The steric hypothesis for DNA replication and fluorine hydrogen bonding revisited in light of structural data

Accounts of Chemical Research

Volumn 45, Issue 8, 2012, Pages 1237-1246

  Egli, Martin ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA DIRECTED DNA POLYMERASE; FLUORINE;

ARTICLE; BASE PAIRING; BIOSYNTHESIS; CHEMISTRY; DNA REPLICATION; GENETICS; HUMAN; HYDROGEN BOND; METABOLISM; NUCLEOTIDE SEQUENCE;

BASE PAIRING; BASE SEQUENCE; DNA; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; FLUORINE; HUMANS; HYDROGEN BONDING;

EID: 84865327750     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar200303k     Document Type: Article

References (43)

1. Moran, S.; Ren, R. X.-F.; Rumney, S.; Kool, E. T. Difluorotoluene, a Nonpolar Isostere of Thymine, Codes Specifically and Efficiently for Adenine in DNA Replication J. Am. Chem. Soc. 1997, 119, 2056-2057
2. Moran, S.; Ren, R. X.; Kool, E. T. A Thymidine Triphosphate Shape Analog Lacking Watson-Crick Pairing Ability is Replicated With High Sequence Selectivity Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 10506-10511
3. Morales, J. C.; Kool, E. T. Efficient Replication Between Non-Hydrogen-Bonded Nucleoside Shape Analogs Nat. Struct. Biol. 1998, 5, 950-954
4. Fischer, E. Einfluss der Configuration auf die Wirkung der Enzyme Ber. Dtsch. Chem. Ges. 1894, 27, 2985-2993
5. Koshland, D. E., Jr. The Key-Lock Theory and the Induced Fit Theory Angew. Chem., Int. Ed. 1994, 33, 2375-2378
6. Kool, E. T. Hydrogen Bonding, Base Stacking, and Steric Effects in DNA Replication Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 1-22
7. Kool, E. T. Active Site Tightness and Substrate Fit in DNA Replication Annu. Rev. Biochem. 2002, 71, 191-219
8. Sintim, H. O.; Kool., E. T. The Difluorotoluene Debate-A Decade Later Chem. Commun. 2006, 35, 3665-3675
9. Lee, I.; Berdis, A. J. Non-Natural Nucleotides as Probes for the Mechanism and Fidelity of DNA Polymerases Biochim. Biophys. Acta 2010, 1804, 1064-1080
10. Howard, J. A. K.; Hoy, V. J.; O'Hagan, D.; Smith, G. T. How Good is Fluorine as a Hydrogen Bond Acceptor? Tetrahedron 1996, 52, 12613-12622
11. Dunitz, J. D. Organic Fluorine: Odd Man Out ChemBioChem 2004, 5, 614-621
12. Rybalova, T. V.; Bagryanskaya, I. Y. C-F···π, F···H, and F···F Intermolecular Interactions and F-Aggregation: Role in Crystal Engineering of Fluoroorganic Compounds J. Struct. Chem. 2009, 50, 741-753
13. Zhou, P.; Zou, J.; Tian, F.; Shang, Z. Fluorine Bonding - How Does It Work in Protein-Ligand Interactions? J. Chem. Inf. Model. 2009, 49, 2344-2355
14. Chopra, D.; Guru Row, T. N. Role of Organic Fluorine in Crystal Engineering CrystEngComm 2011, 13, 2175-2186
15. Sun, Z.; McLaughlin, L. W. Probing the Nature of Three-Centered Hydrogen Bonds in Minor-Groove Ligand-DNA Interactions: The Contribution of Fluorine Hydrogen Bonds to Complex Stability J. Am. Chem. Soc. 2007, 129, 12531-12536
16. Schweitzer, B. A.; Kool, E. T. Hydrophobic, Non-Hydrogen-Bonding Bases and Base Pairs in DNA J. Am. Chem. Soc. 1995, 117, 1863-1872
17. Koller, A. N.; Bozilovic, J.; Engels, J. W.; Gohlke, H. Aromatic N Versus Aromatic F: Bioisosterism Discovered in RNA Base Pairing Interactions Leads to a Novel Class of Universal Base Analogs Nucleic Acids. Res. 2010, 38, 3133-3146
18. Guckian, K; Schweitzer, B. A.; Ren, R. X.-F.; Sheils, C J.; Paris, P. L.; Tahmassebi, D. C.; Kool, E. T. Experimental Measurement of Aromatic Stacking in the Context of Duplex DNA J. Am. Chem. Soc. 1996, 118, 8182-8183
19. Guckian, K. M.; Krugh, T. R.; Kool, E. T. Solution Structure of a Duplex DNA Containing a Replicable Difluorotoluene-Adenine Pair Nat. Struct. Biol. 1998, 5, 954-959
20. Wang, X.; Houk, K. N. Difluorotoluene, a Thymine Isostere, Does Not Hydrogen Bond at All Chem. Commun. 1998, 2631-2632
21. Kim, T.; Brieba, L. G.; Ellenberger, T.; Kool, E. T. Functional Evidence for a Small and Rigid Active Site in a High Fdelity DNA Polymerase: Probing T7 DNA Polymerase with Variably Sized Base Pairs J. Biol. Chem. 2006, 281, 2289-2295
22. Potapova, O.; Chan, C.; DeLucia, A. M.; Helquist, S. A.; Kool, E. T.; Grindley, N. D. F.; Joyce, C. M. DNA Polymerase Catalysis in the Absence of Watson-Crick Hydrogen Bonds: Analysis by Single-Turnover Kinetics Biochemistry 2006, 45, 890-898
23. Lee, H. R.; Helquist, S. A.; Kool, E. T.; Johnson, K. A. Importance of Hydrogen Bonding for Efficiency and Specificity of the Human Mitochondrial DNA Polymerase J. Biol. Chem. 2008, 283, 14402-14410
24. Mizukami, S.; Kim, T.; Helquist, S. A.; Kool, E. T. Varying DNA Base-Pair Size in Subangstrom Increments: Evidence for a Loose, Not Large, Active Site in Low-Fidelity Dpo4 Polymerase Biochemistry 2006, 45, 2772-2778
25. Irimia, A.; Eoff, R. L.; Pallan, P. S.; Guengerich, F. P.; Egli, M. Structure and Activity of Y-class DNA Polymerase Dpo4 from Sulfolobus solfataricus with Templates Containing the Hydrophobic Thymine Analog 2,4-Difluorotoluene J. Biol. Chem. 2007, 282, 36421-36433
26. Washington, M. T.; Helquist, S. A.; Kool, E. T.; Prakash, L.; Prakash, S. Requirement of Watson-Crick Hydrogen Bonding for DNA Synthesis by Yeast DNA Polymerase η Mol. Cell. Biol. 2003, 23, 5107-5112
27. Wolfle, W. T.; Washington, M. T.; Kool, E. T.; Spratt, T. E.; Helquist, S. A.; Prakash, L.; Prakash, S. Evidence for a Watson-Crick Hydrogen Bonding Requirement in DNA Synthesis by Human DNA Polymerase κ Mol. Cell. Biol. 2005, 25, 7137-7143
28. Hogg, M.; Wallace, S. S.; Doublié, S. Bumps in the Road: How Replicative DNA Polymerases See DNA Damage Curr. Opin. Struct. Biol. 2005, 15, 86-93
29. Egli, M. DNA-Cation Interactions: Quo Vadis? Chem. Biol. 2002, 9, 277-286
30. Pallan, P. S.; Egli, M. The Pairing Geometry of the Hydrophobic Thymine Analog 2,4-Difluorotoluene in Duplex DNA as Analyzed by X-ray Crystallography J. Am. Chem. Soc. 2009, 131, 12548-12549
31. Pallan, P. S.; Egli, M. Insights into RNA/DNA Hybrid Recognition and Processing by RNase H from the Crystal Structure of a Non-specific Enzyme-dsDNA Complex Cell Cycle 2008, 7, 2562-2569
32. Tereshko, V.; Minasov, G.; Egli, M. The Dickerson-Drew B-DNA Dodecamer Revisited at Atomic Resolution J. Am. Chem. Soc. 1999, 121, 470-471
33. Xia, J.; Noronha, A.; Toudjarska, I.; Li, F.; Akinc, A.; Braich, R.; Rajeev, K. G.; Egli, M.; Manoharan, M. siRNAs with a Ribo-difluorotoluyl Nucleotide: Structure, RISC-mediated Recognition, and Silencing ACS Chem. Biol. 2006, 1, 176-183
34. Somoza, A.; Chelliserrykattil, J.; Kool, E. T. The Roles of Hydrogen Bonding and Sterics in RNA Interference Angew. Chem., Int. Ed. 2006, 45, 4994-4997
35. Li, F.; Pallan, P. S.; Maier, M. A.; Rajeev, K. G.; Mathieu, S. L.; Kreutz, C.; Fan, Y.; Sanghvi, J.; Micura, R.; Rozners, E.; Manoharan, M.; Egli, M. Crystal Structure, Stability and in Vitro RNAi Activity of Oligoribonucleotides Containing the Ribo-difluorotoluyl Nucleotide: Insights into Substrate Requirements by the Human RISC Ago2 Enzyme Nucleic Acids Res. 2007, 35, 6424-6438
36. Zacharias, M.; Engels, J. W. Influence of a Fluorobenzene Nucleobase Analogue on the Conformational Flexibility of RNA Studied by Molecular Dynamics Simulations Nucleic Acids Res. 2004, 32, 6304-6311
37. Pfaff, D. A.; Clarke, K. M.; Parr, T. A.; Cole, J. M.; Geierstanger, B. H.; Tahmassebi, D. C.; Dwyer, T. J. Solution Structure of a DNA Duplex Containing a Guanine-Difluorotoluene Pair: A Wobble Pair without Hydrogen Bonding? J. Am. Chem. Soc. 2008, 130, 4869-4878
38. Ala from Escherichia coli Shows Unique G.U Wobble Base Pair at 1.16 Å Resolution RNA 1999, 5, 670-677
39. Manoharan, M.; Akinc, A.; Pandey, R. K.; Qin, J.; Hadwiger, P.; John, M.; Mills, K.; Charisse, K.; Maier, M. A; Nechev, L.; Greene, E. M.; Pallan, P. S.; Rozners, E.; Rajeev, K. G.; Egli, M. Unique Gene-Silencing and Structural Properties of 2′-F Modified siRNAs Angew. Chem., Int. Ed. 2011, 50, 2284-2288
40. Pallan, P. S.; Greene, E.; Jicman, P.; Pandey, R.; Manoharan, M.; Rozners, E.; Egli, M. Unexpected Origins of the Enhanced Pairing Affinity of 2′-Fluoro-Modified RNA Nucleic Acids Res. 2011, 39, 3482-3495
41. Li, F.; Sarkhel, S.; Wilds, C. J.; Wawrzak, Z.; Prakash, T. P.; Manoharan, M.; Egli, M. 2′-Fluoroarabino- and Arabinonucleic Acid Show Different Conformations, Resulting in Deviating RNA Affinities and Processing of Their Heteroduplexes with RNA by RNase H Biochemistry 2006, 45, 4141-4152
42. Yahyaee Anzahaee, M.; Watts, J. K.; Alla, N. R.; Nicholson, A. W.; Damha, M. J. Energetically Important C-H···F-C Pseudohydrogen Bonding in Water: Evidence and Application to Rational Design of Oligonucleotides with High Binding Affinity J. Am. Chem. Soc. 2011, 133, 728-731
43. Xia, S.; Eom, S. H.; Konigsberg, W. H.; Wang, J. Structural Basis for Differential Insertion Kinetics of dNMPs Opposite a Difluorotoluene Nucleotide Residue Biochemistry 2012, 51, 1476-1485