Abstract
Canonical Watson-Crick base pairs and four representative mismatched base pairs have been studied by quantum chemical computations. Detailed anharmonic vibrational analysis was carried out to reveal some vibrational signatures characteristic of structural aspects of the base monomers and dimers, which were well manifested in simulated 1D IR and 2D IR spectra. The degree of delocalization of the selected normal modes, represented by the potential energy distribution, was found to vary significantly from isolated bases to H-bonded dimers, and was accompanied by changes in anharmonicities of these modes. Examples are given for the generally accepted carbonyl stretching mode of base pairs appearing in the 6-μm wavelength region of IR spectra.
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References
Watson JD, Crick FHC. Molecular structure of nucleic acids. Nature, 1953, 171: 737–738
Saenger W. Principles of Nucleic Acid Structure. New York: Springer-Verlag, 1984
Dai J, Attila A, Hurley LH, Yang D. A direct and nondestructive approach to determine the folding structure of the I-Motif DNA secondary structure by NMR. J Am Chem Soc, 2009, 131: 6102–6104
Hartmut F. Infrared linear dichroism studies of DNA-drug complexes: Quantitative determination of the drug-induced restriction of the B-A transition. Nucleic Acids Res, 1994, 22: 787–791
Mazur AK. Titration in silico of reversible B-A transitions in DNA. J Am Chem Soc, 2003, 125: 7849–7859
Mazur AK. Electrostatic polymer condensation and the A/B polymorphism in DNA: Sequence effects. J Chem Theo Com, 2005, 1: 325–336
Tunis-Schneider MJ, Maestre MF. Circular dichroism spectra of oriented and unoriented deoxyribonucleic acid films—A preliminary study. J Mol Biol, 1970, 52: 521–541
Ivanov VI, Lyudmila EM, Minyat EE, Frank-Kamenetskii MD, Schyolkina AK. The B to A transition of DNA in solution. J Mol Biol, 1974, 87: 817–833
Catasti P, Chen X, Mariappan SVS, Bradbury EM, Gupta G. DNA repeats in the human genome. Genetica, 1999, 106: 15–36
Seela F, Budow S. Mismatch formation in solution and on DNA microarrays: how modified nucleosides can overcome shortcomings of imperfect hybridization caused by oligonucleotide composition and base pairing. Mol BioSyst, 2008, 4: 232–245
Davis JT. G-Quartets 40 years later: From 5-GMP to molecular biology and supramolecular chemistry. Angew Chem, Int Ed, 2004, 43: 686–698
Gehring K, Leroy J-L, Guéron M. A tetrameric DNA structure with protonated cytosine-cytosine base pairs. Nature, 1993, 363: 561–565
SantaLucia JJ, Hicks D. The thermodynamics of DNA structural motifs. Annu Rev Biophys Bimol Struct, 2004, 33: 415–440
Peyret PN, Seneviratne A, Allawi HT, SantaLucia JJ. Nearest-neighbor thermodynamics and NMR of DNA sequences with internal A·A, C·C, G·G, and T·T mismatches. Biochemistry, 1999, 38: 3468–3477
Hunter NW, Brown T, Anand NN, Olga K. Structure of an adenine-cytosine base pair in DNA and its implications for mismatch repair. Nature, 1986, 320: 552–555
Boulard Y, Cognet JAH, Gabarro-Arpa J, Le Bret M, Sowers LC, Fazakerley GV. The pH dependent configurations of the C·A mispair in DNA. Nucl Acids Res, 1992, 20: 1933–1941
Boulard Y, Cognet JAH, Fazakerley GV. Solution structure as a function of pH of two central mismatches, C-T and C-C, in the 29 to 39 K-ras gene sequence, by nuclear magnetic resonance and molecular dynamics. J Mol Biol, 1997, 268: 331–347
Brown T, Leonard GA, Booth ED, Kneale G. Influence of pH on the conformation and stability of mismatch base-pairs in DNA. J Mol Biol, 1990, 212: 437–440
Jayaram B, Sprous D, Young MA, Beveridge DL. Free energy analysis of the conformational preferences of A and B forms of DNA in solution. J Am Chem Soc, 1998, 120: 10629–10633
Darlow JM, Leach DRF. Secondary structures in d(CGG) and d(CCG) repeat tracts. J Mol Biol, 1998, 275: 3–16
Nir E, Kleinermanns K, de Vries MS. Pairing of isolated nucleic-acid bases in the absence of the DNA backbone. Nature, 2000, 408: 949–951
Khandogin J, York DM. Quantum mechanical characterization of nucleic acids in solution: A linear-scaling study of charge fluctuations in DNA and RNA. J Phys Chem B, 2002, 106: 7693–7703
Sychrovsky V, Vacek J, Hobza P, Zidek L, Sklenar V, Cremer D. Exploring the structure of a DNA hairpin with the help of NMR spin-spin coupling constants: An experimental and quantum chemical investigation. J Phys Chem B, 2002, 106: 10242–10250
Jurećka P, Hobza P. True stabilization energies for the optimal planar hydrogen-bonded and stacked structures of guanine — cytosine, adenine—thymine, and their 9- and 1-methyl derivatives: Complete basis set calculations at the MP2 and CCSD(T) levels and comparison with experiment. J Am Chem Soc, 2003, 125: 15608–15613
Isaacs RJ, Spielmann HP. Insight into G-T mismatch recognition using molecular dynamics with time-averaged restraints derived from NMR spectroscopy. J Am Chem Soc, 2004, 126: 583–590
Banavali NK, Roux B. Free energy landscape of A-DNA to B-DNA conversion in aqueous solution. J Am Chem Soc, 2005, 127: 6866–6876
Svozil D, Hobza P, Šponer J. Comparison of intrinsic stacking energies of ten unique dinucleotide steps in A-RNA and B-DNA duplexes. Can we determine correct order of stability by quantum-chemical Calculations? J Phys Chem B, 2010, 114: 1191–1203
Asplund MC, Zanni MT, Hochstrasser RM. Two-dimensional infrared spectroscopy of peptides by phase-controlled femtosecond vibrational photon echoes. Proc Natl Acad Sci USA, 2000, 97: 8219–8224
Khalil M, Demirdoven N, Tokmakoff A. Coherent 2D IR spectroscopy: Molecular structure and dynamics in solution. J Phys Chem A, 2003, 107: 5258–5279
Bredenbeck J, Helbing J, Behrendt R, Renner C, Moroder L, Wachtveitl J, Hamm P. Transient 2D-IR spectroscopy: Snapshots of the nonequilibrium ensemble during the picosecond conformational transition of a small peptide. J Phys Chem B, 2003, 107: 8654–8660
Ding F, Fulmer EC, Zanni MT. Heterodyned fifth-order two-dimensional IR spectroscopy: Third-quantum states and polarization selectivity. J Chem Phys, 2005, 123: 094502/1–094502/13
Wang J, Chen J, Hochstrasser RM. Local structure of β-hairpin isotopomers by FTIR, 2D IR, and ab initio theory. J Phys Chem B, 2006, 110: 7545–7555
Kolano C, Helbing J, Kozinski M, Sander W, Hamm P. Watching hydrogen-bond dynamics in a β-turn by transient two-dimensional infrared spectroscopy. Nature, 2006, 444: 469–472
Zhuang W, Abramavicius D, Hayashi T, Mukamel S. Simulation protocols for coherent femtosecond vibrational spectra of peptides. J Phys Chem B, 2006, 110: 3362–3374
Maekawa H, Toniolo C, Broxterman QB, Ge N-H. Two-dimensional infrared spectral signatures of 310- and α-selical peptides. J Phys Chem B, 2007, 111: 3222–3235
Vorobyev DY, Kuo C-H, Kuroda DG, Scott JN, Vanderkooi JM, Hochstrasser RM. Water-induced relaxation of a degenerate vibration of guanidinium using 2D IR echo spectroscopy. J Phys Chem B, 2010, 114: 2944–2953
Maekawa H, Poli MD, Moretto A, Toniolo C, Ge N-H. Toward detecting the formation of a fingle helical turn by 2D IR cross peaks between the amide-I and -II modes. J Phys Chem B, 2009, 113: 11775–11786
Ling YL, Strasfeld DB, Shim S-H, Raleigh DP, Zanni MT. Two-dimensional infrared spectroscopy provides evidence of an intermediate in the membrane-catalyzed assembly of diabetic amyloid. J Phys Chem B, 2009, 113: 2498–2505
Zheng ML, Zheng DC, Wang J. Non-native side chain IR probe in peptides: Ab initio computation and 1D and 2D IR spectral simulation. J Phys Chem B, 2010, 114: 2327–2336
Hamm P, Lim M, DeGrado WF, Hochstrasser RM. The two-dimensional IR nonlinear spectroscopy of a cyclic penta-peptide in relation to its three-dimensional structure. Proc Natl Acad Sci USA, 1999, 96: 2036–2041
Krimm S, Bandekar J. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv Protein Chem, 1986, 38: 181–364
Wang J. Ab initio-based all-mode two-dimensional infrared spectroscopy of a sugar molecule. J Phys Chem B, 2007, 111: 9193–9196
Fodor SPA, Spiro TG. Ultraviolet resonance Raman spectroscopy of DNA with 200–266-nm laser excitation. J Am Chem Soc, 1986, 108: 3198–3205
Krummel AT, Zanni MT. DNA vibrational coupling revealed with two-dimensional infrared spectroscopy: Insight into why vibrational spectroscopy is sensitive to DNA structure. J Phys Chem B, 2006, 110: 13991–14000
Woutersen S, Cristalli G. Strong enhancement of vibrational relaxation by Watson-Crick base pairing. J Chem Phys, 2004, 121: 5381–5386
Heyne K, Krishnan GM, Kühn O. Revealing anharmonic couplings and energy relaxation in DNA oligomers by ultrafast infrared spectroscopy. J Phys Chem B, 2008, 112: 7909–7915
Dwyer JR, Szyc Ł, Nibbering ETJ, Elsaesser T. Ultrafast vibrational dynamics of adenine-thymine base pairs in DNA oligomers. J Phys Chem B, 2008, 112: 11194–11197
Lee C, Park K, Kim J, Hahn S, Cho M. Vibrational dynamics of DNA. III. Molecular dynamics simulations of DNA in water and theoretical calculations of the two-dimensional vibrational spectra J Chem Phys, 2006, 125: 114510
Lee C, Park K-H, Cho M. Vibrational dynamics of DNA. I. Vibrational basis modes and couplings. J Chem Phys, 2006, 125: 114508–16
Biczysko M, Panek P, Barone V. Toward spectroscopic studies of biologically relevant systems: Vibrational spectrum of adenine as a test case for performances of long-range/dispersion corrected density functionals. Chem Phys Lett, 2009, 475: 105–110
Barone V, Festa G, Grandi A, Rega N, Sanna N. Accurate vibrational spectra of large molecules by density functional computations beyond the harmonic approximation: The case of uracil and 2-thiouracil. Chem Phys Lett, 2004, 388: 279–283
Brauer B, Gerber RB, Kabeláč M, Hobza P, Bakker JM, Abo Riziq AG, de Vries MS. Vibrational spectroscopy of the G—C base pair: Experiment, harmonic and anharmonic calculations, and the nature of the anharmonic couplings. J Phys Chem A, 2005, 109: 6974–6984
Wang G, Ma X, Wang J. Anharmonic vibrational signatures of DNA bases and Watson-Crick base pairs. Chin J Chem Phys, 2009, 22: 563–570
Wang J. Conformational dependence of anharmonic Vibrations in peptides: Amide-I modes in model dipeptide. J Phys Chem B, 2008, 112: 4790–4800
Brown T, Hunter WN, Kneale G, Kennard O. Molecular structure of the G.A base pair in DNA and its implications for the mechanism of transversion mutations. Proc Natl Acad Sci USA, 1986, 83: 2402–2406
Wang S, Schaefer III HF. The small planarization barriers for the amino group in the nucleic acid bases. J Chem Phys, 2006, 124: 044303
Oliva R, Cavallo L, Tramontano A. Accurate energies of hydrogen bonded nucleic acid base pairs and triplets in tRNA tertiary interactions. Nucl Acids Res, 2006, 34: 865–879
Hobza P, Sponer J. Structure, energetics, and dynamics of the nucleic acid base pairs: Nonempirical ab initio calculations. Chem Rev, 1999, 99: 3247–3276
Berashevich J, Chakraborty T. Thermodynamics of G·A mispairs in DNA: Continuum electrostatic model. J Chem Phys, 2009, 130: 015101
Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Vreven JT, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA, Gaussian 03, Revision B05. Gaussian, Inc., Pittsburgh PA, 2003
Barone V. Anharmonic vibrational properties by a fully automated second-order perturbative approach. J Chem Phys, 2005, 122: 014108
Califano S. Vibrational States. London, New York, Sydney, Toronto: John Wiley and Sons, 1976
Wang J, Hochstrasser RM. Anharmonicity of amide modes. J Phys Chem B, 2006, 110: 3798–3807
Hinchliffe A. Modelling Molecular Structures. Chichester, New York: John Wiley & Sons Ltd., 2000
Gould IR, Kollman PA. Theoretical investigation of the hydrogen bond strengths in guanine-cytosine and adenine-thymine base pairs. J Am Chem Soc, 1994, 116: 2493–2499
Jeffrey GA. An Introduction to Hydrogen Bonding. New York: Oxford University Press, 1997
Sponer J, Leszczynski J, Hobza P. Structures and energies of hydrogen-bonded DNA base pairs. A nonempirical study with inclusion of electron correlation. J Phys Chem, 1996, 100: 1965–1974
Rosenberg JM, Seeman NC, Day RO, Rich A. RNA double-helical fragments at atomic resolution: II. The crystal structure of sodium guanylyl-3′,5′-cytidine nonahydrate. J Mol Biol, 1976, 104: 145–167
Asensio A, Kobko N, Dannenberg JJ. Cooperative hydrogen-bonding in adenine-thymine and guanine-cytosine base pairs. Density functional theory and Mϕller-Plesset molecular orbital study. J Phys Chem A, 2003, 107: 6441–6443
Grunenberg J. Direct assessment of interresidue forces in Watson-Crick base pairs using theoretical compliance constants. J Am Chem Soc, 2004, 126: 16310–16311
Grunenberg J, Streubel R, von Frantzius G, Marten W. The strongest bond in the universe? Accurate calculation of compliance matrices for the ions N2H+, HCO+, and HOC+. J Chem Phys, 2003, 119: 165–169
Swart M, Fonseca Guerra C, Bickelhaupt FM. Hydrogen bonds of RNA are stronger than those of DNA, but NMR monitors only presence of methyl substituent in uracil/thymine. J Am Chem Soc, 2004, 126: 16718–16719
Vakonakis I, LiWang AC. N1—N3 Hydrogen Bonds of A:U Base Pairs of RNA Are Stronger than Those of A:T Base Pairs of DNA. J Am Chem Soc, 2004, 126: 5688–5689
Jiří Š, Petr J, Hobza P. Accurate interaction energies of hydrogen-bonded nucleic acid base pairs. J Am Chem Soc, 2004, 126: 10142–10151
Krummel AT, Mukherjee P, Zanni MT. Inter and intrastrand vibrational coupling in DNA studied with heterodyned 2D-IR spectroscopy. J Phys Chem B, 2003, 107: 9165–9169
Park J, Hochstrasser RM. Multidimensional infrared spectroscopy of a peptide intramolecular hydrogen bond. Chem Phys, 2006, 323: 78–96
Cai K, Wang J. Multiple anharmonic vibrational probes of sugar structure and dynamics. J Phys Chem B, 2009, 113: 1681–1692
Cances E, Mennucci B, Tomasi J. A new integral equation formalism for the polarizable continuum model: Theoretical background and applications to isotropic and anisotropic dielectrics. J Chem Phys, 1997, 107: 3032–3041
Zanni MT, Asplund MC, Hochstrasser RM. Two-dimensional heterodyned and stimulated infrared photon echoes of N-methylace-tamide-D. J Chem Phys, 2001, 114: 4579–4590
Zanni MT, Ge N-H, Kim YS, Hochstrasser RM. Two-dimensional IR spectroscopy can be designed to eliminate the diagonal peaks and expose only the crosspeaks needed for structure determination. Proc Natl Acad Sci USA, 2001, 98: 11265–11270
Demirdöven N, Khalil M, Golonzka O, Tokmakoff A. Correlation effects in the two-dimensional vibrational spectroscopy of coupled vibrations. J Phys Chem A, 2001, 105: 8025–8030
Ge N-H, Zanni MT, Hochstrasser RM. Effects of vibrational frequency correlations on two-dimensional infrared spectra. J Phys Chem A, 2002, 106: 962–972
Mukamel S, Abramavicius D. Many-body approaches for simulating coherent nonlinear spectroscopies of electronic and vibrational excitons. Chem Rev, 2004, 104: 2073–2098
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Wang, G., Zhao, J. & Wang, J. Anharmonic vibrations of nucleobases: Structural basis of one- and two-dimensional infrared spectra for canonical and mismatched base pairs. Sci. China Chem. 54, 1590–1606 (2011). https://doi.org/10.1007/s11426-011-4309-8
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DOI: https://doi.org/10.1007/s11426-011-4309-8