The structure of a Streptomyces avermitilis α-L-Rhamnosidase reveals a novel carbohydrate-binding module CBM67 within the six-domain arrangement

Journal of Biological Chemistry

Volumn 288, Issue 17, 2013, Pages 12376-12385

  Fujimoto, Zui ^a   Jackson, Adam ^b   Michikawa, Mari ^c   Maehara, Tomoko ^c   Momma, Mitsuru ^a   Henrissat, Bernard ^d   Gilbert, Harry J ^b   Kaneko, Satoshi ^c  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

^d AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE-BINDING MODULES; CATALYTIC MECHANISMS; CATALYTIC MODULES; GLYCOSIDE HYDROLASES; INSOLUBLE SUBSTRATES; LIGAND COMPLEXES; STREPTOMYCES AVERMITILIS; SUBSTANTIAL REDUCTION;

AMINO ACIDS; BACTERIA; COMPLEXATION; ENZYMES; PLANT CELL CULTURE;

CARBOHYDRATES;

ALANINE; ALPHA LEVO RHAMNOSIDASE; ASPARAGINE; ASPARTIC ACID; CALCIUM; CARBOHYDRATE BINDING PROTEIN; CYSTEINE; GLUTAMIC ACID; GLYCOSIDASE; GUM ARABIC; OXYGEN; PHENYLALANINE; POLYSACCHARIDE; PROTEIN CBM67; PROTON; RHAMNOSE; UNCLASSIFIED DRUG; WATER;

ARTICLE; CATALYSIS; CELL WALL; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; LIGAND BINDING; MUTAGENESIS; NUCLEOPHILICITY; PLANT CELL; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; STREPTOMYCES AVERMITILIS;

BACTERIAL PROTEINS; CALCIUM; CRYSTALLOGRAPHY, X-RAY; GLYCOSIDE HYDROLASES; MUTAGENESIS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RHAMNOSE; STREPTOMYCES; SUBSTRATE SPECIFICITY;

ACACIA SENEGAL; STREPTOMYCES AVERMITILIS;

EID: 84876889073     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.460097     Document Type: Article

References (43)

1. Ochsner, U. A., Fiechter, A., and Reiser, J. (1994) Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J. Biol. Chem. 269, 19787-19795
2. Mutter, M., Renard, CM., Beldman, G., Schols, H. A., and Voragen, A. G. (1998) Mode of action of RG-hydrolase and RG-lyase toward rhamnogalacturonan oligomers. Characterization of degradation products using RG-rhamnohydrolase and RG-galacturonohydrolase. Carbohydr. Res. 311, 155-164
3. Drewnowski, A., Henderson, S. A., and Shore, A. B. (1997) Taste responses to naringin, a flavonoid, and the acceptance of grapefruit juice are related to genetic sensitivity to 6-n-propylthiouracil. Am. J. Clin. Nutr. 66, 391-397
4. Vila-Real, H., Alfaia, A. J., Bronze, M. R., Calado, A. R., and Ribeiro, M. H. (2011) Enzymatic synthesis of the flavone glucosides, prunin and isoquercetin, and the aglycones, naringenin and quercetin, with selective a-L-rhamnosidase and β-D-glucosidase activities of naringinase. Enzyme Res. 2011, 692618
5. 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
6. Henrissat, B., and Davies, G. (1997) Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7, 637-644
7. Cui, Z., Maruyama, Y., Mikami, B., Hashimoto, W., and Murata, K. (2007) Crystal structure of glycoside hydrolase family 78 α-L-rhamnosidase from Bacillus sp. GL1. J. Mol. Biol. 374, 384-398
8. Bonanno, J. B., Almo, S. C., Bresnick, A., Chance, M. R., Fiser, A., Swaminathan, S., Jiang, J., Studier, F. W., Shapiro, L., Lima, C. D., Gaasterland, T. M., Sali, A., Bain, K., Feil, I., Gao, X., Lorimer, D., Ramos, A., Sauder, J. M., Wasserman, S. R., Emtage, S., D'Amico, K. L., and Burley, S. K. (2005) New York-Structural GenomiX Research Consortium (NYSGXRC). A large scale center for the protein structure initiative. J. Struct. Funct. Genomics 6, 225-232
9. Ichinose, H., Fujimoto, Z., and Kaneko, S. (2013) Characterization of an a-L-rhamnosidase from Streptomyces avermitilis. Biosci. Biotechnol. Biochem. 77, 213-216
10. LeMaster, D. M., and Richards, F. M. (1985) 1H-15N heteronuclear NMR studies of Escherichia coli thioredoxin in samples isotopically labeled by residue type. Biochemistry 24, 7263-7268
11. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
12. Terwilliger, T. C. (2003) SOLVE and RESOLVE. Automated structure solution and density modification. Methods Enzymol. 374, 22-37
13. Terwilliger, T. C. (2003) Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr. D Biol. Crystallogr. 59, 38-44
14. Perrakis, A., Morris, R., and Lamzin, V. (1999) Automated protein model building combined with iterative structure refinement. Nat Struct. Biol. 6, 458-463
15. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
16. Emsley, P., and Cowtan, K. (2004) Coo. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
17. Murshudov, G. N., Skubak, 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
18. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
19. Lovell, S. C., Davis, I. W., Arendall, W. B., 3rd, deBakker, P. I., 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 50, 437-450
20. Yang, H., Ichinose, H., Nakajima, M., Kobayashi, H., and Kaneko, S. (2006) Synergy between an α-L-arabinofuranosidase from Aspergillus oryzae and an endo-arabinanase from Streptomyces coelicolor for degradation of arabinan. Food Sci. Technol. Res. 12, 43-49
21. Ichinose, H., Fujimoto, Z., Honda, M., Harazono, K., Nishimoto, Y., Uzura, A., and Kaneko, S. (2009) A β-L-arabinopyranosidase from Streptomyces avermitilis is a novel member of glycoside hydrolase family 27. J. Biol. Chem. 284, 25097-25106
22. 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
23. Zverlov, V. V., Hertel, C., Bronnenmeier, K., Hroch, A., Kellermann, J., and Schwarz, W. H. (2000) The thermostable α-L-rhamnosidase RamA of Clostridium stercorarium. Biochemical characterization and primary structure of a bacterial α-L-rhamnoside hydrolase, a new type of inverting glycoside hydrolase. Mol. Microbiol. 35, 173-179
24. Guerin, D. M., Lascombe, M. B., Costabel, M., Souchon, H., Lamzin, V., Beguin, P., and Alzari, P. M. (2002) Atomic (0.94 Å) resolution structure of an inverting glycosidase in complex with substrate. J. Mol. Biol. 316, 1061-1069
25. Brüx, C., Ben-David, A., Shallom-Shezifi, D., Leon, M., Niefind, K., Shoham, G., Shoham, Y., and Schomburg, D. (2006) The structure of an inverting GH43 β-xylosidase from Geobacillus stearothermophilus with its substrate reveals the role of the three catalytic residues. J. Mol. Biol. 359, 97-109
26. Sidhu, G., Withers, S. G., Nguyen, N. T., McIntosh, L. P., Ziser, L., and Brayer, G. D. (1999) Sugar ring distortion in the glycosyl-enzyme intermediate of a family G/11 xylanase. Biochemistry 38, 5346-5354
27. Petersen, L., Ardevol, A., Rovira, C., and Reilly, P. J. (2009) Mechanism of cellulose hydrolysis by inverting GH8 endoglucanases. A QM/MM metadynamics study. J. Phys. Chem. B 113, 7331-7339
28. Barker, I. J., Petersen, L., and Reilly, P. J. (2010) Mechanism of xylobiose hydrolysis by GH43 β-xylosidase. J. Phys. Chem. B 114, 15389-15393
29. Ly, H. D., and Withers, S. G. (1999) Mutagenesis of glycosidases. Annu. Rev. Biochem. 68, 487-522
30. Ficko-Blean, E., Stubbs, K. A., Nemirovsky, O., Vocadlo, D. J., and Boraston, A. B. (2008) Structural and mechanistic insight into the basis of mucopolysaccharidosis IIIB. Proc. Natl. Acad. Sci. U. S. A. 105, 6560-6565
31. Montanier, C., Flint, J. E., Bolam, D. N., Xie, H., Liu, Z., Rogowski, A., Weiner, D. P., Ratnaparkhe, S., Nurizzo, D., Roberts, S. M., Turkenburg, J. P., Davies, G. J., and Gilbert, H. J. (2010) Circular permutation provides an evolutionary link between two families of calcium-dependent carbohy-drate binding modules. J. Biol. Chem. 285, 31742-31754
32. Yazawa, R., Takakura, J., Sakata, T., Ihsanawati, Yatsunami, R., Fukui, T., Kumasaka, T., Tanaka, N., and Nakamura, S. (2011) A calcium-dependent xylan-binding domain of alkaline xylanase from alkaliphilic Bacillus sp. strain 41M-1. Biosci. Biotechnol. Biochem. 75, 379-381
33. Montanier, C., van Bueren, A. L., Dumon, C., Flint, J. E., Correia, M. A., Prates, J. A., Firbank, S. J., Lewis, R. J., Grondin, G. G., Ghinet, M. G., Gloster, T. M., Herve, C., Knox, J. P., Talbot, B. G., Turkenburg, J. P., Kerovuo, J., Brzezinski, R., Fontes, C. M., Davies, G. J., Boraston, A. B., and Gilbert, H. J. (2009) Evidence that family 35 carbohydrate binding modules display conserved specificity but divergent function. Proc. Natl. Acad. Sci. U. S. A. 106, 3065-3070
34. Oguri, S., Ando, A., and Nagata, Y. (1996) A novel developmental stagespecific lectin of the basidiomycete Pleurotus cornucopiae. J. Bacteriol. 178, 5692-5698
35. Sumisa, F., Ichijo, N., Yamaguchi, H., Nakatsumi, H., Ando, A., Iijima, N., Oguri, S., Uehara, K., Nagata, Y. (2004) Molecular properties of mycelial aggregate-specific lectin of Pleurotus cornucopiae. J. Biosci. Bioeng. 98, 257-262
36. Vakonakis, I., Langenhan, T., Prömel, S., Russ, A., and Campbell, I. D. (2008) Solution structure and sugar-binding mechanism of mouse latrophilin-1 RBL. A 7TM receptor-attached lectin-like domain. Structure 16, 944-953
37. Shirai, T., Watanabe, Y., Lee, M. S., Ogawa, T., and Muramoto, K. (2009) Structure of rhamnose-binding lectin CSL3. Unique pseudo-tetrameric architecture of a pattern recognition protein. J. Mol. Biol. 391, 390-403
38. Hall, J., Black, G. W., Ferreira, L. M., Millward-Sadler, S. J., Ali, B. R., Hazlewood, G. P., and Gilbert, H. J. (1995) The non-catalytic cellulosebinding domain of a novel cellulase from Pseudomonas fluorescens subsp. cellulosais important for the efficient hydrolysis of Avicel. Biochem. J. 309, 749-756
39. Hervé, C., Rogowski, A., Blake, A. W., Marcus, S. E., Gilbert, H. J., and Knox, J. P. (2010) Carbohydrate-binding modules promote the enzymatic deconstruction ofintact plant cell walls by targeting and proximity effects. Proc. Natl. Acad. Sci. U. S. A. 107, 15293-15298
40. Defaye, J., and Wong, E. (1986) Structural studies of gum arabic, the exudate polysaccharide from Acacia senegal. Carbohydr. Res. 150, 221-231
41. Cuskin, F., Flint, J. E., Gloster, T. M., Morland, C., Baslé, A., Henrissat, B., Coutinho, P. M., Strazzulli, A., Solovyova, A. S., Davies, G. J., and Gilbert, H. J. (2012) How nature can exploit nonspecific catalytic and carbohydrate binding modules to create enzymatic specificity. Proc. Natl. Acad. Sci. U. S. A. 109, 20889-20894
42. Boraston, A. B., Ficko-Blean, E., and Healey, M. (2007) Carbohydrate recognition by a large sialidase toxin from Clostridium perfringens. Biochemistry 46, 11352-11360
43. Jamal-Talabani, S., Boraston, A. B., Turkenburg, J. P., Tarbouriech, N., Ducros, V. M., and Davies, G. J. (2004) Ab initio structure determination and functional characterization of CBM36. A new family of calcium-dependent carbohydrate binding modules. Structure 12, 1177-1187