A test of enhancing model accuracy in high-throughput crystallography

  • W. Bryan ArendallIII
  • Wolfram Tempel
  • Jane S. Richardson
  • Weihong Zhou
  • Shuren Wang
  • Ian W. Davis
  • Zhi-Jie Liu
  • John P. Rose
  • W. Michael Carson
  • Ming Luo
  • David C. Richardson
  • Bi-Cheng Wang
Article

Abstract

The high throughput of structure determination pipelines relies on increased automation and, consequently, a reduction of time spent on interactive quality control. In order to meet and exceed current standards in model accuracy, new approaches are needed for the facile identification and correction of model errors during refinement. One such approach is provided by the validation and structure-improvement tools of the MOLPROBITY web service. To test their effectiveness in high-throughput mode, a large subset of the crystal structures from the SouthEast Collaboratory for Structural Genomics (SECSG) has used protocols based on the MOLPROBITY tools. Comparison of 29 working-set and 19 control-set SECSG structures shows that working-set outlier scores for updated Ramachandran-plot, sidechain rotamer, and all-atom steric criteria have been improved by factors of 5- to 10-fold (relative to the control set or to a Protein Data Bank sample), while quality of covalent geometry, Rwork, Rfree, electron density and difference density are maintained or improved. Some parts of this correction process are already fully automated; other parts involve manual rebuilding of conformations flagged by the tests as trapped in the wrong local minimum, often altering features of functional significance. The ease and effectiveness of this technique shows that macromolecular crystal structures from either traditional or high-throughput determinations can feasibly reach a new level of excellence in conformational accuracy and reliability.

Keywords:

all-atom contacts MOLPROBITY Ramachandran plot sidechain rotamers structural genomics structure validation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Mowbray, S.L., Helgstrand, C., Sigrell, J.A., Cameron, A.D., Jones, T.A. 1999Acta Cryst. D5513091319CrossRefGoogle Scholar
  2. 2.
    Kleywegt, G.J. 1999Acta Cryst. D5518781884CrossRefGoogle Scholar
  3. 3.
    Laskowski, R.A., MacArthur, M.W., Moss, D.S., Thornton, J.M. 1993J. Appl. Crystallogr.26283291CrossRefGoogle Scholar
  4. 4.
    Vriend, G. 1990J. Mol. Graph.85256CrossRefPubMedGoogle Scholar
  5. 5.
    Jones, T.A., Zou, J.-Y., Cowan, S.W., Kjeldgaard, M. 1991Acta Cryst. A47110119CrossRefGoogle Scholar
  6. 6.
    Lovell, S.C., Davis, I.W., Arendall, W.B.,III, Bakker, P.I.W., Word, J.M., Prisant, M.G., Richardson, J.S., Richardson, D.C. 2003Proteins50437450CrossRefPubMedGoogle Scholar
  7. 7.
    Davis, I.W., Murray, L.W., Richardson, J.S., Richardson, D.C. 2004Nucleic Acids Res.32W615W619PubMedGoogle Scholar
  8. 8.
    Vaguine, A.A., Richelle, J., Wodak, S.J. 1999Acta Cryst. D55191205CrossRefGoogle Scholar
  9. 9.
    Kleywegt, G.J., Harris, M.R., Zou, J.Y., Taylor, T.C., Wahlby, A., Jones, T.A. 2004Acta Cryst. D6022402249CrossRefGoogle Scholar
  10. 10.
    Akker, F., Hol, W.G.J. 1999Acta Cryst. D55206218CrossRefGoogle Scholar
  11. 11.
    Brunger, A.T. 1992Nature355472475CrossRefGoogle Scholar
  12. 12.
    Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E. 2000Nucleic Acids Res.28235242CrossRefPubMedGoogle Scholar
  13. 13.
    Norvell, J.C., Machalek, A.Z. 2000Nat. Struct. Biol.7931CrossRefPubMedGoogle Scholar
  14. 14.
    Dauter, Z. 2002Acta Cryst D5819581967CrossRefGoogle Scholar
  15. 15.
    Fu, Z.-Q., Rose, J.P., Wang, B.-C. 2004Acta Cryst. D60499506CrossRefGoogle Scholar
  16. 16.
    Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.-W., Ioerger, T.R., McCoy, A.J., Moriarty, N.W., Read, R.J., Sacchettini, J.C., Sauter, N.K., Terwilliger, T.C. 2002Acta Cryst. D5819481954CrossRefGoogle Scholar
  17. 17.
    Badger, J., Hendle, J. 2002Acta Cryst. D58284291CrossRefGoogle Scholar
  18. 18.
    Lesley, S.A., Kuhn, P., Godzik, A., Deacon, A.M., Mathews, I., Kreusch, A., Spraggon, G., Klock, H.E., McMullan, D., Shin, T., Vincent, J., Robb, A., Brinen, L.S., Miller, M.D., McPhillips, T.M., Miller, M.A., Scheibe, D., Canaves, J.M., Guda, C., Jaroszewski, L., Selby, T.L., Elsliger, M.-A., Wooley, J., Taylor, S.S., Hodgson, K.O., Wilson, I.A., Schultz, P.G., Stevens, R.C. 2002Proc. Natl. Acad. Sci. USA991166411669CrossRefPubMedGoogle Scholar
  19. 19.
    Montelione, G.T., Zheng, D., Huang, Y.J., Gunsalus, K.C., Szyperski, T. 2000Nat. Struct. Biol.7982985CrossRefPubMedGoogle Scholar
  20. 20.
    Huang, Y.J., Powers, R. and Montelione, G.T. (2005) J. Am. Chem. Soc., 127, 1665–1674Google Scholar
  21. 21.
    Adams, M.W.W., Dailey, H.A., Delucas, L.J., Luo, M., Prestegard, J.H., Rose, J.P., Wang, B.-C. 2003Acc. Chem. Res.36191198CrossRefPubMedGoogle Scholar
  22. 22.
    Terwilliger, T.C., Berendzen, J. 1999Acta Cryst. D55849861CrossRefGoogle Scholar
  23. 23.
    Schneider, T.R., Sheldrick, G.M. 2002Acta Cryst. D5817721779CrossRefGoogle Scholar
  24. 24.
    Wang, B.-C. 1985Methods Enzymol.11590112PubMedGoogle Scholar
  25. 25.
    Collaborative Computational Project, No. 4 1994Acta Cryst. D50760763CrossRefGoogle Scholar
  26. 26.
    Terwilliger, T.C. 2002Acta Cryst. D5819371940CrossRefGoogle Scholar
  27. 27.
    Perrakis, A., Morris, R., Lamzin, V.S. 1999Nat. Struct. Biol.6458463CrossRefPubMedGoogle Scholar
  28. 28.
    Murshudov, G.N., Vagin, A.A., Dodson, E.J. 1997Acta Cryst. D53240255CrossRefGoogle Scholar
  29. 29.
    Potterton, E., Briggs, P., Turkenburg, M., Dodson, E.J. 2003Acta Cryst. D5911311137CrossRefGoogle Scholar
  30. 30.
    Winn, M.D. 2003J. Synchron. Rad.102325CrossRefGoogle Scholar
  31. 31.
    Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N.S., Read, R.J., Rice, L.M., Simonson, T., Warren, G.L. 1998Acta Cryst. D54905921CrossRefGoogle Scholar
  32. 32.
    McRee, D.E. 1999J. Struct. Biol.125156165CrossRefPubMedGoogle Scholar
  33. 33.
    Richardson, J.S., Arendall, W.B.,III, Richardson, D.C. 2003Carter, C.W.,Jr.Sweet, R.M. eds. Methods in Enzymology: Macromolecular Crystallography, Pt. DAcademic PressNew York385412Google Scholar
  34. 34.
    Lovell, S.C., Word, J.M., Richardson, J.S., Richardson, D.C. 2000Proteins40389408CrossRefPubMedGoogle Scholar
  35. 35.
    Word, J.M., Lovell, S.C., Richardson, J.S., Richardson, D.C. 1999J. Mol. Biol.28517351747CrossRefPubMedGoogle Scholar
  36. 36.
    Word, J.M., Lovell, S.C., LaBean, T.H., Taylor, H.C., Zalis, M.E., Presley, B.K., Richardson, J.S., Richardson, D.C. 1999J. Mol. Biol.28517111733CrossRefPubMedGoogle Scholar
  37. 37.
    Richardson, J.S. 2003Bourne, P.E.Weissig, H. eds. Structural BioinformaticsJohn Wiley & Sons, Inc.New York305320Google Scholar
  38. 38.
    Word, J.M., Bateman, R.C.,Jr., Presley, B.K., Lovell, S.C., Richardson, D.C. 2000Protein Sci.922512259PubMedGoogle Scholar
  39. 39.
    Sack, J.S. 1988J. Mol. Graph.6224225CrossRefGoogle Scholar
  40. 40.
    Murzin, A., Brenner, S.E., Hubband, T., Chothia, C. 1995J. Mol. Biol.247536540CrossRefPubMedGoogle Scholar
  41. 41.
    Butterfoss, G., Richardson, J.S., Hermans, J. 2005Acta Cryst. D618898CrossRefGoogle Scholar
  42. 42.
    Higman, V.A., Boyd, J., Smith, L.J., Redfield, C. 2004J. Biomol. NMR30327346CrossRefPubMedGoogle Scholar
  43. 43.
    Kleywegt, G.J., Jones, T.A. 1996Structure413951400CrossRefPubMedGoogle Scholar
  44. 44.
    Videau, L.L., Arendall, W.B.,III, Richardson, J.S. 2004Proteins56298309CrossRefPubMedGoogle Scholar
  45. 45.
    Richardson, J.S., Richardson, D.C. 2003Wang, J.T.L.Wu, C.H.Wang, P.P. eds. Computational Biology and Genome InformaticsWorld Scientific Publishing CompanyLondon139161Google Scholar
  46. 46.
    Hu, H., Elstner, M., Hermans, J. 2003Proteins50451463CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • W. Bryan ArendallIII
    • 1
  • Wolfram Tempel
    • 2
  • Jane S. Richardson
    • 1
  • Weihong Zhou
    • 2
  • Shuren Wang
    • 1
    • 4
  • Ian W. Davis
    • 1
  • Zhi-Jie Liu
    • 2
  • John P. Rose
    • 2
  • W. Michael Carson
    • 3
  • Ming Luo
    • 3
  • David C. Richardson
    • 1
  • Bi-Cheng Wang
    • 2
  1. 1.Department of BiochemistryDuke University Medical CenterDurhamUSA
  2. 2.Department of Biochemistry and Molecular BiologyUniversity of GeorgiaAthensUSA
  3. 3.Center for Biophysical Sciences and EngineeringUniversity of Alabama at BirminghamBirminghamUSA
  4. 4.Department of Molecular Physiology and Biological PhysicsUniversity of VirginiaCharlottesvilleUSA

Personalised recommendations