Metal Dependence of the Xylose Isomerase from Piromyces sp. E2 Explored by Activity Profiling and Protein Crystallography

Biochemistry

Volumn 56, Issue 45, 2017, Pages 5991-6005

  Lee, Misun ^a   Rozeboom, Henriëtte J ^a   De Waal, Paul P ^b   De Jong, Rene M ^b   Dudek, Hanna M ^a,c   Janssen, Dick B ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b DSM BIOTECHNOLOGY CENTER   (Netherlands)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING SITES; BINS; CARBOXYLATION; CATALYST ACTIVITY; ENZYMES; ESCHERICHIA COLI; MANGANESE; METAL ANALYSIS; SUBSTRATES; XYLOSE; YEAST;

ACTIVITY PROFILING; BIOCHEMICAL PROPERTIES; CATALYTIC PROPERTIES; HIGH LEVEL EXPRESSION; ISOMERASE ACTIVITY; METAL BINDING SITES; PROTEIN CRYSTALLOGRAPHY; XYLOSE UTILIZATIONS;

METALS;

ALCOHOL; ASPARTIC ACID; CADMIUM; CALCIUM ION; CARBOXYLIC ACID; COBALT; FERROUS ION; GLUTAMIC ACID; HISTIDINE; MAGNESIUM; MANGANESE; METAL; NICKEL; TRYPTOPHAN; XYLOSE; XYLOSE ISOMERASE; XYLULOSE; ISOMERASE; XYLITOL;

ACTIVATION CONSTANT; ALCOHOL PRODUCTION; ALPHA HELIX; ARTICLE; BINDING AFFINITY; BIOTECHNOLOGICAL PRODUCTION; CHEMICAL ANALYSIS; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ISOLATION; ENZYME MECHANISM; ENZYME SUBSTRATE; IN VIVO STUDY; ISOMERIZATION; METAL BINDING; NONHUMAN; PIROMYCES; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; BINDING SITE; CATALYSIS; CHEMISTRY; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

ALDOSE-KETOSE ISOMERASES; BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; METALS; MODELS, MOLECULAR; PIROMYCES; PROTEIN CONFORMATION; XYLITOL; XYLOSE;

EID: 85034092831     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.7b00777     Document Type: Article

References (76)

1. Hahn-Hägerdal, B., Karhumaa, K., Fonseca, C., Spencer-Martins, I., and Gorwa-Grauslund, M. F. (2007) Towards industrial pentose-fermenting yeast strains Appl. Microbiol. Biotechnol. 74, 937-953 10.1007/s00253-006-0827-2
2. Sànchez Nogué, V. and Karhumaa, K. (2015) Xylose fermentation as a challenge for commercialization of lignocellulosic fuels and chemicals Biotechnol. Lett. 37, 761-772 10.1007/s10529-014-1756-2
3. Madhavan, A., Tamalampudi, S., Ushida, K., Kanai, D., Katahira, S., Srivastava, A., Fukuda, H., Bisaria, V. S., and Kondo, A. (2009) Xylose isomerase from polycentric fungus Orpinomyces: gene sequencing, cloning, and expression in Saccharomyces cerevisiae for bioconversion of xylose to ethanol Appl. Microbiol. Biotechnol. 82, 1067-78 10.1007/s00253-008-1794-6
4. Hector, R. E., Dien, B. S., Cotta, M. A., and Mertens, J. A. (2013) Growth and fermentation of D-xylose by Saccharomyces cerevisiae expressing a novel D-xylose isomerase originating from the bacterium Prevotella ruminicola TC2-24 Biotechnol. Biofuels 6, 84 10.1186/1754-6834-6-84
5. Kuyper, M., Harhangi, H. R., Stave, A. K., Winkler, A. A., Jetten, M. S. M., de Laat, W. T. A. M., den Ridder, J. J. J., Op den Camp, H. J. M, van Dijken, J. P., and Pronk, J. T. (2003) High-level functional expression of a fungal xylose isomerase: the key to efficient ethanolic fermentation of xylose by Saccharomyces cerevisiae FEMS Yeast Res. 4, 69-78 10.1016/S1567-1356(03)00141-7
6. de Figueiredo Vilela, L., de Mello, V. M., Reis, V. C. B., Bon, E. P. da S., Gonçalves Torres, F. A., Neves, B. C., and Eleutherio, E. C. A. (2013) Functional expression of Burkholderia cenocepacia xylose isomerase in yeast increases ethanol production from a glucose-xylose blend Bioresour. Technol. 128, 792-796 10.1016/j.biortech.2012.10.014
7. Matsushika, A., Inoue, H., Kodaki, T., and Sawayama, S. (2009) Ethanol production from xylose in engineered Saccharomyces cerevisiae strains: Current state and perspectives Appl. Microbiol. Biotechnol. 84, 37-53 10.1007/s00253-009-2101-x
8. Walfridsson, M., Anderlund, M., Bao, X., and Hahn-Hägerdal, B. (1997) Expression of different levels of enzymes from the Pichia stipitisXYL1 and XYL2 genes in Saccharomyces cerevisiae and its effects on product formation during xylose utilisation Appl. Microbiol. Biotechnol. 48, 218-224 10.1007/s002530051041
9. Young, E., Lee, S., and Alper, H. (2010) Optimizing pentose utilization in yeast: the need for novel tools and approaches Biotechnol. Biofuels 3, 24 10.1186/1754-6834-3-24
10. Karhumaa, K., Garcia Sanchez, R., Hahn-Hägerdal, B., and Gorwa-Grauslund, M.-F. (2007) Comparison of the xylose reductase-xylitol dehydrogenase and the xylose isomerase pathways for xylose fermentation by recombinant Saccharomyces cerevisiae Microb. Cell Fact. 6, 5 10.1186/1475-2859-6-5
11. Bhosale, S. H., Rao, M. B., and Deshpande, V. V. (1996) Molecular and industrial aspects of glucose isomerase Microbiol. Rev. 60, 280-300
12. Amore, R., Wilhelm, M., and Hollenberg, C. P. (1989) The fermentation of xylose-an analysis of the expression of Bacillus and Actinoplanes xylose isomerase genes in yeast Appl. Microbiol. Biotechnol. 30, 351-357 10.1007/BF00296623
13. Moes, C., Pretorius, I., and van Zyl, W. H. (1996) Cloning and expression of the Clostridium thermosulfurogenes D-xylose isomerase gene (xyLA) in Saccharomyces cerevisiae Biotechnol. Lett. 18, 269-274 10.1007/BF00142943
14. Sarthy, A. V., Mcconaughy, B. L., Lobo, Z., Sundstorm, J. A., Furlong, C. E., and Hall, B. D. (2000) Expression of the Escherichia coli xylose isomerase gene in Saccharomyces cerevisiae Appl. Environ. Microbiol. 53, 1996-2000
15. Gárdonyi, M. and Hahn-Hägerdal, B. (2003) The Streptomyces rubiginosus xylose isomerase is misfolded when expressed in Saccharomyces cerevisiae Enzyme Microb. Technol. 32, 252-259 10.1016/S0141-0229(02)00285-5
16. Walfridsson, M., Bao, X., Anderlund, M., Lilius, G., Bülow, L., and Hahn-Hägerdal, B. (1996) Ethanolic fermentation of xylose with Saccharomyces cerevisiae harboring the Thermus thermophilus xylA gene, which expresses an active xylose (glucose) isomerase Appl. Environ. Microbiol. 62, 4648-4651
17. Harhangi, H., Akhmanova, A. S., Emmens, R., van der Drift, C., de Laat, W. T. A. M., van Dijken, J. P., Jetten, M. S. M., Pronk, J. T., and Op den Camp, H. J. M. (2003) Xylose metabolism in the anaerobic fungus Piromyces sp. strain E2 follows the bacterial pathway Arch. Microbiol. 180, 134-141 10.1007/s00203-003-0565-0
18. van Maris, A. J. A., Winkler, A. A., Kuyper, M., de Laat, W. T. A. M., van Dijken, J. P., and Pronk, J. T. (2007) Development of efficient xylose fermentation in Saccharomyces cerevisiae: xylose isomerase as a key component Adv. Biochem. Eng./Biotechnol. 108, 179-204 10.1007/10-2007-057
19. Brat, D., Boles, E., and Wiedemann, B. (2009) Functional expression of a bacterial xylose isomerase in Saccharomyces cerevisiae Appl. Environ. Microbiol. 75, 2304-11 10.1128/AEM.02522-08
20. Zhou, H., Cheng, J.-s., Wang, B. L., Fink, G. R., and Stephanopoulos, G. (2012) Xylose isomerase overexpression along with engineering of the pentose phosphate pathway and evolutionary engineering enable rapid xylose utilization and ethanol production by Saccharomyces cerevisiae Metab. Eng. 14, 611-622 10.1016/j.ymben.2012.07.011
21. Kuyper, M., Hartog, M. M. P., Toirkens, M. J., Almering, M. J. H., Winkler, A. A., van Dijken, J. P., and Pronk, J. T. (2005) Metabolic engineering of a xylose-isomerase-expressing Saccharomyces cerevisiae strain for rapid anaerobic xylose fermentation FEMS Yeast Res. 5, 399-409 10.1016/j.femsyr.2004.09.010
22. Wisselink, H. W., Toirkens, M. J., del Rosario Franco Berriel, M., Winkler, A. A., van Dijken, J. P., Pronk, J. T., and Van Maris, A. J. A. (2007) Engineering of Saccharomyces cerevisiae for efficient anaerobic alcoholic fermentation of L-arabinose Appl. Environ. Microbiol. 73, 4881-4891 10.1128/AEM.00177-07
23. Kuyper, M., Toirkens, M. J., Diderich, J. A., Winkler, A. A., van Dijken, J. P., and Pronk, J. T. (2005) Evolutionary engineering of mixed-sugar utilization by a xylose-fermenting Saccharomyces cerevisiae strain FEMS Yeast Res. 5, 925-34 10.1016/j.femsyr.2005.04.004
24. Lee, S. M., Jellison, T., and Alper, H. S. (2012) Directed evolution of xylose isomerase for improved xylose catabolism and fermentation in the yeast Saccharomyces cerevisiae Appl. Environ. Microbiol. 78, 5708-16 10.1128/AEM.01419-12
25. Fuxreiter, M., Farkas, Ö., and Náray-Szabó, G. (1995) Molecular modelling of xylose isomerase catalysis: The role of electrostatics and charge transfer to metals Protein Eng., Des. Sel. 8, 925-933 10.1093/protein/8.9.925
26. Kovalevsky, A. Y., Hanson, L., Fisher, S. Z., Mustyakimov, M., Mason, S. A., Trevor Forsyth, V., Blakeley, M. P., Keen, D. A., Wagner, T., Carrell, H. L., Katz, A. K., Glusker, J. P., and Langan, P. (2010) Metal ion roles and the movement of hydrogen during reaction catalyzed by D-xylose isomerase: A joint x-ray and neutron diffraction study Structure 18, 688-699 10.1016/j.str.2010.03.011
27. 2+-inhibition and metal competence in the double mutant D254E/D256E Proteins: Struct., Funct., Genet. 28, 183-193 10.1002/(SICI)1097-0134(199706)28:2<183::AID-PROT7>3.0.CO;2-G
28. 2+-activated D-xylose isomerases Biochem. J. 278, 285-292 10.1042/bj2780285
29. Callens, M., Tomme, P., Kersters-Hilderson, H., Cornelis, R., Vangrysperre, W., and De Bruyne, C. K. (1988) Metal ion binding to D-xylose isomerase from Streptomyces violaceoruber Biochem. J. 250, 285-290 10.1042/bj2500285
30. Rangarajan, M. and Hartley, B. S. (1992) Mechanism of D-fructose isomerization by Arthrobacter D-xylose isomerase Biochem. J. 283, 223-233 10.1042/bj2830223
31. van Tilbeurgh, H., Jenkins, J., Chiadmi, M., Janin, J., Wodak, S. J., Mrabet, N. T., and Lambeir, A. M. (1992) Protein engineering of xylose (glucose) isomerase from Actinoplanes missouriensis. 3. Changing metal specificity and the pH profile by site- directed mutagenesis Biochemistry 31, 5467-5471 10.1021/bi00139a007
32. Smith, C., Rangarajan, M., and Hartley, B. (1991) D-Xylose (D-glucose) isomerase from Arthrobacter strain NRRL B3728. Purification and properties Biochem. J. 277, 255-261 10.1042/bj2770255
33. Verhoeven, M. D., Lee, M., Kamoen, L., van den Broek, M., Janssen, D. B., Daran, J.-M. G., van Maris, A. J. A., and Pronk, J. T. (2017) Mutations in PMR1 stimulate xylose isomerase activity and anaerobic growth on xylose of engineered Saccharomyces cerevisiae by influencing manganese homeostasis Sci. Rep. 7, 46155 10.1038/srep46155
34. Han, B., Bong, S. M., Cho, J., Kim, M., Kim, S. J., and Lee, B. I. (2015) Crystal structure of a Class 2 D-xylose isomerase from the human intestinal tract microbe Bacteroides thetaiotaomicron Bio Design 289, 41-47
35. Yamanaka, K. (1974) Enzymatic assay of D-xylose isomerase with D-sorbitol dehydrogenase Agric. Biol. Chem. 38, 2035-2037 10.1271/bbb1961.38.2035
36. Matthews, B. W. (1968) Solvent content of protein crystals J. Mol. Biol. 33, 491-497 10.1016/0022-2836(68)90205-2
37. Berejnov, V., Husseini, N. S., Alsaied, O. A., and Thorne, R. E. (2006) Effects of cryoprotectant concentration and cooling rate on vitrification of aqueous solutions J. Appl. Crystallogr. 39, 244-251 10.1107/S0021889806004717
38. Battye, T. G. G., Kontogiannis, L., Johnson, O., Powell, H. R., and Leslie, A. G. W. (2011) iMOSFLM: A new graphical interface for diffraction-image processing with MOSFLM Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 271-281 10.1107/S0907444910048675
39. Evans, P. R. and Murshudov, G. N. (2013) How good are my data and what is the resolution? Acta Crystallogr., Sect. D: Biol. Crystallogr. 69, 1204-1214 10.1107/S0907444913000061
40. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674 10.1107/S0021889807021206
41. Langer, G. G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Nat. Protoc. 3, 1171-1179 10.1038/nprot.2008.91
42. 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 10.1107/S0907444910007493
43. 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., Sect. D: Biol. Crystallogr. 67, 355-367 10.1107/S0907444911001314
44. 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., Sect. D: Biol. Crystallogr. 66, 213-221 10.1107/S0907444909052925
45. Chen, V. B., Arendall, W. B., 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 10.1107/S0907444909042073
46. Krissinel, E. and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2256-2268 10.1107/S0907444904026460
47. Robert, X. and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server Nucleic Acids Res. 42, W320-W324 10.1093/nar/gku316
48. Sugahara, M., Mizohata, E., Nango, E., Suzuki, M., Tanaka, T., Masuda, T., Tanaka, R., Shimamura, T., Tanaka, Y., Suno, C., Ihara, K., Pan, D., Kakinouchi, K., Sugiyama, S., Murata, M., Inoue, T., Tono, K., Song, C., Park, J., Kameshima, T., Hatsui, T., Joti, Y., Yabashi, M., and Iwata, S. (2014) Grease matrix as a versatile carrier of proteins for serial crystallography Nat. Methods 12, 61-63 10.1038/nmeth.3172
49. Pei, J., Kim, B.-H., and Grishin, N. V. (2008) PROMALS3D: a tool for multiple protein sequence and structure alignments Nucleic Acids Res. 36, 2295-300 10.1093/nar/gkn072
50. Gouet, P., Courcelle, E., Stuart, D., and Metoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 15, 305-308 10.1093/bioinformatics/15.4.305
51. Allen, K. N., Lavie, A., Glasfeld, A., Tanada, T. N., Gerrity, D. P., Carlson, S. C., Farber, G. K., Petsko, G. A., and Ringe, D. (1994) Role of the divalent metal ion in sugar binding, ring opening, and isomerization by D-xylose isomerase: replacement of a catalytic metal by an amino acid Biochemistry 33, 1488-94 10.1021/bi00172a027
52. Valli, M., Sauer, M., Branduardi, P., Borth, N., Porro, D., and Mattanovich, D. (2005) Intracellular pH distribution in Saccharomyces cerevisiae cell populations, analyzed by flow cytometry Appl. Environ. Microbiol. 71, 1515-1521 10.1128/AEM.71.3.1515-1521.2005
53. Palmqvist, E. and Hahn-Hägerdal, B. (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition Bioresour. Technol. 74, 25-33 10.1016/S0960-8524(99)00161-3
54. Harding, M. M. (2001) Geometry of metal-ligand interactions in proteins Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 401-411 10.1107/S0907444900019168
55. Whitlow, M., Howard, A. J., Finzel, B. C., Poulos, T. L., Winborne, E., and Gilliland, G. L. (1991) A metal-mediated hydride shift mechanism for xylose isomerase based on the 1.6 Å Streptomycs rubiginosus structure with xylitol and D-xylose Proteins: Struct., Funct., Genet. 9, 153-173 10.1002/prot.340090302
56. Rozeboom, H. J., Yu, S., Madrid, S., Kalk, K. H., Zhang, R., and Dijkstra, B. W. (2013) Crystal structure of α-1,4-glucan lyase, a unique glycoside hydrolase family member with a novel catalytic mechanism J. Biol. Chem. 288, 26764-74 10.1074/jbc.M113.485896
57. Kovalevsky, A. Y., Katz, A. K., Carrell, H. L., Hanson, L., Mustyakimov, M., Fisher, S. Z., Coates, L., Schoenborn, B. P., Bunick, G. J., Glusker, J. P., and Langan, P. (2008) Hydrogen location in stages of an enzyme-catalyzed reaction: Time-of-flight neutron structure of D-xylose isomerase with bound D-xylulose Biochemistry 47, 7595-7597 10.1021/bi8005434
58. Katz, A. K., Li, X., Carrell, H. L., Hanson, B. L., Langan, P., Coates, L., Schoenborn, B. P., Glusker, J. P., and Bunick, G. J. (2006) Locating active-site hydrogen atoms in D-xylose isomerase: time-of-flight neutron diffraction Proc. Natl. Acad. Sci. U. S. A. 103, 8342-7 10.1073/pnas.0602598103
59. Collyer, C. A., Henrick, K., and Blow, D. M. (1990) Mechanism for aldose-ketose interconversion by D-xylose isomerase involving ring opening followed by a 1,2-hydride shift J. Mol. Biol. 212, 211-235 10.1016/0022-2836(90)90316-E
60. Garcia-Viloca, M., Alhambra, C., Truhlar, D. G., and Gao, J. (2003) Hydride transfer catalyzed by xylose isomerase: Mechanism and quantum effects J. Comput. Chem. 24, 177-190 10.1002/jcc.10154
61. Collyer, C. A. and Blow, D. M. (1990) Observations of reaction intermediates and the mechanism of aldose-ketose interconversion by D-xylose isomerase Proc. Natl. Acad. Sci. U. S. A. 87, 1362-6 10.1073/pnas.87.4.1362
62. Jenkins, J., Janin, J., Rey, F., Chiadmi, M., van Tilbeurgh, H., Lasters, I., de Maeyer, M., Ven Belle, D., Wodak, S. J., Lauwereys, M., Stanssens, P., Mrabet, N. T., Snauwaert, J., Matthyssens, G., and Lambeir, A. (1992) Protein engineering of xylose (glucose) isomerase from Actinoplanes missouriensis. 1. Crystallography and site-directed mutagenesis of metal binding sites Biochemistry 31, 5449-5458 10.1021/bi00139a005
63. Kovalevsky, A., Hanson, B. L., Mason, S. A., Forsyth, V. T., Fisher, Z., Mustyakimov, M., Blakeley, M. P., Keen, D. A., and Langan, P. (2012) Inhibition of D-xylose isomerase by polyols: atomic details by joint X-ray/neutron crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 68, 1201-6 10.1107/S0907444912024808
64. Carrell, H. L., Hoier, H., and Glusker, J. P. (1994) Modes of binding substrates and their analogues to the enzyme D-xylose isomerase Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 113-123 10.1107/S0907444993009345
65. 3+ complex of the D254,256E mutant of Arthrobacter D -xylose isomerase at 2.40 Å resolution. Further evidence for inhibitor-induced metal ion movement Int. J. Biol. Macromol. 25, 329-336 10.1016/S0141-8130(99)00051-3
66. Fenn, T. D., Ringe, D., and Petsko, G. A. (2004) Xylose isomerase in substrate and inhibitor michaelis states: atomic resolution studies of a metal-mediated hydride shift Biochemistry 43, 6464-74 10.1021/bi049812o
67. Karaoglu, H., Yanmis, D., Sal, F. A., Celik, A., Canakci, S., and Belduz, A. O. (2013) Biochemical characterization of a novel glucose isomerase from Anoxybacillus gonensis G2T that displays a high level of activity and thermal stability J. Mol. Catal. B: Enzym. 97, 215-224 10.1016/j.molcatb.2013.08.019
68. Callens, M., Kersters-Hilderson, H., Van Opstal, O., and De Bruyne, C. K. (1986) Catalytic properties of D-xylose isomerase from Streptomyces violaceoruber Enzyme Microb. Technol. 8, 696-700 10.1016/0141-0229(86)90069-4
69. Lee, C. Y. and Zeikus, J. G. (1991) Purification and characterization of thermostable glucose isomerase from Clostridium thermosulfurogenes and Thermoanaerobacter strain B6A Biochem. J. 273, 565-571 10.1042/bj2730565
70. Henrick, K., Collyer, C. A., and Blow, D. M. (1989) Structures of D-xylose isomerase from Arthrobacter strain B3728 containing the inhibitors xylitol and D-sorbitol at 2.5 Å and 2.3 Å resolution, respectively J. Mol. Biol. 208, 129-157 10.1016/0022-2836(89)90092-2
71. Ben Hlima, H., Ayadi, D., Aghajari, N., and Bejar, S. (2013) Differential properties of native and tagged or untagged recombinant glucose isomerases of Streptomyces sp. SK and possible implication of the glycosylation J. Mol. Catal. B: Enzym. 94, 82-87 10.1016/j.molcatb.2013.05.008
72. Staudigl, P., Haltrich, D., and Peterbauer, C. K. (2014) L-arabinose isomerase and D-xylose isomerase from Lactobacillus reuteri: Characterization, coexpression in the food grade host Lactobacillus plantarum, and application in the conversion of D-galactose and D-glucose J. Agric. Food Chem. 62, 1617-1624 10.1021/jf404785m
73. Srih-Belghith, K. and Bejar, S. (1998) A thermostable glucose isomerase having a relatively low optimum pH: Study of activity and molecular cloning of the corresponding gene Biotechnol. Lett. 20, 553-556 10.1023/A:1005393510435
74. Liu, S. Y., Wiegel, J., and Gherardini, F. C. (1996) Purification and cloning of a thermostable xylose (glucose) isomerase with an acidic pH optimum from Thermoanaerobacterium strain JW/SL-YS 489 J. Bacteriol. 178, 5938-5945 10.1128/jb.178.20.5938-5945.1996
75. van Bastelaere, P. B. M., Kersters-Hilderson, H. L. M., and Lambeir, A. M. (1995) Wild-type and mutant D-xylose isomerase from Actinoplanes missouriensis: metal-ion dissociation constants, kinetic parameters of deuterated and non-deuterated substrates and solvent-isotope effects Biochem. J. 307, 135-142 10.1042/bj3070135
76. Cha, J. and Batt, C. (1998) Lowering the pH optimum of D-xylose isomerase: the effect of mutations of the negatively charged residues Mol. Cells 8, 374-382