Protein Structure Calculation from NMR Data

  • Tapas K. Mal
  • Stefan Bagby
  • Mitsuhiko Ikura
Part of the Methods in Molecular Biology™ book series (MIMB, volume 173)

Abstract

Until 1984, structural information of biomolecules at atomic resolution could only be determined by X-ray diffraction techniques with protein single crystals (1). In the mid-1980s, Wüthrich and co-workers demonstrated that nuclear magnetic resonance (NMR) spectroscopy (2) could be used as a technique for protein structure determination (3). This permits biomolecular structure determination

References

  1. 1.
    Drenth, J. (1994) Principles of Protein X-ray Crystallography. Springer, New York.Google Scholar
  2. 2.
    Abragam, A. (1961) Principles of Nuclear Magnetism. Clarendon, Oxford.Google Scholar
  3. 3.
    Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids. Wiley, New York.Google Scholar
  4. 4.
    Arseniev, A. S., Kondakov, V. I., Maiorov, V. N., and Bystrov, V. F. and Ovchinnikov, I. A. (1983) Conformation NMR Annalysis of the spatial structure of Butkus eupeus insectotoxin 15A. Bioeng. Rhim. 9, 1667–1689.Google Scholar
  5. 5.
    Braun, W., Bosch, C., Brown, L. R., Gö, N., and Wüthrich, K. (1981) Combined use of proton-proton Overhauser enhancements and a distance geometry algorithm for determination of polypeptide conformations. Application to micelle-bound glucagon. Biochim. Biophys. Acta 667, 377–396.PubMedGoogle Scholar
  6. 6.
    Clore, G. M., Brünger, A. T., Karplus, M., and Gronenborn, A. M. (1986) Application of molecular dynamics with interproton distance restraints to three dimensional protein structure determination: a model study of crambin. J. Mol. Biol. 191, 523–551.PubMedCrossRefGoogle Scholar
  7. 7.
    Williamson, M. P., Havel, T. F., and Wüthrich, K. (1985) Solution conformation of proteinase inhibitor IIa from bull seminal plasma by 1H nuclear magnetic resonance and distance geometry. J. Mol. Biol. 182, 295–315.PubMedCrossRefGoogle Scholar
  8. 8.
    Zuiderweg, E. R. P., Billeter, M., Boelens, R., Scheek, R. M., Wüthrich, K., and Kaptein, R. (1984) Spatial arrangement of the three a helices in a solution structure of E. coli lac repressor DNA-binding domain. FEBS Lett. 174, 243–247.PubMedCrossRefGoogle Scholar
  9. 9.
    Havel, T. F. and Wüthrich, K. (1984) A distance geometry program for determining the structures of small proteins and other macromolecules from nuclear magnetic resonance measurements of intramolecular 1H-1H proximities in solution. Bull. Math. Biol. 46, 673–698.Google Scholar
  10. 10.
    Braun, W. and Gö, N. (1985) Calculation of protein conformation by proton-proton distance constraints: a new efficient algorithm. J. Mol. Biol. 186, 611–626.PubMedCrossRefGoogle Scholar
  11. 11.
    Brünger, A. T. (1992) X-PLOR, Version 3. 1. A System for X-Ray Crystallography and NMR. Yale University Press, New Haven, Connecticut.Google Scholar
  12. 12.
    Nilges, M. (1995) Calculation of protein structures with ambiguous distance restraints. Automated assignment of ambiguous NOE crosspeaks and disulphide connectivities. J. Mol. Biol. 245, 645–660.PubMedCrossRefGoogle Scholar
  13. 13.
    Nilges, M., Macias, M., O’Donoghue, S. I., and Oschkinat, H. (1997) Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from β spectrin. J. Mol. Biol. 269, 408–422.PubMedCrossRefGoogle Scholar
  14. 14.
    Güntert, P., Mumenthaler, C., and Wüthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273. 283–298.PubMedCrossRefGoogle Scholar
  15. 15.
    Güntert, P. (1998) Structure calculation of biological macromolecules from NMR data. Quart. Rev. Biophys. 31, 145–237.CrossRefGoogle Scholar
  16. 16.
    Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., Di Nola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684–3690.CrossRefGoogle Scholar
  17. 17.
    Laskowski, R. A., Ruilmay, J. A. C., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477–486.PubMedCrossRefGoogle Scholar
  18. 18.
    Vriend, G. and Sander, C. (1993) Quality control of protein models: directional atomic contact analysis. J. Appl. Crystallogr. 26, 47–60.CrossRefGoogle Scholar
  19. 19.
    Kuszewski, J, Qin, J., Gronenborn, A. M., and Clore, G. M. (1995) The impact of direct refinement against 13Cαand 13Cβ chemical shifts on protein structure determination by NMR. J. Magn. Reson. Ser. B 106, 92–96.CrossRefGoogle Scholar
  20. 20.
    Kuszewski, J., Gronenborn, A. M., and Clore, G. M. (1995) The impact of direct refinement against proton chemical shifts on protein structure determination by NMR. J. Magn. Reson. Ser. B 107, 293–297.CrossRefGoogle Scholar
  21. 21.
    Kuszewski, J., Gronenborn, A. M., and Clore, G. M. (1996) A potential involving multiple proton chemical shift restraints for nonstereospecifically assigned methyl and methylene protons. J. Magn. Reson. Ser. B 112, 79–81.CrossRefGoogle Scholar
  22. 22.
    Brüschweiler, R., Liao, X., and Wright, P. E. (1995) Long-range motional restrictions in a multidomain zinc-finger protein from anisotropic tumbling. Science 268, 886–889.PubMedCrossRefGoogle Scholar
  23. 23.
    Tjandra, N., Omichinski, J. G., Gronenborn, A. M., Clore, G. M., and Bax, A. (1997) Use of dipolar 1H-15N and 1H-13C couplings in the structure determination of magnetically oriented macromolecules in solution. Nat. Struct. Biol. 4, 732–738.PubMedCrossRefGoogle Scholar
  24. 24.
    Clore, G. M. and Gronenborn, A. M. (1998) Determining the structures of large proteins and protein complexes by NMR. Trends Biotechnol. 16, 22–34.PubMedCrossRefGoogle Scholar
  25. 25.
    Güntert, P., Berndt, K. D., and Wüthrich, K. (1993) The program ASNO for computer-supported collection of NOE upper distance restraints as input for protein structure determination. J. Biol. NMR 3, 601–606.Google Scholar
  26. 26.
    Nilges, M., Gronenborn, A. M., Brünger, A. T., and Clore, G. M. (1988) Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor 2. Protein Eng. 2, 27–38.PubMedCrossRefGoogle Scholar
  27. 27.
    Hanggi, G. and Braun, W. (1994) Pattern recognition and self-correcting distance geometry calculations applied to myohemerythrin. FEBS Lett. 344, 147–153.PubMedCrossRefGoogle Scholar
  28. 28.
    Folmer, R. H. A., Nilges, M., Papavoine, C. H. M., Harmsen, B. J. M., Konings, R. N. H., and Hilbers, C. W. (1997) Refined structure, DNA binding studies, and dynamics of the bacteriophage Pf3 encoded single-stranded DNA binding protein. Biochemistry 36, 9120–9135.PubMedCrossRefGoogle Scholar
  29. 29.
    Abe, H., Braun, W., Noguti, T., and Gö, N. (1984) Rapid calculation of first and second derivatives of conformational energy with respect to dihedral angles in proteins. General recurrent equations. Comput. Chem. 8, 239–247.CrossRefGoogle Scholar
  30. 30.
    Solomon, I. (1955) Relaxation processes in a system of two spins. Phys. Rev. 99, 559–565.CrossRefGoogle Scholar
  31. 31.
    Macura, S. and Ernst, R. R. (1980) Elucidation of cross relaxation in liquids by 2D NMR spectroscopy. Mol. Phys. 41, 95–117.CrossRefGoogle Scholar
  32. 32.
    Neuhaus, D. and Williamson, M. P. (1989) The Nuclear Overhauser Effect in Structural and Conformational Analysis. VCH, New York.Google Scholar
  33. 33.
    Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546–4553.CrossRefGoogle Scholar
  34. 34.
    Kumar, A., Ernst, R. R., and Wüthrich, K. (1980) A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem. Biophys. Res. Commun. 95, 1–6.PubMedCrossRefGoogle Scholar
  35. 35.
    Ernst, R. R., Bodenhausen, G., and Wokaun, A. (1987) The Principles of Nuclear Magnetic Resonance in One and Two Dimensions. Clarendon, Oxford.Google Scholar
  36. 36.
    Billeter, M., Braun, W., and Wüthrich, K. (1982) Sequential resonance assignments in protein 1H nuclear magnetic resonance spectra. Computation of sterically allowed proton-proton distances and statistical analysis of proton-proton distances in single crystal protein conformations. J. Mol. Biol. 155, 321–346.PubMedCrossRefGoogle Scholar
  37. 37.
    Güntert, P., Qian, Y. Q., Otting, G., Muller, M., Gehring, W. J., and Wüthrich, K. (1991) Structure determination of the Antp(C39?S) homeodomain from nuclear magnetic resonance data in solution using a novel strategy for the structure calculation with the programs DIANA, CALIBA, HABAS and GLOMSA. J. Mol. Biol. 217, 531–540.PubMedCrossRefGoogle Scholar
  38. 38.
    Clore, G. M., Nilges, M., Sukumaran, D. K., Brünger, A. T., Karplus, M., and Gronenborn, A. M. (1986) The three-dimensional structure of α-purothionin in solution: combined use of nuclear magnetic resonance, distance geometry and restrainted molecular dynamics. EMBO J. 5, 2729–2735.PubMedGoogle Scholar
  39. 39.
    Borgias, B. A. and James, T. L. (1989) Two-dimensional nuclear Overhauser effect: complete relaxation matrix analysis. Methods Enzymol. 176, 169–183.PubMedCrossRefGoogle Scholar
  40. 40.
    Bonvin, A. M., Rullmann, J. A., Lamerichs, R. M., Boelens, R., and Kaptein, R. (1993) Ensemble iterative relaxation matrix approach: a new NMR refinement protocol applied to the solution structure of Crambin. Proteins 15, 385–400.PubMedCrossRefGoogle Scholar
  41. 41.
    Wüthrich, K., Billeter, M., and Braun, W. (1983) Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurements of intramolecular proton-proton distance restraints with nuclear magnetic resonance. J. Mol. Biol. 169, 949–961.PubMedCrossRefGoogle Scholar
  42. 42.
    Markley, J. L., Bax, A., Arata, Y., Hilbers, C. W., Kaptein, R., Sykes, B. D., et al. (1998) Recommendation for the presentation of NMR structures of proteins and nucleic acids. PureAppl. Chem. 70, 117–142.CrossRefGoogle Scholar
  43. 43.
    Babu, Y. S., Sack, J. S., Greenhough, J. J., Bugg, C. E., Means, A. R., and Cook, W. J. (1985) Three-dimensional structure of calmodulin. Nature 315, 37–40.PubMedCrossRefGoogle Scholar
  44. 44.
    Wylie, D. C. and Vanaman, T. C. (1988) Structure and evolution of the calmodulin family of calcium regulatory protein, in Calmodulin (Cohen, P. and Klee, C. B., eds.), ELSEVIER Science Publishers, Amsterdam, pp. 1–15.Google Scholar
  45. 45.
    Ikura, M., Clore, G. M., Gronenborn, A. M., Zhu, G., Klee, C. B., and Bax, A. (1992) Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256, 632–638.PubMedCrossRefGoogle Scholar
  46. 46.
    Karplus, M. (1963) Vicinal proton coupling in nuclear magnetic resonance. J. Am. Chem.Soc. 85, 2870–2871.CrossRefGoogle Scholar
  47. 47.
    Wang, A. C. and Bax, A. (1996) Determination of the backbone dihedral angles ϕ in human ubiquitin from reparametrized empirical Karplus equations. J. Am. Chem. Soc. 118, 2483–2494.CrossRefGoogle Scholar
  48. 48.
    Wang, A. C. and Bax, A. (1995) Reparametrization of the Karplus relation for 3J(Hα-N) in peptides from uniformly 13C/15N enriched human ubiquitin. J. Am. Chem. Soc. 117, 1810–1813.CrossRefGoogle Scholar
  49. 49.
    De Marco, A. C., Llinas, M., and Wüthrich, K. (1978) Analysis of the 1H-NMR spectra of ferrichrome peptides. I. The non-amide protons. Biopolymers 17, 617–636.CrossRefGoogle Scholar
  50. 50.
    De Marco, A. C., Llinas, M., and Wüthrich, K. (1978) 1H-15N spin-spin couplings in alumichrome. Biopolymers 17, 2727–2742.CrossRefGoogle Scholar
  51. 51.
    Fischman, A. J., Live, D. H., Wyssbrod, H. R., Agosta, W. C., and Cowburn, D. (1980) Torsion angles in the cystine bridge of oxytocin in aqueous solution. Measurements of circumjacent vicinal couplings between 1H, 13C, and 15N. J. Am. Chem. Soc. 102, 2533–2539.CrossRefGoogle Scholar
  52. 52.
    Wishart, D. S. and Nip, A. M. (1998) Protein chemical shift analysis: a practical guide. Biochem. Cell Biol. 76, 153–163.PubMedCrossRefGoogle Scholar
  53. 53.
    Venters, R. A., FarmerII, B. T., Fierke, C. A., and Spicer, L. D. (1996) Characterizing the use of perdeuteration in NMR studies of large proteins: 13C, 15N and 1H assignments of human carbonic anhydrase II. J. Mol. Biol. 264, 1101–1116.PubMedCrossRefGoogle Scholar
  54. 54.
    Wishart, D. S. and Sykes, B. D. (1994) Chemical shifts as a tool for structure determination. Methods Enzymol. 239, 363–392.PubMedCrossRefGoogle Scholar
  55. 55.
    Metzler, W. J., Constantine, K. L., Friedrichs, M. S., Bell, A. J., and Ernst, E. G. (1993) Characterization of the three-dimensional solution structure of human profilin: 1H, 13C and 15N assignments and global folding pattern. Biochemistry 32, 13,818–13,829.PubMedCrossRefGoogle Scholar
  56. 56.
    Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biolmol. NMR 13, 289–302.CrossRefGoogle Scholar

Copyright information

© Humana Press Inc. 2002

Authors and Affiliations

  • Tapas K. Mal
    • 1
  • Stefan Bagby
    • 1
  • Mitsuhiko Ikura
    • 2
  1. 1.Department of Medical BiophysicsOntario Cancer Institute, University of TorontoTorontoCanada
  2. 2.Division of Medical and Structural Biology, Department of Medical BiophysicsOntario Cancer Institute, University of TorontoTorontoCanada

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