Tautomerism in nucleic acid bases and base pairs: A brief overview

Wiley Interdisciplinary Reviews: Computational Molecular Science

Volumn 3, Issue 6, 2013, Pages 637-649

  Shukla, Manoj K ^a,b   Leszczynski, Jerzy ^a  

^a JACKSON STATE UNIVERSITY   (United States)

^b US ARMY ENGINEER RESEARCH AND DEVELOPMENT CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTATIONAL ALGORITHM; CURRENT STATUS; NUCLEIC ACID BASIS; QUANTUM CHEMISTRY CALCULATIONS; RIGOROUS ANALYSIS; TAUTOMERIC FORMS; THEORETICAL CALCULATIONS; THEORETICAL METHODS;

EXPERIMENTS; ISOMERS; NUCLEIC ACIDS; POSITIVE IONS; QUANTUM CHEMISTRY;

BIOMOLECULES;

EID: 84886257685     PISSN: 17590876     EISSN: 17590884     Source Type: Journal    
DOI: 10.1002/wcms.1145     Document Type: Review

References (116)

1. Saenger W. Principles of Nucleic Acid Structures. New York: Springer-Verlag 1984.
2. Shukla MK, Leszczynski J., eds. Radiation induced Molecular Phenomena In nucleic Acid: A Comprehensive Theoretical and Experimental Analysis. Challenges and Advances in Computational Chemistry and Physics, Vol. 5. Dordrecht, the Netherlands: Springer+Business Media B.V.; 2008.
3. Crespo-Hernandez CE, Cohen B, Hare PM, Kohler B. Ultrafast excited-state dynamics in nucleic acids. Chem Rev 2004, 104:1977-2020.
4. Shukla MK, Leszczynski J. Electronic spectra, excited state structures and interactions of nucleic acid bases and base assemblies: a review. J Biomol Struct Dynam 2007, 25:93-118.
5. Serrano-Andres L, Merchan M, Borin AC. Adenine and 2-aminopurine: paradigms of modern theoretical photochemistry. Proc Natl Acad Sci USA 2006, 103: 8691-8696.
6. Cleaves HJ, Scott AM, Hill FC, Leszczynski J, Sahai N, Hazen R. Mineral-organic interfacial processes: potential roles in the origins of life. Chem Soc Rev 2012, 41: 5502-5525.
7. Schreier WJ, Schrader TE, Koller FO, Gilch P, Crespo-Hernandez CE, Swaminathan VN, Carell T, Zinth W, Kohler B. Thymine dimerization in DNA is an ultrafast photoreaction. Science 2007, 315:625-629.
8. Hiyama A, Nohara C, Kinjo S, Taira W, Gima S, Tanahara A, Otaki JM. The biological impacts of the Fukushima nuclear accident on the pale grass blue butterfly. Sci Rep 2012, 2:570.
9. Mons M, Piuzzi F, Dimicoli I, Gorb L, Leszczynki J. Near-UV resonant two-photon ionization spectroscopy of gas phase guanine-evidence for the observation of three rare tautomers. J Phys Chem A 2006, 110:10921-10924.
10. * studies. Int J Quantum Chem: Quant Biol Symp 1992, 19:43-55.
11. McMullan RK, Benci P, Craven BM. The neutron crystal structure of 9-methyladenine at 126 K. Acta Crystallogr B 1980, 36:1424-1430.
12. Dong F, Miller RE. Vibrational transition moment angles in isolated biomolecules: a structural tool. Science 2002, 298:1227-1230.
13. Leszczynski J. Isolated, solvated and complexed nucleic acid bases: structures and properties. In: Hargittai M, Hargittai I, eds. Advances in Molecular Structure and Research, Vol. 6. Stamford, CT: JAI Press; 2000, 209-265.
14. Burda JV, Sponer J., Leszczynski J. Metal interactions with nucleobases, base pairs, and oligomer sequences; computational approach. In: Leszczynski J., ed.; Kaczmarek-Kedziera A, Papadopoulos MG, Reis H, Sadlej AJ, Shukla MK. coeds. Handbook of Computational Chemistry. Dordrecht, the Netherlands: Springer+Business Media B.V.; 2012, 1277-1308.
15. Shukla MK, Leszczynski J. Excited states of nucleic acid bases. In: Leszczynski J, ed. Computational Chemistry: Reviews of Current Trends, Vol. 8. Singapore: World Scientific; 2003, 249-344.
16. Watson JD, Crick FHC. Genetical implications of the structure of deoxyribonucleic acid. Nature 1953, 171:964-967.
17. Sheina GG, Stepanian SG, Radchenko ED, Blagoi YuP. IR spectra of guanine and hypoxanthine isolated molecules. J Mol Struct 1987, 158:275-292.
18. Szczepaniak K, Szczesniak M, Person WB. Infrared studies and the effect of ultraviolet irradiation on the tautomers of 9-methylguanine isolated in an argon matrix. Chem Phys Lett 1988, 153:39-44.
19. Szczepaniak K, Szczesniak M, Szajda W, Person WB, Leszczynski J. Infrared spectra of tautomers and rotamers of 9-methylguanine. An experimental and theoretical study. Can J Chem 1991, 69:1705-1720.
20. Leszczynski J. The potential energy surface of guanine is not flat: an ab initio study with large basis sets and higher order electron correlation contributions. J Phys Chem A 1998, 102: 2357-2362.
21. Gorb L, Leszczynski J. Intramolecular proton transfer in mono- and dihydrated tautomers of guanine: an ab initio post Hartree-Fock study. J Am Chem Soc 1998, 120:5024-5032.
22. Gorb L, Kaczmarek A, Gorb A, Sadlej AJ, Leszczynski J. Thermodynamics and kinetics of intramolecular proton transfer in guanine. Post Hartree-Fock study. J Phys Chem B 2005, 109:13770-13776.
23. Colominas C, Luque FJ, Orozco M. Tautomerism and protonation of guanine and cytosine. Implications in the formation of hydrogen-bonded complexes. J Am Chem Soc 1996, 118:6811-6821.
24. Shukla MK, Leszczynski J. Excited state proton transfer in guanine in the gas phase and in water solution: a theoretical study. J Phys Chem A 2005, 109:7775-7780.
25. Nir E, Janzen Ch, Imhof P, Kleinermanns K, de Vries MS. Guanine tautomerism revealed by UV-UV and IR-UV hole burning spectroscopy. J Chem Phys 2001, 115:4604-4611.
26. Piuzzi F, Mons M, Dimicoli I, Tardivel B, Zhao Q. Ultraviolet spectroscopy and tautomerism of the DNA base guanine and its hydrate formed in a supersonic jet. Chem Phys 2001, 270:205-214.
27. Mons M, Dimicoli I, Piuzzi F, Tardivel B, Elhanine M. Tautomerism of the DNA base guanine and its methylated derivatives as studied by gas-phase infrared and ultraviolet spectroscopy. J Phys Chem A 2002, 106:5088-5094.
28. Choi MY, Miller RE. Four tautomers of isolated guanine from infrared laser spectroscopy in helium nanodroplets. J Am Chem Soc 2006, 128:7320-7328.
29. Shukla MK, Leszczynski J. Spectral origins and ionization potentials of guanine tautomers: theoretical elucidation of experimental findings. Chem Phys Lett 2006, 429:261-265.
30. Chenon MT, Pugmire RJ, Grant DM, Panzica RP, Townsend LB. Carbon-13 magnetic resonance. XXVI. Quantitative determination of the tautomeric populations of certain purines. J Am Chem Soc 1975, 97: 4636-4642.
31. Lin J, Yu C, Peng S, Akiyama I, Li K, Lee LK, LeBreton PR. Ultraviolet photoelectron studies of the ground-state electronic structure and gas-phase tautomerism of purine and adenine. J Am Chem Soc 1980, 102: 4627-4631.
32. Nowak MJ, Rostkowska H, Lapinski L, Kwiatkowski JS, Leszczynski J. Tautomerism N(9)H ⇌ N(7)H of purine, adenine, and 2-chloroadenine: combined experimental IR matrix isolation and ab initio quantum mechanical studies. J Phys Chem 1994, 98: 2813-2816.
33. 5)-Labeled adenine derivatives: synthesis and studies of tautomerism by 15N NMR spectroscopy and theoretical calculations. J Org Chem 2001, 66:5463-5481.
34. Hanus M, Kabelac M, Rejnek J, Ryjacek F, 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. Part 3. Adenine. J Phys Chem B 2004, 108: 2087-2097.
35. Guerra CF, Bickelhaupt FM, Saha S, Wang F. Adenine tautomers: relative stabilities, ionization energies, and mismatch with cytosine. J Phys Chem A 2006, 110: 4012-4020.
36. Gu J, Leszczynski J. A DFT study of the water-assisted intramolecular proton transfer in the tautomers of adenine. J Phys Chem A 1999, 103:2744-2750.
37. Holley RW, Apgar J, Everett GA, Madison JT, Marquisee M, Merrill SH, Penswick JR, Zamir A. Structure of a ribonucleic acid. Science 1965, 147: 1462-1465.
38. Grunberger D, Holy A, Sorm F. The coding properties of some triribonucleoside diphosphates containing inosine. Biochim Biophys Acta 1967, 134: 484-486.
39. Friedberg EC, Walker GC, Siede W. DNA Repair and Mutagenesis. Washington, DC: ASM Press; 1995.
40. Ramaekers R, Maes G, Adamowicz L, Dkhissi A. Matrix-isolation FT-IR study and theoretical calculations of the vibrational, tautomeric and H-bonding properties of hypoxanthine. J Mol Struct 2001, 560:205-221.
41. Lin J, Yu C, Peng S, Akiyama I, Li K, Lee LK, LeBreton PR. Ultraviolet photoelectron studies of the ground-state electronic structure and gas-phase tautomerism of hypoxanthine and guanine. J Phys Chem 1980, 84:1006-1012.
42. Chenon MT, Pugmire RJ, Grant DM, Panzica RP, Townsend LB. Carbon-13 magnetic resonance. XXV. Basic set of parameters for the investigation of tautomerism in purines established from carbon-13 magnetic resonance studies using certain purines and pyrrolo[2, 3-d]pyrimidines. J Am Chem Soc 1975, 97:4627-4636.
43. Munns ARI, Tollin P. The crystal and molecular structure of inosine. Acta Crystallogr B 1970, 26:1101-1113.
44. Shukla MK, Leszczynski J. Theoretical study of proton transfer in hypoxanthine tautomers: effects of hydration. J Phys Chem A 2000, 104:3021-3027.
45. Shukla MK, Leszczynski J. A DFT investigation on effects of hydration on the tautomeric equilibria of hypoxanthine. J Mol Struct (Theochem) 2000, 529:99-112.
46. Hernandez B, Luque FT, Orozco M. Tautomerism of xanthine oxidase substrates hypoxanthine and allopurinol. J Org Chem 1996, 61:5964-5971.
47. Costas ME, Acevedo-Chavez R. Density functional study of the neutral hypoxanthine tautomeric forms. J Phys Chem A 1997, 101:8309-8318.
48. Shukla MK, Leszczynski J. Time-dependent density functional theory (TD-DFT) study of the excited state proton transfer in hypoxanthine. Int J Quantum Chem 2005, 105:387-395.
49. Sadeghi RR, Cheng H-P. The dynamics of proton transfer in a water chain. J Chem Phys 1999, 111:2086.
50. Leszczynski J. Ab initio study on tautomeric properties of nucleic acid bases. In: The Encyclopedia of Computational Chemistry, Vol. V. Hoboken, NJ: John Wiley & Sons; 1998, 2951-2960.
51. Szczesniak M, Szczepaniak K, Kwiatowski JS, KuBulat K, Person WB. Matrix isolation infrared studies of nucleic acid constituents. 5. Experimental matrix-isolation and theoretical ab initio SCF molecular orbital studies of the infrared spectra of cytosine monomers. J Am Chem Soc 1988, 110:8319-8330.
52. Kwiatkowski JS, Leszczynski J. Molecular structure and vibrational IR spectra of cytosine and its Thio and Seleno analogues by density functional theory and conventional ab initio calculations. J Phys Chem 1996, 100:941-953.
53. 2O in Ar Matrices. J Phys Chem 1996, 100:6434-6444.
54. Lapinski L, Nowak MJ, Fulara J, Les A, Adamowicz L. Matrix isolation and ab initio theoretical studies of the IR spectrum of 5-methylcytosine. J Phys Chem 1990, 94:6555-6564.
55. Brown RD, Godfrey PD, McNaughton D, Pierlot AP. Tautomers of cytosine by microwave spectroscopy. J Am Chem Soc 1989, 111:2308-2310.
56. Drefus M, Bensaude O, Dodin G, Dubois JE. Tautomerism in cytosine and 3-methylcytosine. A thermodynamic and kinetic study. J Am Chem Soc 1976, 98:6338-6349.
57. McClure RJ, Craven BM. New investigations of cytosine and its monohydrate. Acta Crystallogr B 1973, 29:1234-1238.
58. Choi MY, Dong F, Miller RE. Multiple tautomers of cytosine identified and characterized by infrared laser spectroscopy in helium nanodroplets: probing structure using vibrational transition moment angles. Phil Trans R Soc A 2005, 363:393-413.
59. Fogarasi G. Relative stabilities of three low-energy tautomers of cytosine: a coupled cluster electron correlation study. J Phys Chem A 2002, 106:1381-1390.
60. Kobayashi R. A CCSD(T) study of the relative stabilities of cytosine tautomers. J Phys Chem A 1998, 102: 10813-10817.
61. Fogarasi G, Szalay PG. The interaction between cytosine tautomers and water: an MP2 and coupled cluster electron correlation study. Chem Phys Lett 2002, 356:383-390.
62. Trygubenko SA, Bogdan TV, Rueda M, Orozco M, Luque JF, Sponer J, Slavicek P, 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 Part 1. Cytosine. Phys Chem Chem Phys 2002, 4:4192-4203.
63. 14N NMR shielding of cytosine tautomers: continuous set of gauge transformation calculation using polarizable continuum model. J Mol Struct (Theochem) 2002, 581:51-58.
64. Estrin DA, Paglieri L, Corongiu G. A density functional study of tautomerism of uracil and cytosine. J Phys Chem 1994, 98:5653-5660.
65. Chandra AK, Nguyen MT, Zeegers-Huyskens Th. Theoretical study of the protonation and deprotonation of cytosine. Implications for the interaction of cytosine with water. J Mol Struct 2000, 519:1-11.
66. Gorb L, Podolyan Y, Leszczynski J. A theoretical investigation of tautomeric equilibria and proton transfer in isolated and monohydrated cytosine and isocytosine molecules. J Mol Struct (Theochem) 1999, 487:47-55.
67. Morsy MA, Al-Somali AM, Suwaiyan A. Fluorescence of thymine tautomers at room temperature in aqueous solutions. J Phys Chem B 1999, 103:11205-11210.
68. Shukla MK, Leszczynski J. Interaction of water molecules with cytosine tautomers: an excited-state quantum chemical investigation. J Phys Chem A 2002, 106:11338-11346.
69. Tsuchiya Y, Tamura T, Fujii M, Ito M. Keto-enol tautomer of uracil and thymine. J Phys Chem 1988, 92:1760-1765.
70. Fujii M, Tamura T, Mikami N, Ito M. Electronic spectra of uracil in a supersonic jet. Chem Phys Lett 1986, 126:583-587.
71. Brady BB, Peteanu LA, Levy DH. The electronic spectra of the pyrimidine bases uracil and thymine in a supersonic molecular beam. Chem Phys Lett 1988, 147:538-543.
72. Suwaiyan A, Morsy MA, Odah KA. Room temperature fluorescence of 5-chlorouracil tautomers. Chem Phys Lett 1995, 237:349-355.
73. Ferenczy G, Harsanyi L, Rozsondai B, Hargittai I. The molecular structure of uracil: an electron diffraction study. J Mol Struct 1986, 140:71-77.
74. Voet D, Rich A. The crystal structures of purines, pyrimidines and their intermolecular complexes. Prog Nucl Acid Res Mol Biol 1970, 10:183-265.
75. 15N labeled tRNA. Nucleic Acids Res 1982, 10:7027-7039.
76. Nowak MJ, Szczepaniak K, Barski A, Shugar D. Spectroscopic studies on vapor phase tautomerism of natural bases found in nucleic acids. Z Naturforsch C 1978, 33:876-883.
77. Shugar D, Szczepaniak K. Tautomerism of pyrimidines and purines in the gas phase and in low-temperature matrices, and some biological implications. Int J Quantum Chem 1981, 20:573-585.
78. Szczesniak M, Nowak MJ, Rostkowska H, Szczepaniak K, Person WB, Shugar D. Matrix isolation studies of nucleic acid constituents. 1. Infrared spectra of uracil monomers. J Am Chem Soc 1983, 105:5969-5976.
79. Chin S, Scott I, Szczepaniak K, Person WB. Matrix isolation studies of nucleic acid constituents. 2. Quantitative ab initio prediction of the infrared spectrum of in-plane modes of uracil. J Am Chem Soc 1984, 106:3415-3422.
80. Radchenko YD, Scheina GG, Smorygo NA, Blagoi YP. Experimental and theoretical studies of molecular structure features of cytosine. J Mol Struct 1984, 116:387-396.
81. Leszczynski J. Tautomerism of uracil: the final chapter? Fourth-order electron correlation contributions to the relative energies of tautomers. J Phys Chem 1992, 96:1649-1653.
82. Rejnek J, Hanus M, Kabelac M, Ryjacek F, 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. Part 4. Uracil and thymine. Phys Chem Chem Phys 2005, 7:2006-2017.
83. Lapinski L, Nowak MJ, Kwiatkowski JS, Leszczynski J. Phototautomeric reaction, tautomerism, and infrared spectra of 6-thiopurine. Experimental matrix isolation and quantum-mechanical (conventional ab initio and density-functional theory) studies. J Phys Chem A 1999, 103:280-288.
84. Stewart MJ, Leszczynski J, Rubin YV, Blagoi YP. Tautomerism of thioguanine: from gas phase to DNA. J Phys Chem A 1997, 101:4753-4760.
85. Venkateswarlu D, Leszczynski J. Tautomerism and proton transfer in 6-selenoguanine: a post Hartree-Fock level ab initio SCF-MO investigation. J Phys Chem A 1998, 102:6161-6166.
86. Kwiatkowski JS, and Leszczynski J. Molecular structure and vibrational IR spectra of cytosine and its Thio and Seleno analogues by density functional theory and conventional ab initio calculations. J Phys Chem 1996, 100:941-953.
87. Shukla MK, Leszczynski J. Electronic transitions of thiouracils in the gas phase and in solutions: time-dependent density functional theory (TD-DFT) study. J Phys Chem A 2004, 108:10367-10375.
88. Blas JR, Luque FJ, Orozco M. Unique tautomeric properties of isoguanine. J Am Chem Soc 2004, 126:154-164.
89. Robinson H, Gao Y-G, Bauer C, Roberts C, Switzer C, Wang AH-J. 2′-Deoxyisoguanosine adopts more than one tautomer to form base pairs with thymidine observed by high-resolution crystal structure analysis. Biochemistry 1998, 37:10897-10905.
90. Hobza P, Sponer J. Structure, energetics, and dynamics of the nucleic acid base pairs: nonempirical ab initio calculations. Chem Rev 1999, 99:3247-3276.
91. Shukla MK, Leszczynski J. A theoretical investigation of excited-state properties of the adenine-uracil base pair. J Phys Chem A 2002, 106:1011-1018.
92. Shukla MK, Leszczynski J. A theoretical study of excited state properties of adenine - thymine and guanine - cytosine base pairs. J Phys Chem A 2002, 106:4709-4717.
93. Gorb L, Podolyan Y, Dziekonski P, Sokalski WA, Leszczynski J. Double-proton transfer in adenine-thymine and guanine-cytosine base pairs. A post-Hartree-Fock ab initio study. J Am Chem Soc 2004, 126:10119-10129.
94. Podolyan Y, Nowak MJ, Lapinski L, Leszczynski J. Probing ab initio MP2 approach towards the prediction of vibrational infrared spectra of DNA base pairs. J Mol Struct 2005, 744:19-34.
95. Kurita N, Danilov VI, Anisimov VM. The structure of Watson-Crick DNA base pairs obtained by MP2 optimization. Chem Phys Lett 2005, 404:164-170.
96. Sponer J, Florian J, Hobza P, Leszczynski J. Nonplanar DNA base pairs. J Biomol Struct Dyn 1996, 13:827-833.
97. Nir E, Janzen Ch, Imhof P, Kleinermanns K, de Vries MS. Pairing of the nucleobases guanine and cytosine in the gas phase studied by IR-UV double-resonance spectroscopy and ab initio calculations. Phys Chem Chem Phys 2002, 4:732-739.
98. Leonard GA, McAuley-Hecht K, Brown T, Hunter WN. Do C-H.O hydrogen bonds contribute to the stability of nucleic acid base pairs? Acta Crystallogr D 1995, 51:136-139.
99. Starikov EB, Steiner T. Computational support for the suggested contribution of C-H···O=C interactions to the stability of nucleic acid base pairs. Acta Crystallogr D 1997, 53:345-347.
100. Hobza P, Sponer J, Cubero E, Orozco M, Luque FJ. C-H···O contacts in the adenine···uracil Watson-Crick and uracil···uracil nucleic acid base pairs: nonempirical ab initio study with inclusion of electron correlation effects. J Phys Chem B 2000, 104:6286-6292.
101. Dabkowska I, Jurecka P, Hobza P. On geometries of stacked and H-bonded nucleic acid base pairs determined at various DFT, MP2, and CCSD(T) levels up to the CCSD(T)/complete basis set limit level. J Chem Phys 2005, 122:204322.
102. Sponer J, Jurecka P, Hobza P. Accurate interaction energies of hydrogen-bonded nucleic acid base pairs. J Am Chem Soc 2004, 126:10142-10151.
103. Jurecka P, Sponer J, Cerny J, Hobza P. 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 2006, 8:1985-1993.
104. Sponer J, Jurecka P, Marchan I, Luque FJ, Orozco M, Hobza P. Nature of base stacking: reference quantum-chemical stacking energies in ten unique B-DNA base-pair steps. Chem Eur J 2006, 12:2854-2865.
105. Zendlova L, Hobza P, Kabelac M. Potential energy surfaces of the microhydrated guanine-cytosine base pair and its methylated analogue. ChemPhysChem 2006, 7:439-447.
106. Rejnek J, Hobza P. Hydrogen-bonded nucleic acid base pairs containing unusual base tautomers: complete basis set calculations at the MP2 and CCSD(T) levels. J Phys Chem B 2007, 111:641-645.
107. Szyperska A, Rak J, Leszczynski J, Li X, Ko YJ, Wang H, Bowen KH. Low-energy-barrier proton transfer induced by electron attachment to the guanine-cytosine base pair. ChemPhysChem 2010, 11:880-888.
108. Kosenkov D, Kholod Y, Gorb L, Shishkin O, Hovorun DM, Mons M, Leszczynski J. Ab initio kinetic simulation of gas-phase experiments: tautomerization of cytosine and guanine. J Phys Chem B 2009, 113:6140-6150.
109. Eichhorn GL. The effect of metal ions on the structure and function of nucleic acids. Adv Inorg Biochem 1981, 3:1-46.
110. Eichhorn GL. Complexes of polynucleotides and nucleic acids. In: Eichhorn GL, ed. Inorganic Biochemistry. Amsterdam: Elsevier; 1973, 2:1210-1243.
111. Blagoi YP, Sorokin VA, Valeyev VA, Khomenko SA, Gladchenko GO. Magnesium ion effect on the helix-coil transition of DNA. Biopolymers 1978, 17:1103-1118.
112. Sigel H. Acid-base properties of purine residues and the effect of metal ions: quantification of rare nucleobase tautomers. Pure Appl Chem 2004, 76:1869-1886.
113. Martin RB. Dichotomy of metal ion binding to N1 and N7 of purines. Metal Ions Biol Sys 1996, 32:61-89.
114. Burda JV, Sponer J, Hobza P. Ab Initio Study of the Interaction of Guanine and Adenine with Various Mono- and Bivalent Metal Cations (Li+, Na+, K+, Rb+, Cs+; Cu+, Ag+, Au+; Mg2+, Ca2+, Sr2+, Ba2+; Zn2+, Cd2+, and Hg2+) J Phys Chem 1996, 100:7250-7255.
115. Rodgers MT, Armentrout PB. Noncovalent interactions of nucleic acid bases (uracil, thymine, and adenine) with alkali metal ions. Threshold collision-induced dissociation and theoretical studies. J Am Chem Soc 2000, 122:8548-8558.
116. Knobloch B, Sigel H. A quantitative appraisal of the ambivalent metal ion binding properties of cytidine in aqueous solution and an estimation of the anti.syn energy barrier of cytidine derivatives. J Biol Inorg Chem 2004, 9:365-373.