Abstract
B-DNA is the most common DNA helix conformation under physiological conditions. However, when the amount of water in a DNA solution is decreased, B-to-A helix transitions have been observed. To understand what type of helix conformations exist in a solvent-free environment, a series of poly d(CG) n and mixed sequence DNA duplexes from 18 to 30 bp were examined with circular dichroism (CD), ESI-MS, ion mobility, and molecular dynamics. From the CD spectra, it was observed that all sequences had B-form helices in solution. However, the solvent-free results were more complex. For the poly d(CG) n series, the 18 bp duplex had an A-form helix conformation, both A- and B-helices were present for the 22 bp duplex, and only B-helices were observed for the 26 and 30 bp duplexes. Since these sequences were all present as B-DNA in solution, the observed solvent-free structures illustrate that smaller helices with fewer base pairs convert to A-DNA more easily than larger helices in the absence of solvent. A similar trend was observed for the mixed sequence duplexes where both an A- and B-helix were present for the 18 bp duplex, while only B-helices occur for the larger 22, 26, and 30 bp duplexes. Since the solvent-free B-helices appear at smaller sizes for the mixed sequences than for the pure d(CG) n duplexes, the pure d(CG) n duplexes have a greater A-philicity.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Watson, J. D.; Crick, F. H. Molecular Structure of Nucleic Acids: A Structure for Deoxyribose Nucleic Acid. Nature 1953, 171, 737.
Langridge, R.; Wilson, H. R.; Hooper, C. W.; Wilkins, M. H. F.; Hamilton, L. D. The Molecular Configuration of Deoxyribonucleic Acid. I. X-ray Diffraction Study of a Crystalline Form of the Lithium Salt. J. Mol. Biol. 1960, 2, 19–37.
Langridge, R.; Marvin, D. A.; Seeds, W. E.; Wilson, H. R.; Hamilton, L. D. The Molecular Configuration of Deoxyribonucleic Acid. II. Molecular Models and their Fourier Transforms. J. Mol. Biol. 1960, 2, 38.
Fuller, W.; Wilkins, M. H. F.; Wilson, H. R.; Hamilton, L. D.; Arnott, S. The Molecular Configuration of Deoxyribonucleic Acid. IV. X-ray Diffraction Study of the A Form. J. Mol. Biol. 1965, 12, 60.
Wang, A. H. J.; Quigley, G. J.; Kolpak, F. J.; Crawford, J. L.; vanBoom, J. H.; van der Marel, G.; Rich, A. Molecular Structure of a Left-Handed Double Helical DNA Fragment at Atomic Resolution. Nature 1979, 282, 680.
Franklin, R. E.; Gosling, R. G. The structure of sodium thymonucleate fibers. I. The influence of water content. Acta Crystallogr 1953, 6, 673.
Kim, Y.; Geiger, J. H.; Hahn, S.; Sigler, P. B. Crystal Structure of a Yeast TBP/TATA-Box Complex. Nature 1993, 365, 512.
Kim, J. L.; Nikolov, D. B.; Burley, S. K. Cocrystal Structure of TBP Recognizing the minor groove of a TATA element. Nature 1993, 365, 520.
Florentiev, V. L.; Ivanov, V. I. RNA Polymerase: Two-step Mechanism with Overlapping Steps. Nature 1970, 228, 519.
Beabealashvily, R. S.; Ivanov, V. I.; Minchenkova, L. E.; Savotchkina, L. P. RNA polymerase-DNA complexes I: The study of the conformation of nucleic acids at the growing point of RNA in an RNA polymerase-DNA system. Biochim. Biophys. Acta 1972, 259, 35.
Setlow, P. DNA in dormant spores of Bacillus species is in an A-like conformation. Mol. Microbiol 1992, 6, 563.
Ivanov, V. I.; Minchenkova, L. E.; Chernov, B. K.; McPhie, P.; Ryu, S.; Garges, S.; Barber, A. M.; Zhurkin, V. B.; Adhya, S. CRP-DNA Complexes: Inducing the A-like Form in the Binding Sites with an Extended Central Spacer. J. Mol. Biol. 1995, 245, 228.
Eom, S. H.; Wang, J.; Steitz, T. A. Structure of Taq polymerase with DNA at the Polymerase Active Site. Nature 1996, 382, 278.
Jones, S.; Heyningen, P.; Berman, H. M.; Thornton, J. M. Protein-DNA Interactions: A Structural Analysis. J. Mol. Biol. 1999, 287, 877.
Brahm, J.; Mommaerts, W. F. H. M. A Study of Conformation of Nucleic Acids in Solution by Means of Circular Dichroism. J. Mol. Biol. 1964, 10, 73.
Ivanov, V. I.; Minchenkova, L. E.; Minyat, E. E.; Frank-Kamenetskii, M. D.; Schyolkina, A. K. The B to A Transition of DNA in Solution. J. Mol. Biol. 1974, 87, 817.
Vorlickova, M.; Minyat, E. E.; Kypr, J. Cooperative Changes in the Chiroptical Properties of DNA Induced by Methanol. Biopolymers 1984, 23, 1.
Minyat, E. E.; Ivanov, V. I.; Kritzyn, A. M.; Minchenkova, L. E.; Schyolkina, A. K. Spermine and Spermidine-Induced B to A Transition of DNA in Solution. J. Mol. Biol. 1978, 128, 397.
Xu, Q.; Shoemaker, R. K.; Braunlin, W. H. Induction of B-A transitions of Deoxyoligonucleotides by Multivalent Cations in Dilute Aqueous Solution. Biophys. J. 1993, 65, 1039.
Ivanov, V. I.; Minchenkova, L. E. The A-form of DNA—In search of Biological Role (A Review). Mol. Biol. 1995, 28, 780.
Gorin, A. A.; Ulyanov, N. B.; Zhurkin, V. B. S-N Transition of the Sugar Ring in B-form DNA. Mol. Biol. 1990, 24, 1036.
Foloppe, N.; MacKerell, A. D. Intrinsic Conformational Properties of Deoxyribonucleosides: Implicated Role for Cytosine in the Equilibrium Among the A, B, and Z Forms of DNA. Biophys. J. 1999, 76, 3206.
Gidden, J.; Ferzoco, A.; Baker, E. S.; Bowers, M. T. Duplex Formation and the Onset of Helicity in Poly d(CG) n Oligonucleotides in a Solvent-Free Environment. J. Am. Chem. Soc 2004, 126, 15132.
Gidden, J.; Baker, E. S.; Ferzoco, A.; Bowers, M. T. Structural Motifs of DNA Complexes in the Gas Phase. Int. J. Mass Spectrom. 2005, 240, 183.
Wyttenbach, T.; Kemper, P. R.; Bowers, M. T. Design of a New Electrospray Ion Mobility Mass Spectrometer. Int. J. Mass Spectrom. 2001, 212, 13.
Mason, E. A.; McDaniel, E. W. Transport Properties of Ions in Gases Wiley: New York, NY, 1988.
Cheatham, T. E.; Cieplak, P.; Kollman, P. A.. J. Biomol. Struct. Dyn. 1999, 16, 8458.
Case, D. A.; Pearlman, D. A.; Caldwell, J. W.; Cheatham, T. E. III; Wang, J.; Ross, W. S.; Simmerling, C. L.; Darden, T. A.; Merz, K. M.; Stanton, R. V.; Cheng, A. L.; Vincent, J. J.; Crowley, M.; Tsui, V.; Gohlke, H.; Radmer, R. J.; Duan, Y.; Pitera, J.; Massova, I.; Seibel, G. L.; Singh, U. C.; Weiner, P. K.; Kollman, P. A. AMBER 7; University of California: San Francisco, CA, 2002.
HyperChem 7.0; Hypercube Inc., Gainesville, FL.
Mesleh, M. F.; Hunter, J. M.; Shvartsburg, A. A.; Schwartz, G. C.; Jarrold, M. F. Structural Information from Ion Mobility Measurements: Effects of the Long-Range Potential. J. Phys. Chem. 1996, 100, 16082.
Shvartsburg, A. A.; Jarrold, M. F. An Exact Hard-Spheres Scattering Model for the Mobilities of Polyatomic Ions. Chem. Phys. Lett. 1996, 261, 86.
Maher, L. J.; Wold, B.; Dervan, P. B. Inhibition of DNA Binding Proteins by Oligonucleotide-Directed Triple Helix Formation. Science 1989, 245, 725.
Demidov, V. V.; Potaman, V. N.; Frank-Kamenetskii, M. D.; Egholm, M.; Buchard, O.; Sönnichsen, S. H.; Nielsen, P. E. Stability of Peptide Nucleic Acids in Human Serum and Cellular Extracts. Biochem. Pharmacol. 1994, 48, 1310.
Tyagi, S.; Kramer, F. R. Molecular Beacons: Probes that Fluoresce upon Hybridization. Nat. Biotechnol. 1996, 14, 303.
Holland, P. M.; Abramson, R. D.; Watson, R.; Gefland, D. H. Detection of Specific Polymerase Chain Reaction Product by Utilizing the 5′→3′ Exonuclease Activity of Thermus aquaticus DNA Polymerase. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 7276.
Thelwell, N.; Millington, S.; Solinas, A.; Booth, J.; Brown, T. Mode of Action and Application of Scorpion Primers to Mutation Detection. Nucleic Acids Res. 2000, 28, 3752.
Rueda, M.; Kalko, S. G.; Luque, F. J.; Orozco, M. The Structure and Dynamics of DNA in the Gas Phase. J. Am. Chem. Soc. 2003, 125, 8007.
Veenstra, T. D. Electrospray Ionization Mass Spectrometry: A Promising New Technique in the Study of Protein/DNA Noncovalent Complexes. Biochem. Biophys. Res. Commun. 1999, 257, 1.
Riazance, J. H.; Baase, W. A.; Johnson, W. C., Jr.; Hall, K.; Cruz, P.; Tinoco, I. Jr. Evidence for Z-form RNA by vacuum UV circular dichroism. Nucleic Acids Res. 1985, 13, 4983.
Segersnolten, G. M. J.; Sijtsema, N. M.; Otto, C. Evidence for Hoogsteen GC Base Pairs in the Proton-Induced Transition from Right-Handed to Left-Handed Poly(dG-dC)·Poly(dG-dC). Biochemistry 1997, 36, 13241.
Poehl, F. M.; Jovin, T. M. Salt-Induced Cooperative Conformational Change of a Synthetic DNA: Equilibrium and Kinetic Studies with Poly(dG-dC). J. Mol. Biol. 1972, 67, 375.
Trantirek, L.; Stefl, R.; Vorlickova, M.; Koca, J.; Sklenar, V.; Kypr, J. An A-type Double Helix of DNA Having B-Type Puckering of the Deoxyribose Rings. J. Mol. Biol. 2000, 297, 907.
Baker, E. S.; Hong, J. W.; Gaylord, B. S.; Bazan, G. C.; Bowers, M. T. PNA/dsDNA Complexes: Site-Specific Binding and dsDNA Biosensor Applications. J. Am. Chem. Soc. 2006, 128, 8484.
Baker, E. S.; Bernstein, S. L.; Gabelica, V.; De Pauw, E.; Bowers, M. T. G-Quadruplexes in Telomeric Repeats Are Conserved in a Solvent-Free Environment. Int. J. Mass Spectrom. 2006, 253, 225.
Schnier, P. D.; Klassen, J. S.; Strittmatter, E. F.; Williams, E. R. Activation Energies for Dissociation of Double Strand Oligonucleotide Anions: Evidence for Watson-Crick Base Pairing in Vacuo. J. Am. Chem. Soc. 1998, 120, 9605.
Gabelica, V.; De Pauw, E. Comparison Between Solution-Phase Stability and Gas-Phase Kinetic Stability of Oligodeoxynucleotide Duplexes. J. Mass Spectrom. 2001, 36, 397.
Gabelica, V.; Rosu, F.; Houssier, C.; De Pauw, E. Gas-Phase Thermal Denaturation of an Oligonucleotide Duplex and Its Complexes with Minor Groove Binders. Rapid Commun. Mass Spectrom. 2000, 14, 464.
Gabelica, V.; De Pauw, E. Collision-Induced Dissociation of 16-mer DNA Duplexes with Various Sequences: Evidence for Conservation of the Double Helix Conformation in the Gas Phase. Int. J. Mass Spectrom. 2002, 219, 151.
Author information
Authors and Affiliations
Corresponding author
Additional information
Published online March 12, 2007
Rights and permissions
About this article
Cite this article
Baker, E.S., Bowers, M.T. B-DNA Helix Stability in a Solvent-Free Environment. J Am Soc Mass Spectrom 18, 1188–1195 (2007). https://doi.org/10.1016/j.jasms.2007.03.001
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1016/j.jasms.2007.03.001