Multiple rewards from a treasure trove of novel glycoside hydrolase and polysaccharide lyase structures: New folds, mechanistic details, and evolutionary relationships

Current Opinion in Structural Biology

Volumn 23, Issue 5, 2013, Pages 652-659

  Fushinobu, Shinya ^a   Alves, Victor D ^b   Coutinho, Pedro M ^c  

^a UNIVERSITY OF TOKYO   (Japan)

^b FACULDADE DE MEDICINA VETERINÁRIA   (Portugal)

^c AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; CELLULASE; GALACTOSYLCERAMIDASE; GLYCAN; GLYCOSIDASE; HEMICELLULASE; POLYSACCHARIDE LYASE; UNCLASSIFIED DRUG;

BACTERIAL STRAIN; BIFIDOBACTERIUM; CLOSTRIDIUM PERFRINGENS; CLOSTRIDIUM THERMOCELLUM; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME STRUCTURE; HUMAN; HYPOCREA JECORINA; INTESTINE FLORA; MOUTH FLORA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN HYDROLYSIS; REVIEW; SEAWEED; STREPTOCOCCUS MUTANS; STREPTOCOCCUS PNEUMONIAE; STRUCTURE ANALYSIS; TRICHODERMA VIRIDE;

ANIMALS; CATALYSIS; CELLULASE; GALACTOSYLCERAMIDASE; GLYCOSIDE HYDROLASES; HUMANS; HYDROLYSIS; PLANTS; POLYSACCHARIDE-LYASES; POLYSACCHARIDES; PROTEIN CONFORMATION;

EID: 84885472999     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.06.001     Document Type: Review

References (46)

1. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombard V., Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 2009, 37:D233-D238.
2. Henrissat B. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 1991, 280:309-316.
3. Lombard V., Bernard T., Rancurel C., Brumer H., Coutinho P.M., Henrissat B. A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem J 2010, 432:437-444.
4. Henrissat B., Sulzenbacher G., Bourne Y. Glycosyltransferases, glycoside hydrolases: surprise, surprise!. Curr Opin Struct Biol 2008, 18:527-533.
5. Brás J.L., Cartmell A., Carvalho A.L., Verzé G., Bayer E.A., Vazana Y., Correia M.A., Prates J.A., Ratnaparkhe S., Boraston A.B., et al. Structural insights into a unique cellulase fold and mechanism of cellulose hydrolysis. Proc Natl Acad Sci U S A 2011, 108:5237-5242.
6. Ficko-Blean E., Stuart C.P., Boraston A.B. Structural analysis of CPF_2247, a novel alpha-amylase from Clostridium perfringens. Proteins 2011, 79:2771-2777.
7. Gregg K.J., Zandberg W.F., Hehemann J.H., Whitworth G.E., Deng L., Vocadlo D.J., Boraston A.B. Analysis of a new family of widely distributed metal-independent alpha-mannosidases provides unique insight into the processing of N-linked glycans. J Biol Chem 2011, 286:15586-15596.
8. Kawahara R., Saburi W., Odaka R., Taguchi H., Ito S., Mori H., Matsui H. Metabolic mechanism of mannan in a ruminal bacterium, Ruminococcus albus, involving two mannoside phosphorylases and cellobiose 2-epimerase: discovery of a new carbohydrate phosphorylase, beta-1,4-mannooligosaccharide phosphorylase. J Biol Chem 2012, 287:42389-42399.
9. Levasseur A., Drula E., Lombard V., Coutinho P.M., Henrissat B. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 2013, 6:41.
10. Carapito R., Imberty A., Jeltsch J.M., Byrns S.C., Tam P.H., Lowary T.L., Varrot A., Phalip V. Molecular basis of arabinobio-hydrolase activity in phytopathogenic fungi: crystal structure and catalytic mechanism of Fusarium graminearum GH93 exo-alpha-l-arabinanase. J Biol Chem 2009, 284:12285-12296.
11. Ishida T., Fushinobu S., Kawai R., Kitaoka M., Igarashi K., Samejima M. Crystal structure of glycoside hydrolase family 55 beta-1,3-glucanase from the basidiomycete Phanerochaete chrysosporium. J Biol Chem 2009, 284:10100-10109.
12. Wu H.M., Liu S.W., Hsu M.T., Hung C.L., Lai C.C., Cheng W.C., Wang H.J., Li Y.K., Wang W.C. Structure, mechanistic action, and essential residues of a GH-64 enzyme, laminaripentaose-producing beta-1,3-glucanase. J Biol Chem 2009, 284:26708-26715.
13. Huang C.H., Sun Y., Ko T.P., Chen C.C., Zheng Y., Chan H.C., Pang X., Wiegel J., Shao W., Guo R.T. The substrate/product-binding modes of a novel GH120 beta-xylosidase (XylC) from Thermoanaerobacterium saccharolyticum JW/SL-YS485. Biochem J 2012, 448:401-407.
14. Deane J.E., Graham S.C., Kim N.N., Stein P.E., McNair R., Cachon-Gonzalez M.B., Cox T.M., Read R.J. Insights into Krabbe disease from structures of galactocerebrosidase. Proc Natl Acad Sci U S A 2011, 108:15169-15173.
15. Cho I., Blaser M.J. The human microbiome: at the interface of health and disease. Nat Rev Genet 2012, 13:260-270.
16. Higgins M.A., Whitworth G.E., El Warry N., Randriantsoa M., Samain E., Burke R.D., Vocadlo D.J., Boraston A.B. Differential recognition and hydrolysis of host carbohydrate antigens by Streptococcus pneumoniae family 98 glycoside hydrolases. J Biol Chem 2009, 284:26161-26173.
17. Stam M.R., Blanc E., Coutinho P.M., Henrissat B. Evolutionary and mechanistic relationships between glycosidases acting on alpha- and beta-bonds. Carbohydr Res 2005, 340:2728-2734.
18. Sela D.A., Mills D.A. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol 2010, 18:298-307.
19. Fushinobu S. Unique sugar metabolic pathways of bifidobacteria. Biosci Biotechnol Biochem 2010, 74:2374-2384.
20. Hidaka M., Nishimoto M., Kitaoka M., Wakagi T., Shoun H., Fushinobu S. The crystal structure of galacto-N-biose/lacto-N-biose I phosphorylase: a large deformation of a TIM barrel scaffold. J Biol Chem 2009, 284:7273-7283.
21. 2+-dependent family of alpha-mannosidases in a human gut symbiont. Nat Chem Biol 2010, 6:125-132.
22. Thompson A.J., Williams R.J., Hakki Z., Alonzi D.S., Wennekes T., Gloster T.M., Songsrirote K., Thomas-Oates J.E., Wrodnigg T.M., Spreitz J., et al. Structural and mechanistic insight into N-glycan processing by endo-alpha-mannosidase. Proc Natl Acad Sci U S A 2012, 109:781-786.
23. Vujicic-Zagar A., Pijning T., Kralj S., Lopez C.A., Eeuwema W., Dijkhuizen L., Dijkstra B.W. Crystal structure of a 117kDa glucansucrase fragment provides insight into evolution and product specificity of GH70 enzymes. Proc Natl Acad Sci U S A 2010, 107:21406-21411.
24. Ito K., Ito S., Shimamura T., Weyand S., Kawarasaki Y., Misaka T., Abe K., Kobayashi T., Cameron A.D., Iwata S. Crystal structure of glucansucrase from the dental caries pathogen Streptococcus mutans. J Mol Biol 2011, 408:177-186.
25. Suzuki N., Kim Y.M., Fujimoto Z., Momma M., Okuyama M., Mori H., Funane K., Kimura A. Structural elucidation of dextran degradation mechanism by Streptococcus mutans dextranase belonging to glycoside hydrolase family 66. J Biol Chem 2012, 287:19916-19926.
26. Michikawa M., Ichinose H., Momma M., Biely P., Jongkees S., Yoshida M., Kotake T., Tsumuraya Y., Withers S.G., Fujimoto Z., et al. Structural and biochemical characterization of glycoside hydrolase family 79 beta-glucuronidase from Acidobacterium capsulatum. J Biol Chem 2012, 287:14069-14077.
27. Hehemann J.H., Correc G., Barbeyron T., Helbert W., Czjzek M., Michel G. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 2010, 464:908-912.
28. Rebuffet E., Groisillier A., Thompson A., Jeudy A., Barbeyron T., Czjzek M., Michel G. Discovery and structural characterization of a novel glycosidase family of marine origin. Environ Microbiol 2011, 13:1253-1270.
29. Hehemann J.H., Kelly A.G., Pudlo N.A., Martens E.C., Boraston A.B. Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci U S A 2012, 109:19786-19791.
30. Vuong T.V., Wilson D.B. Glycoside hydrolases: catalytic base/nucleophile diversity. Biotechnol Bioeng 2010, 107:195-205.
31. Litzinger S., Fischer S., Polzer P., Diederichs K., Welte W., Mayer C. Structural and kinetic analysis of Bacillus subtilis N-acetylglucosaminidase reveals a unique Asp-His dyad mechanism. J Biol Chem 2010, 285:35675-35684.
32. Hehemann J.H., Smyth L., Yadav A., Vocadlo D.J., Boraston A.B. Analysis of keystone enzyme in Agar hydrolysis provides insight into the degradation (of a polysaccharide from) red seaweeds. J Biol Chem 2012, 287:13985-13995.
33. Han Y.H., Garron M.L., Kim H.Y., Kim W.S., Zhang Z., Ryu K.S., Shaya D., Xiao Z., Cheong C., Kim Y.S., et al. Structural snapshots of heparin depolymerization by heparin lyase I. J Biol Chem 2009, 284:34019-34027.
34. Ochiai A., Yamasaki M., Mikami B., Hashimoto W., Murata K. Crystal structure of exotype alginate lyase Atu3025 from Agrobacterium tumefaciens. J Biol Chem 2010, 285:24519-24528.
35. Ogura K., Yamasaki M., Yamada T., Mikami B., Hashimoto W., Murata K. Crystal structure of family 14 polysaccharide lyase with pH-dependent modes of action. J Biol Chem 2009, 284:35572-35579.
36. Abbott D.W., Gilbert H.J., Boraston A.B. The active site of oligogalacturonate lyase provides unique insights into cytoplasmic oligogalacturonate beta-elimination. J Biol Chem 2010, 285:39029-39038.
37. Konno N., Ishida T., Igarashi K., Fushinobu S., Habu N., Samejima M., Isogai A. Crystal structure of polysaccharide lyase family 20 endo-beta-1,4-glucuronan lyase from the filamentous fungus Trichoderma reesei. FEBS Lett 2009, 583:1323-1326.
38. Ando T., Kodera N., Takai E., Maruyama D., Saito K., Toda A. A high-speed atomic force microscope for studying biological macromolecules. Proc Natl Acad Sci U S A 2001, 98:12468-12472.
39. Igarashi K., Koivula A., Wada M., Kimura S., Penttila M., Samejima M. High speed atomic force microscopy visualizes processive movement of Trichoderma reesei cellobiohydrolase I on crystalline cellulose. J Biol Chem 2009, 284:36186-36190.
40. Igarashi K., Uchihashi T., Koivula A., Wada M., Kimura S., Okamoto T., Penttila M., Ando T., Samejima M. Traffic jams reduce hydrolytic efficiency of cellulase on cellulose surface. Science 2011, 333:1279-1282.
41. Fox J.M., Jess P., Jambusaria R.B., Moo G.M., Liphardt J., Clark D.S., Blanch H.W. A single-molecule analysis reveals morphological targets for cellulase synergy. Nat Chem Biol 2013, 9:356-361. 10.1038/nchembio.1227.
42. Davies G.J., Planas A., Rovira C. Conformational analyses of the reaction coordinate of glycosidases. Acc Chem Res 2012, 45:308-316.
43. Zheng M., Zhang H., Xu D. Initial events in the degradation of hyaluronan catalyzed by hyaluronate lyase from Spectrococcus pneumoniae: QM/MM simulation. J Phys Chem B 2012, 116:11166-11172.
44. Stam M.R., Danchin E.G., Rancurel C., Coutinho P.M., Henrissat B. Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of alpha-amylase-related proteins. Protein Eng Des Sel 2006, 19:555-562.
45. St John F.J., Gonzalez J.M., Pozharski E. Consolidation of glycosyl hydrolase family 30: a dual domain 4/7 hydrolase family consisting of two structurally distinct groups. FEBS Lett 2010, 584:4435-4441.
46. Aspeborg H., Coutinho P.M., Wang Y., Brumer H., Henrissat B. Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol 2012, 12:186.