Improving the glycosyltransferase activity of Agrobacterium tumefaciens glycogen synthase by fusion of N-terminal starch binding domains (SBDs)

Biochimie

Volumn 95, Issue 10, 2013, Pages 1865-1870

  Martín, Mariana ^a   Wayllace, Nahuel Z ^a   Valdez, Hugo A ^b   Gomez Casati, Diego F ^a   Busi, María V ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

Author keywords

CBM; Glycogen synthase; Starch binding domains; Starch synthase

Indexed keywords

GLYCOGEN SYNTHASE; GLYCOSYLTRANSFERASE; POLYSACCHARIDE; STARCH;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; BACTERIAL CELL; BINDING AFFINITY; CATALYSIS; ENZYME ACTIVITY; ESCHERICHIA COLI; GLYCOGEN SYNTHESIS; N TERMINAL STARCH BINDING DOMAIN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RHIZOBIUM RADIOBACTER; STRUCTURE ANALYSIS;

AGROBACTERIUM TUMEFACIENS; ARABIDOPSIS THALIANA; ESCHERICHIA COLI;

CBM; GLYCOGEN SYNTHASE; STARCH BINDING DOMAINS; STARCH SYNTHASE;

AGROBACTERIUM TUMEFACIENS; ARABIDOPSIS; BACTERIAL PROTEINS; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC COMPLEMENTATION TEST; GLYCOGEN; GLYCOGEN SYNTHASE; KINETICS; METABOLIC ENGINEERING; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS;

EID: 84883222952     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2013.06.009     Document Type: Article

References (52)

1. S.G. Ball, and M.K. Morell From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule Annu. Rev. Plant Biol. 54 2003 207 233
2. J. Preiss, K. Ball, B. Smith-White, A. Iglesias, G. Kakefuda, and L. Li Starch biosynthesis and its regulation Biochem. Soc. Trans. 19 1991 539 547
3. A.M. Smith, K. Denyer, and C. Martin The synthesis of the starch granule Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 1997 67 87
4. S.C. Zeeman, J. Kossmann, and A.M. Smith Starch: its metabolism, evolution, and biotechnological modification in plants Annu. Rev. Plant Biol. 61 2010 209 234
5. J. Preiss Biosynthesis of bacterial and mammalian glycogen and plant starch synthesis and their regulation S.M. Hecht, Bioinorganic Chemistry: Carbohydrates 1999 Oxford University Press Oxford 489 554
6. B.L. Cantarel, P.M. Coutinho, C. Rancurel, T. Bernard, V. Lombard, and B. Henrissat The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Nucleic Acids Res. 37 2009 D233 D238
7. J.A. Campbell, G.J. Davies, V. Bulone, and B. Henrissat A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities Biochem. J. 326 Pt 3 1997 929 939
8. P.M. Coutinho, E. Deleury, G.J. Davies, and B. Henrissat An evolving hierarchical family classification for glycosyltransferases J. Mol. Biol. 328 2003 307 317
9. Z. Li, G. Mouille, B. Kosar-Hashemi, S. Rahman, B. Clarke, K.R. Gale, R. Appels, and M.K. Morell The structure and expression of the wheat starch synthase III gene. Motifs in the expressed gene define the lineage of the starch synthase III gene family Plant Physiol. 123 2000 613 624
10. H.A. Valdez, M.V. Busi, N.Z. Wayllace, G. Parisi, R.A. Ugalde, and D.F. Gomez-Casati Role of the N-terminal starch-binding domains in the kinetic properties of starch synthase III from Arabidopsis thaliana Biochemistry 47 2008 3026 3032
11. D.F. Gomez Casati, M. Martin, and M.V. Busi Polysaccharide-synthesizing glycosyltransferases and carbohydrate binding modules: the case of starch synthase III Prot. Pept. Lett. 20 2013 856 863
12. T. Senoura, A. Asao, Y. Takashima, N. Isono, S. Hamada, H. Ito, and H. Matsui Enzymatic characterization of starch synthase III from kidney bean (Phaseolus vulgaris L.) FEBS J. 274 2007 4550 4560
13. W. Dian, H. Jiang, and P. Wu Evolution and expression analysis of starch synthase III and IV in rice J. Exp. Bot. 56 2005 623 632
14. G.J. Abel, F. Springer, L. Willmitzer, and J. Kossmann Cloning and functional analysis of a cDNA encoding a novel 139 kDa starch synthase from potato (Solanum tuberosum L.) Plant J. 10 1996 981 991
15. O. Shoseyov, Z. Shani, and I. Levy Carbohydrate binding modules: biochemical properties and novel applications Microbiol. Mol. Biol. Rev. 70 2006 283 295
16. R. Rodriguez-Sanoja, N. Oviedo, and S. Sanchez Microbial starch-binding domain Curr. Opin. Microbiol. 8 2005 260 267
17. M. Machovic, and S. Janecek Starch-binding domains in the post-genome era Cell Mol. Life Sci. 63 2006 2710 2724
18. C. Christiansen, M. Abou Hachem, S. Janecek, A. Vikso-Nielsen, A. Blennow, and B. Svensson The carbohydrate-binding module family 20 - diversity, structure, and function FEBS J. 276 2009 5006 5029
19. S. Janecek, B. Svensson, and E.A. MacGregor Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals Enzym. Microb. Technol. 49 2011 429 440
20. N.Z. Wayllace, H.A. Valdez, R.A. Ugalde, M.V. Busi, and D.F. Gomez-Casati The starch-binding capacity of the noncatalytic SBD2 region and the interaction between the N- and C-terminal domains are involved in the modulation of the activity of starch synthase III from Arabidopsis thaliana FEBS J. 277 2010 428 440
21. A. Buschiazzo, J.E. Ugalde, M.E. Guerin, W. Shepard, R.A. Ugalde, and P.M. Alzari Crystal structure of glycogen synthase: homologous enzymes catalyze glycogen synthesis and degradation EMBO J. 23 2004 3196 3205
22. M.V. Busi, N. Palopoli, H.A. Valdez, M.S. Fornasari, N.Z. Wayllace, D.F. Gomez-Casati, G. Parisi, and R.A. Ugalde Functional and structural characterization of the catalytic domain of the starch synthase III from Arabidopsis thaliana Proteins: Struct. Funct. Bioinform. 70 2008 31 40
23. G. Eydallin, A.M. Viale, M.T. Moran-Zorzano, F.J. Munoz, M. Montero, E. Baroja-Fernandez, and J. Pozueta-Romero Genome-wide screening of genes affecting glycogen metabolism in Escherichia coli K-12 FEBS Lett. 581 2007 2947 2953
24. H.A. Valdez, D.A. Peralta, N.Z. Wayllace, M.J. Grisolía, D.F. Gomez-Casati, and M.V. Busi Preferential binding of SBD from Arabidopsis thaliana SSIII to polysaccharides. Study of amino acid residues involved Starch/Stärke 63 2011 451 460
25. N.Z. Wayllace, H.A. Valdez, A. Meras, R.A. Ugalde, M.V. Busi, and D.F. Gomez-Casati An enzyme-coupled continuous spectrophotometric assay for glycogen synthases Mol. Biol. Rep. 39 2012 585 591
26. S.P. Brooks A simple computer program with statistical tests for the analysis of enzyme kinetics BioTechniques 13 1992 906 911
27. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
28. J. Sambrook, and A. Russell Molecular Cloning: A Laboratory Manual 2001 Cold Spring Harbor Laboratory Press 2344
29. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
30. D.M. Bollag, M.D. Rozycki, and S.J. Edelstein Protein Methods 1996 Wiley-Liss New York 415 xvi
31. B. Guerra, K. Niefind, I. Ermakowa, and I. Olaf-Georg Characterization of CK2 holoenzyme variants regard to crystallization K.A. Ahmed, J.E. Allende, O.G. Issinger, Protein Kinase CK2. from Structure to Regulation 2001 Kluwer Academic Publishers Massachusetts, USA 188
32. L. Latorre-Garcia, A.C. Adam, P. Manzanares, and J. Polaina Improving the amylolytic activity of Saccharomyces cerevisiae glucoamylase by the addition of a starch binding domain J. Biotechnol. 118 2005 167 176
33. N. Juge, J. Nohr, M.F. Le Gal-Coeffet, B. Kramhoft, C.S. Furniss, V. Planchot, D.B. Archer, G. Williamson, and B. Svensson The activity of barley alpha-amylase on starch granules is enhanced by fusion of a starch binding domain from Aspergillus niger glucoamylase Biochim. Biophys. Acta 1764 2006 275 284
34. K. Ohdan, T. Kuriki, H. Takata, H. Kaneko, and S. Okada Introduction of raw starch-binding domains into Bacillus subtilis alpha-amylase by fusion with the starch-binding domain of Bacillus cyclomaltodextrin glucanotransferase Appl. Environ. Microbiol. 66 2000 3058 3064
35. Y.W. Hua, M.C. Chi, H.F. Lo, W.H. Hsu, and L.L. Lin Fusion of Bacillus stearothermophilus leucine aminopeptidase II with the raw-starch-binding domain of Bacillus sp. strain TS-23 alpha-amylase generates a chimeric enzyme with enhanced thermostability and catalytic activity J. Ind. Microbiol. Biotechnol. 31 2004 273 277
36. H.B. Huang, M.C. Chi, W.H. Hsu, W.C. Liang, and L.L. Lin Construction and one-step purification of Bacillus kaustophilus leucine aminopeptidase fused to the starch-binding domain of Bacillus sp. strain TS-23 alpha-amylase Bioprocess Biosyst. Eng. 27 2005 389 398
37. A.A. Telke, S.S. Ghatge, S.H. Kang, S. Thangapandian, K.W. Lee, H.D. Shin, Y. Um, and S.W. Kim Construction and characterization of chimeric cellulases with enhanced catalytic activity towards insoluble cellulosic substrates Bioresour. Technol. 112 2012 10 17
38. G. Mamo, R. Hatti-Kaul, and B. Mattiasson Fusion of carbohydrate binding modules from Thermotoga neapolitana with a family 10 xylanase from Bacillus halodurans S7 Extremophiles 11 2007 169 177
39. F.S. Kittur, S.L. Mangala, A.A. Rus'd, M. Kitaoka, H. Tsujibo, and K. Hayashi Fusion of family 2b carbohydrate-binding module increases the catalytic activity of a xylanase from Thermotoga maritima to soluble xylan FEBS Lett. 549 2003 147 151
40. R. Mikkelsen, K. Suszkiewicz, and A. Blennow A novel type carbohydrate-binding module identified in alpha-glucan, water dikinases is specific for regulated plastidial starch metabolism Biochemistry 45 2006 4674 4682
41. S. Orzechowski, A. Grabowska, D. Sitnicka, J. Siminska, M. Felus, M. Dudkiewicz, S. Fudali, and M. Sobczak Analysis of the expression, subcellular and tissue localisation of phosphoglucan, water dikinase (PWD/GWD3) in Solanum tuberosum L.: a bioinformatics approach for the comparative analysis of two a -glucan, water dikinases (GWDs) from Solanum tuberosum L Acta Physiol. Plant 35 2013 483 500
42. A. Blennow, and B. Svensson Dynamic os starch granule biogenesis - the role of redox-regulated enzymes and low-affinity carbohydrate-binding modules Biocatal. Biotransf. 28 2010 3 9
43. M.A. Glaring, M.J. Baumann, M. Abou Hachem, H. Nakai, N. Nakai, D. Santelia, B.W. Sigurskjold, S.C. Zeeman, A. Blennow, and B. Svensson Starch-binding domains in the CBM45 family - low-affinity domains from glucan, water dikinase and alpha-amylase involved in plastidial starch metabolism FEBS J. 278 2011 1175 1185
44. S. Geremia, M. Campagnolo, R. Schinzel, and L.N. Johnson Enzymatic catalysis in crystals of Escherichia coli maltodextrin phosphorylase J. Mol. Biol. 322 2002 413 423
45. D. Barford, and L.N. Johnson The molecular mechanism for the tetrameric association of glycogen phosphorylase promoted by protein phosphorylation Protein Sci. 1 1992 472 493
46. M. O'reilly, K.A. Watson, R. Schinzel, D. Palm, and L.N. Johnson Oligosaccharide substrate binding to E. coli maltodextrin phosphorylase Nat. Struct. Biol. 4 1997 405 412
47. K.A. Watson, C. McCleverty, S. Geremia, S. Cottaz, H. Driguez, and L.N. Johnson Phosphorylase recognition and phosphorolysis of its oligosaccharide substrate: answers to a long outstanding question EMBO J. 18 1999 4619 4632
48. D.F. Gomez-Casati, M.A. Aon, and A.A. Iglesias Kinetic and structural analysis of the ultrasensitive behaviour of cyanobacterial ADP-glucose pyrophosphorylase Biochem. J. 350 Pt 1 2000 139 147
49. D.F. Gomez-Casati, M.A. Aon, and A.A. Iglesias Ultrasensitive glycogen synthesis in Cyanobacteria FEBS Lett. 446 1999 117 121
50. D.F. Gomez-Casati, M.A. Aon, and A.A. Iglesias Molecular crowding and cytoskeletal proteins affect the allosteric regulatory properties of ADP-glucose pyrophosphorylase G.E. Garab, Photosynthesis: Mechanisms and Effects 1998 Luwer Academic Publishers Dordrecht 3695 3698
51. S. Baskaran, V.M. Chikwana, C.J. Contreras, K.D. Davis, W.A. Wilson, A.A. DePaoli-Roach, P.J. Roach, and T.D. Hurley Multiple glycogen-binding sites in eukaryotic glycogen synthase are required for high catalytic efficiency toward glycogen J. Biol. Chem. 286 2011 33999 34006
52. A. Diaz, C. Martinez-Pons, I. Fita, J.C. Ferrer, and J.J. Guinovart Processivity and subcellular localization of glycogen synthase depend on a non-catalytic high affinity glycogen-binding site J. Biol. Chem. 286 2011 18505 18514