Energetic signatures of single base bulges: Thermodynamic consequences and biological implications

Nucleic Acids Research

Volumn 38, Issue 1, 2009, Pages 97-116

  Minetti, Conceiç̃o A S A ^a   Remeta, David P ^a   Dickstein, Rian ^a   Breslauer, Kenneth J ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; CYTIDINE; DNA BASE; DOUBLE STRANDED DNA; GUANOSINE; PRIMER DNA; SINGLE STRANDED DNA; THYMIDINE;

ARTICLE; BASE PAIRING; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; DISSOCIATION; DNA CONFORMATION; DNA DAMAGE; DNA DENATURATION; DNA REPAIR; DNA REPLICATION; DNA TEMPLATE; ENTHALPY; ENTROPY; EXPERIMENTAL MODEL; MOLECULAR STABILITY; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; RADIATION ABSORPTION; TEMPERATURE DEPENDENCE; THERMOSTABILITY; ULTRAVIOLET RADIATION;

CALORIMETRY, DIFFERENTIAL SCANNING; DNA; DNA REPAIR; DNA REPLICATION; MODELS, GENETIC; NUCLEIC ACID CONFORMATION; PURINES; PYRIMIDINES; THERMODYNAMICS;

EID: 75649100485     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1036     Document Type: Article

References (83)

1. Watson, J.D. and Crick, F.H. (1953) Molecular structure of nucleic acids: A structure for deoxyribose nucleic acid. Nature, 171, 737-738.
2. Fresco, J.R. and Alberts, B.M. (1960) The accommodation of noncomplementary bases in helical polyribonucleotides and deoxyribonucleic acids. Proc. Natl Acad. Sci. USA, 46, 311-321.
3. Garcia-Diaz, M. and Kunkel, T.A. (2006) Mechanism of a genetic glissando: structural biology of indel mutations. Trends Biochem. Sci., 31, 206-214.
4. Fink, T.R. and Crothers, D.M. (1972) Free energy of imperfect nucleic acid helices. I. The bulge defect. J. Mol. Biol., 66, 1-12.
5. Kunkel, T.A. (1990) Misalignment-mediated DNA synthesis errors. Biochemistry, 29, 8003-8011.
6. Streisinger, G. and Owen, J. (1985) Mechanisms of spontaneous and induced frameshift mutation in bacteriophage T4. Genetics, 109, 633-659.
7. Fucharoen, S., Kobayashi, Y., Fucharoen, G., Ohba, Y., Miyazono, K., Fukumaki, Y. and Takaku, F. (1990) A single nucleotide deletion in codon 123 of the beta-globin gene causes an inclusion body beta-thalassaemia trait: a novel elongated globin chain beta Makabe. Br. J. Haematol., 75, 393-399.
8. Linton, M.F., Pierotti, V. and Young, S.G. (1992) Reading-frame restoration with an apolipoprotein B gene frameshift mutation. Proc. Natl Acad. Sci. USA, 89, 11431-11435.
9. Kunkel, T.A. and Erie, D.A. (2005) DNA mismatch repair. Ann. Rev. Biochem., 74, 681-710.
10. Joshua-Tor, L., Frolow, F., Appella, E., Hope, H., Rabinovich, D. and Sussman, J.L. (1992) Three-dimensional structures of bulge-containing DNA fragments. J. Mol. Biol., 225, 397-431.
11. Portmann, S., Grimm, S., Workman, C., Usman, N. and Egli, M. (1996) Crystal structures of an A-form duplex with single-adenosine bulges and a conformational basis for site-specific RNA self-cleavage. Chem. Biol., 3, 173-184.
12. Patel, D.J., Kozlowski, S.A., Marky, L.A., Rice, J.A., Broka, C., Itakura, K. and Breslauer, K.J. (1982) Extra adenosine stacks into the self-complementary d(CGCAGAATTCGCG) duplex in solution. Biochemistry, 21, 445-451.
13. Pardi, A., Morden, K., Patel, D. and Tinoco, I. Jr (1982) Kinetics for exchange of imino protons in the d (CGCGAATTCGCG) double helix and in two similar helices that contain a G.cntdot.T base pair, d(CGTGAATTCGCG), and an extra adenine, d(CGCAGAATTCGCG). Biochemistry, 21, 6567-6574.
14. Morden, K.M., Chu, Y.G., Martin, F.H. and Tinoco, I. Jr (1983) Unpaired cytosine in the deoxyoligonucleotide duplex dCA3CA3G*dCT6G is outside of the helix. Biochemistry, 22, 5557-5563.
15. Woodson, S.A. and Crothers, D.M. (1989) Conformation of a bulge-containing oligomer from a hot-spot sequence by NMR and energy minimization. Biopolymers, 28, 1149-1177.
16. Woodson, S.A. and Crothers, D.M. (1988) Structural model for an oligonucleotide containing a bulged guanosine by NMR and energy minimization. Biochemistry, 27, 3130-3141.
17. Morden, K.M., Gunn, B.M. and Maskos, K. (1990) NMR studies of a deoxyribodecanucleotide containing an extrahelical thymidine surrounded by an oligo(dA).oligo(dT) tract. Biochemistry, 29, 8835-8845.
18. Kalnik, M.W., Norman, D.G., Zagorski, M.G., Swann, P.F. and Patel, D.J. (1989) Conformational transitions in cytidine bulge-containing deoxytridecanucleotide duplexes: extra cytidine equilibrates between looped out (low temperature) and stacked (elevated temperature) conformations in solution. Biochemistry, 28, 294-303.
19. Kalnik, M.W., Norman, D.G., Swann, P.F. and Patel, D.J. (1989) Conformation of adenosine bulge-containing deoxytridecanucleotide duplexes in solution. Extra adenosine stacks into duplex independent of flanking sequence and temperature. J. Biol. Chem., 264, 3702-3712.
20. Popenda, L., Adamiak, R.W. and Gdaniec, Z. (2008) Bulged adenosine influence on the RNA duplex conformation in solution. Biochemistry, 47, 5059-5067.
21. Zacharias, M. and Sklenar, H. (1997) Analysis of the stability of looped-out and stacked-in conformations of an adenine bulge in DNA using a continuum model for solvent and ions. Biophys. J., 73, 2990-3003.
22. Feig, M., Zacharias, R. and Pettitt, B.M. (2001) Conformations of an adenine bulge in a DNA octamer and its influence on DNA structure from molecular dynamics simulations. Biophys. J., 81, 352-370.
23. Groebe, D.R. and Uhlenbeck, O.C. (1989) Thermal stability of RNA hairpins containing a four-membered loop and a bulge nucleotide. Biochemistry, 28, 742-747.
24. Longfellow, C.E., Kierzek, R. and Turner, D.H. (1990) Thermodynamic and spectroscopic study of bulge loops in oligoribonucleotides. Biochemistry, 29, 278-285.
25. LeBlanc, D.A. and Morden, K.M. (1991) Thermodynamic characterization of deoxyribooligonucleotide duplexes containing bulges. Biochemistry, 30, 4042-4047.
26. Woodson, S.A. and Crothers, D.M. (1987) Proton nuclear magnetic resonance studies on bulge-containing DNA oligonucleotides from a mutational hot-spot sequence. Biochemistry, 26, 904-912.
27. Garcia, A., Lambert, I.B. and Fuchs, R.P. (1993) DNA adduct-induced stabilization of slipped frameshift intermediates within repetitive sequences: implications for mutagenesis. Proc. Natl Acad. Sci. USA, 90, 5989-5993.
28. Milhe, C., Dhalluin, C., Fuchs, R.P. and Lefevre, J.F. (1994) NMR evidence of the stabilisation by the carcinogen N-2-acetylaminofluorene of a frameshift mutagenesis intermediate. Nucleic Acids Res., 22, 4646-4652.
29. Ke, S.H. and Wartell, R.M. (1995) Influence of neighboring base pairs on the stability of single base bulges and base pairs in a DNA fragment. Biochemistry, 34, 4593-4600.
30. Zhu, J. and Wartell, R.M. (1999) The effect of base sequence on the stability of RNA and DNA single base bulges. Biochemistry, 38, 15986-15993.
31. Tanaka, F., Kameda, A., Yamamoto, M. and Ohuchi, A. (2004) Thermodynamic parameters based on a nearest-neighbor model for DNA sequences with a single-bulge loop. Biochemistry, 43, 7143-7150.
32. Gelfand, C.A., Plum, G.E., Grollman, A.P., Johnson, F. and Breslauer, K.J. (1998) Thermodynamic consequences of an abasic lesion in duplex DNA are strongly dependent on base sequence. Biochemistry, 37, 7321-7327.
33. Plum, G.E., Gelfand, C.A. and Breslauer, K.J. (1999) Effects of 3, N4-ethenodeoxycytidine on duplex stability and energetics. In Singer, B. and Bartsch, H. (eds), Exocyclic DNA Adducts in Mutagenesis and Carcinogenesis. International Agency for Research on Cancer, Lyon, pp. 169-177.
34. Tikhomirova, A., Beletskaya, V. and Chalikian, T.V. (2006) Stability of duplexes containing GG,CC,AA, ant TT mismatches. Biochemistry, 45, 10563-10571.
35. Zieba, K., Chu, T.M., Kupke, D.W. and Marky, L.A. (1991) Differential hydration of dA.dT base pairing and dA and dT bulges in deoxyoligonucleotides. Biochemistry, 30, 8018-8026.
36. Plum, G.E., Grollman, A.P., Johnson, F. and Breslauer, K.J. (1995) Influence of the oxidatively damaged adduct 8-oxodeoxyguanosine on the conformation, energetics, and thermodynamic stability of a DNA duplex. Biochemistry, 34, 16148-16160.
37. Hang, B., Sagi, J. and Singer, B. (1998) Correlation between sequence-dependent glycosylase repair and the thermal stability of oligonucleotide duplexes containing 1, N6-ethenoadenine. J. Biol. Chem., 273, 33406-33413.
38. Sagi, J., Hang, B. and Singer, B. (1999) Sequence-dependent repair of synthetic AP sites in 15-mer and 35-mer oligonucleotides: role of thermodynamic stability imposed by neighbor bases. Chem. Res. Toxicol., 12, 917-923.
39. Ruan, Q., Liu, T., Kolbanovskiy, A., Liu, Y., Ren, J., Skorvaga, M., Zou, Y., Lader, J., Malkani, B., Amin, S. et al. (2007) Sequence context-and temperature-dependent nucleotide excision repair of a benzo a pyrene diol epoxide-guanine DNA adduct catalyzed by thermophilic UvrABC proteins. Biochemistry, 46, 7006-7015.
40. Wang, Y.H. and Griffith, J. (1991) Effects of bulge composition and flanking sequence on the kinking of DNA by bulged bases. Biochemistry, 30, 1358-1363.
41. Plum, G.E., Grollman, A.P., Johnson, F. and Breslauer, K.J. (1992) Influence of an exocyclic guanine adduct on the thermal stability, conformation, and melting thermodynamics of a DNA duplex. Biochemistry, 31, 12096-12102.
42. Vesnaver, G., Chang, C.N., Eisenberg, M., Grollman, A.P. and Breslauer, K.J. (1989) Influence of abasic and anucleosidic sites on the stability, conformation, and melting behavior of a DNA duplex: correlations of thermodynamic and structural data. Proc. Natl Acad. Sci. USA, 86, 3614-3618.
43. Plum, G.E. and Breslauer, K.J. (1994) DNA lesions. A thermodynamic perspective. Ann. NY Acad. Sci., 726, 45-55, discussion 55-46.
44. Gelfand, C.A., Plum, G.E., Grollman, A.P., Johnson, F. and Breslauer, K.J. (1996) The impact of a bistrand abasic lesion on DNA duplex properties. Biopolymers, 38, 439-445.
45. Gelfand, C.A., Plum, G.E., Grollman, A.P., Johnson, F. and Breslauer, K.J. (1998) The impact of an exocyclic cytosine adduct on DNA duplex properties: Significant thermodynamic consequences despite modest lesion-induced structural alterations. Biochemistry, 37, 12507-12512.
46. Minetti, C.A.S.A., Remeta, D.P., Miller, H., Gelfand, C.A., Plum, G.E., Grollman, A.P. and Breslauer, K.J. (2003) The thermodynamics of template-directed DNA synthesis: Base insertion and extension enthalpies. Proc. Natl Acad. Sci. USA, 100, 14719-14724.
47. Minetti, C.A.S.A., Remeta, D.P., Zharkov, D.O., Plum, G.E., Johnson, F., Grollman, A.P. and Breslauer, K.J. (2003) Energetics of lesion recognition by a DNA repair protein: Thermodynamic characterization of formamidopyrimidine-glycosylase (Fpg) interactions with damaged DNA duplexes. J. Mol. Biol., 328, 1047-1060.
48. Minetti, C.A.S.A., Remeta, D.P. and Breslauer, K.J. (2008) A continuous hyperchromicity assay to characterize the kinetics and thermodynamics of DNA lesion recognition and base excision. Proc. Natl Acad. Sci USA, 105, 70-75.
49. Griswold, B., Humoller, F. and McIntyre, A. (1951) Inorganic phosphates and phosphate esters in tissue extracts. Anal. Chemistry, 23, 192-194.
50. Marky, L.A. and Breslauer, K.J. (1987) Calculating thermodynamic data for transitions of any molecularity from equilibrium melting curves. Biopolymers, 26, 1601-1620.
51. Pilch, D.S., Plum, G.E. and Breslauer, K.J. (1995) The thermodynamics of DNA structures that contain lesions or guanine tetrads. Curr. Opin. Struct. Biol., 5, 334-342.
52. Kalnik, M.W., Norman, D.G., Li, B.F., Swann, P.F. and Patel, D.J. (1990) Conformational transitions in thymidine bulge-containing deoxytridecanucleotide duplexes. Role of flanking sequence and temperature in modulating the equilibrium between looped out and stacked thymidine bulge states. J. Biol. Chem., 265, 636-647.
53. Breslauer, K.J., Frank, R., Blocker, H. and Marky, L.A. (1986) Predicting DNA duplex stability from the base sequence. Proc. Natl Acad. Sci. USA, 83, 3746-3750.
54. Plum, G.E. and Breslauer, K.J. (1995) Calorimetry of proteins and nucleic acids. Curr. Opin. Struct. Biol., 5, 682-690.
55. Plum, G.E., Breslauer, K.J. and Roberts, R.W. (1999) Thermodynamics and kinetics of nucleic acid association/dissociation and folding processes. Comprehensive Natural Products Chemistry. Elsevier Science Ltd., Vol. 7. Oxford, UK, pp. 15-33.
56. Malkov, V.A., Biswas, I., Camerini-Otero, R.D. and Hsieh, P. (1997) Photocross-linking of the NH2-terminal region of Taq MutS protein to the major groove of a heteroduplex DNA. J. Biol. Chem., 272, 23811-23817.
57. Dohet, C., Wagner, R. and Radman, M. (1986) Methyl-directed repair of frameshift mutations in heteroduplex DNA. Proc. Natl Acad. Sci. USA, 83, 3395-3397.
58. Learn, B.A. and Grafstrom, R.H. (1989) Methyl-directed repair of frameshift heteroduplexes in cell extracts from Escherichia coli. J. Bacteriol., 171, 6473-6481.
59. Zeglis, B.M., Boland, J.A. and Barton, J.K. (2009) Recognition of abasic sites and single base bulges in DNA by a metalloinsertor. Biochemistry, 48, 839-849.
60. Sugimoto, N., Yamamoto, K. and Satoh, N. (1999) Positional effect of single bulge nucleotide on PNA(peptide nucleic acid)/DNA hybrid stability. Nucleic Acids Symp. Ser., 42, 95-96.
61. Ohmichi, T., Nakamuta, H., Yasuda, K. and Sugimoto, N. (2000) Kinetic property of bulged helix formation: Analysis of kinetic behavior using nearest-neighbor parameters. J. Am. Chem. Soc., 122, 11286-11294.
62. Mathews, D.H., Disney, M.D., Childs, J.L., Schroeder, S.J., Zuker, M. and Turner, D.H. (2004) Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl Acad. Sci. USA, 101, 7287-7292.
63. Markham, N.R. and Zuker, M. (2005) DINAMelt web server for nucleic acid melting prediction. Nucleic Acids. Res., 33, W577-W581.
64. Markham, N.R. and Zuker, M. (2008) UNAFold: software for nucleic acid folding and hybridization. In Keith, J.M. (ed.), Bioinformatics. Structure, Functions and Applications, Vol. II. Human Press, Totowa, NJ, pp. 3-31.
65. Znosko, B.M., Silvestri, S.B., Volkman, H., Boswell, B. and Serra, M.J. (2002) Thermodynamic parameters for an expanded nearest-neighbor model for the formation of RNA duplexes with single nucleotide bulges. Biochemistry, 41, 10406-10417.
66. Blose, J.M., Manni, M.L., Klapec, K.A., Stranger-Jones, Y., Zyra, A.C., Sim, V., Griffith, C.A., Long, J.D. and Serra, M.J. (2007) Non-nearest-neighbor dependence of the stability for RNA bulge loops based on the complete set of group I single-nucleotide bulge loops. Biochemistry, 46, 15123-15135.
67. Papanicolaou, C., Gouy, M. and Ninio, J. (1984) An energy model that predicts the correct folding of both tRNA and 5S RNA molecules. Nucleic Acid Res., 12, 31-44.
68. Sugimoto, N., Nakano, S., Yoneyama, M. and Honda, K. (1996) Improved thermodynamic parameters and helix initiation factor to predict the stability of DNA duplexes. Nucleic Acids Res., 24, 4501-4505.
69. Santa Lucia, J. Jr, Allawi, H.T. and Seneviratne, P.A. (1996) Improved nearest-neighbor parameters for predicting DNA duplex stability. Biochemistry, 35, 3555-3562.
70. Chalikian, T.V., Volker, J., Plum, G.E. and Breslauer, K.J. (1999) A more unified picture for the thermodynamics of nucleic acid duplex melting: a characterization by calorimetric and volumetric techniques. Proc. Natl Acad. Sci. USA, 96, 7853-7858.
71. Rouzina, I. and Bloomfield, V.A. (1999) Heat capacity effects on the melting of DNA. 1. General aspects. Biophys. J., 77, 3242-3251.
72. Mikulecky, P.J. and Feig, A.L. (2006) Heat capacity changes associated with nucleic acid folding. Biopolymers, 82, 38-58.
73. Jelesarov, I., Crane-Robinson, C. and Privalov, P.L. (1999) The energetics of HMG box interactions with DNA: Thermodynamic description of the target DNA duplexes. J. Mol. Biol., 294, 981-995.
74. Holbrook, J.A., Capp, M.W., Saecker, R.M. and Record, M.T. (1999) Enthalpy and heat capacity changes for formation of an oligomeric DNA duplex: Interpretation in terms of coupled processes of formation and association of single-stranded helices. Biochemistry, 38, 8409-8422.
75. Tikhomirova, A., Taulier, N. and Chalikian, T.V. (2004) Energetics of nucleic acid stability: The effect of Delta C-P. J. Am. Chem. Soc., 126, 16387-16394.
76. Rouzina, I. and Bloomfield, V.A. (1999) Heat capacity effects on the melting of DNA. 2. Analysis of nearest-neighbor base pair effects. Biophys. J., 77, 3252-3255.
77. Kauzmann, W. (1959) Some factors in the interpretation of protein denaturation. Adv. Protein Chem., 14, 1-63.
78. Barthel, A. and Zacharias, M. (2006) Conformational transitions in RNA single uridine and adenosine bulge structures: A molecular dynamics free energy simulation study. Biophys. J., 90, 2450-2462.
79. Hastings, W.A., Yingling, Y.G., Chirikjian, G.S. and Shapiro, B.A. (2006) Structural and dynamical classification of RNA single-base bulges for nanostructure design. J. Comp. Theor. Nanoscience, 3, 63-77.
80. Shibutani, S. and Grollman, A.P. (1993) On the mechanism of frameshift (deletion) mutagenesis in vitro. J. Biol. Chem., 268, 11703-11710.
81. Lambert, I.B., Napolitano, R.L. and Fuchs, R.P. (1992) Carcinogen-induced frameshift mutagenesis in repetitive sequences. Proc. Natl Acad. Sci. USA, 89, 1310-1314.
82. Chi, L.M. and Lam, S.L. (2008) Nuclear magnetic resonance investigation of primer-template models: Formation, of a pyrimidine bulge upon misincorporation. Biochemistry, 47, 4469-4476.
83. Branstrom, M. and Ellegren, H. (2007) The genomic landscape of short insertion and deletion polymorphisms in the chicken (Gallus gallus) genome: a high frequency of deletions in tandem duplicates. Genetics, 176, 1691-1701.