Two structurally related starch-binding domain families CBM25 and CBM26

Biologia

Volumn 69, Issue 9, 2014, Pages 1087-1096

  Majzlová, Katarína ^a   Janeček, Štefan ^a,b  

^a Institute of Molecular Biology Slovak Academy of Sciences   (Slovakia)

^b UNIVERSITY OF SS CYRIL AND METHODIUS   (Slovakia)

Author keywords

alpha amylase; amylolytic enzymes; carbohydrate binding module; evolutionary relatedness; families CBM25 and CBM26; sequence comparison; starch binding domain

Indexed keywords

EID: 84907562690     PISSN: 00063088     EISSN: 13369563     Source Type: Journal    
DOI: 10.2478/s11756-014-0415-3     Document Type: Review

References (62)

1. Abe A., Tonozuka T., Sakano Y. & Kamitori S. 2004. Complex structures of Thermoactinomyces vulgaris R-47 α-amylase 1 with malto-oligosaccharides demonstrate the role of domain N acting as a starch-binding domain. J. Mol. Biol. 335: 811–822.
2. 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.
3. Ashikari T., Nakamura N., Tanaka Y., Kiuchi N., Shibano Y., Tanaka T., Amachi T. & Yoshizumi H. 1986. Rhizopus rawstarch-degrading glucoamylase: its cloning and expression in yeast. Agric. Biol. Chem. 50: 957–964.
4. 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.
5. Boraston A.B., Healey M., Klassen J., Ficko-Blean E., Lammerts van Bueren A. & Law V. 2006. A structural and functional analysis of α-glucan recognition by family 25 and 26 carbohydrate-binding modules reveals a conserved mode of starch recognition. J. Biol. Chem. 281: 587–598.
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.
7. Christiansen C., Abou Hachem M., Janecek S., Viksř-Nielsen A., Blennow A. & Svensson B. 2009. The carbohydrate-binding module family 20 — diversity, structure, and function. FEBS J. 276: 5006–5029.
8. Cockburn D., Wilkens C., Ruzanski C., Andersen S., Nielsen J.W., Smith A.M., Field R.A., Willemoës M., Abou Hachem M. & Svensson B. 2014. Analysis of surface binding sites (SBSs) in carbohydrate active enzymes with focus on glycoside hydrolase families 13 and 77 — a mini-review. Biologia 69: 705–712.
9. Deshpande N., Addess K.J., Bluhm W.F., Merino-Ott J.C., Townsend-Merino W., Zhang Q., Knezevich C., Xie L., Chen L., Feng Z., Green R.K., Flippen-Anderson J.L., Westbrook J., Berman H.M. & Bourne P.E. 2005. Nucleic Acids Res. 33: D233–D237.
10. Gentry M.S., Dixon J.E. & Worby C.A. 2009. Lafora disease: insights into neurodegeneration from plant metabolism. Trends Biochem. Sci. 34: 628–639.
11. Gentry M.S., Romá-Mateo C. & Sanz P. 2013. Laforin, a protein with many faces: glucan phosphatase, adapter protein, et alii. FEBS J. 280: 525–537.
12. Giraud E. & Cuny G. 1997. Molecular characterization of the α-amylase genes of Lactobacillus plantarum A6 and Lactobacillus amylovorus reveals an unusual 3’ end structure with direct tandem repeats and suggests a common evolutionary origin. Gene 198: 149–157.
13. Glaring M.A., Baumann M.J., Abou Hachem M., Nakai H., Nakai N., Santelia D., Sigurskjold B.W., Zeeman S.C., Blennow A. & Svensson B. 2011. Starch-binding domains in the CBM45 family — low-affinity domains from glucan, water dikinase and α-amylase involved in plastidial starch metabolism. FEBS J. 278: 1175–1185.
14. Guillen D., Sanchez S. & Rodriguez-Sanoja R. 2010. Carbohydrate-binding domains: multiplicity of biological roles. Appl. Microbiol. Biotechnol. 85: 1241–1249.
15. Guillen D., Santiago M., Linares L., Perez R., Morlon J., Ruiz B., Sanchez S. & Rodriguez-Sanoja R. 2007. α-Amylase starch binding domains: cooperative effects of binding to starch granules of multiple tandemly arranged domains. Appl. Environ. Microbiol. 73: 3833–3837.
16. Haas B.J., Kamoun S., Zody M.C., Jiang R.H., Handsaker R.E., Cano L.M., Grabherr M., … & Nusbaum C. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393–398.
17. Hudson E.R., Pan D.A., James J., Lucocq J.M., Hawley S.A., Green K.A., Baba O., Terashima T. & Hardie D.G. 2003. A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr. Biol. 13: 861–866.
18. Janecek S. 2002. A motif of a microbial starch-binding domain found in human genethonin. Bioinformatics 18: 1534–1537.
19. Janecek S. & Kuchtova A. 2012. In silico identification of catalytic residues and domain fold of the family GH119 sharing the catalytic machinery with the α-amylase family GH57. FEBS Lett. 586: 3360–3366.
20. Janecek S. & Sevcik J. 1999. The evolution of starch-binding domain. FEBS Lett. 456: 119–125.
21. 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 starchbinding domain. Eur. J. Biochem. 270: 635–645.
22. 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 proteins from microbes, plants and animals. Enzyme Microb. Technol. 49: 429–440.
23. 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: 1149–1170.
24. Jiang S., Heller B., Tagliabracci V.S., Zhai L., Irimia J.M., DePaoli-Roach A.A., Wells C.D., Skurat A.V. & Roach P.J. 2010. Starch binding domain-containing protein 1/genethonin 1 is a novel participant in glycogen metabolism. J. Biol. Chem. 285: 34960–34971.
25. Kelley L.A. & Sternberg M.J. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4: 363–371.
26. 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: 200–215.
27. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J. & Higgins D.G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.
28. Letunic I. & Bork P. 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127–128.
29. Lombard V., Golaconda Ramulu H., Drula E., Coutinho P.M. & Henrissat B. 2014. The Carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42: D490–D495.
30. Machovic M. & Janecek S. 2006a. The evolution of putative starch-binding domains. FEBS Lett. 580: 6349–6356.
31. Machovic M. & Janecek S. 2006b. Starch-binding domains in the post-genome era. Cell. Mol. Life Sci. 63: 2710–2724.
32. Machovic M., Svensson B., MacGregor E.A. & Janecek S. 2005. A new clan of CBM families based on bioinformatics of starchbinding domains from families CBM20 and CBM21. FEBS J. 272: 5497–5513.
33. Matsui Y., Okada S., Uchimura T., Kondo A. & Satoh E. 2007. Determination and analysis of the starch binding domain of Streptococcus bovis 148 raw-starch-hydrolyzing α-amylase. J. Appl. Glycosci. 54: 217–222.
34. 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.
35. 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.
36. Orzechowski S., Grabowska A., Sitnicka D., Siminska J., Felus M., Dudkiewicz M., Fudali S. & Sobczak M. 2013. 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 α-glucan, water dikinases (GWDs) from Solanum tuberosum L. Acta Physiol. Plant. 35: 483–500.
37. Peng H., Zheng Y., Chen M., Wang Y., Xiao Y. & Gao Y. 2014. A starch-binding domain identified in α-amylase (AmyP) represents a new family of carbohydrate-binding modules that contribute to enzymatic hydrolysis of soluble starch. FEBS Lett. 588: 1161–1167.
38. Penninga D., van der Veen B.A., Knegtel R.M., van Hijum S.A., Rozeboom H.J., Kalk K.H., Dijkstra B.W. & Dijkhuizen L. 1996. The raw starch binding domain of cyclodextrin glycosyltransferase from Bacillus circulans strain 251. J. Biol. Chem. 271: 32777–32784.
39. Polekhina G., Gupta A., Michell B.J., van Denderen B., Murthy S., Feil S.C., Jennings I.G., Campbell D.J., Witters L.A., Parker M.W., Kemp B.E. & Stapleton D. 2003. AMPK β subunit targets metabolic stress sensing to glycogen. Curr. Biol. 13: 867–871.
40. Polekhina G., Gupta A., van Denderen B.J., Feil S.C., Kemp B.E., Stapleton D. & Parker M.W. Structural basis for glycogen recognition by AMP-activated protein kinase. Structure 13: 1453–1462.
41. Rodriguez Sanoja R., Morlon-Guyot J., Jore J., Pintado J., Juge N. & Guyot J.P. 2000. Comparative characterization of complete and truncated forms of Lactobacillus amylovorus α-amylase and role of the C-terminal direct repeats in rawstarch binding. Appl. Environ. Microbiol. 66: 3350–3356.
42. Rodriguez-Sanoja R., Oviedo N., Escalante L., Ruiz B. & Sanchez S. 2009. A single residue mutation abolishes attachment of the CBM26 starch-binding domain from Lactobacillus amylovorus α-amylase. J. Ind. Microbiol. Biotechnol. 36: 341–346.
43. Rodriguez-Sanoja R., Oviedo N. & Sanchez S. 2005a. Microbial starch-binding domain. Curr. Opin. Microbiol. 8: 260–267.
44. Rodriguez-Sanoja R., Ruiz B., Guyot J.P. & Sanchez S. 2005b. Starch-binding domain affects catalysis in two Lactobacillus α-amylases. Appl. Environ. Microbiol. 71: 297–302.
45. Ryan S.M., Fitzgerald G.F. & van Sinderen D. 2006. Screening for and identification of starch-, amylopectin-, and pullulandegrading activities in bifidobacterial strains. Appl. Environ. Microbiol. 72: 5289–5296.
46. Saitou N. & Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.
47. Shatsky M., Nussinov R. & Wolfson H.J. 2004. A method for simultaneous alignment of multiple protein structures. Proteins 56: 143–156.
48. Siggens K.W. 1987. Molecular cloning and characterization of the β-amylase gene from Bacillus circulans. Mol. Microbiol. 1: 86–91.
49. Sorimachi K., Le Gal-Coëffet 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.
50. 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: 58–60.
51. Sumitani J., Tottori T., Kawaguchi T. & Arai M. 2000. New type of starch-binding domain: the direct repeat motif in the Cterminal region of Bacillus sp. no. 195 α-amylase contributes to starch binding and raw starch degrading. Biochem. J. 350: 477–484.
52. 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.
53. Tung J.Y., Chang M.D., Chou W.I., Liu Y.Y., Yeh Y.H., Chang F.Y., Lin S.C., Qiu Z.L. & Sun Y.J. 2008. Crystal structures of the starch-binding domain from Rhizopus oryzae glucoamylase reveal a polysaccharide-binding path. Biochem. J. 416: 27–36.
54. UniProt Consortium. 2013. Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 41: D43–D47.
55. van Bueren A.L. & Boraston A.B. 2007. The structural basis of α-glucan recognition by a family 41 carbohydrate-binding module from Thermotoga maritima. J. Mol. Biol. 365: 555–560.
56. Vander Kooi C.W., Taylor A.O., Pace R.M., Meekins D.A., Guo H.F., Kim Y. & Gentry M.S. 2010. Structural basis for the glucan phosphatase activity of Starch Excess4. Proc. Natl. Acad. Sci. USA 107: 15379–15384.
57. Watanabe H., Nishimoto T., Kubota M., Chaen H. & Fukuda S. 2006. Cloning, sequencing, and expression of the genes encoding an isocyclomaltooligosaccharide glucanotransferase and an α-amylase from a Bacillus circulans strain. Biosci. Biotechnol. Biochem. 70: 2690–2702.
58. Wayllace N.Z., Valdez H.A., Ugalde R.A., Busi M.V. & Gomez-Casati D.F. 2010. 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: 428–440.
59. Xu J., Ren F., Huang C.H., Zheng Y., Zhen J., Sun H., Ko T.P., He M., Chen C.C., Chan H.C., Guo R.T., Song H. & Ma Y. 2014. Functional and structural studies of pullulanase from Anoxybacillus sp. LM18-11. Proteins (in press); doi: 10.1002/prot.24498.
60. Yamaguchi R., Arakawa T., Tokunaga H., Ishibashi M. & Tokunaga M. 2012a. Distinct characteristics of single starchbinding domain SBD1 derived from tandem domains SBD1-SBD2 of halophilic Kocuria varians α-amylase. Protein J. 31: 250–258.
61. Yamaguchi R., Inoue Y., Tokunaga H., Ishibashi M., Arakawa T., Sumitani J., Kawaguchi T. & Tokunaga M. 2012b. Halophilic characterization of starch-binding domain from Kocuria varians α-amylase. Int. J. Biol. Macromol. 50: 95–102.
62. Yamaguchi R., Tokunaga H., Ishibashi M., Arakawa T. & Tokunaga M. 2011. Salt-dependent thermo-reversible α-amylase: cloning and characterization of halophilic α-amylase from moderately halophilic bacterium, Kocuria varians. Appl. Microbiol. Biotechnol. 89: 673–684.