1887

Abstract

Glycosylation of bacterial proteins is an important process for bacterial physiology and pathophysiology. Both - and -linked glycan moieties have been identified in bacterial glycoproteins. The -linked glycosylation pathways are well established in Gram-negative bacteria. However, the -linked glycosylation pathways are not well defined due to the complex nature of known -linked glycoproteins in bacteria. In this review, we examine a new family of serine-rich -linked glycoproteins which are represented by fimbriae-associated adhesin Fap1 of and human platelet-binding protein GspB of . This family of glycoproteins is conserved in streptococcal and staphylococcal species. A gene cluster coding for glycosyltransferases and accessory Sec proteins has been implicated in the protein glycosylation. A two-step glycosylation model is proposed. Two glycosyltransferases interact with each other and catalyse the first step of the protein glycosylation in the cytoplasm; the cross-talk between glycosylation-associated proteins and accessory Sec components mediates the second step of the protein glycosylation, an emerging mechanism for bacterial -linked protein glycosylation. Dissecting the molecular mechanism of this conserved biosynthetic pathway offers opportunities to develop new therapeutic strategies targeting this previously unrecognized pathway, as serine-rich glycoproteins have been shown to play a role in bacterial pathogenesis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.025221-0
2009-02-01
2020-02-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/2/317.html?itemId=/content/journal/micro/10.1099/mic.0.025221-0&mimeType=html&fmt=ahah

References

  1. Arora S. K., Bangera M., Lory S., Ramphal R.. 2001; A genomic island in Pseudomonas aeruginosa carries the determinants of flagellin glycosylation. Proc Natl Acad Sci U S A98:9342–9347
    [Google Scholar]
  2. Baba T., Takeuchi F., Kuroda M., Yuzawa H., Aoki K., Oguchi A., Nagai Y., Iwama N., Asano K.. other authors 2002; Genome and virulence determinants of high virulence community-acquired MRSA. Lancet359:1819–1827
    [Google Scholar]
  3. Banerjee A., Wang R., Supernavage S. L., Ghosh S. K., Parker J., Ganesh N. F., Wang P. G., Gulati S., Rice P. A.. 2002; Implications of phase variation of a gene ( pgtA ) encoding a pilin galactosyl transferase in gonococcal pathogenesis. J Exp Med196:147–162
    [Google Scholar]
  4. Bensing B. A., Sullam P. M.. 2002; An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol Microbiol44:1081–1094
    [Google Scholar]
  5. Bensing B. A., Gibson B. W., Sullam P. M.. 2004a; The Streptococcus gordonii platelet binding protein GspB undergoes glycosylation independently of export. J Bacteriol186:638–645
    [Google Scholar]
  6. Bensing B. A., Lopez J. A., Sullam P. M.. 2004b; The Streptococcus gordonii surface proteins GspB and Hsa mediate binding to sialylated carbohydrate epitopes on the platelet membrane glycoprotein Ib α . Infect Immun72:6528–6537
    [Google Scholar]
  7. Bensing B. A., Takamatsu D., Sullam P. M.. 2005; Determinants of the streptococcal surface glycoprotein GspB that facilitate export by the accessory Sec system. Mol Microbiol58:1468–1481
    [Google Scholar]
  8. Bu S., Li Y., Zhou M., Azadin P., Zeng M., Fives-Taylor P., Wu H.. 2008; Interaction between two putative glycosyltransferases is required for glycosylation of a serine-rich streptococcal adhesin. J Bacteriol190:1256–1266
    [Google Scholar]
  9. Chen Q., Wu H., Fives-Taylor P. M.. 2004; Investigating the role of secA2 in secretion and glycosylation of a fimbrial adhesin in Streptococcus parasanguis FW213. Mol Microbiol53:843–856
    [Google Scholar]
  10. Chen Q., Wu H., Kumar R., Peng Z., Fives-Taylor P. M.. 2006; SecA2 is distinct from SecA in immunogenic specificity, subcellular distribution and requirement for membrane anchoring in Streptococcus parasanguis . FEMS Microbiol Lett264:174–181
    [Google Scholar]
  11. Chen Q., Sun B., Wu H., Peng Z., Fives-Taylor P. M.. 2007; Differential roles of individual domains in selection of secretion route of a Streptococcus parasanguinis serine-rich adhesin, Fap1. J Bacteriol189:7610–7617
    [Google Scholar]
  12. Drickamer K., Taylor M. E.. 1998; Evolving views of protein glycosylation. Trends Biochem Sci23:321–324
    [Google Scholar]
  13. Erickson P. R., Herzberg M. C.. 1993; Evidence for the covalent linkage of carbohydrate polymers to a glycoprotein from Streptococcus sanguis . J Biol Chem268:23780–23783
    [Google Scholar]
  14. Fachon-Kalweit S., Elder B. L., Fives-Taylor P.. 1985; Antibodies that bind to fimbriae block adhesion of Streptococcus sanguis to saliva-coated hydroxyapatite. Infect Immun48:617–624
    [Google Scholar]
  15. Froeliger E. H., Fives-Taylor P.. 2001; Streptococcus parasanguis fimbria-associated adhesin Fap1 is required for biofilm formation. Infect Immun69:2512–2519
    [Google Scholar]
  16. Glaser P., Rusniok C., Buchrieser C., Chevalier F., Frangeul L., Msadek T., Zouine M., Couvé E., Lalioui L.. other authors 2002; Genome sequence of Streptococcus agalactiae , a pathogen causing invasive neonatal disease. Mol Microbiol45:1499–1513
    [Google Scholar]
  17. Hamadeh R. M., Estabrook M. M., Zhou P., Jarvis G. A., Griffiss J. M.. 1995; Anti-Gal binds to pili of Neisseria meningitidis : the immunoglobulin A isotype blocks complement-mediated killing. Infect Immun63:4900–4906
    [Google Scholar]
  18. Handley P. S., Correia F. F., Russell K., Rosan B., DiRienzo J. M.. 2005; Association of a novel high molecular weight, serine-rich protein (SrpA) with fibril-mediated adhesion of the oral biofilm bacterium Streptococcus cristatus . Oral Microbiol Immunol20:131–140
    [Google Scholar]
  19. Hegge F. T., Hitchen P. G., Aas F. E., Kristiansen H., Løvold C., Egge-Jacobsen W., Panico M., Leong W. Y., Bull V.. other authors 2004; Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc Natl Acad Sci U S A101:10798–10803
    [Google Scholar]
  20. Hounsell E. F., Davies M. J., Renouf D. V.. 1996; O -linked protein glycosylation structure and function. Glycoconj J13:19–26
    [Google Scholar]
  21. Jakubovics N. S., Kerrigan S. W., Nobbs A. H., Stromberg N., van Dolleweerd C. J., Cox D. M., Kelly C. G., Jenkinson H. F.. 2005; Functions of cell surface-anchored antigen I/II family and Hsa polypeptides in interactions of Streptococcus gordonii with host receptors. Infect Immun73:6629–6638
    [Google Scholar]
  22. Lenz L. L., Portnoy D. A.. 2002; Identification of a second Listeria secA gene associated with protein secretion and the rough phenotype. Mol Microbiol45:1043–1056
    [Google Scholar]
  23. Levesque C., Vadeboncoeur C., Chandad F., Frenette M.. 2001; Streptococcus salivarius fimbriae are composed of a glycoprotein containing a repeated motif assembled into a filamentous nondissociable structure. J Bacteriol183:2724–2732
    [Google Scholar]
  24. Li Y., Chen Y., Huang X., Zhou M., Wu R., Dong S., Pritchard D. G., Fives-Taylor P., Wu H.. 2008; A conserved domain of previously unknown function in Gap1 mediates protein–protein interaction and is required for biogenesis of a serine-rich streptococcal adhesin. Mol Microbiol70:1094–1104
    [Google Scholar]
  25. Moens S., Vanderleyden J.. 1997; Glycoproteins in prokaryotes. Arch Microbiol168:169–175
    [Google Scholar]
  26. Nobbs A. H., Zhang Y., Khammanivong A., Herzberg M. C.. 2007; Streptococcus gordonii Hsa environmentally constrains competitive binding by Streptococcus sanguinis to saliva-coated hydroxyapatite. J Bacteriol189:3106–3114
    [Google Scholar]
  27. Obert C., Sublett J., Kaushal D., Hinojosa E., Barton T., Tuomanen E. I., Orihuela C. J.. 2006; Identification of a candidate Streptococcus pneumoniae core genome and regions of diversity correlated with invasive pneumococcal disease. Infect Immun74:4766–4777
    [Google Scholar]
  28. Peng Z., Wu H., Ruiz T., Chen Q., Zhou M., Sun B., Fives-Taylor P.. 2008; Role of gap3 in Fap1 glycosylation, stability, in vitro adhesion, and fimbrial and biofilm formation of Streptococcus parasanguinis . Oral Microbiol Immunol23:70–78
    [Google Scholar]
  29. Plummer C., Wu H., Kerrigan S. W., Meade G., Cox D., Ian Douglas C. W.. 2005; A serine-rich glycoprotein of Streptococcus sanguis mediates adhesion to platelets via GPIb. Br J Haematol129:101–109
    [Google Scholar]
  30. Pombert C. B., Levesque C., Frenette M.. 2008; Genetic organization of fimbriae's secretion/glycosylation machinery in Streptococcus salivarius . J Dent Res87:3422
    [Google Scholar]
  31. Power P. M., Roddam L. F., Rutter K., Fitzpatrick S. Z., Srikhanta Y. N., Jennings M. P.. 2003; Genetic characterization of pilin glycosylation and phase variation in Neisseria meningitidis . Mol Microbiol49:833–847
    [Google Scholar]
  32. Rigel N. W., Braunstein M.. 2008; A new twist on an old pathway – accessory secretion systems. Mol Microbiol69:291–302
    [Google Scholar]
  33. Rose L., Shivshankar P., Hinojosa E., Rodriguez A., Sanchez C. J., Orihuela C. J.. 2008; Antibodies against PsrP, a novel Streptococcus pneumoniae adhesin, block adhesion and protect mice against pneumococcal challenge. J Infect Dis198:375–383
    [Google Scholar]
  34. Samen U., Eikmanns B. J., Reinscheid D. J., Borges F.. 2007; The surface protein Srr-1 of Streptococcus agalactiae binds human keratin 4 and promotes adherence to epithelial HEp-2 cells. Infect Immun75:5405–5414
    [Google Scholar]
  35. Schmidt M. A., Riley L. W., Benz I.. 2003; Sweet new world: glycoproteins in bacterial pathogens. Trends Microbiol11:554–561
    [Google Scholar]
  36. Seifert K. N., Adderson E. E., Whiting A. A., Bohnsack J. F., Crowley P. J., Brady L. J.. 2006; A unique serine-rich repeat protein (Srr-2) and novel surface antigen (epsilon) associated with a virulent lineage of serotype III Streptococcus agalactiae . Microbiology152:1029–1040
    [Google Scholar]
  37. Siboo I. R., Chambers H. F., Sullam P. M.. 2005; Role of SraP, a serine-rich surface protein of Staphylococcus aureus , in binding to human platelets. Infect Immun73:2273–2280
    [Google Scholar]
  38. Siboo I. R., Chaffin D. O., Rubens C. E., Sullam P. M.. 2008; Characterization of the accessory Sec system of Staphylococcus aureus . J Bacteriol190:6188–6196
    [Google Scholar]
  39. Stephenson A. E., Wu H., Novak J., Tomana M., Mintz K., Fives-Taylor P.. 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 Microbiol43:147–157
    [Google Scholar]
  40. Szymanski C. M., Wren B. W.. 2005; Protein glycosylation in bacterial mucosal pathogens. Nat Rev Microbiol3:225–237
    [Google Scholar]
  41. Szymanski C. M., Logan S. M., Linton D., Wren B. W.. 2003; Campylobacter – a tale of two protein glycosylation systems. Trends Microbiol11:233–238
    [Google Scholar]
  42. Takahashi Y., Konishi K., Cisar J. O., Yoshikawa M.. 2002; Identification and characterization of hsa , the gene encoding the sialic acid-binding adhesin of Streptococcus gordonii DL1. Infect Immun70:1209–1218
    [Google Scholar]
  43. Takahashi Y., Yajima A., Cisar J. O., Konishi K.. 2004; Functional analysis of the Streptococcus gordonii DL1 sialic acid-binding adhesin and its essential role in bacterial binding to platelets. Infect Immun72:3876–3882
    [Google Scholar]
  44. Takahashi Y., Takashima E., Shimazu K., Yagishita H., Aoba T., Konishi K.. 2006; Contribution of sialic acid-binding adhesin to pathogenesis of experimental endocarditis caused by Streptococcus gordonii DL1. Infect Immun74:740–743
    [Google Scholar]
  45. Takamatsu D., Bensing B. A., Sullam P. M.. 2004a; Genes in the accessory sec locus of Streptococcus gordonii have three functionally distinct effects on the expression of the platelet-binding protein GspB. Mol Microbiol52:189–203
    [Google Scholar]
  46. Takamatsu D., Bensing B. A., Sullam P. M.. 2004b; Four proteins encoded in the gspB-secY2A2 operon of Streptococcus gordonii mediate the intracellular glycosylation of the platelet-binding protein GspB. J Bacteriol186:7100–7111
    [Google Scholar]
  47. Takamatsu D., Bensing B. A., Cheng H., Jarvis G. A., Siboo I. R., Lopez J. A., Griffiss J. M., Sullam P. M.. 2005a; Binding of the Streptococcus gordonii surface glycoproteins GspB and Hsa to specific carbohydrate structures on platelet membrane glycoprotein Ibalpha. Mol Microbiol58:380–392
    [Google Scholar]
  48. Takamatsu D., Bensing B. A., Sullam P. M.. 2005b; Two additional components of the accessory sec system mediating export of the Streptococcus gordonii platelet-binding protein GspB. J Bacteriol187:3878–3883
    [Google Scholar]
  49. Takamatsu D., Bensing B. A., Prakobphol A., Fisher S. J., Sullam P. M.. 2006; Binding of the streptococcal surface glycoproteins GspB and Hsa to human salivary proteins. Infect Immun74:1933–1940
    [Google Scholar]
  50. Takeuchi F., Watanabe S., Baba T., Yuzawa H., Ito T., Morimoto Y., Kuroda M., Cui L., Takahashi M.. other authors 2005; Whole-genome sequencing of Staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol187:7292–7308
    [Google Scholar]
  51. Tettelin H., Nelson K. E., Paulsen I. T., Eisen J. A., Read T. D., Peterson S., Heidelberg J., DeBoy R. T., Haft D. H.. other authors 2001; Complete genome sequence of a virulent isolate of Streptococcus pneumoniae . Science293:498–506
    [Google Scholar]
  52. Upreti R. K., Kumar M., Shankar V.. 2003; Bacterial glycoproteins: functions, biosynthesis and applications. Proteomics3:363–379
    [Google Scholar]
  53. VanderVen B. C., Harder J. D., Crick D. C., Belisle J. T.. 2005; Export-mediated assembly of mycobacterial glycoproteins parallels eukaryotic pathways. Science309:941–943
    [Google Scholar]
  54. Vickerman M. M., Iobst S., Jesionowski A. M., Gill S. R.. 2007; Genome-wide transcriptional changes in Streptococcus gordonii in response to competence signaling peptide. J Bacteriol189:7799–7807
    [Google Scholar]
  55. Wacker M., Linton D., Hitchen P. G., Nita-Lazar M., Haslam S. M., North S. J., Panico M., Morris H. R., Dell A.. other authors 2002; N -linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli . Science298:1790–1793
    [Google Scholar]
  56. Weerkamp A. H., Handley P. S., Baars A., Slot J. W.. 1986a; Negative staining and immunoelectron microscopy of adhesion-deficient mutants of Streptococcus salivarius reveal that the adhesive protein antigens are separate classes of cell surface fibril. J Bacteriol165:746–755
    [Google Scholar]
  57. Weerkamp A. H., van der Mei H. C., Liem R. S.. 1986b; Structural properties of fibrillar proteins isolated from the cell surface and cytoplasm of Streptococcus salivarius (K+) cells and nonadhesive mutants. J Bacteriol165:756–762
    [Google Scholar]
  58. Wu H., Fives-Taylor P. M.. 1999; Identification of dipeptide repeats and a cell wall sorting signal in the fimbriae-associated adhesin, Fap1, of Streptococcus parasanguis . Mol Microbiol34:1070–1081
    [Google Scholar]
  59. Wu H., Fives-Taylor P. M.. 2001; Molecular strategies for fimbrial expression and assembly. Crit Rev Oral Biol Med12:101–115
    [Google Scholar]
  60. Wu H., Mintz K. P., Ladha M., Fives-Taylor P. M.. 1998; Isolation and characterization of Fap1, a fimbriae-associated adhesin of Streptococcus parasanguis FW213. Mol Microbiol28:487–500
    [Google Scholar]
  61. Wu H., Bu S., Newell P., Chen Q., Fives-Taylor P.. 2007a; Two gene determinants are differentially involved in the biogenesis of Fap1 precursors in Streptococcus parasanguis . J Bacteriol189:1390–1398
    [Google Scholar]
  62. Wu H., Zeng M., Fives-Taylor P.. 2007b; 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 Immun75:2181–2188
    [Google Scholar]
  63. Xiong Y. Q., Bensing B. A., Bayer A. S., Chambers H. F., Sullam P. M.. 2008; Role of the serine-rich surface glycoprotein GspB of Streptococcus gordonii in the pathogenesis of infective endocarditis. Microb Pathog45:297–301
    [Google Scholar]
  64. Xu P., Alves J. M., Kitten T., Brown A., Chen Z., Ozaki L. S., Manque P., Ge X., Serrano M. G.. other authors 2007; Genome of the opportunistic pathogen Streptococcus sanguinis . J Bacteriol189:3166–3175
    [Google Scholar]
  65. Yajima A., Urano-Tashiro Y., Shimazu K., Takashima E., Takahashi Y., Konishi K.. 2008; Hsa, an adhesin of Streptococcus gordonii DL1, binds to α 2-3-linked sialic acid on glycophorin A of the erythrocyte membrane. Microbiol Immunol52:69–77
    [Google Scholar]
  66. Young Lee S., Cisar J. O., Bryant J. L., Eckhaus M. A., Sandberg A. L.. 2006; Resistance of Streptococcus gordonii to polymorphonuclear leukocyte killing is a potential virulence determinant of infective endocarditis. Infect Immun74:3148–3155
    [Google Scholar]
  67. Zhang Y. Q., Ren S. X., Li H. L., Wang Y. X., Fu G., Yang J., Qin Z. Q., Miao Y. G., Wang W. Y.. other authors 2003; Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228. Mol Microbiol49:1577–1593
    [Google Scholar]
  68. Zhou M., Peng Z., Fives-Taylor P., Wu H.. 2008; A conserved C-terminal thirteen amino acid motif of Gap1 is required for the Gap1 function and necessary for biogenesis of a serine-rich glycoprotein of Streptococcus parasanguinis . Infect Immun76:5624–5631
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.025221-0
Loading
/content/journal/micro/10.1099/mic.0.025221-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error