d(CGGTGGT) forms an octameric parallel G-quadruplex via stacking of unusual G(:C):G(:C):G(:C):G(:C) octads

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Keywords :

mass spectrometry; nucleic acids; non-covalent; G-quadruplex; electrospray; FTICR

Abstract :

[en] Among non-canonical DNA secondary structures, G-quadruplexes are currently widely studied because of their probable involvement in many pivotal biological roles, and for their potential use in nanotechnology. The overall quadruplex scaffold can exhibit several morphologies through intramolecular or intermolecular organization of G-rich oligodeoxyribonucleic acid strands. In particular, several G-rich strands can form higher order assemblies by multimerization between several G-quadruplex units. Here, we report on the identification of a novel dimerization pathway. Our Nuclear magnetic resonance, circular dichroism, UV, gel electrophoresis and mass spectrometry studies on the DNA sequence dCGGTGGT demonstrate that this sequence forms an octamer when annealed in presence of K+ or NH4+ ions, through the 5′-5′ stacking of two tetramolecular G-quadruplex subunits via unusual G(:C):G(:C):G(:C):G(:C) octads.

Research Center/Unit :

Giga-Systems Biology and Chemical Biology - ULiège

Disciplines :

Chemistry
Biochemistry, biophysics & molecular biology

Author, co-author :

Borbone, Nicola; University of Naples Federico II, 80131 Naples, Italy

Amato, Jussara; University of Naples Federico II, 80131 Naples, Italy

Oliviero, Giorgia; University of Naples Federico II, 80131 Naples, Italy

D'Atri, Valentina; University of Naples Federico II, 80131 Naples, Italy

Gabelica, Valérie ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)

De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)

Piccialli, Gennaro; University of Naples Federico II, 80131 Naples, Italy

Mayol, Luciano; University of Naples Federico II, 80131 Naples, Italy

Language :

English

Title :

d(CGGTGGT) forms an octameric parallel G-quadruplex via stacking of unusual G(:C):G(:C):G(:C):G(:C) octads

Publication date :

2011

Journal title :

Nucleic Acids Research

ISSN :

0305-1048

eISSN :

1362-4962

Publisher :

Oxford University Press, Oxford, United Kingdom

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique

Available on ORBi :

since 04 July 2011

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Bibliography

Parkinson, G.N. (2006) Fundamentals of quadruplex structures. In Quadruplex Nucleic Acids. RSC Publishing, London, UK, pp. 1-30.
Patel, D.J., Phan, A.T. and Kuryavyi, V. (2007) Human telomere, oncogenic promoter and 50-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res., 35, 7429-7455.
Riou, J.-F., Gomez, D., Morjani, H. and Trentesaux, C. (2006) Quadruplex ligand recognition: biological aspects. In Quadruplex Nucleic Acids. RSC Publisher, London, UK, pp. 154-179.
Dexheimer, T.S., Fry, M. and Hurley, L.H. (2006) DNA quadruplexes and gene regulation. In Quadruplex Nucleic Acids. RSC Publisher, London, UK, pp. 180-207.
Huppert, J. (2006) Quadruplexes in the genome. In Quadruplex Nucleic Acids. RSC Publisher, London, UK, pp. 208-227.
Levesque, D., Beaudoin, J.-D., Roy, S. and Perreault, J.-P. (2007) In vitro selection and characterization of RNA aptamers binding thyroxine hormone. Biochem. J., 403, 129-138. (Pubitemid 46569874)
Pileur, F., Andreola, M.L., Dausse, E., Michel, J., Moreau, S., Yamada, H., Gaidamarov, S.A., Crouch, R.J., Toulmé, J.J. and Cazenave, C. (2003) Selective inhibitory DNA aptamers of the human RNase H1. Nucleic Acids Res., 31, 5776-5788. (Pubitemid 37448480)
Wang, K.Y., McCurdy, S., Shea, R.G., Swaminathan, S. and Bolton, P.H. (1993) A DNA aptamer which binds to and inhibits thrombin exhibits a new structural motif for DNA. Biochemistry, 32, 1899-1904. (Pubitemid 23086037)
Chou, S.-H., Chin, K.-H. and Wang, A.H.-J. (2005) DNA aptamers as potential anti-HIV agents. Trends Biochem. Sci., 30, 231-234. (Pubitemid 40693864)
Girvan, A.C., Teng, Y., Casson, L.K., Thomas, S.D., Ju?liger, S., Ball, M.W., Klein, J.B., Pierce, W.M., Barve, S.S. and Bates, P.J. (2006) AGRO100 inhibits activation of nuclear factor-kappaB (NF-kappaB) by forming a complex with NF-kappaB essential modulator (NEMO) and nucleolin. Mol. Cancer Ther., 5, 1790-1799. (Pubitemid 44323247)
Phan, A.T., Kuryavyi, V., Luu, K.N. and Patel, D.J. (2006) Structural diversity of G-quadruplex scaffolds. In Quadruplex Nucleic Acids. RSC Publisher, London, UK, pp. 81-99.
Bhavesh, N., Patel, P., Karthikeyan, S. and Hosur, R. (2004) Distinctive features in the structure and dynamics of the DNA repeat sequence GGCGGG. Biochem. Biophys. Res. Commun., 317, 625-633. (Pubitemid 38452529)
Oliviero, G., Amato, J., Borbone, N., Galeone, A., Varra, M., Piccialli, G. and Mayol, L. (2006) Synthesis and characterization of DNA quadruplexes containing T-tetrads formed by bunch-oligonucleotides. Biopolymers, 81, 194-201.
Searle, M.S., Williams, H.E.L., Gallagher, C.T., Grant, R.J. and Stevens, M.F.G. (2004) Structure and K+ion-dependent stability of a parallel-stranded DNA quadruplex containing a core A-tetrad. Org. Biomol. Chem., 2, 810-812.
Chen, J., Zhang, R.L., Min, J.M. and Zhang, L.H. (2002) Studies on the synthesis of a G-rich octaoligoisonucleotide (isoT)2(isoG)4-(isoT)2 by the phosphotriester approach and its formation of G-quartet structure. Nucleic Acids Res., 30, 3005-3014. (Pubitemid 34778161)
Virgilio, A., Esposito, V., Randazzo, A., Mayol, L. and Galeone, A. (2005) Effects of 8-methyl-20-deoxyadenosine incorporation into quadruplex forming oligodeoxyriboncleotides. Bioorg. Med. Chem., 13, 1037-1044. (Pubitemid 40164587)
Haider, S., Parkinson, G.N. and Neidle, S. (2008) Molecular dynamics and principal components analysis of human telomeric quadruplex multimers. Biophys. J., 95, 296-311.
Matsugami, A., Okuizumi, T., Uesugi, S. and Katahira, M. (2003) Intramolecular higher order packing of parallel quadruplexes comprising a G:G:G:G tetrad and a G(:A):G(:A):G(:A):G heptad of GGA triplet repeat DNA. J. Biol. Chem., 278, 28147-28153. (Pubitemid 36900013)
Xu, Y., Ishizuka, T., Kurabayashi, K. and Komiyama, M. (2009) Consecutive formation of G-quadruplexes in human telomeric-overhang DNA: a protective capping structure for telomere ends13. Angew. Chem, Int. Ed., 48, 7833-7836.
Kato, Y., Ohyama, T., Mita, H. and Yamamoto, Y. (2005) Dynamics and thermodynamics of dimerization of parallel G-quadruplexed DNA formed from d(TTAGn) (n=3-5). J. Am. Chem. Soc., 127, 9980-9981. (Pubitemid 40995425)
Sotoya, H., Matsugami, A., Ikeda, T., Ouhashi, K., Uesugi, S. and Katahira, M. (2004) Method for direct discrimination of intraand intermolecular hydrogen bonds, and characterization of the G(:A):G(:A):G(:A):G heptad, with scalar couplings across hydrogen bonds. Nucleic Acids Res., 32, 5113-5118. (Pubitemid 39445498)
Collie, G.W., Parkinson, G.N., Neidle, S., Rosu, F., De Pauw, E. and Gabelica, V. (2010) Electrospray mass spectrometry of telomeric RNA (TERRA) reveals the formation of stable multimeric G-quadruplex structures. J. Am. Chem. Soc., 132, 9328-9334.
Krishnan-Ghosh, Y., Liu, D. and Balasubramanian, S. (2004) Formation of an interlocked quadruplex dimer by d(GGGT). J. Am. Chem. Soc., 126, 11009-11016. (Pubitemid 39180585)
Guéin, A., De Cian, A., Gros, J., Lacroix, L. and Mergny, J.L. (2008) Sequence effects in single base loops for quadruplexes. Biochimie, 90, 686-696.
Gabelica, V., Rosu, F. and De Pauw, E. (2009) A Simple Method to Determine Electrospray Response Factors of Noncovalent Complexes. Anal. Chem., 81, 6708-6715.
Hwang, T.L. and Shaka, A.J. (1995) Water suppression that works. Excitation sculpting using arbitrary wave forms and pulsed field gradients. J. Magn. Reson. Ser. A, A112, 275-279.
Dalvit, C. (1998) Efficient multiple-solvent suppression for the study of the interactions of organic solvents with biomolecules. J. Biomol. NMR, 11, 437-444. (Pubitemid 128512224)
Wuthrich, K. (1986) NMR of Proteins and Nucleic Acids. John Wiley and Sons, New York, NY.
Hosur, R.V., Govil, G. and Miles, H.T. (1988) Application of two-dimensional NMR spectroscopy in the determination of solution conformation of nucleic acids. Magn. Reson. Chem, 26.
Patel, P.K. and Hosur, R.V. (1999) NMR observation of T-tetrads in a parallel stranded DNA quadruplex formed by Saccharomyces cerevisiae telomere repeats. Nucleic Acids Res., 27, 2457-2464.
Mergny, J.L., Phan, A.T. and Lacroix, L. (1998) Following G-quartet formation by UV-spectroscopy. FEBS Lett., 435, 74-78. (Pubitemid 28432018)
Mergny, J.-L., Li, J., Lacroix, L., Amrane, S. and Chaires, J.B. (2005) Thermal difference spectra: a specific signature for nucleic acid structures. Nucleic Acids Res., 33, e138.
Hardin, C.C., Perry, A.G. and White, K. (2001) Thermodynamic and kinetic characterization of the dissociation and assembly of quadruplex nucleic acids. Biopolymers (Nucleic Acid Sci.), 56, 147-194. (Pubitemid 33115750)
Mergny, J.-L., De Cian, A., Ghelab, A., Saccà, B. and Lacroix, L. (2005) Kinetics of tetramolecular quadruplexes. Nucleic Acids Res., 33, 81-94. (Pubitemid 40276930)
Masiero, S., Trotta, R., Pieraccini, S., De Tito, S., Perone, R., Randazzo, A. and Spada, G.P. (2010) A non-empirical chromophoric interpretation of CD spectra of DNA G-quadruplex structures. Org. Biomol. Chem., 8, 2683-2692.
Graziano, C., Masiero, S., Pieraccini, S., Lucarini, M. and Spada, G.P. (2008) A cation-directed switch of intermolecular spin-spin interaction of guanosine derivatives functionalized with open-shell units. Org. Lett., 10, 1739-1742.
Jin, R., Gaffney, B.L., Wang, C., Jones, R.A. and Breslauer, K.J. (1992) 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. USA, 89, 8832-8836.
Feigon, J., Koshlap, K.M. and Smith, F.W. (1995) 1H NMR spectroscopy of DNA triplexes and quadruplexes. Methods Enzymol., 261, 225-255.
Feigon, J. (1996) DNA triplexes, quadruplexes, and aptamers. Encyclopedia of NMR, 3, 1726-1731.
Mergny, J.-L., De Cian, A., Amrane, S. and Webba da Silva, M. (2006) Kinetics of double-chain reversals bridging contiguous quartets in tetramolecular quadruplexes. Nucleic Acids Res., 34, 2386-2397. (Pubitemid 43985676)
Matsugami, A., Ouhashi, K., Kanagawa, M., Liu, H., Kanagawa, S., Uesugi, S. and Katahira, M. (2001) An intramolecular quadruplex of (GGA)(4) triplet repeat DNA with a G:G:G:G tetrad and a G(:A):G(:A):G(:A):G heptad, and its dimeric interaction. J. Mol. Biol., 313, 255-269. (Pubitemid 33587186)
Rosu, F., Gabelica, V., Poncelet, H. and De Pauw, E. (2010) Tetramolecular G-quadruplex formation pathways studied by electrospray mass spectrometry. Nucleic Acids Res., 38, 5217-5225.
Sket, P. and Plavec, J. (2010) Tetramolecular DNA Quadruplexes in Solution: Insights into Structural Diversity and Cation Movement. J. Am. Chem. Soc., 132, 12724-12732.