Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1995 May 25;23(10):1722–1728. doi: 10.1093/nar/23.10.1722

Spectroscopic studies of chimeric DNA-RNA and RNA 29-base intramolecular triple helices.

J Liquier 1, E Taillandier 1, R Klinck 1, E Guittet 1, C Gouyette 1, T Huynh-Dinh 1
PMCID: PMC306928  PMID: 7540286

Abstract

Fourier transform infrared (FTIR), UV absorption and exchangeable proton NMR spectroscopies have been used to study the formation and stability of two intramolecular pH-dependent triple helices composed by a chimeric 29mer DNA-RNA (DNA double strand and RNA third strand) or by the analogous 29mer RNA. In both cases decrease of pH induces formation of a triple helical structure containing either rU*dA.dT and rC+*dG.dC or rU*rA.rU and rC+*rG.rC triplets. FTIR spectroscopy shows that exclusively N-type sugars are present in the triple helix formed by the 29mer RNA while both N- and S-type sugars are detected in the case of the chimeric 29mer DNA-RNA triple helix. Triple helix formation with the third strand RNA and the duplex as DNA appears to be associated with the conversion of the duplex part from a B-form secondary structure to one which contains partly A-form sugars. Thermal denaturation experiments followed by UV spectroscopy show that a major stabilization occurs upon formation of the triple helices. Monophasic melting curves indicate a simultaneous disruption of the Hoogsteen and Watson-Crick hydrogen bonds in the intramolecular triplexes when the temperature is increased. This is in agreement with imino proton NMR spectra recorded as a function of temperature. Comparison with experiments concerning intermolecular triplexes of identical base and sugar composition shows the important role played by the two tetrameric loops in the stabilization of the intramolecular triple helices studied.

Full text

PDF
1722

Selected References

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

  1. Adam S., Bourtayre P., Liquier J., Taillandier E. Interaction of transition metal ions with Z form poly d(A-C).poly d(G-T) and poly d(A-T) studied by I.R. spectroscopy. Nucleic Acids Res. 1986 Apr 25;14(8):3501–3513. doi: 10.1093/nar/14.8.3501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akhebat A., Dagneaux C., Liquier J., Taillandier E. Triple helical polynucleotidic structures: an FTIR study of the C+ .G. Ctriplet. J Biomol Struct Dyn. 1992 Dec;10(3):577–588. doi: 10.1080/07391102.1992.10508669. [DOI] [PubMed] [Google Scholar]
  3. Arnott S., Bond P. J., Selsing E., Smith P. J. Models of triple-stranded polynucleotides with optimised stereochemistry. Nucleic Acids Res. 1976 Oct;3(10):2459–2470. doi: 10.1093/nar/3.10.2459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Arnott S., Selsing E. Structures for the polynucleotide complexes poly(dA) with poly (dT) and poly(dT) with poly(dA) with poly (dT). J Mol Biol. 1974 Sep 15;88(2):509–521. doi: 10.1016/0022-2836(74)90498-7. [DOI] [PubMed] [Google Scholar]
  5. Escudé C., François J. C., Sun J. S., Ott G., Sprinzl M., Garestier T., Hélène C. Stability of triple helices containing RNA and DNA strands: experimental and molecular modeling studies. Nucleic Acids Res. 1993 Dec 11;21(24):5547–5553. doi: 10.1093/nar/21.24.5547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Grigoriev M., Praseuth D., Guieysse A. L., Robin P., Thuong N. T., Hélène C., Harel-Bellan A. Inhibition of interleukin-2 receptor alpha-subunit gene expression by oligonucleotide-directed triple helix formation. C R Acad Sci III. 1993;316(5):492–495. [PubMed] [Google Scholar]
  7. Haasnoot C. A., Hilbers C. W., van der Marel G. A., van Boom J. H., Singh U. C., Pattabiraman N., Kollman P. A. On loop folding in nucleic acid hairpin-type structures. J Biomol Struct Dyn. 1986 Apr;3(5):843–857. doi: 10.1080/07391102.1986.10508468. [DOI] [PubMed] [Google Scholar]
  8. Han H., Dervan P. B. Different conformational families of pyrimidine.purine.pyrimidine triple helices depending on backbone composition. Nucleic Acids Res. 1994 Jul 25;22(14):2837–2844. doi: 10.1093/nar/22.14.2837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Han H., Dervan P. B. Sequence-specific recognition of double helical RNA and RNA.DNA by triple helix formation. Proc Natl Acad Sci U S A. 1993 May 1;90(9):3806–3810. doi: 10.1073/pnas.90.9.3806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Howard F. B., Miles H. T., Liu K., Frazier J., Raghunathan G., Sasisekharan V. Structure of d(T)n.d(A)n.d(T)n: the DNA triple helix has B-form geometry with C2'-endo sugar pucker. Biochemistry. 1992 Nov 10;31(44):10671–10677. doi: 10.1021/bi00159a005. [DOI] [PubMed] [Google Scholar]
  11. Kan L. S., Callahan D. E., Trapane T. L., Miller P. S., Ts'o P. O., Huang D. H. Proton NMR and optical spectroscopic studies on the DNA triplex formed by d-A-(G-A)7-G and d-C-(T-C)7-T. J Biomol Struct Dyn. 1991 Apr;8(5):911–933. doi: 10.1080/07391102.1991.10507857. [DOI] [PubMed] [Google Scholar]
  12. Klinck R., Guittet E., Liquier J., Taillandier E., Gouyette C., Huynh-Dinh T. Spectroscopic evidence for an intramolecular RNA triple helix. FEBS Lett. 1994 Dec 5;355(3):297–300. doi: 10.1016/0014-5793(94)01228-8. [DOI] [PubMed] [Google Scholar]
  13. Le Doan T., Perrouault L., Praseuth D., Habhoub N., Decout J. L., Thuong N. T., Lhomme J., Hélène C. Sequence-specific recognition, photocrosslinking and cleavage of the DNA double helix by an oligo-[alpha]-thymidylate covalently linked to an azidoproflavine derivative. Nucleic Acids Res. 1987 Oct 12;15(19):7749–7760. doi: 10.1093/nar/15.19.7749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Liquier J., Coffinier P., Firon M., Taillandier E. Triple helical polynucleotidic structures: sugar conformations determined by FTIR spectroscopy. J Biomol Struct Dyn. 1991 Dec;9(3):437–445. doi: 10.1080/07391102.1991.10507927. [DOI] [PubMed] [Google Scholar]
  15. Liquier J., Letellier R., Dagneaux C., Ouali M., Morvan F., Raynier B., Imbach J. L., Taillandier E. Triple helix formation by alpha-oligodeoxynucleotides: a vibrational spectroscopy and molecular modeling study. Biochemistry. 1993 Oct 12;32(40):10591–10598. doi: 10.1021/bi00091a008. [DOI] [PubMed] [Google Scholar]
  16. Lyamichev V. I., Mirkin S. M., Frank-Kamenetskii M. D., Cantor C. R. A stable complex between homopyrimidine oligomers and the homologous regions of duplex DNAs. Nucleic Acids Res. 1988 Mar 25;16(5):2165–2178. doi: 10.1093/nar/16.5.2165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Macaya R. F., Gilbert D. E., Malek S., Sinsheimer J. S., Feigon J. Structure and stability of X.G.C mismatches in the third strand of intramolecular triplexes. Science. 1991 Oct 11;254(5029):270–274. doi: 10.1126/science.254.5029.270. [DOI] [PubMed] [Google Scholar]
  18. Macaya R., Wang E., Schultze P., Sklenár V., Feigon J. Proton nuclear magnetic resonance assignments and structural characterization of an intramolecular DNA triplex. J Mol Biol. 1992 Jun 5;225(3):755–773. doi: 10.1016/0022-2836(92)90399-5. [DOI] [PubMed] [Google Scholar]
  19. Maher L. J., 3rd, Wold B., Dervan P. B. Inhibition of DNA binding proteins by oligonucleotide-directed triple helix formation. Science. 1989 Aug 18;245(4919):725–730. doi: 10.1126/science.2549631. [DOI] [PubMed] [Google Scholar]
  20. Mergny J. L., Collier D., Rougée M., Montenay-Garestier T., Hélène C. Intercalation of ethidium bromide into a triple-stranded oligonucleotide. Nucleic Acids Res. 1991 Apr 11;19(7):1521–1526. doi: 10.1093/nar/19.7.1521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Miles H. T., Frazier J. Infrared study of helix strandedness in the poly A-poly U system. Biochem Biophys Res Commun. 1964;14:21–28. doi: 10.1016/0006-291x(63)90204-3. [DOI] [PubMed] [Google Scholar]
  22. Moser H. E., Dervan P. B. Sequence-specific cleavage of double helical DNA by triple helix formation. Science. 1987 Oct 30;238(4827):645–650. doi: 10.1126/science.3118463. [DOI] [PubMed] [Google Scholar]
  23. Ohms J., Ackermann T. Thermodynamics of double- and triple-helical aggregates formed by self-complementary oligoribonucleotides of the type rAxUy. Biochemistry. 1990 Jun 5;29(22):5237–5244. doi: 10.1021/bi00474a004. [DOI] [PubMed] [Google Scholar]
  24. Ouali M., Letellier R., Adnet F., Liquier J., Sun J. S., Lavery R., Taillandier E. A possible family of B-like triple helix structures: comparison with the Arnott A-like triple helix. Biochemistry. 1993 Mar 2;32(8):2098–2103. doi: 10.1021/bi00059a030. [DOI] [PubMed] [Google Scholar]
  25. Parniewski P., Kwinkowski M., Wilk A., Klysik J. Dam methyltransferase sites located within the loop region of the oligopurine-oligopyrimidine sequences capable of forming H-DNA are undermethylated in vivo. Nucleic Acids Res. 1990 Feb 11;18(3):605–611. doi: 10.1093/nar/18.3.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pilch D. S., Levenson C., Shafer R. H. Structural analysis of the (dA)10.2(dT)10 triple helix. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1942–1946. doi: 10.1073/pnas.87.5.1942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Postel E. H., Flint S. J., Kessler D. J., Hogan M. E. Evidence that a triplex-forming oligodeoxyribonucleotide binds to the c-myc promoter in HeLa cells, thereby reducing c-myc mRNA levels. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8227–8231. doi: 10.1073/pnas.88.18.8227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rajagopal P., Feigon J. Triple-strand formation in the homopurine:homopyrimidine DNA oligonucleotides d(G-A)4 and d(T-C)4. Nature. 1989 Jun 22;339(6226):637–640. doi: 10.1038/339637a0. [DOI] [PubMed] [Google Scholar]
  29. Roberts R. W., Crothers D. M. Stability and properties of double and triple helices: dramatic effects of RNA or DNA backbone composition. Science. 1992 Nov 27;258(5087):1463–1466. doi: 10.1126/science.1279808. [DOI] [PubMed] [Google Scholar]
  30. Rougée M., Faucon B., Mergny J. L., Barcelo F., Giovannangeli C., Garestier T., Hélène C. Kinetics and thermodynamics of triple-helix formation: effects of ionic strength and mismatches. Biochemistry. 1992 Sep 29;31(38):9269–9278. doi: 10.1021/bi00153a021. [DOI] [PubMed] [Google Scholar]
  31. Semerad C. L., Maher L. J., 3rd Exclusion of RNA strands from a purine motif triple helix. Nucleic Acids Res. 1994 Dec 11;22(24):5321–5325. doi: 10.1093/nar/22.24.5321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sklenár V., Feigon J. Formation of a stable triplex from a single DNA strand. Nature. 1990 Jun 28;345(6278):836–838. doi: 10.1038/345836a0. [DOI] [PubMed] [Google Scholar]
  33. Strobel S. A., Dervan P. B. Single-site enzymatic cleavage of yeast genomic DNA mediated by triple helix formation. Nature. 1991 Mar 14;350(6314):172–174. doi: 10.1038/350172a0. [DOI] [PubMed] [Google Scholar]
  34. Taillandier E., Liquier J. Infrared spectroscopy of DNA. Methods Enzymol. 1992;211:307–335. doi: 10.1016/0076-6879(92)11018-e. [DOI] [PubMed] [Google Scholar]
  35. Wang E., Malek S., Feigon J. Structure of a G.T.A triplet in an intramolecular DNA triplex. Biochemistry. 1992 May 26;31(20):4838–4846. doi: 10.1021/bi00135a015. [DOI] [PubMed] [Google Scholar]
  36. Xodo L. E., Manzini G., Quadrifoglio F., van der Marel G. A., van Boom J. H. Effect of 5-methylcytosine on the stability of triple-stranded DNA--a thermodynamic study. Nucleic Acids Res. 1991 Oct 25;19(20):5625–5631. doi: 10.1093/nar/19.20.5625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Xodo L. E., Manzini G., Quadrifoglio F., van der Marel G. A., van Boom J. H. Oligodeoxynucleotide folding in solution: loop size and stability of B-hairpins. Biochemistry. 1988 Aug 23;27(17):6321–6326. doi: 10.1021/bi00417a018. [DOI] [PubMed] [Google Scholar]
  38. de los Santos C., Rosen M., Patel D. NMR studies of DNA (R+)n.(Y-)n.(Y+)n triple helices in solution: imino and amino proton markers of T.A.T and C.G.C+ base-triple formation. Biochemistry. 1989 Sep 5;28(18):7282–7289. doi: 10.1021/bi00444a021. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES