1887

Microbiology Society logo

Volume 155, Issue 8

Localization of the equine IgG-binding domain in the fibrinogen-binding protein (FgBP) of subsp. Free

Abstract

Fibrinogen-binding protein (FgBP, also termed SeM) is a cell-wall-associated anti-phagocytic M-like protein of the equine pathogen subsp. , and binds fibrinogen (Fg) and IgG. FgBP binds Fg avidly through residues located at the extreme N terminus of the molecule, whereas the IgG-binding site is more centrally located between the A and B repeats. FgBP binds equine IgG4 and IgG7 subclasses through interaction with the CH2–CH3 interdomain region of IgG-Fc, and possesses overlapping Fc-binding sites with protein A and protein G. In this study, FgBP truncates containing defined internal deletions were used to identify a stretch of 14 aa (residues 335–348) critical for IgG binding. Protein chimeras consisting of the non-IgG-binding -helical coiled-coil M5 protein fused to FgBP sequences were used to identify a minimal equine IgG-binding domain consisting of residues 329–360. Competition ELISA tests suggested that IgG does not compromise Fg binding and vice versa.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): eqFg, equine Fg , eqIgG, equine IgG , Fg, fibrinogen , FgBP, fibrinogen-binding protein and HRP, horseradish peroxidase
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.028845-0
2009-08-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/8/2583.html?itemId=/content/journal/micro/10.1099/mic.0.028845-0&mimeType=html&fmt=ahah

References

  1. Anzai T., Kuwamoto Y., Wada R., Sugita S., Kakuda T., Takai S., Higuchi T., Timoney J. F. 2005; Variation in the N-terminal region of an M-like protein of Streptococcus equi and evaluation of its potential as a tool in epidemiologic studies. Am J Vet Res 66:2167–2171
     [Google Scholar]
  2. Atkins K. L., Burman J. D., Chamberlain E. S., Cooper J. E., Poutrel B., Bagby S., Jenkins A. T., Feil E. J., van den Elsen J. M. H. 2008; S. aureus IgG-binding proteins SpA and Sbi: host specificity and mechanisms of immune complex formation. Mol Immunol 45:1600–1611
     [Google Scholar]
  3. Beres S. B., Sesso R., Pinto S. W. L., Hoe N. P., Porcella S. F., DeLeo F. R., Musser J. M. 2008; Genome sequence of a Lancefield group C Streptococcus zooepidemicus strain causing epidemic nephritis: new information about an old disease. PLoS One 3:e3026
     [Google Scholar]
  4. Bessen D. E., Izzo M. W., McCabe E. J., Sotir C. M. 1997; Two-domain motif for IgG-binding activity of group A streptococcal emm gene products. Gene 196:75–82
     [Google Scholar]
  5. Björck L., Kastern W., Lindahl G., Widebäck K. 1987; Streptococcal protein G, expressed by streptococci or by Escherichia coli, has separate binding sites for human albumin and IgG. Mol Immunol 24:1113–1122
     [Google Scholar]
  6. Boschwitz J. S., Timoney J. F. 1994a; Characterization of the antiphagocytic activity of equine fibrinogen for Streptococcus equi subsp. equi . Microb Pathog 17:121–129
     [Google Scholar]
  7. Boschwitz J. S., Timoney J. F. 1994b; Inhibition of C3 deposition on Streptococcus equi subsp. equi by M protein: a mechanism for survival in equine blood. Infect Immun 62:3515–3520
     [Google Scholar]
  8. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
     [Google Scholar]
  9. Burton D. R. 1985; Immunoglobulin G: functional sites. Mol Immunol 22:161–206
     [Google Scholar]
  10. Carlsson F., Berggård K., Stålhammer-Carlemalm M., Lindahl G. 2003; Evasion of phagocytosis through cooperation between two ligand-binding regions in Streptococcus pyogenes M protein. J Exp Med 198:1057–1068
     [Google Scholar]
  11. Chanter N., Talbot N. C., Newton J. R., Hewson D., Verheyen K. 2000; Streptococcus equi with truncated M-proteins isolated from outwardly healthy horses. Microbiology 146:1361–1369
     [Google Scholar]
  12. Dale J. B., Chiang E. Y., Liu S., Courtney H. S., Hasty D. L. 1999; New protective antigen of group A streptococci. J Clin Invest 103:1261–1268
     [Google Scholar]
  13. DeLano W. L., Ultsch M. H., de Vos A. M., Wells J. A. 2000; Convergent solutions to binding at a protein–protein interface. Science 287:1279–1283
     [Google Scholar]
  14. Flock M., Jacobsson K., Frykberg L., Hirst T. R., Franklin A., Guss B., Flock J. I. 2004; Recombinant Streptococcus equi proteins protect mice in challenge experiments and induce immune response in horses. Infect Immun 72:3228–3236
     [Google Scholar]
  15. Frick I.-M., Wikström M., Forsén S., Drakenberg T., Gomi H., Sjöbring U., Björck L. 1992; Convergent evolution among immunoglobulin G-binding bacterial proteins. Proc Natl Acad Sci U S A 89:8532–8536
     [Google Scholar]
  16. Goward C. R., Scawen M. D., Murphy J. P., Atkinson T. 1993; Molecular evolution of bacterial surface proteins. Trends Biochem Sci 18:136–140
     [Google Scholar]
  17. Harrington D. J., Sutcliff I. C., Chanter N. 2002; The molecular basis of Streptococcus equi infection and disease. Microbes Infect 4:501–510
     [Google Scholar]
  18. Heath D. G., Boyle M. D., Cleary P. P. 1990; Isolated DNA repeat region from fcrA76, the Fc-binding protein gene from an M-type 76 strain of group A streptococci, encodes a protein with Fc-binding activity. Mol Microbiol 4:2071–2079
     [Google Scholar]
  19. Johnsson E., Berggård K., Kotarsky H., Hellwage J., Zipfel P. F., Sjöbring U., Lindahl G. 1998; Role of the hypervariable region in streptococcal M proteins: binding of a human complement inhibitor. J Immunol 161:4894–4901
     [Google Scholar]
  20. Kelly C., Bugg M., Robinson C., Mitchell Z., Davis-Poynter N., Newton J. R., Jolley K. A., Maiden M. C. J., Waller A. S. 2006; Sequence variation of the SeM gene of Streptococcus equi allows discrimination of the source of strangles outbreak. J Clin Microbiol 44:480–486
     [Google Scholar]
  21. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
     [Google Scholar]
  22. Lewis M. J., Meehan M., Owen P., Woof J. M. 2008a; A common theme in interaction of bacterial immunoglobulin-binding proteins with immunoglobulins illustrated in the equine system. J Biol Chem 283:17615–17623
     [Google Scholar]
  23. Lewis M. J., Wagner B., Woof J. M. 2008b; The different effector function capabilities of the seven equine IgG subclasses have implications for vaccine strategies. Mol Immunol 45:818–827
     [Google Scholar]
  24. Lupas A. 1996; Prediction and analysis of coiled-coil structures. Methods Enzymol 266:513–525
     [Google Scholar]
  25. Lupas A., Van Dyke M., Stock J. 1991; Predicting coiled coils from protein sequences. Science 252:1162–1164
     [Google Scholar]
  26. Mason J. M., Arndt K. M. 2004; Coiled-coil domains: stability, specificity, and biological implications. ChemBioChem 5:170–176
     [Google Scholar]
  27. McLellan D. G. J., Chiang E. Y., Courtney H. S., Hasty D. L., Wei S. C., Hu M. C., Walls M. A., Bloom J. J., Dale J. B. 2001; Spa contributes to the virulence of type 18 group A streptococci. Infect Immun 69:2943–2949
     [Google Scholar]
  28. Meehan M., Nowlan P., Owen P. 1998; Affinity purification and characterization of a fibrinogen-binding protein complex which protects mice against lethal challenge with Streptococcus equi subsp. equi . Microbiology 144:993–1003
     [Google Scholar]
  29. Meehan M., Muldowney D. A., Watkins N. J., Owen P. 2000a; Localization and characterization of the ligand-binding domain of the fibrinogen-binding protein (FgBP) of Streptococcus equi subsp. equi . Microbiology 146:1187–1194
     [Google Scholar]
  30. Meehan M., Muldowney D. A., O'Meara F., Owen P. 2000b; Neither the A- nor B-repeat regions of the fibrinogen-binding protein of Streptococcus equi subsp. equi are essential for fibrinogen binding. FEMS Microbiol Lett 190:317–321
     [Google Scholar]
  31. Meehan M., Lynagh Y., Woods C., Owen P. 2001; The fibrinogen-binding protein (FgBP) of Streptococcus equi subsp. equi additionally binds IgG and contributes to virulence in a mouse model. Microbiology 147:3311–3322
     [Google Scholar]
  32. Meehan M., Kelly S. M., Price N. C., Owen P. 2002; The C-terminal portion of the fibrinogen-binding protein of Streptococcus equi subsp. equi contains extensive α-helical coiled-coil structure and contributes to thermal stability. FEMS Microbiol Lett 206:81–86
     [Google Scholar]
  33. Moks T., Abrahmsén L., Nilsson B., Hellman U., Sjöquist J., Uhlén M. 1986; Staphylococcal protein A consists of five IgG-binding domains. Eur J Biochem 156:637–643
     [Google Scholar]
  34. Navarre W. W., Schneewind O. 1999; Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174–229
     [Google Scholar]
  35. O'Toole P., Stenberg L., Rissler M., Lindahl G. 1992; Two major classes in the M protein family in group A streptococci. Proc Natl Acad Sci U S A 89:8661–8665
     [Google Scholar]
  36. Pack T. D., Podbielski A., Boyle M. D. 1996; Identification of an amino acid signature sequence predictive of protein G-inhibitable IgG3-binding activity in group-A streptococcal IgG-binding proteins. Gene 171:65–70
     [Google Scholar]
  37. Pleass R. J., Areschoug T., Lindahl G., Woof J. M. 2001; Streptococcal IgA-binding proteins bind in the C α2–C α3 interdomain region and inhibit binding of IgA to human CD89. J Biol Chem 276:8197–8204
     [Google Scholar]
  38. Ringdahl U., Svensson H. G., Kotarsky H., Gustafsson M., Weineisen M., Sjöbring U. 2000; A role for the fibrinogen-binding regions of streptococcal M proteins in phagocytosis resistance. Mol Microbiol 37:1318–1326
     [Google Scholar]
  39. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  40. Sauer-Eriksson A. E., Kleywegt G. J., Uhlén M., Jones T. A. 1995; Crystal structure of the C2 fragment of streptococcal protein G in complex with the Fc domain of human IgG. Structure 3:265–278
     [Google Scholar]
  41. Sheoran A. S., Sponseller B. T., Holmes M. A., Timoney J. F. 1997; Serum and mucosal antibody isotype response to M-like protein (SeM) of Streptococcus equi in convalescent and vaccinated horses. Vet Immunol Immunopathol 59:239–251
     [Google Scholar]
  42. Sloan D. J., Hellinga H. W. 1999; Dissection of the protein G B1 domain binding site for human IgG Fc fragment. Protein Sci 8:1643–1648
     [Google Scholar]
  43. Timoney J. F. 1993; Strangles. Vet Clin North Am Equine Pract 9:365–374
     [Google Scholar]
  44. Timoney J. F. 2004; The pathogenic equine streptococci. Vet Res 35:397–409
     [Google Scholar]
  45. Timoney J. F., Artiushin S. C., Boschwitz J. S. 1997; Comparison of the sequences and functions of Streptococcus equi M-like proteins SeM and SzPSe. Infect Immun 65:3600–3605
     [Google Scholar]
  46. Uhlén M., Guss B., Nilsson B., Gatenbeck S., Philipson L., Lindberg M. 1984; Complete sequence of the staphylococcal gene encoding protein A. A gene evolved through multiple duplications. J Biol Chem 259:1695–1702
     [Google Scholar]
  47. Vasi J., Frykberg L., Carlsson L. E., Lindberg M., Guss B. 2000; M-like proteins of Streptococcus dysgalactiae . Infect Immun 68:294–302
     [Google Scholar]
  48. Waller A. S., Jolley K. A. 2007; Getting a grip on strangles: recent progress towards improved diagnostics and vaccines. Vet J 173:492–501
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.028845-0
Loading
Localization of the equine IgG-binding domain in the fibrinogen-binding protein (FgBP) of Streptococcus equi subsp. equi
Microbiology 155, 2583 (2009); https://doi.org/10.1099/mic.0.028845-0
/content/journal/micro/10.1099/mic.0.028845-0
/content/journal/micro/10.1099/mic.0.028845-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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