Identification of structural determinants for inhibition strength and specificity of wheat xylanase inhibitors TAXI-IA and TAXI-IIA

FEBS Journal

Volumn 276, Issue 14, 2009, Pages 3916-3927

  Pollet, Annick ^a   Sansen, Stefaan ^b   Raedschelders, Gert ^c   Gebruers, Kurt ^a   Rabijns, Anja ^b   Delcour, Jan A ^a   Courtin, Christophe M ^a  

^a LEUVEN FOOD SCIENCE AND NUTRITION RESEARCH CENTRE LFORCE   (Belgium)

^b DEPARTMENT OF PHARMACEUTICAL AND PHARMACOLOGICAL SCIENCES   (Belgium)

^c LABORATORY OF GENE TECHNOLOGY   (Belgium)

Author keywords

Bacillus subtilis; Inhibition; Triticum aestivum; X ray structure; Xylanase

Indexed keywords

ASPARAGINE; ASPARTIC ACID; ENZYME INHIBITOR; GLYCOSIDASE; LEUCINE; PROLINE; TRITICUM AESTIVUM XYLANASE INHIBITOR 1A; TRITICUM AESTIVUM XYLANASE INHIBITOR 2A; UNCLASSIFIED DRUG; XYLAN ENDO 1,3 BETA XYLOSIDASE; ENDO 1,4 BETA XYLANASE; ISOPROTEIN; TAXI I PROTEIN, TRITICUM AESTIVUM; TAXI II PROTEIN, TRITICUM AESTIVUM; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BINDING SITE; COMPLEX FORMATION; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; MOLECULAR INTERACTION; MOLECULAR MIMICRY; NONHUMAN; PH; PRIORITY JOURNAL; STRUCTURE ANALYSIS; WHEAT; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; PROTEIN BINDING; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STRUCTURAL HOMOLOGY;

BACILLUS SUBTILIS; TRITICUM AESTIVUM;

BACILLUS SUBTILIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ENDO-1,4-BETA XYLANASES; ENZYME INHIBITORS; MODELS, MOLECULAR; MUTATION; PLANT PROTEINS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; TRITICUM;

EID: 67650693777     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07105.x     Document Type: Article

References (38)

1. Fierens K, Gils A, Sansen S, Brijs K, Courtin CM, Declerck PJ, De Ranter CJ, Gebruers K, Rabijns A, Robben J et al. (2005) His374 of wheat endoxylanase inhibitor TAXI-I stabilizes complex formation with glycoside hydrolase family 11 endoxylanases. FEBS J 272, 5872 5882. (Pubitemid 41689359)
2. Raedschelders G, Fierens K, Sansen S, Rombouts S, Gebruers K, Robben J, Rabijns A, Courtin CM, Delcour JA, Van Campenhou S et al. (2005) Molecular identification of wheat endoxylanase inhibitor TAXI-II and the determinants of its inhibition specificity. Biochem Biophys Res Commun 335, 512 522. (Pubitemid 41140252)
3. Sørensen JF Sibbesen O (2006) Mapping of residues involved in the interaction between the Bacillus subtilis xylanase A and proteinaceous wheat xylanase inhibitors. Protein Eng Des Sel 19, 205 210.
4. Bourgois TM, Nguyen DV, Sansen S, Rombouts S, Beliën T, Fierens K, Raedschelders G, Rabijns A, Courtin CM, Delcour JA et al. (2007) Targeted molecular engineering of a family 11 endoxylanase to decrease its sensitivity towards Triticum aestivum endoxylanase inhibitor types. J Biotechnol 130, 95 105. (Pubitemid 46656300)
5. Reilly PJ (1981) Xylanases: structure and function. In Trends in the Biology of Fermentation for Fuels and Chemicals (Hollaender A, ed.), pp. 111 129. Basic Life Sciences, Plenum Press, New York, NY.
6. Henrissat B (1991) A classification of glycosyl hydrolases based on amino-acid-sequence similarities. Biochem J 280, 309 316.
7. Törrönen A, Harkki A Rouvinen J (1994) 3-Dimensional structure of endo-1,4-beta-xylanase-II from Trichoderma reesei - 2 conformational states in the active-site. EMBO J 13, 2493 2501. (Pubitemid 24188381)
8. Törrönen A Rouvinen J (1995) Structural comparison of 2 major endo-1,4-xylanases from Trichoderma reesei. Biochemistry 34, 847 856.
9. Joshi MD, Sidhu G, Pot I, Brayer GD, Withers SG McIntosh LP (2000) Hydrogen bonding and catalysis: a novel explanation for how a single amino acid substitution can change the pH optimum of a glycosidase. J Mol Biol 299, 255 279.
10. Sapag A, Wouters J, Lambert C, de Ioannes P, Eyzaguirre J Depiereux E (2002) The endoxylanases from family 11: computer analysis of protein sequences reveals important structural and phylogenetic relationships. J Biotechnol 95, 109 131. (Pubitemid 34245389)
11. Fushinobu S, Ito K, Konno M, Wakagi T Matsuzawa H (1998) Crystallographic and mutational analyses of an extremely acidophilic and acid-stable xylanase: biased distribution of acidic residues and importance of Asp37 for catalysis at low pH. Protein Eng 11, 1121 1128. (Pubitemid 29012122)
12. Debyser W, Derdelinckx G Delcour JA (1997) Arabinoxylan solubilization and inhibition of the barley malt xylanolytic system by wheat during mashing with wheat wholemeal adjunct: Evidence for a new class of enzyme inhibitors in wheat. J Am Soc Brew Chem 55, 153 156. (Pubitemid 127681958)
13. McLauchlan WR, Garcia-Conesa MT, Williamson G, Roza M, Ravestein P Maat J (1999) A novel class of protein from wheat which inhibits xylanases. Biochem J 338, 441 446.
14. Fierens E, Rombouts S, Gebruers K, Goesaert H, Brijs K, Beaugrand J, Volckaert G, Van Campenhout S, Proost P, Courtin CM et al. (2007) TLXI, a novel type of xylanase inhibitor from wheat (Triticum aestivum) belonging to the thaumatin family. Biochem J 403, 583 591. (Pubitemid 46706987)
15. Gebruers K, Debyser W, Goesaert H, Proost P, Van Damme J Delcour JA (2001) Triticum aestivum L. endoxylanase inhibitor (TAXI) consists of two inhibitors, TAXI I and TAXI II, with different specificities. Biochem J 353, 239 244. (Pubitemid 32096931)
16. Fierens K, Brijs K, Courtin CM, Gebruers K, Goesaert H, Raedschelders G, Robben J, Van Campenhout S, Volckaert G Delcour JA (2003) Molecular identification of wheat endoxylanase inhibitor TAXI-I, member of a new class of plant proteins. FEBS Lett 540, 259 263. (Pubitemid 36398068)
17. Croes E, Gebruers K, Robben J, Noben JP, Samyn B, Debyser G, Van Beeumen J, Delcour JA Courtin CM (2008) Variability of polymorphic families of three types of xylanase inhibitors in the wheat grain proteome. Proteomics 8, 1692 1705. (Pubitemid 351580213)
18. Gebruers K (2002) Endoxylanase inhibitors in wheat (Triticum aestivum L.): isolation, characterisation and use for endoxylanase purification. PhD Thesis, Katholieke Universiteit Leuven, Leuven, Belgium.
19. Gebruers K, Brijs K, Courtin CM, Fierens K, Goesaert H, Rabijns A, Raedschelders G, Robben J, Sansen S, Sorensen JF et al. (2004) Properties of TAXI-type endoxylanase inhibitors. Biochim Biophys Acta, Proteins Proteomics 1696, 213 221. (Pubitemid 38202261)
20. Fierens K, Geudens N, Brijs K, Courtin CM, Gebruers K, Robben J, Van Campenhout S, Volckaert G Delcour JA (2004) High-level expression, purification, and characterization of recombinant wheat xylanase inhibitor TAXI-I secreted by the yeast Pichia pastoris. Protein Expr Purif 37, 39 46. (Pubitemid 39027241)
21. Sansen S, De Ranter CJ, Gebruers K, Brijs K, Courtin CM, Delcour JA Rabijns A (2004) Structural basis for inhibition of Aspergillus niger xylanase by Triticum aestivum xylanase inhibitor-I. J Biol Chem 279, 36022 36028. (Pubitemid 39100610)
22. Vandermarliere E, Bourgois TM, Rombouts S, Van Campenhout S, Volckaert G, Strelkov SV, Delcour JA, Rabijns A Courtin CM (2008) Crystallographic analysis shows substrate binding at the -3 to +1 active-site subsites and at the surface of glycoside hydrolase family 11 endo-1,4-beta-xylanases. Biochem J 410, 71 79. (Pubitemid 351300326)
23. Gruber K, Klintschar G, Hayn M, Schlacher A, Steiner W Kratky C (1998) Thermophilic xylanase from Thermomyces lanuginosus: High-resolution X-ray structure and modeling studies. Biochemistry 37, 13475 13485. (Pubitemid 28455521)
24. Brutus A, Villard C, Durand A, Tahir T, Furniss C, Puigserver A, Juge N Giardina T (2004) The inhibition specificity of recombinant Penicillium funiculosum xylanase B towards wheat proteinaceous inhibitors. Biochim Biophys Acta, Proteins Proteomics 1701, 121 128. (Pubitemid 39140791)
25. Brutus A, Reca IB, Herga S, Mattei B, Puigserver A, Chaix JC, Juge N, Bellincampi D Giardina T (2005) A family 11 xylanase from the pathogen Botrytis cinerea is inhibited by plant endoxylanase inhibitors XIP-I and TAXI-I. Biochem Biophys Res Commun 337, 160 166. (Pubitemid 41393773)
26. Furniss CSM, Williamson G Kroon PA (2005) The substrate specificity and susceptibility to wheat inhibitor proteins of Penicillium funiculosum xylanases from a commercial enzyme preparation. J Sci Food Agric 85, 574 582. (Pubitemid 40281300)
27. Gebruers K, Goesaert H, Brijs K, Courtin CM Delcour JA (2002) Purification of TAXI-like endoxylanase inhibitors from wheat (Triticum aestivum L.) whole meal reveals a family of iso-forms. J Enzyme Inhib Med Chem 17, 61 68. (Pubitemid 34855322)
28. Sansen S, De Ranter CJ, Gebruers K, Brijs K, Courtin CM, Delcour JA Rabijns A (2004) Crystallization and preliminary X-ray diffraction study of two complexes of a TAXI-type xylanase inhibitor with glycoside hydrolase family 11 xylanases from Aspergillus niger and Bacillus subtilis. Acta Crystallogr D Biol Crystallogr 60, 555 557. (Pubitemid 41087595)
29. Leslie AG (2006) The integration of macromolecular diffraction data. Acta Crystallogr D Biol Crystallogr 62, 48 57.
30. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62, 72 82.
31. Matthews BW (1968) Solvent content of protein crystals. J Mol Biol 33, 491 497.
32. Joshi MD, Sidhu G, Nielsen JE, Brayer GD, Withers SG McIntosh LP (2001) Dissecting the electrostatic interactions and pH-dependent activity of a family 11 glycosidase. Biochemistry 40, 10115 10139. (Pubitemid 32800119)
33. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54, 905 921.
34. Murshudov GN, Vagin AA Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240 255. (Pubitemid 27235885)
35. Vagin A Teplyakov A (1997) MOLREP: an automated program for molecular replacement. J Appl Crystallogr 30, 1022 1025. (Pubitemid 127485985)
36. Jones TA, Zou JY, Cowan SW Kjeldgaard M (1991) Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr, Sect A: Found Crystallogr 47, 110 119.
37. Krengel U Dijkstra BW (1996) Three-dimensional structure of endo-1,4-beta-xylanase I from Aspergillus niger: Molecular basis for its low pH optimum. J Mol Biol 263, 70 78. (Pubitemid 26361513)
38. ANX, Aspergillus niger xylanase AANX·TAXI-IA, TAXI-IA in complex with ANXBSX, Bacillus subtilis xylanase ABSX·rTAXI-IIA, recombinant TAXI-IIA in complex with BSXBSX·TAXI-IA, TAXI-IA in complex with BSXGH, glycoside hydrolase familyPDB