Involvement of individual subsites and secondary substrate binding sites in multiple attack on amylose by barley α-amylase

Biochemistry

Volumn 44, Issue 6, 2005, Pages 1824-1832

  Kramhøft, Birte ^a,b   Bak Jensen, Kristian Sass ^a,e   Mori, Haruhide ^a,f   Juge, Nathalie ^c   Nøhr, Jane ^d,g   Svensson, Birte ^a,b  

^a CARLSBERG LABORATORY   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^e MERCK RESEARCH LABORATORIES   (United States)

^f HOKKAIDO UNIVERSITY   (Japan)

^g Invitrogen A/S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; BINDING ENERGY; GLUCOSE; HYDROLYSIS; MUTAGENESIS; STARCH; SUBSTRATES;

BINDING CLEFT; DEGREE OF MULTIPLE ATTACKS; OLIGOSACCHARIDE PRODUCT; STARCH BINDING DOMAIN;

ENZYMES;

AMYLASE; AMYLOSE; GLUCAN 1,4 ALPHA GLUCOSIDASE; HYBRID PROTEIN; OLIGOSACCHARIDE;

ARTICLE; ASPERGILLUS NIGER; BINDING SITE; CATALYSIS; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; HYDROLYSIS; MUTANT; NONHUMAN; PRIORITY JOURNAL;

ALPHA-AMYLASE; AMYLOSE; BINDING SITES; GLUCANS; GLUCOSE; HORDEUM; HYDROLYSIS; ISOENZYMES; KINETICS; MALTOSE; OLIGOSACCHARIDES; PLANT PROTEINS; SUBSTRATE SPECIFICITY; TRISACCHARIDES; VARIATION (GENETICS);

ASPERGILLUS NIGER; HORDEUM VULGARE SUBSP. VULGARE;

EID: 13544266212     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048100v     Document Type: Article

References (52)

1. Bailey, J. M., and French, D. (1956) The significance of multiple reactions in enzyme-polymer systems, J. Biol. Chem. 226, 1-14.
2. Robyt, J. F., and French, D. (1967) Multiple attack hypothesis of α-amylase action: action of porcine pancreatic, human salivary, and Aspergillus oryzae α-amylases, Arch. Biochem. Biophys. 122, 8-16.
3. Nakatani, H. (1997) Monte Carlo simulation of multiple attack mechanism of β-amylase catalyzed reaction, Biopolymers 42, 831-836.
4. French, D. (1981) Amylases: Enzymatic mechanisms, Basic Life Sci. 18, 151-182.
5. Irwin, D., Shin, D.-H., Zhang, S., Barr, B. K., Sakon, J., Karplus, P. A., and Wilson, D. B. (1998) Role of the catalytic domain and two cellulose binding domains of Thermospora fusca E4 in cellulose hydrolysis, J. Bacteriol. 180, 1709-1714.
6. Pagès, S., Kester, H. C. M., Visser, J., and Benen, J. A. E. (2001) Changing a single amino acid residue switches processive and nonprocessive behaviour of Aspergillus niger endopolygalacturonase I and II, J. Biol. Chem. 276, 33652-33656.
7. Breyer, W. A., and Matthews, B. W. (2001) A structural basis for processivity, Protein Sci. 10, 1699-1711.
8. Mazur, A. K., and Nakatani, H. (1993) Multiple attack mechanism in the porcine pancreatic α-amylase hydrolysis of amylose and amylopectin, Arch. Biochem. Biophys. 306, 29-38.
9. 2+ on the degree of multiple attack exhibited by mesophilic and thermophilic α-amylases, Progress in Biotechnology 15, (Ballasteros, A., Plou, F. J., Iborra, J. L., and Hailing, P. J.,Eds) pp 343-347, Elsevier, Amsterdam.
10. Irwin, D. C., Spezio, M., Walker, L. P., and Wilson, D. B. (1993) Activity studies of eight purified cellulases: specificity, synergism, and binding domain effects, Biotechnol. Bioeng. 42, 1002-1013.
11. Zang, S., Irwin, D. C., and Wilson, D. B. (2000) Site-directed mutation of noncatalytic residues of Thermobifida fusca exocellulase Ce16B, Eur. J. Biochem. 267, 3101-3115.
12. Uchiyama, T., Katouno, F., Nikaidou, N., Nonaka, T., Sugiyama, J., and Watanabe, T. (2001) Role of the exposed aromatic residues in crystalline chitin hydrolysis by chitinase A from Serratia marcescens 2170, J. Biol. Chem. 276, 41346-41349.
13. Kadziola, A., Søgård, M., Svensson, B., and Haser, R. (1998) Molecular structure of a barley α-amylase inhibitor complex: implications for starch binding and catalysis, J. Mol. Biol. 278, 205-217.
14. Koivula, A., Kinnari, T., Harjunpää, V., Ruohonen, L., Teleman, A., and Teeri, T. T. (1998) Tryptophan 272: an essential determinant of crystalline cellulase degradation by Trichoderma reesei cellobiohydrolase Ce16A, FEES Lett. 428, 341-346.
15. Robert, X., Haser, R., Svensson, B., and Aghajari, N. (2002) Comparison of crystal structures of barley α-amylase 1 and 2: implications for isozyme differences in stability and activity. Biologia 57 (Suppl. 11), 59-70.
16. Koukiekolo, R., Desseaux, V., Moreau, Y., Marchis-Mouren, G., and Santimone, M. (2001) Mechanism of porcine pancreatic alpha-amylase. Inhibition of amylose and maltopentaose hydrolysis by alpha-, beta-, and gamma-cyclodextrins, Eur. J. Biochem. 268. 841-848.
17. Ji, Q., Winken, J. P., Suurs, L. C., and Visser, R. G. (2003) Microbial starch-binding domains as a tool for targeting proteins to granules during starch biosynthesis, Plant Mol. Biol. 51, 789-801.
18. André, G., Buléon, A., Haser, R., and Tran, V. (1999) Amylose chain behaviour in an interacting context III. Complete occupancy of the barley amylase cleft and comparison with biochemical data, Biopolymers 50, 751-762.
19. Varrot, A., Frandsen, T. P., von Ossowski, I., Boyer, V., Cottaz, S., Driguez, H., Schülein, M., and Davies, G. J. (2003) Structural basis of ligand binding and processivity in cellobiohydrolase Ce16A from Humicola insolens, Structure 11, 855-864.
20. MacGregor, E. A., Janeček, Š., and Svensson, B. (2001) Relationship of sequence and structure to specificity in the α-amylase family of enzymes, Biochim. Biophys. Acta 1546, 1-20.
21. Henrissat, B., and Coutinho, P. M. Carbohydrate active enzymes, http://afmb.cnrs-mrs.fr/CAZY/index.html.
22. Janeček, S. (2000) Structural features and evolutionary relationships in the alpha-amylase family, in Glycoenzymes (Ohnishi, M., Aayashi, T., Ishima, S., and Kuriki, T., Eds) pp 19-54, The Japanese Scientific Societies Press, Tokyo.
23. Mori, H., Bak-Jensen, K. S., and Svensson, B. (2002) Barley α-amylase Met53 situated at the high-affinity subsite -2 belongs to a substrate binding motif in the β→α loop 2 of the catalytic (β/α)8-barrel and is critical for activity and substrate specificity, Eur. J. Biochem. 269, 5377-5390.
24. Robyt, J. F., and French, D. (1970) The action pattern of porcine pancreatic α-amylase in relationship to the substrate binding site of the enzyme, J. Biol. Chem. 245, 3917-3927.
25. Ajandouz, E. H., Abe, J., Svensson, B., and Marchis-Mouren, G. (1992) Barley malt α-amylase. Purification, action pattern and subsite mapping of isozyme 1 and two members of the isozyme 2 subfamily using p-nitrophenylated maltooligosaccharide substrates, Biochim. Biophys. Acta 1159, 193-202.
26. Kandra, L., Gyémánt, G, Remenyik, J., Hovánski, G., and Lipták, A. (2002) Action pattern and subsite mapping of Bacillus licheniformis α-amylase (BLA) with modified maltooligosaccharide substrates, FEBS Lett. 518, 79-82.
27. Petukhov, M. G., and Mazur, K. (1992) Modelling of possible methods of substrate binding in the active site of α-amylase from Aspergillus oryzae, Mol. Biol. 26, 292-299.
28. Dutzler, R., Schirmer, T., Karplus, M., and Fischer, S. (2002) Translocation mechanism of long sugar chains across the maltoporin membrane channel, Structure 10, 1273-1284.
29. Uchiyama, T., Katouno, F., Nikaidou, N., Nonaka, T., Sugiyama, J., and Watanabe, T. (2001) Roles of exposed aromatic residues in crystalline chitin hydrolysis by chitinase A from Serratia marcescens 2170, J. Biol. Chem. 276, 41343-41349.
30. Adachi, M., Mikami, B., Katsube, T., and Utsumi, S. (1998) Crystal structure of recombinant soybean β-amylase complexed with β-cyclodextrin, J. Biol. Chem. 273, 19859-19865.
31. Svensson, B., Mundy, J., Gibson, R. M., and Svendsen, I. (1985) Partial amino acid sequences of α-amylase isozymes from barley malt, Carlsberg Res. Commun. 50, 15-22.
32. Kadziola, A., Abe, J., Svensson, B., and Haser, R. (1994) Crystal and molecular structure of barley α-amylase, J. Mol. Biol. 239, 104-31.
33. Robert, X., Gottschalk, T. E., Haser, R., Svensson, B., and Aghajari, N. (2002) Expression, purification and preliminary crystallographic studies of alpha-amylase isozyme 1 from barley seeds, Acta Crystallogr. D: Biol. Crystallogr. 58, 683-686.
34. André, G., and Tran, V. (1999) Molecular modelling of complexes between α-amylases and amylose fragments of high DP, in Recent Advances in Carbohydrate Bioengineering (Gilbert, H. J., Davies, G. J., Henrissat, B., and Svensson, B., Eds) pp 165-175, Royal Society of Chemistry, London.
35. Bak-Jensen, K. S., André, G., Gottschalk, T. E., Päes, G., Tran, V., and Svensson, B. (2004) Tyrosine 105 and Threonine 212 at outermost substrate binding subsites -6 and +4 control substrate specificity, oligosaccharide cleavage patterns, and multiple binding modes of barley α-amylase 1, J. Biol. Chem. 279, 10093-10102.
36. Mori, H., Bak-Jensen, K. S., Gottschalk, T. E., Motawia, M. S., Damager, I., Møller, B. L., and Svensson, B. (2001) Modulation of activity and substrate binding modes by mutation of single and double subsites +1/+2 and -5/-6, Eur. J. Biochem. 268, 6545-6558.
37. Juge, N., Le Gal-Coëffet, M.-F., Furniss, C. S. M., Gunning, A. P., Kramhøft, B., Morris, V. J., Williamson, G., and Svensson, B. (2002) The starch binding domain of glucoamylase from Aspergillus niger: an overview of its structure, function, and role in raw starch hydrolysis, Biologica 57 (Suppl. 11), 230-245.
38. 8-barrel domain of barley α-amylase 1, J. Biol. Chem. 272, 22456-22436.
39. 8-barrel domain, Biochemistry 40, 12844-12854.
40. Juge, N., Andersen, J. S., Tull, D., Roepstorff, P., and Svensson, B. (1996) Overexpression, purification, and characterization of recombinant barley α-amylases 1 and 2 secreted by the methylotrophic yeast Pichia pastoris, Protein Expression Purif. 8, 204-214.
41. Coutinho, P. M., and Henrissat, B. (1999) Carbohydrate-active enzymes: an integrated database approach, in Proceedings of the 3rd Carbohydrate Bioengineering Meeting on Recent Advances in Carbohydrate Bioengmeering (Gilbert, H. J., Davies, G. J., Henrissat, B., and Svensson, B., Eds.) pp 3-12, Royal Society of Chemistry, Cambridge, U.K.
42. Sauer, J., Sigurskjold, B. W., Christensen, U., Frandsen, T. P., Mirgorodskaya, E., Harrison, M., Roepstorff, P., and Svensson, B. (2000) Glucoamylase: structure/function relationship and protein engineering, Biochim. Biophys. Acta 1543, 275-293.
43. Le Gal-Coëffet, M.-F., Jacks, A. J., Sorimachi, K., Williamson, M. P., Williamson, G., and Archer, D. B. (1995) Expression in Aspergillus niger of the starch binding domain of glucoamylase. Comparison with the proteolytically produced starch binding domain, Eur. J. Biochem. 233, 561-567.
44. Robert, X., Haser, R., Gottschalk, T., Ratajczak, F., Driguez, H., Svensson, B., and Aghajari, N. (2003) The structure of barley α-amylase 1 reveals a novel role of domain C in substrate recognition and binding: a pair of sugar tongs, Structure 11, 973-984.
45. Søgaard, M., Kadziola, A., Haser, R., and Svensson, B. (1993) Site-directed mutagenesis of histidine 93, aspartic acid 180, glutamic acid 205, histidine 290, and aspartic acid 291 at the active site and tryptophan 279 at the raw starch binding site in barley α-amylase 1, J. Biol. Chem. 268, 22480-22484.
46. Chaplin, M. F. (1986) Monosaccharides, In Carbohydrate analysis, a practical approach (Chaplin, M. F., and Kennedy, J. F., Eds.) pp 1-36, IRL Press Ltd., Oxford, Washington, DC.
47. McFetters, R. F. (1980) A manual method for reducing sugar determinations with 2,2′-bicinchoninate reagent, Anal. Biochem. 103, 302-306.
48. MacGregor, E. A., MacGregor, A. W., Macri, L. J., and Morgan, J. E. (1994) Models for the action of barley alpha-amylase isozymes on linear substrates, Carbohydr. Res. 257, 249-268.
49. Robyt, J. F., and French, D. (1970) Multiple attack and polarity of action of porcine α-amylase, Arch. Biochem. Biophys. 138, 662-670.
50. Bak-Jensen, K. S. (1999) Protein engineering of the action pattern and the influence of calcium ions and halides on the activity of barley α-amylase 1, M.Sc. Thesis, University of Copenhagen, Denmark.
51. MacGregor, E. A., and MacGregor, A. W. (1985) A model for the action of cereal alpha amylases on amylose, Carbohydr. Res. 142, 223-236.
52. Banks, W., Greenwood, C. T., and Khan, K. M. (1970) Studies on starch-degrading enzymes. Part XII. The initial stages of the action on amylose of the alpha-amylases from B. subtilis, human saliva, malted rye, and porcine pancreas, Carbohydr. Res. 12, 79-87.