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Journal of Computer-Aided Molecular Design

, Volume 19, Issue 12, pp 887–901 | Cite as

Modelling of carbohydrate–aromatic interactions: ab initio energetics and force field performance

  • Vojtěch SpiwokEmail author
  • Petra Lipovová
  • Tereza Skálová
  • Eva Vondráčková
  • Jan Dohnálek
  • Jindřich Hašek
  • Blanka Králová
Article
First Online:

Summary

Aromatic amino acid residues are often present in carbohydrate-binding sites of proteins. These binding sites are characterized by a placement of a carbohydrate moiety in a stacking orientation to an aromatic ring. This arrangement is an example of CH/π interactions. Ab initio interaction energies for 20 carbohydrate–aromatic complexes taken from 6 selected ultra-high resolution X-ray structures of glycosidases and carbohydrate-binding proteins were calculated. All interaction energies of a pyranose moiety with a side chain of an aromatic residue were calculated as attractive with interaction energy ranging from −2.8 to −12.3 kcal/mol as calculated at the MP2/6-311+G(d) level. Strong attractive interactions were observed for a wide range of orientations of carbohydrate and aromatic ring as present in selected X-ray structures. The most attractive interaction was associated with apparent combination of CH/π interactions and classical H-bonds. The failure of Hartree–Fock method (interaction energies from +1.0 to −6.9 kcal/mol) can be explained by a dispersion nature of a majority of the studied complexes. We also present a comparison of interaction energies calculated at the MP2 level with those calculated using molecular mechanics force fields (OPLS, GROMOS, CSFF/CHARMM, CHEAT/CHARMM, Glycam/AMBER, MM2 and MM3). For a majority of force fields there was a strong correlation with MP2 values. RMSD between MP2 and force field values were 1.0 for CSFF/CHARMM, 1.2 for Glycam/AMBER, 1.2 for GROMOS, 1.3 for MM3, 1.4 for MM2, 1.5 for OPLS and to 2.3 for CHEAT/CHARMM (in kcal/mol). These results show that molecular mechanics approximates interaction energies very well and support an application of molecular mechanics methods in the area of glycochemistry and glycobiology.

Keywords

ab initio carbohydrate recognition C–H/π interactions force field glycobiology glycosidases lectins 

Abbreviations

AMBER

assisted model building with energy refinement

B3LYP

Becke–Slater-HF 3-term exchange and Lee–Yang–Parr correlation hybrid functional

BSSE

basis set superposition error

CBM

carbohydrate-binding module

CBS

complete basis set

CCSD(T)

coupled cluster with single, double and perturbative triple excitation

CHARMM

chemistry at Harvard molecular mechanics

CHEAT

carbohydrate hydroxyl groups represented by extended atoms

CSFF

carbohydrate solution force field

DFT

density functional theory

GROMOS

Groningen molecular simulation

HF

Hartree–Fock␣method

MM2

molecular mechanics version 2

MM3

molecular mechanics version 3

MP2

Møller–Plesset perturbation theory; second order

OPLS

optimized potentials for liquid simulations

PDB

protein data bank

RMSD

root mean square deviation

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Notes

Acknowledgements

Authors would like to gratefully acknowledge the Czech Science Foundation (GACR 204/02/0843) and the Academy of Sciences of the Czech Republic (projects B500500512 and AVOZ 40500505) for financial support.

References

  1. 1.
    Hobza P., Zahradník R., 1980. Weak Intermolecular Interactions in Chemistry and Biology Elsevier Scientific Pub. Co. Amsterdam, New YorkGoogle Scholar
  2. 2.
    Nishio M., Hirota M., Umezawa Y., 1998. The CH/π Interaction: Evidence, Nature, and Consequences John Wiley & Sons New York Google Scholar
  3. 3.
    Tamres M., (1952) J. Am. Chem. Soc. 74: 3375CrossRefGoogle Scholar
  4. 4.
    Hobza P., Havlas Z., (2000) Chem. Rev. 100: 4253CrossRefPubMedGoogle Scholar
  5. 5.
    Brandl M., Weiss M.S., Jabs A., Sühnel J., Hilgenfeld R., (2001) J. Mol. Biol. 307: 357CrossRefPubMedGoogle Scholar
  6. 6.
    Takahashi O., Kohno Y., Iwasaki S., Saito K., Iwaoka M., Tomoda S., Umezawa Y., Tsuboyama S., Nishio M., (2001) Bull. Chem. Soc. Jpn. 74: 2421CrossRefGoogle Scholar
  7. 7.
    Nishio M., (2004) Cryst. Eng. Comm. 6: 130Google Scholar
  8. 8.
    Tsuzuki S., Honda K., Uchimaru T., Mikami M., Tanabe K., (2000) J. Am. Chem. Soc. 122: 3746CrossRefGoogle Scholar
  9. 9.
    Tarakeshwar P., Choi H.S., Kim K.S., (2001) J. Am. Chem. Soc. 123: 3323PubMedCrossRefGoogle Scholar
  10. 10.
    Bagno A., Saielli G., Scorrano G., (2002) Chem. Eur. J. 8: 2047CrossRefGoogle Scholar
  11. 11.
    Karlstrom G., Linse P., Wallqvist A., Jonssonf B., (1983) J. Am. Chem. Soc. 105: 3717CrossRefGoogle Scholar
  12. 12.
    Hobza P., Selzle H.L., Schlag E.W., (1994) J. Am. Chem. Soc. 116: 3500CrossRefGoogle Scholar
  13. 13.
    Hobza P., Selzle H.L., Schlag E.W., (1996) J. Phys. Chem. 100: 18790CrossRefGoogle Scholar
  14. 14.
    Tsuzuki S., Uchimaru T., Matsumura K., Mikami M., Tanabe K., (2000) Chem. Phys. Lett. 319: 547CrossRefGoogle Scholar
  15. 15.
    Hobza P., Spirko V., Havlas Z., Buchhold K., Reimann B., Barth H.-D., Brutschy B., (1999) Chem. Phys. Lett. 299: 180CrossRefGoogle Scholar
  16. 16.
    Muraki M., (2002) Protein Pept. Lett.9: 195CrossRefPubMedGoogle Scholar
  17. 17.
    Sujatha M.S., Balaji B.V., (2004) Proteins55: 44CrossRefPubMedGoogle Scholar
  18. 18.
    Muraki M., Harata K., (2000) Biochemistry39: 292CrossRefPubMedGoogle Scholar
  19. 19.
    Huber R.E., Hakda S., Cheng C., Cupples C.G., Edwards R.A., (2003) Biochemistry42: 1796CrossRefPubMedGoogle Scholar
  20. 20.
    Zolotnitsky G., Cogan U., Adir N., Solomon V., Shoham G., Shoham Y., (2004) Proc. Natl. Acad. Sci. USA 101: 11275CrossRefPubMedGoogle Scholar
  21. 21.
    Davis A.P., Wareham R.S., (1999) Angew. Chem. Int. Ed. Engl. 38: 2978CrossRefPubMedGoogle Scholar
  22. 22.
    Spiwok V., Lipovová P., Skálová T., Buchtelová E., Hašek J., Králová B., (2004) Carbohydr. Res. 339: 2275CrossRefPubMedGoogle Scholar
  23. 23.
    Sujatha M.S., Sasidhar Y.U., Balaji P.V., (2004) Protein Sci.13: 2502CrossRefPubMedGoogle Scholar
  24. 24.
    Sujatha M.S., Sasidhar Y.U., Balaji P.V., (2005) Biochemistry44: 8554CrossRefPubMedGoogle Scholar
  25. 25.
    del Carmen Fernandez-Alonso M., Cañada F.J., Jiménez-Barbero J., Cuevas G., (2005) J. Am. Chem. Soc. 127: 7379CrossRefPubMedGoogle Scholar
  26. 26.
    Damm W., Frontera A., Tirado-Rives J., Jorgensen W.L., (1997) J. Comp. Chem. 18: 1955CrossRefGoogle Scholar
  27. 27.
    Kuttel M., Brady J.W., Naidoo K.J., (2002) J. Comput. Chem. 23: 1236CrossRefPubMedGoogle Scholar
  28. 28.
    Kouwijzer M.L.C.E., Grootenhuis P.D.J., (1995) J. Phys. Chem. 99: 13426CrossRefGoogle Scholar
  29. 29.
    Woods R.J., Dwek R.A., Edge C.J., Fraser-Reid B., (1995) J. Phys. Chem. 99: 3832CrossRefGoogle Scholar
  30. 30.
    Pérez S., Imberty A., Engelsen S.B., Gruza J., Mazeau K., Jiménez-Barbero J., Poveda A., Espinosa J.-F., van Eyck B.P., Johnson G.J., et al., (1998) Carbohydr. Res. 314: 141CrossRefGoogle Scholar
  31. 31.
    Hemmingsen L., Madsen D.E., Esbensen A.L., Olsen L., Engelsen S.B., (2004) Carbohydr. Res. 339: 937CrossRefPubMedGoogle Scholar
  32. 32.
    Kubinyi, H., In Testa, B., van de Waterbeemd, H., Folkers, G. and Guy, R., (Eds.), Pharmacokinetic Optimization in Drug Research. Biological, Physicochemical, and Computational Strategies, Helvetica Chimica Acta and Wiley-VCH, Zürich, 2001, pp. 513–524Google Scholar
  33. 33.
    Ladbury J.E., (1996) Chem. Biol. 3: 973CrossRefPubMedGoogle Scholar
  34. 34.
    Kellenberger E., Rodrigo J., Muller P., Rognan D., (2004) Proteins57: 225CrossRefPubMedGoogle Scholar
  35. 35.
    Møller C., Plesset M.S., (1934) Phys. Rev. 46: 618CrossRefGoogle Scholar
  36. 36.
    Lütteke T., Frank M., von der Lieth C.W., (2004) Carbohydr. Res. 339: 1015CrossRefPubMedGoogle Scholar
  37. 37.
    Guérin D.M.A., Lascombe M.-B., Costabel M.B., Souchon H., Lamzin V., Béguin P., Alzari P.M., (2002) J. Mol. Biol. 316: 1061CrossRefPubMedGoogle Scholar
  38. 38.
    Sanders D.A.R., Moothoo D.N., Raftery J., Howard A.J., Helliwell J.R., Naismith J.H., (2001) J. Mol. Biol. 310: 875CrossRefPubMedGoogle Scholar
  39. 39.
    Merritt E.A., Kuhn P., Sarfaty S., Erbe J.L., Holmes R.K., Hol W.G.J., (1998) J. Mol. Biol. 282: 1043CrossRefPubMedGoogle Scholar
  40. 40.
    Notenboom V., Boraston A.B., Williams J.S., Kilburn D.G., Rose D.R., (2002) Biochemistry 41: 4246CrossRefPubMedGoogle Scholar
  41. 41.
    Varrot A., Frandsen T.B., von Ossowski I., Boyer V., Cottaz S., Driguez H., Schülein M., Davies G.J., (2003) Structure 11: 855CrossRefPubMedGoogle Scholar
  42. 42.
    Charnock S.J., Bolam D.N., Nurizzo D., Szabó L., McKie V.A., Gilbert H.J., Davies G.J., (2002) Proc. Natl. Acad. Sci. USA 99: 14077CrossRefPubMedGoogle Scholar
  43. 43.
    Schmidt M.W., Baldridge K.K., Boatz J.A., Elbert S.T., Gordon M.S., Jensen J.H., Koseki S., Matsunaga N., Nguyen K.A., Su S., Windus T.L., Dupuis M., Montgomery J.A., (1993) J. Comput. Chem. 14: 1347CrossRefGoogle Scholar
  44. 44.
    Boys S.F., Bernardi F., (1970) Mol. Phys. (UK) 19: 553Google Scholar
  45. 45.
    Jorgensen W.L., Tirado-Rives J., (1988) J. Am. Chem. Soc. 110: 1657CrossRefGoogle Scholar
  46. 46.
    van Gunsteren, W.F., Billeter, S., Eising, A.A., Hübenberger, P.H., Krüger, P., Mark, A.E., Scott, W.R.P. and Tironi, I.G., Biomolecular Simulations: The GROMOS 96 Manual and User Guide VDF Zürich, 1996Google Scholar
  47. 47.
    MacKerell Jr., A.D., Bashford D., Bellott M., Dunbrack Jr. R.L., Evanseck J.D., Field M.J., Fischer S., Gao J., Guo H., Ha S., Joseph-McCarthy D., Kuchnir L., Kuczera K., Lau F.T.K., Mattos C., Michnick S., Ngo T., Nguyen D.T., Prodhom B., Reiher III., W.E., Roux B., Schlenkrich M., Smith J.C., Stote R., Straub J., Watanabe M., Wiorkiewicz-Kuczera J., Yin D., Karplus M., (1998) J. Phys. Chem. B. 102: 3586CrossRefGoogle Scholar
  48. 48.
    Pearlman D.A., Case D.A., Caldwell J.W., Ross W.R., Cheatham T.E., DeBolt III., S., Ferguson D., Seibel G., Kollman P., (1995) Comp. Phys. Commun. 91: 1CrossRefGoogle Scholar
  49. 49.
    Allinger N.L., Kok R.A., Imam M.R., (1988) J. Comput. Chem.9: 591CrossRefGoogle Scholar
  50. 50.
    Lii J.-H., Allinger N.L., (1989) J. Am. Chem. Soc. 111: 8576CrossRefGoogle Scholar
  51. 51.
    Pappu R.V., Hart R.K., Ponder J.W., (1998) J. Phys. Chem. B. 102: 9725CrossRefGoogle Scholar
  52. 52.
    Guex N., Peitsch M.C., (1997) Electrophoresis 18: 2714CrossRefPubMedGoogle Scholar
  53. 53.
    Turnbull W.B., Precious B.L., Homans S.W., (2004) J Am Chem Soc. 126: 1047PubMedCrossRefGoogle Scholar
  54. 54.
    Coutinho, P.M. and Henrissat, B., Carbohydrate-Active Enzymes server, 1999: http://afmb.cnrs-mrs.fr/CAZY/Google Scholar
  55. 55.
    Coutinho, P.M. and Henrissat, B., In Gilbert, H.J., Davies, G., Henrissat, B. and Svensson, B. (Eds.), Recent Advances in Carbohydrate Bioengineering. The Royal Society of Chemistry, Cambridge, 1999, pp. 3–12Google Scholar
  56. 56.
    Johnson E.R., Wolkow R.A., DiLabio G.A., (2004) Chem. Phys. Lett. 394: 334CrossRefGoogle Scholar
  57. 57.
    Grimme S., (2004) J. Comput. Chem. 25: 1463PubMedCrossRefGoogle Scholar
  58. 58.
    Morales J.C., Penadés S., (1998) Angew. Chem. Int. Edit. 37: 654CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Vojtěch Spiwok
    • 1
    Email author
  • Petra Lipovová
    • 1
  • Tereza Skálová
    • 2
  • Eva Vondráčková
    • 2
  • Jan Dohnálek
    • 2
  • Jindřich Hašek
    • 2
  • Blanka Králová
    • 1
  1. 1.Department of BiochemistryInstitute of Chemical Technology in PraguePrague 6Czech Republic
  2. 2.Institute of Macromolecular ChemistryAcademy of Sciences of the Czech RepublicPraha 6Czech Republic

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