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Analysis of branched nucleic acid structure using comparative gel electrophoresis

Published online by Cambridge University Press:  29 August 2008

David M. J. Lilley
David M. J. Lilley*
Affiliation:
Cancer Research UK Nucleic Acid Structure Research Group, University of Dundee, Dundee, UK
*
*Professor D. M. J. Lilley, Cancer Research UK Nucleic Acid Structure Research Group, University of Dundee, MSI/WTB Complex, Dundee DD1 5EH, UK. Tel.: +44 1382 384 243; Fax: +44 1382 385 893; Email: d.m.j.lilley@dundee.ac.uk
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Abstract

Electrophoresis in polyacrylamide gels provides a simple yet powerful means of analyzing the relative disposition of helical arms in branched nucleic acids. The electrophoretic mobility of DNA or RNA with a central discontinuity is determined by the angle subtended between the arms radiating from the branchpoint. In a multi-helical branchpoint, comparative gel electrophoresis can provide a relative measure of all the inter-helical angles and thus the shape and symmetry of the molecule. Using the long–short arm approach, the electrophoretic mobility of all the species with two helical arms that are longer than all others is compared. This can be done as a function of conditions, allowing the analysis of ion-dependent folding of branched DNA and RNA species. Notable successes for the technique include the four-way (Holliday) junction in DNA and helical junctions in functionally significant RNA species such as ribozymes. Many of these structures have subsequently been proved correct by crystallography or other methods, up to 10 years later in the case of the Holliday junction. Just as important, the technique has not failed to date. Comparative gel electrophoresis can provide a window on both fast and slow conformational equilibria such as conformer exchange in four-way DNA junctions. But perhaps the biggest test of the approach has been to deduce the structures of complexes of four-way DNA junctions with proteins. Two recent crystallographic structures show that the global structures were correctly deduced by electrophoresis, proving the worth of the method even in these rather complex systems. Comparative gel electrophoresis is a robust method for the analysis of branched nucleic acids and their complexes.

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Review Article
Information
Quarterly Reviews of Biophysics , Volume 41 , Issue 1 , February 2008 , pp. 1 - 39
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Copyright © 2008 Cambridge University Press

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References

Ban, N., Nissen, P., Hansen, J., Moore, P. B. & Steitz, T. A. (2000). The complete atomic structure of the large ribosomal subunit at 2·4 Å resolution. Science 289, 905–920.CrossRefGoogle ScholarPubMed
Barkema, G. T., Marko, J. F. & Widom, B. (1994). Electrophoresis of charged polymers: simulation and scaling in a lattice model of reptation. Physical Review. E, Statistical Physics, Plasmas, Fluids, and Related Interdisciplinary Topics 49, 5303–5309.CrossRefGoogle Scholar
Bassi, G., Møllegaard, N. E., Murchie, A. I. H., von Kitzing, E. & Lilley, D. M. J. (1995). Ionic interactions and the global conformations of the hammerhead ribozyme. Nature Structural Biology 2, 45–55.CrossRefGoogle ScholarPubMed
Bassi, G. S., Møllegaard, N. E., Murchie, A. I. H. & Lilley, D. M. J. (1999). RNA folding and misfolding of the hammerhead ribozyme. Biochemistry 38, 3345–3354.CrossRefGoogle ScholarPubMed
Bassi, G. S., Murchie, A. I. H. & Lilley, D. M. J. (1996). The ion-induced folding of the hammerhead ribozyme: core sequence changes that perturb folding into the active conformation. RNA 2, 756–768.Google ScholarPubMed
Bassi, G. S., Murchie, A. I. H., Walter, F., Clegg, R. M. & Lilley, D. M. J. (1997). Ion-induced folding of the hammerhead ribozyme: a fluorescence resonance energy transfer study. EMBO Journal 16, 7481–7489.CrossRefGoogle ScholarPubMed
Beattie, T. L., Olive, J. E. & Collins, R. A. (1995). A secondary-structure model for the self-cleaving region of Neurospora VS RNA. Proceedings of the National Academy of Sciences USA 92, 4686–4690.CrossRefGoogle ScholarPubMed
Bennett, R. J. & West, S. C. (1995). Structural analysis of the RuvC–Holliday junction complex reveals an unfolded junction. Journal of Molecular Biology 252, 213–226.CrossRefGoogle ScholarPubMed
Bhattacharyya, A. & Lilley, D. M. J. (1989). The contrasting structures of mismatched DNA sequences containing looped-out bases (bulges) and multiple mismatches (bubbles). Nucleic Acids Research 17, 6821–6840.CrossRefGoogle ScholarPubMed
Bhattacharyya, A., Murchie, A. I. H. & Lilley, D. M. J. (1990). RNA bulges and the helical periodicity of double-stranded RNA. Nature 343, 484–487.CrossRefGoogle ScholarPubMed
Biertümpfel, C., Yang, W. & Suck, D. (2007). Crystal structure of T4 endonuclease VII resolving a Holliday junction. Nature 449, 616–620.CrossRefGoogle ScholarPubMed
Canny, M. D., Jucker, F. M., Kellogg, E., Khvorova, A., Jayasena, S. D. & Pardi, A. (2004). Fast cleavage kinetics of a natural hammerhead ribozyme. Journal American Chemical Society 126, 10848–10849.CrossRefGoogle ScholarPubMed
Cate, J. H., Gooding, A. R., Podell, E., Zhou, K. H., Golden, B. L., Kundrot, C. E., Cech, T. R. & Doudna, J. A. (1996). Crystal structure of a group I ribozyme domain: principles of RNA packing. Science 273, 1678–1685.CrossRefGoogle ScholarPubMed
Challberg, S. S. & Englund, P. T. (1980). Heterogeneity of minicircles in kinetoplast DNA of Leishmania tarentolae. Journal of Molecular Biology 138, 447–472.CrossRefGoogle ScholarPubMed
Clegg, R. M., Murchie, A. I. H., Zechel, A., Carlberg, C., Diekmann, S. & Lilley, D. M. J. (1992). Fluorescence resonance energy transfer analysis of the structure of the four-way DNA junction. Biochemistry 31, 4846–4856.CrossRefGoogle ScholarPubMed
Clegg, R. M., Murchie, A. I. H., Zechel, A. & Lilley, D. M. J. (1994). The solution structure of the four-way DNA junction at low salt concentration; a fluorescence resonance energy transfer analysis. Biophysics Journal 66, 99–109.CrossRefGoogle ScholarPubMed
Cooper, J. P. & Hagerman, P. J. (1987). Gel electrophoretic analysis of the geometry of a DNA four-way junction. Journal of Molecular Biology 198, 711–719.CrossRefGoogle ScholarPubMed
Cooper, J. P. & Hagerman, P. J. (1989). Geometry of a branched DNA structure in solution. Proceedings of the National Academy of Sciences USA 86, 7336–7340.CrossRefGoogle ScholarPubMed
Déclais, A.-C., Fogg, J. M., Freeman, A., Coste, F., Hadden, J. M., Phillips, S. E. V. & Lilley, D. M. J. (2003). The complex between a four-way DNA junction and T7 endonuclease I. EMBO Journal 22, 1398–1409.CrossRefGoogle ScholarPubMed
Déclais, A.-C. & Lilley, D. M. J. (2000). Extensive central disruption of a four-way junction on binding CCE1 resolving enzyme. Journal of Molecular Biology 296, 421–433.CrossRefGoogle ScholarPubMed
Déclais, A. C., Liu, J., Freeman, A. D. J. & Lilley, D. M. J. (2006). Structural recognition between a four-way DNA junction and a resolving enzyme. Journal of Molecular Biology 359, 1261–1276.CrossRefGoogle Scholar
De Gennes, P. G. (1971). Reptation of a polymer chain in the presence of fixed obstacles. Journal of Chemical Physics 55, 572–578.CrossRefGoogle Scholar
Deutsch, J. M. (1988). Theoretical studies of DNA during gel electrophoresis. Science 240, 922–924.CrossRefGoogle ScholarPubMed
Diekmann, S. & Wang, J. C. (1985). On the sequence determinants and flexibility of the kinetoplast DNA fragment with abnormal gel electrophoretic mobilities. Journal of Molecular Biology 186, 1–11.CrossRefGoogle ScholarPubMed
Drak, J. & Crothers, D. M. (1991). Helical repeat and chirality effects on DNA gel electrophoretic mobility. Proceedings of the National Academy of Sciences USA 88, 3074–3078.CrossRefGoogle ScholarPubMed
Duckett, D. R. & Lilley, D. M. J. (1990). The three-way DNA junction is a Y-shaped molecule in which there is no helix–helix stacking. EMBO Journal 9, 1659–1664.CrossRefGoogle ScholarPubMed
Duckett, D. R., Murchie, A. I. H., Diekmann, S., von Kitzing, E., Kemper, B. & Lilley, D. M. J. (1988). The structure of the Holliday junction and its resolution. Cell 55, 79–89.CrossRefGoogle ScholarPubMed
Duckett, D. R., Murchie, A. I. H. & Lilley, D. M. J. (1995). The global folding of four-way helical junctions in RNA, including that in U1 snRNA. Cell 83, 1027–1036.CrossRefGoogle ScholarPubMed
Duke, T. A., Semenov, A. N. & Viovy, J. L. (1992). Mobility of a reptating polymer. Physical Review Letters 69, 3260–3263.CrossRefGoogle ScholarPubMed
Eichman, B. F., Vargason, J. M., Mooers, B. H. M. & Ho, P. S. (2000). The Holliday junction in an inverted repeat DNA sequence: sequence effects on the structure of four-way junctions. Proceedings of the National Academy of Sciences USA 97, 3971–3976.CrossRefGoogle Scholar
Feig, A. L., Scott, W. G. & Uhlenbeck, O. C. (1998). Inhibition of the hammerhead ribozyme cleavage reaction by site-specific binding of Tb(III). Science 279, 81–84.CrossRefGoogle Scholar
Fogg, J. M., Kvaratskhelia, M., White, M. F. & Lilley, D. M. J. (2001). Distortion of DNA junctions imposed by the binding of resolving enzymes: a fluorescence study. Journal of Molecular Biology 313, 751–764.CrossRefGoogle ScholarPubMed
Gohlke, C., Murchie, A. I. H., Lilley, D. M. J. & Clegg, R. M. (1994). The kinking of DNA and RNA helices by bulged nucleotides observed by fluorescence resonance energy transfer. Proceedings of the National Academy of Sciences USA 91, 11660–11664.CrossRefGoogle ScholarPubMed
Goody, T. A., Lilley, D. M. J. & Norman, D. G. (2004). The chirality of a four-way helical junction in RNA. Journal of the American Chemical Society 126, 4126–4127.CrossRefGoogle ScholarPubMed
Goody, T. A., Melcher, S. E., Norman, D. G. & Lilley, D. M. J. (2003). The kink-turn motif in RNA is dimorphic and metal ion dependent. RNA 10, 254–264.CrossRefGoogle Scholar
Gough, G. W. & Lilley, D. M. J. (1985). DNA bending induced by cruciform formation. Nature 313, 154–156.CrossRefGoogle ScholarPubMed
Grainger, R. J., Murchie, A. I. H. & Lilley, D. M. J. (1998). Exchange between stacking conformers in a four-way DNA junction. Biochemistry 37, 23–32.CrossRefGoogle Scholar
Grainger, R. J., Murchie, A. I. H., Norman, D. G. & Lilley, D. M. J. (1997). Severe axial bending of RNA induced by the U1A binding element present in the 3′ untranslated region of the U1A mRNA. Journal of Molecular Biology 273, 84–92.CrossRefGoogle ScholarPubMed
Hadden, J. M., Déclais, A.-C., Carr, S., Lilley, D. M. J. & Phillips, S. E. V. (2007). The structural basis of Holliday junction resolution by T7 endonuclease I. Nature 449, 621–624.CrossRefGoogle ScholarPubMed
Hagerman, P. J. (1984). Evidence for the existence of stable curvature of DNA in solution. Proceedings of the National Academy of Sciences USA 81, 4632–4636.CrossRefGoogle ScholarPubMed
Heuer, D. M., Yuan, C., Saha, S. & Archer, L. A. (2005). Effect of topological asymmetry on the electrophoretic mobility of branched DNA structures with and without single-base mismatches. Electrophoresis 26, 64–70.CrossRefGoogle ScholarPubMed
Hohng, S., Wilson, T. J., Tan, E., Clegg, R. M., Lilley, D. M. J. & Ha, T. (2004). Conformational flexibility of four-way junctions in RNA. Journal of Molecular Biology 336, 69–79.CrossRefGoogle ScholarPubMed
Husain, I., Griffith, J. D. & Sancar, A. (1988). Thymine dimers bend DNA. Proceedings of the National Academy of Sciences USA 85, 2558–2562.CrossRefGoogle ScholarPubMed
Khvorova, A., Lescoute, A., Westhof, E. & Jayasena, S. D. (2003). Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity. Nature Structural Biology 10, 1–5.Google ScholarPubMed
Kieft, J. S., Zhou, K., Grech, A., Jubin, R. & Doudna, J. A. (2002). Crystal structure of an RNA tertiary domain essential to HCV IRES-mediated translation initiation. Nature Structural Biology 9, 370–374.Google ScholarPubMed
Klein, D. J., Schmeing, T. M., Moore, P. B. & Steitz, T. A. (2001). The kink-turn: a new RNA secondary structure motif. EMBO Journal 20, 4214–4221.CrossRefGoogle ScholarPubMed
Lafontaine, D. A., Norman, D. G. & Lilley, D. M. J. (2001). Structure, folding and activity of the VS ribozyme: importance of the 2–3–6 helical junction. EMBO Journal 20, 1415–1424.CrossRefGoogle ScholarPubMed
Lafontaine, D. A., Norman, D. G. & Lilley, D. M. J. (2002). The global structure of the VS ribozyme. EMBO Journal 21, 2461–2471.CrossRefGoogle ScholarPubMed
Leontis, N. B., Hills, M. T., Piotto, M., Malhotra, A., Nussbaum, J. & Gorenstein, D. G. (1993). A model for the solution structure of a branched, three-strand DNA complex. Journal of Biomolecular and Structure and Dynamics 11, 215–223.CrossRefGoogle Scholar
Leontis, N. B., Kwok, W. & Newman, J. S. (1991). Stability and structure of three-way junctions containing unpaired nucleotides. Nucleic Acids Research 19, 759–766.CrossRefGoogle ScholarPubMed
Lerman, L. S. & Frisch, H. L. (1982). Why does the electrophoretic mobility of DNA in gels vary with the length of the molecule. Biopolymers 21, 995–997.CrossRefGoogle ScholarPubMed
Lescoute, A. & Westhof, E. (2006). Topology of three-way junctions in folded RNAs. RNA 12, 83–93.CrossRefGoogle ScholarPubMed
Levene, S. D. & Zimm, B. H. (1989). Understanding the anomalous electrophoresis of bent DNA molecules: a reptation model. Science 245, 396–399.CrossRefGoogle ScholarPubMed
Lilley, D. M. J. (1995). Kinking of DNA and RNA by base bulges. Proceedings of the National Academy of Sciences USA 92, 7140–7142.CrossRefGoogle ScholarPubMed
Lilley, D. M. J. (2000). Structures of helical junctions in nucleic acids. Quarterly Reviews of Biophysics 33, 109–159.CrossRefGoogle ScholarPubMed
Lilley, D. M. J., Clegg, R. M., Diekmann, S., Seeman, N. C., von Kitzing, E. & Hagerman, P. (1995). Nomenclature Committee of the International Union of Biochemistry: a nomenclature of junctions and branchpoints in nucleic acids. Recommendations 1994. European Journal of Biochemistry 230, 1–2.CrossRefGoogle ScholarPubMed
Lilley, D. M. J. & White, M. F. (2000). Resolving the relationships of resolving enzymes. Proceedings of the National Academy of Sciences USA 97, 9351–9353.CrossRefGoogle ScholarPubMed
Lilley, D. M. J. & White, M. F. (2001). The junction-resolving enzymes. Nature Reviews Molecular Cell Biology 2, 433–443.CrossRefGoogle ScholarPubMed
Lipfert, J., Ouellet, J., Norman, D. G., Doniach, S. & Lilley, D. M. J. (2008). The complete VS ribozyme in solution studied by small-angle X-ray scattering. Structure In the press.CrossRefGoogle ScholarPubMed
Liu, J., Déclais, A.-C., Mckinney, S. A., Ha, T., Norman, D. G. & Lilley, D. M. J. (2005). Stereospecific effects determine the structure of a four-way DNA junction. Chemistry and Biology 12, 217–228.CrossRefGoogle ScholarPubMed
Liu, J., Déclais, A. C. & Lilley, D. M. J. (2006). Mechanistic aspects of the DNA junction-resolving enzyme T7 endonuclease I. Biochemistry 45, 3934–3942.CrossRefGoogle ScholarPubMed
Liu, J. & Lilley, D. M. J. (2007). The role of specific 2′-hydroxyl groups in the stabilization of the folded conformation of kink-turn RNA. RNA 13, 200–210.CrossRefGoogle Scholar
Luebke, K. J. & Tinoco, I. (1996). Sequence effects on RNA bulge-induced helix bending and a conserved five-nucleotide bulge from the group I introns. Biochemistry 35, 11677–11684.CrossRefGoogle Scholar
Lumpkin, O., Levene, S. D. & Zimm, B. H. (1989). Exactly solvable reptation model. Physical Review. A 39, 6557–6566.CrossRefGoogle ScholarPubMed
Lumpkin, O. J., Dejardin, P. & Zimm, B. H. (1985). Theory of gel electrophoresis of DNA. Biopolymers 24, 1573–1593.CrossRefGoogle ScholarPubMed
Lumpkin, O. J. & Zimm, B. H. (1982). Mobility of DNA in gel electrophoresis. Biopolymers 21, 2315–2316.CrossRefGoogle ScholarPubMed
Makarova, K. S., Aravind, L. & Koonin, E. V. (2000). Holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Research 28, 3417–3432.Google Scholar
Marini, J. C., Levene, S. D., Crothers, D. M. & Englund, P. T. (1982). Bent helical structure in kinetoplast DNA. Proceedings of the National Academy of Sciences USA 79, 7664–7668.CrossRefGoogle ScholarPubMed
Martick, M. & Scott, W. G. (2006). Tertiary contacts distant from the active site prime a ribozyme for catalysis. Cell 126, 309–320.CrossRefGoogle Scholar
Matsumura, S., Ikawa, Y. & Inoue, T. (2003). Biochemical characterization of the kink-turn RNA motif. Nucleic Acids Research 31, 5544–5551.CrossRefGoogle ScholarPubMed
McGregor, N., Ayora, S., Sedelnikova, S., Carrasco, B., Alonso, J. C., Thaw, P. & Rafferty, J. (2005). The structure of Bacillus subtilis RecU Holliday junction resolvase and its role in substrate selection and sequence-specific cleavage. Structure 13, 1341–1351.CrossRefGoogle ScholarPubMed
McKinney, S. A., Déclais, A.-C., Lilley, D. M. J. & Ha, T. (2003). Structural dynamics of individual Holliday junctions. Nature Structural Biology 10, 93–97.CrossRefGoogle ScholarPubMed
Melcher, S. E., Wilson, T. J. & Lilley, D. M. J. (2003). The dynamic nature of the four-way junction of the hepatitis C virus IRES. RNA 9, 809–820.CrossRefGoogle ScholarPubMed
Miick, S. M., Fee, R. S., Millar, D. P. & Chazin, W. J. (1997). Crossover isomer bias is the primary sequence-dependent property of immobilized Holliday junctions. Proceedings of the National Academy of Sciences USA 94, 9080–9084.CrossRefGoogle ScholarPubMed
Moore, T., Zhang, Y., Fenley, M. O. & Li, H. (2004). Molecular basis of box C/D RNA–protein interactions; cocrystal structure of archaeal L7Ae and a box C/D RNA. Structure 12, 807–818.CrossRefGoogle Scholar
Murchie, A. I. H., Clegg, R. M., von Kitzing, E., Duckett, D. R., Diekmann, S. & Lilley, D. M. J. (1989). Fluorescence energy transfer shows that the four-way DNA junction is a right-handed cross of antiparallel molecules. Nature 341, 763–766.CrossRefGoogle ScholarPubMed
Murchie, A. I. H., Portugal, J. & Lilley, D. M. J. (1991). Cleavage of a four-way DNA junction by a restriction enzyme spanning the point of strand exchange. EMBO Journal 10, 713–718.CrossRefGoogle ScholarPubMed
Murchie, A. I. H., Thomson, J. B., Walter, F. & Lilley, D. M. J. (1998). Folding of the hairpin ribozyme in its natural conformation achieves close physical proximity of the loops. Molecular Cell 1, 873–881.CrossRefGoogle ScholarPubMed
Nowakowski, J., Shim, P. J., Prasad, G. S., Stout, C. D. & Joyce, G. F. (1999). Crystal structure of an 82 nucleotide RNA–DNA complex formed by the 10–23 DNA enzyme. Nature Structural Biology 6, 151–156.Google ScholarPubMed
Ortiz-Lombardía, M., González, A., Erijta, R., Aymamí, J., Azorín, F. & Coll, M. (1999). Crystal structure of a DNA Holliday junction. Nature Structural Biology 6, 913–917.Google ScholarPubMed
Ouporov, I. V. & Leontis, N. B. (1995). Refinement of the solution structure of a branched DNA three-way junction. Biophysical Journal 68, 266–274.CrossRefGoogle ScholarPubMed
Oussatcheva, E. A., Shlyakhtenko, L. S., Glass, R., Sinden, R. R., Lyubchenko, Y. L. & Potaman, V. N. (1999). Structure of branched DNA molecules: gel retardation and atomic force microscopy studies. Journal of Molecular Biology 292, 75–86.CrossRefGoogle ScholarPubMed
Overmars, F. J. J., Pikkemaat, J. A., van den Elst, H., van Boom, J. H. & Altona, C. (1996). NMR studies of DNA three-way junctions containing two unpaired thymidine bases: the influence of the sequence at the junction on the stability of the stacking conformers. Journal of Molecular Biology 255, 702–713.CrossRefGoogle ScholarPubMed
Parsons, C. A., Stasiak, A., Bennett, R. J. & West, S. C. (1995). Structure of a multisubunit complex that promotes DNA branch migration. Nature 374, 375–378.CrossRefGoogle ScholarPubMed
Penedo, J. C., Wilson, T. J., Jayasena, S. D., Khvorova, A. & Lilley, D. M. J. (2004). Folding of the natural hammerhead ribozyme is enhanced by interaction of auxiliary elements. RNA 10, 880–888.CrossRefGoogle ScholarPubMed
Pley, H. W., Flaherty, K. M. & McKay, D. B. (1994). Three-dimensional structure of a hammerhead ribozyme. Nature 372, 68–74.CrossRefGoogle ScholarPubMed
Pöhler, J. R. G., Giraud-Panis, M.-J. E. & Lilley, D. M. J. (1996). T4 endonuclease VII selects and alters the structure of the four-way DNA junction; binding of a resolution-defective mutant enzyme. Journal of Molecular Biology 260, 678–696.CrossRefGoogle ScholarPubMed
Rafferty, J. B., Sedelnikova, S. E., Hargreaves, D., Artymiuk, P. J., Baker, P. J., Sharples, G. J., Mahdi, A. A., Lloyd, R. G. & Rice, D. W. (1996). Crystal structure of DNA recombination protein RuvA and a model for its binding to the Holliday junction. Science 274, 415–421.CrossRefGoogle Scholar
Rice, J. A. & Crothers, D. M. (1989). DNA bending by the bulge defect. Biochemistry 28, 4512–4516.CrossRefGoogle ScholarPubMed
Riordan, F. A., Bhattacharyya, A., Mcateer, S. & Lilley, D. M. J. (1992). Kinking of RNA helices by bulged bases and the structure of the human immunodeficiency virus transactivator response element. Journal of Molecular Biology 226, 305–310.CrossRefGoogle ScholarPubMed
Roe, S. M., Barlow, T., Brown, T., Oram, M., Keeley, A., Tsaneva, I. R. & Pearl, L. H. (1998). Crystal structure of an octameric RuvA-Holliday junction complex. Molec. Cell 2, 361–372.CrossRefGoogle ScholarPubMed
Rosen, M. A. & Patel, D. J. (1993a). Conformational differences between bulged pyrimidines (C–C) and purines (A–A, I–I) at the branch point of three-stranded DNA junctions. Biochemistry 32, 6563–6575.CrossRefGoogle Scholar
Rosen, M. A. & Patel, D. J. (1993b). Structural features of a three-stranded DNA junction containing a C–C junctional bulge. Biochemistry 32, 6576–6587.CrossRefGoogle Scholar
Rupert, P. B. & Ferré-D'Amaré, A. R. (2001). Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 410, 780–786.CrossRefGoogle ScholarPubMed
Saha, S., Heuer, D. M. & Archer, L. A. (2006). Electrophoretic mobility of linear and star-branched DNA in semidilute polymer solutions. Electrophoresis 27, 3181–3194.CrossRefGoogle ScholarPubMed
Scott, W. G., Finch, J. T. & Klug, A. (1995). The crystal structure of an all-RNA hammerhead ribozyme: a proposed mechanism for RNA catalytic cleavage. Cell 81, 991–1002.CrossRefGoogle ScholarPubMed
Shlyakhtenko, L. S., Appella, E., Harrington, R. E., Kutyavin, I. & Lyubchenko, Y. L. (1994). Structure of three-way DNA junctions. 2. Effects of extra bases and mismatches. Journal of Biomolecular Structure and Dynamics 12, 131–143.CrossRefGoogle ScholarPubMed
Silverman, S. K. & Cech, T. R. (1999). Energetics and cooperativity of tertiary hydrogen bonds in RNA structure. Biochemistry 38, 8691–8702.CrossRefGoogle ScholarPubMed
Sip, M., Schwartz, A., Vovelle, F., Ptak, M. & Leng, M. (1992). Distortions induced in DNA by cis-platinum interstrand adducts. Biochemistry 31, 2508–2513.CrossRefGoogle ScholarPubMed
Stühmeier, F., Welch, J. B., Murchie, A. I. H., Lilley, D. M. J. & Clegg, R. M. (1997). The global structure of three-way DNA junctions with and without bulges: fluorescence studies. Biochemistry 36, 13530–13538.CrossRefGoogle Scholar
Tan, E., Wilson, T. J., Nahas, M. K., Clegg, R. M., Lilley, D. M. J. & Ha, T. (2003). A four-way junction accelerates hairpin ribozyme folding via a discrete intermediate. Proceedings of the National Academy of Sciences USA 100, 9308–9313.CrossRefGoogle Scholar
Tang, R. S. & Draper, D. E. (1990). Bulge loops used to measure the helical twist of RNA in solution. Biochemistry 29, 5232–5237.CrossRefGoogle ScholarPubMed
Tang, R. S. & Draper, D. E. (1994). On the use of phasing experiments to measure helical repeat and bulge loop-associated twist in RNA. Nucleic Acids Research 22, 835–841.CrossRefGoogle ScholarPubMed
Thiviyanathan, V., Luxon, B. A., Leontis, N. B., Illangasekare, N., Donne, D. G. & Gorenstein, D. G. (1999). Hybrid–hybrid matrix structural refinement of a DNA three-way junction from 3D NOESY–NOESY. Journal of Biomolecular NMR 14, 209–221.CrossRefGoogle ScholarPubMed
Von Kitzing, E., Lilley, D. M. J. & Diekmann, S. (1990). The stereochemistry of a four-way DNA junction: a theoretical study. Nucleic Acids Research 18, 2671–2683.CrossRefGoogle ScholarPubMed
Walter, F., Murchie, A. I. H., Duckett, D. R. & Lilley, D. M. J. (1998a). Global structure of four-way RNA junctions studied using fluorescence resonance energy transfer. RNA 4, 719–728.CrossRefGoogle ScholarPubMed
Walter, F., Murchie, A. I. H. & Lilley, D. M. J. (1998b). The folding of the four-way RNA junction of the hairpin ribozyme. Biochemistry 37, 17629–17636.CrossRefGoogle ScholarPubMed
Walter, F., Murchie, A. I. H., Thomson, J. B. & Lilley, D. M. J. (1998c). Structure and activity of the hairpin ribozyme in its natural junction conformation: effect of metal ions. Biochemistry 37, 14195–14203.CrossRefGoogle ScholarPubMed
Wang, Y. H. & Griffith, J. (1991). Effects of bulge composition and flanking sequence on the kinking of DNA by bulged bases. Biochemistry 30, 1358–1363.CrossRefGoogle ScholarPubMed
Welch, J. B., Duckett, D. R. & Lilley, D. M. J. (1993). Structures of bulged three-way DNA junctions. Nucleic Acids Research 21, 4548–4555.CrossRefGoogle ScholarPubMed
Welch, J. B., Walter, F. & Lilley, D. M. J. (1995). Two inequivalent folding isomers of the three-way DNA junction with unpaired bases: sequence-dependence of the folded conformation. Journal of Molecular Biology 251, 507–519.CrossRefGoogle ScholarPubMed
White, M. F. & Lilley, D. M. J. (1997). The resolving enzyme CCE1 of yeast opens the structure of the four-way DNA junction. Journal of Molecular Biology 266, 122–134.CrossRefGoogle ScholarPubMed
White, M. F. & Lilley, D. M. J. (1998). Interaction of the resolving enzyme YDC2 with the four-way DNA junction. Nucleic Acids Research 26, 5609–5616.CrossRefGoogle ScholarPubMed
Wu, H.-M. & Crothers, D. M. (1984). The locus of sequence-directed and protein-induced DNA bending. Nature 308, 509–513.CrossRefGoogle ScholarPubMed
Yang, M. S. & Millar, D. P. (1996). Conformational flexibility of three-way DNA junctions containing unpaired nucleotides. Biochemistry 35, 7959–7967.CrossRefGoogle ScholarPubMed
Zacharias, M. & Hagerman, P. J. (1995a). The bend in RNA created by the trans-activation response element bulge of human immunodeficiency virus is straightened by arginine and by Tat-derived peptide. Proceedings of the National Academy of Sciences USA 92, 6052–6056.CrossRefGoogle ScholarPubMed
Zacharias, M. & Hagerman, P. J. (1995b). Bulge-induced bends in RNA: quantification by transient electric birefringence. Journal of Molecular Biology 247, 486–500.CrossRefGoogle ScholarPubMed