SpeB modulates fibronectin-dependent internalization of Streptococcus pyogenes by efficient proteolysis of cell-wall-anchored protein F1

Microbiology

Volumn 150, Issue 5, 2004, Pages 1559-1569

  Nyberg, Patrik ^a   Rasmussen, Magnus ^a,b   von Pawel Rammingen, Ulrich ^a   Björck, Lars ^a  

^a LUND UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYSTEINE PROTEINASE; LIGAND; PROTEIN F1; PROTEIN H; PROTEIN M1; PROTEIN SPEB; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL MEMBRANE; CELL TRANSPORT; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME SUBSTRATE COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; PLASMA PROTEIN BINDING; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; STREPTOCOCCUS PYOGENES;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS PYOGENES;

EID: 2942618331     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.27076-0     Document Type: Article

References (63)

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 Immun 41, 1261-1268.
2. Åkesson, P., Cooney, J., Kishimoto, F. & Bjorck, L. (1990). Protein H - a novel IgG binding bacterial protein. Mol Immunol 27, 523-531.
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 1300, 877-886.
4. Berge, A. & Björck, L. (1995). Streptococcal cysteine proteinase releases biologically active fragments of streptococcal surface proteins. J Biol Chem 270, 9862-9867.
5. Berry, A. M. & Paton, J. C. (1996). Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect Immun 64, 5255-5262.
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 Immun 56, 1665-1667.
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 Immun 64, 4744-4750.
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 Pathog 24, 333-339.
9. Bustin, M., Lin, M. C., Stein, W. H. & Moore, S. (1970). Activity of the reduced zymogen of streptococcal proteinase. J Biol Chem 245, 846-849.
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 Immun 65, 1956-1959.
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 Immun 68, 3226-3232.
12. Collin, M. & Olsén, A. (2000). Generation of a mature streptococcal cysteine proteinase is dependent on cell wall-anchored M1 protein. Mol Microbiol 36, 1306-1318.
13. Collin, M. & Olsén, A. (2001a). Effect of SpeB and EndoS from Streptococcus pyogenes on human immunoglobulins. Infect Immun 69, 7187-7189.
14. Collin, M. & Olsén, A. (2001b). EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J 20, 3046-3055.
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 Immun 62, 3937-3946.
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 Microbiol 32, 89-98.
17. Courtney, H. S., Hasty, D. L. & Dale, J. B. (2002). Molecular mechanisms of adhesion, colonization, and invasion of group A streptococci. Ann Med 34, 77-87.
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 Immun 66, 4593-4601.
19. 1-fibronectin-M1 protein complexes. Proc Natl Acad Sci U S A 97, 2858-2863.
20. Cunningham, M. W. (2000). Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13, 470-511.
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 Microbiol 47, 861-869.
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 Biochem 263, 145-151.
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 J 14, 1674-1679.
24. Gerlach, D., Knoll, H., Kohler, W., Ozegowski, J. H. & Hribalova, V. (1983). Isolation and characterization of erythrogenic toxins. V. Communication: identity of crythrogenic toxin type B and streptococcal proteinase precursor. Zentbl Bakteriol Mikrobiol Hyg A 255, 221-233.
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 Microbiol 38, 389-392.
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 A 89, 6172-6176.
27. Herwald, H., Collin, M., Müller-Esterl, W. & Björck, L. (1996). Streptococcal cysteine proteinase releases kinins: a novel virulence mechanism. J Exp Med 184, 665-673.
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 Biol 418, 511-515.
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 Dis 178, 147-158.
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 Immun 70, 462-469.
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 Microbiol 21, 373-384.
32. Kantor, F. S. (1965). Fibrinogen precipitation by streptococcal M protein. J Exp Med 121, 849-859.
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 A 90, 7676-7680.
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 Pathog 15, 327-346.
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. Microbiology 144, 119-126.
36. Kihlberg, B. M., Collin, M., Olsén, A. & Björck, L. (1999). Protein H, an antiphagocytic surface protein in Streptococcus pyogenes. Infect Immun 67, 1708-1714.
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 A 91, 12115-12119.
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 Immun 67, 4326-4333.
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 Immun 70, 3865-3873.
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 Dis 177, 1600-1607.
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 Immun 65, 1357-1363.
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 Microbiol 2, 145-154.
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 Dis 171, 871-878.
44. Nesbitt, S. A. & Horton, M. A. (1992). A nonradioactive biochemical characterization of membrane proteins using enhanced chemiluminescence. Anal Biochem 206, 267-272.
45. Okada, N., Tatsuno, I., Hanski, E., Caparon, M. & Sasakawa, C. (1998). Streptococcus pyogenes protein F promotes invasion of HeLa cells. Microbiology 144, 3079-3086.
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 J 15, 989-998.
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 Microbiol 30, 625-637.
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 Med 176, 415-426.
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 Microbiol 149, 539-548.
50. Rasmussen, M. & Björck, L. (2001). Unique regulation of SclB - a novel collagen-like surface protein of Streptococcus pyogenes. Mol Microbiol 40, 1427-1438.
51. Rasmussen, M. & Björck, L. (2002). Proteolysis and its regulation at the surface of Streptococcus pyogenes. Mol Microbiol 43, 537544.
52. 2,-macroglobulin. J Biol Chem 274, 15336-15344.
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 Microbiol 37, 1318-1326.
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 lmmun 67, 2720-2728.
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 Microbiol 7, 135-143.
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. Nature 423, 177-181.
57. + by transfer of a plasmid containing an M6 gene. J Exp Med 164, 1641-1651.
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 Microbiol 10, 1049-1055.
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 Immun 60, 3837-3844.
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 Microbiol 2, 521-535.
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 Microbiol 42, 75-86.
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 Chem 277, 47428-47435.
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 Immun 66, 1460-1466.