Structural insights into the substrate specificity of a 6-phospho-β-glucosidase BglA-2 from Streptococcus pneumoniae TIGR4

Journal of Biological Chemistry

Volumn 288, Issue 21, 2013, Pages 14949-14958

  Yu, Wei Li ^a   Jiang, Yong Liang ^a   Pikis, Andreas ^b,c   Cheng, Wang ^a   Bai, Xiao Hui ^a   Ren, Yan Min ^a   Thompson, John ^b   Zhou, Cong Zhao ^a   Chen, Yuxing ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC RESIDUES; CONVEX SURFACES; GLYCOLYTIC PATHWAYS; GLYCOSIDE HYDROLASE FAMILY 1; STREPTOCOCCUS PNEUMONIAE; STRUCTURAL INSIGHTS; SUBSTRATE SELECTIVITY; SUBSTRATE SPECIFICITY;

GLUCOSE; PHOSPHORYLATION; STRUCTURAL ANALYSIS;

AMINO ACIDS;

ALANINE; BETA GLUCOSIDASE; CELLOBIOSE; LYSINE; METHIONINE; PROTEIN BGLA 2; SERINE; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STRUCTURE; HYDROLYSIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS PNEUMONIAE;

6-PHOSPHO-Β-GLUCOSIDASE; CRYSTAL STRUCTURE; ENZYME CATALYSIS; ENZYME MECHANISMS; PEP-PTS; PNEUMONIA; STREPTOCOCCUS; SUBSTRATE SPECIFICITY; THIOCELLOBIOSE 6-PHOSPHATE;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GLUCOSIDASES; MUTATION, MISSENSE; PROTEIN STRUCTURE, SECONDARY; STREPTOCOCCUS PNEUMONIAE; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84878259065     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.454751     Document Type: Article

References (43)

1. Kadioglu, A., Weiser, J. N., Paton, J. C., and Andrew, P. W. (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 6, 288-301 (Pubitemid 351404773)
2. Cartwright, K. (2002) Pneumococcal disease in western Europe. Burden of disease, antibiotic resistance and management. Eur. J. Pediatr. 161, 188-195
3. Steinfort, C., Wilson, R., and Mitchell, T. (1989) Effects of Streptococcus pneumoniae on human respiratory epithelium in vitro. Infect. Immun. 57, 2006-2013 (Pubitemid 19186876)
4. Bidossi, A., Mulas, L., Decorosi, F., Colomba, L., Ricci, S., Pozzi, G., Deutscher, J., Viti, C., and Oggioni, M. R. (2012) A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PloS One 7, e33320
5. Saier, M. H., Jr. (2000) Families of transmembrane sugar transport proteins. Mol. Microbiol. 35, 699-710
6. Ajdić, D., and Pham, V. T. (2007) Global Transcriptional analysis of Streptococcus mutans sugar transporters using microarrays. J. Bacteriol. 189, 5049-5059 (Pubitemid 47076050)
7. Kundig, W., Ghosh, S., and Roseman, S. (1964) Phosphate bound to histidine in a protein as an intermediate in a novel phosphotransferase system. Proc. Natl. Acad. Sci. U.S.A. 52, 1067-1074
8. Reizer, J., Saier, M. H., Jr., Deutscher, J., Grenier, F., Thompson, J., and Hengstenberg, W. (1988) The phosphoenolpyruvate:sugar phosphotransferase system in gram-positive bacteria. Properties, mechanism, and regulation. Crit. Rev. Microbiol. 15, 297-338
9. Roseman, S. (1989) Sialic acid, serendipity, and sugar transport. Discovery of the bacterial phosphotransferase system. FEMS Microbiol. Rev. 5, 3-11
10. Meadow, N. D., Fox, D. K., and Roseman, S. (1990) The bacterial phosphoenol-pyruvate. Glycose phosphotransferase system. Annu. Rev. Biochem. 59, 497-542
11. Postma, P. W., Lengeler, J. W., and Jacobson, G. R. (1993) Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57, 543-594 (Pubitemid 23262509)
12. Henderson, P. J., Baldwin, S. A., Cairns, M. T., Charalambous, B. M., Dent, H. C., Gunn, F., Liang, W. J., Lucas, V. A., Martin, G. E., and McDonald, T. P. (1992) Sugar-cation symport systems in bacteria. Int. Rev. Cytol. 137, 149-208
13. Poolman, B., Knol, J., van der Does, C., Henderson, P. J., Liang, W. J., Leblanc, G., Pourcher, T., and Mus-Veteau, I. (1996) Cation and sugar selectivity determinants in a novel family of transport proteins. Mol. Microbiol. 19, 911-922 (Pubitemid 26084424)
14. Davidson, A. L. (2002) Mechanism of coupling of transport to hydrolysis in bacterial ATP-binding cassette transporters. J. Bacteriol. 184, 1225-1233
15. Davidson, A. L., and Chen, J. (2004) ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 73, 241-268 (Pubitemid 39050369)
16. Patzlaff, J. S., van der Heide, T., and Poolman, B. (2003) The ATP/substrate stoichiometry of the ATP-binding cassette (ABC) transporter OpuA. J. Biol. Chem. 278, 29546-29551 (Pubitemid 36962336)
17. Thompson, J., Pikis, A., Ruvinov, S. B., Henrissat, B., Yamamoto, H., and Sekiguchi, J. (1998) The gene glvA of Bacillus subtilis 168 encodes a metal-requiring, NAD(H)-dependent 6-phospho-α-glucosidase. Assignment to family 4 of the glycosylhydrolase superfamily. J. Biol. Chem. 273, 27347-27356 (Pubitemid 28500451)
18. Cote, C. K., Cvitkovitch, D., Bleiweis, A. S., Honeyman, A. L. (2000) A novel β-glucoside-specific PTS locus from Streptococcus mutans that is not inhibited by glucose. Microbiology 146, 1555-1563 (Pubitemid 30458710)
19. Tettelin, H., Nelson, K. E., Paulsen, I. T., Eisen, J. A., Read, T. D., Peterson, S., Heidelberg, J., DeBoy, R. T., Haft, D. H., Dodson, R. J., Durkin, A. S., Gwinn, M., Kolonay, J. F., Nelson, W. C., Peterson, J. D., Umayam, L. A., White, O., Salzberg, S. L., Lewis, M. R., Radune, D., Holtzapple, E., Khouri, H., Wolf, A. M., Utterback, T. R., Hansen, C. L., McDonald, L. A., Feldblyum, T. V., Angiuoli, S., Dickinson, T., Hickey, E. K., Holt, I. E., Loftus, B. J., Yang, F., Smith, H. O., Venter, J. C., Dougherty, B. A., Morrison, D. A., Hollingshead, S. K., and Fraser, C. M. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293, 498-506 (Pubitemid 32679078)
20. Henrissat, B. (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280, 309-316
21. Koshland, D. E. (1953) Stereochemistry and the mechanism of enzymic reactions. Biol. Rev. Camb. Philos. Soc. 28, 416-436
22. Henrissat, B., Callebaut, I., Fabrega, S., Lehn, P., Mornon, J. P., and Davies, G. (1995) Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. Proc. Natl. Acad. Sci. U.S.A. 92, 7090-7094
23. Wiesmann, C., Beste, G., Hengstenberg, W., and Schulz, G. E. (1995) The three-dimensional structure of 6-phospho-β-galactosidase from Lactococcus lactis. Structure 3, 961-968
24. Wiesmann, C., Hengstenberg, W., and Schulz, G. E. (1997) Crystal structures and mechanism of 6-phospho-β-galactosidase from Lactococcus lactis. J. Mol. Biol. 269, 851-860 (Pubitemid 27280851)
25. Sanz-Aparicio, J., Hermoso, J. A., Martínez-Ripoli, M., Lequerica, J. L., and Polaina, J. (1998) Crystal structure of β-glucosidase A from Bacillus polymyxa. Insights into the catalytic activity in family 1 glycosyl hydrolases. J. Mol. Biol. 275, 491-502 (Pubitemid 28055068)
26. Tribolo, S., Berrin, J. G., Kroon, P. A., Czjzek, M., and Juge, N. (2007) The crystal structure of human cytosolic β-glucosidase unravels the substrate aglycone specificity of a family 1 glycoside hydrolase. J. Mol. Biol. 370, 964-975 (Pubitemid 46899071)
27. Leslie, A. G. (1999) Integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr. 55, 1696-1702
28. Collaborative Computational Project, Number 4 (1994) The CCP4 suite. Programs for protein crystallography. Acta Crystallogr.DBiol. Crystallogr. 50, 760-763
29. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
30. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
31. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity. All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
32. Laskowski, R. A., Macarthur, M. W., Moss, D. S., and Thornton, J. M. (1993) Procheck. A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
33. DeLano, W. (2010) The PyMol Molecular Graphics System, version 1.3r1, Schrodinger LLC, New York
34. Thompson, J., Robrish, S. A., Bouma, C. L., Freedberg, D. I., and Folk, J. E. (1997) Phospho-β-glucosidase from Fusobacterium mortiferum. Purification, cloning, and inactivation by 6-phosphoglucono-δ-lactone. J. Bacteriol. 179, 1636-1645
35. Prag, G., Papanikolau, Y., Tavlas, G., Vorgias, C. E., Petratos, K., and Oppenheim, A. B. (2000) Structures of chitobiase mutants complexed with the substrate Di-N-acetyl-D-glucosamine. The catalytic role of the conserved acidic pair, aspartate 539 and glutamate 540. J. Mol. Biol. 300, 611-617
36. Yang, X., Zhao, Y., Wang, Q., Wang, H., and Mei, Q. (2005) Analysis of the monosaccharide components in Angelica polysaccharides by high performance liquid chromatography. Anal. Sci. 21, 1177-1180 (Pubitemid 41563428)
37. Honda, S., Akao, E., Suzuki, S., Okuda, M., Kakehi, K., and Nakamura, J. (1989) High-performance liquid-chromatography of reducing carbohydrates as strongly ultraviolet-absorbing and electrochemically sensitive 1-phenyl-3-methyl-5-pyrazolone derivatives. Anal. Biochem. 180, 351-357 (Pubitemid 19198072)
38. Jiang, Y. L., Yu, W. L., Zhang, J. W., Frolet, C., Di Guilmi, A. M., Zhou, C. Z., Vernet, T., and Chen, Y. (2011) Structural basis for the substrate specificity of a novel β-N-acetylhexosaminidase StrH protein from Streptococcus pneumoniae R6. J. Biol. Chem. 286, 43004-43012
39. Thompson, J., Lichtenthaler, F. W., Peters, S., and Pikis, A. (2002) β-Glucoside kinase (BglK) from Klebsiella pneumoniae. Purification, properties, and preparative synthesis of 6-phospho-β-D-glucosides. J. Biol. Chem. 277, 34310-34321
40. Yip, V. L., Varrot, A., Davies, G. J., Rajan, S. S., Yang, X., Thompson, J., Anderson, W. F., and Withers, S. G. (2004) An unusual mechanism of glycoside hydrolysis involving redox and elimination steps by a Family 4 β-glycosidase from Thermotoga maritima. J. Am. Chem. Soc. 126, 8354-8355 (Pubitemid 38917940)
41. Yip, V. L. Y., and Withers, S. G. (2006) Family 4 glycosidases carry out efficient hydrolysis of thioglycosides by an α,β-elimination mechanism. Angew. Chem. Int. Ed. 45, 1-5
42. Puri, V., Goyal, A., Sankaranarayanan, R., Enright, A. J., and Vaidya, T. (2011) Evolutionary and functional insights into Leishmania META1. Evidence for lateral gene transfer and a role for META1 in secretion. BMC Evol. Biol. 11, 334
43. McKessar, S. J, Hakenbeck, R. (2007) The two-component regulatory system TCS08 is involved in cellobiose metabolism of Streptococcus pneumoniae R6. J. Bacteriol. 189, 1342-1350 (Pubitemid 46239755)