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Crystal structure of a family 54 alpha-L-arabinofuranosidase reveals a novel carbohydrate-binding module that can bind arabinose.

Miyanaga A, Koseki T, Matsuzawa H, Wakagi T, Shoun H, Fushinobu S
J Biol Chem 279 44907-14 (2004)
Cited: 52 times
EuropePMC logo PMID: 15292273

Abstract

As the first known structures of a glycoside hydrolase family 54 (GH54) enzyme, we determined the crystal structures of free and arabinose-complex forms of Aspergillus kawachii IFO4308 alpha-l-arabinofuranosidase (AkAbfB). AkAbfB comprises two domains: a catalytic domain and an arabinose-binding domain (ABD). The catalytic domain has a beta-sandwich fold similar to those of clan-B glycoside hydrolases. ABD has a beta-trefoil fold similar to that of carbohydrate-binding module (CBM) family 13. However, ABD shows a number of characteristics distinctive from those of CBM family 13, suggesting that it could be classified into a new CBM family. In the arabinose-complex structure, one of three arabinofuranose molecules is bound to the catalytic domain through many interactions. Interestingly, a disulfide bond formed between two adjacent cysteine residues recognized the arabinofuranose molecule in the active site. From the location of this arabinofuranose and the results of a mutational study, the nucleophile and acid/base residues were determined to be Glu(221) and Asp(297), respectively. The other two arabinofuranose molecules are bound to ABD. The O-1 atoms of the two arabinofuranose molecules bound at ABD are both pointed toward the solvent, indicating that these sites can both accommodate an arabinofuranose side-chain moiety linked to decorated arabinoxylans.

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  8. Specific and non-specific enzymes for furanosyl-containing conjugates: biosynthesis, metabolism, and chemo-enzymatic synthesis. Chlubnova I, Legentil L, Dureau R, Pennec A, Almendros M, Daniellou R, Nugier-Chauvin C, Ferrières V. Carbohydr Res 356 44-61 (2012)
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  2. The unique set of putative membrane-associated anti-sigma factors in Clostridium thermocellum suggests a novel extracellular carbohydrate-sensing mechanism involved in gene regulation. Kahel-Raifer H, Jindou S, Bahari L, Nataf Y, Shoham Y, Bayer EA, Borovok I, Lamed R. FEMS Microbiol Lett 308 84-93 (2010)
  3. Plasticity of the β-trefoil protein fold in the recognition and control of invertebrate predators and parasites by a fungal defence system. Schubert M, Bleuler-Martinez S, Butschi A, Wälti MA, Egloff P, Stutz K, Yan S, Collot M, Mallet JM, Wilson IB, Hengartner MO, Aebi M, Allain FH, Künzler M. PLoS Pathog 8 e1002706 (2012)
  4. Crystal structure of an inverting GH 43 1,5-alpha-L-arabinanase from Geobacillus stearothermophilus complexed with its substrate. Alhassid A, Ben-David A, Tabachnikov O, Libster D, Naveh E, Zolotnitsky G, Shoham Y, Shoham G. Biochem J 422 73-82 (2009)
  5. 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)
  6. Characterization of a modular enzyme of exo-1,5-alpha-L-arabinofuranosidase and arabinan binding module from Streptomyces avermitilis NBRC14893. Ichinose H, Yoshida M, Fujimoto Z, Kaneko S. Appl Microbiol Biotechnol 80 399-408 (2008)
  7. Detecting internally symmetric protein structures. Kim C, Basner J, Lee B. BMC Bioinformatics 11 303 (2010)
  8. An elaboration on the syn-anti proton donor concept of glycoside hydrolases: electrostatic stabilisation of the transition state as a general strategy. Nerinckx W, Desmet T, Piens K, Claeyssens M. FEBS Lett 579 302-312 (2005)
  9. Crystal structures of a glycoside hydrolase family 20 lacto-N-biosidase from Bifidobacterium bifidum. Ito T, Katayama T, Hattie M, Sakurama H, Wada J, Suzuki R, Ashida H, Wakagi T, Yamamoto K, Stubbs KA, Fushinobu S. J Biol Chem 288 11795-11806 (2013)
  10. Molecular basis of arabinobio-hydrolase activity in phytopathogenic fungi: crystal structure and catalytic mechanism of Fusarium graminearum GH93 exo-alpha-L-arabinanase. Carapito R, Imberty A, Jeltsch JM, Byrns SC, Tam PH, Lowary TL, Varrot A, Phalip V. J Biol Chem 284 12285-12296 (2009)
  11. Elucidation of the molecular basis for arabinoxylan-debranching activity of a thermostable family GH62 α-l-arabinofuranosidase from Streptomyces thermoviolaceus. Wang W, Mai-Gisondi G, Stogios PJ, Kaur A, Xu X, Cui H, Turunen O, Savchenko A, Master ER. Appl Environ Microbiol 80 5317-5329 (2014)
  12. n→π* Interactions Modulate the Properties of Cysteine Residues and Disulfide Bonds in Proteins. Kilgore HR, Raines RT. J Am Chem Soc 140 17606-17611 (2018)
  13. Crystal structure and characterization of the glycoside hydrolase family 62 α-L-arabinofuranosidase from Streptomyces coelicolor. Maehara T, Fujimoto Z, Ichinose H, Michikawa M, Harazono K, Kaneko S. J Biol Chem 289 7962-7972 (2014)
  14. Characterization of a family 54 alpha-L-arabinofuranosidase from Aureobasidium pullulans. de Wet BJ, Matthew MK, Storbeck KH, van Zyl WH, Prior BA. Appl Microbiol Biotechnol 77 975-983 (2008)
  15. Substrate specificity and gene expression of two Penicillium chrysogenum α-L-arabinofuranosidases (AFQ1 and AFS1) belonging to glycoside hydrolase families 51 and 54. Sakamoto T, Inui M, Yasui K, Hosokawa S, Ihara H. Appl Microbiol Biotechnol 97 1121-1130 (2013)
  16. Characterization of the family GH54 alpha-L-arabinofuranosidases in Penicillium funiculosum, including a novel protein bearing a cellulose-binding domain. Guais O, Tourrasse O, Dourdoigne M, Parrou JL, Francois JM. Appl Microbiol Biotechnol 87 1007-1021 (2010)
  17. Mutagenesis and mechanistic study of a glycoside hydrolase family 54 alpha-L-arabinofuranosidase from Trichoderma koningii. Wan CF, Chen WH, Chen CT, Chang MD, Lo LC, Li YK. Biochem J 401 551-558 (2007)
  18. The first crystal structure of a family 129 glycoside hydrolase from a probiotic bacterium reveals critical residues and metal cofactors. Sato M, Liebschner D, Yamada Y, Matsugaki N, Arakawa T, Wills SS, Hattie M, Stubbs KA, Ito T, Senda T, Ashida H, Fushinobu S. J Biol Chem 292 12126-12138 (2017)
  19. Characterization of a new α-L: -arabinofuranosidase from Penicillium sp. LYG 0704, and their application in lignocelluloses degradation. Lee DS, Wi SG, Lee YG, Cho EJ, Chung BY, Bae HJ. Mol Biotechnol 49 229-239 (2011)
  20. Characterization of a chimeric enzyme comprising feruloyl esterase and family 42 carbohydrate-binding module. Koseki T, Mochizuki K, Kisara H, Miyanaga A, Fushinobu S, Murayama T, Shiono Y. Appl Microbiol Biotechnol 86 155-161 (2010)
  21. Do cultural conditions induce differential protein expression: Profiling of extracellular proteome of Aspergillus terreus CM20. M S, Singh S, Tiwari R, Goel R, Nain L. Microbiol Res 192 73-83 (2016)
  22. Differential expression of α-L-arabinofuranosidases during maize (Zea mays L.) root elongation. Kozlova LV, Gorshkov OV, Mokshina NE, Gorshkova TA. Planta 241 1159-1172 (2015)
  23. Double blind microarray-based polysaccharide profiling enables parallel identification of uncharacterized polysaccharides and carbohydrate-binding proteins with unknown specificities. Salmeán AA, Guillouzo A, Duffieux D, Jam M, Matard-Mann M, Larocque R, Pedersen HL, Michel G, Czjzek M, Willats WGT, Hervé C. Sci Rep 8 2500 (2018)
  24. Heterologous expression and characterization of α-L-arabinofuranosidase 4 from Penicillium purpurogenum and comparison with the other isoenzymes produced by the fungus. Ravanal MC, Eyzaguirre J. Fungal Biol 119 641-647 (2015)
  25. Structure of a GH51 α-L-arabinofuranosidase from Meripilus giganteus: conserved substrate recognition from bacteria to fungi. McGregor NGS, Turkenburg JP, Mørkeberg Krogh KBR, Nielsen JE, Artola M, Stubbs KA, Overkleeft HS, Davies GJ. Acta Crystallogr D Struct Biol 76 1124-1133 (2020)
  26. Analysis of the carbohydrate-binding-module from Fragaria x ananassa α-L-arabinofuranosidase 1. Sin IN, Perini MA, Martínez GA, Civello PM. Plant Physiol Biochem 107 96-103 (2016)
  27. Towards an Understanding of Oxidative Damage in an α-L-Arabinofuranosidase of Trichoderma reesei: a Molecular Dynamics Approach. Castaño JD, Zhou M, Schilling J. Appl Biochem Biotechnol 193 3287-3300 (2021)
  28. Integrative structure determination reveals functional global flexibility for an ultra-multimodular arabinanase. Lansky S, Salama R, Biarnés X, Shwartstein O, Schneidman-Duhovny D, Planas A, Shoham Y, Shoham G. Commun Biol 5 465 (2022)
  29. Structures of endo-1,5-α-L-arabinanase mutants from Bacillus thermodenitrificans TS-3 in complex with arabino-oligosaccharides. Yamaguchi A, Sogabe Y, Fukuoka S, Sakai T, Tada T. Acta Crystallogr F Struct Biol Commun 74 774-780 (2018)
  30. Production of a Fungal Punicalagin-Degrading Enzyme by Solid-State Fermentation: Studies of Purification and Characterization. Aguilar-Zárate P, Gutiérrez-Sánchez G, Michel MR, Bergmann CW, Buenrostro-Figueroa JJ, Ascacio-Valdés JA, Contreras-Esquivel JC, Aguilar CN. Foods 12 903 (2023)


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