Jump to ContentJump to Main Navigation
Show Summary Details
More options …


More options …
Volume 63, Issue 6


Domain evolution in the GH13 pullulanase subfamily with focus on the carbohydrate-binding module family 48

Martin Machovič / Štefan Janeček
  • Institute of Molecular Biology, Slovak Academy of Sciences, Dúbravská cesta 21, SK-84551, Bratislava, Slovakia
  • Department of Biotechnologies, Faculty of Natural Sciences, University of SS. Cyril and Methodius, Nám. J. Herdu 2, SK-91701, Trnava, Slovakia
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2008-12-04 | DOI: https://doi.org/10.2478/s11756-008-0162-4


Glycoside hydrolase (GH) family 13 comprises about 30 different specificities. Four of them have been proposed to form the GH13 pullulanase subfamily: pullulanase, isoamylase, maltooligosyl trehalohydrolase and branching enzyme forming the seven CAZy GH13 subfamilies: GH13 8-GH13 14. Recently, a new family of carbohydrate-binding modules (CBMs), the family CBM48 has been established containing the putative starch-binding domains from the pullulanase subfamily, the β-subunit of AMP-activated protein kinase and some other GH13 enzymes with pullulanase and/or α-amylase-pullulanase specificity. Since all of these enzymes are multidomain proteins and the structure for at least one representative of each enzyme specificity has already been determined, the main goal of the present study was to elucidate domain evolution within this GH13 pullulanase subfamily (84 real enzymes) focusing on the CBM48 module. With regard to CBM48 positioning in the amino acid sequence, the N-terminal end of a protein appears to be a predominant position. This is especially true for isoamylases and maltooligosyl trehalohydrolases. Secondary structure-based alignment of CBM modules from CBM48, CBM20 and CBM21 revealed that several residues known as consensus for CBM20 and CBM21 could also be identified in CBM48, but only branching enzymes possess the aromatic residues that correspond with the two tryptophans forming the evolutionary conserved starch-binding site 1 in CBM20. The evolutionary trees constructed for the individual domains, complete alignment, and the conserved sequence regions of the α-amylase family were found to be comparable to each other (except for the C-domain tree) with two basic parts: (i) branching enzymes and maltooligosyl trehalohydrolases; and (ii) pullulanases and isoamylases. Taxonomy was respected only within clusters with pure specificity, i.e. the evolution of CBM48 reflects the evolution of specificities rather than evolution of species. This is a feature different from the one observed for the starch-binding domain of the family CBM20 where the starch-binding domain evolution reflects the evolution of species.

Keywords: α-amylase enzyme family; pullulanase subfamily; starch-binding domain; domain evolution; evolutionary tree

  • [1] Abad M.C., Binderup K., Rios-Steiner J., Arni R.K., Preiss J. & Geiger J.H. 2002. The X-ray crystallographic structure of Escherichia coli branching enzyme. J. Biol. Chem. 277: 42164–42170. http://dx.doi.org/10.1074/jbc.M205746200CrossrefGoogle Scholar

  • [2] Abbott D.W., Eirin-Lopez J.M. & Boraston A.B. 2008. Insight into ligand diversity and novel biological roles for family 32 carbohydrate-binding modules. Mol. Biol. Evol. 25: 155–167. http://dx.doi.org/10.1093/molbev/msm243CrossrefGoogle Scholar

  • [3] Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410. Google Scholar

  • [4] Apweiler R., Bairoch A., Wu C.H., Barker W.C., Boeckmann B., Ferro S., Gasteiger E., Huang H., Lopez R., Magrane M. & Yeh L.S. 2004. UniProt: the Universal Protein knowledgebase. Nucleic Acids Res. 32: D115–D119. http://dx.doi.org/10.1093/nar/gkh131CrossrefGoogle Scholar

  • [5] Bateman A., Birney E., Cerruti L., Durbin R., Etwiller L., Eddy S.R., Griffiths-Jones S., Howe K.L., Marshall M. & Sonnhammer E.L. 2002. The Pfam protein families database. Nucleic Acids Res. 30: 276–280. http://dx.doi.org/10.1093/nar/30.1.276CrossrefGoogle Scholar

  • [6] Baunsgaard L., Lutken H., Mikkelsen R., Glaring M.A., Pham T.T. & Blennow A. 2005. A novel isoform of glucan, water dikinase phosphorylates pre-phosphorylated α-glucans and is involved in starch degradation in Arabidopsis. Plant J. 41: 595–605. http://dx.doi.org/10.1111/j.1365-313X.2004.02322.xCrossrefGoogle Scholar

  • [7] Benson D.A., Karsch-Mizrachi I., Lipman D.J., Ostell J. & Wheeler D.L. 2004. GenBank: update. Nucleic Acids Res. 32: D23–D26. http://dx.doi.org/10.1093/nar/gkh045CrossrefGoogle Scholar

  • [8] Berman H.M., Battistuz T., Bhat T.N., Bluhm W.F., Bourne P.E., Burkhardt K., Feng Z., Gilliland G.L., Iype L., Jain S. & Zardecki C. 2002. The protein data bank. Acta Crystallogr. D58: 899–907. CrossrefGoogle Scholar

  • [9] Boraston A.B., Bolam D.N., Gilbert H.J. & Davies G.J. 2004. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382: 769–781. http://dx.doi.org/10.1042/BJ20040892CrossrefGoogle Scholar

  • [10] Bozonnet S., Bonsager B.C., Kramhoft B., Mori H., Abou Hachem M., Willemoes M., Jensen M.T., Fukuda K., Nielsen P.K., Juge N., Aghajari N., Tranier S., Robert X., Haser R. & Svensson B. 2005. Binding of carbohydrates and protein inhibitors to the surface of α-amylases. Biologia 60(Suppl. 16): 27–36. Google Scholar

  • [11] Chen J.T., Chen M.C., Chen L.L. & Chu W.S. 2001. Structure and expression of an amylopullulanase gene from Bacillus stearothermophilus TS-23. Biotechnol. Appl. Biochem. 33: 189–199. http://dx.doi.org/10.1042/BA20010003CrossrefGoogle Scholar

  • [12] Coutinho P.M. & Henrissat B. 1999a. Carbohydrate-active enzymes: an integrated database approach, pp. 3–12. In: Recent Advances in Carbohydrate Bioengineering (Gilbert H.J., Davies G., Henrissat B. & Svensson B., eds), The Royal Society of Chemistry, Cambridge; http://www.cazy.org. Google Scholar

  • [13] Coutinho P.M. & Henrissat B. 1999b. The modular structure of cellulases and other carbohydrate-active enzymes: an integrated database approach, pp. 15–23. In: Genetics, Biochemistry and Ecology of Cellulose Degradation (Ohmiya K., Hayashi K., Sakka K., Kobayashi Y., Karita S. & Kimura T., eds), Uni Publishers Company, Tokyo. Google Scholar

  • [14] Durand A., Hughes R., Roussel A., Flatman R., Henrissat B. & Juge N. 2005. Emergence of a subfamily of xylanase inhibitors within glycoside hydrolase family 18. FEBS J. 272: 1745–1755. http://dx.doi.org/10.1111/j.1742-4658.2005.04606.xCrossrefGoogle Scholar

  • [15] Feese M.D., Kato Y., Tamada T., Kato M., Komeda T., Miura Y., Hirose M., Hondo K., Kobayashi K. & Kuroki R. 2000. Crystal structure of glycosyltrehalose trehalohydrolase from the hyperthermophilic archaeum Sulfolobus solfataricus. J. Mol. Biol. 301: 451–464. http://dx.doi.org/10.1006/jmbi.2000.3977CrossrefGoogle Scholar

  • [16] Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791. http://dx.doi.org/10.2307/2408678CrossrefGoogle Scholar

  • [17] Gasperik J., Hostinova E. & Sevcik J. 2005 Acarbose binding at the surface of Saccharomycopsis fibuligera glucoamylase suggests the presence of a raw starch binding site. Biologia 60(Suppl. 16): 167–170. Google Scholar

  • [18] Gentry M.S., Dowen R.H. 3rd, Worby C.A., Mattoo S., Ecker J.R. & Dixon J.E. 2007. The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. J. Cell Biol. 178: 477–488. http://dx.doi.org/10.1083/jcb.200704094CrossrefGoogle Scholar

  • [19] Hatada Y., Igarashi K., Ozaki K., Ara K., Hitomi J., Kobayashi T., Kawai S., Watabe T. & Ito S. 1996. Amino acid sequence and molecular structure of an alkaline amylopullulanase from Bacillus that hydrolyzes α-1,4 and α-1,6 linkages in polysaccharides at different active sites. J. Biol. Chem. 271: 24075–24083. http://dx.doi.org/10.1074/jbc.271.39.24075CrossrefGoogle Scholar

  • [20] Hashimoto H. 2006. Recent structural studies of carbohydrate-binding modules. Cell. Mol. Life Sci. 63: 2954–2967. http://dx.doi.org/10.1007/s00018-006-6195-3CrossrefGoogle Scholar

  • [21] Henrissat B. & Bairoch A. 1996. Updating the sequence-based classification of glycosyl hydrolases. Biochem. J. 316: 695–696. Google Scholar

  • [22] Janecek S. 1997. α-Amylase family: molecular biology and evolution. Prog. Biophys. Mol. Biol. 67: 67–97. http://dx.doi.org/10.1016/S0079-6107(97)00015-1CrossrefGoogle Scholar

  • [23] Janecek S. 2002a. How many conserved sequence regions are there in the α-amylase family? Biologia 57(Suppl. 11): 29–41. Google Scholar

  • [24] Janecek S. 2002b. A motif of a microbial starch-binding domain found in human genethonin. Bioinformatics 18: 1534–1537. http://dx.doi.org/10.1093/bioinformatics/18.11.1534CrossrefGoogle Scholar

  • [25] Janecek S. & Sevcik J. 1999. The evolution of starch-binding domain. FEBS Lett. 456: 119–125. http://dx.doi.org/10.1016/S0014-5793(99)00919-9CrossrefGoogle Scholar

  • [26] Janecek S., Svensson B. & MacGregor E.A. 2003. Relation between domain evolution, specificity, and taxonomy of the α-amylase family members containing a C-terminal starch-binding domain. Eur. J. Biochem. 270: 635–645. http://dx.doi.org/10.1046/j.1432-1033.2003.03404.xCrossrefGoogle Scholar

  • [27] Janecek S., Svensson B. & MacGregor E.A. 2007. A remote but significant sequence homology between glycoside hydrolase clan GH-H and family GH31. FEBS Lett. 581: 1261–1268. http://dx.doi.org/10.1016/j.febslet.2007.02.036CrossrefGoogle Scholar

  • [28] Jeanmougin F., Thompson J.D., Gouy M., Higgins D.G. & Gibson T.J. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23: 403–405. http://dx.doi.org/10.1016/S0968-0004(98)01285-7CrossrefGoogle Scholar

  • [29] Katsuya Y., Mezaki Y., Kubota M. & Matsuura Y. 1998. Three-dimensional structure of Pseudomonas isoamylase at 2.2 Å resolution. J. Mol. Biol. 281: 885–897. http://dx.doi.org/10.1006/jmbi.1998.1992CrossrefGoogle Scholar

  • [30] Kerk D., Conley T.R., Rodriguez F.A., Tran H.T., Nimick M., Muench D.G. & Moorhead G.B. 2006. A chloroplast localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydrate-binding domain, which binds the polysaccharide starch. Plant J. 46: 400–413. http://dx.doi.org/10.1111/j.1365-313X.2006.02704.xCrossrefGoogle Scholar

  • [31] Kuriki T. & Imanaka T. 1999. The concept of the α-amylase family: structural similarity and common catalytic mechanism. J. Biosci. Bioeng. 87: 5575–5565. http://dx.doi.org/10.1016/S1389-1723(99)80114-5CrossrefGoogle Scholar

  • [32] Kuriki T., Takata H., Yanase M., Ohdan K., Fujii K., Terada Y., Takaha T., Hondoh H., Matsuura Y. & Imanaka T. 2006. The concept of the α-amylase family: a rational tool for interconverting glucanohydrolases/ glucanotransferases, and their specificities. J. Appl. Glycosci. 53: 155–161. CrossrefGoogle Scholar

  • [33] Lawson C.L., van Montfort R., Strokopytov B., Rozeboom H.J., Kalk K.H., de Vries G.E., Penninga D., Dijkhuizen L. & Dijkstra B.W. 1994. Nucleotide sequence and X-ray structure of cyclodextrin glycosyltransferase from Bacillus circulans strain 251 in a maltose-dependent crystal form. J. Mol. Biol. 236: 590–600. http://dx.doi.org/10.1006/jmbi.1994.1168CrossrefGoogle Scholar

  • [34] Lee S.P., Morikawa M., Takagi M. & Imanaka T. 1994. Cloning of the aapT gene and characterization of its product, α-amylase-pullulanase (AapT), from thermophilic and alkaliphilic Bacillus sp. strain XAL601. Appl. Environ. Microbiol. 60: 3764–3773. Google Scholar

  • [35] Liu Y.N., Lai Y.T., Chou W.I., Chang M.D. & Lyu P.C. 2007. Solution structure of family 21 carbohydrate-binding module from Rhizopus oryzae glucoamylase. Biochem. J. 403: 21–30. http://dx.doi.org/10.1042/BJ20061312CrossrefGoogle Scholar

  • [36] Lo Leggio L., Ernst H.A., Hilden I. & Larsen S. 2002. A structural model for the N-terminal N1 module of E. coli glycogen branching enzyme. Biologia 57(Suppl. 11): 109–118. Google Scholar

  • [37] MacGregor E.A. 2005. An overview of clan GH-H and distantly related families. Biologia 60(Suppl. 16): 5–12. Google Scholar

  • [38] MacGregor E.A., Janecek S. & Svensson B. 2001. Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochim. Biophys. Acta 1546: 1–20. Google Scholar

  • [39] Machovic M. & Janecek S. 2006a. Starch-binding domains in the post-genome era. Cell. Mol. Life Sci. 63: 2710–2724. http://dx.doi.org/10.1007/s00018-006-6246-9CrossrefGoogle Scholar

  • [40] Machovic M. & Janecek S. 2006b. The evolution of putative starch-binding domains. FEBS Lett. 580: 6349–6356. http://dx.doi.org/10.1016/j.febslet.2006.10.041CrossrefGoogle Scholar

  • [41] Machovic M., Svensson B., MacGregor E.A. & Janecek S. 2005. A new clan of CBM families based on bioinformatics of starch-binding domains from families CBM20 and CBM21. FEBS J. 272: 5497–5513. http://dx.doi.org/10.1111/j.1742-4658.2005.04942.xCrossrefGoogle Scholar

  • [42] Marchler-Bauer A., Anderson J.B., Derbyshire M.K., DeWeese-Scott C., Gonzales N.R., Gwadz M., Hao L., He S., Hurwitz D.I., Jackson J.D., Ke Z., Krylov D., Lanczycki C.J., Liebert C.A., Liu C., Lu F., Lu S., Marchler G.H., Mullokandov M., Song J.S., Thanki N., Yamashita R.A., Yin J.J., Zhang D. & Bryant S.H. (2007) CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 35: D237–D240. http://dx.doi.org/10.1093/nar/gkl951CrossrefGoogle Scholar

  • [43] Marques A.R., Coutinho P.M., Videira P., Fialho A.M. & SaCorreia I. 2003. Sphingomonas paucimobilis β-glucosidase Bgl1: a member of a new bacterial subfamily in glycoside hydrolase family 1. Biochem J. 370: 793–804. http://dx.doi.org/10.1042/BJ20021249CrossrefGoogle Scholar

  • [44] Mikami B., Iwamoto H., Malle D., Yoon H.J., Demirkan-Sarikaya E., Mezaki Y. & Katsuya Y. 2006. Crystal structure of pullulanase: evidence for parallel binding of oligosaccharides in the active site. J. Mol. Biol. 359: 690–707. http://dx.doi.org/10.1016/j.jmb.2006.03.058CrossrefGoogle Scholar

  • [45] Mikkelsen R., Suszkiewicz K. & Blennow A. 2006. A novel type carbohydrate-binding module identified in α-glucan, water dikinases is specific for regulated plastidial starch metabolism. Biochemistry 45: 4674–4682. http://dx.doi.org/10.1021/bi051712aCrossrefGoogle Scholar

  • [46] Minassian B.A., Ianzano L., Meloche M., Andermann E., Rouleau G.A., Delgado-Escueta A.V. & Scherer S.W. 2000. Mutation spectrum and predicted function of laforin in Lafora’s progressive myoclonus epilepsy. Neurology 55: 341–346. CrossrefGoogle Scholar

  • [47] Mukai K., Maruta K., Satouchi K., Kubota M., Fukuda S., Kurimoto M. & Tsujisaka Y. 2004. Cyclic tetrasaccharidesynthesizing enzymes from Arthrobacter globiformis A19. Biosci. Biotechnol. Biochem. 68: 2529–2540. http://dx.doi.org/10.1271/bbb.68.2529CrossrefGoogle Scholar

  • [48] Naumoff D.G. 2005. GH97 is a new family of glycoside hydrolases, which is related to the α-galactosidase superfamily. BMC Genomics 6: 112. http://dx.doi.org/10.1186/1471-2164-6-112Google Scholar

  • [49] Niehaus F., Peters A., Groudieva T. & Antranikian G. 2000. Cloning, expression and biochemical characterisation of a unique thermostable pullulan-hydrolysing enzyme from the hyperthermophilic archaeon Thermococcus aggregans. FEMS Microbiol. Lett. 190: 223–229. http://dx.doi.org/10.1111/j.1574-6968.2000.tb09290.xCrossrefGoogle Scholar

  • [50] 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: 2567–2571. http://dx.doi.org/10.1016/j.febslet.2008.06.027CrossrefGoogle Scholar

  • [51] Niittyla T., Comparot-Moss S., Lue W.L., Messerli G., Trevisan M., Seymour M.D., Gatehouse J.A., Villadsen D., Smith S.M., Chen J., Zeeman S.C. & Smith A.M. 2006. Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J. Biol. Chem. 281: 11815–11818. http://dx.doi.org/10.1074/jbc.M600519200CrossrefGoogle Scholar

  • [52] Notredame C., Holme L. & Higgins D.G. 1998. COFFEE: a new objective function for multiple sequence alignmnent. Bioinformatics 14: 407–422. http://dx.doi.org/10.1093/bioinformatics/14.5.407CrossrefGoogle Scholar

  • [53] Oslancova A. & Janecek S. 2002. Oligo-1,6-glucosidase and neopullulanase enzyme subfamilies from the α-amylase family defined by the fifth conserved sequence region. Cell. Mol. Life Sci. 59: 1945–1959. http://dx.doi.org/10.1007/PL00012517CrossrefGoogle Scholar

  • [54] Page R.D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12: 357–358. Google Scholar

  • [55] Polekhina G., Gupta A., van Denderen B.J., Feil S.C., Kemp B.E., Stapleton D. & Parker M.W. 2005. Structural basis for glycogen recognition by AMP-activated protein kinase. Structure 13: 1453–1462. http://dx.doi.org/10.1016/j.str.2005.07.008CrossrefGoogle Scholar

  • [56] Ragunath C., Manuel S.G.A., Kasinathan C. & Ramasubbu N. 2008. Structure-function relationships in human salivary α-amylase: role of aromatic residues in a secondary binding site. Biologia 63: 1028–1034. http://dx.doi.org/10.2478/s11756-008-0163-3CrossrefGoogle Scholar

  • [57] Rahman S., Regina A., Li Z., Mukai Y., Yamamoto M., Kosar-Hashemi B., Abrahams S. & Morell M.K. 2001. Comparison of starch-branching enzyme genes reveals evolutionary relationships among isoforms. Characterization of a gene for starch-branching enzyme IIa from the wheat genome donor Aegilops tauschii. Plant Physiol. 125: 1314–1324. http://dx.doi.org/10.1104/pp.125.3.1314CrossrefGoogle Scholar

  • [58] Ramsay A.G., Scott K.P., Martin J.C., Rincon M.T. & Flint H.J. 2006. Cell-associated α-amylases of butyrate-producing Firmicute bacteria from the human colon. Microbiology 152: 3281–3290. http://dx.doi.org/10.1099/mic.0.29233-0CrossrefGoogle Scholar

  • [59] Rodriguez-Sanoja R., Oviedo N. & Sanchez S. 2005. Microbial starch-binding domain. Curr. Opin. Microbiol. 8: 260–267. http://dx.doi.org/10.1016/j.mib.2005.04.013CrossrefGoogle Scholar

  • [60] Ryan S.M., Fitzgerald G.F. & van Sinderen D. 2006. Screening for and identification of starch-, amylopectin-, and pullulan-degrading activities in bifidobacterial strains. Appl. Environ. Microbiol. 72: 5289–5296. http://dx.doi.org/10.1128/AEM.00257-06CrossrefGoogle Scholar

  • [61] Saitou N. & Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425. Google Scholar

  • [62] 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: 967–979. Google Scholar

  • [63] Shatsky M., Nussinov R. & Wolfson H.J. 2004. A method for simultaneous alignment of multiple protein structures. Proteins 56:143–156. http://dx.doi.org/10.1002/prot.10628CrossrefGoogle Scholar

  • [64] Sorimachi K., Le Gal-Coeffet M.F., Williamson G., Archer D.B. & Williamson M.P. 1997. Solution structure of the granular starch binding domain of Aspergillus niger glucoamylase bound to β-cyclodextrin. Structure 5: 647–661. http://dx.doi.org/10.1016/S0969-2126(97)00220-7CrossrefGoogle Scholar

  • [65] 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: 555–562. http://dx.doi.org/10.1093/protein/gzl044CrossrefGoogle Scholar

  • [66] Svensson B. 1994. Protein engineering in the α-amylase family: catalytic mechanism, substrate specificity, and stability. Plant Mol. Biol. 25: 141–157. http://dx.doi.org/10.1007/BF00023233CrossrefGoogle Scholar

  • [67] Svensson B., Jespersen H., Sierks M.R. & MacGregor E.A. 1989. Sequence homology between putative raw-starch binding domains from different starch-degrading enzymes. Biochem. J. 264: 309–311. Google Scholar

  • [68] Thompson J.D., Higgins D.G. & Gibson T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673–4680. http://dx.doi.org/10.1093/nar/22.22.4673CrossrefGoogle Scholar

  • [69] Tibbot B.K., Wong D.W.S. & Robertson G.H. 2002. Studies on the C-terminal region of barley α-amylase 1 with emphasis on raw starch-binding. Biologia 57(Suppl. 11): 229–238. Google Scholar

  • [70] Tranier S., Deville K., Robert X., Bozonnet S., Haser R., Svensson B. & Aghajari N. 2005. Insights into the “pair of sugar tongs” surface binding site in barley alpha-amylase isozymes and crystallization of appropriate sugar tongs mutants. Biologia 60(Suppl. 16): 37–46. Google Scholar

  • [71] van der Maarel M.J., van der Veen B., Uitdehaag J.C., Leemhuis H. & Dijkhuizen L. 2002. Properties and applications of starch-converting enzymes of the α-amylase family. J. Biotechnol. 94: 137–155. http://dx.doi.org/10.1016/S0168-1656(01)00407-2CrossrefGoogle Scholar

  • [72] Zona R., Chang-Pi-Hin F., O’Donohue M.J. & Janecek S. 2004. Bioinformatics of the family 57 glycoside hydrolases and identification of catalytic residues in amylopullulanase from Thermococcus hydrothermalis. Eur. J. Biochem. 271: 2863–2872. http://dx.doi.org/10.1111/j.1432-1033.2004.04144.xCrossrefGoogle Scholar

About the article

Published Online: 2008-12-04

Published in Print: 2008-12-01

Citation Information: Biologia, Volume 63, Issue 6, Pages 1057–1068, ISSN (Online) 1336-9563, ISSN (Print) 0006-3088, DOI: https://doi.org/10.2478/s11756-008-0162-4.

Export Citation

© 2008 Slovak Academy of Sciences. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

Štefan Janeček, Filip Mareček, E. Ann MacGregor, and Birte Svensson
Biotechnology Advances, 2019, Page 107451
Wenping Zhang, Wenbin Liu, Rong Hou, Liang Zhang, Stephan Schmitz-Esser, Huaibo Sun, Junjin Xie, Yunfei Zhang, Chengdong Wang, Lifeng Li, Bisong Yue, He Huang, Hairui Wang, Fujun Shen, and Zhihe Zhang
The ISME Journal, 2018
Mabel T. Wong, Weijun Wang, Marie Couturier, Fakhria M. Razeq, Vincent Lombard, Pascal Lapebie, Elizabeth A. Edwards, Nicolas Terrapon, Bernard Henrissat, and Emma R. Master
Frontiers in Microbiology, 2017, Volume 8
Tae-Yang Jung, Dan Li, Jong-Tae Park, Se-Mi Yoon, Phuong Lan Tran, Byung-Ha Oh, Štefan Janeček, Sung Goo Park, Eui-Jeon Woo, and Kwan-Hwa Park
Journal of Biological Chemistry, 2012, Volume 287, Number 11, Page 7979
Wanping Chen, Ting Xie, Yanchun Shao, Fusheng Chen, and Michael Freitag
PLoS ONE, 2012, Volume 7, Number 11, Page e49679
Nicolas Hedin, Julieta Barchiesi, Diego F. Gomez-Casati, Alberto A. Iglesias, Miguel A. Ballicora, and María V. Busi
Archives of Biochemistry and Biophysics, 2017, Volume 618, Page 52
Skander Elleuche, Alina Krull, Ute Lorenz, and Garabed Antranikian
The Protein Journal, 2017, Volume 36, Number 1, Page 56
Marie Sofie Møller, Anette Henriksen, and Birte Svensson
Cellular and Molecular Life Sciences, 2016, Volume 73, Number 14, Page 2619
Jonathan Dunne, William Kelly, Sinead Leahy, Dong Li, Judy Bond, Lifeng Peng, Graeme Attwood, and T. Jordan
Proteomes, 2015, Volume 3, Number 4, Page 347
Julieta Barchiesi, Nicolás Hedin, Diego F. Gomez-Casati, Miguel A. Ballicora, and María V. Busi
BMC Research Notes, 2015, Volume 8, Number 1
Hye-Jin Jo, Sunghoon Park, Hee-Gon Jeong, Jung-Wan Kim, and Jong-Tae Park
FEBS Letters, 2015, Volume 589, Number 10, Page 1089
Ryuichiro Suzuki, Keiichi Koide, Mari Hayashi, Tomoko Suzuki, Takayuki Sawada, Takashi Ohdan, Hidekazu Takahashi, Yasunori Nakamura, Naoko Fujita, and Eiji Suzuki
Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 2015, Volume 1854, Number 5, Page 476
Caio C. Carvalho, Ngoc N. Phan, Yingfei Chen, and Peter J. Reilly
Biopolymers, 2015, Volume 103, Number 4, Page 203
Il-Nam Oh, Jay-lin Jane, Kan Wang, Jong-Tae Park, and Kwan-Hwa Park
Extremophiles, 2015, Volume 19, Number 2, Page 363
Marek Gabriško and Štefan Janeček
Journal of Molecular Evolution, 2011, Volume 72, Number 1, Page 104
Fu-Pang Lin, Yi-Hsuan Ho, Hsu-Yang Lin, and Hui-Ju Lin
Extremophiles, 2012, Volume 16, Number 3, Page 395
Catherine Eyre, Wafa Muftah, Jennifer Hiscox, Julie Hunt, Peter Kille, Lynne Boddy, and Hilary J. Rogers
Fungal Biology, 2010, Volume 114, Number 8, Page 646
Camilla Christiansen, Maher Abou Hachem, Štefan Janeček, Anders Viksø-Nielsen, Andreas Blennow, and Birte Svensson
FEBS Journal, 2009, Volume 276, Number 18, Page 5006
Fu-Pang Lin, Hsiu-Yen Ma, Hui-Ju Lin, Shiu-Mei Liu, and Wen-Shyong Tzou
Applied Biochemistry and Biotechnology, 2011, Volume 165, Number 3-4, Page 1047
Štefan Janeček, Birte Svensson, and E. Ann MacGregor
Enzyme and Microbial Technology, 2011, Volume 49, Number 5, Page 429
Malene Bech Vester-Christensen, Maher Abou Hachem, Birte Svensson, and Anette Henriksen
Journal of Molecular Biology, 2010, Volume 403, Number 5, Page 739
Eun-Seong Seo, Camilla Christiansen, Maher Abou Hachem, Morten Nielsen, Kenji Fukuda, Sophie Bozonnet, Andreas Blennow, Nushin Aghajari, Richard Haser, and Birte Svensson
Biologia, 2008, Volume 63, Number 6

Comments (0)

Please log in or register to comment.
Log in