Characterization of the functional roles of amino acid residues in acceptor-binding subsite +1 in the active site of the glucansucrase GTF180 from lactobacillus reuteri 180

Journal of Biological Chemistry

Volumn 290, Issue 50, 2015, Pages 30131-30141

  Meng, Xiangfeng ^a   Pijning, Tjaard ^a   Dobruchowska, Justyna M ^a   Gerwig, Gerrit J ^a   Dijkhuizen, Lubbert ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYMES; POLYSACCHARIDES;

AMINO ACID RESIDUES; ENZYME ENGINEERING; LACTOBACILLUS REUTERI; LINKAGE SYNTHESIS; PRODUCT SPECIFICITY; SITE DIRECTED MUTAGENESIS; STRUCTURE-FUNCTION RELATIONSHIP; TRANSGLYCOSYLATION REACTION;

BIOCHEMICAL ENGINEERING;

ALANINE; AMINO ACID; ASPARAGINE; ASPARTIC ACID; GTF180 PROTEIN; LEUCINE; MALTOSE; PROLINE; SUCRASE; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG; ALTERNANSUCRASE; GLYCOSYLTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STRUCTURE; GLYCOSYLATION; LACTOBACILLUS REUTERI; MUTANT; MUTATION; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; CHEMISTRY; ENZYMOLOGY; GENETICS; MASS FRAGMENTOGRAPHY; METABOLISM; METHYLATION; MOLECULAR GENETICS; MUTAGENESIS; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; AMINO ACIDS; CATALYTIC DOMAIN; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GLYCOSYLTRANSFERASES; LACTOBACILLUS REUTERI; METHYLATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTON MAGNETIC RESONANCE SPECTROSCOPY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84949633712     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.687558     Document Type: Article

References (43)

1. Badel, S., Bernardi, T., and Michaud, P. (2011) New perspectives for lactobacilli exopolysaccharides. Biotechnol. Adv. 29, 54-66
2. Jolly,L.,Vincent,S.J.,Duboc,P.,andNeeser,J.R.(2002)Exploitingexpolysaccharides from lactic acid bacteria. Antonie Van Leeuwenhoek 82, 367-374
3. Monsan, P., Bozonnet, S., Albenne, C., Joucla, G., Willemot, R.-M., and Remaud-Simeon, M. (2001) Homopolysaccharides from lactic acid bacteria. Int. Dairy J. 11, 675-685
4. Welman, A. D., and Maddox, I. S. (2003) Exopolysaccharides from lactic acid bacteria: Perspectives and challenges. Trends Biotechnol. 21, 269-274
5. Leemhuis, H., Pijning, T., Dobruchowska, J. M., van Leeuwen, S. S., Kralj, S., Dijkstra, B. W., and Dijkhuizen, L. (2013) Glucansucrases: Three-dimensional structures, reactions, mechanism, α-glucan analysis and their implications in biotechnology and food applications. J. Biotechnol. 163, 250-272
6. Naessens, M., Cerdobbel, A., Soetaert, W., and Vandamme, E. J. (2005) Leuconostoc dextransucrase and dextran: Production, properties and applications. J. Chem. Technol. Biotechnol. 80, 845-860
7. Monchois, V., Willemot, R.-M., and Monsan, P. (1999) Glucansucrases: Mechanism of action and structure-function relationships. FEMS Microbiol. Rev. 23, 131-151
8. 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
9. Kralj, S., van Geel-Schutten, I. G., Faber, E. J., van der Maarel, M. J., and Dijkhuizen, L. (2005) Rational transformation of Lactobacillus reuteri 121 reuteransucrase into a dextransucrase. Biochemistry 44, 9206-9216
10. Svensson, B. (1994) Protein engineering in the α-amylase family: Catalytic mechanism, substrate specificity, and stability. Plant Mol. Biol. 25, 141-157
11. MacGregor, E. A., Jespersen, H. M., and Svensson, B. (1996) A circularly permuted α-amylase-type α/β-barrel structure in glucan-synthesizing glucosyltransferases. FEBS Lett. 378, 263-266
12. Vujičić-Žagar, A., Pijning, T., Kralj, S., Lopez, C. A., Eeuwema, W., Dijkhuizen, L., and Dijkstra, B. W. (2010) Crystal structure of a 117-kDa glucansucrase fragment provides insight into evolution and product specificity of GH70 enzymes. Proc. Natl. Acad. Sci. U.S.A. 107, 21406-21411
13. Cote, G. L., and Sheng, S. (2006) Penta-, hexa-, and heptasaccharide acceptor products of alternansucrase. Carbohydr. Res. 341, 2066-2072
14. Cote, G. L. (2009) Acceptor products of alternansucrase with gentiobiose. Production of novel oligosaccharides for food and feed and elimination of bitterness. Carbohydr. Res. 344, 187-190
15. Desmet, T., Soetaert, W., Bojarova, P., Kr?en, V., Dijkhuizen, L., Eastwick-Field, V., and Schiller, A. (2012) Enzymatic glycosylation of small molecules: Challenging substrates require tailored catalysts. Chem. Eur. J. 18, 10786-107801
16. Seo, E.-S., Lee, J.-H., Park, J.-Y., Kim, D., Han, H.-J., and Robyt, J. F. (2005) Enzymatic synthesis and anti-coagulant effect of salicin analogs by using the Leuconostoc mesenteroides glucansucrase acceptor reaction. J. Biotechnol. 117, 31-38
17. Leemhuis, H., Pijning, T., Dobruchowska, J. M., Dijkstra, B. W., and Dijkhuizen, L. (2012) Glycosidic bond specificity of glucansucrases: On the role of acceptor substrate binding residues. Biocatal. Biotransform. 30, 366-376
18. Brison, Y., Pijning, T., Malbert, Y., Fabre, E., Mourey, L., Morel, S., Potocki-Veronese, G., Monsan, P., Tranier, S., Remaud-Simeon, M., and Dijkstra, B. W. (2012) Functional and structural characterization of α-(1→2) branching sucrase derived from DSR-E glucansucrase. J. Biol. Chem. 287, 7915-7924
19. Bozonnet, S., Dols-Laffargue, M., Fabre, E., Pizzut, S., Remaud-Simeon, M., Monsan, P., and Willemot, R.-M. (2002) Molecular characterization of DSR-E, an α-1,2 linkage-synthesizing dextransucrase with two catalytic domains. J. Bacteriol. 184, 5753-5761
20. Brison, Y., Fabre, E., Moulis, C., Portais, J. C., Monsan, P., and Remaud-Simeon, M. (2010) Synthesis of dextrans with controlled amounts ofα-1,2 linkages using the transglucosidase GBD-CD2. Appl. Microbiol. Biotechnol. 86, 545-554
21. Brison, Y., Laguerre, S., Lefoulon, F., Morel, S., Monties, N., Potocki-Veronese, G., Monsan, P., and Remaud-Simeon, M. (2013) Branching pattern of gluco-oligosaccharides and 1.5-kDa dextran grafted by the α-1,2 branching sucrase GBD-CD2. Carbohydr. Polym. 94, 567-576
22. Moulis, C., Joucla, G., Harrison, D., Fabre, E., Potocki-Veronese, G., Monsan, P., and Remaud-Simeon, M. (2006) Understanding the polymerization mechanism of glycoside-hydrolase family 70 glucansucrases. J. Biol. Chem. 281, 31254-31267
23. van Hijum, S. A., Kralj, S., Ozimek, L. K., Dijkhuizen, L., and van Geel-Schutten, I. G. (2006) Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol. Mol. Biol. Rev. 70, 157-176
24. Cote, G. L., and Skory, C. D. (2014) Effects of mutations at threonine-654 on the insoluble glucan synthesized by Leuconostoc mesenteroides NRRL B-1118 glucansucrase. Appl. Microbiol. Biotechnol. 98, 6651-6658
25. Hellmuth, H., Wittrock, S., Kralj, S., Dijkhuizen, L., Hofer, B., and Seibel, J. (2008) Engineering the glucansucrase GTFR enzyme reaction and glycosidic bond specificity: Toward tailor-made polymer and oligosaccharide products. Biochemistry 47, 6678-6684
26. Monchois, V., Vignon, M., and Russell, R. R. (2000) Mutagenesis of Asp-569 of glucosyltransferase I glucansucrase modulates glucan and oligosaccharide synthesis. Appl. Environ. Microbiol. 66, 1923-1927
27. van Leeuwen, S. S., Kralj, S., Eeuwema, W., Gerwig, G. J., Dijkhuizen, L., and Kamerling, J. P. (2009) Structural characterization of bioengineered α-D-glucans produced by mutant glucansucrase GTF180 enzymes of Lactobacillus reuteri strain 180. Biomacromolecules 10, 580-588
28. Kralj, S., Eeuwema, W., Eckhardt, T. H., and Dijkhuizen, L. (2006) Role of asparagine 1134 in glucosidic bond and transglycosylation specificity of reuteransucrase from Lactobacillus reuteri 121. FEBS J. 273, 3735-3742
29. van Leeuwen, S. S., Kralj, S., van Geel-Schutten, I. H., Gerwig, G. J., Dijkhuizen, L., and Kamerling, J. P. (2008) Structural analysis of the α-Dglucan (EPS180) produced by the Lactobacillus reuteri strain 180 glucansucrase GTF180 enzyme. Carbohydr. Res. 343, 1237-1250
30. Davies, G. J., Wilson, K. S., and Henrissat, B. (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321, 557-559
31. Irague, R., Tarquis, L., Andre, I., Moulis, C., Morel, S., Monsan, P., Potocki-Veronese, G., and Remaud-Simeon, M. (2013) Combinatorial engineering of dextransucrase specificity. PloS one 8, e77837
32. Meng, X., Dobruchowska, J. M., Pijning, T., Lopez, C. A., Kamerling, J. P., and Dijkhuizen, L. (2014) Residue Leu940 has a crucial role in the linkage and reaction specificity of the glucansucrase GTF180 of the probiotic bacterium Lactobacillus reuteri 180. J. Biol. Chem. 289, 32773-32782
33. Tsumori, H., Minami, T., and Kuramitsu, H. K. (1997) Identification of essential amino acids in the Streptococcus mutans glucosyltransferases. J. Bacteriol. 179, 3391-3396
34. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: Analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308
35. Miller, G. L. (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31, 426-428
36. Kralj, S., van Geel-Schutten, G. H., van der Maarel, M. J., and Dijkhuizen, L. (2004) Biochemical and molecular characterization of Lactobacillus reuteri 121 reuteransucrase. Microbiology 150, 2099-2112
37. Van Geel-Schutten, G. H., Faber, E. J., Smit, E., Bonting, K., Smith, M. R., Ten Brink, B., Kamerling, J. P., Vliegenthart, J. F., and Dijkhuizen, L. (1999) Biochemical and structural characterization of the glucan and fructan exopolysaccharides synthesized by the Lactobacillus reuteri wild-type strain and by mutant strains. Appl. Environ. Microbiol. 65, 3008-3014
38. Ciucanu,I.,andKerek,F.(1984)Asimpleandrapidmethodforthepermethylation of carbohydrates. Carbohydr. Res. 131, 209-217
39. van Leeuwen, S. S., Leeflang, B. R., Gerwig, G. J., and Kamerling, J. P. (2008) Development of a 1H NMR structural-reporter-group concept for the primary structural characterisation of α-D-glucans. Carbohydr. Res. 343, 1114-1119
40. van Leeuwen, S. S., Kralj, S., Gerwig, G. J., Dijkhuizen, L., and Kamerling, J. P. (2008) Structural analysis of bioengineered α-D-glucan produced by a triple mutant of the glucansucrase GTF180 enzyme from Lactobacillus reuteri strain 180: Generation of (α1→4) linkages in a native (1→3)/(1→6)-α-D-glucan. Biomacromolecules 9, 2251-2258
41. Ito, K., Ito, S., Shimamura, T., Weyand, S., Kawarasaki, Y., Misaka, T., Abe, K., Kobayashi, T., Cameron, A. D., and Iwata, S. (2011) Crystal structure of glucansucrase from the dental caries pathogen Streptococcus mutans. J. Mol. Biol. 408, 177-186
42. Irague, R., Massou, S., Moulis, C., Saurel, O., Milon, A., Monsan, P., Remaud-Simeon, M., Portais, J. C., and Potocki-Veronese, G. (2011) NMRbased structural glycomics for high-throughput screening of carbohydrate-active enzyme specificity. Anal. Chem. 83, 1202-1206
43. Irague, R., Rolland-Sabate, A., Tarquis, L., Doublier, J. L., Moulis, C., Monsan, P., Remaud-Simeon, M., Potocki-Veronese, G., and Buleon, A. (2012) Structure and property engineering of α-D-glucans synthesized by dextransucrase mutants. Biomacromolecules 13, 187-195