Probing the Role of Aromatic Residues at the Secondary Saccharide-Binding Sites of Human Salivary α-Amylase in Substrate Hydrolysis and Bacterial Binding

Journal of Molecular Biology

Volumn 384, Issue 5, 2008, Pages 1232-1248

  Ragunath, Chandran ^a   Manuel, Suba G A ^a   Venkataraman, Venkat ^a   Sait, Hameetha B R ^a   Kasinathan, Chinnasamy ^a   Ramasubbu, Narayanan ^a  

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

Author keywords

only five keywords allowed. >; amylase, site directed mutagenesis, enzyme mechanism, hydrolysis, bacterial binding

Indexed keywords

ACARBOSE; ALANINE; AMYLASE; AROMATIC AMINO ACID; OLIGOSACCHARIDE; STARCH;

ANIMAL CELL; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STRUCTURE; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; RESIDUE ANALYSIS; STREPTOCOCCUS GORDONII; SURFACE PLASMON RESONANCE;

BACTERIA (MICROORGANISMS);

EID: 56949098309     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.09.089     Document Type: Article

References (66)

1. MacGregor E.A., Janecek S., and Svensson B. Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes. Biochim. Biophys. Acta 1546 (2001) 1-20
2. Scannapieco F.A., Torres G.I., and Levine M.J. Salivary amylase promotes adhesion of oral streptococci to hydroxyapatite. J. Dent. Res. 74 (1995) 1360-1366
3. Ramasubbu N., Paloth V., Luo Y., Brayer G.D., and Levine M.J. Structure of human salivary alpha-amylase at 1.6 A resolution: implications for its role in the oral cavity. Acta Crystallogr. Sect. D 52 (1996) 435-446
4. Brayer G.D., Luo Y., and Withers S.G. The structure of human pancreatic alpha-amylase at 1.8 A resolution and comparisons with related enzymes. Protein Sci. 4 (1995) 1730-1742
5. Scannapieco F.A., Solomon L., and Wadenya R.O. Emergence in human dental plaque and host distribution of amylase-binding streptococci. J. Dent. Res. 73 (1994) 1627-1635
6. Handley P., Coykendall A., Beighton D., Hardie J.M., and Whiley R.A. Streptococcus crista sp. nov., a viridans Streptococcus with tufted fibrils, isolated from the human oral cavity and throat. Int. J. Syst. Bacteriol. 41 (1991) 543-547
7. Tseng C.C., Scannapieco F.A., and Levine M.J. Use of a replica-plate assay for the rapid assessment of salivary protein-bacteria interactions. Oral Microbiol. Immunol. 7 (1992) 53-56
8. Douglas C.W. The binding of human salivary alpha-amylase by oral strains of streptococcal bacteria. Arch. Oral Biol. 28 (1983) 567-573
9. Scannapieco F.A., Bergey E.J., Reddy M.S., and Levine M.J. Characterization of salivary alpha-amylase binding to Streptococcus sanguis. Infect. Immun. 57 (1989) 2853-2863
10. Scannapieco F.A., Torres G., and Levine M.J. Salivary alpha-amylase: role in dental plaque and caries formation. Crit. Rev. Oral Biol. Med. 4 (1993) 301-307
11. Brown A.E., Rogers J.D., Haase E.M., Zelasko P.M., and Scannapieco F.A. Prevalence of the amylase-binding protein A gene (abpA) in oral streptococci. J. Clin. Microbiol. 37 (1999) 4081-4085
12. Scannapieco F.A. Saliva-bacterium interactions in oral microbial ecology. Crit. Rev. Oral Biol. Med. 5 (1994) 203-248
13. Scannapieco F.A., Haraszthy G.G., Cho M.I., and Levine M.J. Characterization of an amylase-binding component of Streptococcus gordonii G9B. Infect. Immun. 60 (1992) 4726-4733
14. Douglas C.W. Characterization of the alpha-amylase receptor of Streptococcus gordonii NCTC 7868. J. Dent. Res. 69 (1990) 1746-1752
15. Gwynn J.P., and Douglas C.W. Comparison of amylase-binding proteins in oral streptococci. FEMS Microbiol. Lett. 124 (1994) 373-379
16. Rogers J.D., Haase E.M., Brown A.E., Douglas C.W., Gwynn J.P., and Scannapieco F.A. Identification and analysis of a gene (abpA) encoding a major amylase-binding protein in Streptococcus gordonii. Microbiology 144 Pt 5 (1998) 1223-1233
17. Rogers J.D., Palmer Jr. R.J., Kolenbrander P.E., and Scannapieco F.A. Role of Streptococcus gordonii amylase-binding protein A in adhesion to hydroxyapatite, starch metabolism, and biofilm formation. Infect. Immun. 69 (2001) 7046-7056
18. Loo C.Y., Corliss D.A., and Ganeshkumar N. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J. Bacteriol. 182 (2000) 1374-1382
19. Scannapieco F.A., Bhandary K., Ramasubbu N., and 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
20. Tseng C.C., Miyamoto M., Ramalingam K., Hemavathy K.C., Levine M.J., and 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
21. Ramasubbu N., Ragunath C., and 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
22. Nagy T., Simpson P., Williamson M.P., Hazlewood G.P., Gilbert H.J., and Orosz L. All three surface tryptophans in Type IIa cellulose binding domains play a pivotal role in binding both soluble and insoluble ligands. FEBS Lett. 429 (1998) 312-316
23. Ramasubbu N., Ragunath C., Mishra P.J., Thomas L.M., Gyemant G., and Kandra L. Human salivary alpha-amylase Trp58 situated at subsite-2 is critical for enzyme activity. Eur. J. Biochem. 271 (2004) 2517-2529
24. Ragunath C., Manuel S.G., Kasinathan C., and Ramasubbu N. Structure-function relationships in human salivary alpha-amylase: role of aromatic residues in a secondary binding site. Biologia 63 (2008) 1028-1034
25. Vuilleumier S., Sancho J., Loewenthal R., and Fersht A.R. Circular dichroism studies of barnase and its mutants: characterization of the contribution of aromatic side chains. Biochemistry 32 (1993) 10303-10313
26. Kuwajima K., Garvey E.P., Finn B.E., Matthews C.R., and Sugai S. Transient intermediates in the folding of dihydrofolate reductase as detected by far-ultraviolet circular dichroism spectroscopy. Biochemistry 30 (1991) 7693-7703
27. Sreerama N., and Woody R.W. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287 (2000) 252-260
28. Davies G.J., Wilson K.S., and Henrissat B. Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321 Pt 2 (1997) 557-559
29. Qian M., Haser R., Buisson G., Duee E., and 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-A resolution. Biochemistry 33 (1994) 6284-6294
30. Qian M., Spinelli S., Driguez H., and Payan F. Structure of a pancreatic alpha-amylase bound to a substrate analogue at 2.03 A resolution. Protein Sci. 6 (1997) 2285-2296
31. Brzozowski A.M., and Davies G.J. Structure of the Aspergillus oryzae alpha-amylase complexed with the inhibitor acarbose at 2.0 A resolution. Biochemistry 36 (1997) 10837-10845
32. 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
33. Qian M., Nahoum V., Bonicel J., Bischoff H., Henrissat B., and 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. Aghajari N., Roth M., and Haser R. Crystallographic evidence of a transglycosylation reaction: ternary complexes of a psychrophilic alpha-amylase. Biochemistry 41 (2002) 4273-4280
35. Remenyik J., Ragunath C., Ramasubbu N., Gyemant G., Liptak A., and Kandra L. Introducing transglycosylation activity into human salivary alpha-amylase (HSA). Org. Lett. 5 (2003) 4895-4898
36. Qian M., Haser R., and Payan F. Carbohydrate binding sites in a pancreatic alpha-amylase-substrate complex, derived from X-ray structure analysis at 2.1 A resolution. Protein Sci. 4 (1995) 747-755
37. Iefuji H., Chino M., Kato M., and Iimura Y. Raw-starch-digesting and thermostable alpha-amylase from the yeast Cryptococcus sp. S-2: purification, characterization, cloning and sequencing. Biochem. J. 318 Pt 3 (1996) 989-996
38. Raj P.A., Johnsson M., Levine M.J., and Nancollas G.H. Salivary statherin. Dependence on sequence, charge, hydrogen bonding potency, and helical conformation for adsorption to hydroxyapatite and inhibition of mineralization. J. Biol. Chem. 267 (1992) 5968-5976
39. Johnsson M., Levine M.J., and Nancollas G.H. Hydroxyapatite binding domains in salivary proteins. Crit. Rev. Oral Biol. Med. 4 (1993) 371-378
40. Ramasubbu N., Thomas L.M., Bhandary K.K., and Levine M.J. Structural characteristics of human salivary statherin: a model for boundary lubrication at the enamel surface. Crit. Rev. Oral Biol. Med. 4 (1993) 363-370
41. Gilles C., Astier J.P., Marchis-Mouren G., Cambillau C., and 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
42. DeLano W.L. The PyMOL User's Manual (2002), Delano Scientific, San Carlos, CA
43. Sumitani J., Tottori T., Kawaguchi T., and Arai M. New type of starch-binding domain: the direct repeat motif in the C-terminal region of Bacillus sp. no. 195 alpha-amylase contributes to starch binding and raw starch degrading. Biochem. J. 350 Pt 2 (2000) 477-484
44. Tibbot B.K., Wong D.W., and Robertson G.H. A functional raw starch-binding domain of barley alpha-amylase expressed in Escherichia coli. J. Protein Chem. 19 (2000) 663-669
45. Sogaard M., Kadziola A., Haser R., and Svensson B. Site-directed mutagenesis of histidine 93, aspartic acid 180, glutamic acid 205, histidine 290, and aspartic acid 291 at the active site and tryptophan 279 at the raw starch binding site in barley alpha-amylase 1. J. Biol. Chem. 268 (1993) 22480-22484
46. Robert X., Haser R., Mori H., Svensson B., and Aghajari N. Oligosaccharide binding to barley alpha-amylase 1. J. Biol. Chem. 280 (2005) 32968-32978
47. Boraston A.B., Bolam D.N., Gilbert H.J., and Davies G.J. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382 (2004) 769-781
48. Machovic M., and Janecek S. The evolution of putative starch-binding domains. FEBS Lett. 580 (2006) 6349-6356
49. Machovic M., and Janecek S. Starch-binding domains in the post-genome era. Cell. Mol. Life Sci. 63 (2006) 2710-2724
50. Machovic M., Svensson B., MacGregor E.A., and Janecek S. A new clan of CBM families based on bioinformatics of starch-binding domains from families CBM20 and CBM21. FEBS J. 272 (2005) 5497-5513
51. Robert X., Haser R., Gottschalk T.E., Ratajczak F., Driguez H., Svensson B., and Aghajari N. The structure of barley alpha-amylase isozyme 1 reveals a novel role of domain C in substrate recognition and binding: a pair of sugar tongs. Structure 11 (2003) 973-984
52. Bozonnet S., Jensen M.T., Nielsen M.M., Aghajari N., Jensen M.H., Kramhoft B., et al. The 'pair of sugar tongs' site on the non-catalytic domain C of barley alpha-amylase participates in substrate binding and activity. FEBS J. 274 (2007) 5055-5067
53. Mishra P.J., Ragunath C., and Ramasubbu N. The mechanism of salivary amylase hydrolysis: role of residues at subsite S2′. Biochem. Biophys. Res. Commun. 292 (2002) 468-473
54. Ragunath C., Sundar K., and Ramasubbu N. Expression, characterization, and biochemical properties of recombinant human salivary amylase. Protein Expression Purif. 24 (2002) 202-211
55. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
56. Ramasubbu N., Thomas L.M., Ragunath C., and Kaplan J.B. Structural analysis of dispersin B, a biofilm-releasing glycoside hydrolase from the periodontopathogen Actinobacillus actinomycetemcomitans. J. Mol. Biol. 349 (2005) 475-486
57. Dubendorff J.W., and Studier F.W. Creation of a T7 autogene. Cloning and expression of the gene for bacteriophage T7 RNA polymerase under control of its cognate promoter. J. Mol. Biol. 219 (1991) 61-68
58. Sambrook J., Fritsch E., and Maniatis T. Molecular Cloning. A Laboratory Manual. 2nd ed (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor
59. Bernfeld P. Amylase, a and b. Methods Enzymol. 1 (1955) 49-150
60. Greenwood F.C., Hunter W.M., and Glover J.S. The preparation of I-131-labelled human growth hormone of high specific radioactivity. Biochem. J. 89 (1963) 114-123
61. Ramasubbu N., Bhandary K.K., Scannapieco F.A., and Levine M.J. Crystallization and preliminary X-ray diffraction studies of human salivary alpha-amylase. Proteins 11 (1991) 230-232
62. Otwinowski Z., and Minor W. Processing of X-ray crystallographic data in oscillation mode. Methods Enzymol. 276 (1997) 307-326
63. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D 50 (1994) 760-763
64. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D 60 (2004) 2126-2132
65. Lamzin V.S., and Wilson K.S. Automated refinement of protein models. Acta Crystallogr. Sect. D 49 (1993) 129-149
66. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291