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Two-dimensional gel electrophoresis analysis of the abundance of virulent exoproteins of group A streptococcus caused by environmental changes

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Abstract

Group A streptococci regulate the expression of virulence factors in response to environmental change. In order to investigate this mechanism, the growth of group A streptococci and the abundance of virulent exoprotein production in culture supernatant were analyzed by two-dimensional gel electrophoresis (2-D electrophoresis) under several culture conditions. Judging from alterations in their growth, group A streptococci were affected by various environmental stresses. Under high O2 and low CO2 concentrations, streptococcal pyrogenic exotoxin B (SpeB) and streptococcal pyrogenic exotoxin F (SpeF) significantly decreased, and the streptococcal inhibitor of complement (Sic) increased . At 30 °C, increases in endo-β-N-acetylglucosaminidase (EndoS) and α-amylase were also detected, while at 41 °C EndoS became undetectable and SpeB and SpeF decreased. Sic, SpeF and mitogenic factor 3 (Mf3) decreased when cells were cultured in higher NaCl concentrations, and EndoS disappeared following culture of the cells in high glucose concentration. An increase in acid phosphatase and a decrease in several other proteins were detected when the cells were cultivated in high iron concentrations. These results suggest that group A streptococci have a versatile adaptation system that responds to several environmental stresses by altering the level of exoprotein production.

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Abbreviations

SpeB :

Streptococcal pyrogenic exotoxin B

SpeF :

Streptococcal pyrogenic exotoxin F

Sic :

Streptococcal inhibitor of complement

EndoS :

Endo-β-N-acetylglucosaminidase

References

  • Caparon MG, Geist RT, Perez-Casal J, Scott JR (1992) Environmental regulation of virulence in group A streptococci: transcription of the gene encoding M protein is stimulated by carbon dioxide. J Bacteriol 174:5693–5701

    CAS  PubMed  Google Scholar 

  • Chaussee MS, Liu J, Stevens DL, Ferretti JJ (1997) Effects of environmental factors on streptococcal erythrogenic toxin A (SPE A) production by Streptococcus pyogenes. Adv Exp Med Biol 418:551–554

    CAS  PubMed  Google Scholar 

  • Chaussee MS, Sylva GL, Sturdevant DE, Smoot LM, Graham MR, Watson RO, Musser JM (2002) Rgg influences the expression of multiple regulatory loci to coregulate virulence factor expression in Streptococcus pyogenes. Infect Immun 70:762–770

    Article  CAS  PubMed  Google Scholar 

  • Collin M, Olsen A (2001a) Effect of SpeB and EndoS from Streptococcus pyogenes on human immunoglobulins. Infect Immun 69:7187–7189

    Article  CAS  PubMed  Google Scholar 

  • Collin M, Olsen A (2001b) EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J 20:3046–3055

    Article  CAS  PubMed  Google Scholar 

  • Eichenbaum Z, Green BD, Scott JR (1996) Iron starvation causes release from the group A streptococcus of the ADP-ribosylating protein called plasmin receptor or surface glyceraldehyde-3-phosphate-dehydrogenase. Infect Immun 64:1956–1960

    CAS  PubMed  Google Scholar 

  • Ferretti JJ, McShan WM, Ajdic D, Savic DJ, Savic G, Lyon K, Primeaux C, Sezate S, Suvorov AN, Kenton S, Lai HS, Lin SP, Qian Y, Jia HG, Najar FZ, Ren Q, Zhu H, Song L, White J, Yuan X, Clifton SW, Roe BA, McLaughlin R (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci U S A 98:4658–4663

    Article  CAS  PubMed  Google Scholar 

  • Fogg GC, Gibson CM, Caparon MG (1994) The identification of rofA, a positive-acting regulatory component of prtF expression: use of an m γδ-based shuttle mutagenesis strategy in Streptococcus pyogenes. Mol Microbiol 11:671–684

    CAS  PubMed  Google Scholar 

  • Graham MR, Smoot LM, Migliaccio CA, Virtaneva K, Sturdevant DE, Porcella SF, Federle MJ, Adams GJ, Scott JR, Musser JM (2002) Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling. Proc Natl Acad Sci U S A 99:13855–13860

    Article  CAS  PubMed  Google Scholar 

  • Granger DL, Perfect JR, Durack DT (1985) Virulence of Cryptococcus neoformans. Regulation of capsule synthesis by carbon dioxide. J Clin Invest 76:508–516

    CAS  PubMed  Google Scholar 

  • Hasegawa T, Torii K, Hashikawa S, Iinuma Y, Ohta M (2002a) Cloning and characterization of the deoxyribonuclease sdα gene from Streptococcus pyogenes. Cur Microbiol 45:13–17

    Article  CAS  Google Scholar 

  • Hasegawa T, Torii K, Hashikawa S, Iinuma Y, Ohta M (2002b) Cloning and characterization of two novel DNases from Streptococcus pyogenes. Arch Microbiol 177:451–456

    Article  CAS  PubMed  Google Scholar 

  • Heath A, DiRita VJ, Barg NL, Engleberg NC (1999) A two-component regulatory system, CsrR-CsrS, represses expression of three Streptococcus pyogenes virulence factors, hyaluronic acid capsule, streptolysin S, and pyrogenic exotoxin B. Infect Immun 67:5298–5305

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kawano Y, Kawagishi, M Nakano M, Mase K, Yamashino T, Hasagawa T, Ohta M (2001) Proteolytic cleavage of staphylococcal exoproteins analyzed by two-dimensional gel electrophoresis. Microbiol Immunol 45:285–290

    CAS  PubMed  Google Scholar 

  • Kihlberg BM, Cooney J, Caparon MG, Olsen A, Bjorck L (1995) Biological properties of a Streptococcus pyogenes mutant generated by Tn916 insertion in mga. Microb Pathog 19:299–315

    CAS  PubMed  Google Scholar 

  • Makino S, Sasakawa C, Uchida I, Terakado N, Yoshikawa M (1988) Cloning and CO2-dependent expression of the genetic region for encapsulation from Bacillus anthracis. Mol Microbiol 2:371–376

    CAS  PubMed  Google Scholar 

  • McIver KS, Heath AS, Scott JR (1995) Regulation of virulence by environmental signals in group A streptococci: influence of osmolarity, temperature, group A streptococci exchange, and iron limitation on emm transcription. Infect Immun 63:4540–4542

    CAS  PubMed  Google Scholar 

  • Okada N, Geist RT, Caparon MG (1993) Positive transcriptional control of mry regulates virulence in the group A streptococcus. Mol Microbiol 7:893–903

    CAS  PubMed  Google Scholar 

  • Podbielski A, Woischnik M, Kreikemeyer B, Bettenbrock K, Buttaro BA (1999) Cysteine protease SpeB expression in group A streptococci is influenced by the nutritional environment but SpeB does not contribute to obtaining essential nutrients. Med Microbiol Immunol 188:99–109

    Article  CAS  PubMed  Google Scholar 

  • Read CM, Patel UA, Moss T (1989) Coordinate replication of dispersed repetitive sequences in Physarum polycephalum. Exp Cell Res 181:505–517

    CAS  PubMed  Google Scholar 

  • Sirard JC, Mock M, Fouet A (1994) The three Bacillus anthracis toxin genes are coordinately regulated by bicarbonate and temperature. J Bacteriol 176:5188–5192

    CAS  PubMed  Google Scholar 

  • Smoot LM, Smoot JC, Graham MR, Iturdevant DE, Migliaccio CA, Sylva GL, Musser JM (2001) Global differential gene expression in response to growth temperature alteration in group A Streptococcus. Proc Natl Acad Sci U S A 98:10416–10421

    Article  CAS  PubMed  Google Scholar 

  • Stevens DL (1992) Invasive group A streptococcus infections. Clin Infect Dis 14:2–11

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. Ferretti of Oklahoma University for providing strain SF370. This work was supported by a Grant-in-Aid for Scientific Research (11670261 and 12557027) from the Ministry of Education, Culture, Sports, Science and Technology, and a grant for research on emerging and reemerging infectious disease (H12 Sinkou-7) from the Ministry of Health and Welfare, Japan.

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Correspondence to Tadao Hasegawa.

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Nakamura, T., Hasegawa, T., Torii, K. et al. Two-dimensional gel electrophoresis analysis of the abundance of virulent exoproteins of group A streptococcus caused by environmental changes. Arch Microbiol 181, 74–81 (2004). https://doi.org/10.1007/s00203-003-0632-6

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  • DOI: https://doi.org/10.1007/s00203-003-0632-6

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