Interaction between two putative glycosyltransferases is required for glycosylation of a serine-rich streptococcal adhesin

Journal of Bacteriology

Volumn 190, Issue 4, 2008, Pages 1256-1266

  Bu, Su ^a   Li, Yirong ^a,e   Zhou, Meixian ^a   Azadin, Parastoo ^c   Zeng, Meiqin ^a   Fives Taylor, Paula ^d   Wu, Hui ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^e HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; GLUTATHIONE TRANSFERASE; GLYCOPROTEIN; GLYCOSYLTRANSFERASE; MONOSACCHARIDE; N ACETYLGLUCOSAMINE; PROTEIN FAP1; PROTEIN GTF1; PROTEIN GTF2; RECOMBINANT PROTEIN; SERINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL VIRULENCE; BIOFILM; COMPLEX FORMATION; CONTROLLED STUDY; ESCHERICHIA COLI; FIMBRIA; GENE CLUSTER; GLYCOSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; STAPHYLOCOCCUS; STREPTOCOCCUS; STREPTOCOCCUS PARASANGUINIS; TWO HYBRID SYSTEM;

ACETYLGLUCOSAMINE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; ESCHERICHIA COLI; FIMBRIAE PROTEINS; GENETIC COMPLEMENTATION TEST; GLYCOSYLATION; GLYCOSYLTRANSFERASES; ISOENZYMES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; PHENOTYPE; PLASMIDS; PROTEIN BINDING; RECOMBINANT PROTEINS; SERINE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STREPTOCOCCUS; TANDEM MASS SPECTROMETRY; TWO-HYBRID SYSTEM TECHNIQUES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; STAPHYLOCOCCUS; STREPTOCOCCUS PARASANGUINIS;

EID: 38949153119     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01078-07     Document Type: Article

References (38)

1. Bensing, B. A., B. W. Gibson, and P. M. Sullam. 2004. The Streptococcus gordonii platelet binding protein GspB undergoes glycosylation independently of export. J. Bacteriol. 186:638-645.
2. Carlsson, J., H. Grahnen, G. Jonsson, and S. Wikner. 1970. Establishment of Streptococcus sanguis in the mouths of infants. Arch. Oral Biol. 15:1143-1148.
3. Chen, Q., H. Wu, and P. M. Fives-Taylor. 2004. Investigating the role of secA2 in secretion and glycosylation of a fimbrial adhesin in Streptococcus parasanguis FW213. Mol. Microbiol. 53:843-856.
4. Chen, Q., H. Wu, R. Kumar, Z. Peng, and P. M. Fives-Taylor. 2006. SecA2 is distinct from SecA in immunogenic specificity, subcellular distribution and requirement for membrane anchoring in Streptococcus parasanguis. FEMS Microbiol. Lett. 264:174-181.
5. Cole, R. M., G. B. Calandra, E. Huff, and K. M. Nugent. 1976. Attributes of potential utility in differentiating among "group H" streptococci or Streptococcus sanguis. J. Dent. Res. 55:A142-A153.
6. de Graffenried, C. L., and C. R. Bertozzi. 2004. The roles of enzyme localisation and complex formation in glycan assembly within the Golgi apparatus. Curr. Opin. Cell Biol. 16:356-363.
7. Dell, A. 1990. Preparation and desorption mass spectrometry of permethyl and peracetyl derivatives of oligosaccharides. Methods Enzymol. 193:647-660.
8. Erickson, P. R., and M. C. Herzberg. 1993. Evidence for the covalent linkage of carbohydrate polymers to a glycoprotein from Streptococcus sanguis. J. Biol. Chem. 268:23780-23783.
9. Fachon-Kalweit, S., B. L. Elder, and P. Fives-Taylor. 1985. Antibodies that bind to fimbriae block adhesion of Streptococcus sanguis to saliva-coated hydroxyapatite. Infect. Immun. 48:617-624.
10. Fenno, J. C., A. Shaikh, and P. Fives-Taylor. 1993. Characterization of allelic replacement in Streptococcus parasanguis: transformation and homologous recombination in a 'nontransformable' streptococcus. Gene 130:81-90.
11. Fives-Taylor, P. M., and D. W. Thompson. 1985. Surface properties of Streptococcus sanguis FW213 mutants nonadherent to saliva-coated hydroxyapatite. Infect. Immun. 47:752-759.
12. Gibbons, R. J., and J. van Houte. 1975. Dental caries. Annu. Rev. Med. 26:121-136.
13. Giraudo, C. G., and H. J. Maccioni. 2003. Ganglioside glycosyltransferases organize in distinct multienzyme complexes in CHO-K1 cells. J. Biol. Chem. 278:40262-40271.
14. Kremer, B. H. A., M. van der Kraan, P. J. Crowley, I. R. Hamilton, L. J. Brady, and A. S. Bleiweis. 2001. Characterization of the sat operon in Streptococcus mutans: evidence for a role of Ffh in acid tolerance. J. Bacteriol. 183:2543-2552.
15. Lawrence, M. L., M. M. Banes, P. Azadi, and B. Y. Reeks. 2003. The Edwardsiella ictaluri O polysaccharide biosynthesis gene cluster and the role of O polysaccharide in resistance to normal catfish serum and catfish neutrophils. Microbiology 149:1409-1421.
16. Lehle, L., S. Strahl, and W. Tanner. 2006. Protein glycosylation, conserved from yeast to man: a model organism helps elucidate congenital human diseases. Angew. Chem. Int. Ed. Engl. 45:6802-6818.
17. Macrina, F. L., J. A. Tobian, K. R. Jones, R. P. Evans, and D. B. Clewell. 1982. A cloning vector able to replicate in Escherichia coli and Streptococcus sanguis. Gene 19:345-353.
18. Marsh, P. D. 1995. The role of microbiology in models of dental caries. Adv. Dent. Res. 9:244-269.
19. Mintz, K. P., and P. M. Fives-Taylor. 2000. Development of a recA- strain of Actinobacillus actinomycetemcomitans. J. Dent. Res. 79:338.
20. Obert, C., J. Sublett, D. Kaushal, E. Hinojosa, T. Barton, E. I. Tuomanen, and C. J. Orihuela. 2006. Identification of a candidate Streptococcus pneumoniae core genome and regions of diversity correlated with invasive pneumococcal disease. Infect. Immun. 74:4766-4777.
21. Plummer, C., H. Wu, S. W. Kerrigan, G. Meade, D. Cox, and C. W. Ian Douglas. 2005. A serine-rich glycoprotein of Streptococcus sanguis mediates adhesion to platelets via GPIb. Br. J. Haematol. 129:101-109.
22. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
23. Seifert, K. N., E. E. Adderson, A. A. Whiting, J. F. Bohnsack, P. J. Crowley, and L. J. Brady. 2006. A unique serine-rich repeat protein (Srr-2) and novel surface antigen (epsilon) associated with a virulent lineage of serotype III Streptococcus agalactiae. Microbiology 152:1029-1040.
24. Seko, A., and K. Yamashita. 2005. Characterization of a novel galactose beta1,3-N-acetylglucosaminyltransferase (beta3Gn-T8): the complex formation of beta3Gn-T2 and beta3Gn-T8 enhances enzymatic activity. Glycobiology 15:943-951.
25. Siboo, I. R., H. F. Chambers, and P. M. Sullam. 2005. Role of SraP, a serine-rich surface protein of Staphylococcus aureus, in binding to human platelets. Infect. Immun. 73:2273-2280.
26. Smith, L. M., J. Z. Sanders, R. J. Kaiser, P. Hughes, C. Dodd, C. R. Connell, C. Heiner, S. B. Kent, and L. E. Hood. 1986. Fluorescence detection in automated DNA sequence analysis. Nature 321:674-679.
27. Stephenson, A. E., H. Wu, J. Novak, M. Tomana, K. Mintz, and P. Fives-Taylor. 2002. The Fap1 fimbrial adhesin is a glycoprotein: antibodies specific for the glycan moiety block the adhesion of Streptococcus parasanguis in an in vitro tooth model. Mol. Microbiol. 43:147-157.
28. Szymanski, C. M., and B. W. Wren. 2005. Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3:225-237.
29. Takahashi, Y., K. Konishi, J. O. Cisar, and M. Yoshikawa. 2002. Identification and characterization of hsa, the gene encoding the sialic acid-binding adhesin of Streptococcus gordonii DL1. Infect. Immun. 70:1209-1218.
30. Takahashi, Y., E. Takashima, K. Shimazu, H. Yagishita, T. Aoba, and K. Konishi. 2006. Contribution of sialic acid-binding adhesin to pathogenesis of experimental endocarditis caused by Streptococcus gordonii DL1. Infect. Immun. 74:740-743.
31. Takamatsu, D., B. A. Bensing, and P. M. Sullam. 2004. Four proteins encoded in the gspB-secY2A2 operon of Streptococcus gordonii mediate the intracellular glycosylation of the platelet-binding protein GspB. J. Bacteriol. 186:7100-7111.
32. Tao, L., D. J. LeBlanc, and J. J. Ferretti. 1992. Novel streptococcal-integration shuttle vectors for gene cloning and inactivation. Gene 120:105-110.
33. Wacker, M., M. F. Feldman, N. Callewaert, M. Kowarik, B. R. Clarke, N. L. Pohl, M. Hernandez, E. D. Vines, M. A. Valvano, C. Whitfield, and M. Aebi. 2006. Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems. Proc. Natl. Acad. Sci. USA 103:7088-7093.
34. Wu, H., S. Bu, P. Newell, Q. Chen, and P. Fives-Taylor. 2007. Two gene determinants are differentially involved in the biogenesis of Fap1 precursors in Streptococcus parasanguis. J. Bacteriol. 189:1390-1398.
35. Wu, H., and P. M. Fives-Taylor. 1999. Identification of dipeptide repeats and a cell wall sorting signal in the fimbriae-associated adhesin, Fap1, of Streptococcus parasanguis. Mol. Microbiol. 34:1070-1081.
36. Wu, H., and P. M. Fives-Taylor. 2001. Molecular strategies for fimbrial expression and assembly. Crit. Rev. Oral Biol. Med. 12:101-115.
37. Wu, H., K. P. Mintz, M. Ladha, and P. M. Fives-Taylor. 1998. Isolation and characterization of Fap1, a fimbriae-associated adhesin of Streptococcus parasanguis FW213. Mol. Microbiol. 28:487-500.
38. Wu, H., M. Zeng, and P. Fives-Taylor. 2007. The glycan moieties and the N-terminal polypeptide backbone of a fimbria-associated adhesin, Fap1, play distinct roles in the biofilm development of Streptococcus parasanguinis. Infect. Immun. 75:2181-2188.