Parallel substrate binding sites in a β-agarase suggest a novel mode of action on double-helical agarose

Structure

Volumn 12, Issue 4, 2004, Pages 623-632

  Allouch, Julie ^a   Helbert, William ^b   Henrissat, Bernard ^a   Czjzek, Mirjam ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AGAROSE; BACTERIAL PROTEIN; BETA AGARASE; CARBOHYDRATE BINDING PROTEIN; ENZYME; GALACTOSE; MUTANT PROTEIN; OLIGOSACCHARIDE; POLYSACCHARIDE; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL WALL; BINDING SITE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME BINDING; GENE MUTATION; GRAM NEGATIVE BACTERIUM; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RED ALGA; ZOBELLIA GALACTANIVORANS;

BINDING SITES; CATALYTIC DOMAIN; CRYSTALLIZATION; GLYCOSIDE HYDROLASES; GRAM-NEGATIVE BACTERIA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEPHAROSE;

ALGAE; BACTERIA (MICROORGANISMS); NEGIBACTERIA; RHODOPHYTA; ZOBELLIA GALACTANIVORANS;

EID: 1842554929     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2004.02.020     Document Type: Article

References (57)

1. Albenne C., Skov L.K., Mirza O., Gajhede M., Feller G., D'Amico S., Andre G., Potocki-Veronese G., Van Der Veen B.A., Monsan P.et al. Molecular basis of the amylose-like polymer formation catalyzed by Neisseria polysaccharea amylosucrase. J. Biol. Chem. 279:2004;726-734.
2. Allouch J., Jam M., Helbert W., Barbeyron T., Kloareg B., Henrissat B., Czjzek M. The three-dimensional structures of two β-agarases. J. Biol. Chem. 278:2003;47171-47180.
3. Arnott S., Fulmer A., Scott W.E., Dea I.C., Moorhouse R., Rees D.A. The agarose double helix and its function in agarose gel structure. J. Mol. Biol. 90:1974;269-284.
4. 13C-n.m.r. spectroscopic analysis of agar, kappa-carrageenan and iota-carrageenan. Carbohydr. Res. 60:1978;C1-C3.
5. Bourne Y., Henrissat B. Glycoside hydrolases and glycosyltransferases. families and functional modules Curr. Opin. Struct. Biol. 11:2001;593-600.
6. Burmeister W.P., Cottaz S., Driguez H., Iori R., Palmieri S., Henrissat B. The crystal structures of Sinapis alba myrosinase and a covalent glycosyl-enzyme intermediate provide insights into the substrate recognition and active-site machinery of an S-glycosidase. Structure. 5:1997;663-675.
7. CCP4 The (Collaborative Computational Project Number 4) CCP4 suite. programs for protein crystallography Acta Crystallogr. D. 50:1994;760-763.
8. Czjzek M., Cicek M., Zamboni V., Bevan D.R., Henrissat B., Esen A. The mechanism of substrate (aglycone) specificity in beta-glucosidases is revealed by crystal structures of mutant maize beta-glucosidase-DIMBOA, -DIMBOAGlc, and -dhurrin complexes. Proc. Natl. Acad. Sci. USA. 97:2000;13555-13560.
9. Davies G.J., Tolley S.P., Henrissat B., Hjort C., Schulein M. Structures of oligosaccharide-bound forms of the endoglucanase V from Humicola insolens at 1.9 Å resolution. Biochemistry. 34:1995;16210-16220.
10. Davies G.J., Wilson K.S., Henrissat B. Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321:1997;557-559.
11. Davies G.J., Mackenzie L., Varrot A., Dauter M., Brzozowski A.M., Schulein M., Withers S.G. Snapshots along an enzymatic reaction coordinate. analysis of a retaining beta-glycoside hydrolase Biochemistry. 37:1998;15280-15287.
12. De Ruiter G.A., Rudolph B. Carrageenan biotechnology. Trends Food Sci. Technol. 8:1997;389-395.
13. Delagoutte E., von Hippel P.H. Helicase mechanisms and the coupling of helicases within macromolecular machines. Part I. structures and properties of isolated helicases Q. Rev. Biophys. 35:2002;431-478.
14. Ducros V.M., Zechel D.L., Murshudov G.N., Gilbert H.J., Szabo L., Stoll D., Withers S.G., Davies G.J. Substrate distortion by a beta-mannanase. snapshots of the Michaelis and covalent-intermediate complexes suggest a B(2,5) conformation for the transition state Angew. Chem. Int. Ed. Engl. 41:2002;2824-2827.
15. Ducros V.M., Tarling C.A., Zechel D.L., Brzozowski A.M., Frandsen T.P., von Ossowski I., Schulein M., Withers S.G., Davies G.J. Anatomy of glycosynthesis. structure and kinetics of the Humicola insolens Cel7B E197A and E197S glycosynthase mutants Chem. Biol. 10:2003;619-628.
16. Gill J., Rixon J.E., Bolam D.N., McQueen-Mason S., Simpson P.J., Williamson M.P., Hazlewood G.P., Gilbert H.J. The type II and X cellulose-binding domains of Pseudomonas xylanase A potentiate catalytic activity against complex substrates by a common mechanism. Biochem. J. 342:1999;473-480.
17. Guenet J.M., Brulet A., Rochas C. Agarose chain conformation in the sol state by neutron scattering. Int. J. Biol. Macromol. 15:1993;131-132.
18. 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. Crystal structure of the mutant D52S hen egg white lysozyme with an oligosaccharide product. J. Mol. Biol. 243:1994;856-872.
19. Haggett N.M.W., Hoffmann R.A., Howlin B.J., Webb G.A. Molecular modelling of six-ring agarose chains. effects of explicit and implicit solvent J. Mol.Model. 3:1997;301-310.
20. Hahn M., Olsen O., Politz O., Borriss R., Heinemann U. Crystal structure and site-directed mutagenesis of Bacillus macerans endo-1,3-1,4-beta-glucanase. J. Biol. Chem. 270:1995;3081-3088. a.
21. Hahn M., Pons J., Planas A., Querol E., Heinemann U. Crystal structure of Bacillus licheniformis 1,3-1,4-beta-D-glucan 4-glucanhydrolase at 1.8 Å resolution. FEBS Lett. 374:1995;221-224. b.
22. Henrissat B., Davies G.J. Glycoside hydrolases and glycosyltransferases. Families, modules, and implications for genomics. Plant Physiol. 124:2000;1515-1519.
23. Imberty A. Oligosaccharide structures. theory versus experiment Curr. Opin. Struct. Biol. 7:1997;617-623.
24. Jahn, M., Stoll, D., Warren, R.A., Szabo, L., Singh, P., Gilbert, H.J., Ducros, V.M., Davies, G.J., and Withers, S.G. (2003). Expansion of the glycosynthase repertoire to produce defined manno-oligosaccharides. Chem. Commun. (Camb.), 1327-1329.
25. Jimenez-Barbero J., Bouffar-Roupe C., Rochas C., Perez S. Modelling studies of solvent effects on the conformational stability of agarobiose and neoagarobiose and their relationship to agarose. Int. J. Biol. Macromol. 11:1989;265-272.
26. Johansson P., Denman S., Brumer H., Kallas A.M., Henriksson H., Bergfors T., Teeri T.T., Jones T.A. Crystallization and preliminary X-ray analysis of a xyloglucan endotransglycosylase from Populus tremula x tremuloides. Acta Crystallogr. D. 59:2003;535-537.
27. Juncosa M., Pons J., Dot T., Querol E., Planas A. Identification of active site carboxylic residues in Bacillus licheniformis 1,3-1,4-beta-D-glucan 4-glucanhydrolase by site-directed mutagenesis. J. Biol. Chem. 269:1994;14530-14535.
28. Kadziola A., Abe J., Svensson B., Haser R. Crystal and molecular structure of barley alpha-amylase. J. Mol. Biol. 239:1994;104-121.
29. Kadziola A., Sogaard M., Svensson B., Haser R. Molecular structure of a barley alpha-amylase-inhibitor complex. implications for starch binding and catalysis J. Mol. Biol. 278:1998;205-217.
30. Keitel T., Simon O., Borriss R., Heinemann U. Molecular and active-site structure of a Bacillus 1,3-1,4-beta-glucanase. Proc. Natl. Acad. Sci. USA. 90:1993;5287-5291.
31. Kloareg B., Quatrano R.S. Structure of the cell walls of marine algae and ecophysiological function of the matrix polysaccharides. Oceanogr. Mar. Biol. Annu. Rev. 26:1988;259-315.
32. Kogelberg H., Soli D., Jimenez-Barbero J. New structural insights into carbohydrate-protein interactions from NMR spectroscopy. Curr. Opin. Struct. Biol. 13:2003;646-653.
33. Koshland D.E. Stereochemistry and the mechanism of enzymatic reactions. Biol. Rev. Camb. Philos. Soc. 28:1953;416-436.
34. Kraulis P.J. Molscript. a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24:1991;946-950.
35. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. Procheck. a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26:1993;283-291.
36. MacKenzie L.F., Sulzenbacher G., Divne C., Jones T.A., Woldike H.F., Schulein M., Withers S.G., Davies G.J. Crystal structure of the family 7 endoglucanase I (Cel7B) from Humicola insolens at 2.2 A resolution and identification of the catalytic nucleophile by trapping of the covalent glycosyl-enzyme intermediate. Biochem. J. 335:1998;409-416.
37. Michel G., Chantalat L., Duee E., Barbeyron T., Henrissat B., Kloareg B., Dideberg O. The kappa-carrageenase of P. carrageenovora features a tunnel-shaped active site. a novel insight in the evolution of Clan-B glycoside hydrolases Structure. 9:2001;513-525.
38. Navaza J. AmoRe. an automated package for molecular replacement Acta Crystallogr. A. 50:1994;157-163.
39. Notenboom V., Birsan C., Nitz M., Rose D.R., Warren R.A., Withers S.G. Insights into transition state stabilization of the beta-1,4-glycosidase Cex by covalent intermediate accumulation in active site mutants. Nat. Struct. Biol. 5:1998;812-818.
40. Numao S., Kuntz D.A., Withers S.G., Rose D.R. Insights into the mechanism of drosophila melanogaster Golgi α-mannosidase through the structural analysis of covalent reaction intermediates. J. Biol. Chem. 278:2003;48074-48083.
41. Perrakis A., Sixma T.K., Wilson K.S., Lamzin V.S. wARP. improvement and extension of crystallographic phases by weightedaveraging of multiple-refined dummy atomic models Acta Crystallogr D. 53:1997;448-455.
42. Potin P., Richard C., Rochas C., Kloareg B. Purification and characterization of the alpha-agarase from Alteromonas agarlyticus (Cataldi) comb. nov., strain GJ1B. Eur. J. Biochem. 214:1993;599-607.
43. Robert X., Haser R., Gottschalk T.E., Ratajczak F., Driguez H., Svensson B., Aghajari N. The structure of barley alpha-amylase isozyme 1 reveals a novel role of domain C in substrate recognition and binding. a pair of sugar tongs Structure. 11:2003;973-984.
44. 13C N.M.R.-spectroscopic investigation of agarose oligomers. Carbohydr. Res. 148:1986;199-207.
45. Roussel, A., and Cambillau, C. (1991). TURBO-FRODO program. In Silicon Graphics Geometry Partners Directory 88. (Mountain View, CA: Silicon Graphics).
46. Skov L.K., Mirza O., Sprogoe D., Dar I., Remaud-Simeon M., Albenne C., Monsan P., Gajhede M. Oligosaccharide and sucrose complexes of amylosucrase. Structural implications for the polymerase activity. J. Biol. Chem. 277:2002;47741-47747.
47. Sorimachi K., Le Gal-Coeffet M.F., Williamson G., Archer D.B., Williamson M.P. Solution structure of the granular starch binding domain of Aspergillus niger glucoamylase bound to beta-cyclodextrin. Structure. 5:1997;647-661.
48. Southall S.M., Simpson P.J., Gilbert H.J., Williamson G., Williamson M.P. The starch-binding domain from glucoamylase disrupts the structure of starch. FEBS Lett. 447:1999;58-60.
49. Sulzenbacher G., Driguez H., Henrissat B., Schülein M., Davies G.J. Structure of the Fusarium oxysporum endoglucanase I with a nonhydrolyzable substrate analogue. substrate distortion gives rise to the preferred axial orientation for the leaving group Biochemistry. 35:1996;15280-15287.
50. Tews I., Perrakis A., Oppenheim A., Dauter Z., Wilson K.S., Vorgias C.E. Bacterial chitobiase structure provides insight into catalytic mechanism and thes basis of Tay-Sachs disease. Nat. Struct. Biol. 3:1996;638-648.
51. Tomme P., Driver D.P., Amandoron E.A., Miller R.C. Jr., Antony R., Warren J., Kilburn D.G. Comparison of a fungal (family I) and bacterial (family II) cellulose-binding domain. J. Bacteriol. 177:1995;4356-4363.
52. van Aalten D.M.F., Komander D., Synstad B., Gaseidnes S., Peter M.G., Eijsink V.G.H. Strutcural insights into the catalytic mechanism of a family 18 exo-chitinase. Proc. Natl. Acad. Sci. USA. 98:2001;8979-8984.
53. Varrot A., Davies G.J. Direct experimental observation of the hydrogen-bonding network of a glycosidase along its reaction coordinate revealed by atomic resolution analyses of endoglucanase Cel5A. Acta Crystallogr D. 59:2003;447-452.
54. Varrot A., Frandsen T., Driguez H., Davies G. Structure of the Humicola insolens cellobiohydrolase Cel6A D416A mutant in complex with a non-hydrolysable substrate analogue, methyl-cellobiosyl-4-thio-beta- cellobioside. Acta Crystallogr D. 58:2002;2201-2204.
55. Vocadlo D.J., Davies G.J., Laine R., Withers S.G. Catalysis by hen egg white lysozyme proceeds via a covalent intermediate. Nature. 412:2001;835-838.
56. Wallace A.C., Laskowski R.A., Thornton J.M. Ligplot. a program to generate schematic diagrams of protein-ligand interactions Protein Eng. 8:1995;127-134.
57. White A., Tull D., Johns K., Withers S.G., Rose D.R. Crystallographic observation of a covalent catalytic intermediate in a beta-glycosidase. Nat. Struct. Biol. 3:1996;149-154.