300
Views
11
CrossRef citations to date
0
Altmetric
Research Article

Comparing NMR and X-ray protein structure: Lindemann-like parameters and NMR disorder

ORCID Icon, , &
Pages 2331-2341 | Received 25 May 2017, Accepted 30 Jun 2017, Published online: 08 Aug 2017

References

  • Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.
  • Andrec, M., Snyder, D. A., Zhou, Z., Young, J., Montelione, G. T., & Levy, R. M. (2007). A large data set comparison of protein structures determined by crystallography and NMR: Statistical test for structural differences and the effect of crystal packing. Proteins: Structure. Function, and Bioinformatics, 69, 449–465.
  • Aramini, J. M., Sharma, S., Huang, Y. J., Swapna, G. V. T., Ho, C. K., Shetty, K., . . . Jiang, M. (2008). Solution NMR structure of the SOS response protein YNZC from bacillus subtilis. Proteins: Structure. Function, and Bioinformatics, 72, 526–530.
  • Berlow, R. B., Dyson, H. J., & Wright, P. E. (2015). Functional advantages of dynamic protein disorder. FEBS Letters, 589, 2433–2440.
  • Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T., Weissig, H., . . . Bourne, P. E. (2000). The protein data bank. Nucleic Acids Research, 28, 235–242.
  • Billeter, M., Kline, A. D., Braun, W., Huber, R., & Wüthrich, K. (1989). Comparison of the high-resolution structures of the -amylase inhibitor tendamistat determined by nuclear magnetic resonance in solution and by x-ray diffraction in single crystals. Journal of Molecular Biology, 206, 677–687.
  • Blake, P. R., Day, M. W., Hsu, B. T., Joshua-Tor, L., Park, J.-B., Hare, D. R., . . . Summers, M. F., (1992). Comparison of the x-ray structure of native rubredoxin from pyrococcus furiosus with the NMR structure of the zinc-substituted protein. Protein Science, 1, 1522–1525.
  • Braun, W., Vasak, M., Robbins, A., Stout, C., Wagner, G., Kägi, J., & Wüthrich, K. (1992). Comparison of the NMR solution structure and the x-ray crystal structure of rat metallothionein-2. Proceedings of the National Academy of Sciences, 89, 10124–10128.
  • Chakravarty, C., Debenedetti, P. G., & Stillinger, F. H. (2007). Lindemann measures for the solid-liquid phase transition. The Journal of Chemical Physics, 126, 204–508.
  • Chiti, F., & Dobson, C. M. (2006). Protein misfolding, functional amyloid, and human disease. Annual Review Biochemistry, 75, 333–366.
  • Delaglio, F., Kontaxis, G., & Bax, A. (2000). Protein structure determination using molecular fragment replacement and NMR dipolar couplings. Journal of the American Chemical Society, 122, 2142–2143.
  • Dolan, P. T., Roth, A. P., Xue, B., Sun, R., Dunker, A. K., Uversky, V. N., & LaCount, D. J. (2015). Intrinsic disorder mediates hepatitis c virus core-host cell protein interactions. Protein Science, 24, 221–235.
  • Dunker, A. K., Garner, E., Guilliot, S., Romero, P., Albrecht, K., Hart, J., . . . Villafranca, J. E. (1998). Protein disorder and the evolution of molecular recognition: Theory, predictions and observations. Pacific Symposium on Biocomputing, 3, 473–484.
  • Engh, R. A., Dieckmann, T., Bode, W., Auerswald, E. A., Turk, V., Huber, R., & Oschkinat, H. (1993). Conformational variability of chicken cystatin: Comparison of structures determined by x-ray diffraction and NMR spectroscopy. Journal of Molecular Biology, 234, 1060–1069.
  • Everett, J. K., Tejero, R., Murthy, S. B., Acton, T. B., Aramini, J. M., Baran, M. C., . . . Guan, R. (2016). A community resource of experimental data for NMR/x-ray crystal structure pairs. Protein Science, 25, 30–45.
  • Faraggi, E., Zhang, T., Yang, Y., Kurgan, L., & Zhou, Y. (2012). Spine x: Improving protein secondary structure prediction by multistep learning coupled with prediction of solvent accessible surface area and backbone torsion angles. Journal of Computational Chemistry, 33, 259–267.
  • Fraenkel, E., & Pabo, C. O. (1998). Comparison of x-ray and NMR structures for the antennapedia homeodomain-dna complex. Nature Structural & Molecular Biology, 5, 692–697.
  • Gajhede, M., Osmark, P., Poulsen, F. M., Ipsen, H., Larsen, J. N., van Neerven, R. J., & Spangfort, M. D. (1996). X-ray and NMR structure of bet v 1, the origin of birch pollen allergy. Nature Structural & Molecular Biology, 3, 1040–1045.
  • Gallagher, T., Alexander, P., Bryan, P., & Gilliland, G. L. (1994). Two crystal structures of the b1 immunoglobulin-binding domain of streptococcal protein g and comparison with NMR. Biochemistry, 33, 4721–4729.
  • Garbuzynskiy, S. O., Melnik, B. S., Lobanov, M. Y., Finkelstein, A. V., & Galzitskaya, O. V. (2005). Comparison of x-ray and nmr structures: Is there a systematic difference in residue contacts between x-ray-and NMR-resolved protein structures? Proteins: Structure. Function, and Bioinformatics, 60, 139–147.
  • Haliloglu, T., & Bahar, I. (1999). Structure-based analysis of protein dynamics: Comparison of theoretical results for hen lysozyme with x-ray diffraction and NMR relaxation data. Proteins: Structure. Function, and Bioinformatics, 37, 654–667.
  • Haynes, C., Oldfield, C. J., Ji, F., Klitgord, N., Cusick, M. E., Radivojac, P., ... Iakoucheva, L. M. (2006). Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLOS Computational Biology, 2, e100.
  • Iakoucheva, L. M., Brown, C. J., Lawson, J. D., Obradović, Z., & Dunker, A. K. (2002). Intrinsic disorder in cell-signaling and cancer-associated proteins. Journal of Molecular Biology, 323, 573–584.
  • Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577–2637.
  • Kuzin, A. P., Su, M., Seetharaman, J., Janjua, H., Cunningham, K., Maglaqui, M., . . . Acton, T. B. (2008). Crystal structure of upf0291 protein ynzc from bacillus subtilis at resolution 2.0 a. Northeast Structural Genomics Consortium target SR384, 10.
  • Lazar, T., Schad, E., Szabo, B., Horvath, T., Meszaros, A., Tompa, P., & Tantos, A. (2016). Intrinsic protein disorder in histone lysine methylation. Biology Direct, 11, 30.
  • Lindemann, F. (1910). Molecular frequencies phys. Z, 11, 609–612.
  • Lindorff-Larsen, K., Best, R. B., DePristo, M. A., Dobson, C. M., & Vendruscolo, M. (2005). Simultaneous determination of protein structure and dynamics. Nature, 433, 128–132.
  • Martí-Renom, M. A., Stuart, A. C., Fiser, A., Sánchez, R., Melo, F., & Sali, A. (2000). Comparative protein structure modeling of genes and genomes. Annual Review of Biophysics and Biomolecular Structure, 29, 291–325.
  • Massiah, M. A., Worthylake, D., Christensen, A. M., Sundquist, W. I., Hill, C. P., & Summers, M. F. (1996). Comparison of the NMR and x-ray structures of the hiv-1 matrix protein: Evidence for conformational changes during viral assembly. Protein Science, 5, 2391–2398.
  • Meyer, T. J. (2008). Catalysis: The art of splitting water. Nature, 451, 778–779.
  • Mittag, T., Marzahn, M., Lee, J., Palud, A., Marada, S., Nourse, A., ... Ogden, S. (2015). The role of protein disorder and self-association in the formation of cellular bodies. The FASEB Journal, 29, 109–112.
  • Muchmore, S. W., Sattler, M., Liang, H., Meadows, R. P., Harlan, J. E., Yoon, H. S., . . . Ng, S. C. (1996). X-ray and NMR structure of human bcl-xl, an inhibitor of programmed cell death. Nature, 381, 335–341.
  • Oldfield, C. J., & Dunker, A. K. (2014). Intrinsically disordered proteins and intrinsically disordered protein regions. Annual Review of Biochemistry, 83, 553–584.
  • Parish, D., Benach, J., Liu, G., Singarapu, K. K., Xiao, R., Acton, T., . . . Montelione, G. T. (2008). Protein chaperones q8zp25 salty from salmonella typhimurium and hyae ecoli from escherichia coli exhibit thioredoxin-like structures despite lack of canonical thioredoxin active site sequence motif. Journal of Structural and Functional Genomics, 9, 41.
  • Phelan, M. M., McLean, L., Simpson, D. M., Hurst, J. L., Beynon, R. J., & Lian, L.-Y. (2010). 1h, 15n and 13c resonance assignment of darcin, a mouse major urinary protein. Biomolecular NMR Assignments, 4, 239–241.
  • Philippopoulos, M., & Lim, C. (1999). Exploring the dynamic information content of a protein NMR structure: Comparison of a molecular dynamics simulation with the NMR and x-ray structures of Escherichia coli ribonuclease hi. Proteins: Structure. Function, and Bioinformatics, 36, 87–110.
  • Romero, P. R., Zaidi, S., Fang, Y. Y., Uversky, V. N., Radivojac, P., Oldfield, C. J., . . . Dunker, A. K. (2006). Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proceedings of the National Academy of Sciences, 103, 8390–8395.
  • Schrödinger, L. L. C. (2015). The PyMOL molecular graphics system. Retrieved from http://pymol.org
  • Shapiro, J. N. (1970). Lindemann law and lattice dynamics. Physical Review B, 1, 3982.
  • Siew, N., Elofsson, A., Rychlewski, L., & Fischer, D. (2000). Maxsub: An automated measure for the assessment of protein structure prediction quality. Bioinformatics, 16, 776–785.
  • Timm, D. E., Baker, L., Mueller, H., Zidek, L., & Novotny, M. V. (2001). Structural basis of pheromone binding to mouse major urinary protein (mup-i). Protein Science, 10, 997–1004.
  • Uversky, V. N. (2013). A decade and a half of protein intrinsic disorder: Biology still waits for physics. Protein Science, 22, 693–724.
  • Varpness, Z., Peters, J., Young, M., & Douglas, T. (2005). Biomimetic synthesis of a h2 catalyst using a protein cage architecture. Nano Letters, 5, 2306–2309.
  • Vetsch, M., Puorger, C., Spirig, T., Grauschopf, U., Weber-Ban, E. U., & Glockshuber, R. (2004). Pilus chaperones represent a new type of protein-folding catalyst. Nature, 431, 329–333.
  • Wagner, G., Hyberts, S. G., & Havel, T. F. (1992). Nmr structure determination in solution: A critique and comparison with x-ray crystallography. Annual Review of Biophysics and Biomolecular Structure, 21, 167–198.
  • Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F., & Jones, D. T. (2004). Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. Journal of Molecular Biology, 337, 635–645.
  • Wright, P. E., & Dyson, H. J. (1999). Intrinsically unstructured proteins: Re-assessing the protein structure-function paradigm. Journal of Molecular Biology, 293, 321–331.
  • Xu, J., & Zhang, Y. (2010). How significant is a protein structure similarity with tm-score = 0.5? Bioinformatics, 26, 889–895.
  • Yan, J., Dunker, A. K., Uversky, V. N., & Kurgan, L. (2016). Molecular recognition features (morfs) in three domains of life. Molecular BioSystems, 12, 697–710.
  • Yang, L.-W., Eyal, E., Chennubhotla, C., Jee, J., Gronenborn, A. M., & Bahar, I. (2007). Insights into equilibrium dynamics of proteins from comparison of NMR and x-ray data with computational predictions. Structure, 15, 741–749.
  • Zahn, K., Lenke, R., & Maret, G. (1999). Two-stage melting of paramagnetic colloidal crystals in two dimensions. Physical Review Letters, 82, 2721.
  • Zemla, A., Venclovas, A., Moult, J., & Fidelis, K. (1999). Processing and analysis of casp3 protein structure predictions. Proteins: Structure. Function, and Bioinformatics, 37, 22–29.
  • Zhang, T., Faraggi, E., Xue, B., Dunker, A. K., Uversky, V. N., & Zhou, Y. (2012). Spine-d: Accurate prediction of short and long disordered regions by a single neural-network based method. Journal of Biomolecular Structure and Dynamics, 29, 799–813.
  • Zhang, T., Faraggi, E., & Zhou, Y. (2010). Fluctuations of backbone torsion angles obtained from NMR-determined structures and their prediction. Proteins: Structure. Function, and Bioinformatics, 78, 3353–3362.
  • Zhang, Y., & Skolnick, J. (2004). Scoring function for automated assessment of protein structure template quality. Proteins: Structure. Function, and Bioinformatics, 57, 702–710.
  • Zhou, Y., Vitkup, D., & Karplus, M. (1999). Native proteins are surface-molten solids: Application of the lindemann criterion for the solid versus liquid state. Journal of Molecular Biology, 285, 1371–1375.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.