 34, 6327-6336 (2006).
50. Frank, C.J., Hyde, M. & Greider, C.W. Regulation of telomere elongation by the cyclin-dependent kinase CDK1. Mol. Cell 24, 423-432 (2006).
51. Vodenicharov, M.D. & Wellinger, R.J. DNA degradation at unprotected telomeres in yeast is regulated by the CDK1 (Cdc28/Clb) cell-cycle kinase. Mol. Cell 24, 127-137 (2006).
52. Churikov, D. & Price, C.M. Pot1 and cell cycle progression cooperate in telomere length regulation. Nat. Struct. Mol. Biol. 15, 79-84 (2008).
53. Oganesian, L., Graham, M.E., Robinson, P.J. & Bryan, T.M. Telomerase recognizes G-quadruplex and linear DNA as distinct substrates. Biochemistry 46, 11279-11290 (2007).
54. Jackson, D.A., Yuan, J. & Cook, P.R. A gentle method for preparing cyto- and nucleo-skeletons and associated chromatin. J. Cell Sci. 90, 365-378 (1988).
55. Schaffitzel, C., Hanes, J., Jermutus, L. & Pluckthun, A. Ribosome display: an in vitro method for selection and evolution of antibodies from libraries. J. Immunol. Methods 231, 119-135 (1999).
56. Bryan, T.M., Sperger, J.M., Chapman, K.B. & Cech, T.R. Telomerase reverse transcriptase genes identified in Tetrahymena thermophila and Oxytricha trifallax. Proc. Natl. Acad. Sci. USA 95, 8479-8484 (1998).
57. Lingner, J., Hendrick, L.L. & Cech, T.R. Telomerase RNAs of different ciliates have a common secondary structure and a permuted template. Genes Dev. 8, 1984-1998 (1994).
58. Timmons, L. & Fire, A. Specific interference by ingested dsRNA. Nature 395, 854 (1998).