1ta3 Citations

The dual nature of the wheat xylanase protein inhibitor XIP-I: structural basis for the inhibition of family 10 and family 11 xylanases.

Abstract

The xylanase inhibitor protein I (XIP-I) from wheat Triticum aestivum is the prototype of a novel class of cereal protein inhibitors that inhibit fungal xylanases belonging to glycoside hydrolase families 10 (GH10) and 11 (GH11). The crystal structures of XIP-I in complex with Aspergillus nidulans (GH10) and Penicillium funiculosum (GH11) xylanases have been solved at 1.7 and 2.5 A resolution, respectively. The inhibition strategy is novel because XIP-I possesses two independent enzyme-binding sites, allowing binding to two glycoside hydrolases that display a different fold. Inhibition of the GH11 xylanase is mediated by the insertion of an XIP-I Pi-shaped loop (Lalpha(4)beta(5)) into the enzyme active site, whereas residues in the helix alpha7 of XIP-I, pointing into the four central active site subsites, are mainly responsible for the reversible inactivation of GH10 xylanases. The XIP-I strategy for inhibition of xylanases involves substrate-mimetic contacts and interactions occluding the active site. The structural determinants of XIP-I specificity demonstrate that the inhibitor is able to interact with GH10 and GH11 xylanases of both fungal and bacterial origin. The biological role of the xylanase inhibitors is discussed in light of the present structural data.

Articles - 1ta3 mentioned but not cited (7)

  1. Protein subunit interfaces: heterodimers versus homodimers. Zhanhua C, Gan JG, Lei L, Sakharkar MK, Kangueane P. Bioinformation 1 28-39 (2005)
  2. Structural interface parameters are discriminatory in recognising near-native poses of protein-protein interactions. Malhotra S, Sankar K, Sowdhamini R. PLoS One 9 e80255 (2014)
  3. Parallel implementation of 3D protein structure similarity searches using a GPU and the CUDA. Mrozek D, Brożek M, Małysiak-Mrozek B. J Mol Model 20 2067 (2014)
  4. Classification of heterodimer interfaces using docking models and construction of scoring functions for the complex structure prediction. Tsuchiya Y, Kanamori E, Nakamura H, Kinoshita K. Adv Appl Bioinform Chem 2 79-100 (2009)
  5. Complex fitness landscape shapes variation in a hyperpolymorphic species. Stolyarova AV, Neretina TV, Zvyagina EA, Fedotova AV, Kondrashov AS, Bazykin GA. Elife 11 e76073 (2022)
  6. Aspergillus sydowii: Genome Analysis and Characterization of Two Heterologous Expressed, Non-redundant Xylanases. Brandt SC, Ellinger B, van Nguyen T, Harder S, Schlüter H, Hahnke RL, Rühl M, Schäfer W, Gand M. Front Microbiol 11 2154 (2020)
  7. Interface residues of transient protein-protein complexes have extensive intra-protein interactions apart from inter-protein interactions. Jayashree S, Murugavel P, Sowdhamini R, Srinivasan N. Biol. Direct 14 1 (2019)


Reviews citing this publication (11)

  1. Recent advances in plant cell wall proteomics. Jamet E, Albenne C, Boudart G, Irshad M, Canut H, Pont-Lezica R. Proteomics 8 893-908 (2008)
  2. Plant protein inhibitors of cell wall degrading enzymes. Juge N. Trends Plant Sci. 11 359-367 (2006)
  3. Glycosidase inhibition: assessing mimicry of the transition state. Gloster TM, Davies GJ. Org. Biomol. Chem. 8 305-320 (2010)
  4. Enzyme-inhibitor interactions at the plant-pathogen interface. Misas-Villamil JC, van der Hoorn RA. Curr. Opin. Plant Biol. 11 380-388 (2008)
  5. Microbial endoxylanases: effective weapons to breach the plant cell-wall barrier or, rather, triggers of plant defense systems? Beliën T, Van Campenhout S, Robben J, Volckaert G. Mol. Plant Microbe Interact. 19 1072-1081 (2006)
  6. Plant cell walls: Protecting the barrier from degradation by microbial enzymes. Lagaert S, Beliën T, Volckaert G. Semin. Cell Dev. Biol. 20 1064-1073 (2009)
  7. Factors affecting xylanase functionality in the degradation of arabinoxylans. Berrin JG, Juge N. Biotechnol. Lett. 30 1139-1150 (2008)
  8. Structural and functional evolution of chitinase-like proteins from plants. Kesari P, Patil DN, Kumar P, Tomar S, Sharma AK, Kumar P. Proteomics 15 1693-1705 (2015)
  9. Proteinaceous inhibitors of microbial xylanases. Gusakov AV. Biochemistry Mosc. 75 1185-1199 (2010)
  10. Rational protein design for thermostabilization of glycoside hydrolases based on structural analysis. Watanabe M, Matsuzawa T, Yaoi K. Appl. Microbiol. Biotechnol. 102 8677-8684 (2018)
  11. Xylanase Inhibitors: Defense Players in Plant Immunity with Implications in Agro-Industrial Processing. Tundo S, Mandalà G, Sella L, Favaron F, Bedre R, Kalunke RM. Int J Mol Sci 23 14994 (2022)

Articles citing this publication (59)

  1. Structural basis for inhibition of Aspergillus niger xylanase by triticum aestivum xylanase inhibitor-I. Sansen S, De Ranter CJ, Gebruers K, Brijs K, Courtin CM, Delcour JA, Rabijns A. J. Biol. Chem. 279 36022-36028 (2004)
  2. TLXI, a novel type of xylanase inhibitor from wheat (Triticum aestivum) belonging to the thaumatin family. Fierens E, Rombouts S, Gebruers K, Goesaert H, Brijs K, Beaugrand J, Volckaert G, Van Campenhout S, Proost P, Courtin CM, Delcour JA. Biochem. J. 403 583-591 (2007)
  3. The synergistic action of accessory enzymes enhances the hydrolytic potential of a "cellulase mixture" but is highly substrate specific. Hu J, Arantes V, Pribowo A, Saddler JN. Biotechnol Biofuels 6 112 (2013)
  4. Genome-wide analysis of transposon insertion polymorphisms reveals intraspecific variation in cultivated rice. Huang X, Lu G, Zhao Q, Liu X, Han B. Plant Physiol. 148 25-40 (2008)
  5. A wheat xylanase inhibitor gene, Xip-I, but not Taxi-I, is significantly induced by biotic and abiotic signals that trigger plant defense. Igawa T, Tokai T, Kudo T, Yamaguchi I, Kimura M. Biosci. Biotechnol. Biochem. 69 1058-1063 (2005)
  6. Nectarin IV, a potent endoglucanase inhibitor secreted into the nectar of ornamental tobacco plants. Isolation, cloning, and characterization. Naqvi SM, Harper A, Carter C, Ren G, Guirgis A, York WS, Thornburg RW. Plant Physiol. 139 1389-1400 (2005)
  7. Emergence of a subfamily of xylanase inhibitors within glycoside hydrolase family 18. Durand A, Hughes R, Roussel A, Flatman R, Henrissat B, Juge N. FEBS J. 272 1745-1755 (2005)
  8. CAPRI rounds 3-5 reveal promising successes and future challenges for RosettaDock. Daily MD, Masica D, Sivasubramanian A, Somarouthu S, Gray JJ. Proteins 60 181-186 (2005)
  9. Understanding the structural basis for substrate and inhibitor recognition in eukaryotic GH11 xylanases. Vardakou M, Dumon C, Murray JW, Christakopoulos P, Weiner DP, Juge N, Lewis RJ, Gilbert HJ, Flint JE. J. Mol. Biol. 375 1293-1305 (2008)
  10. Cloning and characterization of two endoxylanases from the cereal phytopathogen Fusarium graminearum and their inhibition profile against endoxylanase inhibitors from wheat. Beliën T, Van Campenhout S, Van Acker M, Volckaert G. Biochem. Biophys. Res. Commun. 327 407-414 (2005)
  11. Crystal structures of native and xylosaccharide-bound alkali thermostable xylanase from an alkalophilic Bacillus sp. NG-27: structural insights into alkalophilicity and implications for adaptation to polyextreme conditions. Manikandan K, Bhardwaj A, Gupta N, Lokanath NK, Ghosh A, Reddy VS, Ramakumar S. Protein Sci. 15 1951-1960 (2006)
  12. Structural basis of the substrate subsite and the highly thermal stability of xylanase 10B from Thermotoga maritima MSB8. Ihsanawati, Kumasaka T, Kaneko T, Morokuma C, Yatsunami R, Sato T, Nakamura S, Tanaka N. Proteins 61 999-1009 (2005)
  13. A family 11 xylanase from the pathogen Botrytis cinerea is inhibited by plant endoxylanase inhibitors XIP-I and TAXI-I. Brutus A, Reca IB, Herga S, Mattei B, Puigserver A, Chaix JC, Juge N, Bellincampi D, Giardina T. Biochem. Biophys. Res. Commun. 337 160-166 (2005)
  14. Docking to single-domain and multiple-domain proteins: old and new challenges. Ben-Zeev E, Kowalsman N, Ben-Shimon A, Segal D, Atarot T, Noivirt O, Shay T, Eisenstein M. Proteins 60 195-201 (2005)
  15. Structural basis for inhibition of xyloglucan-specific endo-β-1,4-glucanase (XEG) by XEG-protein inhibitor. Yoshizawa T, Shimizu T, Hirano H, Sato M, Hashimoto H. J. Biol. Chem. 287 18710-18716 (2012)
  16. Substrate and product hydrolysis specificity in family 11 glycoside hydrolases: an analysis of Penicillium funiculosum and Penicillium griseofulvum xylanases. Berrin JG, Ajandouz el H, Georis J, Arnaut F, Juge N. Appl. Microbiol. Biotechnol. 74 1001-1010 (2007)
  17. Performance of the first protein docking server ClusPro in CAPRI rounds 3-5. Comeau SR, Vajda S, Camacho CJ. Proteins 60 239-244 (2005)
  18. Proteomic Analysis Reveals Key Proteins and Phosphoproteins upon Seed Germination of Wheat (Triticum aestivum L.). Dong K, Zhen S, Cheng Z, Cao H, Ge P, Yan Y. Front Plant Sci 6 1017 (2015)
  19. Structural resolution of the complex between a fungal polygalacturonase and a plant polygalacturonase-inhibiting protein by small-angle X-ray scattering. Benedetti M, Leggio C, Federici L, De Lorenzo G, Pavel NV, Cervone F. Plant Physiol. 157 599-607 (2011)
  20. Functional characterization and synergic action of fungal xylanase and arabinofuranosidase for production of xylooligosaccharides. Gonçalves TA, Damásio AR, Segato F, Alvarez TM, Bragatto J, Brenelli LB, Citadini AP, Murakami MT, Ruller R, Ruller R, Paes Leme AF, Prade RA, Squina FM. Bioresour. Technol. 119 293-299 (2012)
  21. Viewing the human microbiome through three-dimensional glasses: integrating structural and functional studies to better define the properties of myriad carbohydrate-active enzymes. Turnbaugh PJ, Henrissat B, Gordon JI. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66 1261-1264 (2010)
  22. Crystal structure of truncated Fibrobacter succinogenes 1,3-1,4-beta-D-glucanase in complex with beta-1,3-1,4-cellotriose. Tsai LC, Shyur LF, Cheng YS, Lee SH. J. Mol. Biol. 354 642-651 (2005)
  23. Mutational analysis of endoxylanases XylA and XylB from the phytopathogen Fusarium graminearum reveals comprehensive insights into their inhibitor insensitivity. Beliën T, Van Campenhout S, Van Acker M, Robben J, Courtin CM, Delcour JA, Volckaert G. Appl. Environ. Microbiol. 73 4602-4608 (2007)
  24. New insights into the role of the thumb-like loop in GH-11 xylanases. Paës G, Tran V, Takahashi M, Boukari I, O'Donohue MJ. Protein Eng. Des. Sel. 20 15-23 (2007)
  25. A new chitinase-like xylanase inhibitor protein (XIP) from coffee (Coffea arabica) affects Soybean Asian rust (Phakopsora pachyrhizi) spore germination. Vasconcelos EA, Santana CG, Godoy CV, Seixas CD, Silva MS, Moreira LR, Oliveira-Neto OB, Price D, Fitches E, Filho EX, Mehta A, Gatehouse JA, Grossi-De-Sa MF. BMC Biotechnol. 11 14 (2011)
  26. Combining interface core and whole interface descriptors in postscan processing of protein-protein docking models. Kowalsman N, Eisenstein M. Proteins 77 297-318 (2009)
  27. Mapping of residues involved in the interaction between the Bacillus subtilis xylanase A and proteinaceous wheat xylanase inhibitors. Sørensen JF, Sibbesen O. Protein Eng. Des. Sel. 19 205-210 (2006)
  28. Molecular identification of wheat endoxylanase inhibitor TAXI-II and the determinants of its inhibition specificity. Raedschelders G, Fierens K, Sansen S, Rombouts S, Gebruers K, Robben J, Rabijns A, Courtin CM, Delcour JA, Van Campenhout S, Volckaert G. Biochem. Biophys. Res. Commun. 335 512-522 (2005)
  29. Optimization of transplastomic production of hemicellulases in tobacco: effects of expression cassette configuration and tobacco cultivar used as production platform on recombinant protein yields. Kolotilin I, Kaldis A, Pereira EO, Laberge S, Menassa R. Biotechnol Biofuels 6 65 (2013)
  30. Identification of changes in wheat (Triticum aestivum L.) seeds proteome in response to anti-trx s gene. Guo H, Zhang H, Li Y, Ren J, Wang X, Niu H, Yin J. PLoS ONE 6 e22255 (2011)
  31. Insights into the fold organization of TIM barrel from interaction energy based structure networks. Vijayabaskar MS, Vishveshwara S. PLoS Comput. Biol. 8 e1002505 (2012)
  32. Metabolomic Profiling of the Nectars of Aquilegia pubescens and A. Canadensis. Noutsos C, Perera AM, Nikolau BJ, Seaver SM, Ware DH. PLoS ONE 10 e0124501 (2015)
  33. RNAi-mediated knockdown of the XIP-type endoxylanase inhibitor gene, OsXIP, has no effect on grain development and germination in rice. Tokunaga T, Miyata Y, Fujikawa Y, Esaka M. Plant Cell Physiol. 49 1122-1127 (2008)
  34. Biochemical and structural characterization of TLXI, the Triticum aestivum L. thaumatin-like xylanase inhibitor. Fierens E, Gebruers K, Voet AR, De Maeyer M, Courtin CM, Delcour JA. J Enzyme Inhib Med Chem 24 646-654 (2009)
  35. Characterization of glycosynthase mutants derived from glycoside hydrolase family 10 xylanases. Sugimura M, Nishimoto M, Kitaoka M. Biosci. Biotechnol. Biochem. 70 1210-1217 (2006)
  36. Engineering molecular recognition of endoxylanase enzymes and their inhibitors through phage display. Beliën T, Van Campenhout S, Vanden Bosch A, Bourgois TM, Rombouts S, Robben J, Courtin CM, Delcour JA, Volckaert G. J. Mol. Recognit. 20 103-112 (2007)
  37. Molecular cloning and characterization of a GH11 endoxylanase from Chaetomium globosum, and its use in enzymatic pretreatment of biomass. Singh RK, Tiwari MK, Kim D, Kang YC, Ramachandran P, Lee JK. Appl. Microbiol. Biotechnol. 97 7205-7214 (2013)
  38. Cloning and expression of an endo-1,4-β-xylanase from the coffee berry borer, Hypothenemus hampei. Padilla-Hurtado B, Flórez-Ramos C, Aguilera-Gálvez C, Medina-Olaya J, Ramírez-Sanjuan A, Rubio-Gómez J, Acuña-Zornosa R. BMC Res Notes 5 23 (2012)
  39. Mutational analysis of target enzyme recognition of the beta-trefoil fold barley alpha-amylase/subtilisin inhibitor. Bønsager BC, Nielsen PK, Abou Hachem M, Fukuda K, Praetorius-Ibba M, Svensson B. J. Biol. Chem. 280 14855-14864 (2005)
  40. Evolutionary history of eukaryotic α-glucosidases from the α-amylase family. Gabriško M. J. Mol. Evol. 76 129-145 (2013)
  41. Structural investigation of a novel N-acetyl glucosamine binding chi-lectin which reveals evolutionary relationship with class III chitinases. Patil DN, Datta M, Dev A, Dhindwal S, Singh N, Dasauni P, Kundu S, Sharma AK, Tomar S, Kumar P. PLoS ONE 8 e63779 (2013)
  42. Genomic characterization of plant cell wall degrading enzymes and in silico analysis of xylanases and polygalacturonases of Fusarium virguliforme. Chang HX, Yendrek CR, Caetano-Anolles G, Hartman GL. BMC Microbiol. 16 147 (2016)
  43. Reprogramming of Seed Metabolism Facilitates Pre-harvest Sprouting Resistance of Wheat. Liu C, Ding F, Hao F, Yu M, Lei H, Wu X, Zhao Z, Guo H, Yin J, Wang Y, Tang H. Sci Rep 6 20593 (2016)
  44. Crystal structure determination and inhibition studies of a novel xylanase and alpha-amylase inhibitor protein (XAIP) from Scadoxus multiflorus. Kumar S, Singh N, Sinha M, Dube D, Singh SB, Bhushan A, Kaur P, Srinivasan A, Sharma S, Singh TP. FEBS J. 277 2868-2882 (2010)
  45. Structure-based mutagenesis of Penicillium griseofulvum xylanase using computational design. André-Leroux G, Berrin JG, Georis J, Arnaut F, Juge N. Proteins 72 1298-1307 (2008)
  46. Cloning and characterization of the first GH10 and GH11 xylanases from Rhizopus oryzae. Xiao Z, Grosse S, Bergeron H, Lau PC. Appl. Microbiol. Biotechnol. 98 8211-8222 (2014)
  47. Cloning and enzymatic characterization of four thermostable fungal endo-1,4-β-xylanases. Sydenham R, Zheng Y, Riemens A, Tsang A, Powlowski J, Storms R. Appl. Microbiol. Biotechnol. 98 3613-3628 (2014)
  48. Solution scattering studies of conformation stability of xylanase XYNII from Trichoderma longibrachiatum. Kozak M. Biopolymers 83 95-102 (2006)
  49. Crystal structure of the noncompetitive xylanase inhibitor TLXI, member of the small thaumatin-like protein family. Vandermarliere E, Lammens W, Schoepe J, Rombouts S, Fierens E, Gebruers K, Volckaert G, Rabijns A, Delcour JA, Strelkov SV, Courtin CM. Proteins 78 2391-2394 (2010)
  50. Functional characterization of Penicillium occitanis Pol6 and Penicillium funiculosum GH11 xylanases. Driss D, Berrin JG, Juge N, Bhiri F, Ghorbel R, Chaabouni SE. Protein Expr. Purif. 90 195-201 (2013)
  51. His22 of TLXI plays a critical role in the inhibition of glycoside hydrolase family 11 xylanases. Rombouts S, Fierens E, Vandermarliere E, Voet A, Gebruers K, Beaugrand J, Courtin CM, Delcour JA, de Maeyer M, Rabijns A, Van Campenhout S, Volckaert G. J Enzyme Inhib Med Chem 24 38-46 (2009)
  52. Differential representation of albumins and globulins during grain development in durum wheat and its possible functional consequences. Arena S, D'Ambrosio C, Vitale M, Mazzeo F, Mamone G, Di Stasio L, Maccaferri M, Curci PL, Sonnante G, Zambrano N, Scaloni A. J Proteomics 162 86-98 (2017)
  53. Improving the temperature characteristics and catalytic efficiency of a mesophilic xylanase from Aspergillus oryzae, AoXyn11A, by iterative mutagenesis based on in silico design. Li XQ, Wu Q, Hu D, Wang R, Liu Y, Wu MC, Li JF. AMB Express 7 97 (2017)
  54. Modulation of inhibitory activity of xylanase-α-amylase inhibitor protein (XAIP): binding studies and crystal structure determination of XAIP-II from Scadoxus multiflorus at 1.2 Å resolution. Kumar S, Singh N, Mishra B, Dube D, Sinha M, Singh SB, Dey S, Kaur P, Sharma S, Singh TP. BMC Struct. Biol. 10 41 (2010)
  55. A Fungal Versatile GH10 Endoxylanase and Its Glycosynthase Variant: Synthesis of Xylooligosaccharides and Glycosides of Bioactive Phenolic Compounds. Pozo-Rodríguez A, Méndez-Líter JA, de Eugenio LI, Nieto-Domínguez M, Calviño E, Cañada FJ, Santana AG, Díez J, Asensio JL, Barriuso J, Prieto A, Martínez MJ. Int J Mol Sci 23 1383 (2022)
  56. CRISPR/Cas9-Mediated Disruption of Xylanase inhibitor protein (XIP) Gene Improved the Dough Quality of Common Wheat. Sun Z, Zhang M, An Y, Han X, Guo B, Lv G, Zhao Y, Guo Y, Li S. Front Plant Sci 13 811668 (2022)
  57. Directed Modification of a GHF11 Thermostable Xylanase AusM for Enhancing Inhibitory Resistance towards SyXIP-I and Application of AusMPKK in Bread Making. Zhang D, Huang J, Liu Y, Chen X, Gao T, Li N, Huang W, Wu M. Foods 12 3574 (2023)
  58. Laboratory Evolution of GH11 Endoxylanase Through DNA Shuffling: Effects of Distal Residue Substitution on Catalytic Activity and Active Site Architecture. Liu MQ, Li JY, Rehman AU, Xu X, Gu ZJ, Wu RC. Front Bioeng Biotechnol 7 350 (2019)
  59. Molecular Cloning and Characterizations of Xylanase Inhibitor Protein from Wheat (Triticum Aestivum). Liu X, Zhang Y, Wei Z, Chen H, Jia X. J. Food Sci. 82 1582-1587 (2017)