Structural insights into the substrate specificity of Streptococcus pneumoniae β(1,3)-galactosidase BgaC

Journal of Biological Chemistry

Volumn 287, Issue 27, 2012, Pages 22910-22918

  Cheng, Wang ^a   Wang, Lei ^a   Jiang, Yong Liang ^a   Bai, Xiao Hui ^a   Chu, Jun ^a   Li, Qiong ^a   Yu, Ge ^a   Liang, Qiu Ling ^a   Zhou, Cong Zhao ^a   Chen, Yuxing ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ACTIVITY ASSAYS; AROMATIC RESIDUES; CATALYTIC DOMAINS; COMPLEX STRUCTURE; CONFORMATIONAL CHANGE; GALACTOSIDASES; HOMODIMERS; HOST MOLECULES; HYDROLYSIS ACTIVITY; KEY RESIDUES; N-ACETYLGLUCOSAMINE; SIDE WALLS; SITE DIRECTED MUTAGENESIS; STREPTOCOCCUS PNEUMONIAE; STRUCTURAL INSIGHTS; SUBSTRATE SPECIFICITY; VIRULENCE FACTORS;

BIOCHEMISTRY;

BIOLOGY;

AROMATIC COMPOUND; BACTERIAL ENZYME; BETA GALACTOSIDASE; BETA(1,3) LINKED GALACTOSE; GALACTOSE; HOMODIMER; N ACETYLGLUCOSAMINE; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ALL BETA DOMAIN; ARTICLE; CATALYSIS; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBUNIT; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; SIMULATION; SITE DIRECTED MUTAGENESIS; STREPTOCOCCUS PNEUMONIAE; TIM BARREL;

ACETYLGLUCOSAMINE; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY; DIMERIZATION; GALACTOSE; MUTAGENESIS; PROTEIN STRUCTURE, TERTIARY; STREPTOCOCCUS PNEUMONIAE; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; VIRULENCE; VIRULENCE FACTORS;

STREPTOCOCCUS PNEUMONIAE;

EID: 84863300900     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.367128     Document Type: Article

References (46)

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. Andersson, B., Gray, B., and Eden, C. S. (1988) Role of attachment for the virulence of Streptococcus pneumoniae. Acta Otolaryngol. Suppl. 454, 163-166 (Pubitemid 19017721)
3. Cámara, M., Boulnois, G. J., Andrew, P. W., and Mitchell, T. J. (1994) A neuraminidase from Streptococcus pneumoniae has the features of a surface protein. Infect. Immun. 62, 3688-3695 (Pubitemid 24264308)
4. Zähner, D., and Hakenbeck, R. (2000) The Streptococcus pneumoniae β-galactosidase is a surface protein. J. Bacteriol. 182, 5919-5921
5. Hava, D. L., and Camilli, A. (2002) Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol. Microbiol. 45, 1389-1406
6. 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)
7. King, S. J., Hippe, K. R., and Weiser, J. N. (2006) Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol. Microbiol. 59, 961-974
8. Tong, H. H., McIver, M. A., Fisher, L. M., and DeMaria, T. F. (1999) Effect of lacto-N-neotetraose, asialoganglioside-GM1, and neuraminidase on adherence of otitis media-associated serotypes of Streptococcus pneumoniae to chinchilla tracheal epithelium. Microb. Pathog. 26, 111-119 (Pubitemid 29106283)
9. Burnaugh, A. M., Frantz, L. J., and King, S. J. (2008) Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J. Bacteriol 190, 221-230
10. Terra, V. S., Homer, K. A., Rao, S. G., Andrew, P. W., and Yesilkaya, H. (2010) Characterization of novel β-galactosidase activity that contributes to glycoprotein degradation and virulence in Streptococcus pneumoniae. Infect. Immun. 78, 348-357
11. Jeong, J. K., Kwon, O., Lee, Y. M., Oh, D. B., Lee, J. M., Kim, S., Kim, E. H., Le, T. N., Rhee, D. K., and Kang, H. A. (2009) Characterization of the Streptococcus pneumoniae BgaC protein as a novel surface β-galactosidase with specific hydrolysis activity for the Galß1-3GlcNAc moiety of oligosaccharides. J. Bacteriol. 191, 3011-3023
12. Henrissat, B., and Davies, G. (1997) Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7, 637-644 (Pubitemid 27472582)
13. Dickson, R. C., Dickson, L. R., and Markin, J. S. (1979) Purification and properties of an inducible β-galactosidase isolated from the yeast Kluyveromyces lactis. J. Bacteriol 137, 51-61 (Pubitemid 9093917)
14. Kestwal, R. M., and Bhide, S. V. (2007) Purification of β-galactosidase from Erythrina indica. Involvement of tryptophan in active site. Biochim. Biophys. Acta 1770, 1506-1512 (Pubitemid 47384995)
15. Shaikh, S. A., Khire, J. M., and Khan, M. I. (1999) Characterization of a thermostable extracellular beta-galactosidase from a thermophilic fungus Rhizomucor sp. Biochim. Biophys. Acta 1472, 314-322 (Pubitemid 29486542)
16. Wang, Z. H., Zeng, B., Shibuya, H., Johnson, G. S., Alroy, J., Pastores, G. M., Raghavan, S., and Kolodny, E. H. (2000) Isolation and characterization of the normal canine β-galactosidase gene and its mutation in a dog model of GM1-gangliosidosis. J. inherit. Metab. Dis. 23, 593-606
17. Davies, G., and Henrissat, B. (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3, 853-859
18. Henrissat, B. (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280, 309-316
19. Henrissat, B., and Bairoch, A. (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 293, 781-788 (Pubitemid 23244564)
20. Henrissat, B., and Bairoch, A. (1996) Updating the sequence-based classification of glycosyl hydrolases. Biochem. J. 316, 695-696 (Pubitemid 26182174)
21. Jenkins, J., Lo Leggio, L., Harris, G., and Pickersgill, R. (1995) β-glucosidase, β-galactosidase, family A cellulases, family F xylanases, and two barley glycanases form a superfamily of enzymes with 8-fold β/α architecture and with two conserved glutamates near the carboxyl-terminal ends of β-strands four and seven. FEBS Lett. 362, 281-285
22. Jacobson, R. H., Zhang, X. J., DuBose, R. F., and Matthews, B. W. (1994 Three-dimensional structure of β-galactosidase from E. coli. Nature 369, 761-766
23. Skálová, T., Dohnálek, J., Spiwok, V., Lipovová, P., Vondrácková, E., Petroková, H., Dusková, J., Strnad, H., Králová, B., and Hasek, J. (2005) Cold-active β-galactosidase from Arthrobacter sp. C2-2 forms compact 660-kDa hexamers. Crystal structure at 1.9 Å resolution. J. Mol. Biol. 353, 282-294
24. Pereira-Rodríguez, A., Fernández-Leiro, R., González-Siso, M. I., Cerdán, M. E., Becerra, M., and Sanz-Aparicio, J. (2012) Structural basis of specificity in tetrameric Kluyveromyces lactis β-galactosidase. J. Struct. Biol. 177, 392-401
25. Hidaka, M., Fushinobu, S., Ohtsu, N., Motoshima, H., Matsuzawa, H., Shoun, H., and Wakagi, T. (2002) Trimeric crystal structure of the glycoside hydrolase family 42 β-galactosidase from Thermus thermophilus A4 and the structure of its complex with galactose. J. Mol. Biol. 322, 79-91 (Pubitemid 36132672)
26. Maksimainen, M., Paavilainen, S., Hakulinen, N., and Rouvinen, J. (2012) Structural analysis, enzymatic characterization, and catalytic mechanisms of β-galactosidase from Bacillus circulans sp. alkalophilus. FEBS J. 279, 1788-1798
27. Aguilar, C. F., Sanderson, I., Moracci, M., Ciaramella, M., Nucci, R., Rossi, M., and Pearl, L. H. (1997) Crystal structure of the β-glycosidase from the hyperthermophilic archeon Sulfolobus solfataricus. Resilience as a key factor in thermostability. J. Mol. Biol. 271, 789-802 (Pubitemid 27376054)
28. Rojas, A. L., Nagem, R. A., Neustroev, K. N., Arand, M., Adamska, M., Eneyskaya, E. V., Kulminskaya, A. A., Garratt, R. C., Golubev, A. M., and Polikarpov, I. (2004) Crystal structures of β-galactosidase from Penicillium sp. and its complex with galactose. J. Mol. Biol. 343, 1281-1292 (Pubitemid 39387827)
29. Maksimainen, M., Hakulinen, N., Kallio, J. M., Timoharju, T., Turunen, O., and Rouvinen, J. (2011) Crystal structures of Trichoderma reesei β-galactosidase reveal conformational changes in the active site. J. Struct. Biol. 174, 156-163
30. Ohto, U., Usui, K., Ochi, T., Yuki, K., Satow, Y., and Shimizu, T. (2012) Crystal structure of human β-galactosidase. The structural basis of GM1 gangliosidosis and Morquio B diseases. J. Biol. Chem. 287, 1801-1812
31. Asp, N. G., and Dahlqvist, A. (1972) Human small intestine β-galactosidases. specific assay of three different enzymes. Anal. Biochem. 47, 527-538
32. Alpers, D. H. (1969) Separation and isolation of rat and human intestinal β-galactosidases. J. Biol. Chem. 244, 1238-1246
33. Distler, J. J., and Jourdian, G. W. (1973) The purification and properties of β-galactosidase from bovine testes. J. Biol. Chem. 248, 6772-6780
34. Juers, D. H., Huber, R. E., and Matthews, B. W. (1999) Structural comparisons of TIM barrel proteins suggest functional and evolutionary relationships between β-galactosidase and other glycohydrolases. Protein Sci. 8, 122-136 (Pubitemid 29035526)
35. Juers, D. H., Jacobson, R. H., Wigley, D., Zhang, X. J., Huber, R. E., Tronrud, D. E., and Matthews, B. W. (2000) High resolution refinement of β-galactosidase in a new crystal form reveals multiple metal-binding sites and provides a structural basis for α-complementation. Protein Sci. 9, 1685-1699
36. Miller, J. H. (1972) Experiments in Molecular Genetics, pp. 398-404, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
37. 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)
38. 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)
39. DeLano, W. L. (2002) The PyMol Molecular Graphics System, Version 0.99rc2, DeLano Scientific, Palo Alto, CA
40. Stirk, H. J., Woolfson, D. N., Hutchinson, E. G., and Thornton, J. M. (1992) Depicting topology and handedness in jellyroll structures. FEBS Lett. 308, 1-3
41. Nucci, R., Moracci, M., Vaccaro, C., Vespa, N., and Rossi, M. (1993) Exoglucosidase activity and substrate specificity of the β-glycosidase isolated from the extreme thermophile Sulfolobus solfataricus. Biotechnol. Appl. Biochem. 17, 239-250
42. Davies, G. J., Wilson, K. S., and Henrissat, B. (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem. J. 321, 557-559 (Pubitemid 27056509)
43. Huber, R. E., Hakda, S., Cheng, C., Cupples, C. G., and Edwards, R. A. (2003) Trp-999 of β-galactosidase (Escherichia coli) is a key residue for binding, catalysis, and synthesis of allolactose, the natural lac operon inducer. Biochemistry 42, 1796-1803 (Pubitemid 36205989)
44. Ahn, Y. O., Zheng, M., Bevan, D. R., Esen, A., Shiu, S. H., Benson, J., Peng, H. P., Miller, J. T., Cheng, C. L., Poulton, J. E., and Shih, M. C. (2007) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 35. Phytochemistry 68, 1510-1520 (Pubitemid 46764779)
45. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890
46. Gouet, P., Robert, X., and Courcelle, E. (2003) ESPript/ENDscript. Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31, 3320-3323 (Pubitemid 37442149)