1d3c Citations

The cyclization mechanism of cyclodextrin glycosyltransferase (CGTase) as revealed by a gamma-cyclodextrin-CGTase complex at 1.8-A resolution.

J. Biol. Chem. 274 34868-76 (1999)
Cited: 47 times
EuropePMC logo PMID: 10574960

Abstract

The enzyme cyclodextrin glycosyltransferase is closely related to alpha-amylases but has the unique ability to produce cyclodextrins (circular alpha(1-->4)-linked glucoses) from starch. To characterize this specificity we determined a 1.8-A structure of an E257Q/D229N mutant cyclodextrin glycosyltransferase in complex with its product gamma-cyclodextrin, which reveals for the first time how cyclodextrin is competently bound. Across subsites -2, -1, and +1, the cyclodextrin ring binds in a twisted mode similar to linear sugars, giving rise to deformation of its circular symmetry. At subsites -3 and +2, the cyclodextrin binds in a manner different from linear sugars. Sequence comparisons and site-directed mutagenesis experiments support the conclusion that subsites -3 and +2 confer the cyclization activity in addition to subsite -6 and Tyr-195. On this basis, a role of the individual residues during the cyclization reaction cycle is proposed.

Articles - 1d3c mentioned but not cited (1)



Reviews citing this publication (8)

  1. Recent advances in discovery, heterologous expression, and molecular engineering of cyclodextrin glycosyltransferase for versatile applications. Han R, Li J, Shin HD, Chen RR, Du G, Liu L, Chen J. Biotechnol. Adv. 32 415-428 (2014)
  2. Occurrence and functional significance of secondary carbohydrate binding sites in glycoside hydrolases. Cuyvers S, Dornez E, Delcour JA, Courtin CM. Crit. Rev. Biotechnol. 32 93-107 (2012)
  3. Engineering of cyclodextrin glucanotransferases and the impact for biotechnological applications. Leemhuis H, Kelly RM, Dijkhuizen L. Appl. Microbiol. Biotechnol. 85 823-835 (2010)
  4. The carbohydrate-binding module family 20--diversity, structure, and function. Christiansen C, Abou Hachem M, Janecek S, Viksø-Nielsen A, Blennow A, Svensson B. FEBS J. 276 5006-5029 (2009)
  5. gamma-Cyclodextrin: a review on enzymatic production and applications. Li Z, Wang M, Wang F, Gu Z, Du G, Wu J, Chen J. Appl. Microbiol. Biotechnol. 77 245-255 (2007)
  6. Cyclodextrin glucanotransferase: from gene to applications. Qi Q, Zimmermann W. Appl. Microbiol. Biotechnol. 66 475-485 (2005)
  7. Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes. MacGregor EA, Janecek S, Svensson B. Biochim. Biophys. Acta 1546 1-20 (2001)
  8. Glycosidase mechanisms. Rye CS, Withers SG. Curr Opin Chem Biol 4 573-580 (2000)

Articles citing this publication (38)

  1. Q-SiteFinder: an energy-based method for the prediction of protein-ligand binding sites. Laurie AT, Jackson RM. Bioinformatics 21 1908-1916 (2005)
  2. The three transglycosylation reactions catalyzed by cyclodextrin glycosyltransferase from Bacillus circulans (strain 251) proceed via different kinetic mechanisms. van der Veen BA, van Alebeek GJ, Uitdehaag JC, Dijkstra BW, Dijkhuizen L. Eur. J. Biochem. 267 658-665 (2000)
  3. Rational design of cyclodextrin glycosyltransferase from Bacillus circulans strain 251 to increase alpha-cyclodextrin production. van der Veen BA, Uitdehaag JC, Penninga D, van Alebeek GJ, Smith LM, Dijkstra BW, Dijkhuizen L. J. Mol. Biol. 296 1027-1038 (2000)
  4. Predicting protein function and binding profile via matching of local evolutionary and geometric surface patterns. Tseng YY, Dundas J, Liang J. J. Mol. Biol. 387 451-464 (2009)
  5. The role of arginine 47 in the cyclization and coupling reactions of cyclodextrin glycosyltransferase from Bacillus circulans strain 251 implications for product inhibition and product specificity. van der Veen BA, Uitdehaag JC, Dijkstra BW, Dijkhuizen L. Eur. J. Biochem. 267 3432-3441 (2000)
  6. The evolution of cyclodextrin glucanotransferase product specificity. Kelly RM, Dijkhuizen L, Leemhuis H. Appl. Microbiol. Biotechnol. 84 119-133 (2009)
  7. Glycosynthesis in a waterworld: new insight into the molecular basis of transglycosylation in retaining glycoside hydrolases. Bissaro B, Monsan P, Fauré R, O'Donohue MJ. Biochem. J. 467 17-35 (2015)
  8. Improved thermostability of bacillus circulans cyclodextrin glycosyltransferase by the introduction of a salt bridge. Leemhuis H, Rozeboom HJ, Dijkstra BW, Dijkhuizen L. Proteins 54 128-134 (2004)
  9. Molecular cloning and characterization of a novel gamma-CGTase from alkalophilic Bacillus sp. Hirano K, Ishihara T, Ogasawara S, Maeda H, Abe K, Nakajima T, Yamagata Y. Appl. Microbiol. Biotechnol. 70 193-201 (2006)
  10. Analysis of the key active subsites of glycoside hydrolase 13 family members. Kumar V. Carbohydr. Res. 345 893-898 (2010)
  11. Enzymatic circularization of a malto-octaose linear chain studied by stochastic reaction path calculations on cyclodextrin glycosyltransferase. Uitdehaag JC, van der Veen BA, Dijkhuizen L, Elber R, Dijkstra BW. Proteins 43 327-335 (2001)
  12. X-ray crystal structures of Phanerochaete chrysosporium Laminarinase 16A in complex with products from lichenin and laminarin hydrolysis. Vasur J, Kawai R, Andersson E, Igarashi K, Sandgren M, Samejima M, Ståhlberg J. FEBS J. 276 3858-3869 (2009)
  13. Crystal structure of a compact α-amylase from Geobacillus thermoleovorans. Mok SC, Teh AH, Saito JA, Najimudin N, Alam M. Enzyme Microb. Technol. 53 46-54 (2013)
  14. Comparative study of the cyclization reactions of three bacterial cyclomaltodextrin glucanotransferases. Terada Y, Sanbe H, Takaha T, Kitahata S, Koizumi K, Okada S. Appl. Environ. Microbiol. 67 1453-1460 (2001)
  15. Alteration of oligomeric state and domain architecture is essential for functional transformation between transferase and hydrolase with the same scaffold. Koike R, Kidera A, Ota M. Protein Sci. 18 2060-2066 (2009)
  16. Thermoanaerobacterium thermosulfurigenes cyclodextrin glycosyltransferase. Leemhuis H, Dijkstra BW, Dijkhuizen L. Eur. J. Biochem. 270 155-162 (2003)
  17. Systems engineering of tyrosine 195, tyrosine 260, and glutamine 265 in cyclodextrin glycosyltransferase from Paenibacillus macerans to enhance maltodextrin specificity for 2-O-(D)-glucopyranosyl-(L)-ascorbic acid synthesis. Han R, Liu L, Shin HD, Chen RR, Li J, Du G, Chen J. Appl. Environ. Microbiol. 79 672-677 (2013)
  18. Structural base for enzymatic cyclodextrin hydrolysis. Buedenbender S, Schulz GE. J. Mol. Biol. 385 606-617 (2009)
  19. Site-saturation engineering of lysine 47 in cyclodextrin glycosyltransferase from Paenibacillus macerans to enhance substrate specificity towards maltodextrin for enzymatic synthesis of 2-O-D-glucopyranosyl-L-ascorbic acid (AA-2G). Han R, Liu L, Shin HD, Chen RR, Du G, Chen J. Appl. Microbiol. Biotechnol. 97 5851-5860 (2013)
  20. Structural elucidation of the cyclization mechanism of α-1,6-glucan by Bacillus circulans T-3040 cycloisomaltooligosaccharide glucanotransferase. Suzuki N, Fujimoto Z, Kim YM, Momma M, Kishine N, Suzuki R, Suzuki S, Kitamura S, Kobayashi M, Kimura A, Funane K. J. Biol. Chem. 289 12040-12051 (2014)
  21. The residue 179 is involved in product specificity of the Bacillus circulans DF 9R cyclodextrin glycosyltransferase. Costa H, Distéfano AJ, Marino-Buslje C, Hidalgo A, Berenguer J, Biscoglio de Jiménez Bonino M, Ferrarotti SA. Appl. Microbiol. Biotechnol. 94 123-130 (2012)
  22. Role of Phe283 in enzymatic reaction of cyclodextrin glycosyltransferase from alkalophilic Bacillus sp.1011: Substrate binding and arrangement of the catalytic site. Kanai R, Haga K, Akiba T, Yamane K, Harata K. Protein Sci. 13 457-465 (2004)
  23. The cyclodextrin glycosyltransferase of Paenibacillus pabuli US132 strain: molecular characterization and overproduction of the recombinant enzyme. Jemli S, Ben Messaoud E, Ben Mabrouk S, Bejar S. J. Biomed. Biotechnol. 2008 692573 (2008)
  24. Structural basis for cyclodextrin recognition by Thermoactinomyces vulgaris cyclo/maltodextrin-binding protein. Tonozuka T, Sogawa A, Yamada M, Matsumoto N, Yoshida H, Kamitori S, Ichikawa K, Mizuno M, Nishikawa A, Sakano Y. FEBS J. 274 2109-2120 (2007)
  25. Purification, characterization, and gene cloning of a novel maltosyltransferase from an Arthrobacter globiformis strain that produces an alternating alpha-1,4- and alpha-1,6-cyclic tetrasaccharide from starch. Mukai K, Watanabe H, Kubota M, Chaen H, Fukuda S, Kurimoto M. Appl. Environ. Microbiol. 72 1065-1071 (2006)
  26. Hydrophilic aromatic residue and in silico structure for carbohydrate binding module. Chou WY, Pai TW, Jiang TY, Chou WI, Tang CY, Chang MD. PLoS ONE 6 e24814 (2011)
  27. NMR spectroscopic characterization of inclusion complexes comprising cyclodextrins and gallated catechins in aqueous solution: cavity size dependency. Ishizu T, Tsutsumi H, Yamamoto H, Harano K. Magn Reson Chem 47 283-287 (2009)
  28. A novel glucanotransferase from a Bacillus circulans strain that produces a cyclomaltopentaose cyclized by an alpha-1,6-linkage. Watanabe H, Nishimoto T, Mukai K, Kubota M, Chaen H, Fukuda S. Biosci. Biotechnol. Biochem. 70 1954-1960 (2006)
  29. Synergistic effects of trace amounts of water in the enantiodiscrimination processes by lipodex E: a spectroscopic and computational investigation. Uccello-Barretta G, Schurig V, Balzano F, Vanni L, Aiello F, Mori M, Ghirga F. Chirality 27 95-103 (2015)
  30. Mutations enhance β-cyclodextrin specificity of cyclodextrin glycosyltransferase from Bacillus circulans. Li Z, Ban X, Gu Z, Li C, Huang M, Hong Y, Cheng L. Carbohydr Polym 108 112-117 (2014)
  31. β-cyclodextrin production by the cyclodextrin glucanotransferase from Paenibacillus illinoisensis ZY-08: cloning, purification, and properties. Lee YS, Zhou Y, Park DJ, Chang J, Choi YL. World J. Microbiol. Biotechnol. 29 865-873 (2013)
  32. Site-saturation mutagenesis of central tyrosine 195 leading to diverse product specificities of an α-cyclodextrin glycosyltransferase from Paenibacillus sp. 602-1. Xie T, Song B, Yue Y, Chao Y, Qian S. J. Biotechnol. 170 10-16 (2014)
  33. β-cyclodextrin production by the cyclodextrin glucanotransferase from Paenibacillus illinoisensis ZY-08: cloning, purification, and properties Lee YS, Zhou Y, Park DJ, Chang J, Choi YL. World J. Microbiol. Biotechnol. 29 865-873 (2013)
  34. Structural basis of a mutant Y195I α-cyclodextrin glycosyltransferase with switched product specificity from α-cyclodextrin to β-/γ-cyclodextrin. Xie T, Hou Y, Li D, Yue Y, Qian S, Chao Y. J. Biotechnol. 182-183 92-96 (2014)
  35. Acceptor-induced modification of regioselectivity in CGTase-catalyzed glycosylations of p-nitrophenyl-glucopyranosides. Strompen S, Miranda-Molina A, López-Munguía A, Castillo E, Saab-Rincón G. Carbohydr. Res. 404 46-54 (2015)
  36. Molecular dynamic analysis of mutant Y195I α-cyclodextrin glycosyltransferase with switched product specificity from α-cyclodextrin to γ-cyclodextrin. Chen F, Xie T, Yue Y, Qian S, Chao Y, Pei J. J Mol Model 21 208 (2015)
  37. US132 Cyclodextrin Glucanotransferase Engineering by Random Mutagenesis for an Anti-Staling Purpose. Jemli S, Jaoua M, Bejar S. Mol. Biotechnol. 58 551-557 (2016)
  38. Amylose recognition and ring-size determination of amylomaltase. Roth C, Weizenmann N, Bexten N, Saenger W, Zimmermann W, Maier T, Sträter N. Sci Adv 3 e1601386 (2017)


Related citations provided by authors (3)

  1. X-ray Structures Along the Reaction Pathway of Cyclodextrin Glycosyltransferase Elucidate Catalysis in the Alpha-amylase Family. Uitdehaag JCM, Mosi R, Kalk KH, van der Veen BA, Dijkhuizen L, Withers SG, Dijkstra BW Nat. Struct. Biol. 6 432-436 (1999)
  2. Crystallographic Studies of the Interaction of Cyclodextrin Glycosyltransferase from Bacillus Circulans Strain 251 with Natural Substrates and Products. Knegtel RM, Strokopytov B, Penninga D, Faber OG, Rozeboom HJ, Kalk KH, Dijkhuizen L, Dijkstra BW J. Biol. Chem. 270 29256-29264 (1995)
  3. Structure of Cyclodextrin Glycosyltransferase Complexed with a Maltononaose Inhibitor at 2.6 Angstrom Resolution. Implications for Product Specificity. Strokopytov B, Knegtel RM, Penninga D, Rozeboom HJ, Kalk KH, Dijkhuizen L, Dijkstra BW Biochemistry 35 4241-4249 (1996)