Characterization of the Streptococcus pneumoniae BgaC protein as a novel surface β-galactosidase with specific hydrolysis activity for the Galβ1-3GlcNAc moiety of oligosaccharides

Journal of Bacteriology

Volumn 191, Issue 9, 2009, Pages 3011-3023

  Jeong, Jae Kap ^a   Kwon, Ohsuk ^a   Lee, Yun Mi ^a   Oh, Doo Byoung ^a   Lee, Jung Mi ^a   Kim, Seonghun ^a   Kim, Eun Hye ^b   Le, Tu Nhat ^b   Rhee, Dong Kwon ^b,c   Kang, Hyun Ah ^c  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Sungkyunkwan University   (South Korea)

^c Chung Ang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BACTERIAL ENZYME; BACTERIAL PROTEIN; BETA GALACTOSIDASE; BGAC PROTEIN; FLUORESCEIN ISOTHIOCYANATE; MEMBRANE PROTEIN; OLIGOSACCHARIDE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL SURFACE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENE MUTATION; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; STREPTOCOCCUS PNEUMONIAE; WILD TYPE; ANIMAL; BACTERIAL COUNT; BIOSYNTHESIS; BLOOD; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; ISOLATION AND PURIFICATION; LUNG; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; NASOPHARYNX; PATHOGENICITY; PNEUMOCOCCAL INFECTION; VIRULENCE;

ESCHERICHIA COLI; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; BLOOD; COLONY COUNT, MICROBIAL; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; HYDROLYSIS; LUNG; MICE; MICROBIAL VIABILITY; NASOPHARYNX; OLIGOSACCHARIDES; PNEUMOCOCCAL INFECTIONS; PROTEIN SORTING SIGNALS; RECOMBINANT PROTEINS; STREPTOCOCCUS PNEUMONIAE; SUBSTRATE SPECIFICITY; VIRULENCE;

EID: 65549094677     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01601-08     Document Type: Article

References (41)

1. Andersson, B., J. Dahmen, T. Frejd, H. Leffler, G. Magnusson, G. Noori, and C. S. Eden. 1983. Identification of an active disaccharide unit of a glycocon- jugate receptor for pneumococci attaching to human pharyngeal epithelial cells. J. Exp. Med. 158:559-570.
2. Andersson, B., B. Gray, and C. S. Eden. 1988. Role of attachment for the virulence of Streptococcus pneumoniae. Acta Otolaryngol. Suppl. 454:163-166.
3. Avery, O. T., C. M. MacLeod, and M. McCarty. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Induction of transformation by a deoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 79:137-158.
4. Bobrov, A. G., and R. D. Perry. 2006. Yersinia pestis lacZ expresses a beta-galactosidase with low enzymatic activity. FEMS Microbiol. Lett. 255: 43-51.
5. Burnaugh, A. M., L. J. Frantz, and S. J. King. 2008. Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J. Bacteriol. 190:221-230.
6. Cámara, M., G. J. Boulnois, P. W. Andrew, and T. J. Mitchell. 1994. A neuraminidase from Streptococcus pneumoniae has the features of a surface protein. Infect. Immun. 62:3688-3695.
7. Chhatwal, G. S. 2002. Anchorless adhesins and invasins of Gram-positive bacteria: a new class of virulence factors. Trends Microbiol. 10:205-208.
8. Colman, P. M. 1999. A novel approach to antiviral therapy for influenza. J. Antimicrob. Chemother. 44(Suppl. B): 17-22.
9. Conzelmann, E., and K. Sandhoff. 1987. Glycolipid and glycoprotein degradation. Adv. Enzymol. Relat. Areas Mol. Biol. 60:89-216.
10. Dohrman, A., S. Miyata, M. Gallup, J. D. Li, C. Chapelin, A. Coste, E. Escudier, J. Nadel, and C. Basbaum. 1998. Mucin (MUC 2 and MUC 5 AC) transcriptional regulation in response to Gram-positive and -negative bacteria. Biochim. Biophys. Acta 1406:251-259.
11. Fujimoto, H., M. Miyasato, Y. Ito, T. Sasaki, and K. Ajisaka. 1998. Purification and properties of recombinant beta-galactosidase from Bacillus circulans. Glycoconj. J. 15:155-160.
12. Henrissat, B., and G. Davies. 1997. Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7:637-644.
13. Hoskins, J., W. E. Alborn, Jr., J. Arnold, L. C. Blaszczak, S. Burgett, B. S. DeHoff, S. T. Estrem, L. Fritz, D. J. Fu, W. Fuller, C. Geringer, R. Gilmour, J. S. Glass, H. Khoja, A. R. Kraft, R. E. Lagace, D. J. LeBlanc, L. N. Lee, E. J. Lefkowitz, J. Lu, P. Matsushima, S. M. McAhren, M. McHenney, K. McLeaster, C. W. Mundy, T. I. Nicas, F. H. Norris, M. O'Gara, R. B. Peery, G. T. Robertson, P. Rockey, P. M. Sun, M. E. Winkler, Y. Yang, M. Young- Bellido, G. Zhao, C. A. Zook, R. H. Baltz, S. R. Jaskunas, P. R. Rosteck, Jr., P. L. Skatrud, and J. I. Glass. 2001. Genome of the bacterium Streptococcus pneumoniae strain R6. J. Bacteriol. 183:5709-5717.
14. Huber, R. E., C. Parfett, H. Woulfe-Flanagan, and D. J. Thompson. 1979. Interaction of divalent cations with beta-galactosidase (Escherichia coli). Biochemistry 18:4090-4095.
15. Ito, Y., and T. Sasaki. 1997. Cloning and characterization of the gene encoding a novel beta-galactosidase from Bacillus circulans. Biosci. Biotechnol. Biochem. 61:1270-1276.
16. Kadioglu, A., J. N. Weiser, J. C. Paton, and P. W. Andrew. 2008. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 6:288-301.
17. Kaufman, G. E., and J. Yother. 2007. CcpA-dependent and -independent control of beta-galactosidase expression in Streptococcus pneumoniae occurs via regulation of an upstream phosphotransferase system-encoding operon. J. Bacteriol. 189:5183-5192.
18. King, S. J., K. R. Hippe, J. M. Gould, D. Bae, S. Peterson, R. Cline, C. Fasching, E. N. Janoff, and J. N. Weiser. 2004. Phase variable desialylation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol. Microbiol. 54:159-171.
19. King, S. J., K. R. Hippe, and J. N. Weiser. 2006. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol. Microbiol. 59:961-974.
20. Kwon, H. Y., S. W. Kim, M. H. Choi, A. D. Ogunniyi, J. C. Paton, S. H. Park, S. N. Pyo, and D. K. Rhee. 2003. Effect of heat shock and mutations in ClpL and ClpP on virulence gene expression in Streptococcus pneumoniae. Infect. Immun. 71:3757-3765.
21. Lanie, J. A., W. L. Ng, K. M. Kazmierczak, T. M. Andrzejewski, T. M. Davidsen, K. J. Wayne, H. Tettelin, J. I. Glass, and M. E. Winkler. 2007. Genome sequence of Avery's virulent serotype 2 strain D 39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J. Bacteriol. 189:38-51.
22. Lemjabbar, H., and C. Basbaum. 2002. Platelet-activating factor receptor and ADAM10 mediate responses to Staphylococcus aureus in epithelial cells. Nat. Med. 8:41-46.
23. Li, J. D., A. F. Dohrman, M. Gallup, S. Miyata, J. R. Gum, Y. S. Kim, J. A. Nadel, A. Prince, and C. B. Basbaum. 1997. Transcriptional activation of mucin by Pseudomonas aeruginosa lipopolysaccharide in the pathogenesis of cystic fibrosis lung disease. Proc. Natl. Acad. Sci. USA 94:967-972.
24. Li, J. D., W. Feng, M. Gallup, J. H. Kim, J. Gum, Y. Kim, and C. Basbaum. 1998. Activation of NFkB via a Src-dependent Ras-MAPK-pp90rsk pathway is required for P. aeruginosa-induced mucin overproduction in epithelial cells. Proc. Natl. Acad. Sci. USA 95:5718-5723.
25. Merrill, A. H., Jr., M. D. Wang, M. Park, and M. C. Sullards. 2007. (Glyco) sphingolipidology: an amazing challenge and opportunity for systems biology. Trends Biochem. Sci. 32:457-468.
26. Poch, O., H. L'Hote, V. Dallery, F. Debeaux, R. Fleer, and R. Sodoyer. 1992. Sequence of the Kluyveromyces lactis beta-galactosidase: comparison with prokaryotic enzymes and secondary structure analysis. Gene 118:55-63.
27. Schmidt, B. F., R. M. Adams, C. Requadt, S. Power, and S. E. Mainzer. 1989. Expression and nucleotide sequence of the Lactobacillus bulgaricus beta- galactosidase gene cloned in Escherichia coli. J. Bacteriol. 171:625-635.
28. Slack, F. J., and G. Ruvkun. 1998. A novel repeat domain that is often associated with RING finger and B-box motifs. Trends Biochem. Sci. 23: 474-475.
29. Springer, T. A. 1998. An extracellular beta-propeller module predicted in lipoprotein and scavenger receptors, tyrosine kinases, epidermal growth factor precursor, and extracellular matrix components. J. Mol. Biol. 283:837-862.
30. Talbot, U. M., A. W. Paton, and J. C. Paton. 1996. Uptake of Streptococcus pneumoniae by respiratory epithelial cells. Infect. Immun. 64:3772-3777.
31. Taron, C. H., J. S. Benner, L. J. Hornstra, and E. P. Guthrie. 1995. A novel beta-galactosidase gene isolated from the bacterium Xanthomonas manihotis exhibits strong homology to several eukaryotic beta-galactosidases. Glycobiology 5:603-610.
32. Tettelin, H., K. E. Nelson, I. T. Paulsen, J. A. Eisen, T. D. Read, S. Peterson, J. Heidelberg, R. T. DeBoy, D. H. Haft, R. J. Dodson, A. S. Durkin, M. Gwinn, J. F. Kolonay, W. C. Nelson, J. D. Peterson, L. A. Umayam, O. White, S. L. Salzberg, M. R. Lewis, D. Radune, E. Holtzapple, H. Khouri, A. M. Wolf, T. R. Utterback, C. L. Hansen, L. A. McDonald, T. V. Feldblyum, S. Angiuoli, T. Dickinson, E. K. Hickey, I. E. Holt, B. J. Loftus, F. Yang, H. O. Smith, J. C. Venter, B. A. Dougherty, D. A. Morrison, S. K. Hollingshead, and C. M. Fraser. 2001. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293:498-506.
33. Tong, H. H., M. A. McIver, L. M. Fisher, and T. F. DeMaria. 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.
34. Tong, H. H., X. Liu, Y. Chen, M. James, and T. Demaria. 2002. Effect of neuraminidase on receptor-mediated adherence of Streptococcus pneumoniae to chinchilla tracheal epithelium. Acta Otolaryngol. 122:413-419.
35. Tu, L. N., H. Y. Jeong, H. Y. Kwon, A. D. Ogunniyi, J. C. Paton, S. N. Pyo, and D. K. Rhee. 2007. Modulation of adherence, invasion, and tumor necrosis factor alpha secretion during the early stages of infection by Streptococcus pneumoniae ClpL. Infect. Immun. 75:2996-3005.
36. van Bueren, A. L., M. Higgins, D. Wang, R. D. Burke, and A. B. Boraston. 2007. Identification and structural basis of binding to host lung glycogen by streptococcal virulence factors. Nat. Struct. Mol. Biol. 14:76-84.
37. Vasseghi, H., and J. P. Claverys. 1983. Amplification of a chimeric plasmid carrying an erythromycin-resistance determinant introduced into the genome of Streptococcus pneumoniae. Gene 21:285-292.
38. Vijayakumar, M. N., and D. A. Morrison. 1986. Localization of competence- induced proteins in Streptococcus pneumoniae. J. Bacteriol. 165:689-695.
39. Weiser, J. N., D. Bae, H. Epino, S. B. Gordon, M. Kapoor, L. A. Zenewicz, and M. Shchepetov. 2001. Changes in availability of oxygen accentuate differences in capsular polysaccharide expression by phenotypic variants and clinical isolates of Streptococcus pneumoniae. Infect. Immun. 69:5430-5439.
40. Wong-Madden, S. T., and D. Landry. 1995. Purification and characterization of novel glycosidases from the bacterial genus Xanthomonas. Glycobiology 5:19-28.
41. Zahner, D., and R. Hakenbeck. 2000. The Streptococcus pneumoniae beta- galactosidase is a surface protein. J. Bacteriol. 182:5919-5921.