A role for glycosylated serine-rich repeat proteins in Gram-positive bacterial pathogenesis

Molecular Oral Microbiology

Volumn 27, Issue 4, 2012, Pages 257-269

  Lizcano, A ^a   Sanchez, C J ^a   Orihuela, C J ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Adhesion; Biofilm; Gram positive bacteria; Pathogenesis; Serine rich repeat proteins

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; KERATIN; SERINE; SERINE RICH REPEAT PROTEIN; SIALIC ACID; UNCLASSIFIED DRUG;

BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BIOFILM; BLOOD BRAIN BARRIER; COMMUNITY ACQUIRED PNEUMONIA; CRYSTALLIZATION; GRAM POSITIVE INFECTION; HOST CELL; HUMAN; LACTOCOCCUS; NONHUMAN; PNEUMOCOCCAL MENINGITIS; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; REVIEW; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS SAPROPHYTICUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PARASANGUINIS; STREPTOCOCCUS PNEUMONIAE; SUBACUTE ENDOCARDITIS; TRANSCRIPTION REGULATION;

ADHESINS, BACTERIAL; ENDOCARDITIS, SUBACUTE BACTERIAL; FIMBRIAE PROTEINS; GLYCOSYLATION; GRAM-POSITIVE BACTERIA; HUMANS; KERATINS; MEMBRANE TRANSPORT PROTEINS; MENINGITIS, PNEUMOCOCCAL; MICROBIAL CONSORTIA; N-ACETYLNEURAMINIC ACID; PNEUMONIA, PNEUMOCOCCAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; SERINE;

EID: 84863566088     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/j.2041-1014.2012.00653.x     Document Type: Review

References (72)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Baba, T., Takeuchi, F., Kuroda, M. et al. (2002) Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359: 1819-1827.
3. Bensing, B.A. and 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 Microbiol 44: 1081-1094.
4. Bensing, B.A. and Sullam, P.M. (2009) Characterization of Streptococcus gordonii SecA2 as a paralogue of SecA. J Bacteriol 191: 3482-3491.
5. Bensing, B.A. and Sullam, P.M. (2010) Transport of preproteins by the accessory Sec system requires a specific domain adjacent to the signal peptide. J Bacteriol 192: 4223-4232.
6. Bensing, B.A., Gibson, B.W. and Sullam, P.M. (2004) The Streptococcus gordonii platelet binding protein GspB undergoes glycosylation independently of export. J Bacteriol 186: 638-645.
7. Bensing, B.A., Takamatsu, D. and Sullam, P.M. (2005) Determinants of the streptococcal surface glycoprotein GspB that facilitate export by the accessory Sec system. Mol Microbiol 58: 1468-1481.
8. Bensing, B.A., Siboo, I.R. and Sullam, P.M. (2007) Glycine residues in the hydrophobic core of the GspB signal sequence route export toward the accessory Sec pathway. J Bacteriol 189: 3846-3854.
9. Bu, S., Li, Y., Zhou, M. et al. (2008) Interaction between two putative glycosyltransferases is required for glycosylation of a serine-rich streptococcal adhesin. J Bacteriol 190: 1256-1266.
10. Chen, Q., Wu, H. and Fives-Taylor, P.M. (2004) Investigating the role of secA2 in secretion and glycosylation of a fimbrial adhesin in Streptococcus parasanguis FW213. Mol Microbiol 53: 843-856.
11. Chen, Q., Wu, H., Kumar, R., Peng, Z. and 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 Lett 264: 174-181.
12. Chenna, R., Sugawara, H., Koike, T. et al. (2003) Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res 31: 3497-3500.
13. Fachon-Kalweit, S., Elder, B.L. and Fives-Taylor, P. (1985) Antibodies that bind to fimbriae block adhesion of Streptococcus sanguis to saliva-coated hydroxyapatite. Infect Immun 48: 617-624.
14. Froeliger, E.H. and Fives-Taylor, P. (2001) Streptococcus parasanguis fimbria-associated adhesin fap1 is required for biofilm formation. Infect Immun 69: 2512-2519.
15. Garnett, J.A., Ramboarina, S., Lee, W.C., Tagliaferri, C., Wu, W. and Matthews, S. (2011) Crystallization and initial crystallographic analysis of the Streptococcus parasanguinis FW213 Fap1-NRalpha adhesive domain at pH 5.0. Acta Crystallogr Sect F Struct Biol Cryst Commun 67: 274-276.
16. Garnett, J.A., Simpson, P.J., Taylor, J. et al. (2012) Structural insight into the role of Streptococcus parasanguinis Fap1 within oral biofilm formation. Biochem Biophys Res Commun 417: 421-426.
17. Glaser, P., Rusniok, C., Buchrieser, C. et al. (2002) Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol 45: 1499-1513.
18. Gu, L.H. and Coulombe, P.A. (2007) Keratin function in skin epithelia: a broadening palette with surprising shades. Curr Opin Cell Biol 19: 13-23.
19. Handley, P.S., Correia, F.F., Russell, K., Rosan, B. and 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 Immunol 20: 131-140.
20. Kuroda, M., Tanaka, Y., Aoki, R., Shu, D., Tsumoto, K. and Ohta, T. (2008) Staphylococcus aureus giant protein Ebh is involved in tolerance to transient hyperosmotic pressure. Biochem Biophys Res Commun 374: 237-241.
21. Lauer, P., Rinaudo, C.D., Soriani, M. et al. (2005) Genome analysis reveals pili in Group B Streptococcus. Science 309: 105.
22. Leube, R.E., Bader, B.L., Bosch, F.X., Zimbelmann, R., Achtstaetter, T. and Franke, W.W. (1988) Molecular characterization and expression of the stratification-related cytokeratins 4 and 15. J Cell Biol 106: 1249-1261.
23. Li, Y., Chen, Y., Huang, X. et al. (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 Microbiol 70: 1094-1104.
24. Mistou, M.Y., Dramsi, S., Brega, S., Poyart, C. and Trieu-Cuot, P. (2009) Molecular dissection of the secA2 locus of Group B Streptococcus reveals that glycosylation of the Srr1 LPXTG protein is required for full virulence. J Bacteriol 191: 4195-4206.
25. Nobbs, A.H., Lamont, R.J. and Jenkinson, H.F. (2009) Streptococcus adherence and colonization. Microbiol Mol Biol Rev 73: 407-450.
26. Obert, C., Sublett, J., Kaushal, D. et al. (2006) Identification of a candidate Streptococcus pneumoniae core genome and regions of diversity correlated with invasive pneumococcal disease. Infect Immun 74: 4766-4777.
27. Peng, Z., Fives-Taylor, P., Ruiz, T. et al. (2008a) Identification of critical residues in Gap3 of Streptococcus parasanguinis involved in Fap1 glycosylation, fimbrial formation and in vitro adhesion. BMC Microbiol 8: 52.
28. Peng, Z., Wu, H., Ruiz, T. et al. (2008b) Role of gap3 in Fap1 glycosylation, stability, in vitro adhesion, and fimbrial and biofilm formation of Streptococcus parasanguinis. Oral Microbiol Immunol 23: 70-78.
29. Plummer, C., Wu, H., Kerrigan, S.W., Meade, G., Cox, D. and Ian Douglas, C.W. (2005) A serine-rich glycoprotein of Streptococcus sanguis mediates adhesion to platelets via GPIb. Br J Haematol 129: 101-109.
30. Pyburn, T.M., Bensing, B.A., Xiong, Y.Q. et al. (2011) A structural model for binding of the serine-rich repeat adhesin GspB to host carbohydrate receptors. PLoS Pathog 7: e1002112.
31. Ramboarina, S., Garnett, J.A., Zhou, M. et al. (2010) Structural insights into serine-rich fimbriae from Gram-positive bacteria. J Biol Chem 285: 32446-32457.
32. Rigel, N.W. and Braunstein, M. (2008) A new twist on an old pathway - accessory Sec systems. Mol Microbiol 69: 291-302.
33. Rose, L., Shivshankar, P., Hinojosa, E., Rodriguez, A., Sanchez, C.J. and Orihuela, C.J. (2008) Antibodies against PsrP, a novel Streptococcus pneumoniae adhesin, block adhesion and protect mice against pneumococcal challenge. J Infect Dis 198: 375-383.
34. Samen, U., Eikmanns, B.J., Reinscheid, D.J. and Borges, F. (2007) The surface protein Srr-1 of Streptococcus agalactiae binds human keratin 4 and promotes adherence to epithelial HEp-2 cells. Infect Immun 75: 5405-5414.
35. Sanchez, C.J., Shivshankar, P., Stol, K. et al. (2010) The pneumococcal serine-rich repeat protein is an intra-species bacterial adhesin that promotes bacterial aggregation in vivo and in biofilms. PLoS Pathog 6: e1001044.
36. Sanchez, C.J., Hurtgen, B.J., Lizcano, A., Shivshankar, P., Cole, G.T. and Orihuela, C.J. (2011a) Biofilm and planktonic pneumococci demonstrate disparate immunoreactivity to human convalescent sera. BMC Microbiol 11: 245.
37. Sanchez, C.J., Kumar, N., Lizcano, A. et al. (2011b) Streptococcus pneumoniae in biofilms are unable to cause invasive disease due to altered virulence determinant production. PLoS ONE 6: e28738.
38. Seepersaud, R., Bensing, B.A., Yen, Y.T. and Sullam, P.M. (2010) Asp3 mediates multiple protein-protein interactions within the accessory Sec system of Streptococcus gordonii. Mol Microbiol 78: 490-505.
39. Seifert, K.N., Adderson, E.E., Whiting, A.A., Bohnsack, J.F., Crowley, P.J. and 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. Microbiology 152: 1029-1040.
40. Shivshankar, P., Sanchez, C., Rose, L.F. and Orihuela, C.J. (2009) The Streptococcus pneumoniae adhesin PsrP binds to keratin 10 on lung cells. Mol Microbiol 73: 663-679.
41. Shivshankar, P., Boyd, A.R., Le Saux, C.J., Yeh, I.T. and Orihuela, C.J. (2011) Cellular senescence increases expression of bacterial ligands in the lungs and is positively correlated with increased susceptibility to pneumococcal pneumonia. Aging Cell 10: 798-806.
42. Siboo, I.R., Chambers, H.F. and Sullam, P.M. (2005) Role of SraP, a Serine-Rich Surface Protein of Staphylococcus aureus, in binding to human platelets. Infect Immun 73: 2273-2280.
43. Siboo, I.R., Chaffin, D.O., Rubens, C.E. and Sullam, P.M. (2008) Characterization of the accessory Sec system of Staphylococcus aureus. J Bacteriol 190: 6188-6196.
44. van Sorge, N.M., Quach, D., Gurney, M.A., Sullam, P.M., Nizet, V. and Doran, K.S. (2009) The Group B Streptococcal serine-rich repeat 1 glycoprotein mediates penetration of the blood-brain barrier. J Infect Dis 199: 1479-1487.
45. Stephenson, A.E., Wu, H., Novak, J., Tomana, M., Mintz, K. and 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 Microbiol 43: 147-157.
46. Sundaresan, R., Samen, U. and Ponnuraj, K. (2011) Expression, purification, crystallization and preliminary X-ray diffraction studies of the human keratin 4-binding domain of serine-rich repeat protein 1 from Streptococcus agalactiae. Acta Crystallogr Sect F Struct Biol Cryst Commun 67: 1582-1585.
47. Takahashi, Y., Konishi, K., Cisar, J.O. and Yoshikawa, M. (2002) Identification and characterization of hsa, the gene encoding the sialic acid-binding adhesin of Streptococcus gordonii DL1. Infect Immun 70: 1209-1218.
48. Takahashi, Y., Yajima, A., Cisar, J.O. and Konishi, K. (2004) Functional analysis of the Streptococcus gordonii DL1 sialic acid-binding adhesin and its essential role in bacterial binding to platelets. Infect Immun 72: 3876-3882.
49. Takamatsu, D., Bensing, B.A. and Sullam, P.M. (2004a) 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.
50. Takamatsu, D., Bensing, B.A. and Sullam, P.M. (2004b) Genes in the accessory sec locus of Streptococcus gordonii have three functionally distinct effects on the expression of the platelet-binding protein GspB. Mol Microbiol 52: 189-203.
51. Takamatsu, D., Bensing, B.A., Cheng, H. et al. (2005a) Binding of the Streptococcus gordonii surface glycoproteins GspB and Hsa to specific carbohydrate structures on platelet membrane glycoprotein Ibalpha. Mol Microbiol 58: 380-392.
52. Takamatsu, D., Bensing, B.A. and Sullam, P.M. (2005b) Two additional components of the accessory sec system mediating export of the Streptococcus gordonii platelet-binding protein GspB. J Bacteriol 187: 3878-3883.
53. Takamatsu, D., Bensing, B.A., Prakobphol, A., Fisher, S.J. and Sullam, P.M. (2006) Binding of the streptococcal surface glycoproteins GspB and Hsa to human salivary proteins. Infect Immun 74: 1933-1940.
54. Takeuchi, F., Watanabe, S., Baba, T. et al. (2005) Whole-genome sequencing of staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol 187: 7292-7308.
55. Tanaka, Y., Sakamoto, S., Kuroda, M. et al. (2008) A helical string of alternately connected three-helix bundles for the cell wall-associated adhesion protein Ebh from Staphylococcus aureus. Structure 16: 488-496.
56. Tettelin, H., Nelson, K.E., Paulsen, I.T. et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498-506.
57. Tsuji, T., Aoshiba, K. and Nagai, A. (2010) Alveolar cell senescence exacerbates pulmonary inflammation in patients with chronic obstructive pulmonary disease. Respiration 80: 59-70.
58. Vickerman, M.M., Iobst, S., Jesionowski, A.M. and Gill, S.R. (2007) Genome-wide transcriptional changes in Streptococcus gordonii in response to competence signaling peptide. J Bacteriol 189: 7799-7807.
59. Wu, H. and 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 Microbiol 34: 1070-1081.
60. Wu, H., Mintz, K.P., Ladha, M. and Fives-Taylor, P.M. (1998) Isolation and characterization of Fap1, a fimbriae-associated adhesin of Streptococcus parasanguis FW213. Mol Microbiol 28: 487-500.
61. Wu, H., Bu, S., Newell, P., Chen, Q. and Fives-Taylor, P. (2007a) Two gene determinants are differentially involved in the biogenesis of Fap1 precursors in Streptococcus parasanguis. J Bacteriol 189: 1390-1398.
62. Wu, H., Zeng, M. and 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 Immun 75: 2181-2188.
63. Xiong, Y.Q., Bensing, B.A., Bayer, A.S., Chambers, H.F. and Sullam, P.M. (2008) Role of the serine-rich surface glycoprotein GspB of Streptococcus gordonii in the pathogenesis of infective endocarditis. Microb Pathog 45: 297-301.
64. Xu, P., Alves, J.M., Kitten, T. et al. (2007) Genome of the opportunistic pathogen Streptococcus sanguinis. J Bacteriol 189: 3166-3175.
65. Yen, Y.T., Seepersaud, R., Bensing, B.A. and Sullam, P.M. (2011) Asp2 and Asp3 interact directly with GspB, the export substrate of the Streptococcus gordonii accessory Sec System. J Bacteriol 193: 3165-3174.
66. Zhang, Y.Q., Ren, S.X., Li, H.L. et al. (2003) Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol 49: 1577-1593.
67. Zhou, M. and Wu, H. (2009) Glycosylation and biogenesis of a family of serine-rich bacterial adhesins. Microbiology 155: 317-327.
68. Zhou, M., Peng, Z., Fives-Taylor, P. and Wu, H. (2008) A conserved C-terminal 13-amino-acid motif of Gap1 is required for Gap1 function and necessary for the biogenesis of a serine-rich glycoprotein of Streptococcus parasanguinis. Infect Immun 76: 5624-5631.
69. Zhou, M., Zhu, F., Dong, S., Pritchard, D.G. and Wu, H. (2010) A novel glucosyltransferase is required for glycosylation of a serine-rich adhesin and biofilm formation by Streptococcus parasanguinis. J Biol Chem 285: 12140-12148.
70. Zhou, M., Zhang, H., Zhu, F. and Wu, H. (2011) Canonical SecA associates with an accessory secretory protein complex involved in biogenesis of a streptococcal serine-rich repeat glycoprotein. J Bacteriol 193: 6560-6566.
71. Zhou, M., Zhu, F., Li, Y., Zhang, H. and Wu, H. (2012) Gap1 functions as a molecular chaperone to stabilize its interactive partner Gap3 during biogenesis of serine-rich repeat bacterial adhesin. Mol Microbiol 83: 866-878.
72. Zhu, F., Erlandsen, H., Ding, L. et al. (2011) Structural and functional analysis of a new subfamily of glycosyltransferases required for glycosylation of serine-rich streptococcal adhesins. J Biol Chem 286: 27048-27057.