Impact of sugar pucker on base pair and mispair stability

Biochemistry

Volumn 48, Issue 50, 2009, Pages 11994-12004

  Williams, Adides A ^a   Darwanto, Agus ^a   Theruvathu, Jacob A ^a   Burdzy, Artur ^a   Neidigh, Jonathan W ^a   Sowers, Lawrence C ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-TUMORS; ANTIVIRAL AGENTS; BASE PAIRING; BASE PAIRS; BIOLOGICAL PROPERTIES; DEOXYNUCLEOSIDES; DNA LIGASES; DUPLEX FORMATION; ENTROPY-ENTHALPY COMPENSATION; MELTING TEMPERATURES; MODIFIED NUCLEOSIDES; NUCLEOSIDE TRIPHOSPHATES; PRIMER EXTENSION; STRUCTURAL FEATURE; SUGAR PUCKER;

BIOMOLECULES; DNA; GENES; MELTING POINT; NUCLEIC ACIDS; OLIGONUCLEOTIDES; RNA; SUGAR (SUCROSE); THERMODYNAMIC STABILITY; THERMODYNAMICS;

SUGARS;

2' DEOXY 2' FLUOROARABINOFURANOSYLURACIL; 2' DEOXY 2' FLUORORIBOFURANOSYLURACIL; NUCLEOSIDE ANALOG; OLIGONUCLEOTIDE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; SUGAR; UNCLASSIFIED DRUG;

ARTICLE; BASE MISPAIRING; CHEMICAL STRUCTURE; ENTHALPY; ENTROPY; HUMAN; MELTING POINT; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE; THERMODYNAMICS;

BASE PAIR MISMATCH; BASE PAIRING; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CARBOHYDRATES; DEOXYURIDINE; DNA LIGASES; ESCHERICHIA COLI PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID HETERODUPLEXES; OLIGONUCLEOTIDES; THERMODYNAMICS;

ARA;

EID: 72449191194     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9014133     Document Type: Article

References (60)

1. Petruska, J., Sowers, L. C., and Goodman, M. F. (1986) Comparison of nucleotide interactions in water, protein, and vacuum: Model for DNA polymerase fidelity. Proc. Natl. Acad. Sci. U.S.A. 83, 1559-1562.
2. Joyce, C. M., Sun, X. C., and Grindley, N. D. F. (1992) Reactions at the polymerase active site that contribute to the fidelity of Escherichia coli DNA polymerase I (Klenow Fragment). J. Biol. Chem. 267, 24485-24500.
3. Johnson, K. A. (1993) Conformational coupling in DNA polymerase fidelity. Annu. Rev. Biochem. 62, 685-713.
4. Goodman, M. F., and Fygenson, D. K. (1998) DNA polymerase fidelity: From genetics toward a biochemical understanding. Genetics 148, 1475-1482.
5. Beard, W. A., and Wilson, S. H. (2003) Structural insights into the origins of DNA polymerase fidelity. Structure 11, 489-496. (Pubitemid 36579127)
6. Joyce, C. M., and Benkovic, S. J. (2004) DNA polymerase fidelity: Kinetics, structure, and checkpoints. Biochemistry 43, 14318-14324.
7. Thompson, H. T., Sheaff, R. J., and Kuchta, R. D. (1995) Interactions of calf thymus DNA polymerase α with primer/templates. Nucleic Acids Res. 23, 4109-4115.
8. Richardson, F. C., Kuchta, R. D., Mazurkiewicz, A., and Richardson, K. A. (2000) Polymerization of 2′-Fluoro- and 2′-O-Methyl-dNTPs by human DNA polymerase α, polymerase γ, and primase. Biochem. Pharmacol. 59, 1045-1052.
9. Astatke, M., Grindley, M. D. F., and Joyce, C. M. (1998) How E. coli DNA polymerase I (Klenow fragment) distinguishes between deoxy- and dideoxynucleotides. J. Mol. Biol. 278, 147-165.
10. Marquez, V. E., Ben-Kasus, T., Barchi, J. J., Green, K. M., Nicklaus, M. C., and Agbaria, R. (2004) Experimental and structural evidence that herpes 1 kinase and cellular DNA polymerase(s) discriminate on the basis of sugar pucker. J. Am. Chem. Soc. 126, 543-549.
11. Petruska, J., Goodman, M. F., Boosalis, M. S., Sowers, L. S., Cheong, C., and Tinoco, I. (1988) Comparison between DNA melting thermodynamics and DNA polymerase fidelity. Proc. Natl. Acad. Sci. U.S.A. 85, 6252-6256.
12. Perrino, F. W., Preston, B. D., Sandell, L. L., and Loeb, L. A. (1989) Extension of mismatched 3′ termini of DNA is a major determinant of the infidelity of human immunodeficiency virus type 1 reverse transcriptase. Proc. Natl. Acad. Sci. U.S.A. 86, 8343-8347.
13. Zinnen, S., Hsieh, J.-C., and Modrich, P. (1994) Misincorporation and mispaired primer extension by human immunodeficiency virus reverse transcriptase. J. Biol. Chem. 269, 24195-24202.
14. Mendelman, L. V., Petruska, J., and Goodman, M. F. (1990) Base pair extension kinetics. Comparision of DNA polymerase α and reverse transcriptase. J. Biol. Chem. 265, 2338-2346.
15. Shah, A. M., Maitra, M., and Sweasy, J. B. (2003) Variants of DNA polymerase β extend mispaired DNA due to increased affinity for nucleotide substrate. Biochemistry 42, 10709-10717. (Pubitemid 37102110)
16. Altona, C., and Sundaralingam, M. (1972) Conformational analysis of the sugar ring in nucleosides and nucleotides. A new description using the concept of pseudorotation. J. Am. Chem. Soc. 94, 8205-8212.
17. Levitt, M., and Warshel, A. (1978) Extreme conformational flexibility of the furanose ring in DNA and RNA. J. Am. Chem. Soc. 100, 2607-2613.
18. Ferrin, L. J., and Mildvan, A. S. (1985) Nuclear overhauser effect studies of the conformations and binding site environments of deoxynucleoside triphosphate substrates bound to DNA polymerase I and its large fragment. Biochemistry 24, 6904-6913.
19. Harvey, S. C., and Prabhakaran, M. (1986) Ribose puckering: Structure, dynamics, energetics, and the pseudorotation cycle. J. Am. Chem. Soc. 108, 6128-6136.
20. Boulard, Y., Cognet, J. A., Gabarro-Arpa, J., Le Bret, M., Sowers, L. C., and Fazakerley, G. V. (1992) The pH dependent configurations of the C·A mispair in DNA. Nucleic Acids Res. 20, 1933-1941.
21. Cullinan, D., Johnson, F., Grollman, A. P., Eisenberg, M., and De Los Santos, C. (1997) Solution structure of a DNA duplex containing the exocyclic lesion 3, N4-etheno-2′-deoxycytidine opposite 2′-deoxyguanosine. Biochemistry 36, 11933-11943.
22. Allawi, H. T., and SantaLucia, J., Jr. (1998) NMR solution structure of a DNA dodecamer containing single G·T mismatches. Nucleic Acids Res. 26, 4925-4934.
23. Tonelli, M., and James, T. L. (1998) Insights into the dynamic nature of DNA duplex structure via analysis of nuclear Overhauser effect intensities. Biochemistry 37, 11478-11487. (Pubitemid 28388189)
24. Berger, I., Tereshko, V., Ikeda, H., Marquez, V. E., and Egli, M. (1998) Crystal structure of B-DNA with incorporated 2′-deoxy-2′- fluoroarabino-furanosyl thymines: Implications of conformational preorganization for duplex stability. Nucleic Acids Res. 26, 2473-2480. (Pubitemid 28297351)
25. Damha, M. J., Wilds, C. J., Noronha, A., Brukner, I., Borkow, G., Arion, D., and Parniak, M. A. (1998) Hybrids of RNA and arabinonucleic acids (ANA and 2′F-ANA) are substrates of ribonuclease H. J. Am. Chem. Soc. 120, 12976-12977.
26. 2. Nucleic Acids Res. 26, 2237-2244.
27. Wilds, C. J., and Damha, M. J. (1999) Duplex recognition by oligonucleotides containing 2′-deoxy-2′-fluoro-D-arabinose and 2′-deoxy-2′-fluoro-D-ribose. Intermolecular 2′-OH-phosphate contacts versus sugar puckering in the stabilization of triple-helical complexes. Bioconjugate Chem. 10, 299-305.
28. Schultz, R. G., and Gryaznov, S. M. (2000) Arabino-fluorooligonucleotide N3′ → P5′ phosphoramidates: Synthesis and properties. Tetrahedron Lett. 41, 1895-1899.
29. Wilds, C. J., and Damha, M. J. (2000) 2′-Deoxy-2′-fluoro- β-D-arabinonucleosides and oligonucleotides (2′F-ANA): Synthesis and physicochemical studies. Nucleic Acids Res. 28, 3625-3635.
30. Trempe, J.-F., Wilds, C. J., Denisov, A. Y., Pon, R. T., Damha, M. J., and Gehring, K. (2001) NMR solution structure of an oligonucleotide hairpin with a 2′F-ANA/RNA stem: Implications for RNase H specificity toward DNA/RNA hybrid duplexes. J. Am. Chem. Soc. 123, 4896-4903.
31. Kalota, A., Karabon, L., Swider, C. R., Viazovkina, E., Elzagheid, E., Damha, M. J., and Gewirtz, A. M. (2006) 2′-Deoxy-2′-fluoro-β-D- arabinonucleic acid (2′F-ANA) modified oligonucleotides (ON) effect highly efficient, and persistent, gene silencing. Nucleic Acids Res. 34, 451-461.
32. Peng, C. G., and Damha, M. J. (2007) G-Quadruplex induced stabilization by 2′-deoxy-2′-fluoro-D-arabinonucleic acids (2′F-ANA). Nucleic Acids Res. 35, 4977-4988.
33. Ziemkowski, P., Felczak, K., Poznanski, J., Kulikowski, T., Zielinski, Z., Ciesla, J., and Rode, W. (2007) Interactions of 2′-fluoro-substituted dUMP analogues with thymidylate synthase. Biochem. Biophys. Res. Commun. 362, 37-43.
34. Pinto, D., Sarocchi-Landousy, M.-T., and Guschlbauer, W. (1979) 2′-Deoxy-2′-fluorouridine-5′-triphosphates: A possible substrate for E. coli RNA polymerase. Nucleic Acids Res. 6, 1041-1048.
35. Mikita, T., and Beardsley, G. P. (1988) Functional consequences of the arabinosylcytosine structural lesion in DNA. Biochemistry 27, 4698-4705. (Pubitemid 18183586)
36. Kuchta, R. D., Ilsley, D., Kravig, K. D., Schubert, S., and Harris, B. (1992) Inhibition of DNA primase and polymerase α by arabinofuranosylnucleoside triphosphates and related compounds. Biochemistry 31, 4720-4728.
37. Perrino, F. W., and Mekosh, H. L. (1992) Incorporation of cytosine arabinoside monophosphate into DNA at internucleotide linkages by human DNA polymerase α. J. Biol. Chem. 267, 23043-23051.
38. Lewis, W., Meyer, R. R., Simpson, J. F., Colacino, J. M., and Perrino, F. W. (1994) Mammalian DNA polymerases α, β, γ, δ, and ε incorporate fialuridine (FIAU) monophosphate into DNA and are inhibited competitively by FIAU triphosphate. Biochemistry 33, 14620-14624.
39. Ono, T., Scalf, M., and Smith, L. M. (1997) 2′-Fluoro modified nucleic acids: Polymerase-directed synthesis, properties and stability to analysis by matrix-assisted laser desorption/ionization mass spectrometry. Nucleic Acids Res. 25, 4581-4588. (Pubitemid 27500771)
40. Perrino, F. W., Mazur, D. J., Ward, H., and Harvey, S. (1999) Exonucleases and the incorporation of aranucleotides into DNA. Cell Biochem. Biophys. 30, 331-352.
41. Richardson, K. A., Vega, T. P., Richardson, F. C., Moore, C. L., Rohloff, J. C., Tomkinson, B., Bendele, R. A., and Kuchta, R. D. (2004) Polymerization of the triphosphates of AraC, 2′,2′-difluorodeoxycytidine (dFdC) and OSI-7836 (T-araC) by human DNA polymerase α and DNA primase. Biochem. Pharmacol. 68, 2644-3647.
42. Tann, C. H., Brodfuehrer, P. R., Brundidge, S. P., Sapino, C., Jr., and Howell, H. G. (1985) Fluorocarbohydrates in synthesis. An efficient synthesis of 1-(2-deoxy-2-fluoro-β-D-arabinofuranosyl) thymine (β-FMAU). J. Org. Chem. 50, 3644-3647.
43. Howell, H. G., Brodfuehrer, P. R., Brundidge, S. P., Benigni, D. A., and Sapino, C., Jr. (1988) Antiviral nucleosides. A stereospecific, total synthesis of 2′-fluoro-2′-deoxy-β-D-arabinofuranosyl nucleosides. J. Org. Chem. 53, 85-88.
44. Martin, J. A., Bushnell, D. J., Duncan, I. B., Dunsdon, S. J., Hall, M. J., Machin, P. J., Merrett, J. H., Parkes, K. E. B., Roberts, N. A., Thomas, G. J., Galpin, S. A., and Kinchington, D. (1990) Synthesis and antiviral activity of monofluoro and difluoro analogues of pyrimidine deoxyribonucleosides against human immunodeficiency virus (HIV-1). J. Med. Chem. 33, 2137-2145. (Pubitemid 20236657)
45. 211At]astato-1-(2-deoxy-2-fluoro-β- D-arabinofuranosyl) uracil by a halodestannylation reaction. Nucl. Med. Biol. 25, 487-496.
46. Hamamoto, S., and Takaku, K. (1986) New approach to the synthesis of deoxyribonucleoside phosphoramidite derivatives. Chem. Lett., 1401-1404.
47. Gait, M. J. (1984) Oligonucleotide synthesis: A practical approach , Oxford, IRL Press, Washington, DC.
48. Cui, Z., Theruvathu, J. A., Farrel, A., Burdzy, A., and Sowers, L. C. (2008) Characterization of synthetic oligonucleotides containing biologically important modified bases by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Anal. Biochem. 379, 196-207.
49. Connolly, B. A., and Newman, P. C. (1989) Synthesis and properties of oligonucleotides containing 4-thiothymidine, 5-methyl-2-pyrimidinone-1-β-D- (2′-deoxyriboside) and 2-thiothymidine. Nucleic Acids Res. 17, 4957-4974.
50. Pon, R. T., and Yu, R. (1997) Hydroquinone-O,O′-diacetic acid as a more labile replacement for succinic acid linkers in solid-phase oligonucleotide synthesis. Tetrahedron Lett. 38, 3327-3330.
51. Azhayev, A. V., and Antopolsky, M. L. (2001) Amide group assisted 3′-dephosphorylation of oligonucleotides synthesized on universal A-supports. Tetrahedron 57, 4977-4986.
52. Puglisi, J. D., and Tinoco, I., Jr. (1989) Absorbance melting curves of RNA. Methods in Enzymology (Dahlberg, J. E., and Abelson, E. N., Eds.) Vol.180, pp 304-325, Academic Press, Orlando, FL.
53. SantaLucia, J., Jr., Allawi, H. T., and Seneviratne, P. A. (1996) Improved nearest-neighbor parameters for predicting DNA duplex stability. Biochemistry 35, 3555-3562.
54. Allawi, H. T., and SantaLucia, J., Jr. (1997) Thermodynamics and NMR of internal G·T mismatches in DNA. Biochemistry 36, 10581-10594.
55. Liu, P., Burdzy, A., and Sowers, L. C. (2004) DNA ligases ensure fidelity by interrogating minor groove contacts. Nucleic Acids Res. 32, 4503-4511. (Pubitemid 39317728)
56. 1H NMR investigation at 500 MHz. Nucleic Acids Res. 13, 3343-3355.
57. Carbonnaux, C., Fazakerley, G. V., and Sowers, L. C. (1990) An NMR structural study of deaminated base pairs in DNA. Nucleic Acids Res. 18, 4075-4081. (Pubitemid 20240196)
58. Sowers, L. C., Shaw, B. R., and Sedwick, W. D. (1987) Base stacking and molecular polarizability: Effect of a methyl group in the 5-position of pyrimidines. Biochem. Biophys. Res. Commun. 148, 790-794.
59. 3G (X, Y = A, C, G, T). Nucleic Acids Res. 13, 4811-4824.
60. McTigue, P. M., Peterson, R. J., and Kahn, J. D. (2004) Sequence-dependent thermodynamic parameters for locked nucleic acid (LNA)-DNA duplex formation. Biochemistry 43, 5388-5405.