Widespread transient Hoogsteen base pairs in canonical duplex DNA with variable energetics

Nature Communications

Volumn 5, Issue , 2014, Pages

  Alvey, Heidi S ^a   Gottardo, Federico L ^a   Nikolova, Evgenia N ^b   Al Hashimi, Hashim M ^c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; DNA;

DNA; ENERGY BALANCE; NUCLEAR MAGNETIC RESONANCE;

ARTICLE; BASE PAIRING; CIRCULAR DICHROISM; DNA CONFORMATION; ENERGY TRANSFER; HOOGSTEEN BASE PAIRING; PROTON NUCLEAR MAGNETIC RESONANCE; WATSON CRICK BASE PAIRING; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; HYDROGEN BOND; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PROCEDURES; THERMODYNAMICS;

BASE PAIRING; BASE SEQUENCE; DNA; HYDROGEN BONDING; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; THERMODYNAMICS;

EID: 84912555769     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5786     Document Type: Article

References (48)

1. Nikolova, E. N. et al. Transient Hoogsteen base pairs in canonical duplex DNA. Nature 470, 498-502 (2011).
2. Nikolova, E. N., Gottardo, F. L. & Al-Hashimi, H. M. Probing transient Hoogsteen hydrogen bonds in canonical duplex DNA using NMR relaxation dispersion and single-atom substitution. J. Am. Chem. Soc. 134, 3667-3670 (2012).
3. Nikolova, E. N., Goh, G. B., Brooks, III C. L. & Al-Hashimi, H. M. Characterizing the protonation state of cytosine in transient G.C Hoogsteen base pairs in duplex DNA. J. Am. Chem. Soc. 135, 6766-6769 (2013).
4. Palmer, III A. G. Chemical exchange in biomacromolecules: past, present, and future. J. Magn. Reson. 241, 3-17 (2014).
5. Sekhar, A. & Kay, L. E. NMR paves the way for atomic level descriptions of sparsely populated, transiently formed biomolecular conformers. Proc. Natl Acad. Sci. USA 110, 12867-12874 (2013).
6. Hansen, A. L., Nikolova, E. N., Casiano-Negroni, A. & Al-Hashimi, H. M. Extending the range of microsecond-to-millisecond chemical exchange detected in labeled and unlabeled nucleic acids by selective carbon R(1rho) NMR spectroscopy. J. Am. Chem. Soc. 131, 3818-3819 (2009).
7. Hoogsteen, K. The structure ofcrystals containing a hydrogen-bonded complex of 1-methylthymine and 9-methyladenine. Acta Crystallogr. 12, 822-823 (1959).
8. Nikolova, E. N. et al. A historical account of hoogsteen base-pairs in duplex DNA. Biopolymers 99, 955-968 (2013).
9. Rice, P. A., Yang, S., Mizuuchi, K. & Nash, H. A. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 87, 1295-1306 (1996).
10. Aishima, J. et al. A Hoogsteen base pair embedded in undistorted B-DNA. Nucleic Acids Res. 30, 5244-5252 (2002).
11. Patikoglou, G. A. et al. TATA element recognition by the TATA box-binding protein has been conserved throughout evolution. Genes Dev. 13, 3217-3230 (1999).
12. Kitayner, M. et al. Diversity in DNA recognition by p53 revealed by crystal structures with Hoogsteen base pairs. Nat. Struct. Mol. Biol. 17, 423-429 (2010) .
13. Bohnuud, T. et al. Computational mapping reveals dramatic effect of Hoogsteen breathing on duplex DNA reactivity with formaldehyde. Nucleic Acids Res. 40, 7644-7652 (2012).
14. Yang, W. Structure and mechanism for DNA lesion recognition. Cell Res. 18, 184-197 (2008).
15. Yang, H., Zhan, Y., Fenn, D., Chi, L. M. & Lam, S. L. Effect of 1-methyladenine on double-helical DNA structures. FEBS Lett. 582, 1629-1633 (2008).
16. Nair, D. T., Johnson, R. E., Prakash, S., Prakash, L. & Aggarwal, A. K. Replication by human DNA polymerase-iota occurs byHoogsteen base-pairing. Nature 430, 377-380 (2004).
17. Makarova, A. V. & Kulbachinskiy, A. V. Structure of human DNA polymerase iota and the mechanism of DNA synthesis. Biochemistry (Moscow) 77, 547-561 (2012).
18. Harris, R. C. et al. Opposites attract: shape and electrostatic complementarity in protein-DNA complexes. in Innovations in Biomolecular Modeling and Simulations Vol 2 (ed. Schlick, T.) 53-80 (Royal Soc Chemistry, 2012).
19. Rohs, R. et al. The role of DNA shape in protein-DNA recognition. Nature 461, 1248-1253 (2009).
20. Johnson, R. E., Prakash, L. & Prakash, S. Biochemical evidence for the requirement of Hoogsteen base pairing for replication by human DNA polymerase iota. Proc. Natl Acad. Sci. USA 102, 10466-10471 (2005).
21. Liu, K., Miles, H. T., Frazier, J. & Sasisekharan, V. A novel DNA duplex. A parallel-stranded DNA helix with Hoogsteen base pairing. Biochemistry 32, 11802-11809 (1993).
22. Abrescia, N. G., Gonzalez, C., Gouyette, C. & Subirana, J. A. X-ray and NMR studies of the DNA oligomer d(ATATAT): Hoogsteen base pairing in duplex DNA. Biochemistry 43, 4092-4100 (2004).
23. Abrescia, N. G., Thompson, A., Huynh-Dinh, T. & Subirana, J. A. Crystal structure of an antiparallel DNA fragment with Hoogsteen base pairing. Proc. Natl Acad. Sci. USA 99, 2806-2811 (2002).
24. Cubero, E., Luque, F. J. & Orozco, M. Theoretical study of the Hoogsteen-Watson-Crick junctions in DNA. Biophys. J. 90, 1000-1008 (2006).
25. Cubero, E., Abrescia, N. G., Subirana, J. A., Luque, F. J. & Orozco, M. Theoretical study of a new DNA structure: the antiparallel Hoogsteen duplex. J. Am. Chem. Soc. 125, 14603-14612 (2003).
26. Ughetto, G. et al. A comparison of the structure of echinomycin and triostin A complexed to a DNA fragment. Nucleic Acids Res. 13, 2305-2323 (1985).
27. Gilbert, D. E., van der Marel, G. A., van Boom, J. H. & Feigon, J. Unstable Hoogsteen base pairs adjacent to echinomycin binding sites within a DNA duplex. Proc. Natl Acad. Sci. USA 86, 3006-3010 (1989).
28. Schwartz, T., Rould, M. A., Lowenhaupt, K., Herbert, A. & Rich, A. Crystal structure of the Zalpha domain ofthe human editing enzyme ADAR1 bound to left-handed Z-DNA. Science 284, 1841-1845 (1999).
29. Bothe, J. R., Lowenhaupt, K. & Al-Hashimi, H. M. Sequence-specific B-DNA flexibility modulates Z-DNA formation. J. Am. Chem. Soc. 133, 2016-2018 (2011)
30. Ha, S. C., Lowenhaupt, K., Rich, A., Kim, Y. G. & Kim, K. K. Crystal structure of a junction between B-DNA and Z-DNA reveals two extruded bases. Nature 437, 1183-1186 (2005).
31. SantaLucia, Jr J., Allawi, H. T. & Seneviratne, P. A. Improved nearest-neighbor parameters for predicting DNA duplex stability. Biochemistry 35, 3555-3562 (1996).
32. Coman, D. & Russu, I. M. A nuclear magnetic resonance investigation of the energetics of basepair opening pathways in DNA. Biophys. J. 89, 3285-3292 (2005).
33. Gueron, M., Kochoyan, M. & Leroy, J. L. A single mode of DNA base-pair opening drives imino proton exchange. Nature 328, 89-92 (1987).
34. Fersht, A. R., Matouschek, A. & Serrano, L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol. 224, 771-782 (1992).
35. Neudecker, P., Zarrine-Afsar, A., Davidson, A. R. & Kay, L. E. Phi-value analysis of a three-state protein folding pathway by NMR relaxation dispersion spectroscopy. Proc. Natl Acad. Sci. USA 104, 15717-15722 (2007).
36. Wang, J. DNA polymerases: Hoogsteen base-pairing in DNA replication? Nature 437, E6-E7 discussion E7 (2005).
37. Honig, B. & Rohs, R. Biophysics: flipping Watson and Crick. Nature 470, 472-473 (2011).
38. Ronning, D. R. et al. Active site sharing and subterminal hairpin recognition in a new class of DNA transposases. Mol. Cell 20, 143-154 (2005).
39. Wang, A. H. et al. The molecular structure of a DNA-triostin A complex. Science 225, 1115-1121 (1984).
40. Zhang, Y., Xi, Z., Hegde, R. S., Shakked, Z. & Crothers, D. M. Predicting indirect readout effects in protein-DNA interactions. Proc. Natl Acad. Sci. USA 101, 8337-8341 (2004).
41. Zimmer, D. P. & Crothers, D. M. NMR of enzymatically synthesized uniformly 13C15N-labeled DNA oligonucleotides. Proc. Natl Acad. Sci. USA 92, 3091-3095 (1995).
42. Pelupessy, P., Chiarparin, E. & Bodenhausen, G. Excitation of selected proton signals in NMR of isotopically labeled macromolecules. J. Magn. Reson. 138, 178-181 (1999).
43. Delaglio, F. et al. Nmrpipe-a multidimensional spectral processing system based on unix pipes. J. Biomol. NMR 6, 277-293 (1995).
44. Spyracopoulos, L. A suite of mathematica notebooks for the analysis of protein main chain 15N NMR relaxation data. J. Biomol. NMR 36, 215-224 (2006).
45. Miloushev, V. Z. & Palmer, III A. G. R(1rho) relaxation for two-site chemical exchange: general approximations and some exact solutions. J. Magn. Reson. 177, 221-227 (2005).
46. Akaike, H. A new look at the statistical model identification. IEEE Trans. Aut. Contr. 19, 716-723 (1974).
47. Schulz, M. N., Landstrom, J. & Hubbard, R. E. MTSA-a Matlab program to fit thermal shift data. Anal. Biochem. 433, 43-47 (2013).
48. Doktycz, M. J., Morris, M. D., Dormady, S. J., Beattie, K. L. & Jacobson, K. B. Optical melting of 128 octamer DNA duplexes: effects of base pair location and nearest neighbors on thermal stability. J. Biol. Chem. 270, 8439-8445 (1995).