International
Tables for
Crystallography
Volume F
Crystallography of biological macromolecules
Edited by M. G. Rossmann and E. Arnold

International Tables for Crystallography (2006). Vol. F, ch. 26.1, pp. 745-772   | 1 | 2 |
https://doi.org/10.1107/97809553602060000725

Chapter 26.1. How the structure of lysozyme was actually determined

C. C. F. Blake,a R. H. Fenn,a§ L. N. Johnson,a* D. F. Koenig,a‡‡ G. A. Mair,a‡‡ A. C. T. North,a§§ J. W. H. Oldham,a¶¶ D. C. Phillips,a¶¶ R. J. Poljak,a‡‡‡ V. R. Sarmaa§§§ and C. A. Vernonb¶¶

aDavy Faraday Research Laboratory, The Royal Institution, London W1X 4BS, England, and bDepartment of Chemistry, University College London, Gower Street, London WC1E 6BT, England
Correspondence e-mail:  louise@biop.ox.ac.uk

References

Abraham, E. P. & Robinson, R. (1937). The crystallization of lysozyme. Nature (London), 140, 24.Google Scholar
Alderton, G., Ward, W. H. & Fevold, J. (1945). Crystallization of lysozyme chloride. J. Biol. Chem. 157, 43–58.Google Scholar
Arndt, U. W., North, A. C. T. & Phillips, D. C. (1964). Adaptation of a linear diffractometer to measure three X-ray reflections quasi-simultaneously. J. Sci. Instrum. 41, 421–425.Google Scholar
Arndt, U. W. & Phillips, D. C. (1961). The linear diffractometer. Acta Cryst. 14, 807–818.Google Scholar
Arndt, U. W. & Riley, D. P. (1952). Side-window proportional counters. Proc. Phys. Soc. London A, 65, 74–84.Google Scholar
Bijvoet, J. M. (1954). Structure of optically active compounds in the solid state. Nature (London), 173, 888–891.Google Scholar
Blake, C. C. F. (1968). The preparation of isomorphous derivatives. Adv. Protein Chem. 23, 59–120.Google Scholar
Blake, C. C. F., Fenn, R. H., North, A. C. T., Phillips, D. C. & Poljak, R. J. (1962). Structure of lysozyme. A Fourier map of the electron density at 6 Å resolution obtained by X-ray diffraction. Nature (London), 196, 1173–1178.Google Scholar
Blake, C. C. F., Johnson, L. N., Mair, G. A., North, A. C. T., Phillips, D. C. & Sarma, V. R. (1967). Crystallographic studies of the activity of hen egg-white lysozyme. Proc. R. Soc. London Ser. B, 167, 378–388.Google Scholar
Blake, C. C. F., Koenig, D. F., Mair, G. A., North, A. C. T., Phillips, D. C. & Sarma, V. R. (1965). Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2 Å resolution. Nature (London), 206, 757–761.Google Scholar
Blake, C. C. F. & Phillips, D. C. (1962). Effects of X-irradiation on single crystals of myoglobin. In Biological effects of ionizing radiation at the molecular level. Brno, Czechoslovakia: International Atomic Energy Agency, Vienna.Google Scholar
Blow, D. M. (1958). The structure of haemoblobin. VII. Determination of phase angles in the non-centrosymmetric [100] zone. Proc. R. Soc. London Ser. A, 247, 302–336.Google Scholar
Blow, D. M. & Crick, F. H. C. (1959). The treatment of errors in the isomorphous replacement method. Acta Cryst. 12, 794–802.Google Scholar
Blow, D. M. & Rossmann, M. G. (1961). The single isomorphous replacement method. Acta Cryst. 14, 1195–1202.Google Scholar
Bluhm, M. M., Bodo, G., Dintzis, H. M. & Kendrew, J. C. (1958). The crystal structure of myoglobin IV. A Fourier projection of sperm-whale myoglobin by the method of isomorphous replacement. Proc. R. Soc. London Ser. A, 246, 369–389.Google Scholar
Buerger, M. J. (1959). Vector space. New York: Wiley.Google Scholar
Canfield, R. E. & Liu, A. K. (1965). The disulfide bonds of egg white lysozyme (muramidase). J. Biol. Chem. 240, 1997–2002.Google Scholar
Carlstrom, D. (1962). The polysaccharide chain of chitin. Biochim. Biophys. Acta, 59, 361–364.Google Scholar
Cheetham, J. C., Artymiuk, P. J. & Phillips, D. C. (1992). Refinement of an enzyme complex with inhibitor bound at partial occupancy. J. Mol. Biol. 224, 613–628.Google Scholar
Collins, J. F. & Richmond, M. (1962). A structural similarity between N-acetyl muramic acid and penicillin as a basis for antibiotic action. Nature (London), 195, 142–143.Google Scholar
Corey, R. B., Donohue, J., Trueblood, K. N. & Palmer, K. J. (1952). An X-ray investigation of air-dried lysozyme chloride crystals: the three-dimensional Patterson function. Acta Cryst. 5, 701–710.Google Scholar
Cox, E. G. & Jeffrey, G. A. (1939). Crystal structure of glucosamine hydrobromide. Nature (London), 143, 894–895.Google Scholar
Crick, F. H. C. & Magdoff, B. S. (1956). The theory of the method of isomorphous replacement for protein crystals. 1. Acta Cryst. 9, 901–908.Google Scholar
Cullis, A. F., Muirhead, H., Perutz, M. F., Rossmann, M. G. & North, A. C. T. (1961). The structure of haemoglobin VIII. A three-dimensional Fourier synthesis at 5.5 Å resolution: determination of the phase angles. Proc. R. Soc. London Ser. A, 265, 15–38.Google Scholar
Cullis, A. F., Muirhead, H., Perutz, M. F., Rossmann, M. G. & North, A. C. T. (1962). The structure of haemoglobin IX. A three-dimensional Fourier synthesis at 5.5 Å resolution: description of the structure. Proc. R. Soc. London Ser. A, 265, 161–187.Google Scholar
Dauben, C. H. & Templeton, D. H. (1955). A table of dispersion corrections for X-ray scattering of atoms. Acta Cryst. 8, 841–842.Google Scholar
Dickerson, R. E., Kendrew, J. C. & Strandberg, B. E. (1961). The crystal structure of myoglobin: phase determination to a resolution of 2 Å by the method of isomorphous replacement. Acta Cryst. 14, 1188–1195.Google Scholar
Dickerson, R. E., Reddy, J. M., Pinkerton, M. & Steinrauf, L. K. (1962). A 6 Å model of triclinic lysozyme. Nature (London), 196, 1178.Google Scholar
Fenn, R. H. (1964). An X-ray crystallographic study of some mercury compounds and their use in protein structure analysis. Davy Faraday Research Laboratory, The Royal Institution, London 182.Google Scholar
Fenn, R. H., Phillips, D. C. & Oldham, J. W. H. (1963). Crystal structure of (CH3)3S.HgI3 and the configuration of the [HgI_{\it 3}^{-}] ion. Nature (London), 198, 381–382.Google Scholar
Fleming, A. (1922). On a remarkable bacteriolytic element found in tissues and secretions. Proc. R. Soc. London Ser. B, 93, 306–317.Google Scholar
Ford, L. O., Johnson, L. N., Machin, P. A., Phillips, D. C. & Tjian, R. (1974). Crystal structure of a lysozyme–tetrasaccharide lactone complex. J. Mol. Biol. 88, 349–371.Google Scholar
Furnas, T. C. (1957). Single crystal orienter instruction manual. General Electric Company, Milwaukee, USA.Google Scholar
Green, D. W., Ingram, V. M. & Perutz, M. F. (1954). The structure of haemoglobin IV. Sign determination by the isomorphous replacement method. Proc. R. Soc. London Ser. A, 225, 287–307.Google Scholar
Green, D. W., North, A. C. T. & Aschaffenburg, R. (1956). Crystallography of the β-lactoglobulins of cows' milk. Biochim. Biophys. Acta, 21, 583–585.Google Scholar
Hadfield, A. T., Harvey, D. J., Archer, D. B., MacKenzie, D. A., Jeenes, D. J., Radford, S. E., Lowe, G., Dobson, C. M. & Johnson, L. N. (1994). Crystal structure of the mutant D52S hen egg white lysozyme with an oligosaccharide product. J. Mol. Biol. 243, 856–872.Google Scholar
Hamaguchi, K. & Imahori, K. (1964). Optical measurements of the secondary structure of lysozyme. J. Biochem (Tokyo), 55, 388–391.Google Scholar
Hamilton, W. C. (1955). On the treatment of unobserved reflexions in the least-squares adjustment of crystal structures. Acta Cryst. 8, 185–186.Google Scholar
Hamilton, W. C., Rollett, J. S. & Sparks, R. A. (1965). On the relative scaling of X-ray photographs. Acta Cryst. 18, 129–130.Google Scholar
Handoll, H. H. G. (1985). Crystallographic studies of proteins. DPhil thesis, University of Oxford.Google Scholar
Harker, D. (1956). The determination of the phases of the structure factors of non-centrosymmetric crystals by the method of double isomorphous replacement. Acta Cryst. 9, 1–9.Google Scholar
Hart, R. G. (1961). Refinement of heavy atom parameters other than relative y's. Acta Cryst. 14, 1194–1195.Google Scholar
Imoto, T., Johnson, L. N., North, A. C. T., Phillips, D. C. & Rupley, J. A. (1972). Vertebrate lysozymes. New York and London: Academic Press.Google Scholar
Jacobson, R. A., Wunderlich, J. A. & Lipscomb, W. N. (1961). The crystal and molecular structure of cellobiose. Acta Cryst. 14, 598–607.Google Scholar
Jeffrey, G. A. (1990). Crystallographic studies of carbohydrates. Acta Cryst. B46, 89–103.Google Scholar
Johnson, L. N. (1966). The crystal structure of N-acetyl-α-D-glucosamine. Acta Cryst. 21, 885–891.Google Scholar
Johnson, L. N. (1967). An interaction between lysozyme and penicillin. Proc. R. Soc. London Ser. B, 167, 439–440.Google Scholar
Johnson, L. N. & Phillips, D. C. (1964). Crystal structure of N-acetylglucosamine. Nature (London), 202, 588–589.Google Scholar
Johnson, L. N. & Phillips, D. C. (1965). Structure of some crystalline lysozyme–inhibitor complexes determined by X-ray analysis at 6 Å resolution. Nature (London), 206, 761–763.Google Scholar
Jollès, J., Jaurrgui-Adell, J. & Jollès, P. (1964). Amino-acid sequence & S–S bridges of HEWL. C. R. Acad. Sci. Paris, 258, 3926–3928.Google Scholar
Jolles, P. (1996). Editor. Lysozymes: model enzymes in biochemistry and biology. Basel, Boston, Berlin: Birkhauser Verlag.Google Scholar
Kendrew, J. C., Bodo, G., Dintzis, H. M., Parrish, R. G., Wyckoff, H. & Phillips, D. C. (1958). A three-dimensional model of the myoglobin molecule obtained by X-ray analysis. Nature (London), 181, 662–666.Google Scholar
Kendrew, J. C., Dickerson, R. E., Strandberg, B. E., Hart, R. G., Davies, D. R., Phillips, D. C. & Shore, V. C. (1960). Structure of myoglobin. A three-dimensional Fourier synthesis at 2 Å resolution. Nature (London), 185, 422–427.Google Scholar
Kraut, J., Sieker, L. C., High, D. F. & Freer, S. T. (1962). Electron density map of chymotrypsinogen at 6 Å resolution. Proc. Natl Acad. Sci. USA, 48, 1417.Google Scholar
Lavington, S. (1980). Early British computers: the story of vintage computers and the people who built them. Manchester University Press.Google Scholar
Lemieux, R. U. & Huber, G. (1955). Can. J. Res. 33, 128–133.Google Scholar
Lipson, H. & Cochran, W. (1968). The determination of crystal structures. London: Bell.Google Scholar
Mo, F. & Jensen, L. H. (1975). A refined model for N-acetyl-α-D-glucosamine. Acta Cryst. B31, 2867–2873.Google Scholar
North, A. C. T. (1964). Computer processing of automatic diffractometer data. J. Sci. Instrum. 41, 42–45.Google Scholar
North, A. C. T. (1965). The combination of isomorphous replacement and anomalous scattering data in phase determination of non-centrosymmetric reflexions. Acta Cryst. 18, 212–216.Google Scholar
North, A. C. T., Phillips, D. C. & Matthews, F. S. (1968). A semi-empirical method of absorption correction. Acta Cryst. A24, 351–359.Google Scholar
Perutz, M. F. (1967). Concluding remarks. Proc. R. Soc. London Ser. B, 167, 448.Google Scholar
Perutz, M. F., Rossmann, M. G., Cullis, A. F., Muirhead, H., Will, G. & North, A. C. T. (1960). Structure of haemoglobin. A three-dimensional Fourier synthesis at 5.5 Å resolution, obtained by X-ray analysis. Nature (London), 185, 416–422.Google Scholar
Phillips, D. C. (1964). On the design of single crystal diffractometers to measure a number of reflections simultaneously. J. Sci. Instrum. 41, 123–129.Google Scholar
Phillips, D. C. (1966). The three-dimensional structure of an enzyme molecule. Sci. Am. pp. 78–90.Google Scholar
Phillips, D. C. (1967). The hen egg white lysozyme molecule. Proc. Natl Acad. Sci USA, 57, 484–495.Google Scholar
Poljak, R. J. (1963). Heavy atom attachment to crystalline lysozyme. J. Mol. Biol. 6, 244–246.Google Scholar
Ramachandran, G. N., Ramakrishnan, G. & Sasisekharan, V. (1963). Aspects of protein structure. London: Academic Press.Google Scholar
Rollett, J. S. (1961). Least-squares refinement in crystal-structure analysis. In Computing methods and the phase problem in X-ray crystal analysis, p. 122. London: Pergamon Press.Google Scholar
Rollett, J. S. & Sparks, R. A. (1960). The correlation of intersecting layers of X-ray intensity data. Acta Cryst. 13, 273–274.Google Scholar
Rupley, J. A. (1964). The hydrolysis of chitin by concentrated hydrochloric acid and the preparation of low molecular weight substrates for lysozyme. Biochim. Biophys. Acta, 83, 245–255.Google Scholar
Rupley, J. A. (1967). The binding and cleavage by lysozyme of N-acetylglucosamine oligosaccharides. Proc. R. Soc. London Ser. B, 167, 416–428.Google Scholar
Scouloudi, H. (1960). Structure of seal myoglobin in projection. Proc. R. Soc. London Ser. A, 258, 181.Google Scholar
Scouloudi, H. (1965). The nature and configuration of the mercuri-iodide ion in the seal myoglobin derivative. J. Mol. Biol. 12, 17–26.Google Scholar
Stanford, R. H., Marsh, R. E. & Corey, R. B. (1962). An X-ray investigation of lysozyme chloride crystals containing complex ions of niobium and tantalum: three-dimensional Fourier plot obtained from data extending to a minimum spacing of 5 Å. Nature (London), 196, 1172–1177.Google Scholar
Steinrauf, L. K. (1959). Preliminary X-ray data for some new crystalline forms of β-lactoglobulin and hen-egg-white lysozyme. Acta Cryst. 12, 77–79.Google Scholar
Stryer, L., Kendrew, J. C. & Watson, H. C. (1964). The mode of attachment of the azide ion to sperm whale myoglobin. J. Mol. Biol. 8, 96–104.Google Scholar
Strynadka, N. C. J. & James, M. G. (1991). Lysozyme revisited: crystallographic evidence for distortion of an N-acetyl muramic acid residue bound in site D. J. Mol. Biol. 220, 401–424.Google Scholar
Tipper, D. J. & Strominger, J. L. (1965). Mechanism of action of penicillins: a proposal based on their structural similarity to acyl-D-alanyl-D-alanine. Proc. Natl Acad Sci. USA, 54, 1133–1141.Google Scholar
Vernon, C. A. (1967). The mechanisms of hydrolysis of glycosides and their relevance to enzyme-catalysed reactions. Proc. R. Soc. London Ser. B, 167, 389–401.Google Scholar
Waser, J. (1951). Lorentz factor for precession photographs. Rev. Sci. Instrum. 22, 563.Google Scholar
Watson, H. C., Kendrew, J. C., Coulter, C. L. & Brändën, C.-I. (1963). Progress with the 1.4 Å resolution myoglobin-structure determination. Acta Cryst. 16, A81.Google Scholar
Wells, M. (1960). Computation of absorption corrections on EDSAC II. Acta Cryst. 13, 722–736.Google Scholar
Wenzel, M., Lenk, H. P. & Schutte, E. (1962). Z. Physiol. Chem. 327, 13–20.Google Scholar
Wilson, A. J. C. (1942). Determination of absolute from relative X-ray intensity data. Nature (London), 150, 151–152.Google Scholar
Wise, E. M. & Park, J. T. (1965). Penicillin: its basis site of action as an inhibitor of a peptide cross-linking reaction in cell-wall mucopeptide synthesis. Proc. Natl Acad. Sci. USA, 54, 75–81.Google Scholar
Yang, J. T. & Doty, P. (1957). ORD measurements on lysozyme. J. Am. Chem. Soc. 79, 761.Google Scholar