Structural Basis for Xyloglucan Specificity and α- D -Xyl p (1 → 6)- d -Glc p Recognition at the -1 Subsite within the GH5 Family

Biochemistry

Volumn 54, Issue 10, 2015, Pages 1930-1942

  Dos Santos, Camila Ramos ^a   Cordeiro, Rosa Lorizolla ^a   Wong, Dominic W S ^b   Murakami, Mário Tyago ^a  

^a BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^b WESTERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAPPING; OLIGOSACCHARIDES;

GLYCOSIDE HYDROLASES; HIGH RESOLUTION; METAGENOMIC LIBRARIES; MOLECULAR BASIS; STRUCTURAL ADAPTATION; STRUCTURAL BASIS; STRUCTURAL DETERMINANTS; SUBSITE MAPPING;

POLYMERS;

CELLULASE; GLUCAN; GLYCOSIDASE; GLYCOSIDASE GH5; OLIGOSACCHARIDE; UNCLASSIFIED DRUG; XYLOGLUCAN; BACTERIAL PROTEIN; XYLAN;

ARTICLE; CARBOHYDRATE ANALYSIS; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; GENE OVEREXPRESSION; METAGENOMICS; MOLECULAR CLONING; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; RUMINANT STOMACH; SITE DIRECTED MUTAGENESIS; BACTERIUM; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; STRUCTURE ACTIVITY RELATION;

BACTERIA; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CELLULASE; GLUCANS; OLIGOSACCHARIDES; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; XYLANS;

EID: 84924981592     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00011     Document Type: Article

References (64)

1. Fry, S. C. (1989) The Structure and Functions of Xyloglucan J. Exp. Bot. 40, 1-11
2. Popper, Z. A. and Fry, S. C. (2003) Primary cell wall composition of bryophytes and charophytes Ann. Bot. 91, 1-12
3. Popper, Z. A. and Fry, S. C. (2004) Primary cell wall composition of pteridophytes and spermatophytes New Phytol. 164, 165-174
4. Sarkar, P., Bosneaga, E., and Auer, M. (2009) Plant cell walls throughout evolution: towards a molecular understanding of their design principles J. Exp. Bot. 60, 3615-3635
5. Tuomivaara, S. T., Yaoi, K., O'Neill, M. A., and York, W. S. (2015) Generation and structural validation of a library of diverse xyloglucan-derived oligosaccharides, including an update on xyloglucan nomenclature Carbohydr. Res. 402, 56-66
6. Vincken, J. P., York, W. S., Beldman, G., and Voragen, A. G. (1997) Two general branching patterns of xyloglucan, XXXG and XXGG Plant Physiol. 114, 9-13
7. Carpita, N. C. and Gibeaut, D. M. (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth Plant J. 3, 1-30
8. Pauly, M., Albersheim, P., Darvill, A., and York, W. S. (1999) Molecular domains of the cellulose/xyloglucan network in the cell walls of higher plants Plant J. 20, 629-639
9. Cosgrove, D. J. (2005) Growth of the plant cell wall Nat. Rev. Mol. Cell Biol. 6, 850-861
10. Buckeridge, M. S., Pessoa dos Santos, H., and Tiné, M. A. S. (2000) Mobilisation of storage cell wall polysaccharides in seeds Plant Physiol. Biochem. 38, 141-156
11. Scheible, W. R. and Pauly, M. (2004) Glycosyltransferases and cell wall biosynthesis: novel players and insights Curr. Opin. Plant Biol. 7, 285-295
12. Miyazaki, S., Suisha, F., Kawasaki, N., Shirakawa, M., Yamatoya, K., and Attwood, D. (1998) Thermally reversible xyloglucan gels as vehicles for rectal drug delivery J. Controlled Release 56, 75-83
13. Brumer, H., 3rd, Zhou, Q., Baumann, M. J., Carlsson, K., and Teeri, T. T. (2004) Activation of crystalline cellulose surfaces through the chemoenzymatic modification of xyloglucan J. Am. Chem. Soc. 126, 5715-5721
14. Zhou, Q., Baumann, M. J., Brumer, H., and Teeri, T. T. (2006) The influence of surface chemical composition on the adsorption of xyloglucan to chemical and mechanical pulps Carbohydr. Polym. 63, 449-458
15. Zhou, Q., Greffe, L., Baumann, M. J., Malmström, E., Teeri, T. T., and Brumer, H. (2005) Use of Xyloglucan as a Molecular Anchor for the Elaboration of Polymers from Cellulose Surfaces: A General Route for the Design of Biocomposites Macromolecules 38, 3547-3549
16. Greffe, L., Bessueille, L., Bulone, V., and Brumer, H. (2005) Synthesis, preliminary characterization, and application of novel surfactants from highly branched xyloglucan oligosaccharides Glycobiology 15, 437-445
17. Hoffman, M., Jia, Z., Pena, M. J., Cash, M., Harper, A., Blackburn, A. R., 2nd, Darvill, A., and York, W. S. (2005) Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae Carbohydr. Res. 340, 1826-1840
18. Menon, V., Prakash, G., and Rao, M. (2010) Enzymatic hydrolysis and ethanol production using xyloglucanase and Debaromyces hansenii from tamarind kernel powder: galactoxyloglucan predominant hemicellulose J. Biotechnol. 148, 233-239
19. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., and Henrissat, B. (2014) The carbohydrate-active enzymes database (CAZy) in 2013 Nucleic Acids Res. 42, D490-495
20. Davies, G. J., Wilson, K. S., and Henrissat, B. (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases Biochem. J. 321 (Pt 2) 557-559
21. Yaoi, K., Nakai, T., Kameda, Y., Hiyoshi, A., and Mitsuishi, Y. (2005) Cloning and characterization of two xyloglucanases from Paenibacillus sp. strain KM21 Appl. Environ. Microbiol. 71, 7670-7678
22. Desmet, T., Cantaert, T., Gualfetti, P., Nerinckx, W., Gross, L., Mitchinson, C., and Piens, K. (2007) An investigation of the substrate specificity of the xyloglucanase Cel74A from Hypocrea jecorina FEBS J. 274, 356-363
23. Ichinose, H., Araki, Y., Michikawa, M., Harazono, K., Yaoi, K., Karita, S., and Kaneko, S. (2012) Characterization of an endo-processive-type xyloglucanase having a beta-1,4-glucan-binding module and an endo-type xyloglucanase from Streptomyces avermitilis Appl. Environ. Microbiol. 78, 7939-7945
24. Feng, T., Yan, K. P., Mikkelsen, M. D., Meyer, A. S., Schols, H. A., Westereng, B., and Mikkelsen, J. D. (2014) Characterisation of a novel endo-xyloglucanase (XcXGHA) from Xanthomonas that accommodates a xylosyl-substituted glucose at subsite -1 Appl. Microbiol. Biotechnol. 98, 9667-9679
25. Ariza, A., Eklof, J. M., Spadiut, O., Offen, W. A., Roberts, S. M., Besenmatter, W., Friis, E. P., Skjot, M., Wilson, K. S., Brumer, H., and Davies, G. (2011) Structure and activity of Paenibacillus polymyxa xyloglucanase from glycoside hydrolase family 44 J. Biol. Chem. 286, 33890-33900
26. Yaoi, K. and Mitsuishi, Y. (2002) Purification, characterization, cloning, and expression of a novel xyloglucan-specific glycosidase, oligoxyloglucan reducing end-specific cellobiohydrolase J. Biol. Chem. 277, 48276-48281
27. Bauer, S., Vasu, P., Mort, A. J., and Somerville, C. R. (2005) Cloning, expression, and characterization of an oligoxyloglucan reducing end-specific xyloglucanobiohydrolase from Aspergillus nidulans Carbohydr. Res. 340, 2590-2597
28. Wong, D. D., Chan, V. J., McCormack, A. A., and Batt, S. B. (2010) A novel xyloglucan-specific endo-beta-1,4-glucanase: biochemical properties and inhibition studies Appl. Microbiol. Biotechnol. 86, 1463-1471
29. Wong, D. D., Chan, V. J., McCormack, A. A., and Batt, S. B. (2010) Cloning and characterization of an exo-xylogucanase from rumenal microbial metagenome Protein Pept. Lett. 17, 803-808
30. Gloster, T. M., Ibatullin, F. M., Macauley, K., Eklof, J. M., Roberts, S., Turkenburg, J. P., Bjornvad, M. E., Jorgensen, P. L., Danielsen, S., Johansen, K. S., Borchert, T. V., Wilson, K. S., Brumer, H., and Davies, G. J. (2007) Characterization and three-dimensional structures of two distinct bacterial xyloglucanases from families GH5 and GH12 J. Biol. Chem. 282, 19177-19189
31. Larsbrink, J., Rogers, T. E., Hemsworth, G. R., McKee, L. S., Tauzin, A. S., Spadiut, O., Klinter, S., Pudlo, N. A., Urs, K., Koropatkin, N. M., Creagh, A. L., Haynes, C. A., Kelly, A. G., Cederholm, S. N., Davies, G. J., Martens, E. C., and Brumer, H. (2014) A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes Nature 506, 498-502
32. Eklof, J. M., Ruda, M. C., and Brumer, H. (2012) Distinguishing xyloglucanase activity in endo-beta(1 - >4)glucanases Methods Enzymol. 510, 97-120
33. Feng, T., Yan, K. P., Mikkelsen, M. D., Meyer, A. S., Schols, H. A., Westereng, B., and Mikkelsen, J. D. (2014) Characterisation of a novel endo-xyloglucanase (XcXGHA) from Xanthomonas that accommodates a xylosyl-substituted glucose at subsite -1 Appl. Microbiol. Biotechnol. 98, 9667-9679
34. Doublie, S. (2007) Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems Methods Mol. Biol. 363, 91-108
35. Van Duyne, G. D., Standaert, R. F., Karplus, P. A., Schreiber, S. L., and Clardy, J. (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin J. Mol. Biol. 229, 105-124
36. Doublie, S. (1997) Preparation of selenomethionyl proteins for phase determination Methods Enzymol. 276, 523-530
37. McPhillips, T. M., McPhillips, S. E., Chiu, H. J., Cohen, A. E., Deacon, A. M., Ellis, P. J., Garman, E., Gonzalez, A., Sauter, N. K., Phizackerley, R. P., Soltis, S. M., and Kuhn, P. (2002) Blu-Ice and the Distributed Control System: software for data acquisition and instrument control at macromolecular crystallography beamlines J. Synchrotron Radiat. 9, 401-406
38. Evans, G. and Pettifer, R. F. (2001) CHOOCH: a program for deriving anomalous-scattering factors from X-ray fluorescence spectra J. Appl. Crystallogr. 34, 82-86
39. Dauter, Z., Dauter, M., and Rajashankar, K. R. (2000) Novel approach to phasing proteins: derivatization by short cryo-soaking with halides Acta Crystallogr., Sect. D Biol. Crystallogr. 56, 232-237
40. Guimaraes, B. G., Sanfelici, L., Neuenschwander, R. T., Rodrigues, F., Grizolli, W. C., Raulik, M. A., Piton, J. R., Meyer, B. C., Nascimento, A. S., and Polikarpov, I. (2009) The MX2 macromolecular crystallography beamline: a wiggler X-ray source at the LNLS J. Synchrotron Radiat. 16, 69-75
41. Kabsch, W. (2010) Xds Acta Crystallogr., Sect. D, Biol. Crystallogr. 66, 125-132
42. Karplus, P. A. and Diederichs, K. (2012) Linking crystallographic model and data quality Science 336, 1030-1033
43. Sheldrick, G. M. (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification Acta Crystallogr., Sect. D Biol. Crystallogr. 66, 479-485
44. Terwilliger, T. C., Grosse-Kunstleve, R. W., Afonine, P. V., Moriarty, N. W., Zwart, P. H., Hung, L. W., Read, R. J., and Adams, P. D. (2008) Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard Acta Crystallogr., Sect. D Biol. Crystallogr. 64, 61-69
45. Vagin, A. and Teplyakov, A. (2010) Molecular replacement with MOLREP Acta Crystallogr.. Sect. D Biol. Crystallogr. 66, 22-25
46. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D Biol. Crystallogr. 53, 240-255
47. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr., Sect. D Biol. Crystallogr. 66, 486-501
48. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D Biol. Crystallogr. 66, 12-21
49. Terwilliger, T. C., Dimaio, F., Read, R. J., Baker, D., Bunkoczi, G., Adams, P. D., Grosse-Kunstleve, R. W., Afonine, P. V., and Echols, N. (2012) phenix.mr-rosetta: molecular replacement and model rebuilding with Phenix and Rosetta J. Struct. Funct. Genomics 13, 81-90
50. 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
51. Bianchetti, C. M., Brumm, P., Smith, R. W., Dyer, K., Hura, G. L., Rutkoski, T. J., and Phillips, G. N., Jr. (2013) Structure, dynamics, and specificity of endoglucanase D from Clostridium cellulovorans J. Mol. Biol. 425, 4267-4285
52. Aspeborg, H., Coutinho, P. M., Wang, Y., Brumer, H., 3rd, and Henrissat, B. (2012) Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5) BMC Evol. Biol. 12, 186
53. Tseng, C. W., Ko, T. P., Guo, R. T., Huang, J. W., Wang, H. C., Huang, C. H., Cheng, Y. S., Wang, A. H., and Liu, J. R. (2011) Substrate binding of a GH5 endoglucanase from the ruminal fungus Piromyces rhizinflata Acta Crystallogr., Sect. F Struct. Biol. Cryst. Commun. 67, 1189-1194
54. Kim, H. W. and Ishikawa, K. (2011) Functional analysis of hyperthermophilic endocellulase from Pyrococcus horikoshii by crystallographic snapshots Biochem. J. 437, 223-230
55. Sakon, J., Adney, W. S., Himmel, M. E., Thomas, S. R., and Karplus, P. A. (1996) Crystal structure of thermostable family 5 endocellulase E1 from Acidothermus cellulolyticus in complex with cellotetraose Biochemistry 35, 10648-10660
56. Patrick, W. M., Nakatani, Y., Cutfield, S. M., Sharpe, M. L., Ramsay, R. J., and Cutfield, J. F. (2010) Carbohydrate binding sites in Candida albicans exo-beta-1,3-glucanase and the role of the Phe-Phe 'clamp' at the active site entrance FEBS J. 277, 4549-4561
57. 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
58. Santos, C. R., Paiva, J. H., Sforca, M. L., Neves, J. L., Navarro, R. Z., Cota, J., Akao, P. K., Hoffmam, Z. B., Meza, A. N., Smetana, J. H., Nogueira, M. L., Polikarpov, I., Xavier-Neto, J., Squina, F. M., Ward, R. J., Ruller, R., Zeri, A. C., and Murakami, M. T. (2012) Dissecting structure-function-stability relationships of a thermostable GH5-CBM3 cellulase from Bacillus subtilis 168 Biochem. J. 441, 95-104
59. Cuyvers, S., Dornez, E., Delcour, J. A., and Courtin, C. M. (2012) Occurrence and functional significance of secondary carbohydrate binding sites in glycoside hydrolases Crit. Rev. Biotechnol. 32, 93-107
60. Yaoi, K., Kondo, H., Hiyoshi, A., Noro, N., Sugimoto, H., Tsuda, S., Mitsuishi, Y., and Miyazaki, K. (2007) The structural basis for the exo-mode of action in GH74 oligoxyloglucan reducing end-specific cellobiohydrolase J. Mol. Biol. 370, 53-62
61. Yaoi, K., Kondo, H., Hiyoshi, A., Noro, N., Sugimoto, H., Tsuda, S., and Miyazaki, K. (2009) The crystal structure of a xyloglucan-specific endo-beta-1,4-glucanase from Geotrichum sp. M128 xyloglucanase reveals a key amino acid residue for substrate specificity FEBS J. 276, 5094-5100
62. Damasio, A. R., Ribeiro, L. F., Ribeiro, L. F., Furtado, G. P., Segato, F., Almeida, F. B., Crivellari, A. C., Buckeridge, M. S., Souza, T. A., Murakami, M. T., Ward, R. J., Prade, R. A., and Polizeli, M. L. (2012) Functional characterization and oligomerization of a recombinant xyloglucan-specific endo-beta-1,4-glucanase (GH12) from Aspergillus niveus Biochim. Biophys. Acta 1824, 461-467
63. Martinez-Fleites, C., Guerreiro, C. I., Baumann, M. J., Taylor, E. J., Prates, J. A., Ferreira, L. M., Fontes, C. M., Brumer, H., and Davies, G. J. (2006) Crystal structures of Clostridium thermocellum xyloglucanase, XGH74A, reveal the structural basis for xyloglucan recognition and degradation J. Biol. Chem. 281, 24922-24933
64. Master, E. R., Zheng, Y., Storms, R., Tsang, A., and Powlowski, J. (2008) A xyloglucan-specific family 12 glycosyl hydrolase from Aspergillus niger: recombinant expression, purification and characterization Biochem. J. 411, 161-170