Engineering the glucansucrase GTFR enzyme reaction and glycosidic bond specificity: Toward tailor-made polymer and oligosaccharide products

Biochemistry

Volumn 47, Issue 25, 2008, Pages 6678-6684

  Hellmuth, Hendrik ^a   Wittrock, Sabine ^b   Kralj, Slavko ^c   Dijkhuizen, Lubbert ^c   Hofer, Bernd ^b   Seibel, Jürgen ^a,b  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACCEPTOR SUBSTRATE (GALACTOSE); AMERICAN CHEMICAL SOCIETY (ACS); EFFECTIVE TOOL; ENZYME ENGINEERING; ENZYME REACTIONS; GLYCOSIDIC BONDS; GLYCOSIDIC LINKAGES; NOVEL POLYMERS; RANDOM MUTAGENESIS; SATURATION MUTAGENESIS; SYNTHESIS (OF CHIRAL IONIC LIQUIDS); TRANS GLYCOSYLATION ACTIVITY; TRANSGLYCOSYLATION REACTION; TRANSITION STATE (TS);

ADDITION REACTIONS; BIOCHEMICAL ENGINEERING; CHAINS; CHEMICALS; ENZYMES; FOOD ADDITIVES; GLUCOSE; MUTAGENESIS; OLIGOSACCHARIDES; POLYMERS; POLYSACCHARIDES; REGIOSELECTIVITY; SUGAR (SUCROSE); SUGARS; TECHNOLOGY;

REACTION KINETICS;

GLUCANSUCRASE; ISOMALTOSE; LEUCROSE; SUCRASE;

ARTICLE; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME MECHANISM; ENZYME SPECIFICITY; GENETIC LINKAGE; GLYCOSYLATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS ORALIS; SYNTHESIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CARBOHYDRATE SEQUENCE; CHROMATOGRAPHY, THIN LAYER; ENZYME ASSAYS; GLUCANS; GLUCOSYLTRANSFERASES; GLYCOSIDES; GLYCOSYLATION; GLYCOSYLTRANSFERASES; HYDROLYSIS; KINETICS; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MUTATION; OLIGOSACCHARIDES; POLYMERS; PROTEIN ENGINEERING; STREPTOCOCCUS ORALIS; SUBSTRATE SPECIFICITY;

STREPTOCOCCUS ORALIS;

EID: 45749092119     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800563r     Document Type: Article

References (50)

1. Seibel, J., Moraru, R., and Götze, S. (2005) Biocatalytic and chemical investigations in the synthesis of sucrose analogues. Tetrahedron 61, 7081-7086.
2. Lacaze, G., Wick, M., and Cappelle, S. (2007) Emerging fermentation technologies: Development of novel sourdoughs. Food Microbiol. 24, 155-160.
3. Coviello, T., Matricardi, P., and Alhaique, F. (2006) Drug delivery strategies using polysaccharidic gels. Expert Opin. Drug Delivery 3, 395-404.
4. Robyt, J. F., and Walseth, T. F. (1979) Production, purification, and properties of dextransucrase from Leuconostoc mesenteroides NRRL B-512F. Carbohydr. Res. 68, 95-111.
5. Remaud-Simeon, M., Lopez-Munguia, A., Pelenc, V., Paul, F., and Monsan, P. (1994) Production and use of glucosyltransferases from Leuconostoc mesenteroides NRRL B-1299 for the synthesis of oligosaccharides containing α-(1,2) linkages. Appl. Biochem. Biotechnol. 44, 101-117.
6. Kralj, S., van Geel-Schutten, G. H., Dondorff, M. M., Kirsanovs, S., van der Maarel, M. J., and Dijkhuizen, L. (2004) Glucan synthesis in the genus Lactobacillus: Isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiology 150, 3681-3690.
7. Côté, G. L., and Robyt, J. F. (1982) Isolation and partial characterization of an extracellular glucansucrase from Leuconostoc mesenteroides NRRL B-1355 that synthesizes an alternating (1,6),(1,3)-α-D-glucan. Carbohydr. Res. 101, 57-74.
8. 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.
9. Nakakuki, T. (2002) Present status and future of functional oligosaccharide development in Japan. Pure Appl. Chem. 74, 1245-1251.
10. Buchholz, K., and Seibel, J. (2003) Isomaltooligosaccharides. In Oligosaccharides in Food and Agriculture (Eggleston, G., and Cote, G. L., Eds.) Oxford University Press, Washington, DC.
11. Buchholz, K., Noll-Borchers, M., and Schwengers, D. (1998) Production of Leucrose by Dextransucrase. Starch 50, 162-164.
12. Lina, B. A., Jonker, D., and Kozianowski, G. (2002) Isomaltulose (Palatinose): A review of biological and toxicological studies. Food Chem. Toxicol. 40, 1375-1381.
13. Mizubuchi, H., Yajima, T., Aoi, N., Tomita, T., and Yoshikai, Y. (2005) Isomalto-oligosaccharides polarize Th1-like responses in intestinal and systemic immunity in mice. J. Nutr. 135, 2857-2861.
14. Withers, S. G. (2001) Mechanisms of glycosyl transferases and hydrolases. Carbohydr. Polym. 44, 325-337.
15. Ly, H. D., and Withers, S. G. (1999) Mutagenesis of glycosidases. Annu. Rev. Biochem. 68, 487-522.
16. Faijes, M., Perez, X., Perez, O., and Planas, A. (2003) Glycosynthase activity of Bacillus licheniformis 1,3-1,4-β-glucanase mutants: Specificity, kinetics, and mechanism. Biochemistry 42, 13304-13318.
17. Hancock, S. M., Vaughan, M. D., and Withers, S. G. (2006) Engineering of glycosidases and glycosyltransferases. Curr. Opin. Chem. Biol. 10, 509-519.
18. Trincone, A., and Giordano, A. (2006) Glycosyl Hydrolases and Glycosyltransferases in the Synthesis of Oligosaccharides. Curr. Org. Chem. 10, 1163-1193.
19. Fujiwara, T., Hoshino, T., Ooshima, T., Sobue, S., and Hamada, S. (2000) Purification, characterization, and molecular analysis of the gene encoding glucosyltransferase from Streptococcus oralis. Infect. Immun. 68, 2475-2483.
20. Swistowska, A. M., Wittrock, S., Collisi, W., and Hofer, B. (2008) Hyper-expression of a recombinant glycosyltransferase gene of the glucansucrase type. Appl. Microbiol. Biotechnol. 79, 255-261.
21. Sambrook, J., Fritsch, E. F., and Maniatis, T. ( 1989) Molecular cloning. A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, New York.
22. Bartels, F., Backhaus, S., Moore, E. R., Timmis, K. N., and Hofer, B. (1999) Occurrence and expression of glutathione-S-transferase-encoding bphK genes in Burkholderia sp. strain LB400 and other biphenyl-utilizing bacteria. Microbiology 145, 2821-2834.
23. Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B., and Erlich, H. A. (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239, 487-491.
24. Higuchi, R., Krummel, B., and Saiki, R. K. (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: Study of protein and DNA interactions. Nucleic Acids Res. 16, 7351-7367.
25. Giffard, P. M., Simpson, C. L., Milward, C. P., and Jacques, N. A. (1991) Molecular characterization of a cluster of at least two glucosyltransferase genes in Streptococcus salivarius ATCC 25975. J. Gen. Microbiol. 137, 2577-2593.
26. 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.
27. Coutinho, P. M., and Henrissat, B. ( 1999) Carbohydrate-active enzymes: An integrated database approach. In Recent Advances in Carbohydrate Bioengineering (Gilbert, H. J., Davies, G., Henrissat, B., and Svensson, B., Eds.) pp 3-13, The Royal Society of Chemistry, Cambridge, U.K.
28. Henrissat, B., and Davies, G. (1997) Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7, 637-644.
29. Seibel, J., Hellmuth, H., Hofer, B., Kicinska, A. M., and Schmalbruch, B. (2006) Identification of new acceptor specificities of glycosyltransferase R with the aid of substrate microarrays. ChemBioChem 7, 310-320.
30. Bloom, J. D., Meyer, M. M., Meinhold, P., Otey, C. R., MacMillan, D., and Arnold, F. H. (2005) Evolving strategies for enzyme engineering. Curr. Opin. Struct. Biol. 15, 447-452.
31. Shao, Z., and Arnold, F. H. (1996) Engineering new functions and altering existing functions. Curr. Opin. Struct. Biol. 6, 513-518.
32. Shaikh, F. A., and Withers, S. G. (2008) Teaching old enzymes new tricks: Engineering and evolution of glycosidases and glycosyl transferases for improved glycoside synthesis. Biochem. Cell Biol. 86, 169-177.
33. Lairson, L. L., Watts, A. G., Wakarchuk, W. W., and Withers, S. G. (2006) Using substrate engineering to harness enzymatic promiscuity and expand biological catalysis. Nat. Chem. Biol. 2, 724-728.
34. 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.
35. Mooser, G., Hefta, S. A., Paxton, R. J., Shively, J. E., and Lee, T. D. (1991) Isolation and sequence of an active-site peptide containing a catalytic aspartic acid from two Streptococcus sobrinus α- glucosyltransferases. J. Biol. Chem. 266, 8916-8922.
36. MacGregor, E. A., Jespersen, H. M., and Svensson, B. (1996) A circularly permuted α-amylase-type αβ-barrel structure in glucan-synthesizing glucosyltransferases. FEBS Lett. 378, 263-266.
37. Kato, C., Nakano, Y., Lis, M., and Kuramitsu, H. K. (1992) Molecular genetic analysis of the catalytic site of Streptococcus mutans glucosyltransferases. Biochem. Biophys. Res. Commun. 189, 1184-1188.
38. Monchois, V., Remaud-Simeon, M., Russell, R. R., Monsan, P., and Willemot, R. M. (1997) Characterization of Leuconostoc mesenteroides NRRL B-512F dextransucrase (DSRS) and identification of amino-acid residues playing a key role in enzyme activity. Appl. Microbiol. Biotechnol. 48, 465-472.
39. Devulapalle, K. S., Goodman, S. D., Gao, Q., Hemsley, A., and Mooser, G. (1997) Knowledge-based model of a glucosyltransferase from the oral bacterial group of mutans streptococci. Protein Sci. 6, 2489-2493.
40. Swistowska, A. M., Gronert, S., Wittrock, S., Collisi, W., Hecht, H. J., and Hofer, B. (2007) Identification of structural determinants for substrate binding and turnover by glucosyltransferase R supports the permutation hypothesis. FEBS Lett. 581, 4036-4042.
41. Monchois, V., Vignon, M., and Russell, R. R. (2000) Mutagenesis of Asp-569 of glucosyltransferase 1 glucansucrase modulates glucan and oligosaccharide synthesis. Appl. Environ. Microbiol. 66, 1923-1927.
42. Shimamura, A., Nakano, Y. J., Mukasa, H., and Kuramitsu, H. K. (1994) Identification of amino acid residues in Streptococcus mutans glucosyltransferases influencing the structure of the glucan product. J. Bacteriol. 176, 4845-4850.
43. Remaud-Simeon, M., Willemot, R., Sarcabal, P., Potocki de Montalk, G., and Monsan, P. (2000) Glucansucrases: Molecular engineering and oligosaccharide synthesis. J. Mol. Catal. B: Enzym. 10, 117-128.
44. 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.
45. 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.
46. 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.
47. D-glucan from a mutant strain of Leuconostoc mesenteroides NRRL B-1355. J. Ind. Microbiol. Biotechnol. 23, 656-660.
48. Pijning, T., Vuijičić-Žagar, A., Kralj, S., Eeuwema, W.. Dijkhuizen, L., and Dijkstra, B. W. (2008) Biochemical and crystallographic characterization of a glucansucrase from Lactobacillus reuteri 180. Biocatal. Biotrans. 26, 12-17.
49. Ferretti, J. J., Gilpin, M. L., and Russell, R. R. (1987) Nucleotide sequence of a glucosyltransferase gene from Streptococcus sobrinus MFe28. J. Bacteriol. 169, 4271-4278.
50. Kralj, S., van Geel-Schutten, G. H., Rahaoui, H., Leer, R. J., Faber, E. J., van der Maarel, M. J., and Dijkhuizen, L. (2002) Molecular characterization of a novel glucosyltransferase from Lactobacillus reuteri strain 121 synthesizing a unique, highly branched glucan with α-(1,4) and α-(1,6) glucosidic bonds. Appl. Environ. Microbiol. 68, 4283-4291.