1w2t › Citations

Crystal structure of inactivated Thermotoga maritima invertase in complex with the trisaccharide substrate raffinose.

Alberto F, Jordi E, Henrissat B, Czjzek M
Biochem J 395 457-62 (2006)
Cited: 40 times
EuropePMC logo PMID: 16411890

Abstract

Thermotoga maritima invertase (beta-fructosidase), a member of the glycoside hydrolase family GH-32, readily releases beta-D-fructose from sucrose, raffinose and fructan polymers such as inulin. These carbohydrates represent major carbon and energy sources for prokaryotes and eukaryotes. The invertase cleaves beta-fructopyranosidic linkages by a double-displacement mechanism, which involves a nucleophilic aspartate and a catalytic glutamic acid acting as a general acid/base. The three-dimensional structure of invertase shows a bimodular enzyme with a five bladed beta-propeller catalytic domain linked to a beta-sandwich of unknown function. In the present study we report the crystal structure of the inactivated invertase in interaction with the natural substrate molecule alpha-D-galactopyranosyl-(1,6)-alpha-D-glucopyranosyl-beta-D-fructofuranoside (raffinose) at 1.87 A (1 A=0.1 nm) resolution. The structural analysis of the complex reveals the presence of three binding-subsites, which explains why T. maritima invertase exhibits a higher affinity for raffinose than sucrose, but a lower catalytic efficiency with raffinose as substrate than with sucrose.

Articles - 1w2t mentioned but not cited (10)

  1. The carbohydrate-active enzymes database (CAZy) in 2013. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. Nucleic Acids Res 42 D490-5 (2014)
  2. Crystal structure of inactivated Thermotoga maritima invertase in complex with the trisaccharide substrate raffinose. Alberto F, Jordi E, Henrissat B, Czjzek M. Biochem J 395 457-462 (2006)
  3. Crystal structures of Aspergillus japonicus fructosyltransferase complex with donor/acceptor substrates reveal complete subsites in the active site for catalysis. Chuankhayan P, Hsieh CY, Huang YC, Hsieh YY, Guan HH, Hsieh YC, Tien YC, Chen CD, Chiang CM, Chen CJ. J Biol Chem 285 23251-23264 (2010)
  4. Donor substrate recognition in the raffinose-bound E342A mutant of fructosyltransferase Bacillus subtilis levansucrase. Meng G, Fütterer K. BMC Struct Biol 8 16 (2008)
  5. An acceptor-substrate binding site determining glycosyl transfer emerges from mutant analysis of a plant vacuolar invertase and a fructosyltransferase. Altenbach D, Rudiño-Pinera E, Olvera C, Boller T, Wiemken A, Ritsema T. Plant Mol Biol 69 47-56 (2009)
  6. New insights into the fructosyltransferase activity of Schwanniomyces occidentalis ß-fructofuranosidase, emerging from nonconventional codon usage and directed mutation. Alvaro-Benito M, de Abreu M, Portillo F, Sanz-Aparicio J, Fernández-Lobato M. Appl Environ Microbiol 76 7491-7499 (2010)
  7. Sequence and structural analysis of the Asp-box motif and Asp-box beta-propellers; a widespread propeller-type characteristic of the Vps10 domain family and several glycoside hydrolase families. Quistgaard EM, Thirup SS. BMC Struct Biol 9 46 (2009)
  8. Structural basis of the γ-lactone-ring formation in ascorbic acid biosynthesis by the senescence marker protein-30/gluconolactonase. Aizawa S, Senda M, Harada A, Maruyama N, Ishida T, Aigaki T, Ishigami A, Senda T. PLoS One 8 e53706 (2013)
  9. Improving low-temperature activity and thermostability of exo-inulinase InuAGN25 on the basis of increasing rigidity of the terminus and flexibility of the catalytic domain. Zhang R, He L, Shen J, Miao Y, Tang X, Wu Q, Zhou J, Huang Z. Bioengineered 11 1233-1244 (2020)
  10. The Important Roles Played in Substrate Binding of Aromatic Amino Acids in Exo-Inulinase From Kluyveromyces cicerisporus CBS 4857. Ma J, Li T, Tan H, Liu W, Yin H. Front Mol Biosci 7 569797 (2020)


Reviews citing this publication (2)

  1. Structural insights into glycoside hydrolase family 32 and 68 enzymes: functional implications. Lammens W, Le Roy K, Schroeven L, Van Laere A, Rabijns A, Van den Ende W. J Exp Bot 60 727-740 (2009)
  2. Chemo-enzymatic synthesis and functional analysis of natural and modified glycostructures. Homann A, Seibel J. Nat Prod Rep 26 1555-1571 (2009)

Articles citing this publication (28)

  1. Unraveling the difference between invertases and fructan exohydrolases: a single amino acid (Asp-239) substitution transforms Arabidopsis cell wall invertase1 into a fructan 1-exohydrolase. Le Roy K, Lammens W, Verhaest M, De Coninck B, Rabijns A, Van Laere A, Van den Ende W. Plant Physiol 145 616-625 (2007)
  2. Insights into the fine architecture of the active site of chicory fructan 1-exohydrolase: 1-kestose as substrate vs sucrose as inhibitor. Verhaest M, Lammens W, Le Roy K, De Ranter CJ, Van Laere A, Rabijns A, Van den Ende W. New Phytol 174 90-100 (2007)
  3. Structural and kinetic analysis of Schwanniomyces occidentalis invertase reveals a new oligomerization pattern and the role of its supplementary domain in substrate binding. Alvaro-Benito M, Polo A, González B, Fernández-Lobato M, Sanz-Aparicio J. J Biol Chem 285 13930-13941 (2010)
  4. Molecular and biochemical characterization of a beta-fructofuranosidase from Xanthophyllomyces dendrorhous. Linde D, Macias I, Fernández-Arrojo L, Plou FJ, Jiménez A, Fernández-Lobato M. Appl Environ Microbiol 75 1065-1073 (2009)
  5. Polysaccharide synthesis of the levansucrase SacB from Bacillus megaterium is controlled by distinct surface motifs. Strube CP, Homann A, Gamer M, Jahn D, Seibel J, Heinz DW. J Biol Chem 286 17593-17600 (2011)
  6. Crystal structures of the apo form of β-fructofuranosidase from Bifidobacterium longum and its complex with fructose. Bujacz A, Jedrzejczak-Krzepkowska M, Bielecki S, Redzynia I, Bujacz G. FEBS J 278 1728-1744 (2011)
  7. Molecular and biochemical characterization of a novel intracellular invertase from Aspergillus niger with transfructosylating activity. Goosen C, Yuan XL, van Munster JM, Ram AF, van der Maarel MJ, Dijkhuizen L. Eukaryot Cell 6 674-681 (2007)
  8. A comparative molecular dynamics study of thermophilic and mesophilic β-fructosidase enzymes. Mazola Y, Guirola O, Palomares S, Chinea G, Menéndez C, Hernández L, Musacchio A. J Mol Model 21 228 (2015)
  9. Structural and functional insights into intramolecular fructosyl transfer by inulin fructotransferase. Jung WS, Hong CK, Lee S, Kim CS, Kim SJ, Kim SI, Rhee S. J Biol Chem 282 8414-8423 (2007)
  10. Structural and kinetic insights reveal that the amino acid pair Gln-228/Asn-254 modulates the transfructosylating specificity of Schwanniomyces occidentalis β-fructofuranosidase, an enzyme that produces prebiotics. Álvaro-Benito M, Sainz-Polo MA, González-Pérez D, González-Pérez D, González B, Plou FJ, Fernández-Lobato M, Sanz-Aparicio J. J Biol Chem 287 19674-19686 (2012)
  11. First crystal structure of an endo-inulinase, INU2, from Aspergillus ficuum: discovery of an extra-pocket in the catalytic domain responsible for its endo-activity. Pouyez J, Mayard A, Vandamme AM, Roussel G, Perpète EA, Wouters J, Housen I, Michaux C. Biochimie 94 2423-2430 (2012)
  12. An alternate sucrose binding mode in the E203Q Arabidopsis invertase mutant: an X-ray crystallography and docking study. Mátrai J, Lammens W, Jonckheer A, Le Roy K, Rabijns A, Van den Ende W, De Maeyer M. Proteins 71 552-564 (2008)
  13. Crystal structures and mutagenesis of sucrose hydrolase from Xanthomonas axonopodis pv. glycines: insight into the exclusively hydrolytic amylosucrase fold. Kim MI, Kim HS, Jung J, Rhee S. J Mol Biol 380 636-647 (2008)
  14. Expression, purification and use of the soluble domain of Lactobacillus paracasei beta-fructosidase to optimise production of bioethanol from grass fructans. Martel CM, Warrilow AG, Jackson CJ, Mullins JG, Togawa RC, Parker JE, Morris MS, Donnison IS, Kelly DE, Kelly SL. Bioresour Technol 101 4395-4402 (2010)
  15. Structural Analysis of β-Fructofuranosidase from Xanthophyllomyces dendrorhous Reveals Unique Features and the Crucial Role of N-Glycosylation in Oligomerization and Activity. Ramírez-Escudero M, Gimeno-Pérez M, González B, Linde D, Merdzo Z, Fernández-Lobato M, Sanz-Aparicio J. J Biol Chem 291 6843-6857 (2016)
  16. Structural Analysis of the Catalytic Mechanism and Substrate Specificity of Anabaena Alkaline Invertase InvA Reveals a Novel Glucosidase. Xie J, Cai K, Hu HX, Jiang YL, Yang F, Hu PF, Cao DD, Li WF, Chen Y, Zhou CZ. J Biol Chem 291 25667-25677 (2016)
  17. A thermostable exo-β-fructosidase immobilised through rational design. Martínez D, Cutiño-Avila B, Pérez ER, Menéndez C, Hernández L, Del Monte-Martínez A. Food Chem 145 826-831 (2014)
  18. Creating S-type characteristics in the F-type enzyme fructan:fructan 1-fructosyltransferase of Triticum aestivum L. Schroeven L, Lammens W, Kawakami A, Yoshida M, Van Laere A, Van den Ende W. J Exp Bot 60 3687-3696 (2009)
  19. First crystal structure of an endo-levanase - the BT1760 from a human gut commensal Bacteroides thetaiotaomicron. Ernits K, Eek P, Lukk T, Visnapuu T, Alamäe T. Sci Rep 9 8443 (2019)
  20. Mutational analysis of conserved regions harboring catalytic triad residues of the levansucrase protein encoded by the lsc-3 gene (lsc3) of Pseudomonas syringae pv. tomato DC3000. Mardo K, Visnapuu T, Vija H, Elmi T, Alamäe T. Biotechnol Appl Biochem 61 11-22 (2014)
  21. Asparagine 42 of the conserved endo-inulinase INU2 motif WMNDPN from Aspergillus ficuum plays a role in activity specificity. Vandamme AM, Michaux C, Mayard A, Housen I. FEBS Open Bio 3 467-472 (2013)
  22. Purification and biochemical characterization of a native invertase from the hydrogen-producing Thermotoga neapolitana (DSM 4359). Dipasquale L, Gambacorta A, Siciliano RA, Mazzeo MF, Lama L. Extremophiles 13 345-354 (2009)
  23. Letter Structural and enzymatic analyses of Anabaena heterocyst-specific alkaline invertase InvB. Xie J, Hu HX, Cai K, Xia LY, Yang F, Jiang YL, Chen Y, Zhou CZ. FEBS Lett 592 1589-1601 (2018)
  24. C(1)-/C(2)-aromatic-imino-glyco-conjugates: experimental and computational studies of binding, inhibition and docking aspects towards glycosidases isolated from soybean and jack bean. Kumar A, Singhal NK, Ramanujam B, Mitra A, Rameshwaram NR, Nadimpalli SK, Rao CP. Glycoconj J 26 495-510 (2009)
  25. Identification, biochemical characterization, and in-vivo expression of the intracellular invertase BfrA from the pathogenic parasite Leishmania major. Belaz S, Rattier T, Lafite P, Moreau P, Routier FH, Robert-Gangneux F, Gangneux JP, Daniellou R. Carbohydr Res 415 31-38 (2015)
  26. Structural changes and inhibition of sucrase after binding of scopolamine. Minai-Tehrani D, Fooladi N, Minoui S, Sobhani-Damavandifar Z, Aavani T, Heydarzadeh S, Attar F, Ghaffari M, Nazem H. Eur J Pharmacol 635 23-26 (2010)
  27. Identification and functional analysis of the gene cluster for fructan utilization in Prevotella intermedia. Fuse H, Fukamachi H, Inoue M, Igarashi T. Gene 515 291-297 (2013)
  28. Enzymatic hydrolysis and simultaneous saccharification and fermentation of soybean processing intermediates for the production of ethanol and concentration of protein and lipids. Long CC, Gibbons W. ISRN Microbiol 2012 278092 (2012)


Quick links