1887

Abstract

SpeB is a cysteine proteinase and virulence determinant secreted by the important human pathogen . Recent investigations have suggested a role for SpeB in streptococcal entry into human cells. However, conflicting data concerning the contribution of SpeB to internalization have been presented. Protein F1 is a cell-wall-attached fibronectin (Fn)-binding protein that is present in a majority of streptococcal isolates and is important for internalization. This study shows that protein F1 is efficiently degraded by SpeB, and that removal of protein F1 from the bacterial surface leads to reduced internalization. Whereas M1 protein and protein H, two additional surface proteins of that bind human plasma proteins, are protected from proteolytic degradation by their ligands, protein F1 is readily cleaved by SpeB also when in complex with Fn. This finding, and the connection between the presence of Fn at the bacterial surface and entry into human cells, suggest that SpeB plays a role in the regulation of the internalization process.

Keyword(s): Fn, fibronectin
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27076-0
2004-05-01
2020-06-02
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/5/mic1501559.html?itemId=/content/journal/micro/10.1099/mic.0.27076-0&mimeType=html&fmt=ahah

References

  1. Abraham S. N., Beachey E. H., Simpson W. A.. 1983; Adherence of Streptococcus pyogenes, Escherichia coli, and Pseudomonas aeruginosa to fibronectin-coated and uncoated epithelial cells. Infect Immun41:1261–1268
    [Google Scholar]
  2. Åkesson P., Cooney J., Kishimoto F., Bjorck L.. 1990; Protein H – a novel IgG binding bacterial protein. Mol Immunol27:523–531[CrossRef]
    [Google Scholar]
  3. Åkesson P., Schmidt K. H., Cooney J., Björck L.. 1994; M1 protein and protein H: IgGFc- and albumin-binding streptococcal surface proteins encoded by adjacent genes. Biochem J300:877–886
    [Google Scholar]
  4. Berge A., Björck L.. 1995; Streptococcal cysteine proteinase releases biologically active fragments of streptococcal surface proteins. J Biol Chem270:9862–9867[CrossRef]
    [Google Scholar]
  5. Berry A. M., Paton J. C.. 1996; Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect Immun64:5255–5262
    [Google Scholar]
  6. Bohach G. A., Hauser A. R., Schlievert P. M.. 1988; Cloning of the gene, speB, for streptococcal pyrogenic exotoxin type B in Escherichia coli. Infect Immun56:1665–1667
    [Google Scholar]
  7. Burns E. H. Jr, Marciel A. M., Musser J. M.. 1996; Activation of a 66-kilodalton human endothelial cell matrix metalloprotease by Streptococcus pyogenes extracellular cysteine protease. Infect Immun64:4744–4750
    [Google Scholar]
  8. Burns E. H. Jr, Lukomski S., Rurangirwa J., Podbielski A., Musser J. M.. 1998; Genetic inactivation of the extracellular cysteine protease enhances in vitro internalization of group A streptococci by human epithelial and endothelial cells. Microb Pathog24:333–339[CrossRef]
    [Google Scholar]
  9. Bustin M., Lin M. C., Stein W. H., Moore S.. 1970; Activity of the reduced zymogen of streptococcal proteinase. J Biol Chem245:846–849
    [Google Scholar]
  10. Chaussee M. S., Phillips E. R., Ferretti J. J.. 1997; Temporal production of streptococcal erythrogenic toxin B (streptococcal cysteine proteinase) in response to nutrient depletion. Infect Immun65:1956–1959
    [Google Scholar]
  11. Chaussee M. S., Cole R. L., van Putten J. P.. 2000; Streptococcal erythrogenic toxin B abrogates fibronectin-dependent internalization of Streptococcus pyogenes by cultured mammalian cells. Infect Immun68:3226–3232[CrossRef]
    [Google Scholar]
  12. Collin M., Olsén A.. 2000; Generation of a mature streptococcal cysteine proteinase is dependent on cell wall-anchored M1 protein. Mol Microbiol36:1306–1318
    [Google Scholar]
  13. Collin M., Olsén A.. 2001a; Effect of SpeB and EndoS from Streptococcus pyogenes on human immunoglobulins. Infect Immun69:7187–7189[CrossRef]
    [Google Scholar]
  14. Collin M., Olsén A.. 2001b; EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J20:3046–3055[CrossRef]
    [Google Scholar]
  15. Courtney H. S., Li Y., Dale J. B., Hasty D. L.. 1994; Cloning, sequencing, and expression of a fibronectin/fibrinogen-binding protein from group A streptococci. Infect Immun62:3937–3946
    [Google Scholar]
  16. Courtney H. S., Hasty D. L., Li Y., Chiang H. C., Thacker J. L., Dale J. B.. 1999; Serum opacity factor is a major fibronectin-binding protein and a virulence determinant of M type 2 Streptococcus pyogenes. Mol Microbiol32:89–98[CrossRef]
    [Google Scholar]
  17. Courtney H. S., Hasty D. L., Dale J. B.. 2002; Molecular mechanisms of adhesion, colonization, and invasion of group A streptococci. Ann Med34:77–87[CrossRef]
    [Google Scholar]
  18. Cue D., Dombek P. E., Lam H., Cleary P. P.. 1998; Streptococcus pyogenes serotype M1 encodes multiple pathways for entry into human epithelial cells. Infect Immun66:4593–4601
    [Google Scholar]
  19. Cue D., Southern S. O., Southern P. J., Prabhakar J., Lorelli W., Smallheer J. M., Mousa S. A., Cleary P. P.. 2000; A nonpeptide integrin antagonist can inhibit epithelial cell ingestion of Streptococcus pyogenes by blocking formation of integrin α5β1-fibronectin-M1 protein complexes. Proc Natl Acad Sci U S A97:2858–2863[CrossRef]
    [Google Scholar]
  20. Cunningham M. W.. 2000; Pathogenesis of group A streptococcal infections. Clin Microbiol Rev13:470–511[CrossRef]
    [Google Scholar]
  21. Dinkla K., Rohde M., Jansen W. T., Carapetis J. R., Chhatwal G. S., Talay S. R.. 2003; Streptococcus pyogenes recruits collagen via surface-bound fibronectin: a novel colonization and immune evasion mechanism. Mol Microbiol47:861–869[CrossRef]
    [Google Scholar]
  22. Doran J. D., Nomizu M., Takebe S., Menard R., Griffith D., Ziomek E.. 1999; Autocatalytic processing of the streptococcal cysteine protease zymogen: processing mechanism and characterization of the autoproteolytic cleavage sites. Eur J Biochem263:145–151[CrossRef]
    [Google Scholar]
  23. Frick I. M., Crossin K. L., Edelman G. M., Björck L.. 1995; Protein H – a bacterial surface protein with affinity for both immunoglobulin and fibronectin type III domains. EMBO J14:1674–1679
    [Google Scholar]
  24. Gerlach D., Knoll H., Kohler W., Ozegowski J. H., Hribalova V.. 1983; Isolation and characterization of erythrogenic toxins. V. Communication: identity of erythrogenic toxin type B and streptococcal proteinase precursor. Zentbl Bakteriol Mikrobiol Hyg A255:221–233
    [Google Scholar]
  25. Goodfellow A. M., Hibble M., Talay S. R., Kreikemeyer B., Currie B. J., Sriprakash K. S., Chhatwal G. S.. 2000; Distribution and antigenicity of fibronectin binding proteins (SfbI and SfbII) of Streptococcus pyogenes clinical isolates from the Northern Territory, Australia. J Clin Microbiol38:389–392
    [Google Scholar]
  26. Hanski E., Caparon M.. 1992; Protein F, a fibronectin-binding protein, is an adhesin of the group A streptococcus Streptococcus pyogenes. Proc Natl Acad Sci U S A89:6172–6176[CrossRef]
    [Google Scholar]
  27. Herwald H., Collin M., Müller-Esterl W., Björck L.. 1996; Streptococcal cysteine proteinase releases kinins: a novel virulence mechanism. J Exp Med184:665–673[CrossRef]
    [Google Scholar]
  28. Jadoun J., Burstein E., Hanski E., Sela S.. 1997; Proteins M6 and F1 are required for efficient invasion of group A streptococci into cultured epithelial cells. Adv Exp Med Biol418:511–515
    [Google Scholar]
  29. Jadoun J., Ozeri V., Burstein E., Skutelsky E., Hanski E., Sela S.. 1998; Protein F1 is required for efficient entry of Streptococcus pyogenes into epithelial cells. J Infect Dis178:147–158[CrossRef]
    [Google Scholar]
  30. Jadoun J., Eyal O., Sela S.. 2002; Role of CsrR, hyaluronic acid, and SpeB in the internalization of Streptococcus pyogenes M type 3 strain by epithelial cells. Infect Immun70:462–469[CrossRef]
    [Google Scholar]
  31. Jaffe J., Natanson-Yaron S., Caparon M. G., Hanski E.. 1996; Protein F2, a novel fibronectin-binding protein from Streptococcus pyogenes, possesses two binding domains. Mol Microbiol21:373–384[CrossRef]
    [Google Scholar]
  32. Kantor F. S.. 1965; Fibrinogen precipitation by streptococcal M protein. J Exp Med121:849–859[CrossRef]
    [Google Scholar]
  33. Kapur V., Majesky M. W., Li L. L., Black R. A., Musser J. M.. 1993a; Cleavage of interleukin 1β (IL-1β) precursor to produce active IL-1β by a conserved extracellular cysteine protease from Streptococcus pyogenes. Proc Natl Acad Sci U S A90:7676–7680[CrossRef]
    [Google Scholar]
  34. Kapur V., Topouzis S., Majesky M. W., Li L. L., Hamrick M. R., Hamill R. J., Patti J. M., Musser J. M.. 1993b; A conserved Streptococcus pyogenes extracellular cysteine protease cleaves human fibronectin and degrades vitronectin. Microb Pathog15:327–346[CrossRef]
    [Google Scholar]
  35. Katerov V., Andreev A. A., Schalén C., Totolian A.. 1998; Protein F, a fibronectin-binding protein of Streptococcus pyogenes, also binds human fibrinogen: isolation of the protein and mapping of the binding region. Microbiology144:119–126[CrossRef]
    [Google Scholar]
  36. Kihlberg B. M., Collin M., Olsén A., Björck L.. 1999; Protein H, an antiphagocytic surface protein in Streptococcus pyogenes. Infect Immun67:1708–1714
    [Google Scholar]
  37. LaPenta D., Rubens C., Chi E., Cleary P. P.. 1994; Group A streptococci efficiently invade human respiratory epithelial cells. Proc Natl Acad Sci U S A91:12115–12119[CrossRef]
    [Google Scholar]
  38. Matsuka Y. V., Pillai S., Gubba S., Musser J. M., Olmsted S. B.. 1999; Fibrinogen cleavage by the Streptococcus pyogenes extracellular cysteine protease and generation of antibodies that inhibit enzyme proteolytic activity. Infect Immun67:4326–4333
    [Google Scholar]
  39. McElroy M. C., Cain D. J., Tyrrell C., Foster T. J., Haslett C.. 2002; Increased virulence of a fibronectin-binding protein mutant of Staphylococcus aureus in a rat model of pneumonia. Infect Immun70:3865–3873[CrossRef]
    [Google Scholar]
  40. Molinari G., Chhatwal G. S.. 1998; Invasion and survival of Streptococcus pyogenes in eukaryotic cells correlates with the source of the clinical isolates. J Infect Dis177:1600–1607[CrossRef]
    [Google Scholar]
  41. Molinari G., Talay S. R., Valentin-Weigand P., Rohde M., Chhatwal G. S.. 1997; The fibronectin-binding protein of Streptococcus pyogenes, SfbI, is involved in the internalization of group A streptococci by epithelial cells. Infect Immun65:1357–1363
    [Google Scholar]
  42. Molinari G., Rohde M., Guzman C. A., Chhatwal G. S.. 2000; Two distinct pathways for the invasion of Streptococcus pyogenes in non-phagocytic cells. Cell Microbiol2:145–154[CrossRef]
    [Google Scholar]
  43. Natanson S., Sela S., Moses A. E., Musser J. M., Caparon M. G., Hanski E.. 1995; Distribution of fibronectin-binding proteins among group A streptococci of different M types. J Infect Dis171:871–878[CrossRef]
    [Google Scholar]
  44. Nesbitt S. A., Horton M. A.. 1992; A nonradioactive biochemical characterization of membrane proteins using enhanced chemiluminescence. Anal Biochem206:267–272[CrossRef]
    [Google Scholar]
  45. Okada N., Tatsuno I., Hanski E., Caparon M., Sasakawa C.. 1998; Streptococcus pyogenes protein F promotes invasion of HeLa cells. Microbiology144:3079–3086[CrossRef]
    [Google Scholar]
  46. Ozeri V., Tovi A., Burstein I., Natanson-Yaron S., Caparon M. G., Yamada K. M., Akiyama S. K., Vlodavsky I., Hanski E.. 1996; A two-domain mechanism for group A streptococcal adherence through protein F to the extracellular matrix. EMBO J15:989–998
    [Google Scholar]
  47. Ozeri V., Rosenshine I., Mosher D. F., Fassler R., Hanski E.. 1998; Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol Microbiol30:625–637[CrossRef]
    [Google Scholar]
  48. Pancholi V., Fischetti V. A.. 1992; A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J Exp Med176:415–426[CrossRef]
    [Google Scholar]
  49. Raeder R., Woischnik M., Podbielski A., Boyle M. D.. 1998; A secreted streptococcal cysteine protease can cleave a surface-expressed M1 protein and alter the immunoglobulin binding properties. Res Microbiol149:539–548[CrossRef]
    [Google Scholar]
  50. Rasmussen M., Björck L. 2001; Unique regulation of SclB – a novel collagen-like surface protein of Streptococcus pyogenes. Mol Microbiol40:1427–1438[CrossRef]
    [Google Scholar]
  51. Rasmussen M., Björck L. 2002; Proteolysis and its regulation at the surface of Streptococcus pyogenes. Mol Microbiol43:537–544[CrossRef]
    [Google Scholar]
  52. Rasmussen M., Müller H. P., Björck L.. 1999; Protein GRAB of Streptococcus pyogenes regulates proteolysis at the bacterial surface by binding α2-macroglobulin. J Biol Chem274:15336–15344[CrossRef]
    [Google Scholar]
  53. 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 Microbiol37:1318–1326[CrossRef]
    [Google Scholar]
  54. Rocha C. L., Fischetti V. A.. 1999; Identification and characterization of a novel fibronectin-binding protein on the surface of group A streptococci. Infect Immun67:2720–2728
    [Google Scholar]
  55. Schmidt K. H., Mann K., Cooney J., Köhler W.. 1993; Multiple binding of type 3 streptococcal M protein to human fibrinogen, albumin and fibronectin. FEMS Immunol Med Microbiol7:135–143[CrossRef]
    [Google Scholar]
  56. Schwarz-Linek U., Werner J. M., Pickford A. R..7 other authors 2003; Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature423:177–181[CrossRef]
    [Google Scholar]
  57. Scott J. R., Guenther P. C., Malone L. M., Fischetti V. A.. 1986; Conversion of an M group A streptococcus to M+ by transfer of a plasmid containing an M6 gene. J Exp Med164:1641–1651[CrossRef]
    [Google Scholar]
  58. Sela S., Aviv A., Tovi A., Burstein I., Caparon M. G., Hanski E.. 1993; Protein F: an adhesin of Streptococcus pyogenes binds fibronectin via two distinct domains. Mol Microbiol10:1049–1055[CrossRef]
    [Google Scholar]
  59. Talay S. R., Valentin-Weigand P., Jerlström P. G., Timmis K. N., Chhatwal G. S.. 1992; Fibronectin-binding protein of Streptococcus pyogenes: sequence of the binding domain involved in adherence of streptococci to epithelial cells. Infect Immun60:3837–3844
    [Google Scholar]
  60. Talay S. R., Zock A., Rohde M., Molinari G., Oggioni M., Pozzi G., Guzman C. A., Chhatwal G. S.. 2000; Co-operative binding of human fibronectin to Sfbl protein triggers streptococcal invasion into respiratory epithelial cells. Cell Microbiol2:521–535[CrossRef]
    [Google Scholar]
  61. Terao Y., Kawabata S., Kunitomo E., Murakami J., Nakagawa I., Hamada S.. 2001; Fba, a novel fibronectin-binding protein from Streptococcus pyogenes, promotes bacterial entry into epithelial cells, and the fba gene is positively transcribed under the Mga regulator. Mol Microbiol42:75–86
    [Google Scholar]
  62. Terao Y., Kawabata S., Nakata M., Nakagawa I., Hamada S.. 2002; Molecular characterization of a novel fibronectin-binding protein of Streptococcus pyogenes strains isolated from toxic shock-like syndrome patients. J Biol Chem277:47428–47435[CrossRef]
    [Google Scholar]
  63. Tsai P. J., Kuo C. F., Lin K. Y., Lin Y. S., Lei H. Y., Chen F. F., Wang J. R., Wu J. J.. 1998; Effect of group A streptococcal cysteine protease on invasion of epithelial cells. Infect Immun66:1460–1466
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27076-0
Loading
/content/journal/micro/10.1099/mic.0.27076-0
Loading

Data & Media loading...

Most cited this month 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