Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Aug 2;91(16):7658–7662. doi: 10.1073/pnas.91.16.7658

Promotion of parallel DNA quadruplexes by a yeast telomere binding protein: a circular dichroism study.

R Giraldo 1, M Suzuki 1, L Chapman 1, D Rhodes 1
PMCID: PMC44461  PMID: 8052638

Abstract

Repressor-activator protein 1 (RAP1) has an essential role in the maintenance of yeast telomeres. Yeast telomeric DNA consists of simple repeated G-rich sequences that are bound by RAP1. We have found that RAP1, in addition to its known binding activity for double-stranded DNA, interacts with the G-rich strand containing guanine base (G)-tetrads. We show here using circular dichroism spectroscopy that RAP1 promotes the formation of one particular type of DNA quadruplex, parallel G4-DNA. Furthermore, RAP1 is able to bind to both preformed parallel and antiparallel DNA quadruplexes. These results have implications for the possible use of DNA quadruplexes in telomere-telomere association in vivo.

Full text

PDF
7658

Images in this article

7660Image
on p.7660

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aboul-ela F., Murchie A. I., Lilley D. M. NMR study of parallel-stranded tetraplex formation by the hexadeoxynucleotide d(TG4T). Nature. 1992 Nov 19;360(6401):280–282. doi: 10.1038/360280a0. [DOI] [PubMed] [Google Scholar]
  2. Balagurumoorthy P., Brahmachari S. K., Mohanty D., Bansal M., Sasisekharan V. Hairpin and parallel quartet structures for telomeric sequences. Nucleic Acids Res. 1992 Aug 11;20(15):4061–4067. doi: 10.1093/nar/20.15.4061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Fang G., Cech T. R. Characterization of a G-quartet formation reaction promoted by the beta-subunit of the Oxytricha telomere-binding protein. Biochemistry. 1993 Nov 2;32(43):11646–11657. doi: 10.1021/bi00094a022. [DOI] [PubMed] [Google Scholar]
  4. Fang G., Cech T. R. The beta subunit of Oxytricha telomere-binding protein promotes G-quartet formation by telomeric DNA. Cell. 1993 Sep 10;74(5):875–885. doi: 10.1016/0092-8674(93)90467-5. [DOI] [PubMed] [Google Scholar]
  5. Gilson E., Roberge M., Giraldo R., Rhodes D., Gasser S. M. Distortion of the DNA double helix by RAP1 at silencers and multiple telomeric binding sites. J Mol Biol. 1993 May 20;231(2):293–310. doi: 10.1006/jmbi.1993.1283. [DOI] [PubMed] [Google Scholar]
  6. Giraldo R., Rhodes D. The yeast telomere-binding protein RAP1 binds to and promotes the formation of DNA quadruplexes in telomeric DNA. EMBO J. 1994 May 15;13(10):2411–2420. doi: 10.1002/j.1460-2075.1994.tb06526.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Guschlbauer W., Chantot J. F., Thiele D. Four-stranded nucleic acid structures 25 years later: from guanosine gels to telomer DNA. J Biomol Struct Dyn. 1990 Dec;8(3):491–511. doi: 10.1080/07391102.1990.10507825. [DOI] [PubMed] [Google Scholar]
  8. Henry Y. A., Chambers A., Tsang J. S., Kingsman A. J., Kingsman S. M. Characterisation of the DNA binding domain of the yeast RAP1 protein. Nucleic Acids Res. 1990 May 11;18(9):2617–2623. doi: 10.1093/nar/18.9.2617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jin R., Gaffney B. L., Wang C., Jones R. A., Breslauer K. J. Thermodynamics and structure of a DNA tetraplex: a spectroscopic and calorimetric study of the tetramolecular complexes of d(TG3T) and d(TG3T2G3T). Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8832–8836. doi: 10.1073/pnas.89.18.8832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kang C., Zhang X., Ratliff R., Moyzis R., Rich A. Crystal structure of four-stranded Oxytricha telomeric DNA. Nature. 1992 Mar 12;356(6365):126–131. doi: 10.1038/356126a0. [DOI] [PubMed] [Google Scholar]
  11. Klein F., Laroche T., Cardenas M. E., Hofmann J. F., Schweizer D., Gasser S. M. Localization of RAP1 and topoisomerase II in nuclei and meiotic chromosomes of yeast. J Cell Biol. 1992 Jun;117(5):935–948. doi: 10.1083/jcb.117.5.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Liu Z., Frantz J. D., Gilbert W., Tye B. K. Identification and characterization of a nuclease activity specific for G4 tetrastranded DNA. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3157–3161. doi: 10.1073/pnas.90.8.3157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lustig A. J., Kurtz S., Shore D. Involvement of the silencer and UAS binding protein RAP1 in regulation of telomere length. Science. 1990 Oct 26;250(4980):549–553. doi: 10.1126/science.2237406. [DOI] [PubMed] [Google Scholar]
  14. Scaria P. V., Shire S. J., Shafer R. H. Quadruplex structure of d(G3T4G3) stabilized by K+ or Na+ is an asymmetric hairpin dimer. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10336–10340. doi: 10.1073/pnas.89.21.10336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Schierer T., Henderson E. A protein from Tetrahymena thermophila that specifically binds parallel-stranded G4-DNA. Biochemistry. 1994 Mar 1;33(8):2240–2246. doi: 10.1021/bi00174a034. [DOI] [PubMed] [Google Scholar]
  16. Sen D., Gilbert W. A sodium-potassium switch in the formation of four-stranded G4-DNA. Nature. 1990 Mar 29;344(6265):410–414. doi: 10.1038/344410a0. [DOI] [PubMed] [Google Scholar]
  17. Shore D., Nasmyth K. Purification and cloning of a DNA binding protein from yeast that binds to both silencer and activator elements. Cell. 1987 Dec 4;51(5):721–732. doi: 10.1016/0092-8674(87)90095-x. [DOI] [PubMed] [Google Scholar]
  18. Smith F. W., Feigon J. Quadruplex structure of Oxytricha telomeric DNA oligonucleotides. Nature. 1992 Mar 12;356(6365):164–168. doi: 10.1038/356164a0. [DOI] [PubMed] [Google Scholar]
  19. Sundquist W. I., Klug A. Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops. Nature. 1989 Dec 14;342(6251):825–829. doi: 10.1038/342825a0. [DOI] [PubMed] [Google Scholar]
  20. Venczel E. A., Sen D. Parallel and antiparallel G-DNA structures from a complex telomeric sequence. Biochemistry. 1993 Jun 22;32(24):6220–6228. doi: 10.1021/bi00075a015. [DOI] [PubMed] [Google Scholar]
  21. 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. 1992 Sep 8;31(35):8112–8119. doi: 10.1021/bi00150a002. [DOI] [PubMed] [Google Scholar]
  22. Wellinger R. J., Wolf A. J., Zakian V. A. Saccharomyces telomeres acquire single-strand TG1-3 tails late in S phase. Cell. 1993 Jan 15;72(1):51–60. doi: 10.1016/0092-8674(93)90049-v. [DOI] [PubMed] [Google Scholar]
  23. Williamson J. R., Raghuraman M. K., Cech T. R. Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell. 1989 Dec 1;59(5):871–880. doi: 10.1016/0092-8674(89)90610-7. [DOI] [PubMed] [Google Scholar]
  24. Zahler A. M., Williamson J. R., Cech T. R., Prescott D. M. Inhibition of telomerase by G-quartet DNA structures. Nature. 1991 Apr 25;350(6320):718–720. doi: 10.1038/350718a0. [DOI] [PubMed] [Google Scholar]
  25. Zakian V. A. Structure and function of telomeres. Annu Rev Genet. 1989;23:579–604. doi: 10.1146/annurev.ge.23.120189.003051. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES