Hostname: page-component-5c6d5d7d68-thh2z Total loading time: 0 Render date: 2024-08-14T17:56:07.489Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparison of protein structures determined by NMR in solution and by X-ray diffraction in single crystals

Published online by Cambridge University Press:  17 March 2009

Martin Billeter
Martin Billeter
Affiliation:
Institut für Molekularbiologie und Biophysik, Eidgenösische Technische Hochschule-Hönggerberg CH-8093 Zürich, Switzerland
Get access Rights & Permissions [Opens in a new window]

Extract

Following the first determinations of protein structures in the late 1950s and the early 1960s (see for example Kendrew et al. 1960; Perutz, 1964), the three-dimensional structures of several hundred proteins have been elucidated by X-ray diffraction on single crystals. By the end of 1991, approximately 150 entries of proteins with substantially different sequences and a well resolved structure (Hobohm et al. 1992) were deposited in the Protein Data Bank (Bernstein et al. 1977; Abola et al. 1987). In addition, many structures of homologous proteins or of mutants have been described, bringing the total number of entries to about 600. While it was soon accepted that almost all of these structures do indeed give a correct picture of the fold of the active protein in spite of the non-physiological environment of single crystals, it is not clear to what extent structural details are reliably described by these structures. In particular the surface of a protein may be modified due to the dense packing of protein molecules in the crystal lattice. A detailed knowledge of the protein surface is, however, essential for the understanding of the function of the protein.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 25 , Issue 3 , August 1992 , pp. 325 - 377
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abola, E. E., Bernstein, F. C., Bryant, S. H., Koetzle, T. F. & Weng, J. (1987). Protein Data Bank, in: Crystallographic Databases–Information Content, Software Systems, Scientific Applications (ed. Allen, F. H., Bergerhoff, G. and Sievers, R.), Data Commission of the International Union of Crystallography, Bonn/Cambridge/Chester, pp. 107–132.Google Scholar
Aggarwal, A. K., Rodgers, D. W., Drottar, M., Ptashne, M. & Harrison, S. C. (1988). Recognition of a DNA operator by the repressor of phage 434: a view at high resolution. Science, N. Y. 242, 899–907.CrossRefGoogle ScholarPubMed
Anderson, J., Ptashne, M. & Harrison, S. C. (1987). Structure of the repressor-operator complex of bacteriophage 434. Nature, Lond. 326, 846–852.CrossRefGoogle ScholarPubMed
Arseniev, A., Schultze, P., Wörgötter, E., Braun, W., Wagner, G., Vasäk, M., Kägi, J. H. R. & Wüthrich, K. (1988). Three-dimensional structure of rabbit liver [Cd7]metallothionein-2a in aqueous solution determined by nuclear magnetic resonance. J. molec. Biol. 201, 637–657.CrossRefGoogle ScholarPubMed
Baldwin, E. T., Weber, I. T., Charles, R. St., Xuan, J.-C., Appella, E., Yamada, M., Matsushima, K., Edwards, B. F. P., Clore, G. M., Gronenborn, A. M. & Wlodawer, A. (1991). Crystal structure of interleukin-8: Symbiosis of NMR and crystallography. Proc. natn. Acad. Sci. U.S.A. 88, 502–506.CrossRefGoogle ScholarPubMed
Banner, D. W., Kokkinidis, M. & Tsernoglou, D. (1987). Structure of the ColE1 Rop protein at 1·7 Å resolution, J. molec. Biol. 196, 657–675.CrossRefGoogle ScholarPubMed
Berndt, K. D., Güntert, P., Orbons, L. P. M. & Wünthrich, K. (1992). Determination of a high-quality NMR solution structure of the bovine pancreatic trypsin inhibitor (BPTI) and comparison with three crystal structures. J. molec. Biol. (In the press).Google Scholar
Bernstein, F. C., Koetzle, T. F., Williams, G. J. B., Meyer, E. F. Jr., Brice, M. D., Rodgers, J. R., Kennard, O., Shimamouchi, T. & Tasumi, M. (1977). The Protein Data Bank: A computer-based archival file for macromolecular structures. J. molec. Biol. 112, 535–542.CrossRefGoogle Scholar
Billeter, M., Kline, A. D., Braun, W., Huber, R. & Wüthrich, K. (1989). Comparison of the high-resolution structures of the α-amylase inhibitor tendamistat determined by nuclear magnetic resonance in solution and by X-ray diffraction in single crystals. J. molec. Biol. 206, 677–687.CrossRefGoogle ScholarPubMed
Billeter, M., Schaumann, Th., Braun, W. & Wüthrich, K. (1990). Restrained energy refinement with two different algorithms and force fields of the structure of the α-amylase inhibitor tendamistat determined by NMR in solution. Biopolymers 29, 695–706.CrossRefGoogle Scholar
Borkakoti, N., Moss, D. S. & Palmer, R. A. (1982). Ribonuclease-A: least-squares refinement of the structure at 1·45 Å resolution. Acta crystallogr. B 38, 2210–2217.CrossRefGoogle Scholar
Bränden, C.-I. & Jones, T. A. (1990). Between objectivity and subjectivity. Nature, Lond. 343, 687–689.CrossRefGoogle Scholar
Braun, W. & Gō, N. (1985). Calculation of protein conformations by proton–proton distance constraints. A new efficient algorithm. J. molec. Biol. 186, 611–626.CrossRefGoogle ScholarPubMed
Braun, W., Vasák, M., Robbins, A. H., Stout, C. D., Wagner, W., Kägi, J. H. R. & Wüthrich, K. (1992). Comparison of the NMR solution structure and the X-ray crystal structure of rat metallothionein-2. Proc. natn. Acad. Sci. U.S.A. (In the press).CrossRefGoogle Scholar
Brünger, A. T. (1990). X-PLOR 2.1 Manual. Yale University, New Havey CT 06511.Google Scholar
Buerger, M. J. (1980) Crystal-structure Analysis. Robert E. Krieger Publishing Company. New York: Huntington.Google Scholar
Bycroft, M., Sheppard, R. N., Lau, F. T.-K. & Fersht, A. R. (1990). Sequential assignment of the 1H nuclear magnetic resonance spectrum of barnase. Biochemistry 29, 7425–7432.CrossRefGoogle ScholarPubMed
Bycroft, M., Ludvigsen, S., Fersht, A. R. & Poulsen, F. M. (1991). Determination of the three-dimensional solution structure of barnase using nuclear magnetic resonance spectroscopy. Biochemistry 30, 8697–8701.CrossRefGoogle ScholarPubMed
Chazin, W. J., Kördel, J., Drakenberg, T., Thulin, E., Brodin, P., Grundström, T. & Forsén, S. (1989). Proline isomerism leads to multiple folded conformations of calbindin D9k: direct evidence from two-dimensional 1H NMR spectroscopy. Proc. natn. Acad. Sci., U.S.A. 86, 2195–2198.CrossRefGoogle ScholarPubMed
Clore, G. M. & Gronenborn, A. M. (1991 a). Applications of three- and four-dimensional hetero-nuclear NMR spectroscopy to protein structure determination. Prog. NMR Spect. 23, 43–92.CrossRefGoogle Scholar
Clore, G. M. & Gronenborn, A. M. (1991 b). Comparison of the solution nuclear magnetic resonance and X-ray crystal structures of human recombinant interleukin-1β. J. molec. Biol. 221, 47–53.CrossRefGoogle Scholar
Clore, G. M. & Gronenborn, A. M. (1991 b). Comparison of the solution nuclear magnetic resonance and crystal structures of interleukin-8. Possible implications for the mechanism of receptor binding. J. molec. Biol. 217, 611–620.CrossRefGoogle ScholarPubMed
Clore, G. M., Gronenborn, A. M., Kjaer, M. & Poulsen, F. M. (1987 a). The determination of the three-dimensional structure of the barley serine inhibitor 2 by nuclear magnetic resonance, distance geometry and restrained molecular dynamics. Protein Engineering, 1, 305–311.Google Scholar
Clore, G. M., Gronenborn, A. M., James, M. N. G., Kjaer, M., McPhalen, C. A. & Poulsen, F. M. (1987 b). Comparison of the solution and X-ray structures of barley serine protease inhibitor 2. Protein Engineering, 1, 313–318.Google Scholar
Clore, G. M., Driscoll, P. C., Wingfield, P. T. & Gronenborn, A. M. (1990 a). Low resolution structure of interleukin-1β in solution derived from 1H-15N heteronuclear three-dimensional nuclear magnetic resonance spectroscopy. J. molec. Biol. 214, 811–817.CrossRefGoogle Scholar
Clore, G. M., Appella, E., Yamada, M., Matsushima, K. & Gronenborn, A. M. (1990 b). Three-dimensional structure of interleukin 8 in solution. Biochemistry 29, 1689–1696.CrossRefGoogle ScholarPubMed
Clore, G. M., Wingfield, P. T. & Gronenborn, A. M. (1991). High-resolution three-dimensional structure of interleukin 1β in solution by three- and four-dimensional nuclear magnetic resonance spectroscopy. Biochemistry 30, 2315–2323.CrossRefGoogle Scholar
Deisenhofer, J. & Steigemann, W. (1975). Crystallographic refinement of the structure of bovine pancreatic trypsin inhibitor at 1·5 Å resolution. Acta crystallogr. B 31, 238–250.CrossRefGoogle Scholar
Dyson, H. J., Gippert, G. P., Case, D. A., Holmgren, A. & Wright, P. E. (1990). Three-dimensional solution structure of the reduced form of Escherichia coli thioredoxin determined by nuclear magnetic resonance spectroscopy. Biochemistry 29, 4129–4136.CrossRefGoogle ScholarPubMed
Eberle, W., Pastore, A., Sander, C. & Rösch, P. (1991). The structure of ColE1 rop in solution. J. Biomol. NMR 1, 71–82.CrossRefGoogle ScholarPubMed
El-Kabbani, O. A. L., Waygood, E. B. & Delbaere, L. T. J. (1987). Tertiary structure of histidine-containing protein of the phosphoenolpyruvate: sugar phosphotransferase system of Escherichia coli. J. biol. Chem. 262, 12926–12929.CrossRefGoogle Scholar
Ferrin, T. E., Huang, C. C., Jarvis, L. E. & Langridge, R. (1988). The MIDAS display system. J. molec. Graph. 6, 13–27.CrossRefGoogle Scholar
Finzel, B. C., Clancy, L. L., Holland, D. R., Muchmore, S. W., Watenpaugh, K. D. & Einspahr, H. M. (1989). Crystal structure of recombinant human interleukin-1β at 2·0 Å resolution. J. molec. Biol. 209, 779–791.CrossRefGoogle Scholar
Furey, W. F., Robbins, A. H., Clancy, L. L., Winge, D. R., Wang, B. C. & Stout, C. D. (1986). Crystal structure of Cd, Zn metallothionein. Science, N. Y. 231, 704–710.CrossRefGoogle ScholarPubMed
Glusker, J. P. & Trueblood, K. N. (1985). Crystal Structure Analysis. New York: Oxford University Press.Google Scholar
Güntert, P., Braun, W., Billeter, M. & Wüthrich, K. (1989). Automated stereospecific 1H NMR assignments and their impact on the precision of protein structure determinations in solution. J. Am. chem. Soc. III, 3997–4004.CrossRefGoogle Scholar
Güntert, P., Braun, W. & Wüthrich, K. (1991). Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J. molec. Biol. 217, 517–530.CrossRefGoogle ScholarPubMed
Hammen, P. K., Waygood, E. B. & Klevit, R. E. (1991). Reexamination of the secondary and tertiary structure of histidine-containing protein from Escherichia coli by homonuclear and heteronuclear NMR spectroscopy. Biochemistry 30, 11842–11850.CrossRefGoogle ScholarPubMed
Havel, T. F. (1990). The sampling properties of some distance geometry algorithms applied to unconstrained polypeptide chains: A study of 1830 independently computed conformations. Biopolymers 29, 1565–1585.CrossRefGoogle ScholarPubMed
Havel, T. F. & 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
Herzberg, O., Reddy, P., Sutrina, S., Saier, M. H. Jr., Reizer, J. & Kapadia, G. (1992). Structure of the histidine-containing phosphocarrier protein HPr from Bacillus subtilis at 2·0 Å resolution. Proc. natn. Acad. Sci. U.S.A. 89, 2599–2503.CrossRefGoogle ScholarPubMed
Hobohm, U., Scharf, M., Schneider, R. & Sander, C. (1992). Selection of representative protein data sets. Protein Science 1, 409–417.CrossRefGoogle ScholarPubMed
Hynes, T. R., Randal, M., Kennedy, L. A., Eigenbrot, C. & Kossiakoff, A. A. (1990). X-ray crystal structure of the protease inhibitor domain of Alzheimer's amyloid β-protein precursor. Biochemistry 29, 10018–10022.CrossRefGoogle ScholarPubMed
Kaptein, R., Zuiderweg, E. R. P., Scheek, R. M., Boelens, R. & van Gunsteren, W. F. (1985). A protein structure from nuclear magnetic resonance data, lac repressor headpiece. J. molec. Biol. 182, 179–182.CrossRefGoogle ScholarPubMed
Katti, S. K., LeMaster, D. M. & Eklund, H. (1990). Crystal structure of thioredoxin from Escherichia coli at 1·68 Å resolution. J. molec. Biol. 212, 167–184.CrossRefGoogle ScholarPubMed
Kendrew, J. C., Dickerson, R. E., Strandberg, B. E., Hart, R. G., Davies, D. R., Philips, D. C. & Shore, V. C. (1960). Structure of myoglobin. Nature, Lond. 185, 422–427.CrossRefGoogle ScholarPubMed
Klevit, R. E. & Waygood, E. B. (1986). Two-dimensional 1H NMR studies of histidine-containing protein from Escherichia coli. 3. Secondary and tertiary structure as determined by NMR. Biochemistry 25, 7774–7781.CrossRefGoogle ScholarPubMed
Kline, A. D., Braun, W. & Wüthrich, K. (1986). Studies by 1H nuclear magnetic resonance and distance geometry of the α-amylase inhibitor tendamistat. J. molec. Biol. 189, 377–382.CrossRefGoogle ScholarPubMed
Kline, A. D., Braun, W. & Wüthrich, K. (1988). Determination of the complete three-dimensional structure of the α-amylase inhibitor tendamistat in aqueous solution by nuclear magnetic resonance and distance geometry. J. molec. Biol. 204, 675–724.CrossRefGoogle ScholarPubMed
Kuszewski, J., Nilges, M. & Brünger, A. T. (1992). Sampling and efficiency of metric matrix distance geometry: A novel partial metrization algorithm. J. Biomol. NMR 2, 33–56.CrossRefGoogle ScholarPubMed
Ludvigsen, S., Shen, H., Kjaer, M., Madsen, J. Chr. & Poulsen, F. M. (1991). Refinement of the three-dimensional solution structure of barley serine proteinase inhibitor 2 and comparison with the structures in crystals. J. molec. Biol. 222, 621–635.CrossRefGoogle ScholarPubMed
Mauguen, Y., Hartley, R. W., Dodson, E. J., Dodson, G. G., Bricogne, G., Chothia, C. & Jack, A. (1982). Molecular structure of a new family of ribonucleases. Nature, Lond. 297, 162–164.CrossRefGoogle ScholarPubMed
McLachlan, A. D. (1979). Gene duplication in the structural evolution of chymotrypsin. Appendix: Least Square fitting of two structures. J. molec. Biol. 128, 49–79.CrossRefGoogle Scholar
McPhalen, C. A. & James, M. N. G. (1987). Crystal and molecular structure of the serine proteinase inhibitor CI-2 from barley seeds. Biochemistry 26, 261–269.CrossRefGoogle ScholarPubMed
Mondragón, A., Subbiah, S., Almo, S. C., Drottar, M. & Harrison, S. C. (1989). Structure of the amino-terminal domain of phage 434 repressor at 2·0 Å resolution. J. molec. Biol. 205, 189–200.CrossRefGoogle ScholarPubMed
Neri, D., Billeter, M. & Wüthrich, K. (1992). Determination of the nuclear magnetic resonance Solution structure of the DNA-binding domain (residues 1 to 69) of the 434 repressor and comparison with the X-ray crystal structure. J. molec. Biol. 223, 743–767.CrossRefGoogle ScholarPubMed
Perutz, M. F. (1964). The hemoglobin molecule. Scientific American, November, 64–76.CrossRefGoogle Scholar
Pflugrath, J. W., Wiegand, G. & Huber, R. (1986). Crystal structure determination, refinement and the molecular model of the α-amylase inhibitor Hoe-467A. J. molec. Biol. 189, 383–386.CrossRefGoogle ScholarPubMed
Priestle, J. P., Schär, H.-P. & Grütter, M. G. (1989). Crystallographic refinement of interleukin 1β at 2·0 Å resolution. Proc. natn. Acad. Sci. U.S.A. 86, 9667–9671.CrossRefGoogle Scholar
Rico, M., Santoro, J., González, C., Bruix, M., Neira, J. L., Nieto, J. L. & Herranz, J. (1991). 3D structure of bovine pancreatic ribonuclease A in aqueous solution: An approach to tertiary structure determination from a small basis of 1H NMR NOE correlations. J. Biomol. NMR 1, 283–298.CrossRefGoogle ScholarPubMed
Robbins, A. H. & Stout, C. D. (1991). X-ray structure of metallothionein. In Metallobiochemistry, Part B, Metallothionein and Related Molecules (ed. Riordan, J. F. and Vallee, B. L.). Methods in Enzymology 205, 485–502.CrossRefGoogle Scholar
Robbins, A. H., McRee, D. E., Williamson, M., Collett, S. A., Xuong, N. H., Furey, W. F., Wang, B. C. & Stout, C. D. (1991). Refined crystal structure of CD, Zn metallothionein at 2·0 Å resolution, J. molec. Biol. 221, 1269–1293.Google ScholarPubMed
Schultze, P., Wörgötter, E., Braun, W., Wagner, G., Basák, M., Kági, J. H. R. & Wüthrich, K. (1988). Conformation of [Cd7]-metallothionein-2 from rat liver in aqueous solution determined by nuclear magnetic resonance spectroscopy. J. molec. Biol. 203, 251–268.CrossRefGoogle ScholarPubMed
Singh, U. C., Weiner, P. K., Caldwell, J. W. & Kollman, P. A. (1986). AMBER 3·0, University of California, San Francisco CA 94143.Google Scholar
Skelton, N. J., Forsén, S. & Chazin, W. J. (1990). 1H NMR resonance assignments, secondary Structure, and global fold of apo bovine calbindin D9k. Biochemistry 29, 5752–5761.CrossRefGoogle ScholarPubMed
Svensson, L. A., Thulin, E. & Forsén, S. (1992). Proline cis-trans isomers in calbindin D9k observed by X-ray crystallography, J. molec. Biol. 223, 601–606.CrossRefGoogle ScholarPubMed
Szebenyi, D. M. E. & Moffat, K. (1986). The refined structure of vitamin D-dependent calcium-binding protein from bovine intestine, J. biol. Chem. 261, 8761–8777.CrossRefGoogle ScholarPubMed
Torda, A. E., Scheek, R. M. & van Gunsteren, W. F. (1990). Time-averaged nuclear Overhauser effect distance restraints applied to tendamistat. J. molec. Biol. 214, 223–235.CrossRefGoogle ScholarPubMed
Van Gunsteren, W. F. & Berendsen, H. J. C. (1987). Groningen molecular simulation (GROMOS) library manual, Biomos. The Netherlands: Groningen.Google Scholar
Van Nuland, N. A. J., van Dijk, A. A., Dijkstra, K., van Hoesel, F. H. J., Scheek, R. M. & Robillard, G. T. (1992). Three-dimensional 15N-1H-1H and 15N-13C-1H nuclear magnetic resonance studies of HPr a central component of the phosphoenolpyruvate-dependent phosphotransferase system of Escherichia coli. Eur. J. Biochem. 203, 483–491.CrossRefGoogle Scholar
Veerapandian, B., Gilliland, G. L., Raag, R., Svensson, A. L., Masui, Y., Hirai, Y. & Poulos, T. L. (1992). Functional implications of interleukin-1β based on the three-dimensional structure. Proteins 12, 10–23.CrossRefGoogle Scholar
Wagner, G. & Wüthrich, K. (1982). Sequential resonance assignments in protein 1H nuclear magnetic resonance spectra. Basic pancreatic trypsin inhibitor. J. molec. Biol. 155, 347–366.CrossRefGoogle ScholarPubMed
Wagner, G., Braun, W., Havel, T. F., Schaumann, Th. M., Go, N. & Wüthrich, K. (1987). Protein structures in solution by nuclear magnetic resonance and distance geometry. J. molec. Biol. 196, 611–639.CrossRefGoogle ScholarPubMed
Williamson, M. P., Havel, T. F. & Wüthrich, K. (1985). Solution conformation of proteinase inhibitor IIA from bull seminal plasma by 1H nuclear magnetic resonance and distance geometry. J. molec. Biol. 182, 295–315.CrossRefGoogle ScholarPubMed
Wlodawer, M. P. (1985). Structure of bovine pancreatic ribonuclease. Biol. Macromol. Assem. 2, 394–439.Google Scholar
Wlodawer, A., Walter, J., Huber, H. & Sjölin, L. (1984). Structure of bovine pancreatic trypsin inhibitor. Results of joint neutron and X-ray refinement of crystal form II. J. molec. Biol. 180, 301–329.CrossRefGoogle ScholarPubMed
Wlodawer, A., Nachman, J., Gilliland, G. L., Gallagher, W. & Woodward, C. (1987 a). Structure of form III crystals of bovine pancreatic trypsin inhibitor. J. molec. Biol. 198, 469–480.CrossRefGoogle ScholarPubMed
Wlodawer, A., Deisenhofer, J. & Huber, H. (1987 b). Comparison of two highly refined structures of bovine pancreatic trypsin inhibitor. J. molec. Biol. 193, 145–156.CrossRefGoogle ScholarPubMed
Wlodawer, A., Svensson, L. A., Sjölin, L. & Gilliland, G. L. (1988). Structure of phosphate-free ribonuclease A refined at 1·26 Å. Biochemistry 27, 2705–2717.CrossRefGoogle ScholarPubMed
Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids. New York: Wiley.CrossRefGoogle Scholar
Wüthrich, K. (1989). Protein structure determination in solution by nuclear magnetic resonance spectroscopy. Science, N. Y. 243, 45–50.CrossRefGoogle ScholarPubMed
Zuiderweg, E. R. P., Billeter, M., Boelens, R., Scheek, R. M., Wüthrich, K. & Kaptein, R. (1984). Spatial arrangement of the three α helices in the solution conformation of E. coli lac repressor DNA-binding domain. FEBS Lett. 174, 243–247.CrossRefGoogle ScholarPubMed