Probing the role of a mobile loop in substrate binding and enzyme activity of human salivary amylase

Journal of Molecular Biology

Volumn 325, Issue 5, 2003, Pages 1061-1076

  Ramasubbu, Narayanan ^a   Ragunath, Chandran ^a   Mishra, Prasunkumar J ^a  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

Complex; Crystal structure; Mobile loop; Salivary amylase; Starch hydrolysis

Indexed keywords

ACARBOSE; AMYLASE; LIGAND; MALTOPENTAOSE; MALTOSE; OLIGOSACCHARIDE; STARCH; UNCLASSIFIED DRUG; WATER;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME SUBSTRATE; GLYCOSYLATION; HYDROGEN BOND; HYDROLYSIS; HYDROPHOBICITY; MOLECULE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN INTERACTION; STEREOCHEMISTRY;

MAMMALIA;

EID: 0037474545     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01326-8     Document Type: Article

References (53)

1. Gumucio D.L., Wiebauer K., Caldwell R.M., Samuelson L.C., Meisler M.H. Concerted evolution of human amylase genes. Mol. Cell. Biol. 8:1988;1197-1205.
2. Brayer G.D., Luo Y., Withers S.G. The structure of human pancreatic alpha-amylase at 1.8 Å resolution and comparisons with related enzymes. Protein Sci. 4:1995;1730-1742.
3. Ramasubbu N., Paloth V., Luo Y., Brayer G.D., Levine M.J. Structure of human salivary α-amylase at 1.6 Å resolution, Implications for its role in the oral cavity. Acta Crystallog. sect. D. 52:1996;435-446.
4. Douglas C.W. Characterization of the alpha-amylase receptor of Streptococcus gordonii NCTC 7868. J. Dent. Res. 69:1990;1746-1752.
5. Nagamine Y., Omichi K., Ikenaka T. A comparison of the modes of actions of human salivary and pancreatic alpha-amylases on modified maltooligosaccharides. J. Biochem. (Tokyo). 104:1988;667-670.
6. Nagamine Y., Omichi K., Ikenaka T. Investigation of the active site of human salivary alpha-amylase from the modes of action on modified maltooligosaccharides. J. Biochem. (Tokyo). 104:1988;409-415.
7. Scannapieco F.A., Bhandary K., Ramasubbu N., Levine M.J. Structural relationship between the enzymatic and streptococcal binding sites of human salivary alpha-amylase. Biochem. Biophys. Res. Commun. 173:1990;1109-1115.
8. Scannapieco F.A., Haraszthy G.G., Cho M.I., Levine M.J. Characterization of an amylase-binding component of Streptococcus gordonii G9B. Infect. Immun. 60:1992;4726-4733.
9. Scannapieco F.A., Torres G., Levine M.J. Salivary alpha-amylase: role in dental plaque and caries formation. Crit. Rev. Oral. Biol. Med. 4:1993;301-307.
10. Scannapieco F.A., Torres G.I., Levine M.J. Salivary amylase promotes adhesion of oral streptococci to hydroxyapatite. J. Dent. Res. 74:1995;1360-1366.
11. Pujadas G., Palau J. Evolution of alpha-amylases: architectural features and key residues in the stabilization of the (beta/alpha)(8) scaffold. Mol. Biol. Evol. 18:2001;38-54.
12. Bank R.A., Hettema E.H., Arwert F., Amerongen A.V., Pronk J.C. Electrophoretic characterization of posttranslational modifications of human parotid salivary alpha-amylase. Electrophoresis. 12:1991;74-79.
13. Nishide T., Emi M., Nakamura Y., Matsubara K. Corrected sequences of cDNAs for human salivary and pancreatic alpha-amylases. Gene. 28:1984;263-270.
14. Nishide T., Nakamura Y., Emi M., Yamamoto T., Ogawa M., Mori T., Matsubara K. Primary structure of human salivary alpha-amylase gene. Gene. 41:1986;299-304.
15. Qian M., Haser R., Payan F. Structure and molecular model refinement of pig pancreatic alpha-amylase at 2.1 Å resolution. J. Mol. Biol. 231:1993;785-799.
16. Qian M., Haser R., Buisson G., Duee E., Payan F. The active center of a mammalian alpha-amylase. Structure of the complex of a pancreatic alpha-amylase with a carbohydrate inhibitor refined to 2.2-Å resolution. Biochemistry. 33:1994;6284-6294.
17. Qian M., Haser R., Payan F. Carbohydrate binding sites in a pancreatic alpha-amylase-substrate complex, derived from X-ray structure analysis at 2.1 Å resolution. Protein Sci. 4:1995;747-755.
18. Brayer G.D., Sidhu G., Maurus R., Rydberg E.H., Braun C., Wang Y., et al. Subsite mapping of the human pancreatic alpha-amylase active site through structural, kinetic, and mutagenesis techniques. Biochemistry. 39:2000;4778-4791.
19. Rydberg E.H., Li C., Maurus R., Overall C.M., Brayer G.D., Withers S.G. Mechanistic analyses of catalysis in human pancreatic alpha-amylase: detailed kinetic and structural studies of mutants of three conserved carboxylic acids. Biochemistry. 41:2002;4492-4502.
20. Numao S., Maurus R., Sidhu G., Wang Y., Overall C.M., Brayer G.D., Withers S.G. Probing the role of the chloride ion in the mechanism of human pancreatic alpha-amylase. Biochemistry. 41:2002;215-225.
21. Steer M.L., Levitzki A. The metal specificity of mammalian-amylase as revealed by enzyme activity and structural probes. FEBS Letters. 31:1973;89-92.
22. Levitzki A., Steer M.L. The allosteric activation of mammalian alpha-amylase by chloride. Eur. J. Biochem. 41:1974;171-180.
23. Aghajari N., Feller G., Gerday C., Haser R. Structural basis of alpha-amylase activation by chloride. Protein Sci. 11:2002;1435-1441.
24. Rydberg E.H., Sidhu G., Vo H.C., Hewitt J., Cote H.C., Wang Y., et al. Cloning, mutagenesis, and structural analysis of human pancreatic alpha-amylase expressed in Pichia pastoris. Protein Sci. 8:1999;635-643.
25. Ragunath C., Sundar K., Ramasubbu N. Expression, characterization, and biochemical properties of recombinant human salivary amylase. Protein Expr. Purif. 24:2002;202-211.
26. Tseng C.C., Miyamoto M., Ramalingam K., Hemavathy K.C., Levine M.J., Ramasubbu N. The roles of histidine residues at the starch-binding site in streptococcal-binding activities of human salivary amylase. Arch. Oral. Biol. 44:1999;119-127.
27. Scannapieco F.A., Bergey E.J., Reddy M.S., Levine M.J. Characterization of salivary alpha-amylase binding to Streptococcus sanguis. Infect. Immun. 57:1989;2853-2863.
28. Mishra P.J., Ragunath C., Ramasubbu N. The mechanism of salivary amylase hydrolysis: role of residues at subsite S2′ Biochem. Biophys. Res. Commun. 292:2002;468-473.
29. Kandra L., Gyemant G. Examination of the active sites of human salivary alpha-amylase (HSA). Carbohydr. Res. 329:2000;579-585.
30. Omichi K., Hase S., Ikenaka T. Examination of aglycone-binding site of human salivary alpha-amylase by means of transglycosylation reactions. J. Biochem. (Tokyo). 109:1991;410-415.
31. Ramasubbu N., Bhandary K.K., Scannapieco F.A., Levine M.J. Crystallization and preliminary X-ray diffraction studies of human salivary alpha-amylase. Proteins: Struct. Funct. Genet. 11:1991;230-232.
32. Nahoum V., Roux G., Anton V., Rouge P., Puigserver A., Bischoff H., et al. Crystal structures of human pancreatic alpha-amylase in complex with carbohydrate and proteinaceous inhibitors. Biochem. J. 346:2000;201-208.
33. Qian M., Nahoum V., Bonicel J., Bischoff H., Henrissat B., Payan F. Enzyme-catalyzed condensation reaction in a mammalian alpha-amylase. High-resolution structural analysis of an enzyme-inhibitor complex. Biochemistry. 40:2001;7700-7709.
34. Gilles C., Astier J.P., Marchis-Mouren G., Cambillau C., Payan F. Crystal structure of pig pancreatic alpha-amylase isoenzyme II, in complex with the carbohydrate inhibitor acarbose. Eur. J. Biochem. 238:1996;561-569.
35. Brzozowski A.M., Davies G.J. Structure of the Aspergillus oryzae alpha-amylase complexed with the inhibitor acarbose at 2.0 Å resolution. Biochemistry. 36:1997;10837-10845.
36. Aghajari N., Roth M., Haser R. Crystallographic evidence of a transglycosylation reaction: ternary complexes of a psychrophilic alpha-amylase. Biochemistry. 41:2002;4273-4280.
37. Brzozowski A.M., Lawson D.M., Turkenburg J.P., Bisgaard-Frantzen H., Svendsen A., et al. Structural analysis of a chimeric bacterial alpha-amylase. High-resolution analysis of native and ligand complexes. Biochemistry. 39:2000;9099-9107.
38. Matsuura Y., Kusunoki M., Harada W., Kakudo M. Structure and possible catalytic residues of Taka-amylase A. J. Biochem. (Tokyo). 95:1984;697-702.
39. Al Kazaz M., Desseaux V., Marchis-Mouren G., Prodanov E., Santimone M. The mechanism of porcine pancreatic alpha-amylase. Inhibition of maltopentaose hydrolysis by acarbose, maltose and maltotriose. Eur. J. Biochem. 252:1998;100-107.
40. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
41. Goff D.J., Kull F.J. The inhibition of human salivary alpha-amylase by type II alpha-amylase inhibitor from Triticum aestivum is competitive, slow and tight-binding. J. Enzyme. Inhib. 9:1995;163-170.
42. Otwinowski Z., Minor W. Processing of X-ray crystallographic data in oscillation mode. Carter C.W., Sweet R.M. Methods Enzymol. vol. 276:1997;307-326 Academic Press, New York.
43. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163.
44. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D Biol. Crystallog. 54:1998;905-921.
45. Jones T.A. Diffraction methods for biological macromolecules. Interactive computer graphics: FRODO. Methods Enzymol. 115:1985;157-171.
46. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
47. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
48. Lamzin V.S., Wilson K.S. Automated refinement of protein models. Acta Crystallog. sect. D. 49:1993;129-149.
49. 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. 26:1993;283-291.
50. Evans S.V. SETOR: hardware-lighted three-dimensional solid model representations of macromolecules. J. Mol. Graph. 11:1993;134-138.
51. Laskowski R.A. SURFNET: a program for visualizing molecular surfaces, cavities, and intermolecular interactions. J. Mol. Graph. 13:1995;323-330.
52. McDonald I.K., Thornton J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238:1994;777-793.
53. Wallace A.C., Laskowski R.A., Thornton J.M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8:1995;127-134.