Solution structure of family 21 carbohydrate-binding module from Rhizopus oryzae glucoamylase

Biochemical Journal

Volumn 403, Issue 1, 2007, Pages 21-30

  Liu, Yu Nan ^a   Lai, Yen Ting ^a   Chou, Wei I ^a   Chang, Margaret Dah Tsyr ^a   Lyu, Ping Chiang ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

Carbohydrate active enzyme; Carbohydrate binding module (CBM); Glucoamylase; Rhizopus oryzae; Solution structure; Starch binding domain (SBD)

Indexed keywords

BINDING SITES; CARBOHYDRATES; GLUCOSE; LIGANDS; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOSACCHARIDES;

CARBOHYDRATE BINDING MODULE (CBM); CARBOHYDRATE-ACTIVE ENZYMES; GLUCOAMYLASE; RHIZOPUS ORYZAES; SOLUTION STRUCTURE; STARCH BINDING DOMAIN (SBD);

ENZYME KINETICS;

BETA CYCLODEXTRIN; CARBOHYDRATE BINDING PROTEIN; DOCKING PROTEIN; GLUCAN 1,4 ALPHA GLUCOSIDASE; OLIGOSACCHARIDE;

ARTICLE; ASPERGILLUS NIGER; CONTROLLED STUDY; LIGAND BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RHIZOPUS ORYZAE; STRUCTURE ANALYSIS;

BINDING SITES; CALORIMETRY; CARBOHYDRATE CONFORMATION; CARBOHYDRATES; CLONING, MOLECULAR; GLUCAN 1,4-ALPHA-GLUCOSIDASE; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; RHIZOPUS; SOLUTIONS; STARCH;

ASPERGILLUS NIGER; RHIZOPUS ORYZAE;

EID: 34147136166     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061312     Document Type: Article

References (60)

1. Varki, A., Cummings, R., Esko, J., Freeze, H., Hart, G. and Marth, J. (1999) Essentials of Glycobiology, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
2. Kelly, G. S. (1998) The role of glucosamine sulfate and chondroitin sulfates in the treatment of degenerative joint disease. Altern. Med. Rev. 3, 27-39
3. Crossman, L. and Dow, J. M. (2004) Biofilm formation and dispersal in Xanthomonas campestris. Microbes Infect. 6, 623-629
4. Nagai, Y. (1998) Cell regulatory function of glycosphingolipids: carbohydrate recognition and biosignaling. Pure Appl. Chem. 70, 49-53
5. Gessler, K., Uson, I., Takaha, T., Krauss, N., Smith, S. M., Okada, S., Sheldrick, G. M. and Saenger, W. (1999) V-amylose at atomic resolution: X-ray structure of a cycloamylose with 26 glucose residues (cyclomaltohexaicosaose). Proc. Natl. Acad. Sci. U.S.A. 96, 4246-4251
6. Smith, A. M., Denyer, K. and Martin, C. R. (1995) What controls the amount and structure of starch in storage organs? Plant Physiol. 107, 673-677
7. Henrissat, B., Coutinho, P. M. and Davies, G. J. (2001) A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol. Biol. 47, 55-72
8. Davies, G. J. and Henrissat, B. (2002) Structural enzymology of carbohydrate-active enzymes: implications for the post-genomic era. Biochem. Soc. Trans. 30, 291-297
9. Chou, W. I., Pai, T. W., Liu, S. H., Hsiung, B. K. and Chang, M. D. (2006) The family 21 carbohydrate binding module of glucoamylase from Rhizopus oryzae consists of two sites playing distinct roles in ligand binding. Biochem. J. 396, 469-477
10. Takahashi, T., Kato, K., Ikegami, Y. and Irie, M. (1985) Different behavior towards raw starch of three forms of glucoamylase from a Rhizopus sp. J. Biochem. (Tokyo) 3, 663-671
11. Dent, P., Lavoinne, A., Nakielny, S., Caudwell, F. B., Watt, P. and Cohen, P. (1990) The molecular mechanism by which insulin stimulates glycogen synthesis in mammalian skeletal muscle. Nature 348, 302-308
12. Xia, J., Scherer, S. W., Cohen, P. T., Majer, M., Xi, T., Norman, R. A., Knowler, W. C., Bogardus, C. and Prochazka, M. (1998) A common variant in PPP1R3 associated with insulin resistance and type 2 diabetes. Diabetes 47, 1519-1524
13. Armstrong, C. G., Doherty, M. J. and Cohen, P. T. (1998) Identification of the separate domains in the hepatic glycogen-targeting subunit of protein phosphatase 1 that interact with phosphorylase a, glycogen and protein phosphatase 1. Biochem. J. 336, 699-704
14. Giardina, T., Gunning, A. P., Juge, N., Faulds, C. B., Furniss, C. S., Svensson, B., Morris, V. J. and Williamson, G. (2001) Both binding sites of the starch-binding domain of Aspergillus niger glucoamylase are essential for inducing a conformational change in amylose. J. Mol. Biol. 313, 1149-1159
15. Southall, S. M., Simpson, P. J., Gilbert, H. J., Williamson, G. and Williamson, M. P. (1999) The starch-binding domain from glucoamylase disrupts the structure of starch. FEBS Lett. 447, 58-60
16. Bolam, D. N., Ciruela, A., McQueen-Mason, S., Simpson, P., Williamson, M. P., Rixon, J. E., Boraston, A., Hazlewood, G. P. and Gilbert, H. J. (1998) Pseudomonas cellulose-binding domains mediate their effects by increasing enzyme substrate proximity. Biochem. J. 331, 775-781
17. Boraston, A. B., Bolam, D. N., Gilbert, H. J. and Davies, G. J. (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382, 769-781
18. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. and Struhl, K. (1995) Short Protocols In Molecular Biology, Wiley, New York
19. Grzesiek, S. and Bax, A. (1992) Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein. J. Magn. Beson. 96, 432-440
20. Schleucher, J., Sattler, M. and Griesinger, C. (1993) Coherence selection by gradients without signal attenuation: application to the three-dimensional HNCO experiment. Angew. Chem. Int. Ed. Engl. 32, 1489-1491
21. 2O saturation. J. Magn. Reson. Ser. A 109, 129-133
22. Wittekind, M. and Mueller, L. (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the α- and β-carbon resonances in proteins. J. Magn. Reson. Ser. B 101, 201-205
23. 15N- enriched proteins. J. Biomol. NMR 3, 185-204
24. Muhandiram, D. R. and Kay, L. E. (1994) Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity. J. Magn. Reson. Ser. B 103, 203-216
25. Cavanagh, J., Fairbrother, W. J., Palmer, G. A. and Skelton, N. J. (1996) Protein NMR Spectroscopy, Academic Press Inc., New York
26. 13C-labeled proteins via scalar couplings. J. Am. Chem. Soc. 115, 11054-11055
27. Piotto, M., Saudek, V. and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2, 661-665
28. Sklenar, V., Piotto, M. and Saudek, V. (1993) Gradient-tailor water suppression for 1H-15N HSQC experiments optimized to retain full sensitivity. J. Magn. Reson. Ser. A 102, 241-245
29. Palmer, G. A., Cavanagh, J., Wright, P. E. and Rance, M. (1991) Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy. J. Magn. Reson. 93, 151-170
30. Kay, L. E., Keifer, P. and Saarinen, T. (1992) Pure absorption gradient enhanced heternuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665
31. Derome, E. A. and Williamson, M. P. (1990) Rapid-pulsing artifacts in double-quantum-filtered COSY. J. Magn. Reson. 88, 177-185
32. Cordier, F. and Grzesiek, S. (1999) Direct observation of hydrogen bonds in proteins by interresidue 3HJNC′ scalar couplings. J. Am. Chem. Soc. 121, 1601-1602
33. Cornilescu, G., Delaglio, F. and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302
34. Reference deleted
35. Brunger, A. T., Adams, P. D., Clore, G. M., Delano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S. et al. (1998) Acta Crystallogr. Sect. D. Biol. Crystallogyr. 54, 905-921
36. Nilges, M., Macias, M. J., O'Donoghue, S. I. and Oschkinat, H. (1997) Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from β-spectrin. J. Mol. Biol. 269, 408-422
37. Nilges, M., Clore, G. M. and Gronenborn, A. M. (1988) Determination of three-dimensional structures of proteins from interproton distance data by dynamical simulated annealing from a random array of atoms. Circumventing problems associated with folding. FEBS Lett. 239, 129-136
38. Linge, J. P., Williams, M. A., Spronk, C. A., Bonvin, A. M. and Nilges, M. (2003) Refinement of protein structures in explicit solvent. Proteins 50, 496-506
39. Laskowski, R. A., MacArthur, M. W., Moss, D. S. and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
40. Sorimachi, K., Jacks, A. J., Le Gal-Coeffet, M. F., Williamson, G., Archer, D. B. and Williamson, M. P. (1996) Solution structure of the granular starch binding domain of glucoamylase from Aspergillus niger by nuclear magnetic resonance spectroscopy. J. Mol. Biol. 259, 970-987
41. Abe, A., Tonozuka, T., Sakano, Y. and Kamitori, S. (2004) Complex structures of Thermoactinomyces vulgaris R-47 α-amylase 1 with malto-oligosaccharides demonstrate the role of domain N acting as a starch-inding domain. J. Mol. Biol. 335, 811-822
42. Boraston, A. B., Healey, M., Klassen, J., Ficko-Blean, E., Lammerts van Bueren, A. and Law, V. (2006) A structural and functional analysis of α-glucan recognition by family 25 and 26 carbohydrate-binding modules reveals a conserved mode of starch recognition. J. Biol. Chem. 281, 587-598
43. Mikami, B., Iwamoto, H., Malle, D., Yoon, H. J., Demirkan-Sarikaya, E., Mezaki, Y. and Katsuya, Y. (2006) Crystal structure of pullulanase: evidence for parallel binding of oligosaccharides in the active site. J. Mol. Biol. 359, 690-707
44. Grzesiek, S., Bax, A., Clore, G. M., Gronenborn, A. M., Hu, J. S., Kaufman, J., Palmer, I., Stahl, S. J. and Wingfield, P. T. (1996) The solution structure of HIV-1 Nef reveals an unexpected fold and permits delineation of the binding surface for the SH3 domain of Hck tyrosine protein kinase. Nat. Struct. Biol. 3, 340-345
45. Garrett, D. S., Seok, Y. J., Peterkofsky, A., Clore, G. M. and Gronenborn, A. M. (1997) Identification by NMR of the binding surface for the histidine-containing phosphocarrier protein HPr on the N-terminal domain of enzyme I of the Escherichia coli phosphotransferase system. Biochemistry 36, 4393-4398
46. Dehner, A., Furrer, J., Richter, K., Schuster, I., Buchner, J. and Kessler, H. (2003) NMR chemical shift perturbation study of the N-terminal domain of Hsp90 upon binding of ADP, AMP-PNP, geldanamycin, and radicicol. ChemBioChem 4, 870-677
47. Luttgen, H., Robelek, R., Muhlberger, R., Diercks, T., Schuster, S. C., Kohler, P., Kessler, H., Bacher, A. and Richter, G. (2002) Transcriptional regulation by antitermination. Interaction of RNA with NusB protein and NusB/NusE protein complex of Escherichia coli. J. Mol. Biol. 316, 875-885
48. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K. and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J. Comput. Chem. 19, 1639-1662
49. Moseley, H. N., Sahota, G. and Montelione, G. T. (2004) Assignment validation software suite for the evaluation and presentation of protein resonance assignment data. J. Biomol. NMR 28, 341-355
50. Rocchia, W., Alexov, D. and Honig, B. (2001) Extending the applicability of the nonlinear Poisson-Boltzmann equation: multiple dielectric constants and multivalent ions. J. Phys. Chem. B 105, 6507-6514
51. Machovic, M., Svensson, B., MacGregor, E. A. and Janecek, S. (2005) A new clan of CBM families based on bioinformatics of starch-binding domains from families CBM20 and CBM21. FEBS J. 272, 5497-5513
52. Seidel, 3rd, R. D., Amor, J. C., Kahn, R. A. and Prestegard, J. H. (2004) Structural perturbations in human ADP ribosylation factor-1 accompanying the binding of phosphatidylinositides. Biochemistry 43, 15393-15403
53. Williamson, M. P., Le Gal-Coeffet, M. F., Sorimachi, K., Furniss, C. S., Archer, D. B. and Williamson, G. (1997) Function of conserved tryptophans in the Aspergillus niger glucoamylase 1 starch binding domain. Biochemistry 36, 7535-7539
54. Ponyi, T., Szabo, L., Nagy, T., Orosz, L., Simpson, P. J., Williamson, M. P. and Gilbert, H. J. (2000) Trp22, Trp24, and Tyr8 play a pivotal role in the binding of the family 10 cellulose-binding module from Pseudomonas xylanase A to insoluble ligands. Biochemistry 39, 985-991
55. Xie, H., Bolam, D. N., Nagy, T., Szabo, L., Cooper, A., Simpson, P. J., Lakey, J. H., Williamson, M. P. and Gilbert, H. J. (2001) Role of hydrogen bonding in the interaction between a xylan binding module and xylan. Biochemistry 40, 5700-5707
56. Guan, L., Hu, Y. and Kaback, H. R. (2003) Aromatic stacking in the sugar binding site of the lactose permease. Biochemistry 42, 1377-1382
57. Pell, G., Williamson, M. P., Walters, C., Du, H., Gilbert, H. J. and Bolam, D. N. (2003) Importance of hydrophobic and polar residues in ligand binding in the family 15 carbohydrate-binding module from Cellvibrio japonicus Xyn10C. Biochemistry 42, 9316-9323
58. Goto, M., Semimaru, T., Furukawa, K. and Hayastrida, S. (1994) Analysis of the raw starch-binding domain by mutation of a glucoamylase from Aspergillus awamori var. kawachi expressed in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 60, 3926-3930
59. Katsuya, Y., Mezaki, Y., Kubota, M. and Matsuura, Y. (1998) Three-dimensional structure of Pseudomonas isoamylase at 2.2 Å resolution. J. Mol. Biol. 281, 885-897
60. 8-barrel-like fold in the multidomain protein. Protein Sci. 8, 2570-2579