The intracellular status of Streptococcus pyogenes: Role of extracellular matrix-binding proteins and their regulation

International Journal of Medical Microbiology

Volumn 294, Issue 2-3, 2004, Pages 177-188

  Kreikemeyer, Bernd ^a   Klenk, Michael ^a   Podbielski, Andreas ^a  

^a ROSTOCK UNIVERSITY MEDICAL CENTER   (Germany)

Author keywords

Extracellular matrix proteins; MSCRAMM; Persistence; Regulation; Streptococcus pyogenes

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL PROTEIN; COLLAGEN; FIBRONECTIN; INTEGRIN; PROTEIN F1 SFBI; SCLEROPROTEIN; UNCLASSIFIED DRUG;

BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM CARRIER; EXTRACELLULAR MATRIX; HOST RESISTANCE; INTERNALIZATION; NONHUMAN; PATHOGENICITY ISLAND; PROTEIN BINDING; PROTEIN EXPRESSION; RECURRENT INFECTION; REVIEW; SIGNAL TRANSDUCTION; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PYOGENES; TRANSCRIPTION REGULATION;

EID: 4644355088     PISSN: 14384221     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijmm.2004.06.017     Document Type: Review

References (91)

1. Adam, D., Scholz, H., Helmerking, M., 2000. Comparison of short-course (5 day) cefuroxime axetil with a standard 10 day oral penicillin V regimen in the treatment of tonsillopharyngitis. J. Antimicrob. Chemother. 45 (Suppl.), 23-30.
2. Barnett, T.C., Scott, J.R., 2002. Differential recognition of surface proteins in Streptococcus pyogenes by two sortase gene homologs. J. Bacteriol. 184, 2181-2191.
3. Beckert, S., Kreikemeyer, B., Podbielski, A., 2001. The group A streptococcal rofA gene is involved in the control of several virulence genes and eukaryotic cell attachment and internalization. Infect. Immun. 69, 534-537.
4. Beckmann, C., Waggoner, J.D., Harris, T.O., Tamura, G.S., Rubens, C.E., 2002. Identification of novel adhesins from group B streptococci by use of phage display reveals that C5a peptidase mediates fibronectin binding. Infect. Immun. 70, 2869-2876.
5. Beres, S.B., Sylva, G.L., Barbian, K.D., Lei, B., Hoff, J.S., Mammarella, N.D., Liu, M.Y., Smoot, J.C., Porcella, S.F., Parkins, L.D., Campbell, D.S., Smith, T.M., McCormick, J.K., Leung, D.Y., Schlievert, P.M., Musser, J.M., 2002. Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc. Natl. Acad. Sci. USA 99, 10078-10083.
6. Bessen, D.E., Kalia, A., 2002. Genomic localization of a T serotype locus to a recombinatorial zone encoding extracellular matrix-binding proteins in Streptococcus pyogenes. Infect. Immun. 70, 1159-1167.
7. Biswas, I., Scott, J.R., 2003. Identification of rocA, a positive regulator of covR expression in the group A Streptococcus. J. Bacteriol. 185, 3081-3090.
8. Brandt, C.M., Allerberger, F., Spellerberg, B., Holland, R., Lütticken, R., Haase, G., 2001. Characterization of consecutive Streptococcus pyogenes isolates from patients with pharyngitis and bacteriological treatment failure: special reference to prtF1 and sic/drs. J. Infect. Dis. 183, 670-674.
9. Cheng, Q., Stafslien, D., Purushothaman, S.S., Cleary, P., 2002. The group B streptococcal C5a peptidase is both a specific protease and an invasin. Infect. Immun. 70, 2408-2413.
10. Chhatwal, G.S., 2002. Anchorless adhesins and invasins of Gram-positive bacteria: a new class of virulence factors, Trends Microbiol. 10, 205-208.
11. Chhatwal, G.S., Lämmler, C., Blobel, H., 1985. Interactions of plasma proteins with group A, B, C and G streptococci. Zentralbl. Bakteriol. Mikrobiol. Hyg. [A] 259, 219-227.
12. Chhatwal, G.S., Valentin-Weigand, P., Timmis, K.N., 1990. Bacterial infection of wounds: fibronectin-mediated adherence group A and C streptococci to fibrin thrombi in vitro. Infect. Immun. 58, 3015-3019.
13. Courtney, H.S., Hasty, D.L., Dale, J.B., Poirier, T.P., 1992. A 28-kilodalton fibronectin-binding protein of group A streptococci. Curr. Microbiol. 25, 245-250.
14. 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. Immunology 62, 3937-3946.
15. 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.
16. Cue, D., Southern, S.O., Southern, P.J., Prabhakar, J., 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. USA 97, 2858-2863.
17. Cue, D., Lam, H., Cleary, P.P., 2001. Genetic dissection of the Streptococcus pyogenes MI protein: regions involved in fibronectin binding and intracellular invasion. Microb. Pathog. 31, 231-242.
18. Cunningham, M.W., 2000. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13, 470-511.
19. Cywes, C., Wessels, M.R., 2001. Group A Streptococcus tissue invasion by CD44-mediated cell signaling. Nature 414, 648-652.
20. Darmstadt, G., Mentele, L., Fleckman, P., Rubens, C.E., 1999. Role of keratinocyte injury in adherence of Streptococcus pyogenes. Infect. Immun. 67, 6707-6709.
21. DelVecchio, A., Currie, B.J., McArthur, J.D., Walker, M.J., Sriprakash, K.S., 2002. Streptococcus pyogenes prtFII, but not sfbI, sfblI or fbp54, is represented more frequently among invasive-disease isolates of tropical Australia. Epidemiol. Infect. 128, 391-396.
22. Dinkla, K., Rohde, M., Jansen, W.T.M., Kaplan, E.L., Chhatwal, G.S., Talay, S.R., 2003. Rheumatic fever-associated Streptococcus pyogenes isolates aggregate collagen. J. Clin. Invest. 111, 1905-1912.
23. Elsner, A., Kreikemeyer, B., Braun-Kiewnick, A., Spellerberg, B., Buttaro, B.A., Podbielski, A., 2002. Involvement of Lsp, a member of the LraI-lipoprotein family in Streptococcus pyogenes, in eukaryotic cell adhesion and internalization. Infect. Immun. 70, 4859-4869.
24. Ensenberger, M.G., Tomasini-Johansson, B.R., Sottile, J., Ozeri, V., Hanski, E., Mosher, D.F., 2001. Specific interactions between F1 adhesin of Streptococcus pyogenes and N-terminal modules of fibronectin. J. Biol. Chem. 276, 35606-35613.
25. Facinelli, B., Spinaci, C., Magi, G., Giovanetti, E., Varaldo, P.E., 2001. Association between erythromycin resistance and ability to enter human respiratory cells in group A streptococci. Lancet 358, 30-33.
26. Ferretti, J.J., McShan, W.M., Ajdic, D., Savic, D.J., Savic, G., Lyon, K., Primeaux, C., Sezate, S., Suvorov, A.N., Kenton, S., Lai, H.S., Lin, S.P., Qian, Y., Najar, F.Z., Ren, Q., Zhu, H., Song, L., White, J., Yuan, X., Clifton, S.W., Roe, B.A., McLaughlin, R., 2001. Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc. Natl. Acad. Sci. USA 98, 4658-4663.
27. Fiorentino, T.R., Beall, B., Mshar, P., Bessen, D.E., 1997. A genetic evaluation of the principal tissue reservoir for group A streptococci isolated from normally sterile sites. J. Infect. Dis. 176, 177-182.
28. Fogg, G.C., Gibson, C.M., Caparon, M.G., 1994. The identification of rofA, a positive-acting regulatory component of prtF expression: use of an m gamma delta-based shuttle mutagenesis strategy in Streptococcus pyogenes. Mol. Microbiol. 11, 671-684.
29. 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.
30. Granok, A.B., Parsonage, D., Ross, R.P., Caparon, M.G., 2000. The RofA binding site in Streptococcus pyogenes is utilized in multiple transcriptional pathways. J. Bacteriol. 182, 1529-1540.
31. 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. USA 89, 6172-6176.
32. Hidalgo-Grass, C., Ravins, M., Dan-Goor, M., Jaffe, J.J., Moses, A.E., Hanski, E., 2002. A locus of group A Streptococcus involved in invasive disease and DNA transfer. Mol. Microbiol. 46, 87-99.
33. House-Pompeo, K., Xu, Y., Joh, D., Speziale, P., Höök, M., 1996. Conformational changes in the fibronectin binding MSCRAMMs are induced by ligand binding. J. Biol. Chem. 271, 1379-1384.
34. Hytönen, J., Haataja, S., Gerlach, D., Podbielski, A., Finne, J., 2001. The SpeB virulence factor of Streptococcus pyogenes, a multifunctional secreted and cell surface molecule with strepadhesin, laminin-binding and cysteine protease activity. Mol. Microbiol. 39, 512-519.
35. Jadoun, J., Sela, S., 2000. Mutation in csrR global regulator reduces Streptococcus pyogenes internalization. Microb. Pathog. 29, 311-317.
36. 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.
37. Jeffery, C.J., 2003. Moonlighting proteins: old proteins learning new tricks. Trends Genet. 19, 415-417.
38. Jeng, A., Sakota, V., Li, Z., Datta, V., Beall, B., Nizet, V., 2003. Molecular genetic analysis of a group A Streptococcus operon encoding serum opacity factor and a novel fibronectin-binding protein, SfbX. J. Bacteriol. 185, 1208-1217.
39. Joh, H.J., House-Pompeo, K., Patti, J.M., Gurusiddappa, S., Höök, M., 1994. Fibronectin receptors from gram-positive bacteria: comparison of active sites. Biochemistry 33, 6086-6092.
40. Joh, D., Wann, E., Kreikemeyer, B., Speciale, P., Höök, M., 1999. Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol. 18, 211-223.
41. Kotb, M., Norrby-Teglund, A., McGeer, A., El-Sherbini, H., Dorak, M.T., Khurshid, A., Green, K., Peeples, J., Wade, J., Thomson, G., Schwartz, B., Low, D.E., 2002. An immunogenetic and molecular basis for differences in outcomes of invasive group A streptococcal infections. Nature Med. 8, 1398-1404.
42. Kreikemeyer, B., Talay, S.R., Chhatwal, G.S., 1995. Characterization of a novel fibronectin-binding surface protein in group A streptococci. Mol. Microbiol. 17, 137-145.
43. Kreikemeyer, B., Boyle, M.D.P., Buttaro, B.A., Heinemann, M., Podbielski, A., 2001. Group A streptococcal growth phase-associated virulence factor regulation by a novel operon (Fas) with homologies to two-component-type regulators requires a small RNA molecule. Mol. Microbiol. 39, 392-406.
44. Kreikemeyer, B., Beckert, S., Braun-Kiewnick, A., Podbielski, A., 2002. Group A streptococcal RofA-type global regulators exhibit a strain-specific genomic presence and regulation pattern. Microbiology (UK) 148, 1501-1511.
45. Kreikemeyer, B., McIver, K.S., Podbielski, A., 2003. Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen-host interactions. Trends Microbiol. 11, 224-232.
46. Kreikemeyer, B., Oehmcke, S., Nakata, M., Hoffrogge, R., Podbielski, A., 2004. Streotococcus pyogenes fibronectin-binding protein F2: expression profile, binding characteristics, and impact on eukaryotic cell interactions. J. Biol. Chem. 279, 15850-15859.
47. LaPenta, D., Rubens, C., Chi, E., Cleary, P.P., 1994. Group A streptococci efficiently invade human respiratory epithelial cells. Proc. Natl. Acad. Sci. USA 91, 12115-12119.
48. Ma, X., Kikuta, H., Ishiguro, N., Yoshioka, M., Ebihara, T., Murai, T., Kobayashi, I., Kobashi, K., 2002. Association of the prtF1 gene (encoding fibronectin-binding protein F1) and the sic gene (encoding the streptococcal inhibitor of complement) with emm types of group A streptococci isolated from Japanese children with pharyngitis. J. Clin. Microbiol. 40, 3835-3837.
49. Mazmanian, S.K., Ton-That, H., Schneewind, O., 2001. Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus. Mol. Microbiol. 40, 1049-1057.
50. 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.
51. 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.
52. Molinari, G., Rohde, M., Talay, S.R., Chhatwal, G.S., Beckert, S., Podbielski, A., 2001. Role played by the group A streptococcal negative regulator Nra on bacterial interactions with epithelial cells. Mol. Microbiol. 40, 99-114.
53. Myhre, E.B., Kuusela, P., 1983. Binding of human fibronectin to group A, C, and G streptococci. Infect. Immun. 40, 29-34.
54. Nakagawa, I., Nakata, M., Kawabata, S., Hamada, S., 2001. Cytochrome c-mediated caspase-9 activation triggers apoptosis in Streptococcuspyogenes- infected epithelial cells. Cell. Microbiol. 3, 395-405.
55. Nakagawa, I., Kurokawa, K., Yamashita, A., Nakata, M., Tomiyasu, Y., Okahashi, N., Kawabata, S., Yamazaki, K., Shiba, T., Yasunaga, T., Hayashi, H., Hattori, M., Hamada, S., 2003. Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution. Genome Res. 13, 1042-1055.
56. 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.
57. Neeman, R., Keller, N., Barzilai, A., Korenman, Z., Sela, S., 1998. Prevalence of internalization-associated gene, prtF1, among persisting group-A streptococcus strains isolated from asymptomatic carriers. Lancet 352, 1974-1977.
58. Österlund, A., Engstrand, L., 1997. An intracellular sanctuary for Streptococcus pyogenes in human tonsillar epithelium-studies of asymptomatic carriers and in vitro cultured biopsies. Acta Otolaryngol. 117, 883-888.
59. Österlund, A., Popa, R., Nikkilä, T., Scheynius, A., Engstrand, L., 1997. Intracellular reservoir of Streptococcus pyogenes in vivo: a possible explanation for recurrent pharyngotonsillitis. Laryngoscope 107, 640-647.
60. 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.
61. Ozeri, V., Rosenshine, I., Mosher, D.F., Fässler, 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.
62. Ozeri, V., Rosenshine, I., Ben-Ze'ev, A., Bokoch, G.M., Jou, T.S., Hanski, E., 2001. De novo formation of focal complex-like structures in host cells by invading streptococci. Mol. Microbiol. 41, 561-573.
63. Pancholi, V., Fischetti, V.A., 1992. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphatedehydrogenase with multiple binding activity. J. Exp. Med. 176, 415-426.
64. Patti, J.M., Allen, B.L., McGavin, M.J., Höök, M., 1994. MSCRAMM-mediated adherence of microorganisms to host tissue. Annu. Rev. Microbiol. 48, 585-617.
65. Podbielski, A., Kreikemeyer, B., 2001. Persistence of group A streptococci in eukaryotic cells - a safe place ?. Lancet 358, 3-4.
66. Podbielski, A., Krebs, B., Kaufhold, A., 1994. Genetic variability of the emm-related genes of the vir regulon of group A streptococci: potential intra- and intergenomic recombination events. Mol. Gen. Genet. 243, 691-698.
67. Podbielski, A., Woischnik, M., Pohl, B., Schmidt, K.H., 1996. What is the size of the group A streptococcal vir regulon? The Mga regulator affects expression of secreted and surface virulence factors. Med. Microbiol. Immunol. 185, 171-181.
68. Podbielski, A., Woischnik, M., Leonard, B.A., Schmidt, K.H., 1999. Characterization of nra, a global negative regulator gene in group A streptococci. Mol. Microbiol. 31, 1051-1064.
69. Podbielski, A., Beckert, S., Schattke, R., Leithäuser, F., Lestin, F., Goßler, B., Kreikemeyer, B., 2003. Epidemiology and virulence gene expression of intracellular group A streptococci in tonsils of recurrently infected adults. Int. J. Med. Microbiol. 293, 179-190.
70. Pritchard, K.H., Cleary, P.P., 1996. Differential expression of genes in the vir regulon of Streptococcus pyogenes is controlled by transcription termination. Mol. Gen. Genet. 250, 207-213.
71. Rakonjac, J.V., Robbins, J.C., Fischetti, V.A., 1995. DNA sequence of the serum opacity factor of group A streptococci: identification of a fibronectin-binding repeat domain. Infect. Immun. 63, 622-631.
72. Rocha, C.L., Fischetti, V.A., 1999. Identification and characterization of a novel fibronectin-binding protein on the surface of group A streptococci. Infect. Immunol. 67, 2720-2728.
73. Russell, R.R., Aduse-Opoku, J., Sutcliffe, I.C., Tao, L., Ferretti, J.J., 1992. A binding protein-dependent transport system in Streptococcus mutans responsible for multiple sugar metabolism. J. Biol. Chem. 267, 4631-4637.
74. Schmidt, K.H., Mann, K.H., Cooney, J., Köhler, W., 1993. Multiple binding of type 3 streptococcal M protein to human fibrinogen, albumin and fibronectin. FEMS Immunol. Med. Microbiol. 7, 135-144.
75. 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. Microbiology 10, 1049-1055.
76. Sela, S., Neeman, R., Keller, N., Barzilai, A., 2000. Relationship between asymptomatic carriage of Streptococcus pyogenes and the ability of the strains to adhere to and be internalised by cultured epithelial cells. J. Med. Microbiol. 49, 499-502.
77. Smoot, J.C., Barbian, K.D., Van Gompel, J.J., Smoot, L.M., Chaussee, M.S., Sylva, G.L., Sturdevant, D.E., Ricklefs, S.M., Porcella, S.F., Parkins, L.D., Beres, S.B., Campbell, D.S., Smith, T.M., Zhang, Q., Kapur, V., Daly, J.A., Veasy, L.G., Musser, J.M., 2002. Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc. Natl. Acad. Sci. USA 99, 4668-4673.
78. Stevens, D.L., 1994. Invasive group A streptococcal infections: the past, present and future. Pediatr. Infect. Dis. J. 13, 561-566.
79. Switalski, L.M., Ljungh, A., Ryden, C., Rubin, K., Höök, M., Wadström, T., 1982. Binding of fibronectin to the surface of group A, C, and G streptococci isolated from human infections. Eur. J. Clin. Microbiol. 1, 381-387.
80. 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.
81. Talay, S.R., Valentin-Weigand, P., Timmis, K.N., Chhatwal, G.S., 1994. Domain structure and conserved epitopes of Sfb protein, the fibronectin-binding adhesin of Streptococcus pyogenes. Mol. Microbiol. 13, 531-539.
82. Talay, S.R., Zock, A., Rohde, M., Molinari, G., Oggioni, M., Pozzi, G., Guzman, C.A., Chhatwal, G.S., 2000. Cooperative binding of human fibronectin to SfbI protein triggers streptococcal invasion into respiratory epithelial cells. Cell. Microbiol. 2, 521-535.
83. 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.
84. Terao, Y., Kawabata, S., Kunitomo, E., Nakagawa, I., Hamada, S., 2002a. Novel laminin-binding protein of Streptococcus pyogenes, Lbp, is involved in adhesion to epithelial cells. Infect. Immunol. 70, 993-997.
85. Terao, Y., Kawabata, S., Nakata, M., Nakagawa, I., Hamada, S., 2002b. 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.
86. Tomasini-Johansson, B.R., Kaufman, N.R., Ensenberger, M.G., Ozeri, V., Hanski, E., Mosher, D.F., 2001. A 49-residue peptide from adhesin F1 of Streptococcus pyogenes inhibits fibronectin matrix assembly. J. Biol. Chem. 276, 23430-23439.
87. Towers, R.J., Fagan, P.K., Talay, S.R., Currie, B.J., Sriprakash, K.S., Walker, M.J., Chhatwal, G.S., 2003. Evolution of sfbI encoding streptococcal fibronectin-binding protein 1: horizontal genetic transfer and gene mosaic structure. J. Clin. Microbiol. 41, 5398-5406.
88. Tsai, P.J., Lin, Y.S., Kuo, C.F., Lei, H.Y., Wu, J.J., 1999. Group A Streptococcus induces apoptosis in human epithelial cells. Infect. Immunol. 67, 4334-4339.
89. Valentin-Weigand, P., Talay, S.R., Timmis, K.N., Chhatwal, G.S., 1993. Identification of a fibronectin-binding protein as adhesin of Streptococcus pyogenes. Zentralbl. Bakteriol. 278, 238-245.
90. Valentin-Weigand, P., Talay, S.R., Kaufhold, A., Timmis, K.N., Chhatwal, G.S., 1994. The fibronectin binding domain of the Sfb protein adhesin of Streptococcus pyogenes occurs in many group A streptococci and does not cross-react with heart myosin. Microb. Pathog. 17, 111-120.
91. Watanabe-Ohnishi, R., Low, D.E., McGeer, A., Stevens, D.L., Schlievert, P.M., Newton, D., Schwartz, B., Kreiswirth, B., Kotb, M., 1995. Selective depletion of Vβ-bearing T cells in patients with severe invasive group A streptococcal infections and streptococcal toxic shock syndrome. Ontario Streptococcal Study Project. J. Infect. Dis. 171, 74-84.