Molecular basis for the recognition of long-chain substrates by plant α-glucosidases

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 19296-19303

  Tagami, Takayoshi ^a   Yamashita, Keitaro ^a   Okuyama, Masayuki ^a   Mori, Haruhide ^a   Yao, Min ^a   Kimura, Atsuo ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE POCKET; AMINO ACID SEQUENCE; GLYCOSIDE HYDROLASE FAMILY 31; MALTOOLIGOSACCHARIDES; N-TERMINAL DOMAINS; SITE DIRECTED MUTAGENESIS; STRUCTURAL INSIGHTS; SUBSTRATE RECOGNITION;

AMINO ACIDS; ENZYME ACTIVITY; SUGAR BEETS;

SUBSTRATES;

ACARBOSE; ALPHA GLUCOSIDASE; AMINO ACID; ASPARAGINE; GLYCOSIDASE; OLIGOSACCHARIDE; PHENYLALANINE; SERINE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; ENZYME BINDING; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GERMINATION; KINETICS; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT SEED; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SUGAR BEET;

Α-GLUCOSIDASE; ACARBOSE RECOGNITION; CRYSTAL STRUCTURE; ENZYME CATALYSIS; ENZYME KINETICS; ENZYME STRUCTURE; GLYCOSIDE HYDROLASE FAMILY 31; LONG-CHAIN SPECIFICITY; PLANT;

ACARBOSE; ALPHA-GLUCOSIDASES; AMINO ACID SEQUENCE; BETA VULGARIS; DNA MUTATIONAL ANALYSIS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PLANT PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

BETA VULGARIS SUBSP. VULGARIS;

EID: 84879595690     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.465211     Document Type: Article

References (34)

1. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
2. Quezada-Calvillo, R., Robayo-Torres, C. C., Opekun, A. R., Sen, P., Ao, Z., Hamaker, B. R., Quaroni, A., Brayer, G. D., Wattler, S., Nehls, M. C., Sterchi, E. E., and Nichols, B. L. (2007) Contribution of mucosal maltase-glucoamylase activities to mouse small intestinal starch α-glucogenesis. J. Nutr. 137, 1725-1733 (Pubitemid 47037698)
3. Kita, A., Matsui, H., Somoto, A., Kimura, A., Takata, M., and Chiba, S. (1991) Substrate specificity and subsite affinities of crystalline α-glucosidase from Aspergillus niger. Agric. Biol. Chem. 55, 2327-2335
4. Okuyama, M., Tanimoto, Y., Ito, T., Anzai, A., Mori, H., Kimura, A., Matsui, H., and Chiba, S. (2005) Purification and characterization of the hyperglycosylated extracellular α-glucosidase from Schizosaccharomyces pombe. Enzyme Microb. Technol. 37, 472-480 (Pubitemid 41138177)
5. Sato, F., Okuyama, M., Nakai, H., Mori, H., Kimura, A., and Chiba, S. (2005) Glucoamylase originating from Schwanniomyces occidentalis is a typical α-glucosidase. Biosci. Biotechnol. Biochem. 69, 1905-1913 (Pubitemid 41558855)
6. Im, H., and Henson, C. A. (1995) Characterization of high pI α-glucosidase from germinated barley seeds: substrate specificity, subsite affinities and active-site residues. Carbohydr. Res. 277, 145-159
7. Chiba, S., Kanaya, K., Hiromi, K., and Shimomura, T. (1979) Substrate specificity and subsite affinities of buckwheat α-glucosidase. Agric. Biol. Chem. 43, 237-242
8. Matsui, H., Chiba, S., and Shimomura, T. (1978) Substrate specificity of an α-glucosidase in sugar beet seed. Agric. Biol. Chem. 42, 1855-1860
9. Ernst, H. A., Lo Leggio, L., Willemoës, M., Leonard, G., Blum, P., and Larsen, S. (2006) Structure of the Sulfolobus solfataricus α-glucosidase: implications for domain conservation and substrate recognition in GH31. J. Mol. Biol. 358, 1106-1124 (Pubitemid 44403821)
10. Sim, L., Quezada-Calvillo, R., Sterchi, E. E., Nichols, B. L., and Rose, D. R. (2008) Human intestinal maltase-glucoamylase: crystal structure of the N-terminal catalytic subunit and basis of inhibition and substrate specificity. J. Mol. Biol. 375, 782-792
11. Sim, L., Willemsma, C., Mohan, S., Naim, H. Y., Pinto, B. M., and Rose, D. R. (2010) Structural basis for substrate selectivity in human maltase-glucoamylase and sucrase-isomaltase N-terminal domains. J. Biol. Chem. 285, 17763-17770
12. Tan, K., Tesar, C., Wilton, R., Keigher, L., Babnigg, G., and Joachimiak, A. (2010) Novel α-glucosidase from human gut microbiome: substrate specificities and their switch. FASEB J. 24, 3939-3949
13. Ren, L., Qin, X., Cao, X., Wang, L., Bai, F., Bai, G., and Shen, Y. (2011) Structural insight into substrate specificity of human intestinal maltase-glucoamylase. Protein Cell 2, 827-836
14. Tagami, T., Okuyama, M., Nakai, H., Kim, Y.M., Mori, H., Taguchi, K., Svensson, B., and Kimura, A. (2013) Key aromatic residues at subsites +2 and +3 of glycoside hydrolase family 31 α-glucosidases contribute to recognition of long-chain substrates. Biochim. Biophys. Acta 1834, 329-335
15. Wheelan, S. J., Church, D. M., and Ostell, J. M. (2001) Spidey: A tool for mRNA-to genomic alignments. Genome Res. 11, 1952-1957 (Pubitemid 33100436)
16. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
17. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
18. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
19. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
20. Lovell, S. C., Davis, I. W., Arendall, W. B., 3rd, de Bakker, P. I. W., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Cα geometry: φ, ψ and Cβ deviation. Proteins Struct. Funct. Genet. 50, 437-450
21. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, Version 1.5.0.4, Schrödinger, LLC, San Carlos, CA
22. Hizukuri, S., and Osaki, S. (1978) A rapid Smith-degradation for the determination of nonreducing, terminal residues of (1→4)α-D-glucans. Carbohydr. Res. 63, 261-264
23. Hasegawa, H., and Holm, L. (2009) Advances and pitfalls of protein structural alignment. Curr. Opin. Struct. Biol. 19, 341-348
24. Imperiali, B., and Hendrickson, T. L. (1995) Asparagine-linked glycosylation: specificity and function of oligosaccharyl transferase. Bioorg. Med. Chem. 3, 1565-1578 (Pubitemid 26022435)
25. Imperiali, B., Shannon, K. L., Unno, M., and Rickert, K. W. (1992) A mechanistic proposal for asparagine-linked glycosylation. J. Am. Chem. Soc. 114, 7944-7945
26. Tarentino, A. L., and Plummer, T. H., Jr. (1994) Enzymatic deglycosylation of asparagine-linked glycans: purification, properties, and specificity of oligosaccharide-cleaving enzymes from Flavobacterium meningosepticum. Methods Enzymol. 230, 44-57
27. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
28. Larsbrink, J., Izumi, A., Ibatullin, F. M., Nakhai, A., Gilbert, H. J., Davies, G. J., and Brumer, H. (2011) Structural and enzymatic characterization of a glycoside hydrolase family 31 α-xylosidase from Cellvibrio japonicus involved in xyloglucan saccharification. Biochem. J. 436, 567-580
29. Yu, S. (2008) The anhydrofructose pathway of glycogen catabolism. IUBMB Life 60, 798-809
30. Sugimoto, M., Furui, S., and Suzuki, Y. (1995) Multiple molecular forms of α-glucosidase from spinach seeds, Spinacia oleracea L. Biosci. Biotechnol. Biochem. 59, 673-677
31. Nakai, H., Ito, T., Hayashi, M., Kamiya, K., Yamamoto, T., Matsubara, K., Kim, Y. M., Jintanart, W., Okuyama, M., Mori, H., Chiba, S., Sano, Y., and Kimura, A. (2007) Multiple forms of α-glucosidase in rice seeds (Oryza sativa L., var Nipponbare). Biochimie 89, 49-62 (Pubitemid 44959285)
32. Nakai, H., Tanizawa, S., Ito, T., Kamiya, K., Kim, Y. M., Yamamoto, T., Matsubara, K., Sakai, M., Sato, H., Imbe, T., Okuyama, M., Mori, H., Sano, Y., Chiba, S., and Kimura, A. (2007) Function-unknown glycoside hydrolase family 31 proteins, mRNAs of which were expressed in rice ripening and germinating stages, are α-glucosidase and α-xylosidase. J. Biochem. 142, 491-500 (Pubitemid 351197682)
33. Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
34. Gouet, P., Courcelle, E., Stuart, D. I., and Métoz, F. (1999) ESPript: multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (Pubitemid 29213756)