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

Journal of Molecular Biology

Volumn 335, Issue 3, 2004, Pages 811-822

  Abe, Akemi ^a   Tonozuka, Takashi ^a   Sakano, Yoshiyuki ^a   Kamitori, Shigehiro ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

Author keywords

Acarbose; CD, cyclodextrin; Enzymatic glucoside hydrolysis; Starch binding domain; TVAI, Thermoactinomyces vulgaris R 47 amylase 1; TVAII, Thermoactinomyces vulgaris R 47 amylase 2; X ray structure; amylase

Indexed keywords

AMYLASE; CATALASE; ENZYME INHIBITOR; MALTOSE; OLIGOSACCHARIDE; STARCH;

ARTICLE; CHEMICAL REACTION; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME BINDING; GEOMETRY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; THERMOACTINOMYCES VULGARIS; X RAY DIFFRACTION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MICROMONOSPORACEAE; MUTATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

THERMOACTINOMYCES VULGARIS;

ALPHA-AMYLASE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; MALTOSE; MICROMONOSPORACEAE; MODELS, MOLECULAR; MUTATION; OLIGOSACCHARIDES; PROTEIN STRUCTURE, TERTIARY; STARCH;

EID: 1542495429     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.10.078     Document Type: Article

References (42)

1. Yamamoto T., Shinke R. The Amylase Research Society of Japan. Enzyme Chemistry and Molecular Biology of Amylases and Related Enzymes. 1995;3-5 CRC Press, Boca Raton.
2. Tonozuka T., Mogi S., Shimura Y., Ibuka A., Sakai H., Matsuzawa H., et al. Comparison of primary structures and substrate specificities of two pullulan-hydrolyzing α-amylases, TVAI and TVAII, from Thermoactinomyces vulgaris R-47. Biochim. Biophys. Acta. 1252:1995;35-42.
3. 2-α-isomaltosylisomaltose using Thermoactinomyces vulgaris R-47 α-amylase II (TVAII). Carbohydr. Res. 261:1994;157-162.
4. Tonozuka T., Ohtsuka M., Mogi S., Sakai H., Ohta T., Sakano Y. A neoplullulanase-type α-amylase gene from Thermoactinomyces vulgaris R-47. Biosci. Biotechnol. Biochem. 57:1993;395-401.
5. Park K.-H., Kim T.-J., Cheong T.-K., Kim J.-W., Oh B.-H., Svensson B. Structure, specificity and function of cyclomaltodextrinase, a multispecific enzyme of the α-amylase family. Biochim. Biophys. Acta. 1478:2000;165-185.
6. Kamitori S., Abe A., Ohtaki A., Kaji A., Tonozuka T., Sakano Y. Crystal structures and structural comparison of Thermoactinomyces vulgaris R-47 α-amylase 1 (TVAI) at 1.6 Å resolution and α-amylase 2 (TVAII) at 2.3 Å resolution. J. Mol. Biol. 318:2002;443-453.
7. Kamitori S., Kondo S., Okuyama K., Yokota T., Shimura Y., Tonozuka T., Sakano Y. Crystal structure of Thermoactinomyces vulgaris R-47 α-amylase II (TVAII) hydrolyzing cyclodextrins and pullulan at 2.6 Å resolution. J. Mol. Biol. 287:1999;907-921.
8. Kondo S., Ohtaki A., Tonozuka T., Sakano Y., Kamitori S. Studies on the hydrolyzing mechanism for cyclodextrins of Thermoactinomyces vulgaris R-47 α-amylase 2 (TVAII). X-ray structure of mutant E354A complexed with β-cyclodextrin, and kinetic analyses on cyclodextrins. J. Biochem. 129:2001;423-428.
9. Ohtaki A., Kondo S., Shimura Y., Tonozuka T., Sakano Y., Kamitori S. Role of Phe286 in the recognition mechanism of cyclomaltooligosaccharides (cyclodextrins) by Thermoactinomyces vulgaris R-47 α-amylase 2 (TVAII). X-ray structures of the mutant TVAIIs, F286A and F286Y, and kinetic analyses of the Phe286-replaced mutant TVAIIs. Carbohydr. Res. 334:2001;309-313.
10. Lee H.-S., Kim M.-S., Cho H.-S., Kim J.-I., Kim T.-J., Choi J.-H., et al. Cyclomaltodextrinase, neopullulanase, and maltogenic amylase are nearly indistinguishable from each other. J. Biol. Chem. 277:2002;21891-21897.
11. Hondoh H., Kuriki T., Matsuura Y. Three-dimensional structure and substrate binding of Bacillus stearothermophilus neopullulanase. J. Mol. Biol. 326:2003;177-188.
12. Fritzsche H.B., Schwede T., Schulz G.E. Covalent and three-dimensional structure of the cyclodextrinase from Flavobacterium sp. no. 92. Eur. J. Biochem. 270:2003;2332-2341.
13. Luzzati P.V. Traitement statistique des erreurs dans la determination des structures cristallines. Acta Crystallog. 5:1952;802-810.
14. McRee D.E. XtalView/Xfit: a versatile program for manipulating atomic coordinate and electron density. J. Struct. Biol. 125:1999;156-165.
15. Merritt E.A., Bacon D.J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277:1997;505-524.
16. Ramachandran G.N., Sasisekharan V. Conformation of polypeptides and proteins. Advan. Protein Chem. 23:1968;283-437.
17. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1992;283-291.
18. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
19. Sorimachi K., Le Gal-Coeffet M.-F., Williamson G., Archer D.B., Williamson M.P. Solution structure of the granular starch binding domain of Aspergillus niger glucoamylase bound to β-cyclodextrin. Structure. 5:1997;647-661.
20. Kadziola A., Sogaard M., Svensson B., Haser R. Molecular structure of a barley α-amylase-inhibitor complex: implications for starch binding and catalysis. J. Mol. Biol. 278:1998;205-217.
21. Qian M., Haser R., Payan F. Carbohydrate binding sites in a pancreatic α-amylase-substrate complex, derived from X-ray structure analysis at 2.1 Å resolution. Protein Sci. 4:1995;747-755.
22. Janecek S., Svensson B., MacGregor E.A. Relation between domain evolution, specificity, and taxonomy of the α-amylase family members containing a C-terminal starch-binding domain. Eur. J. Biochem. 270:2003;635-645.
23. Ramasubbu N., Ragunath C., Mishra P.J. Probing the role of a mobile loop in substrate binding and enzyme activity of human salivary amylase. J. Mol. Biol. 325:2003;1061-1076.
24. Strokopytov B., Penninga D., Rozeboom H.J., Kalk K.H., Dijkhuizen L., Dijkstra B.W. X-ray structure of cyclodextrin glycosyltransferase complexed with acarbose. Implications for the catalytic mechanism of glycosidases. Biochemistry. 34:1995;2234-2240.
25. Machius M., Vertesy L., Huber R., Wiegand G. Carbohydrate and protein-based inhibitors of porcine pancreatic α-amylase: structure analysis and comparison of their binding characteristics. J. Mol. Biol. 260:1996;409-421.
26. Brzozowski A.M., Davies G.J. Structure of the Aspergillus oryzae α-amylase complexed with the inhibitor acarbose at 2.0 Å resolution. Biochemistry. 36:1997;10837-10845.
27. Qian M., Nahoum V., Bonicel J., Bischoff H., Henrissat B., Payan F. Enzyme-catalyzed condensation reaction in a mammalian α-amylase. high-resolution structural analysis of an enzyme-inhibitor complex. Biochemistry. 40:2001;7700-7709.
28. Nimz O., GeXler K., UsXn I., Laettig S., Welfle H., Sheldrick G.M., Saenger W. X-ray structure of the cyclomaltohexaicosaose triode inclusion complex provides a model for amylose-iodine at atomic resolution. Carbohydr. Res. 338:2003;977-986.
29. Sinnot M.L. Catalytic mechanisms of enzymic glycosyl transfer. Chem. Rev. 90:1990;1171-1202.
30. McCarter J.D., Withers S.G. Mechanisms of enzymatic glycoside hydrolysis. Curr. Opin. Struct. Biol. 4:1994;885-892.
31. Uitdehaag J.C.M., Mosi R., Kalk K.H., van der Veen B.A., Dijkhuizen L., Withers S.G., Dijkstra B.W. X-ray structures along the reaction pathway of cyclodextrin glycosyltransferase elucidate catalysis in the α-amylase family. Nature Struct. Biol. 6:1999;432-436.
32. Swift H.J., Brady L., Derewanda Z.S., Dodson E.J., Dodson G.G., Turkenburg J.P., Wilkinson A.J. Structure and molecular model refinement of Aspergillus oryzae (TAKA) a-amylase: an application of the simulated-annealing method. Acta Crystallog. sect. B. 47:1991;535-544.
33. Ohtaki A., Iguchi A., Mizuno M., Tonozuka T., Sakano Y., Kamitori S. Mutual conversion of substrate specificities of Thermoactinomyces vulgaris R-47 α-amylases TVAI and TVAII by site-directed mutagenesis. Carbohydr. Res. 338:2003;1553-1558.
34. Imberty A., Chanzy H., Perez S., Buleon A., Tran V. The double-helical nature of the crystalline part of A-starch. J. Mol. Biol. 201:1988;365-378.
35. Radosta S., Haberer M., Vorwerg W. Molecular characteristics of amylose and starch in dimethyl sulfoxide. Biomacromolecules. 2:2001;970-978.
36. Kondo S., Kaji A., Yuguchi K., Tonozuka T., Sakano Y., Kamitori S. Crystallization and preliminary X-ray analysis of Thermoactinomyces vulgaris R-47 α-amylase 1. Protein Pept. Letters. 7:2000;197-200.
37. Leslie A.G.W. Moras D., Podjarny A.D., Thierry J.C. Crystallographic Computing V. 1991;27-38 Oxford University Press, Oxford.
38. Collaborative Computational Project, number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
39. Berman H.M., Westbook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., et al. Protein Data Bank. Nucl. Acids Res. 28:2000;235-242.
40. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
41. McRee D.E. XtalView. McRee D.E. Practical Protein Crystallography. 1993;Academic Press, New York.
42. Brünger A.T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 355:1992;472-475.