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Computational and Empirical Trans-hydrogen Bond Deuterium Isotope Shifts Suggest that N1–N3 A:U Hydrogen Bonds of RNA are Shorter than those of A:T Hydrogen Bonds of DNA

Journal of Biomolecular NMR volume 34, pages 229–236 (2006)Cite this article

Abstract

Density functional theory calculations of isolated Watson–Crick A:U and A:T base pairs predict that adenine 13C2 trans-hydrogen bond deuterium isotope shifts due to isotopic substitution at the pyrimidine H3, 2hΔ13C2, are sensitive to the hydrogen-bond distance between the N1 of adenine and the N3 of uracil or thymine, which supports the notion that 2hΔ13C2 is sensitive to hydrogen-bond strength. Calculated 2hΔ13C2 values at a given N1–N3 distance are the same for isolated A:U and A:T base pairs. Replacing uridine residues in RNA with 5-methyl uridine and substituting deoxythymidines in DNA with deoxyuridines do not statistically shift empirical 2hΔ13C2 values. Thus, we show experimentally and computationally that the C7 methyl group of thymine has no measurable affect on 2hΔ13C2 values. Furthermore, 2hΔ13C2 values of modified and unmodified RNA are more negative than those of modified and unmodified DNA, which supports our hypothesis that RNA hydrogen bonds are stronger than those of DNA. It is also shown here that 2hΔ13C2 is context dependent and that this dependence is similar for RNA and DNA.

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References

  • J. Abildgaard S. Bolvig P.E. Hansen (1998) J. Am. Chem. Soc. 120 9063–9069 Occurrence Handle10.1021/ja9809051

    Article  Google Scholar 

  • P. Acharya P. Cheruku S. Chatterjee S. Acharya J. Chattopadhyaya (2004) J. Am. Chem. Soc,. 126 2862–2869 Occurrence Handle10.1021/ja0386546

    Article  Google Scholar 

  • A. Asensio N. Kobko J.J. Dannenberg (2003) J. Phys. Chem. A. 107 6441–6443 Occurrence Handle10.1021/jp0344646

    Article  Google Scholar 

  • P. Atkins (1998) Physical Chemistry W.H. Freeman and Company New York

    Google Scholar 

  • M. Barfield A.J. Dingley J. Feigon S. Grzesiek (2001) J. Am. Chem. Soc. 123 4014–4022 Occurrence Handle10.1021/ja003781c

    Article  Google Scholar 

  • A.D. Becke (1988) Phys. Rev. A 38 3098–3100 Occurrence Handle10.1103/PhysRevA.38.3098 Occurrence Handle1988PhRvA..38.3098B

    Article  ADS  Google Scholar 

  • T.V. Chalikian J. Völker A.R. Srinivasan W.K. Olson K.J. Breslauer (1999) Biopolymers 50 459–471 Occurrence Handle10.1002/(SICI)1097-0282(19991015)50:5<459::AID-BIP1>3.0.CO;2-B

    Article  Google Scholar 

  • R. Ditchfield (1974) Mol. Phys. 27 789–807 Occurrence Handle1974MolPh..27..789D

    ADS  Google Scholar 

  • T. Dziembowska P.E. Hansen Z. Rozwadowski (2004) Prog. Nucl. Magn. Reson. Spectrosc. 45 1–29 Occurrence Handle10.1016/j.pnmrs.2004.04.001

    Article  Google Scholar 

  • M. Egli S. Portmann N. Usman (1996) Biochemistry 35 8489–8494 Occurrence Handle10.1021/bi9607214

    Article  Google Scholar 

  • J.B. Foresman Æ. Frisch (1996) Exploring Chemistry with Electronic Structure Methods Gaussian Inc Pittsburgh

    Google Scholar 

  • Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Stratmann, J., Burant, R. E., Dapprich, J. C., Millam, S., Daniels, J. M., Kudin, A. D., Strain, K. N., Farkas, M. C., Tomasi, O., Barone, J., Cossi, V., Cammi, M., Mennucci, R., Pomelli, B., Adamo, C., Clifford, C., Ochterski, S., Petersson, J., Ayala, G. A., Cui, P. Y., Morokuma, Q., Salvador, K., Dannenberg, P., Malick, J. J., Rabuck, D. K., Raghavachari, A. D., Foresman, K., Cioslowski, J. B., Ortiz, J., Baboul, J. V., Stefanov, A. G., Liu, B. B., Liashenko, G., Piskorz, A., Komaromi, P., Gomperts, I., Martin, R., Fox, R. L., Keith, D. J., Al-Laham, T., Peng, M. A., Nanayakkara, C. Y., Challacombe, A., Gill, M., Johnson, P. M. W., Chen, B., Wong, W., Andres, M. W., Gonzalez, J. L., Head-Gordon, C., Replogle, M. and Pople, J. A. (2004) Wallingford, CT

  • D.S. Garrett R. Powers A.M. Gronenborn G.M. Clore (1991) J. Magn. Res. 95 214–220

    Google Scholar 

  • P.C. Hariharan J.A. Pople (1973) Theoret. Chimica Acta 28 213–222 Occurrence Handle10.1007/BF00533485

    Article  Google Scholar 

  • N. Juranic P.K. Ilich S. Macura (1995) J. Am. Chem. Soc. 117 405–410 Occurrence Handle10.1021/ja00106a046

    Article  Google Scholar 

  • N. Juranic V.A. Likic F.G. Prendergast S. Macura (1996) J. Am. Chem. Soc. 118 7859–7860 Occurrence Handle10.1021/ja9542101

    Article  Google Scholar 

  • B.I. Kankia L.A. Marky (1999) J. Phys. Chem. B. 103 8759–8767 Occurrence Handle10.1021/jp991614x

    Article  Google Scholar 

  • P. Legault A. Pardi (1997) J. Am. Chem. Soc. 119 6621–6628 Occurrence Handle10.1021/ja9640051

    Article  Google Scholar 

  • M.N. Manalo X. Kong A. LiWang (2005) J. Am. Chem. Soc. 127 17974–17975 Occurrence Handle10.1021/ja055826l

    Article  Google Scholar 

  • J.L. Markley A. Bax Y. Arata C.W. Hilbers R. Kaptein B.D. Sykes P.E. Wright K. Wüthrich (1998) Pure Appl. Chem. 70 117–142 Occurrence Handle10.1351/pac199870010117

    Article  Google Scholar 

  • P. Mignon S. Loverix J. Steyaert P. Geerlings (2005) Nucl. Acids Res. 33 1779–1789 Occurrence Handle10.1093/nar/gki317

    Article  Google Scholar 

  • E.M. Moody T.S. Brown P.C. Bevilacqua (2004) J. Am. Chem. Soc. 126 10200–10201 Occurrence Handle10.1021/ja047362h

    Article  Google Scholar 

  • G.J. Narlikar D. Herschlag (1997) Annu. Rev. Biochem. 66 19–59 Occurrence Handle10.1146/annurev.biochem.66.1.19

    Article  Google Scholar 

  • J.P. Perdew Y. Wang (1992) Phys. Rev. B 45 13244–13249 Occurrence Handle10.1103/PhysRevB.45.13244 Occurrence Handle1992PhRvB..4513244P

    Article  ADS  Google Scholar 

  • M. Piotto V. Saudek V. Sklenar (1992) J. Biomol. NMR 2 661–665 Occurrence Handle10.1007/BF02192855

    Article  Google Scholar 

  • W. Saenger (1984) Principles of Nucleic Acid Structure Springer-Verlag New York

    Google Scholar 

  • S.-O. Shan D. Herschlag (1996) Proc. Natl. Acad. Sci. USA 93 14474–14479 Occurrence Handle10.1073/pnas.93.25.14474 Occurrence Handle1996PNAS...9314474S

    Article  ADS  Google Scholar 

  • M. Swart C.F. Guerra F.M. Bickelhaupt (2004) J. Am. Chem. Soc. 126 16718–16719 Occurrence Handle10.1021/ja045276b

    Article  Google Scholar 

  • I. Vakonakis A.C. LiWang (2004a) J. Am. Chem. Soc. 126 5688–5689 Occurrence Handle10.1021/ja048981t

    Article  Google Scholar 

  • I. Vakonakis A.C. LiWang (2004b) J. Biomol. NMR 29 65–72 Occurrence Handle10.1023/B:JNMR.0000019507.95667.3e

    Article  Google Scholar 

  • I. Vakonakis M. Salazar M. Kang K.R. Dunbar A.C. LiWang (2003) J. Biomol. NMR 25 105–112 Occurrence Handle10.1023/A:1022211927051

    Article  Google Scholar 

  • S. Wang E.T. Kool (1995) Biochemistry 34 4125–4132 Occurrence Handle10.1021/bi00012a031

    Article  Google Scholar 

  • K. Wolinski J.F. Hinton P. Pulay (1990) J. Am. Chem. Soc. 112 8251–8260 Occurrence Handle10.1021/ja00179a005

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry & Biophysics, Texas A&M University, 2128 TAMU, College Station, TX, 77843-2128, USA

    Yong-Ick Kim, Marlon N. Manalo & Andy LiWang

  2. Laboratory for Molecular Simulation, Texas A&M University, 3012 TAMU, College Station, TX, 77842-3012, USA

    Lisa M. Peréz

Authors
  1. Yong-Ick Kim
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  2. Marlon N. Manalo
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  3. Lisa M. Peréz
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  4. Andy LiWang
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Correspondence to Andy LiWang.

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Kim, YI., Manalo, M.N., Peréz, L.M. et al. Computational and Empirical Trans-hydrogen Bond Deuterium Isotope Shifts Suggest that N1–N3 A:U Hydrogen Bonds of RNA are Shorter than those of A:T Hydrogen Bonds of DNA. J Biomol NMR 34, 229–236 (2006). https://doi.org/10.1007/s10858-006-0021-y

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  • DOI: https://doi.org/10.1007/s10858-006-0021-y

Keywords

  • DNA
  • density functional theory
  • deuterium isotope shift
  • hydrogen bond
  • NMR
  • RNA