Advertisement

Protein-Oligosaccharide Interactions: Lysozyme, Phosphorylase, Amylases

  • L. N. Johnson
  • J. Cheetham
  • P. J. McLaughlin
  • K. R. Acharya
  • D. Barford
  • D. C. Phillips
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 139)

Abstract

Polysaccharides have many diverse biological roles. They comprise the insoluble structural and supportive elements of bacterial and plant cell walls. They serve as storage macromolecules (e.g., glycogen and starch) to provide fuel for cells, and they form important components in the heteromacromolecules, proteoglycans and glycoproteins, which are involved in the structural elements of connective tissue, in the lubrication of skeletal joints, in cell-cell adhesion and in cell-surface recognition. The enzymes that catalyze the biosynthesis and degradation of these polysaccharides are highly specific, resulting, in the case of biosynthesis, in polymers of defined constitution and sequence and, in the case of degradation in the cleavage of specific linkages. In this article we describe the X-ray structural results for three of these enzymes: lysozyme, glycogen phosphorylase, and amylase. Each catalyzes a specific step in the degradation of different polysaccharides. (To date there are no structural data on any of the biosynthetic enzymes.) Lysozyme catalyzes the hydrolysis of a β-(1–4) linkage of bacterial cell wall polysaccharides; glycogen phosphorylase catalyzes the reversible phosphorylation of α-(1–4) linkages of glycogen and amylase catalyzes the hydrolysis of α-(1–4) linkages in starch. We use these results in an attempt to draw together some general principles that appear to be important in generating a protein-oligosaccharide recognition site and compare these features with protein monosaccharide sites.

Keywords

Catalytic Site Storage Site Glycogen Phosphorylase Pyranose Ring Oligosaccharide Binding 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson WF, Grutter MG, Remington SJ, Matthews BW (1981) Crystallographic determination of the mode of binding of oligosaccharides to T4 bacteriophage lysozyme: implications for the mechanism of catalysis. J Mol Biol 147:523–543.PubMedGoogle Scholar
  2. Ariki M, Fukui T (1977) Affinity of glucose analogues for α-glucan phosphorylases from rabbit muscle and potato tubers. J Biochem (Tokyo) 81:1017–1024.PubMedGoogle Scholar
  3. Arnheim N, Inouye M, Low L, Laudin A (1973) Chemical studies on the enzymatic specificity of goose egg-white lysozyme. J Biol Chem 248:233–236.PubMedGoogle Scholar
  4. Arnott S, Scott WE (1972) Accurate x-ray diffraction analysis of fibrous polysaccharides containing pyranose rings. Part I. The linked atom approach. J Chem Soc Perkin II: 324–335.Google Scholar
  5. Artymiuk PJ (1979) X-Ray Studies of Biological Macromolecules: The Refinement of Human Lysozyme at 1.5 Å Resolution. D. Phil. Thesis, University of Oxford.Google Scholar
  6. Artymiuk PJ, Blake CCF (1981) Human lysozyme at 1.5 Å resolution. J Mol Biol 152:737–762.PubMedGoogle Scholar
  7. Artymiuk PJ, Rice DW (1980-81) Progress report. Laboratory of molecular biophysics, University of Oxford, p 25.Google Scholar
  8. Aschaffenburg R, Blake CCF, Dickie HM, Gayen SK, Keegan R, Sen A (1980) The crystal structure of tortoise egg-white lysozyme at 6 Å resolution. Biochim Biophys Acta 625:64–71.PubMedGoogle Scholar
  9. Baker EN, Hubbard RE (1984) Hydrogen bonding in globular proteins. Prog Biophys Mol Biol 44:97–179.PubMedGoogle Scholar
  10. Banerjee SK, Holler E, Hess GP, Rupley JA (1975) Reaction of N-acetylglucosamine oligosaccharides with lysozyme. J Biol Chem 250:4355–4367.PubMedGoogle Scholar
  11. Banyard SE (1973) X-Ray Diffraction Studies of Enzymes. D Phil Thesis, University of Oxford.Google Scholar
  12. Beddell CR, Moult J, Phillips DC (1970) Crystallographic studies of the active site of lysozyme. In: Porter R, O’Connor M (eds) Ciba found symp on molecular properties of drug receptors. Churchill, London.Google Scholar
  13. Beevers CA, Maconochie GH (1965) The crystal structure of dipotassium glucose-1-phosphate dihydrate. Acta Crystallogr 18:232–236.PubMedGoogle Scholar
  14. Bienkowska K, Taylor A (1979) Low molecular weight substrate for the lysozyme of T4 bacteriophage. Eur J Biochem 96:581–584.PubMedGoogle Scholar
  15. Black WJ, Wang JH (1968) Studies on the allosteric activation of glycogen phosphorylase b by nucleotides. I. Activation of phosphorylase b by inosine monophosphate. J Biol Chem 243:5892–5898.PubMedGoogle Scholar
  16. Blake CCF, Koenig DF, Mair GA, North ACT, Phillips DC, Sarma VR (1965) Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2.0 Å resolution. Nature 206:757–761.PubMedGoogle Scholar
  17. Blake CCF, Mair GA, North ACT, Phillips DC, Sarma VR (1967 a) On the conformation of the hen egg-white lysozyme molecule. Proc R Soc Lond [Biol] B 167:365–377.Google Scholar
  18. Blake CCF, Johnson LN, Mair GA, North ACT, Phillips DC, Sarma VR (1967 b) Crystallographic studies of the activity of hen egg-white lysozyme. Proc R Soc Lond [Biol] B 167:378–388.Google Scholar
  19. Branden CI (1980) Relation between structure and function of α/β proteins. Q Rev Biophys 13:317–338.Google Scholar
  20. Branden CI (1986) The relation between protein structure in α/β domains and the intron-exon arrangement of the corresponding genes. Nobel symposium (in press).Google Scholar
  21. Busby SJW, Rädda GK (1976) Regulation of the glycogen phosphorylase system. Curr Top Cell Regul 10:89–160.PubMedGoogle Scholar
  22. Caudwell B, Antoniw JF, Cohen P (1978) Calsequestrin, myosin and the components of the protein-glycogen complex in rabbit skeletal muscle. Eur J Biochem 86:511–518.PubMedGoogle Scholar
  23. Cassels R (1979) Investigation of protein structure-lysozyme in the crystalline and solution states. Ph D thesis, University of Oxford.Google Scholar
  24. Cheetham JC (1986) Studies of enzyme-inhibitor interactions and protein dynamics. Ph D thesis, University of Oxford.Google Scholar
  25. Cheetham JC, Artymiuk PA, Phillips DC (1987) The refinement of an enzyme complex with inhibitor bound at partial occupancy: HEWL + triNAG at 1.75 Å resolution. (Manuscript in preparation)Google Scholar
  26. Chu SJC, Jeffrey GA (1967) The crystal structure of methyl β-maltopyranoside. Acta Crystallogr 23:1038–1049.PubMedGoogle Scholar
  27. Cohen P (1978) Hormonal control of muscle glycogen metabolism. Curr Top Cell Reg 14:117–196.Google Scholar
  28. Cohen P (1983) Control of enzyme activity, 2nd edn. Chapman and Hall, London.Google Scholar
  29. Dobson CM (1975) The Confirmation of Lysozyme in Solution. D Phil Thesis, University of Oxford.Google Scholar
  30. Dombraidi V (1981) Structural aspects of the catalytic and regulatory function of glycogen phosphorylase. Int J Biochem 13:125–139.Google Scholar
  31. Fleming A (1922) On a remarkable bacteriolytic element found in tissues and secretions. Proc R Soc Lond (Biol) B93:306–317.Google Scholar
  32. Fletterick RJ, Madsen NB (1980) The structures and related functions of phosphorylase a. Annu Rev Biochem 49:31–61.PubMedGoogle Scholar
  33. Fletterick RJ, Sprang SR (1982) Glycogen phosphorylase structure and function. Ace Chem Res 15:361–369.Google Scholar
  34. Ford LO, Johnson LN, Machin PA, Phillips DC, Tjian RJ (1974) Crystal structure of a lysozyme-tetrasaccharide lactone complex. J Mol Biol 88:349–371.PubMedGoogle Scholar
  35. Gallay O (1984) X-ray studies on an enzyme: X-ray crystallography of the binding of a tetrasaccharide to tortoise egg-white lysosome. Part II. Thesis, University of Oxford.Google Scholar
  36. Ghuysen JM (1968) Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol Rev 32:425–464.PubMedGoogle Scholar
  37. Goldsmith E, Fletterick R (1983) Oligosaccharide conformation and protein saccharide interactions in solution. Pure Appl Chem 55:577–588.Google Scholar
  38. Goldsmith E, Sprang S, Fletterick R (1982) Structure of maltoheptose by difference Fourier methods and a model for glycogen. J Mol Biol 156:411–427.PubMedGoogle Scholar
  39. Goldsmith EJ, Fletterick RJ, Withers SG (1987) The three-dimensional structure of acarbose bound to glycogen phosphorylase. J Biol Chem 262:1449–1455.PubMedGoogle Scholar
  40. Grace DEP (1980) A refined analysis of the structure of lysozyme and its interactions with substrates. Phil thesis, University of Oxford.Google Scholar
  41. Graves DJ, Wang JH (1972) α-glucan phosphorylases-chemical and physical basis of catalysis and regulation. Boyer P (ed) The Enzymes, 3rd edn, vol 7. Academic, New York, pp 435–482.Google Scholar
  42. Gress ME, Jeffrey GA (1977) A neutron diffraction refinement of the crystal of β-maltose monohydrate. Acta Cryst B33:2490–2495.Google Scholar
  43. Grutter MG, Matthews BW (1982) Amino acid substitutions far from the active site of bacteriophage T4 lysozyme reduce catalytic activity and suggest that the C-terminal lobe of the enzyme participates in substrate binding. J Mol Biol 154:525–535.PubMedGoogle Scholar
  44. Grutter MG, Weaver LH, Matthews BW (1983) Goose lysozyme structure: an evolutionary link between hen and bacteriophage lysozymes? Nature 303:828–831.PubMedGoogle Scholar
  45. Hajdu J, Acharya KR, Stuart DI, McLaughlin PJ, Barford D, Oikonomakos NG, Klein H, Johnson LN (1987) Catalysis in the crystal: synchrotron radiation studies with glacogen phosphorylase b. EMBO J 6:539–546.PubMedGoogle Scholar
  46. Handoll HHG (1985) PhD thesis, University of Oxford.Google Scholar
  47. Handoll HHG, Artymiuk PJ, Grace DEP, Phillips DC (1987) A description and comparison of the refined structures of the original model of tetragonal hen egg-white lysozyme to 2.0 Å resolution and that of a closely related tetragonal form at 1.6 Å crystallised at higher pH. (Manuscript in preparation).Google Scholar
  48. Haschke RM, Gratz KW, Heilmeyer LMG (1972) The role of phosphorylase activity in a muscle glycogen particle. J Biol Chem 247:5351–5356.PubMedGoogle Scholar
  49. Hehre EJ, Brewer CF, Uchiyama T, Schlesselmann P, Lehmann J (1980) Scope and mechanism of carbohydrase action. Stereospecific hydration of 2,6-anhydro-l-deoxy-D-gluco-hept-1-enitol catalysed by α-and β-glucosidases and an inverting exo-α-glucanase. Biochemistry 19:3557–3564.PubMedGoogle Scholar
  50. Heilmeyer LMG, Meyer F, Haschke RH, Fischer EH (1970) Control of phosphorylase activity in a muscle glycogen particle, Π. Activation by calcium. J Biol Chem 245:6649–6656.PubMedGoogle Scholar
  51. Helmreich EJM, Klein H (1980) The role of pyridoxal phosphate in the catalysis of glycogen phospho-rylases. Angew Chem Int 19:441–455.Google Scholar
  52. Helmreich EJM, Michaelides MC, Cori CF (1967) Effects of substrates and a substrate analog on the binding of 5′-adenylic acid to muscle phosphorylase a. Biochemistry 6:3695–3710.PubMedGoogle Scholar
  53. Hendrickson WA, Konnert JH (1980) Incorporation of stereochemical information into crystallo-graphic refinement. In: Diamond R, Ramaseshan S, Venkatesan K (eds) Computing in crystallography. Indian Academy of Science, pp 13.01–13.23.Google Scholar
  54. Hogle J, Rao ST, Mallikarjunan M, Beddell C, McMullan RK, Sandaralingam M (1981) Studies of monoclinic hen egg-white lysozyme. I. Structure solution at 4 Å resolution and molecular packing comparisons with tetragonal and triclinic lysozymes. Acta Crystallogr B37:591–597.Google Scholar
  55. Holler E, Rupley JA, Hess GP (1975) Productive and unproductive lysozyme-chitosaccharide complexes. Equilibrium measurements. Biochemistry 14:1088–1094.PubMedGoogle Scholar
  56. Hu HY, Gold AM (1975) kinetics of glycogen phosphorylase a with a series of semisynthetic branched saccharides. Biochemistry 14:2224–2230.PubMedGoogle Scholar
  57. Imoto T, Johnson LN, North ACT, Phillips DC, Rupley JA (1972) Vertebrate lysozymes. In: Boyer PD (ed) The enzymes, 3rd edn, vol 7. Academic, New York, pp 665–868.Google Scholar
  58. Jacobson RA, Wunderlich JA, Lipscomb WA (1961) The crystal and molecular structure of cellobiose. Acta Crystallogr 14:598–607.Google Scholar
  59. Jeanloz RW, Sharon N, Flowers HM (1963) The chemical structure of a disaccharide isolated from Micrococcus lysodeiktius cell wall. Biochem Biophys res Commun 13:20–25.PubMedGoogle Scholar
  60. Jenkins JA, Johnson LN, Stuart DI, Stura EA, Wilson KS, Zanotti G (1981) Phosphorylase: control and activity. Philos Trans R Soc Lond [Biol] B293:23–41.Google Scholar
  61. Johnson LM, Phillips DC, Rupley JA (1968) The activity of lysozyme: An interim review of crystallo-graphic and chemical evidence. Brookhaven Symp Biology 21:120–138.Google Scholar
  62. Johnson LN, Phillips DC (1965) Structure of some crystalline lysozyme-inhibitor complexes determined by x-ray analysis at 5 Å resolution. Nature 206:761–763.PubMedGoogle Scholar
  63. Johnson LN, Jenkins JA, Wilson KS, Stura EA, Zanotti G (1980) Proposals for the catalytic mechanism of glycogen phosphorylase b. J Mol Biol 140:565–580.PubMedGoogle Scholar
  64. Johnson LN, Stura EA, Sansom MSP, Babu YS (1983) Oligosaccharide binding to glycogen phosphorylase b. Biochem Soc Trans Π: 142–144.Google Scholar
  65. Johnson LN, Hajdu J, Acharya KR, Stuart DI, McLaughlin PJ, Oikonomakos NG, Barford D (1988) Glycogen Phosphorylase b. In: Herve G (ed) Allosteric Enzymes. CRC Press, Florida (in press).Google Scholar
  66. Jolles P, Jolles J (1984) Review of progress in lysozyme research. Mol Cell Biochem 63:165–189.PubMedGoogle Scholar
  67. Kasvinsky PJ, Madsen NB (1976) Activity of glycogen phosphorylase in the crystalline state. J Biol Chem 251:6852–6859.PubMedGoogle Scholar
  68. Kasvinsky PJ, Madsen NB, Fletterick RJ, Sygusch J (1978) X-ray crystallographic and kinetic studies of oligosaccharide binding to phosphorylase. J Biol Chem 253:1290–1296.PubMedGoogle Scholar
  69. Kelly JA, Sielecki AR, Sykes BD, James MNG, Phillips DC (1979) X-ray crystallography of the binding of the bacterial cell wall trisaccharide NAM-NAG-NAM to lysozyme. Nature 282:875–878.PubMedGoogle Scholar
  70. Kelly JA, Sielecki AR, Sykes BD, James MNG, Phillips DC (1979) X-ray crystallography of the binding of the bacterial cell wall trisaccharide NAM-NAG-NAM to lysozyme. Nature 282:875–878.PubMedGoogle Scholar
  71. Kirkman BR, Whelan WJ (1986) Glucosamine is a normal component of liver glycogen. FEBS Lett 194:6–11.PubMedGoogle Scholar
  72. Klein MW, Im MJ, Palm D, Helmreich EJM (1984) Does pyridoxal 5′-phosphate function in glycogen phosphorylase as an electrophilic or a general acid catalyst? Biochemistry 23:5853–5861.PubMedGoogle Scholar
  73. Klein MW, Im MJ, Palm DL (1986) Mechanism of the phosphorylase reaction: utilisation of D-gluco-hept-1-enitol in the absence of primer. Eur J Biochem 57:107–114.Google Scholar
  74. Kleppe G, Vasstrand E, Jensen HB (1981) The specificity requirements of bacteriophage T4 lysozyme. Involvement of the N-acetamido groups. Eur J Biochem 119:589–593.PubMedGoogle Scholar
  75. Kurachi K, Sieker LC, Jensen LH (1976) Structures of triclinic mono-and di-N-acetylglucosamine: lysozyme complexes — a crystallographic study. J Mol Biol 101:11–24.PubMedGoogle Scholar
  76. Kuramitsu S, Ikeda K, Hamaguchi K (1977) Effects of ionic strength and temperature on the ioniza-tion of the catalytic groups, Asp 52 and Glu 35, in hen lysozyme. J Biochem (Tokyo) 82:585–597.Google Scholar
  77. Larner J, Takeda Y, Hizukuri S (1976) The influence of chain size and molecular weight on the kinetic constants for the span glucose to polysaccharide for rabbit muscle glycogen synthase. Mol Cell Biochem 12:131–136.PubMedGoogle Scholar
  78. Lehrer SS, Fasman GD (1966) The Fluorescence of Lysozyme and Lysozyme Substrate Complexes. Biochem Biophys Res Commun 23:133–139.PubMedGoogle Scholar
  79. Levitt M (1972) Conformation analysis of proteins. Ph D thesis, University of Cambridge.Google Scholar
  80. Levitt M (1974) On the nature of the binding of hexa-N-acetylglucosamine substrate to lysozyme. In: Blout ER, Bovrey FA, Goodman M, Lotan N (eds) Peptides, polypeptides and proteins. Wiley, New York, pp 99–113.Google Scholar
  81. Liddington R (1981) X-ray studies on lysozyme. Chemistry. Part II. Thesis, University of Oxford.Google Scholar
  82. Loyter A, Schramm M (1966) Multimolecular complexes of α-amylase with glycogen limit dextrin. J Biol Chem 241:2611–2617.PubMedGoogle Scholar
  83. Madsen NB, Withers SG (1986) Glycogen phosphorylase in coenzymes and cofactors. In: Dolphin D, Poulson R, Avramovic O (eds) Pyridoxal phosphate and derivatives. Wiley, New York.Google Scholar
  84. Manor PC, Saenger W (1974) Topography of cyclodextrin inclusion complexes. J Am Chem Soc 96:3630–3639.Google Scholar
  85. Mason SA, Bentley GA, McIntyre GJ (1984) Deuterium exchange in lysozyme at 1.4 Å resolution. In: Schoenborn P (ed) Neutrons in biology. Plenum, NY.Google Scholar
  86. Matsuura Y, Kusunoki M, Harada W, Kakudo M (1984) Structure and possible catalytic residues of Taka amylase A. J Biochem (Tokyo) 95:697–702.Google Scholar
  87. Matthews BW, Remington SJ (1974) The three dimensional structure of the lysozyme from bacteriophage T4. Proc Natl Acad Sci USA 71:4178–4182.PubMedGoogle Scholar
  88. McLaughlin PJ, Stuart DI, Klein HW, Oikonomakos NG, Johnson LN (1984) Substrate cofactor interactions for glycogen phosphorylase b. A binding study in the crystal with heptenitol and heptulose-2-phosphate. Biochemistry 23:5862–5873.PubMedGoogle Scholar
  89. Metzger B, Helmreich E, Glaser L (1967) The mechanism of activation of skeletal muscle phosphorylase a by glycogen. Proc Natl Acad Sci USA 57:994–1001.PubMedGoogle Scholar
  90. Meyer F, Heilmeyer LMG, Haschke RM, Fischer EH (1970) Control of phosphorylase activity in the glycogen particle. Isolation and characterisation of the protein glycogen complex. J Biol Chem 245:6642–6648.PubMedGoogle Scholar
  91. Mo F, Jensen LH (1978) The crystal structure of a β-(1–4) linked disaccharide, α-N,N′-Diacetylchitobiose monohydrate. Acta Crystallogr B34:1562–1569.Google Scholar
  92. Monod J, Changeux JP, Wyman J (1965) On the nature of allosteric transitims: a plausible model. J Mol Biol 12:88–118.PubMedGoogle Scholar
  93. Moult J, Yonath A, Traub W, Smilansky A, Podjarny A, Rabionvich P, Saya A (1976) The structure of triclinic lysozyme at 2.5 Å resolution. J Mol Biol 100:179–195.PubMedGoogle Scholar
  94. Najmudin S (1984) The control and activity of Phosphorylase: crystallographic study of some metabolite analogues (Phosphate, Glucosamine 1-Phosphate and Adenosine 5′-O-Monothio-phosphate) binding to Phosphorylase b. Biochemistry. Part II. Thesis, University of Oxford.Google Scholar
  95. Nakano K, Fukui T (1986) The complete amino acid sequence of potato α-glucan phosphorylase. J Biol Chem 261:8230–8236.PubMedGoogle Scholar
  96. Nakano K, Hwang PK, Fletterick RJ (1986) Complete cDNA sequence for rabbit muscle glycogen phosphorylase. FEBS Lett 204:283–287.PubMedGoogle Scholar
  97. Narendra N, Seshadri TP, Viswamittra MA (1984) The structure of the disodium salt of glucose-1-phosphate hydrate. Acta Crystallogr C40:1338–1340.Google Scholar
  98. Oatley SJO (1973) Structural studies of biological macromolecules. Chemistry. Part II. Thesis, University of Oxford.Google Scholar
  99. Palm D, Goerl R, Burger KJ (1985) Evolution of catalytic and regulatory sites in phosphorylases. Nature 313:500–502.PubMedGoogle Scholar
  100. Pauling L (1946) Molecular architecture and biological reactions. Chem Eng News 24:1375–1377.Google Scholar
  101. Payan F, Maser R, Pierrot M, Frey M, Astier JP (1980) The three-dimensional structure of a-amylase from porcine pancreas at 5 Å resolution. Acta Crystallogr B36:416–421.Google Scholar
  102. Perkins SJ, Johnson LN, Machin PA, Phillips DC (1979) Crystal structures of hen egg-white lysozyme complexes with Gd(III) and Gd(III)-N-acetylglucosamine. Biochem J 181:21–36.PubMedGoogle Scholar
  103. Pflugrath JW, Weigand G, Huber R (1986) Crystal structure determination, refinement and molecular model of α-amylase inhibitor Hoe-467A. J Mol Biol 189:383–386.PubMedGoogle Scholar
  104. Philip G, Gringel G, Palm D (1982) Rabbit muscle phosphorylase derivatives with oligosaccharides covalently bound to the glycogen storage sites. Biochemistry 21:3043–3050.PubMedGoogle Scholar
  105. Phillips DC (1966) The three-dimensional structure of an enzyme molecule. Sci Am 215:78–90.PubMedGoogle Scholar
  106. Phillips DC (1986) Protein structure and function. Fifty years of the Patterson function. Oxford University Press, Oxford.Google Scholar
  107. Pincus MR, Scheraga HA (1981) Prediction of the three-dimensional structures of complexes of lysozyme with cell wall substrates. Biochemistry 20:3960–3965.PubMedGoogle Scholar
  108. Post CB, Brooks BR, Karplus M, Dobson CM, Artymiuk PJ, Cheetham JC, Phillips DC (1986) Molecular dynamics simultaneous of native and substrate-bound lysozyme. A study of the average structures and atomic fluctuations. J Mol Biol 190:455–479.PubMedGoogle Scholar
  109. Prager EM, Wilson AC, Arnheim N (1974) Widespread distribution of lysozyme g in egg-white of birds. J Biol Chem 249:7295–7297.PubMedGoogle Scholar
  110. Pulford WCA (1982) X-ray studies of enzyme action. Ph D thesis, University of Oxford.Google Scholar
  111. Quigley GJ, Saiko A, Marchessault RM (1970) Crystal and molecular structure of maltose monohydrate. J Am Chem Soc 92:5834–5839.Google Scholar
  112. Quiocho FA (1986) Carbohydrate binding proteins: Tertiary structures and protein sugar interactions. Annu Rev Biochem 55:287–315.PubMedGoogle Scholar
  113. Quiocho FA, Vyas NK (1984) Novel stereospecificity of the L-arabinose binding protein. Nature 310:381–386.PubMedGoogle Scholar
  114. Rees DA, Smith PJC (1975) Polysaccharide conformation Part IX. Monte Carlo calculation of conformational energies for disaccharides and comparison with experiment. J Chem Soc II: 836–840.Google Scholar
  115. Remington SJ, Anderson WF, Owen J, Ten Eyck LF, Grainger CT, Matthews BW (1978) Structure of the lysozyme from bacteriophage T4: an electron density map at 2.4 A resolution. J Mol Biol 118:81–98.PubMedGoogle Scholar
  116. Romero PA, Smith EE, Whelan WJ (1980) Glucosamines as a substitute for glucose in glycogen metabolism. Biochem Int 1:1–9.Google Scholar
  117. Rossmann MG, Moras D, Olsen KW (1974) Chemical and biological evolution of a nucleotide binding protein. Nature 250:194–199.PubMedGoogle Scholar
  118. Rupley JA, Butler L, Gerring M, Hartdegen FJ, Pacoraro R (1967) Studies on the enzymic activity of lysozyme, III. The binding of saccharides. Proc Natl Acad Sci USA 57:1088–1095.PubMedGoogle Scholar
  119. Saenger W (1979) Circular hydrogen bonds. Nature 279:343–344.Google Scholar
  120. Salton MRJ (1952) Cell wall of microccus lysodeikticus as the substrate of lysozyme. Nature 170:746–747.PubMedGoogle Scholar
  121. Salton MRJ, Ghuysen JM (1959) The structure of di-and tetra-saccharides released from cell walls by lysozyme and streptomyces F1 enzyme and the β(1–4) N-acetyl-hexosaminidase activity of these enzymes. Biochim Biophys Acta 36:552–554.PubMedGoogle Scholar
  122. Salton MRJ, Ghuysen JM (1960) Acetylhexosamine compounds enzymically released from Micrococcus Lysodeikticus cell walls. III. The structure of di-and tetra-saccharides released from cell walls by lysozyme and streptomyces F1 enzyme. Biochim Biophys Acta 45:355–363.PubMedGoogle Scholar
  123. Sansom MSP, Stuart DI, Acharya KR, Hajdu J, Mclaughlin PJ, Johnson LN (1985) Glycogen phosphorylase b — the molecular anatomy of a large regulatory enzyme. J Mol Struct 123:3–25.Google Scholar
  124. Sarma R, Bott R (1977) Crystallographic study of turkey egg-white lysozyme and its complex with a disaccharide. J Mol Biol 113:555–565.PubMedGoogle Scholar
  125. Schellman JA, Hawkes RB (1980) Thermodynamic stability of T4 variant lysozymes. In: Jaenicke R (ed) Protein folding. North-Holland Biomedical, Amsterdam, pp 331–334.Google Scholar
  126. Schellman JA, Lindorfer M, Hawkes RB, Gruter MG (1981) Mutations and protein stability. Biopolymers 20:1989–1999.PubMedGoogle Scholar
  127. Secemski II, Lienhard GE (1971) The role of strain in catalysis by lysozyme. J Am Chem Soc 93:3549–3550.PubMedGoogle Scholar
  128. Smith-Gill SJ, Rupley JA, Pincus MR, Carty PR, Scheraga HA (1984) Experimental identification of a theoretically predicted “left-sided” binding mode for (GlcNAc)6 in the active site of lysozyme. Biochemistry 23:993–997.PubMedGoogle Scholar
  129. Sotiroudis TG, Oikonomakos NG, Evangelopoulos AE (1978) Phosphorylase b covalently bound to glycogen. Eur J Biochem 88:573–581.PubMedGoogle Scholar
  130. Sprang S, Fletterick RJ (1979) The structure of glycogen phosphorylase a at 2.5 Å resolution. J Mol Biol 131:523–551.PubMedGoogle Scholar
  131. Sprang SR, Goldsmith EJ, Fletterick RG, Withers SG, Madsen NB (1982) Catalytic site of glycogen phosphorylase: structure of the T-state and specificity for α-D-glucose. Biochemistry 21:5364–5381.PubMedGoogle Scholar
  132. Steinrauf LK (1959) Preliminary x-ray data for some new crystalline forms of α-lactoglobulin and hen egg-white lysozyme. Acta Crystallogr 12:77.Google Scholar
  133. Stralfors P, Hiraga A, Cohen P (1985) The protein phosphatases involved in cellular regulation. Eur J Biochem 149:295–303.PubMedGoogle Scholar
  134. Street IP, Armstrong CR, Withers SG (1986) Hydrogen bonding and specificity. Fluorodeoxy sugars as probes of hydrogen bondong in the glycogen phosphorylase-glucose complex. Biochemistry 25:6021–6027.PubMedGoogle Scholar
  135. Sundanarajan PR, Rao VSR (1969) Studies on the helical conformations of amylose and possible interconversions. Biopolymers 8:313–323.Google Scholar
  136. Takagi T, Toda H, Isenura T (1971) Bacterial and mold amylases. In: Boyer PD (ed) The enzymes, 3rd edn, vol 5. Academic, New York, pp 235–271.Google Scholar
  137. Takusagawa F, Jacobson RA (1978) The crystal and molecular structure of α-maltose. Acta Crystallogr B 34:213–218.Google Scholar
  138. Tanaka I, Tanaka N, Ashida T, Kakudo M (1976) The crystal and molecular structure of phenyl-α-maltoside. Acta Crystallogr B 32:155–160.Google Scholar
  139. Thoma JA, Spradlin JE, Dygent S (1971) Plant and animal amylases. In: Boyer PD (ed) The enzymes. Academic, New York, pp 115–189.Google Scholar
  140. Titani K, Koide A, Hermann J, Ericsson LH, Kumar S, Wade RD, Walsh KA, Neurath M, Fischer EH (1977) Complete amino acid sequence of rabbit muscle glycogen phosphorylase. Proc Natl Acad Sci USA 74:4762–4777.PubMedGoogle Scholar
  141. Truschuit E, Frommer W, Junge B, Muller L, Schmidt D, Wingender W (1981) Chemistry and biochemistry of microbial α-glucosidase inhibitors. Angew Chem Int Ed Engl 20:744–761.Google Scholar
  142. Tsugita A (1971) Phage lysozyme and other lytic enzymes. In: Boyer PA (ed) The enzymes, vol 5. Academic, New York, pp 343–411.Google Scholar
  143. Wang JH, Shonka ML, Graves DJ (1965) Influence of carbohydrate on phosphorylase structure and activity I. Activation by preincubation with glycogen. Biochemistry 4:2295–2301.Google Scholar
  144. Wanson JC, Drochmans P (1968) Rabbit skeletal muscle glycogen. J Cell Biol 38:130–150.PubMedGoogle Scholar
  145. Weaver LH, Grutter MG, Remington SJ, Gray TM, Isaacs NW, Matthews BW (1985) Comparison of goose-type, chicken-type and phage-type lysozymes: changes in three-dimensional structure during evolution. J Mol Evol 21:97–111.Google Scholar
  146. Weber IT, Johnson LN, Wilson KS, Yeates DGR, Wild DL, Jenkins JA (1978) Crystallographic studies on the activity of glycogen phosphorylase b. Nature 274:433–437.PubMedGoogle Scholar
  147. Whelan WJ (1986) The initiation of glycogen synthesis. Bioessays 5:136–140.PubMedGoogle Scholar
  148. Withers SG, Sykes BD, Madsen NB, Kasvinsky PJ (1979) Identical structural changes induced in glycogen phosphorylase by two non-exclusive allosteric inhibitors. Biochemistry 18:5342–5348.PubMedGoogle Scholar
  149. Withers SG, Madsen NM, Sprang SR, Fletterick RJ (1982) Catalytic site of glycogen phosphorylase: structural changes during activation and mechanistic implications. Biochemistry 21:5372–5382.PubMedGoogle Scholar
  150. Wolfenden R (1969) Transition state analogues for enzyme catalysis. Nature 223:704–705.PubMedGoogle Scholar
  151. Wu HC, Sarko A (1978) The double helical structure of crystalline α-amylose. Carbohydr Res 61:27–40.Google Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1988

Authors and Affiliations

  • L. N. Johnson
    • 1
  • J. Cheetham
    • 1
  • P. J. McLaughlin
    • 1
  • K. R. Acharya
    • 1
  • D. Barford
    • 1
  • D. C. Phillips
    • 1
  1. 1.Laboratory of Molecular BiophysicsOxfordUK

Personalised recommendations