A telomerase-associated RecQ protein-like helicase resolves telomeric G-quadruplex structures during replication

Gene

Volumn 497, Issue 2, 2012, Pages 147-154

  Postberg, Jan ^a,c   Tsytlonok, Maksym ^a   Sparvoli, Daniela ^a   Rhodes, Daniela ^b   Lipps, Hans J ^a  

^a UNIVERSITY OF WITTEN HERDECKE   (Germany)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c Department of Paediatrics   (Germany)

Author keywords

Ciliates; Macronucleus; Replication band; Stylonychia lemnae; Tert

Indexed keywords

BINDING PROTEIN; GUANINE QUADRUPLEX; HELICASE; RECQ HELICASE; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TELOMERE END BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE S PHASE; CILIATE; CONTROLLED STUDY; DNA REPLICATION; DNA STRUCTURE; ENZYME ASSAY; ENZYME BINDING; ENZYME PHOSPHORYLATION; ESCHERICHIA COLI; EUKARYOTE; GENE EXPRESSION; GENE SILENCING; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; RNA INTERFERENCE; STYLONYCHIA LEMNAE; TELOMERE;

AMINO ACID SEQUENCE; DNA HELICASES; DNA REPLICATION; G-QUADRUPLEXES; GENOME; IMMUNOPRECIPITATION; MACRONUCLEUS; MOLECULAR SEQUENCE DATA; RECQ HELICASES; S PHASE; SPORADOTRICHINA; TELOMERASE; TELOMERE; TELOMERE-BINDING PROTEINS;

CILIOPHORA; EUKARYOTA; STYLONYCHIA LEMNAE;

EID: 84858293166     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2012.01.068     Document Type: Article

References (48)

1. Ammermann D., Steinbruck G., Berger L.v., Hennig W. The development of the macronucleus in the ciliated protozoan Stylonychia mytilus. Chromosoma 1974, 45:401-429.
2. Baumann P., Cech T.R. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 2001, 292:1171-1175.
3. Bennett R.J., Keck J.L. Structure and function of RecQ DNA helicases. Crit. Rev. Biochem. Mol. Biol. 2004, 39:79-97.
4. Bernstein D.A., Keck J.L. Conferring substrate specificity to DNA helicases: role of the RecQ HRDC domain. Structure 2005, 13:1173-1182.
5. Burge S., Parkinson G.N., Hazel P., Todd A.K., Neidle S. Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res. 2006, 34:5402-5415.
6. Curtis E.A., Landweber L.F. Evolution of gene scrambling in ciliate micronuclear genes. Ann. N. Y. Acad. Sci. 1999, 870:349-350.
7. de Lange T. T-loops and the origin of telomeres. Nat. Rev. Mol. Cell Biol. 2004, 5:323-329.
8. Dereeper A., et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 36:W465-W469.
9. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
10. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
11. 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. 1998, 12:1504-1514.
12. Gilson E., Geli V. How telomeres are replicated. Nat. Rev. Mol. Cell Biol. 2007, 8:825-838.
13. Griffith J.D., et al. Mammalian telomeres end in a large duplex loop. Cell 1999, 97:503-514.
14. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321.
15. Heyse K.S., Weber S.E., Lipps H.J. Histone modifications are specifically relocated during gene activation and nuclear differentiation. BMC Genomics 2009, 10:554.
16. Huber M.D., Duquette M.L., Shiels J.C., Maizels N. A conserved G4 DNA binding domain in RecQ family helicases. J. Mol. Biol. 2006, 358:1071-1080.
17. Huber M.D., Lee D.C., Maizels N. G4 DNA unwinding by BLM and Sgs1p: substrate specificity and substrate-specific inhibition. Nucleic Acids Res. 2002, 30:3954-3961.
18. Jones D.T., Taylor W.R., Thornton J.M. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 1992, 8:275-282.
19. Juranek S., Jönsson F., Maercker C., Lipps H.J. The telomeres of replicating macronuclear DNA molecules of the ciliate Stylonychia lemnae. Protistology 2000, 1:148-151.
20. Linger B.R., Price C.M. Conservation of telomere protein complexes: shuffling through evolution. Crit. Rev. Biochem. Mol. Biol. 2009, 44:434-446.
21. Lipps H.J., Rhodes D. G-quadruplex structures: in vivo evidence and function. Trends Cell Biol. 2009, 19:414-422.
22. Liu Z., et al. The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins. Structure 1999, 7:1557-1566.
23. Maizels N. Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nat. Struct. Mol. Biol. 2006, 13:1055-1059.
24. Oganesian L., Moon I.K., Bryan T.M., Jarstfer M.B. Extension of G-quadruplex DNA by ciliate telomerase. EMBO J. 2006, 25:1148-1159.
25. Paeschke K., Juranek S., Rhodes D., Lipps H.J. Cell cycle-dependent regulation of telomere tethering in the nucleus. Chromosome Res. 2008, 16:721-728.
26. Paeschke K., Juranek S., Simonsson T., Hempel A., Rhodes D., Lipps H.J. Telomerase recruitment by the telomere end binding protein-beta facilitates G-quadruplex DNA unfolding in ciliates. Nat. Struct. Mol. Biol. 2008, 15:598-604.
27. Paeschke K., McDonald K.R., Zakian V.A. Telomeres: structures in need of unwinding. FEBS Lett. 2010, 584:3760-3772.
28. 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. 2005, 12:847-854.
29. Parfrey L.W., Lahr D.J., Knoll A.H., Katz L.A. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:13624-13629.
30. Patel D.J., Phan A.T., Kuryavyi V. Human telomere, oncogenic promoter and 5'-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res. 2007, 35:7429-7455.
31. Petersen B., Petersen T.N., Andersen P., Nielsen M., Lundegaard C. A generic method for assignment of reliability scores applied to solvent accessibility predictions. BMC Struct. Biol. 2009, 9:51.
32. 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. 2005, 118:3973-3983.
33. Postberg J., Alexandrova O., Lipps H.J. Synthesis of pre-rRNA and mRNA is directed to a chromatin-poor compartment in the macronucleus of the spirotrichous ciliate Stylonychia lemnae. Chromosome Res. 2006, 14:161-175.
34. Postberg J., Heyse K., Cremer M., Cremer T., Lipps H.J. Spatial and temporal plasticity of chromatin during programmed DNA-reorganization in Stylonychia macronuclear development. Epigenetics Chromatin 2008, 1:3.
35. Price C. Ciliate Telomeres. Telomeres 2006, 465-493. Cold Spring Habor Laboratory Press, Cold Spring Habor, New York. T. Lange, V. Lundblad, E. Blackburn (Eds.).
36. Rasband W.S. ImageJ 1997-2004, National Institutes of Health, Bethesda, Maryland, USA.
37. Rhodes D., Giraldo R. Telomere structure and function. Curr. Opin. Struct. Biol. 1995, 5:311-322.
38. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
39. Schaffitzel C., Berger I., Postberg J., Hanes J., Lipps H.J., Pluckthun A. In vitro generated antibodies specific for telomeric guanine-quadruplex DNA react with Stylonychia lemnae macronuclei. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8572-8577.
40. Schaffitzel C., Postberg J., Paeschke K., Lipps H.J. Probing telomeric G-quadruplex DNA structures in cells with in vitro generated single-chain antibody fragments. Methods Mol. Biol. 2010, 608:159-181.
41. Sigrist C.J., et al. PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res. 2010, 38:D161-D166.
42. Sundquist W.I., Klug A. Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops. Nature 1989, 342:825-829.
43. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
44. Vega L.R., Mateyak M.K., Zakian V.A. Getting to the end: telomerase access in yeast and humans. Nat. Rev. Mol. Cell Biol. 2003, 4:948-959.
45. Wang F., et al. The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 2007, 445:506-510.
46. Wang Q., et al. G-quadruplex formation at the 3' end of telomere DNA inhibits its extension by telomerase, polymerase and unwinding by helicase. Nucleic Acids Res. 2011, 39:6229-6237.
47. Zahler A.M., Williamson J.R., Cech T.R., Prescott D.M. Inhibition of telomerase by G-quartet DNA structures. Nature 1991, 350:718-720.
48. Zhang M.L., et al. Yeast telomerase subunit Est1p has guanine quadruplex-promoting activity that is required for telomere elongation. Nat. Struct. Mol. Biol. 2010, 17:202-209.