Analysis of surface binding sites (SBSs) in carbohydrate active enzymes with focus on glycoside hydrolase families 13 and 77 -a mini-review

详细信息查看全文

作者：Darrell Cockburn (1) Casper Wilkens (1) Christian Ruzanski (2) Susan Andersen (1) Jonas Willum Nielsen (3) Alison M. Smith (2) Robert A. Field (2) Martin Willemo?s (3) Maher Abou Hachem (1) Birte Svensson (1)
关键词：secondary binding sites ; carbohydrate binding modules ; GH13 subfamilies ; crystal structures ; surface plasmon resonance ; affinity gel electrophoresis ; amylopectin hydrolysis kinetics
刊名：Biologia
出版年：2014
出版时间：June 2014
年：2014
卷：69
期：6
页码：705-712
全文大小：
参考文献：1. Abe A., Yoshida H., Tonozuka T., Sakano Y. & Kamitori S. 2005. Complexes of / Thermoactinomyces vulgaris R-47 / α-amylase 1 and pullulan model oligosaccharides provide new insight into the mechanism for recognizing substrates with / α-(1,6) glycosidic linkages. FEBS J. 272: 6145-153. blank" title="It opens in new window">CrossRef 2. Albenne C., Skov L.K., Mirza O., Gajhede M., Feller G., D’Amico S., André G., Potocki-Véronèse G., van der Veen B.A., Monsan P. & Remaud-Simeon M. 2004. Molecular basis of the amylose-like polymer formation catalyzed by / Neisseria polysaccharea amylosucrase. J. Biol. Chem. 279: 726-34. bc.M309891200" target="_blank" title="It opens in new window">CrossRef 3. Baskaran S., Chikwana V.M., Contreras C.J., Davis K.D., Wilson W.A., Depaoli-Roach A.A., Roach P.J. & Hurley T.D. 2011. Multiple glycogen binding sites in eukaryotic glycogen synthase are required for high catalytic efficiency toward glycogen. J. Biol. Chem. 286: 33999-4006. bc.M111.264531" target="_blank" title="It opens in new window">CrossRef 4. Bozonnet S., Jensen M.T., Nielsen M.M., Aghajari N., Jensen M.H., Kramh?ft B., Willemo?s M., Tranier S., Haser R. & Svensson B. 2007. The ‘pair of sugar tongs-on the noncatalytic domain C of barley / α-amylase participates in substrate binding and activity. FEBS J. 274: 5055-067. blank" title="It opens in new window">CrossRef 5. Caner S., Nguyen N., Aguda A., Zhang R., Pan Y.T., Withers S.G. & Brayer G. 2013. The structure of / Mycobacterium smegmatis trehalose synthase reveals an unusual active site configuration and acarbose-binding-mode. Glycobiology 23: 1075-083. b/cwt044" target="_blank" title="It opens in new window">CrossRef 6. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombard V. & Henrissat B. 2009. The Carbohydrate-Active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37: D233–D238. blank" title="It opens in new window">CrossRef 7. Chaen K., Noguchi J., Omori T., Kakuta Y. & Kimura M. 2012. Crystal structure of the rice branching enzyme I (BEI) in complex with maltopentaose. Biochem. Biophys. Res. Commun. 424: 508-11. bbrc.2012.06.145" target="_blank" title="It opens in new window">CrossRef 8. Cockburn D. & Svensson B. 2013. Surface binding sites in carbohydrate active enzymes: an emerging picture of structural and functional diversity, pp. 204-21. In: Rauter P. & Lindhorst T. (eds), Carbohydrate Chemistry vol. 39, Royal Society of Chemistry, Cambridge, United Kingdom. 9. Cuesta-Seijo J.A., Nielsen M.M., Marri L., Tanaka H., Beeren S.R. & Palcic M.M. 2013. Structure of starch synthase I from barley: insight into regulatory mechanisms of starch synthase activity. Acta Crystallogr. D Biol, Crystallogr. 69: 1013-025. blank" title="It opens in new window">CrossRef 10. Cuyvers S., Dornez E., Abou Hachem M., Svensson B., Horhorn M., Chory J., Delcour J.A. & Courtin C.M. 2012. Isothermal titration calorimetry and surface plasmon resonance allow quantifying substrate binding to different binding sites of / Bacillus subtilis xylanase. Anal. Biochem. 420: 90-2. b.2011.09.005" target="_blank" title="It opens in new window">CrossRef 11. Cuyvers S., Dornez E., Delcour J.A. & Courtin C.M. 2012. Occurrence and functional significance of secondary carbohydrate binding sites in glycoside hydrolases. Crit. Rev. Biotechnol. 32: 93-07. blank" title="It opens in new window">CrossRef 12. Dauter Z., Dauter M., Brzozowski A.M., Christensen S., Borchert T.V., Beier L., Wilson K.S. & Davies G.J. 1999. X-ray structure of Novamyl, the five-domain “maltogenic- / α-amylase from / Bacillus stearothermophilus: maltose and acarbose complexes at 1.7 ? resolution. Biochemistry 38: 8385-392. bi990256l" target="_blank" title="It opens in new window">CrossRef 13. Diaz A., Martínez-Pons C., Fita I., Ferrer J.C. & Guinovart J.J. 2011. Processivity and subcellular localization of glycogen synthase depend on a non-catalytic high affinity glycogenbinding site. J. Biol. Chem. 286: 18505-8514. bc.M111.236109" target="_blank" title="It opens in new window">CrossRef 14. Diemer S.K., Svensson B., Babol L.N., Cockburn D., Grijpstra P., Dijkhuizen L., Folkenberg D.M., Garrigues C. & Ipsen R.H. 2012. Binding interactions between / α-glucans from / Lactobacillus reuteri and milk proteins characterized by surface plasmon resonance. Food Biophys. 7: 220-26. blank" title="It opens in new window">CrossRef 15. Fawaz R., Feng L., Hovde S., Mort A. & Geiger J.H. 2013. Structure, function and specificity of branching enzyme, p. 27. In: Janecek S. (ed.) ALAMY 5 -5^th Symposium on the Alpha-Amylase Family, Programme and Abstracts, 20-4 October 2013, Smolenice Castle, Slovakia. 16. Fletterick R.J., Sygusch J., Semple H. & Madsen N.B. 1976. Structure of glycogen phosphorylase at 3.0-?-resolution and its ligand binding sites at 6-?. J. Biol. Chem. 251: 6142-146. 17. Fujii K., Minagawa H., Terada Y., Takaha T., Kuriki T., Shimada J. & Kaneko H. 2005. Use of random mutageneses to improve the properties of / Thermus aquaticus amylomaltase for efficient production of cycloamyloses. Appl. Environ. Microbiol. 71: 5823-827. blank" title="It opens in new window">CrossRef 18. Fujii K., Minagawa H., Terada Y., Takaha T., Kuriki T., Shimada J. & Kaneko H. 2007. Function of second glucan binding site including tyrosines 54 and 101 in / Thermus aquaticus amylomaltase. J. Biosci. Bioeng. 103: 167-73. bb.103.167" target="_blank" title="It opens in new window">CrossRef 19. Guce A.I., Clark N.E., Salgado E.N., Ivanen D.R., Kulminskaya A.A., Brumer H. & Garman S.C. 2010. Catalytic mechanism of human / α-galactosidase. J. Biol. Chem. 285: 3625-632. bc.M109.060145" target="_blank" title="It opens in new window">CrossRef 20. Gentry M.S., Dixon J.E. & Worby C.A. 2009. Lafora disease: insights into neurodegeneration from plant metabolism. Trends Biochem. Sci. 34: 628-39. bs.2009.08.002" target="_blank" title="It opens in new window">CrossRef 21. Janecek S., Svensson B. & MacGregor E.A. 2011. Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding from microbes, plant and animals. Enzyme Microb. Technol. 49: 429-40. blank" title="It opens in new window">CrossRef 22. Janecek S., Svensson B. & MacGregor E.A. 2014. / α-Amylase -an enzyme specificity found in various families of glycoside hydrolases. Cell. Mol. Life Sci. 71: 1149-170. blank" title="It opens in new window">CrossRef 23. Juge N., Andersen J.S., Tull D., Roepstorff P. & Svensson B. 1996. Overexpression, purification, and characterization of recombinant barley / α-amylases 1 and 2 secreted by the methylotrophic yeast / Pichia pastoris. Protein Expr. Purif. 8: 204-14. blank" title="It opens in new window">CrossRef 24. Juge N., N?hr J., Le Gal-Co?ffet M.-F., Kramh?ft B., Furniss C.S.M., Planchot V., Archer D.B., Williamson G. & Svensson B. 2006. The activity of barley / α-amylase on starch granules is enhanced by fusion of a starch binding domain from / Aspergillus niger glucoamylase. Biochim. Biophys. Acta 1764: 275-84. bbapap.2005.11.008" target="_blank" title="It opens in new window">CrossRef 25. Koropatkin N.M. & Smith T.J. 2010. SusG: a unique cellmembrane-associated / α-amylase from a prominent human gut symbiont targets complex starch molecules. Structure 18: 200-15. blank" title="It opens in new window">CrossRef 26. Kramh?ft B., Bak-Jensen K.S., Mori H., Juge N., N?hr J. & Svensson B. 2005. Involvement of individual subsites and secondary substrate binding sites in multiple attack on amylase by barley / α-amylase. Biochemistry 44: 1824-832. bi048100v" target="_blank" title="It opens in new window">CrossRef 27. Leemhuis H., Pijning T., Dobruchowska J.M., Leeuwen S.S., Kralj S., Dijkstra B.W. & Dijkhuizen L. 2013. Threedimensional structures, reactions, mechanism, / α-glucan analysis and their implications in biotechnology and food applications. J. Biotechnol. 163: 250-72. biotec.2012.06.037" target="_blank" title="It opens in new window">CrossRef 28. Linden A., Mayans O., Meyer-Klaucke W., Antranikian G. & Wilmanns M. 2003. Differential regulation of a hyperthermophilic / α-amylase with a novel (Ca,Zn) two-metal center by zinc. J. Biol. Chem. 278: 9875-884. bc.M211339200" target="_blank" title="It opens in new window">CrossRef 29. Ludwiczek M.L., Heller M., Kantner T. & McIntosh L.P. 2007. A secondary xylan-binding site enhances the catalytic activity of a single-domain family 11 glycoside hydrolase. J. Mol. Biol. 373: 337-54. b.2007.07.057" target="_blank" title="It opens in new window">CrossRef 30. Lyhne-Iversen L., Hobley T.J., Kaasgaard S.G. & Harris P. 2006 Structure of / Bacillus halmapalus α-amylase crystallized with and without the substrate analogue acarbose and maltose. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62: 849-54. blank" title="It opens in new window">CrossRef 31. Meekins D.A., Guo H.F., Husodo S., Paasch B.C., Bridges T.M., Santelia D., Kottin O., Vander Kooi C.W. & Gentry M.S. 2013. Structure of the / Arabidopsis glucan phosphatase LIKE SEX FOUR2 reveals a unique mechanism for starch dephosphorylation. Plant Cell 25: 2301-314. blank" title="It opens in new window">CrossRef 32. Nielsen J.W., Kramh?ft B., Bozonnet S., Abou Hachem M., Stipp S.L.S., Svensson B. & Willemo?s M. 2012. Degradation of the starch components amylopectin and amylose by barley / α-amylase 1: role of surface binding site 2. Arch. Biochem. Biophys. 528: 1-. bb.2012.08.005" target="_blank" title="It opens in new window">CrossRef 33. Nielsen M.M., Bozonnet S., Seo E.-S., Mótyán J.A., Andersen J.M., Dilokpimol A., Abou Hachem M., Gyémánt G., Naested H., Kandra L., Sigurskjold B.W. & Svensson B. 2009. Two secondary carbohydrate binding sites on the surface of barley / α-amylase 1 have distinct functions and display synergy in hydrolysis of starch granules. Biochemistry 48: 7686-697. bi900795a" target="_blank" title="It opens in new window">CrossRef 34. Nielsen M.M., Seo E.S., Bozonnet S., Aghajari N., Robert X., Haser R. & Svensson B. 2008. Multi-site substrate binding and interplay in barley / α-amylase 1. FEBS Lett. 582: 2567-571. bslet.2008.06.027" target="_blank" title="It opens in new window">CrossRef 35. Oudjeriouat N., Moreau Y., Santimone M., Svensson B., Marchis-Mouren G. & Desseaux V. 2003. Mechanism of barley / α-amylase. Inhibition of amylose, maltodextrin and maltoheptaose hydrolysis by acarbose and cyclodextrin. Eur. J. Biochem. 270: 3871-879. blank" title="It opens in new window">CrossRef 36. Pinotsis N., Leonidas D.D., Chrysina E.D., Oikonomakos N.G. & Mavridis I.M. 2003. The binding of / β- and / γ-cyclodextrins to glycogen phosphorylase b: kinetic and crystallographic studies. Protein Sci. 12: 1914-924. blank" title="It opens in new window">CrossRef 37. Przylas I., Terada Y., Fujii K., Takaha T., Saenger W. & Strater, N. 2000. X-ray structure of acarbose bound to amylomaltase from / Thermus aquaticus -Implications for the synthesis of large cyclic glucans. Eur. J. Biochem. 267: 6903-913. 38. Qian M.X., Haser R. & Payan F. 1995. Carbohydrate-binding sites in a pancreatic / α-amylase-substrate complex derived from X-ray structure analysis at 2.1 ? resolution. Protein Sci. 4: 747-55. blank" title="It opens in new window">CrossRef 39. Ragunath C., Manuel S.G., Venkataraman V., Sait H.B.R., Kasinathan C. & Ramasubbu N. 2008. Probing the role of aromatic residues at the secondary saccharide-binding sites of human salivary / α-amylase in substrate hydrolysis and bacterial binding. J. Mol. Biol. 384: 1232-248. b.2008.09.089" target="_blank" title="It opens in new window">CrossRef 40. Robert X., Haser R., Gottschalk T., Ratajczek F., Driguez H., Svensson B. & Aghajari N. 2003. The structure of barley / α-amylase isozyme 1 reveals a novel role of domain C in substrate recognition and binding. A pair of sugar tongs. Structure 11: 973-84. blank" title="It opens in new window">CrossRef 41. Robert X., Haser R., Mori H., Svensson B. & Aghajari N. 2005. Oligosaccharide binding to barley / α-amylase 1. J. Biol. Chem. 280: 32968-2978. bc.M505515200" target="_blank" title="It opens in new window">CrossRef 42. Robyt J.F. & French D. 1967. Multiple attack hypothesis of / α-amylase action: action of porcine pancreatic, human salivary, and / Aspergillus oryzae α-amylases. Arch. Biochem. Biophys. 122: 8-6. blank" title="It opens in new window">CrossRef 43. Ruzanski C., Smirnova J., Rejzek M., Cockburn D., Pedersen H.L., Pike M., Willats W.G.T., Svensson B., Steup M., Smith A.M. & Field R.A. 2013 A simple bacterial glucanotransferase can complement / Arabidopsis mutants defective in cytosolic maltose metabolism. J. Biol. Chem. 288: 28581-8598. bc.M113.497867" target="_blank" title="It opens in new window">CrossRef 44. Seo E.S., Andersen J.M., Nielsen M.M., Vester-Christensen M.B., Christiansen C., Jensen J.M., Mótyán J.A., Glaring M.A., Blennow A., Kandra L., Gyémánt G., Jane?ek ?., Haser R., Aghajari N., Abou Hachem M. & Svensson B. 2010. New insight into structure/function relationships in plant / α-amylase family GH13 members. J. Appl. Glycosci. 57: 157-62. blank" title="It opens in new window">CrossRef 45. Seo E.S., Christiansen C., Abou Hachem M., Nielsen M.M., Fukuda K., Bozonnet S., Blennow A., Aghajari N., Haser R. & Svensson B. 2008. An enzyme family reunion -similarities, differences and eccentricities in actions on / α-glucans. Biologia 63: 967-79. blank" title="It opens in new window">CrossRef 46. Southall S.M., Simpson P.J., Gilbert H.J., Williamson G. & Williamson M.P. 1999. The starch-binding domain from glucoamylase disrupts the structure of starch. FEBS Lett. 447: 58-0. blank" title="It opens in new window">CrossRef 47. Stam M.R., Danchin E.G.J., Rancurel C., Coutinho P.M. & Henrissat B. 2006. Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of / α-amylase-related proteins. Protein Eng. Des. Sel. 19: 555-62. blank" title="It opens in new window">CrossRef 48. Syson K., Stevenson C.E.M., Rashid A., Leiba J., Tuukkanen A., Svergun D.I., Molle V., Lawson D. & Bornemann S. 2013. Binding, catalysis and regulation of the anti-TB target GH13 3 GlgE, p. 22. In: Janecek S. (ed.) ALAMY 5 -5^th Symposium on the Alpha-Amylase Family, Programme and Abstracts, 20-4 October 2013, Smolenice Castle, Slovakia. 49. Tan T.C., Mijts B.N., Swaminathan K., Patel B.K.C. & Divne C. 2008. Crystal structure of the polyextremophilic / α-amylase AmyB from / Halothermothrix orenii: details of a productive enzyme-substrate complex and an N domain with a role in binding raw starch. J. Mol. Biol. 378: 850-68. b.2008.02.041" target="_blank" title="It opens in new window">CrossRef 50. Timmins J., Leiros H.-K.S., Leonard G., Leiros, I. & McSweeney S. 2005. Crystal structure of maltooligosyltrehalose trehalohydrolase from / Deinococcus radiodurans in complex with disaccharides. J. Mol. Biol. 347: 949-63. b.2005.02.011" target="_blank" title="It opens in new window">CrossRef 51. Vujicic-?agar A. & Dijkstra B.W. 2006. Monoclinic crystal form of / Aspergillus niger α-amylase in complex with maltose at 1.8 ? resolution. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62: 716-21. blank" title="It opens in new window">CrossRef
作者单位：Darrell Cockburn (1) Casper Wilkens (1) Christian Ruzanski (2) Susan Andersen (1) Jonas Willum Nielsen (3) Alison M. Smith (2) Robert A. Field (2) Martin Willemo?s (3) Maher Abou Hachem (1) Birte Svensson (1) 1. Enzyme and Protein Chemistry, Department of Systems Biology, Technical University of Denmark, DK 2800, Kgs. Lyngby, Denmark 2. John Innes Center, Norwich Research Park, Norwich, NR4 7UH, UK 3. Department of Biology, University of Copenhagen, Denmark, Ole Maal?es Vej 5, DK 2200, Copenhagen N, Denmark
ISSN：1336-9563

文摘

Surface binding sites (SBSs) interact with carbohydrates outside of the enzyme active site. They are frequently situated on catalytic domains and are distinct from carbohydrate binding modules (CBMs). SBSs are found in a variety of enzymes and often seen in crystal structures. Notably about half of the > 45 enzymes (in 17 GH and two GT families) with an identified SBS are from GH13 and a few from GH77, both belonging to clan GH-H of carbohydrate active enzymes. The many enzymes of GH13 with SBSs provide an opportunity to analyse their distribution within this very large and diverse family. SBS containing enzymes in GH13 are spread among 15 subfamilies (two were not assigned a subfamily). Comparison of these SBSs reveals a complex evolutionary history with evidence of conservation of key residues and/or structural location between some SBSs, while others are found at entirely distinct structural locations, suggesting convergent evolution. An array of investigations of the two SBSs in barley α-amylase demonstrated they play different functional roles in binding and degradation of polysaccharides. MalQ from Escherichia coli is an α-1,4-glucanotransferase of GH77, a family that is known to have at least one member that contains an SBS. Whereas MalQ is a single domain enzyme lacking CBMs, its plant orthologue DPE2 contains two N-terminal CBM20s. Surface plasmon resonance binding studies showed that MalQ and DPE2 have a similar affinity for β-cyclodextrin and that MalQ binds malto-oligosaccharides of >DP4 at a second site in competition with β-cyclodextrin yielding a stoichiometry >1. This suggests that MalQ may have an SBS, though its structural location remains unknown.

地址：北京市海淀区学院路29号邮编：100083

电话：办公室：(+86 10)66554848；文献借阅、咨询服务、科技查新：66554700