Tracing determinants of dual substrate specificity in glycoside hydrolase family 5

Journal of Biological Chemistry

Volumn 287, Issue 30, 2012, Pages 25335-25343

  Chen, Zhiwei ^a,b   Friedland, Gregory D ^a,b   Pereira, Jose H ^a,c   Reveco, Sonia A ^a,c   Chan, Rosa ^d   Park, Joshua I ^a,b,h   Thelen, Michael P ^a,g   Adams, Paul D ^a,c,e   Arkin, Adam P ^a,c,e   Keasling, Jay D ^a,c,e,f   Blanch, Harvey W ^a,c,f   Simmons, Blake A ^a,b   Sale, Kenneth L ^a,b   Chivian, Dylan ^a,c   Chhabra, Swapnil R ^a,c,i  

^a JOINT BIOENERGY INSTITUTE   (United States)

^b SANDIA NATIONAL LABORATORIES   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e University of California at Berkeley   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^h MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

ⁱ INTREXON CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CATALYTIC EFFICIENCIES; COMBINED STRUCTURE; CONSOLIDATED BIOPROCESSING; EXPERIMENTAL CONFIRMATION; GLYCOSIDE HYDROLASES; MULTIPLE SUBSTRATES; PHYLOGENETIC ANALYSIS; SINGLE DOMAINS; SUBSTRATE SPECIFICITY; WILD TYPES;

ENZYMES;

SUBSTRATES;

GLUCAN; GLYCOSIDASE; GLYCOSIDASE FAMILY 5; MANNAN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN MOTIF; WILD TYPE;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; CATALYSIS; GLYCOSIDE HYDROLASES; PHYLOGENY; PLANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84864095374     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.362640     Document Type: Article

References (45)

1. Nobeli, I., Favia, A. D., and Thornton, J. M. (2009) Protein promiscuity and its implications for biotechnology. Nat. Biotechnol. 27, 157-167
2. Khersonsky, O., and Tawfik, D. S. (2010) Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu. Rev. Biochem. 79, 471-505
3. Peisajovich, S. G., and Tawfik, D. S. (2007) Protein engineers turned evolutionists. Nat. Methods 4, 991-994 (Pubitemid 350201764)
4. Khersonsky, O., Roodveldt, C., and Tawfik, D. S. (2006) Enzyme promiscuity: evolutionary and mechanistic aspects. Curr. Opin. Chem. Biol. 10, 498-508 (Pubitemid 44375065)
5. Khersonsky, O., and Tawfik, D. S. (2006) The histidine 115-histidine 134 dyad mediates the lactonase activity of mammalian serum paraoxonases. J. Biol. Chem. 281, 7649-7656 (Pubitemid 43847535)
6. 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
7. Plewczyśki, D., Paś, J., von Grotthuss, M., and Rychlewski, L. (2002) 3D-Hit: fast structural comparison of proteins. Appl. Bioinformatics 1, 223-225
8. Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797
9. Price, M. N., Dehal, P. S., and Arkin, A. P. (2010) FastTree 2: approximately maximum-likelihood trees for large alignments. PloS One 5, e9490
10. Pereira, J. H., Chen, Z., McAndrew, R. P., Sapra, R., Chhabra, S. R., Sale, K. L., Simmons, B. A., and Adams, P. D. (2010) Biochemical characterization and crystal structure of endoglucanase Cel5A from the hyperthermophilic Thermotoga maritima. J. Struct. Biol. 172, 372-379
11. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
12. Hilge, M., Gloor, S. M., Rypniewski, W., Sauer, O., Heightman, T. D., Zimmermann, W., Winterhalter, K., and Piontek, K. (1998) High-resolution native and complex structures of thermostable β-mannanase from Thermomonospora fusca: substrate specificity in glycosyl hydrolase family 5. Structure 6, 1433-1444 (Pubitemid 28541886)
13. Tailford, L. E., Ducros, V. M., Flint, J. E., Roberts, S. M., Morland, C., Zechel, D. L., Smith, N., Bjørnvad, M. E., Borchert, T. V., Wilson, K. S., Davies, G. J., and Gilbert, H. J. (2009) Understanding how diverse β-mannanases recognize heterogeneous substrates. Biochemistry 48, 7009-7018
14. Bourgault, R., Oakley, A. J., Bewley, J. D., and Wilce, M. C. (2005) Three-dimensional structure of (1,4)-β-D-mannan mannanohydrolase from tomato fruit. Protein Sci. 14, 1233-1241 (Pubitemid 40577803)
15. Sabini, E., Schubert, H., Murshudov, G., Wilson, K. S., Siika-Aho, M., and Penttilä, M. (2000) The three-dimensional structure of a Trichoderma reesei β-mannanase from glycoside hydrolase family 5. Acta Crystallogr. D. Biol. Crystallogr. 56, 3-13 (Pubitemid 30061536)
16. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
17. Xiao, Z., Storms, R., and Tsang, A. (2005) Microplate-based carboxymethylcellulose assay for endoglucanase activity. Anal. Biochem. 342, 176-178 (Pubitemid 40805645)
18. Anthon, G. E., and Barrett, D. M. (2002) Determination of reducing sugars with 3-methyl-2-benzothiazolinonehydrazone. Anal. Biochem. 305, 287-289 (Pubitemid 34666805)
19. Wang, Y., Wang, X., Tang, R., Yu, S., Zheng, B., and Feng, Y. (2010)Anovel thermostable cellulase from Fervidobacterium nodosum. J. Mol. Catal. B. Enzym. 66, 294-301
20. Vlasenko, E., Schülein, M., Cherry, J., and Xu, F. (2010) Substrate specificity of family 5, 6, 7, 9, 12, and 45 endoglucanases. Bioresour. Technol. 101, 2405-2411
21. Tyler, L., Bragg, J. N., Wu, J., Yang, X., Tuskan, G. A., and Vogel, J. P. (2010) Annotation and comparative analysis of the glycoside hydrolase genes in Brachypodium distachyon. BMC Genomics 11, 600
22. Elifantz, H., Waidner, L. A., Michelou, V. K., Cottrell, M. T., and Kirchman, D. L. (2008) Diversity and abundance of glycosyl hydrolase family 5 in the North Atlantic Ocean. FEMS Microbiol. Ecol. 63, 316-327 (Pubitemid 351208034)
23. Danchin, E. G., Rosso, M. N., Vieira, P., de Almeida-Engler, J., Coutinho, P. M., Henrissat, B., and Abad, P. (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc. Natl. Acad. Sci. U.S.A. 107, 17651-17656
24. Chivian, D., and Baker, D. (2006) Homology modeling using parametric alignment ensemble generation with consensus and energy-based model selection. Nucleic Acids Res. 34, e112
25. Kelley, L. A., MacCallum, R. M., and Sternberg, M. J. (2000) Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299, 499-520
26. O'Sullivan, O., Suhre, K., Abergel, C., Higgins, D. G., and Notredame, C. (2004) 3DCoffee: combining protein sequences and structures within multiple sequence alignments. J. Mol. Biol. 340, 385-395 (Pubitemid 38759917)
27. Stebbings, L. A., and Mizuguchi, K. (2004) HOMSTRAD: recent developments of the Homologous Protein Structure Alignment Database. Nucleic Acids Res. 32, D203-D207 (Pubitemid 38081639)
28. Ducros, V., Czjzek, M., Belaich, A., Gaudin, C., Fierobe, H. P., Belaich, J. P., Davies, G. J., and Haser, R. (1995) Crystal structure of the catalytic domain of a bacterial cellulase belonging to family 5. Structure 3, 939-949
29. Domínguez, R., Souchon, H., Lascombe, M., and Alzari, P. M. (1996) The crystal structure of a family 5 endoglucanase mutant in complexed and uncomplexed forms reveals an induced fit activation mechanism. J. Mol. Biol. 257, 1042-1051 (Pubitemid 26117089)
30. Foong, F., Hamamoto, T., Shoseyov, O., and Doi, R. H. (1991) Nucleotide sequence and characteristics of endoglucanase gene engB from Clostridium cellulovorans. J. Gen. Microbiol. 137, 1729-1736
31. Whitehead, T. R. (1993) Analyses of the gene and amino acid sequence of the Prevotella (Bacteroides) ruminicola 23 xylanase reveals unexpected homology with endoglucanases from other genera of bacteria. Curr. Microbiol. 27, 27-33
32. Chhabra, S. R., Shockley, K. R., Ward, D. E., and Kelly, R. M. (2002) Regulation of endo-acting glycosyl hydrolases in the hyperthermophilic bacterium Thermotoga maritima grown on glucan- and mannan-based polysaccharides. Appl. Environ. Microbiol. 68, 545-554 (Pubitemid 34113039)
33. Chhabra, S. R., Shockley, K. R., Conners, S. B., Scott, K. L., Wolfinger, R. D., and Kelly, R. M. (2003) Carbohydrate-induced differential gene expression patterns in the hyperthermophilic bacterium Thermotoga maritima. J. Biol. Chem. 278, 7540-7552 (Pubitemid 36800761)
34. Wu, T. H., Huang, C. H., Ko, T. P., Lai, H. L., Ma, Y., Chen, C. C., Cheng, Y. S., Liu, J. R., and Guo, R. T. (2011) Diverse substrate recognition mechanism revealed by Thermotoga maritima Cel5A structures in complex with cellotetraose, cellobiose, and mannotriose. Biochim. Biophys. Acta 1814, 1832-1840
35. Liang, C., Fioroni, M., Rodríguez-Ropero, F., Xue, Y., Schwaneberg, U., and Ma, Y. (2011) Directed evolution of a thermophilic endoglucanase (Cel5A) into highly active Cel5A variants with an expanded temperature profile. J. Biotechnol. 154, 46-53
36. Reitinger, S., Yu, Y., Wicki, J., Ludwiczek, M., D'Angelo, I., Baturin, S., Okon, M., Strynadka, N. C., Lutz, S., Withers, S. G., and McIntosh, L. P. (2010) Circular permutation of Bacillus circulans xylanase: a kinetic and structural study. Biochemistry 49, 2464-2474
37. Himmel, M. E., Ding, S. Y., Johnson, D. K., Adney, W. S., Nimlos, M. R., Brady, J. W., and Foust, T. D. (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315, 804-807
38. Wen, F., Nair, N. U., and Zhao, H. (2009) Protein engineering in designing tailored enzymes and microorganisms for biofuels production. Curr. Opin. Biotechnol. 20, 412-419
39. Percival Zhang, Y. H., Himmel, M. E., and Mielenz, J. R. (2006) Outlook for cellulase improvement: screening and selection strategies. Biotechnol. Adv. 24, 452-481 (Pubitemid 44082013)
40. Jensen, R. A. (1976) Enzyme recruitment in evolution of new function. Annu. Rev. Microbiol. 30, 409-425
41. Bershtein, S., Goldin, K., and Tawfik, D. S. (2008) Intense neutral drifts yield robust and evolvable consensus proteins. J. Mol. Biol. 379, 1029-1044
42. Letunic, I., and Bork, P. (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 39, W475-W478
43. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190 (Pubitemid 38811555)
44. Davies, G. J., Wilson, K. S., and Henrissat, B. (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321, 557-559 (Pubitemid 27056509)
45. Davies, G. J., Mackenzie, L., Varrot, A., Dauter, M., Brzozowski, A. M., Schülein, M., and Withers, S. G. (1998) Snapshots along an enzymatic reaction coordinate: analysis of a retaining β-glycoside hydrolase. Biochemistry 37, 11707-11713 (Pubitemid 28400042)