DNA-protein π-interactions in nature: Abundance, structure, composition and strength of contacts between aromatic amino acids and DNA nucleobases or deoxyribose sugar

Nucleic Acids Research

Volumn 42, Issue 10, 2014, Pages 6726-6741

  Wilson, Katie A ^a   Kellie, Jennifer L ^a   Wetmore, Stacey D ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC AMINO ACID; DEOXYRIBOSE SUGAR; DNA NUCLEOBASE; HISTIDINE; NUCLEIC ACID BASE; SUGAR; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; MOLECULAR STABILITY; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN LOCALIZATION; STRUCTURAL BIOINFORMATICS; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS;

AMINO ACIDS, AROMATIC; DEOXYRIBOSE; DNA; DNA-BINDING PROTEINS; HISTIDINE; MODELS, MOLECULAR; PHENYLALANINE; PROTEIN BINDING; TRYPTOPHAN; TYROSINE;

EID: 84903191755     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku269     Document Type: Article

References (130)

1. Ciccia, A. and Elledge, S.J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell, 40, 179-204.
2. Hoeijmakers, J.H.J. (2001) Genome maintenance mechanisms for preventing cancer. Nature, 411, 366-374.
3. Jackson, S.P. and Bartek, J. (2009) The DNA-damage response in human biology and disease. Nature, 461, 1071-1078.
4. Stivers, J.T. and Jiang, Y.L. (2003) A mechanistic perspective on the chemistry of DNA repair glycosylases. Chem. Rev., 103, 2729-2759.
5. von Hippel, P.H. and Berg, O.G. (1986) On the specificity of DNA-protein interactions. Proc. Natl. Acad. Sci. U.S.A., 83, 1608-1612.
6. Rohs, R., Jin, X., West, S.M., Joshi, R., Honig, B. and Mann, R.S. (2010) Origins of specificity in protein-DNA recognition. Ann. Rev. Biochem., 79, 233-269.
7. Luscombe, N.M., Laskowski, R.A. and Thornton, J.M. (2001) Amino acid-base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucleic Acids Res., 29, 2860-2874.
8. Baker, C.M. and Grant, G.H. (2007) Role of aromatic amino acids in protein-nucleic acid recognition. Biopolymers, 85, 456-470.
9. Rutledge, L.R. and Wetmore, S.D. (2010), Quantum biochemistry. Wiley-VCH Verlag GmbH & Co. KGaA, pp. 307-336.
10. Mavromoustakos, T., Durdagi, S., Koukoulitsa, C., Simcic, M., G. Papadopoulos, M., Hodoscek, M. and Golic Grdadolnik, S. (2011) Strategies in the rational drug design. Curr. Med. Chem., 18, 2517-2530.
11. Speck-Planche, A., Kleandrova, V.V., Luan, F. and Cordeiro, M.N.D.S. (2012) Rational drug design for anti-cancer chemotherapy: multi-target QSAR models for the in silico discovery of anti-colorectal cancer agents. Bioorg. Med. Chem., 20, 4848-4855.
12. Bultinck, J., Lievens, S. and Tavernier, J. (2012) Protein-protein interactions: network analysis and applications in drug discovery. Curr. Pharm. Des., 18, 4619-4629.
13. Dermitzakis, E.T. (2008) From gene expression to disease risk. Nat. Genet., 40, 492-493.
14. Cuccato, G., Gatta, G.D. and di Bernardo, D. (2009) Systems and synthetic biology: tackling genetic networks and complex diseases. Heredity, 102, 527-532.
15. Stranger, B.E. and Dermitzakis, E.T. (2006) From DNA to RNA to disease and back: the 'central dogma'of regulatory disease variation. Coron. Artery Dis., 2, 383-390.
16. Stranger, B.E. and Raj, T. (2013) Genetics of human gene expression. Curr. Opin. Genet. Dev., 23, 627-634.
17. Matthews, B.W. (1988) No code for recognition. Nature, 335, 294-295.
18. Pabo, C.O. and Sauer, R.T. (1992) Transcription factors: structural families and principles of DNA recognition. Annu. Rev. Biochem., 61, 1053-1095.
19. Suzuki, M. (1994) A framework for the DNA-protein recognition code of the probe helix in transcription factors: the chemical and stereochemical rules. Structure, 2, 317-326.
20. Mandel-Gutfreund, Y., Schueler, O. and Margalit, H. (1995) Comprehensive analysis of hydrogen bonds in regulatory protein DNA-complexes: in search of common principles. J. Mol. Biol., 253, 370-382.
21. Luscombe, N.M. and Thornton, J.M. (2002) Protein-DNA interactions: amino acid conservation and the effects of mutations on binding specificity. J. Mol. Biol., 320, 991-1009.
22. Lejeune, D., Delsaux, N., Charloteaux, B., Thomas, A. and Brasseur, R. (2005) Protein-nucleic acid recognition: statistical analysis of atomic interactions and influence of DNA structure. Proteins: Struct. Funct. Bioinform., 61, 258-271.
23. Sathyapriya, R., Vijayabaskar, M. and Vishveshwara, S. (2008) Insights into protein-DNA interactions through structure network analysis. PLoS Comput. Biol., 4, e1000170.
24. Meyer, E.A., Castellano, R.K. and Diederich, F. (2003) Interactions with aromatic rings in chemical and biological recognition. Angew. Chem. Int. Ed. Engl., 42, 1210-1250.
25. Salonen, L.M., Ellermann, M. and Diederich, F. (2011) Aromatic rings in chemical and biological recognition: energetics and structures. Angew. Chem. Int. Ed., 50, 4808-4842.
26. Brandl, M., Weiss, M.S., Jabs, A., Sühnel, J. and Hilgenfeld, R. (2001) C-H⋯ π interactions in proteins. J. Mol. Biol., 307, 357-377.
27. Thomas, A., Meurisse, R., Charloteaux, B. and Brasseur, R. (2002) Aromatic side-chain interactions in proteins. I. Main structural features. Proteins: Struct. Funct. Bioinform., 48, 628-634.
28. Thomas, A., Meurisse, R. and Brasseur, R. (2002) Aromatic side-chain interactions in proteins. II. Near- and far-sequence phe-X pairs. Proteins: Struct. Functi. Bioinform., 48, 635-644.
29. Meurisse, R., Brasseur, R. and Thomas, A. (2003) Aromatic side-chain interactions in proteins. Near- and far-sequence his-X pairs. Biochim. Biophys. Acta, 1649, 85-96.
30. Chourasia, M., Sastry, G.M. and Sastry, G.N. (2011) Aromatic-aromatic interactions database, A2ID: an analysis of aromatic π-networks in proteins. Int. J. Biol. Macromol., 48, 540-552.
31. Jenkins, D.D., Harris, J.B., Howell, E.E., Hinde, R.J. and Baudry, J. (2013) STAAR: statistical analysis of aromatic rings. J. Comput. Chem., 34, 518-522.
32. Yan, C., Wu, F., Jernigan, R.L., Dobbs, D. and Honavar, V. (2008) Characterization of protein-protein interfaces. The Protein Journal, 27, 59-70.
33. Ellis, J.J., Broom, M. and Jones, S. (2007) Protein-RNA interactions: structural analysis and functional classes. Proteins: Struct. Funct. Bioinform., 66, 903-911.
34. Mao, L., Wang, Y., Liu, Y. and Hu, X. (2004) Molecular determinants for ATP-binding in proteins: a data mining and quantum chemical analysis. J. Mol. Biol., 336, 787-807.
35. Řezáč, J., Riley, K.E. and Hobza, P. (2012) Evaluation of the performance of post-hartree-fock methods in terms of intermolecular distance in noncovalent complexes. J. Comput. Chem., 33, 691-694.
36. Sherrill, C.D. (2012) Energy component analysis of π interactions. Acc. Chem. Res., 46, 1020-1028.
37. Riley, K.E. and Hobza, P. (2011) Noncovalent interactions in biochemistry. Wiley Interdiscip. Rev. Comput. Mol. Sci., 1, 3-17.
38. Grimme, S. and Steinmetz, M. (2013) Effects of london dispersion correction in density functional theory on the structures of organic molecules in the gas phase. Phys. Chem. Chem. Phys., 15, 16031-16042.
39. Johnson, E.R., Otero-de-la-Roza, A., Dale, S.G. and DiLabio, G.A. (2013) Efficient basis sets for non-covalent interactions in XDM-corrected density-functional theory. J. Chem. Phys, 139, 214109.
40. Copeland, K.L., Anderson, J.A., Farley, A.R., Cox, J.R. and Tschumper, G.S. (2008) Probing phenylalanine/adenine pi-stacking interactions in protein complexes with explicitly correlated and CCSD(T) computations. J. Phys. Chem. B, 112, 14291-14295.
41. Cauet, E., Rooman, M., Wintjens, R., Lievin, J. and Biot, C. (2005) Histidine-aromatic interactions in proteins and protein-ligand complexes: quantum chemical study of X-ray and model structures. J. Chem. Theory Comput., 1, 472-483.
42. Copeland, K.L., Pellock, S.J., Cox, J.R., Cafiero, M.L. and Tschumper, G.S. (2013) Examination of tyrosine/adenine stacking interactions in protein complexes. J. Phys. Chem. B, 117, 14001-14008.
43. Cysewski, P. (2008) A Post-SCF complete basis set study on the recognition patterns of uracil and cytosine by aromatic and π-aromatic stacking interactions with amino acid residues. Phys. Chem. Chem. Phys., 10, 2636-2645.
44. Riley, K.E., Pitoňaḱ, M., Černý, J.I. and Hobza, P. (2010) On the structure and geometry of biomolecular binding motifs (hydrogen-bonding, stacking, X-H⋯π): WFT and DFT calculations. J. Chem. Theory Comput., 6, 66-80.
45. Rutledge, L.R., Campbell-Verduyn, L.S. and Wetmore, S.D. (2007) Characterization of the stacking interactions between DNA or RNA nucleobases and the aromatic amino acids. Chem. Phys. Lett., 444, 167-175.
46. Rutledge, L.R., Durst, H.F. and Wetmore, S.D. (2009) Evidence for stabilization of DNA/RNA-protein complexes arising from nucleobase-amino acid stacking and T-shaped interactions. J. Chem. Theory Comput., 5, 1400-1410.
47. Rutledge, L.R., Campbell-Verduyn, L.S., Hunter, K.C. and Wetmore, S.D. (2006) Characterization of nucleobase-amino acid stacking interactions utilized by a DNA repair enzyme. J. Phys. Chem. B, 110, 19652-19663.
48. Wells, R.A., Kellie, J.L. and Wetmore, S.D. (2013) Significant strength of charged DNA-protein π-π interactions: a preliminary study of cytosine. J. Phys. Chem. B, 117, 10462-10474.
49. Churchill, C.D.M. and Wetmore, S.D. (2009) Noncovalent interactions involving histidine: the effect of charge on π-π stacking and T-shaped interactions with the DNA nucleobases. J. Phys. Chem. B, 113, 16046-16058.
50. Rutledge, L.R. and Wetmore, S.D. (2010) The Assessment of density functionals for DNA-protein stacked and T-shaped complexes. Can. J. Chem., 88, 815-830.
51. Rutledge, L.R., Durst, H.F. and Wetmore, S.D. (2008) Computational comparison of the stacking interactions between the aromatic amino acids and the natural or (Cationic) methylated nucleobases. Phys. Chem. Chem. Phys., 10, 2801-2812.
52. Rutledge, L.R. and Wetmore, S.D. (2008) Remarkably strong T-shaped interactions between aromatic amino acids and adenine: their increase upon nucleobase methylation and a comparison to stacking. J. Chem. Theory Comput., 4, 1768-1780.
53. Leavens, F.M.V., Churchill, C.D.M., Wang, S. and Wetmore, S.D. (2011) Evaluating how discrete water molecules affect protein-DNA π-π and π+-π stacking and T-shaped interactions: the case of histidine-adenine dimers. J. Phys. Chem. B, 115, 10990-11003.
54. Churchill, C.D.M., Navarro-Whyte, L., Rutledge, L.R. and Wetmore, S.D. (2009) Effects of the biological backbone on DNA-protein stacking interactions. Phys. Chem. Chem. Phys., 11, 10657-10670.
55. Churchill, C.D.M., Rutledge, L.R. and Wetmore, S.D. (2010) Effects of the biological backbone on sacking interactions at DNA-protein interfaces: the interplay between the backbone-π and π-π components. Phys. Chem. Chem. Phys., 12, 14515-14526.
56. Rutledge, L.R., Navarro-Whyte, L., Peterson, T.L. and Wetmore, S.D. (2011) Effects of extending the computational model on DNA-protein T-shaped interactions: the case of adenine-histidine dimers. J. Phys. Chem. A, 115, 12646-12658.
57. Rutledge, L.R., Churchill, C.D.M. and Wetmore, S.D. (2010) A preliminary investigation of the additivity of π-π or π+-π stacking and T-shaped interactions between natural or damaged DNA nucleobases and histidine. J. Phys. Chem. B, 114, 3355-3367.
58. Spiwok, V., Lipovová, P., Skálová, T., Buchtelová, E., Hašek, J. and Králová, B. (2004) Role of CH/π interactions in substrate binding by escherichia coli β-galactosidase. Carbohydr. Res., 339, 2275-2280.
59. Spiwok, V., Lipovová, P., Skálová, T., Vondráčková, E., Dohnálek, J., Hašek, J. and Králová, B. (2006) Modelling of carbohydrate-aromatic interactions: ab initio energetics and force field performance. J. Comput. Aided Mol. Des., 19, 887-901.
60. Sujatha, M.S., Sasidhar, Y.U. and Balaji, P.V. (2004) Energetics of galactose- and glucose-aromatic amino acid interactions: implications for binding in galactose-specific proteins. Protein Science, 13, 2502-2514.
61. Wimmerová, M., Kozmon, S., Nečasová, I., Mishra, S.K., Komárek, J. and Koča, J. (2012) Stacking interactions between carbohydrate and protein quantified by combination of theoretical and experimental methods. PLoS ONE, 7, e46032.
62. Asensio, J.L., Ardá, A., Cañada, F.J. and Jiménez-Barbero, J. (2012) Carbohydrate-aromatic interactions. Acc. Chem. Res., 46, 946-954.
63. Tatko, C. (2008) Sugars stack up. Nat. Chem. Biol., 4, 586-587.
64. Laughrey, Z.R., Kiehna, S.E., Riemen, A.J. and Waters, M.L. (2008) Carbohydrate-π interactions: what are they worth? J. Am. Chem. Soc., 130, 14625-14633.
65. Lee, Y.C. and Lee, R.T. (1995) Carbohydrate-protein interactions: basis of glycobiology. Acc. Chem. Res., 28, 321-327.
66. Stanca-Kaposta, E.C., Çarçabal, P., Cocinero, E.J., Hurtado, P. and Simons, J.P. (2013) Carbohydrate-aromatic interactions: vibrational spectroscopy and structural assignment of isolated monosaccharide complexes with p-hydroxy toluene and N-acetyl l-tyrosine methylamide. J. Phys. Chem. B, 117, 8135-8142.
67. Kumari, M., Sunoj, R.B. and Balaji, P.V. (2012) Exploration of CH⋯ π mediated stacking interactions in saccharide: aromatic residue complexes through conformational sampling. Carbohydr. Res., 361, 133-140.
68. V. Balaji, P. (2011) Contribution of C-H⋯ π; interactions to the affinity and specificity of carbohydrate binding sites. Mini-Rev. Org. Chem., 8, 222-228.
69. Cao, M., Fu, A., Wang, Z., Liu, J., Kong, N., Zong, X., Liu, H. and Gooding, J.J. (2014) Electrochemical and theoretical study of π-π stacking interactions between graphitic surfaces and pyrene derivatives. J. Phys. Chem. C, 118, 2650-2659.
70. Cho, Y., Min, S.K., Yun, J., Kim, W.Y., Tkatchenko, A. and Kim, K.S. (2013) Noncovalent interactions of DNA bases with naphthalene and graphene. J. Chem. Theory Comput., 9, 2090-2096.
71. Gazit, E. (2007) Self-assembled peptide nanostructures: the design of molecular building blocks and their technological utilization. Chem. Soc. Rev., 36, 1263-1269.
72. Kumar, R.M., Elango, M. and Subramanian, V. (2010) Carbohydrate-aromatic interactions: the role of curvature on XH⋯π interactions. J. Phys. Chem. A, 114, 4313-4324.
73. Sharma, R., McNamara, J.P., Raju, R.K., Vincent, M.A., Hillier, I.H. and Morgado, C.A. (2008) The interaction of carbohydrates and amino acids with aromatic systems studied by density functional and semi-empirical molecular orbital calculations with dispersion corrections. Phys. Chem. Chem. Phys., 10, 2767-2774.
74. Cozens, C., Pinheiro, V.B., Vaisman, A., Woodgate, R. and Holliger, P. (2012) A short adaptive path from DNA to RNA polymerases. Proc. Natl. Acad. Sci. U.S.A., 109, 8067-8072.
75. Tsuzuki, S., Uchimaru, T. and Mikami, M. (2009) Magnitude and nature of carbohydrate-aromatic interactions: ab initio calculations of fucose-benzene complex. J. Phys. Chem. B, 113, 5617-5621.
76. Kozmon, S., Matuška, R., Spiwok, V. and Koča, J. (2011) Three-dimensional potential energy surface of selected carbohydrates' CH/π dispersion interactions calculated by high-level quantum mechanical methods. Chem. Eur. J., 17, 5680-5690.
77. Ramirez-Gualito, K., Alonso-Rios, R., Quiroz-Garcia, B., Rojas-Aguilar, A., Diaz, D., Jimenez-Barbero, J. and Cuevas, G. (2009) enthalpic nature of the CH/pi interaction involved in the recognition of carbohydrates by aromatic compounds, confirmed by a novel interplay of NMR, calorimetry, and theoretical calculations. J. Am. Chem. Soc., 131, 18129-18138.
78. Raju, R.K., Hillier, I.H., Burton, N.A., Vincent, M.A., Doudou, S. and Bryce, R.A. (2010) The effects of perfluorination on carbohydrate-π interactions: computational studies of the interaction of benzene and hexafluorobenzene with fucose and cyclodextrin. Phys. Chem. Chem. Phys., 12, 7959-7967.
79. Bautista-Ibanez, L., Ramirez-Gualito, K., Quiroz-Garcia, B., Rojas-Aguilar, A. and Cuevas, G. (2008) Calorimetric measurement of the CH/pi interaction involved in the molecular recognition of saccharides by aromatic compounds. J. Org. Chem., 73, 849-857.
80. Raju, R.K., Ramraj, A., Vincent, M.A., Hillier, I.H. and Burton, N.A. (2008) Carbohydrate-protein recognition probed by density functional theory and Ab initio calculations including dispersive interactions. Phys. Chem. Chem. Phys., 10, 6500-6508.
81. Su, Z., Cocinero, E.J., Stanca-Kaposta, E.C., Davis, B.G. and Simons, J.P. (2009) Carbohydrate-aromatic interactions: a computational and IR spectroscopic investigation of the complex, methyl alpha-L- fucopyranoside·toluene, isolated in the gas phase. Chem. Phys. Lett., 471, 17-21.
82. Stanca-Kaposta, E.C., Gamblin, D.P., Screen, J., Liu, B., Snoek, L.C., Davis, B.G. and Simons, J.P. (2007) Carbohydrate molecular recognition: a spectroscopic investigation of carbohydrate-aromatic interactions. Phys. Chem. Chem. Phys., 9, 4444-4451.
83. Tsuzuki, S., Uchimaru, T. and Mikami, M. (2011) Magnitude and nature of carbohydrate-aromatic interactions in fucose-phenol and fucose-indole complexes: CCSD(T) level interaction energy calculations. J. Phys. Chem. A, 115, 11256-11262.
84. Mohamed, M.N.A., Watts, H.D., Guo, J., Catchmark, J.M. and Kubicki, J.D. (2010) MP2, density functional theory, and molecular mechanical calculations of C-H⋯π and hydrogen bond interactions in a cellulose-binding Module-Cellulose Model System. Carbohydr. Res., 345, 1741-1751.
85. Sujatha, M.S., Sasidhar, Y.U. and Balaji, P.V. (2005) Insights into the role of the aromatic residue in galactose-binding sites: MP2/6- 311G++** study on galactose- and glucose-aromatic residue analogue complexes. Biochemistry, 44, 8554-8562.
86. Kozmon, S., Matuška, R., Spiwok, V. and Koča, J. (2011) Dispersion interactions of carbohydrates with condensate aromatic moieties: theoretical study on the CH-π interaction additive properties. Phys. Chem. Chem. Phys., 13, 14215-14222.
87. Lucas, R., Gomez-Pinto, I., Avino, A., Reina, J.J., Eritja, R., Gonzalez, C. and Morales, J.C. (2011) Highly polar carbohydrates stack onto DNA duplexes via CH/pi interactions. J. Am. Chem. Soc., 133, 1909-1916.
88. Maresca, M., Derghal, A., Carravagna, C., Dudin, S. and Fantini, J. (2008) Controlled aggregation of adenine by sugars: physicochemical studies, molecular modelling simulations of sugar-aromatic CH-pi stacking interactions, and biological significance. Phys. Chem. Chem. Phys., 10, 2792-2800.
89. Gómez-Pinto, I., Vengut-Climent, E., Lucas, R., Aviñó, A., Eritja, R., González, C. and Morales, J.C. (2013) Carbohydrate-DNA interactions at G-quadruplexes: folding and stability changes by attaching sugars at the 5′-End. Chem. Eur. J., 19, 1920-1927.
90. Lucas, R., Vengut-Climent, E., Gomez-Pinto, I., Avino, A., Eritja, R., Gonzalez, C. and Morales, J.C. (2012) Apolar carbohydrates as DNA capping agents. Chem. Commun., 48, 2991-2993.
91. Schrodinger, L. (2010) The PyMOL molecular graphics system, Version 1.3r1.
92. Macrae, C.F., Bruno, I.J., Chisholm, J.A., Edgington, P.R., McCabe, P., Pidcock, E., Rodriguez-Monge, L., Taylor, R., van de Streek, J. and Wood, P.A. (2008) Mercury CSD 2.0 - new features for the visualization and investigation of crystal structures. J. Appl. Crystallogr., 41, 466-470.
93. Edgcomb, S.P. and Murphy, K.P. (2002) Variability in the pKa of histidine side-chains correlates with burial within proteins. Proteins: Struct. Funct. Bioinform., 49, 1-6.
94. HyperChem(TM). Professional 7.5 ed. Hypercube, Inc., Gainesville, Florida.
95. Cerny, J. and Hobza, P. (2007) Non-covalent interactions in biomacromolecules. Phys. Chem. Chem. Phys., 9, 5291-5303.
96. Raju, R.K., Ramraj, A., Hillier, I.H., Vincent, M.A. and Burton, N.A. (2009) Carbohydrate-aromatic π interactions: a test of density functionals and the DFT-D method. Phys. Chem. Chem. Phys., 11, 3411-3416.
97. Hujo, W. and Grimme, S. (2012) Performance of non-local and atom-pairwise dispersion corrections to DFT for structural parameters of molecules with noncovalent interactions. J. Chem. Theory Comput., 9, 308-315.
98. Burns, L.A., Vazquez-Mayagoitia, A., Sumpter, B.G. and Sherrill, C.D. (2011) Density-functional approaches to noncovalent interactions: a comparison of dispersion corrections (DFT-D), exchange-hole dipole moment (XDM) theory, and specialized functionals. J. Chem. Phys, 134, 084107.
99. Halkier, A., Helgaker, T., Jorgensen, P., Klopper, W., Koch, H., Olsen, J. and Wilson, A.K. (1998) Basis-set convergence in correlated calculations on Ne, N-2, and H2O. Chem. Phys. Lett., 286, 243-252.
100. Halkier, A., Helgaker, T., Jorgensen, P., Klopper, W. and Olsen, J. (1999) Basis-set convergence of the energy in molecular hartree-fock calculations. Chem. Phys. Lett., 302, 437-446.
101. Jurecka, P., Sponer, J. and Hobza, P. (2004) Potential energy surface of the cytosine dimer: MP2 complete basis set limit interaction energies, CCSD(T) correction term, and comparison with the AMBER force field. J. Phys. Chem. B, 108, 5466-5471.
102. Sponer, J., Jurecka, P., Marchan, I., Luque, F.J., Orozco, M. and Hobza, P. (2006) Nature of base stacking: reference quantum-chemical stacking energies in ten unique B-DNA base-pair steps. Chem.-Eur. J., 12, 2854-2865.
103. Sponer, J., Riley, K.E. and Hobza, P. (2008) Nature and magnitude of aromatic stacking of nucleic acid bases. Phys. Chem. Chem. Phys., 10, 2595-2610.
104. Morgado, C.A., Jurecka, P., Svozil, D., Hobza, P. and Sponer, J. (2010) Reference MP2/CBS and CCSD(T) quantum-chemical calculations on stacked adenine dimers. Comparison with DFT-D, MP2.5, SCS(MI)-MP2, M06-2X, CBS(SCS-D) and force field descriptions. Phys. Chem. Chem. Phys., 12, 3522-3534.
105. Mládek, A., Banáš, P., Jurečka, P., Otyepka, M., Zgarbová, M. and Šponer, J. (2013) Energies and 2′-Hydroxyl group orientations of RNA backbone conformations. Benchmark CCSD(T)/CBS database, electronic analysis, and assessment of DFT methods and MD simulations. J. Chem. Theory Comput., 10, 463-480.
106. Mladek, A., Krepl, M., Svozil, D., Cech, P., Otyepka, M., Banas, P., Zgarbova, M., Jurecka, P. and Sponer, J. (2013) Benchmark quantum-chemical calculations on a complete set of rotameric families of the DNA sugar-phosphate backbone and their comparison with modern density functional theory. Phys. Chem. Chem. Phys., 15, 7295-7310.
107. Jurecka, P., Sponer, J., Cerny, J. and Hobza, P. (2006) Benchmark database of accurate (MP2 and CCSD(T) complete basis set limit) interaction energies of small model complexes, DNA base pairs, and amino acid pairs. Phys. Chem. Chem. Phys., 8, 1985-1993.
108. Riley, K.E., Platts, J.A., Řezáč, J., Hobza, P. and Hill, J.G. (2012) Assessment of the performance of MP2 and MP2 variants for the treatment of noncovalent interactions. J. Phys. Chem. A, 116, 4159-4169.
109. 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. (2009). Revision A.02 ed. Gaussian, Inc., Wallingford CT.
110. Shao, Y., Molnar, L.F., Jung, Y., Kussmann, J., Ochsenfeld, C., Brown, S.T., Gilbert, A.T.B., Slipchenko, L.V., Levchenko, S.V., O'Neill, D.P. et al. (2006) Advances in methods and algorithms in a modern quantum chemistry program package. Phys. Chem. Chem. Phys., 8, 3172-3191.
111. Singh, N.J., Min, S.K., Kim, D.Y. and Kim, K.S. (2009) Comprehensive energy analysis for various types of π-interaction. J. Chem. Theory Comput., 5, 515-529.
112. Rutledge, L.R. and Wetmore, S.D. (2011) Modeling the chemical step utilized by human alkyladenine DNA glycosylase: a concerted mechanism AIDS in selectively excising damaged purines. J. Am. Chem. Soc., 133, 16258-16269.
113. Kellie, J.L., Navarro-Whyte, L., Carvey, M.T. and Wetmore, S.D. (2012) Combined effects of π-π stacking and hydrogen bonding on the (N1) acidity of uracil and hydrolysis of 2'-deoxyuridine. J. Phys. Chem. B, 116, 2622-2632.
114. Przybylski, J.L. and Wetmore, S.D. (2011) A QM/QM investigation of the hUNG2 reaction surface: the untold tale of a catalytic residue. Biochemistry, 50, 4218-4227.
115. Calvaresi, M., Bottoni, A. and Garavelli, M. (2007) Computational clues for a new mechanism in the glycosylase activity of the human DNA repair protein hOGG1. A generalized paradigm for purine-repairing systems? J. Phys. Chem. B, 111, 6557-6570.
116. Bruner, S.D., Norman, D.P.G. and Verdine, G.L. (2000) Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature, 403, 859-866.
117. Goedecke, K., Pignot, M., Goody, R.S., Scheidig, A.J. and Weinhold, E. (2001) Structure of the N6-adenine DNA methyltransferase MTaqI in complex with DNA and a cofactor analog. Nat. Struct. Mol. Biol., 8, 121-125.
118. Wang, W., Wu, E.Y., Hellinga, H.W. and Beese, L.S. (2012) Structural factors that determine selectivity of a high fidelity DNA polymerase for deoxy-, dideoxy-, and ribonucleotides. J. Biol. Chem., 287, 28215-28226.
119. Brown, J.A. and Suo, Z. (2011) Unlocking the sugar "steric gate" of DNA polymerases. Biochemistry, 50, 1135-1142.
120. DeLucia, A.M., Grindley, N.D.F. and Joyce, C.M. (2003) An error-prone family Y DNA polymerase (DinB Homolog from sulfolobus solfataricus) uses a 'steric gate' residue for discrimination against ribonucleotides. Nucleic Acids Res., 31, 4129-4137.
121. Kirouac, K.N., Suo, Z. and Ling, H. (2011) Structural mechanism of ribonucleotide discrimination by a Y-family DNA polymerase. J. Mol. Biol., 407, 382-390.
122. Yang, G., Franklin, M., Li, J., Lin, T.C. and Konigsberg, W. (2002) A conserved Tyr residue is required for sugar selectivity in a Pol α DNA polymerase. Biochemistry, 41, 10256-10261.
123. Astatke, M., Ng, K., Grindley, N.D. and Joyce, C.M. (1998) A single side chain prevents escherichia coli DNA polymerase I (klenow fragment) from incorporating ribonucleotides. Proc. Natl. Acad. Sci. U.S.A., 95, 3402-3407.
124. Bonnin, A., Lázaro, J.M., Blanco, L. and Salas, M. (1999) A single tyrosine prevents insertion of ribonucleotides in the eukaryotic-type φ29 DNA polymerase. J. Mol. Biol., 290, 241-251.
125. Gao, G., Orlova, M., Georgiadis, M.M., Hendrickson, W.A. and Goff, S.P. (1997) Conferring RNA polymerase activity to a DNA polymerase: a single residue in reverse transcriptase controls substrate selection. Proc. Natl. Acad. Sci. U.S.A., 94, 407-411.
126. Lindahl, T. and Wood, R.D. (1999) Quality control by DNA repair. Science, 286, 1897-1905.
127. Sale, J.E., Lehmann, A.R. and Woodgate, R. (2012) Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat. Rev. Mol. Cell. Biol., 13, 141-152.
128. Loregian, A., Marsden, H.S. and Palù, G. (2002) Protein-protein interactions as targets for antiviral chemotherapy. Rev. Med. Virol., 12, 239-262.
129. Park, S.-H. and Raines, R.T. (2000) Genetic selection for dissociative inhibitors of designated protein-protein interactions. Nat. Biotech., 18, 847-851.
130. De Clercq, E. (2002) Strategies in the design of antiviral drugs. Nat. Rev. Drug Discov., 1, 13-25. Canada