Skip to main content
SpringerLink
Log in

Probing the nature of hydrogen bonds in DNA base pairs

  • Original Paper
  • Published:
Journal of Molecular Modeling Aims and scope Submit manuscript

Abstract

Energy decomposition analyses based on the block-localized wave-function (BLW-ED) method are conducted to explore the nature of the hydrogen bonds in DNA base pairs in terms of deformation, Heitler–London, polarization, electron-transfer and dispersion-energy terms, where the Heitler–London energy term is composed of electrostatic and Pauli-exchange interactions. A modest electron-transfer effect is found in the Watson–Crick adenine–thymine (AT), guanine–cytosine (GC) and Hoogsteen adenine-thymine (H-AT) pairs, confirming the weak covalence in the hydrogen bonds. The electrostatic attraction and polarization effects account for most of the binding energies, particularly in the GC pair. Both theoretical and experimental data show that the GC pair has a binding energy (−25.4 kcal mol−1 at the MP2/6-31G** level) twice that of the AT (−12.4 kcal mol−1) and H-AT (−12.8 kcal mol−1) pairs, compared with three conventional N-H···O(N) hydrogen bonds in the GC pair and two in the AT or H-AT pair. Although the remarkably strong binding between the guanine and cytosine bases benefits from the opposite orientations of the dipole moments in these two bases assisted by the π-electron delocalization from the amine groups to the carbonyl groups, model calculations demonstrate that π-resonance has very limited influence on the covalence of the hydrogen bonds. Thus, the often adopted terminology “resonance-assisted hydrogen bonding (RHAB)” may be replaced with “resonance-assisted binding” which highlights the electrostatic rather than electron-transfer nature of the enhanced stabilization, as hydrogen bonds are usually regarded as weak covalent bonds.

Electron density difference (EDD) maps for the GC pair: a shows the polarization effect (isodensity 1.2×10−3 a.u.); b shows the charge transfer effect (isodensity 2×10−4 a.u.)

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Scheme 1

Similar content being viewed by others

References

  1. Burkert U, Allinger NL (1982) Molecular mechanics. American Chemical Society, Washington DC

    Google Scholar 

  2. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M (1983) J Comp Chem 4:187–217

    Article  CAS  Google Scholar 

  3. Reindl B, Clark T, Schleyer PvR (1996) J Comp Chem 17:1406–1430

    Article  CAS  Google Scholar 

  4. Kitaura K, Morokuma K (1976) Int J Quantum Chem 10:325–340

    Article  CAS  Google Scholar 

  5. Stevens WJ, Fink WH (1987) Chem Phys Lett 139:15–22

    Article  CAS  Google Scholar 

  6. Gutowski M, Piela L (1988) Mol Phys 64:337–355

    Article  CAS  Google Scholar 

  7. Cybulski SM, Scheiner S (1990) Chem Phys Lett 166:57–64

    Article  CAS  Google Scholar 

  8. Moszynski R, Heijmen TGA, Jeziorski B (1994) Mol Phys 88:741–758

    Article  Google Scholar 

  9. Glendening ED, Streitwieser A (1994) J Chem Phys 100:2900–2909

    Article  CAS  Google Scholar 

  10. van der Vaart A, Merz KM Jr (1999) J Phys Chem A 103:3321–3329

    Article  Google Scholar 

  11. Mo Y, Gao J, Peyerimhoff SD (2000) J Chem Phys 112:5530–5538

    Article  CAS  Google Scholar 

  12. Gentle IR, Ritchie GLD (1989) J Phys Chem 93:7740–7744

    Article  CAS  Google Scholar 

  13. Craven IE, Hesling MR, Laver DR, Lukins PB, Ritchie GLD, Vrbancich J (1989) J Phys Chem 93:627–631

    Article  CAS  Google Scholar 

  14. Dougherty DA (1996) Science 271:163–168

    Article  CAS  Google Scholar 

  15. Mecozzi S, West AP, Dougherty DA (1996) J Am Chem Soc 118:2307–2308

    Article  CAS  Google Scholar 

  16. Cubero E, Luque FJ, Orozco M (1998) Proc Natl Acad Sci USA 95:5976–5980

    Article  CAS  Google Scholar 

  17. Caldwell JW, Kollman PA (1995) J Am Soc Chem 117:4177–4178

    Article  CAS  Google Scholar 

  18. Mo Y, Subramanian G, Ferguson DM, Gao J (2002) J Am Chem Soc 124:4832–4837

    Article  CAS  Google Scholar 

  19. Morokuma K (1977) Acc Chem Res 10:294–300

    Article  CAS  Google Scholar 

  20. Jeffrey GA (1997) An introduction to hydrogen bonding. Oxford University Press, New York

    Google Scholar 

  21. Šponer J, Jurecka P, Hobza P (2004) J Am Chem Soc 126:10142–10151

    Article  CAS  Google Scholar 

  22. Cheatham TE III, Kollman PA (2000) Ann Rev Phys Chem 51:435–471

    Article  CAS  Google Scholar 

  23. Kratochvíl M, Šponer J, Hobza P (2000) J Am Chem Soc 122:3495–3499

    Article  CAS  Google Scholar 

  24. Guerra CF, Bickelhaupt FM (1999) Angew Chem Int Ed 38:2942–2945

    Article  CAS  Google Scholar 

  25. Guerra CF, Bickelhaupt FM, Snijders JG, Baerends EJ (1999) Chem Eur J 5:3581–3594

    Article  CAS  Google Scholar 

  26. Guerra CF, Bickelhaupt FM, Snijders JG, Baerends EJ (2000) J Am Chem Soc 122:4117–4128

    Article  CAS  Google Scholar 

  27. Mo Y, Peyerimhoff SD (1998) J Chem Phys 109:1687–1697

    Article  CAS  Google Scholar 

  28. Cubero E, Luque FJ, Orozco M (2001) J Am Chem Soc 123:12018–12025

    Article  CAS  Google Scholar 

  29. Boys SF, Bernardi F (1970) Mol Phys 19:553–566

    Article  CAS  Google Scholar 

  30. Mo Y, Gao J (2001) J Phys Chem A 105:6530–6536

    Article  CAS  Google Scholar 

  31. Mo Y, Song L, Wu W, Zhang Q (2004) J Am Chem Soc 126:3974–3982

    Article  CAS  Google Scholar 

  32. Gianinetti E, Raimondi, Tornaghi E (1996) Int J Quantum Chem 60:157–166

    Article  CAS  Google Scholar 

  33. Gianinetti E, Vandoni I, Famulari A, Raimondi M (1998) Adv Quantum Chem 31:251–266

    Article  CAS  Google Scholar 

  34. Schmidt MW, Baldridge KK, Boatz JA, Elbert ST, Gordon MS, Jensen JJ, Koseki S, Matsunaga N, Nguyen KA, Su S, Windus TL, Dupuis M, Montgomery JA (1993) J Comput Chem 14:1347–1363

    Article  CAS  Google Scholar 

  35. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Zakrzewski VG, Montgomery JAJ, Stratmann RE, Burant JC, Dapprich S, Millam JM, Daniels AD, Kudin KN, Strain MC, Farkas O, Tomasi J, Barone V, Cossi M, Cammi R, Mennucci B, Pomelli C, Adamo C, Clifford S, Ochterski J, Petersson GA, Ayala PY, Cui Q, Morokuma K, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Cioslowski J, Ortiz JV, Baboul AG, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Gomperts R, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Andres JL, Gonzalez C, Head-Gordon M, Replogle ES, Pople JA (1998) Gaussian 98, Ed. A.9. Gaussian Inc, Pittsburgh PA

  36. Bertran J, Oliva A, Rodríguez-Santiago L, Sodupe M (1998) J Am Chem Soc 120:8159–8167

    Article  CAS  Google Scholar 

  37. Brameld K, Dasgupta S, Goddard WA III (1997) J Phys Chem B 101:4851–4859

    Article  CAS  Google Scholar 

  38. Gilli G, Bellucci F, Ferretti V, Bertolasi V (1989) J Am Chem Soc 111:1023–1028

    Article  CAS  Google Scholar 

  39. Bertolasi V, Gilli P, Ferretti V, Gilli G (1991) J Am Chem Soc 113:4917–4925

    Article  CAS  Google Scholar 

  40. Steiner T (1998) Chem Commun 411–412

  41. Gilli P, Bertolasi V, Ferretti V, Gilli G (2000) J Am Chem Soc 122:10405–10417

    Article  CAS  Google Scholar 

  42. Munn RW, Eckhardt CJ (2001) J Phys Chem A 105:6938–6942

    Article  CAS  Google Scholar 

  43. Gilli P, Bertolasi V, Pretto L, Ferretti V, Gilli G (2004) J Am Chem Soc 126:3845–3855

    Article  CAS  Google Scholar 

  44. Fiacco DL, Mo Y, Hunt SW, Ott ME, Roberts A, Leopold KR (2000) J Phys Chem A 105:484–493

    Article  CAS  Google Scholar 

  45. Sutor DJ (1962) Nature 195:68–69

    Article  CAS  Google Scholar 

  46. Desiraju GR, Steiner T (2001) The weak hydrogen bond in structural chemistry and biology. Oxford University Press, New York

    Google Scholar 

  47. Meadows ES, De Wall SL, Barbour LJ, Fronczek FR, Kim M-S, Gokel GW (2000) J Am Chem Soc 122:3325–3335

    Article  CAS  Google Scholar 

  48. Senes A, Ubarretxena-Belandia I, Engelman DM (2001) Proc Natl Acad Sci USA 98:9056–9061

    Article  CAS  Google Scholar 

  49. Aravinda S, Shamala N, Bandyopadhyay A, Balaram P (2003) J Am Chem Soc 125:15065–15075

    Article  CAS  Google Scholar 

  50. Manikandan K, Ramakumar S (2004) Proteins 56:768–781

    Article  CAS  Google Scholar 

  51. Petrella RJ, Karplus M (2004). Proteins 54:716–726

    Article  CAS  Google Scholar 

  52. Guo H, Beahm RF, Guo H (2004) J Phys Chem B 108:18065–18072

    Article  CAS  Google Scholar 

  53. Šponer J, Leszczynski J, Hobza P (1996) J Phys Chem 100:1965–1974

    Article  Google Scholar 

  54. Šponer J, Hobza P (1998) In: Schleyer PvR (ed) Encyclopedia of computational chemistry. Wiley, New York, pp 777–789

    Google Scholar 

  55. Saenger W (1984) Principles of nucleic acid structure (and references therein). Springer, Berlin Heidelberg New York, pp 123–124

    Google Scholar 

Download references

Acknowledgement

This work was supported by Western Michigan University.

Author information

Authors and Affiliations

  1. Department of Chemistry, Western Michigan University, Kalamazoo, MI, 49008, USA

    Yirong Mo

Authors
  1. Yirong Mo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yirong Mo.

Additional information

Dedicated to Professor Paul von Ragué Schleyer on the occasion of his 75th birthday

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mo, Y. Probing the nature of hydrogen bonds in DNA base pairs. J Mol Model 12, 665–672 (2006). https://doi.org/10.1007/s00894-005-0021-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00894-005-0021-y

Keywords

Search

Navigation