Gas-phase conformations and energetics of protonated 2′-deoxyguanosine and guanosine: IRMPD action spectroscopy and theoretical studies

Journal of Physical Chemistry B

Volumn 118, Issue 51, 2014, Pages 14774-14784

  Wu, R R ^a   Yang, Bo ^a   Berden, G ^b   Oomens, J ^b,c   Rodgers, M T ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMOLECULES; ELECTRONIC STRUCTURE; ELECTRONS; FREE ELECTRON LASERS; GASES; HYDROGEN BONDS; OPTICAL PARAMETRIC OSCILLATORS; RNA;

ACTION SPECTROSCOPY; ELECTRONIC STRUCTURE CALCULATIONS; GAS-PHASE STRUCTURES; HYDROXYL SUBSTITUENTS; INFRARED MULTIPLE PHOTON DISSOCIATIONS; LOW ENERGY STRUCTURES; LOW-ENERGY CONFORMATIONS; RELATIVE STABILITIES;

PROTONATION;

DEOXYGUANOSINE; GUANOSINE; PROTON;

CHEMISTRY; HYDROGEN BOND; INFRARED SPECTROPHOTOMETRY; MASS SPECTROMETRY; PROCEDURES; THEORETICAL MODEL;

DEOXYGUANOSINE; GUANOSINE; HYDROGEN BONDING; MASS SPECTROMETRY; MODELS, THEORETICAL; PROTONS; SPECTROPHOTOMETRY, INFRARED;

EID: 84919884605     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp508019a     Document Type: Article

References (76)

1. Waalkes, T. P.; Abeloff, M. D.; Ettinger, D. S.; Woo, K. B.; Gehrke, C. W.; Kuo, K. C.; Borek, E. Modified Ribonucleosides As Biological Markers for Patients with Small Cell-Carcinoma of the Lung. Eur. J. Cancer Clin. Oncol. 1982, 18, 1267-1274.
2. Mitchell, E. P.; Evans, L.; Schultz, P.; Madsen, R.; Yarbro, J. W.; Gehrke, C. W.; Kuo, K. Modified Nucleosides in Human Serum. J. Chromatogr. 1992, 581, 31-40.
3. Perigaud, C.; Gosselin, G.; Imbach, J. L. Stereospecific Synthesis of Chiral Acyclic Analogs of Guanosine. Bioorg. Med. Chem. Lett. 1992, 2, 677-680.
4. Perigaud, C.; Gosselin, G.; Imbach, J. L. Nucleoside Analogs As Chemotherapeutic-Agents - A Review. Nucleosides Nucleotides 1992, 11, 903-945.
5. Bjelland, S.; Seeberg, E. Mutagenicity, Toxicity and Repair of DNA Base Damage Induced by Oxidation. Mutat. Res. 2003, 531, 37-80.
6. Burrows, C. J.; Muller, G. Oxidative Nucleobase Modifications Leading to Strand Scission. Chem. Rev. 1998, 98, 1109-1151.
7. Wiseman, H.; Halliwell, B. Damage to DNA by Reactive Oxygen and Nitrogen Species: Role in Inflammatory Disease and Progression to Cancer. Biochem. J. 1996, 313, 17-29.
8. Masuda, M.; Suzuki, T.; Friesen, M. D.; Ravanat, J. L.; Cadet, J.; Pignatelli, B.; Nishino, H.; Ohshima, H. Chlorination of Guanosine and Other Nucleosides by Hypochlorous Acid and Myeloperoxidase of Activated Human Neutrophils - Catalysis by Nicotine and Trimethylamine. J. Biol. Chem. 2001, 276, 40486-40496.
9. Liu, J.-A.; Petzold, C. J.; Ramirez-Arizmendi, L. E.; Perez, J.; Kenttamaa, H. Phenyl Radicals React with Dinucleoside Phosphates by Addition to Purine Bases and H-Atom Abstraction From a Sugar Moiety. J. Am. Chem. Soc. 2005, 127, 12758-12759.
10. Serrano, J.; Palmeira, C. M.; Wallace, K. B.; Kuehl, D. W. Determination of 8-Hydroxydeoxyguanosine in Biological Tissue by Liquid Chromatography/Electrospray Ionization-Mass Spectrometry/Mass Spectrometry. Rapid Commun. Mass Spectrom. 1996, 10, 1789-1791.
11. 2+). J. Phys. Chem. 1996, 100, 7250-7255.
12. Lippert, B. Multiplicity of Metal Ion Binding Patterns to Nucleobases. Coord. Chem. Rev. 2000, 200, 487-516.
13. Neidle, S.; Read, M. A. G-Quadruplexes as Therapeutic Targets. Biopolymers 2001, 56, 195-208.
14. Lyonnais, S.; Hounsou, C.; Teulade-Fichou, M.; Jeusset, J.; Cam, E. L.; Mirambeau, G. G-Quartets Assembly within a G-Rich DNA Flap. A Possible Event at the Center of the HIV-1 Genome. Nucleic Acids Res. 2002, 30, 5276-5283.
15. Sen, D.; Gilbert, W. Formation of Parallel 4-Stranded Complexes by Guanine-Rich Motifs in DNA and Its Implications for Meiosis. Nature 1988, 334, 364-366.
16. Evans, T.; Schon, E.; Gora-Maslak, G.; Patterson, J.; Efstratiadis, A. S1-Hypersensitive Sites in Eukaryotic Promoter Regions. Nucleic Acids Res. 1984, 12, 8043-8058.
17. Sarig, G. Purification and Characterization of qTBP42 a New Single-Stranded and Quadruplex Telomeric DNA-Binding Protein from Rat Hepatocytes. J. Biol. Chem. 1997, 272, 4474-4482.
18. Blackburn, E. H. Telomeres - No End in Sight. Cell 1994, 77, 621-623.
19. van Dam, L.; Ouwerkerk, N.; Brinkmann, A.; Raap, J.; Levitt, M. H. Solid-State NMR Determination of Sugar Ring Pucker in C-13-Labeled 2′-Deoxynucleosides. Biophys. J. 2002, 83, 2835-2844.
20. Rich, A.; Nordheim, A.; Wang, A. H. The Chemistry and Biology of Left-Handed Z-DNA. J. Annu. Rev. Biochem. 1984, 53, 791-846.
21. Nir, E.; Janzen, C.; Imhof, P.; Kleinermanns, K.; de Veries, M. S. Pairing of the Nucleobases Guanine and Cytosine in the Gas Phase Studied by IR-UV Double-Resonance Spectroscopy and ab initio Calculation. Phys. Chem. Chem. Phys. 2002, 4, 732-739.
22. Nir, E.; Janzen, C.; Imhof, P.; Kleinermanns, K.; de Veries, M. S. Pairing of the Nucleobase Guanine Studied by IR-UV Double-Resonance Spectroscopy and Ab Initio Calculation. Phys. Chem. Chem. Phys. 2002, 4, 740-750.
23. Hanus, M.; Ryjacek, F.; Kabelac, M.; Kubar, T.; Bogdan, T. V.; Trygubenko, S. A.; Hobza, P. Correlated Ab Initio Study of Nucleic Acid Bases and Their Tautomers in the Gas Phase, in a Microhydrated Environment and in Aqueous Solution. Guanine: Surprising Stabilization of Rare Tautomers in Aqueous Solution. J. Am. Chem. Soc. 2003, 125, 7678-7688.
24. Guallar, V.; Douhal, A.; Moreno, M.; Lluch, J. M. DNA Mutations Induced by Proton and Charge Transfer in the Low-lying Excited Singlet Electronic States of the DNA Base Pairs: A Theoretical Insight. J. Phys. Chem. A 1999, 103, 6251-6256.
25. Zoete, V.; Meuwly, M. Double Proton Transfer in the Isolated and DNA-Embedded Guanine-Cytosine Base Pair. J. Chem. Phys. 2004, 121, 4377-4388.
26. Li, X.; Cai, Z.; Sevilla, M. D. Investigation of Proton Transfer within DNA Base Pair Anion and Cation Radicals by Density Functional Theory (DFT). J. Phys. Chem. B 2001, 105, 10115-10123.
27. Salazar, M.; Fedoroff, O. Y.; Miller, J. M.; Ribeiro, N. S.; Reid, B. R. The DNA Strand in DNA•RNA Hybrid Duplexes is Neither B-form nor A-form in Solution. Biochemistry 1993, 32, 4207-4215.
28. Batey, R. T.; Rambo, R. P.; Doudna, J. A. Tertiary Motifs in RNA Structure and Folding. Angew. Chem., Int. Ed. 1999, 38, 2326-2343.
29. Westhof, E.; Fritsch, V. RNA Folding: Beyond Watson-Crick Pairs. Struct. Fold Des. 2000, 8, R55-R65.
30. 2. J. Am. Chem. Soc. 1991, 113, 5486-5488.
31. Leroy, J. L.; Gehring, K.; Kettani, A.; Gueron, M. Acid Multimers of Oligodeoxycytidine Strands: Stoichiometry, Base-Pair Characterization, and Proton Exchange Properties. Biochemistry 1993, 32, 6019-6031.
32. Moser, H. E.; Dervan, P. B. Sequence-Specific Cleavage of Double Helical DNA by Triple Helix Formation. Science 1987, 238, 645-650.
33. 4. Nature 1989, 239, 637-639.
34. + Base-Triple Formation. Biochemistry 1989, 28, 7282-7290.
35. 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, 19, 5625-5631.
36. Singleton, S. F.; Dervan, P. B. Influence of pH on the Equilibrium Association Constants for Oligodeoxyribonucleotide-Directed Triple Helix Formation at Single DNA Sites. Biochemistry 1992, 31, 10995-11003.
37. McPherson, A.; Jurnak, F.; Wang, A.; Kolpal, F.; Rich, A.; Molineux, I.; Fitzgerald, P. The Structure of A DNA Unwinding Protein and Its Complexes With Oligodeoxynucleotides by X-Ray- Diffraction. Biophys. J. 1980, 32, 155-173.
38. Delamaza, L. M.; Carter, B. J. Molecular Structure of Adeno-Associated Virus Variant DNA. J. Biol. Chem. 1980, 255, 3194-3203.
39. Guo, Q.; Lu, M.; Churchill, M. E. A.; Tullius, T. D.; Kallenbach, N. R. Asymmetric Structure of a Three-Arm DNA Junction. Biochemistry 1990, 29, 10927-10934.
40. Pina, B.; Truss, M.; Ohlenbusch, H.; Postma, J.; Beato, M. DNA Rotational Positioning in a Regulatory Nucleosome is Determined By Base Sequence - An Algorithm to Model the Preferred Superhelix. Nucleic Acids Res. 1990, 18, 6981-6987.
41. 4 - Methoxycytosine. Guanine Base-Pairs in Z-DNA. J. Mol. Biol. 1990, 216, 773-781.
42. Florian, J.; Leszczynski, J. Theoretical Investigation of the Molecular-Structure of the Pi-Kappa DNA-Base Pair. J. Biomol. Struct. Dyn. 1995, 12, 1055-1062.
43. Santamaria, R.; Quirozgutierrez, A.; Juarez, C. Structures and Energetic Properties of B-DNA Nucleotides. J. Mol. Struct.: THEOCHEM 1995, 357, 161-170.
44. Triolo, A.; Arcamone, F. M.; Raffaelli, A.; Salvadori, P. Non-Covalent Complexes Between DNA-Binding Drugs and Double-Stranded Deoxyoligonucleotides: A Study by Ionspray Mass Spectrometry. J. Mass Spectrom. 1997, 32, 1186-1194.
45. Wang, Z.; Wan, K. X.; Ramanathan, R.; Taylor, J. S.; Gross, M. L. Structure and Fragmentation Mechanism of Isomeric T-Rich Oligodeoxynucleotides: A Comparison of Four Tandem Mass Spectrometric Methods. J. Am. Soc. Mass Spectrom. 1998, 9, 683-691.
46. Cheatham, T. E.; Srinivasan, J.; Case, D. A.; Kollman, P. A. Molecular Dynamics and Continuum Solvent Studies of the Stability of polyG-polyC and polyA-polyT DNA Duplexes in Solution. J. Biomol. Struct. Dyn. 1998, 16, 265-280.
47. Kurnikov, I. V.; Tong, G. S. M.; Madrid, M.; Beratan, D. N. Hole Size and Energetics in Double Helical DNA: Competition Between Quantum Delocalization and Solvation Localization. J. Phys. Chem. B 2002, 106, 7-10.
48. 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, 8007-8014.
49. Guo, X. H.; Bruist, M. F.; Davis, D. L.; Bentzley, C. M. Secondary Structural Characterization of Oligonucleotide Strands Using Electrospray Ionization Mass Spectrometry. Nucleic Acids Res. 2005, 33, 3659-3666.
50. Balthasart, F.; Plavec, J.; Gabelica, V. Ammonium Ion Binding to DNA G-Quadruplexes: Do Electrospray Mass Spectra Faithfully Reflect the Solution-Phase Species? J. Am. Soc. Mass Spectrom. 2013, 24, 1-8.
51. Jaeger, J. A.; Turner, D. H.; Zuker, M. Predicting Optimal and Suboptimal Secondary Structure for RNA. Methods Enzymol. 1990, 183, 281-306.
52. Estes, P. A.; Cooke, N. E.; Liebhaber, S. A. A Native RNA Secondary Structure Controls Alternative Splice-Site Selection and Generates 2 Human Growth-Hormone Isoforms. J. Biol. Chem. 1992, 267, 14902-14908.
53. Gutell, R. R.; Power, A.; Hertz, G. Z.; Putz, E. J.; Stormo, G. D. Identifying Constraints on the Higher-Order Structure of RNA - Continued Development and Application of Comparative Sequence- Analysis Methods. Nucleic Acids Res. 1992, 20, 5785-5795.
54. Davis, D. R. Stabilization of RNA Stacking by Pseudouridine. Nucleic Acids Res. 1995, 23, 5020-5026.
55. Jones, S.; Daley, D. T. A.; Luscombe, N. M.; Berman, H. M.; Thornton, J. M. Protein-RNA Interactions: A Structural Analysis. Nucleic Acids Res. 2001, 29, 943-954.
56. Gooch, B. D.; Beal, P. A. Recognition of Duplex RNA by Helix-Threading Peptides. J. Am. Chem. Soc. 2004, 126, 10603-10610.
57. Koculi, E.; Hyeon, C.; Thirumalai, D.; Woodson, S. A. Charge Density of Divalent Metal Cations Determines RNA Stability. J. Am. Chem. Soc. 2007, 129, 2676-2682.
58. Zhang, A. Y. Q.; Bugaut, A.; Balasubramanian, S. A Sequence-Independent Analysis of the Loop Length Dependence of Intramolecular RNA G-Quadruplex Stability and Topology. Biochemistry 2011, 50, 7251-7258.
59. Philips, A.; Milanowska, K.; Lach, G.; Boniecki, M.; Rother, K.; Bujnicki, J. M. MetalionRNA: Computational Predictor of Metal-Binding Sites in RNA Structures. Bioinformatics 2012, 28, 198-205.
60. Nir, E.; Imhof, P.; Kleinermanns, K.; de Vries, M. S. REMPI Spectroscopy of Laser Desorbed Guanosines. J. Am. Chem. Soc. 2000, 122, 8091-8092.
61. Nir, E.; Grace, L.; Brauer, B.; de Vries, M. S. REMPI Spectroscopy of Jet-Cooled Guanine. J. Am. Chem. Soc. 1999, 121, 4896-4897.
62. Stueber, D.; Grant, D. M. C-13 and N-15 Chemical Shift Tensors in Adenosine, Guanosine Dihydrate, 2′-Deoxythymidine, and Cytidine. J. Am. Chem. Soc. 2002, 124, 10539-10551.
63. Stueber, D.; Guenneau, F. N.; Grant, D. M. The Calculation of C-13 Chemical Shielding Tensors in Ionic Compounds Utilizing Point Charge Arrays Obtained From Ewald Lattice Sums. J. Chem. Phys. 2001, 114, 9236-9243.
64. Valle, J. J.; Eyler, J. R.; Oomens, J.; Moore, D. T.; van der Meer, A. F. G.; von Heldon, G.; Meijer, G.; Hendrickson, C. L.; Marshall, A. G.; Blakney, G. T. Free Electron Laser-Fourier Transform Ion Cyclotron Resonance Mass Spectrometry Facility for Obtaining Infrared Multiphoton Dissociation Spectra of Gaseous Ions. Rev. Sci. Instrum. 2005, 76, 023103-1-023103-7.
65. Polfer, N. C.; Oomens, J.; Moore, D. T.; von Helden, G.; Meijer, G.; Dunbar, R. C. Infrared Spectroscopy of Phenylalanine Ag(I) and Zn(II) Complexes in the Gas Phase. J. Am. Chem. Soc. 2006, 128, 517-525.
66. Polfer, N. C.; Oomens, J. Reaction Products in Mass Spectrometry Elucidated with Infrared Spectroscopy. Phys. Chem. Chem. Phys. 2007, 9, 3804-3817.
67. Oepts, D.; van der Meer, A. F. G.; van Amersfoort, P. W. The Free-Electron-Laser User Facility FELIX. Infrared Phys. Techn. 1995, 36, 297-308.
68. HyperChem Computational Chemistry Software Package, Version 5.0; Hypercube, Inc., Gainsville, FL, 1997.
69. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; et al. Gaussian 09, Revision C.01; Gaussian, Inc.: Wallingford, CT, 2009.
70. Abo-riziq, A.; Crews, B. O.; Compagnon, I.; Oomens, J.; Meijer, G.; von Helden, G.; Kabelac, M.; Hobza, P.; de Vries, M. S. The Mid- IR Spectra of 9-Ethyl Guanine, Guanosine, and 2′-Deoxyguanosine. J. Phys. Chem. A 2007, 111, 7529-7536.
71. Wijmenga, S. S.; van Buuren, B. N. M. The Use of NMR Methods for Conformational Studies of Nucleic Acids. Prog. NMR Spectrosc. 1998, 32, 287-387.
72. Flinders, J.; Dieckmann, T. NMR Spectroscopy of Ribonucleic Acids. Prog. NMR Spectrosc. 2006, 48, 137-159.
73. Wimberly, B. T.; Brodersen, D. E.; Clemons, W. M.; Morgan-Warren, R. J.; Carter, A. P.; Vonrhein, C.; Hartsch, T.; Ramakrishnan, V. Structure of the 30S Ribosomal Subunit. Nature 2000, 407, 327-339.
74. Schuwirth, B. S.; Borovinskaya, M. A.; Hau, C. W.; Zhang, W.; Vila-Sanjurjo, A.; Holton, J. M.; Cate, J. H. D. Structures of the Bacterial Ribosome at 3.5 Angstrom Resolution. Science 2005, 310, 827-834.
75. Vokacova, Z.; Bickelhaupt, F. M.; Sponer, J. Y.; Sychrovsky, V. Structural Interpretation of J Coupling Constants in Guanosine and Deoxyguanosine: Modeling the Effects of Sugar Pucker, Backbone Conformation, and Base Pairing. J. Phys. Chem. A 2009, 113, 8379-8386.
76. Russo, N.; Toscano, M.; Grand, A.; Jolibis, F. Protonation of Thymine, Cytosine, Adenine, and Guanine DNA Nucleic Acid Bases: Theoretical Investigation into the Framework of Density Functional Theory. J. Comput. Chem. 1998, 9, 989-1000.