Detection of invasive protein profile of Streptococcus pyogenes M1 isolates from pharyngitis patients
TADAO HASEGAWA
Department of Bacteriology, Nagoya City University Graduate School of Medical Sciences, Nagoya
Search for more papers by this authorAKIRA OKAMOTO
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorTAKUYA KAMIMURA
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorICHIRO TATSUNO
Department of Bacteriology, Nagoya City University Graduate School of Medical Sciences, Nagoya
Search for more papers by this authorSHIN-NOSUKE HASHIKAWA
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorMITSUTAKA YABUTANI
Nagoya City Public Health Research Institute, Nagoya
Search for more papers by this authorMASAKADO MATSUMOTO
Aichi Prefectural Institute of Public Health, Nagoya, Japan
Search for more papers by this authorKEIKO YAMADA
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorMASANORI ISAKA
Department of Bacteriology, Nagoya City University Graduate School of Medical Sciences, Nagoya
Search for more papers by this authorMASAAKI MINAMI
Department of Bacteriology, Nagoya City University Graduate School of Medical Sciences, Nagoya
Search for more papers by this authorMICHIO OHTA
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorTADAO HASEGAWA
Department of Bacteriology, Nagoya City University Graduate School of Medical Sciences, Nagoya
Search for more papers by this authorAKIRA OKAMOTO
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorTAKUYA KAMIMURA
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorICHIRO TATSUNO
Department of Bacteriology, Nagoya City University Graduate School of Medical Sciences, Nagoya
Search for more papers by this authorSHIN-NOSUKE HASHIKAWA
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorMITSUTAKA YABUTANI
Nagoya City Public Health Research Institute, Nagoya
Search for more papers by this authorMASAKADO MATSUMOTO
Aichi Prefectural Institute of Public Health, Nagoya, Japan
Search for more papers by this authorKEIKO YAMADA
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorMASANORI ISAKA
Department of Bacteriology, Nagoya City University Graduate School of Medical Sciences, Nagoya
Search for more papers by this authorMASAAKI MINAMI
Department of Bacteriology, Nagoya City University Graduate School of Medical Sciences, Nagoya
Search for more papers by this authorMICHIO OHTA
Department of Molecular Bacteriology, Nagoya University Graduate School of Medicine, Nagoya
Search for more papers by this authorAbstract
Hasegawa T, Okamoto A, Kamimura T, Tatsuno I, Hashikawa S-N, Yabutani M, Matsumoto M, Yamada K, Isaka M, Minami M, Ohta M. Detection of invasive protein profile of Streptococcus pyogenes M1 isolates from pharyngitis patients. APMIS 2010; 118: 167–78.
Streptococcal toxic shock syndrome (STSS) is a re-emerging infectious disease in Japan and many other developed countries. Epidemiological studies have revealed that the M1 serotype of Streptococcus pyogenes is the most dominant causative isolate of STSS. Recent characterization of M1 isolates revealed that the mutation of covS, one of the two-component regulatory systems, plays an important role in STSS by altering protein expression. We analyzed the M1 S. pyogenes clinical isolates before or after 1990 in Japan, using two-dimensional gel electrophoresis (2-DE) and pulsed-field gel electrophoresis (PFGE). PFGE profiles were different between the isolates before and after 1990. Markedly different profiles among isolates after 1990 from STSS and pharyngitis patients were detected. Sequence analysis of two-component regulatory systems showed that covS mutations were detected not only in STSS but also in three pharyngitis isolates, in which proteins from the culture supernatant displayed the invasive type. The mutated CovS detected in the pharyngitis isolates had impaired function on the production of streptococcal pyrogenic exotoxin B (SpeB) analyzed by 2-DE. These results suggest that several covS mutations that lead to the malfunction of the CovS protein occurred even in pharyngeal infection.
References
- 1 Cone LA, Woodard DR, Schlievert PM, Tomory GS. Clinical and bacteriologic observations of a toxic shock-like syndrome due to Streptococcus pyogenes. N Engl J Med 1987; 317: 146–9.
- 2 Stevens DL, Tanner MH, Winship J, Swarts R, Ries KM, Schlievert PM, et al. Severe group A streptococcal infections associated with a toxic shock-like syndrome and scarlet fever toxin A. N Engl J Med 1989; 321: 1–7.
- 3 Schwartz B, Facklam RR, Breiman RF. Changing epidemiology of group A streptococcal infection in the USA. Lancet 1990; 336: 1167–71.
- 4 Stevens DL. Invasive group A streptococcus infections. Clin Infect Dis 1992; 14: 2–11.
- 5 Hoge CW, Schwartz B, Talkington DF, Breiman RF, MacNeill EM, Englender SJ. The changing epidemiology of invasive group A streptococcal infections and the emergence of streptococcal toxic shock-like syndrome. A retrospective population-based study. JAMA 1993; 269: 384–9.
- 6 Musser JM, Hauser AR, Kim MH, Schlievert PM, Nelson K, Selander RK. Streptococcus pyogenes causing toxic-shock-like syndrome and other invasive diseases: clonal diversity and pyrogenic exotoxin expression. Proc Natl Acad Sci USA 1991; 88: 2668–72.
- 7 Stevens DL. Invasive group A streptococcal infections: the past, present and future. Pediatr Infect Dis J 1994; 13: 561–6.
- 8 Stevens DL, Salmi DB, McIndoo ER, Bryant AE. Molecular epidemiology of nga and NAD glycohydrolase/ADP-ribosyltransferase activity among Streptococcus pyogenes causing streptococcal toxic shock syndrome. J Infect Dis 2000; 182: 1117–28.
- 9 Shimizu Y, Ohyama A, Kasama K, Miyazaki M, Ooe K, Ookochi Y. Case report of toxic shock-like syndrome due to group A streptococcal infection. Kansenshogaku Zasshi 1993; 67: 236–9.
- 10 Shimizu Y, Igarashi H, Murai T, Ohkuni H, Watanabe H, Uchiyama T, et al. Report of surveillance on streptococcal toxic shock syndrome in Japan and presentation of the criteria. Kansenshogaku Zasshi 1998; 72: 258–65.
- 11 The Working Group on Severe Streptococcal Infections. Defining the group A streptococcal toxic shock syndrome. Rationale and consensus definition. JAMA 1993; 269: 390–1.
- 12 Eriksson BK, Andersson J, Holm SE, Norgren M. Epidemiological and clinical aspects of invasive group A streptococcal infections and the streptococcal toxic shock syndrome. Clin Infect Dis 1998; 27: 1428–36.
- 13 Cunningham MW. Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 2000; 13: 470–511.
- 14 Tyrrell GJ, Lovgren M, Forwick B, Hoe NP, Musser JM, Talbot JA. M types of group A streptococcal isolates submitted to the National Centre for Streptococcus (Canada) from 1993 to 1999. J Clin Microbiol 2002; 40: 4466–71.
- 15 Zurawski CA, Bardsley M, Beall B, Elliott JA, Facklam R, Schwartz B, et al. Invasive group A streptococcal disease in metropolitan Atlanta: a population-based assessment. Clin Infect Dis 1998; 27: 150–7.
- 16 Cleary PP, Kaplan EL, Handley JP, Wlazlo A, Kim MH, Hauser AR, et al. Clonal basis for resurgence of serious Streptococcus pyogenes disease in the 1980s. Lancet 1992; 339: 518–21.
- 17 Muotiala A, Seppala H, Huovinen P, Vuopio-Varkila J. Molecular comparison of group A streptococci of T1M1 serotype from invasive and noninvasive infections in Finland. J Infect Dis 1997; 175: 392–9.
- 18 Musser JM, Kapur V, Szeto J, Pan X, Swanson DS, Martin DR. Genetic diversity and relationships among Streptococcus pyogenes strains expressing serotype M1 protein: recent intercontinental spread of a subclone causing episodes of invasive disease. Infect Immun 1995; 63: 994–1003.
- 19 Okuno R, Endoh M, Shimojima Y, Yanagawa Y, Morozumi S, Igarashi H, et al. Epidemiological study on Streptococcus pyogenes strains isolated from the patients with streptococcal toxic shock syndrome (STSS) in Japan in 1992–2001. Kansenshogaku Zasshi 2004; 78: 10–7.
- 20 Ikebe T, Murai N, Endo M, Okuno R, Murayama S, Saitoh K, et al. Changing prevalent T serotypes and emm genotypes of Streptococcus pyogenes isolates from streptococcal toxic shock-like syndrome (TSLS) patients in Japan. Epidemiol Infect 2003; 130: 569–72.
- 21 Ferretti JJ, McShan WM, Ajdic D, Savic DJ, Savic G, Lyon K, et al. Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci USA 2001; 98: 4658–63.
- 22 Sumby P, Porcella SF, Madrigal AG, Barbian KD, Virtaneva K, Ricklefs SM, et al. Evolutionary origin and emergence of a highly successful clone of serotype M1 group A Streptococcus involved multiple horizontal gene transfer events. J Infect Dis 2005; 192: 771–82.
- 23 Aziz RK, Edwards RA, Taylor WW, Low DE, McGeer A, Kotb M. Mosaic prophages with horizontally acquired genes account for the emergence and diversification of the globally disseminated M1T1 clone of Streptococcus pyogenes. J Bacteriol 2005; 187: 3311–8.
- 24 Hasegawa T, Torii K, Hashikawa S, Iinuma Y, Ohta M. Cloning and characterization of two novel DNases from Streptococcus pyogenes. Arch Microbiol 2002; 177: 451–6.
- 25 Hasegawa T, Torii K, Hashikawa S, Iinuma Y, Ohta M. Cloning and characterization of the deoxyribonuclease sdα gene from Streptococcus pyogenes. Curr Microbiol 2002; 45: 13–7.
- 26 Nakamura T, Hasegawa T, Torii K, Hasegawa Y, Shimokata K, Ohta M. Two-dimensional gel electrophoresis analysis of the abundance of virulent exoproteins of group A streptococcus caused by environmental changes. Arch Microbiol 2004; 181: 74–81.
- 27 Tanaka M, Hasegawa T, Okamoto A, Torii K, Ohta M. Effect of antibiotics on group A Streptococcus exoprotein production analyzed by two-dimensional gel electrophoresis. Antimicrob Agents Chemother 2005; 49: 88–96.
- 28 Sawai J, Hasegawa T, Kamimura T, Okamoto A, Ohmori D, Nosaka N, et al. Growth phase-dependent effect of clindamycin on production of exoproteins by Streptococcus pyogenes. Antimicrob Agents Chemother 2007; 51: 461–7.
- 29 Sumby P, Whitney AR, Graviss EA, DeLeo FR, Musser JM. Genome-wide analysis of group A streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog 2006; 2: e5.
- 30 Walker MJ, Hollands A, Sanderson-Smith ML, Cole JN, Kirk JK, Henningham A, et al. DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med 2007; 13: 981–5.
- 31 Hashikawa S, Iinuma Y, Furushita M, Ohkura T, Nada T, Torii K, et al. Characterization of group C and G streptococcal strains that cause streptococcal toxic shock syndrome. J Clin Microbiol 2004; 42: 186–92.
- 32 Okada N, Tatsuno I, Hanski E, Caparon M, Sasakawa C. Streptococcus pyogenes protein F promotes invasion of HeLa cells. Microbiology 1998; 144: 3079–86.
- 33 Bohach GA, Hauser AR, Schlievert PM. Cloning of the gene, speB, for streptococcal pyrogenic exotoxin type B in Escherichia coli. Infect Immun 1988; 56: 1665–7.
- 34 Akesson P, Sjoholm AG, Bjorck L. Protein SIC, a novel extracellular protein of Streptococcus pyogenes interfering with complement function. J Biol Chem 1996; 271: 1081–8.
- 35 Hoe NP, Vuopio-Varkila J, Vaara M, Grigsby D, De Lorenzo D, Fu YX, et al. Distribution of streptococcal inhibitor of complement variants in pharyngitis and invasive isolates in an epidemic of serotype M1 group A Streptococcus infection. J Infect Dis 2001; 183: 633–9.
- 36 Engleberg NC, Heath A, Miller A, Rivera C, DiRita VJ. Spontaneous mutations in the CsrRS two-component regulatory system of Streptococcus pyogenes result in enhanced virulence in a murine model of skin and soft tissue infection. J Infect Dis 2001; 183: 1043–54.
- 37 Levin JC, Wessels MR. Identification of csrR/csrS, a genetic locus that regulates hyaluronic acid capsule synthesis in group A Streptococcus. Mol Microbiol 1998; 30: 209–19.
- 38 Federle MJ, McIver KS, Scott JR. A response regulator that represses transcription of several virulence operons in the group A streptococcus. J Bacteriol 1999; 181: 3649–57.
- 39 Heath A, DiRita VJ, Barg NL, Engleberg NC. 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 1999; 67: 5298–305.
- 40 Shelburne SA III, Granville C, Tokuyama M, Sitkiewicz I, Patel P, Musser JM. Growth characteristics of and virulence factor production by group A Streptococcus during cultivation in human saliva. Infect Immun 2005; 73: 4723–31.
- 41 Nyberg P, Rasmussen M, Bjorck L. α2-macroglobulin-proteinase complexes protect Streptococcus pyogenes from killing by the antimicrobial peptide LL-37. J Biol Chem 2004; 279: 52820–3.
- 42 Collin M, Svensson MD, Sjoholm AG, Jensenius JC, Sjobring U, Olsen A. EndoS and SpeB from Streptococcus pyogenes inhibit immunoglobulin-mediated opsonophagocytosis. Infect Immun 2002; 70: 6646–51.
- 43 Eriksson A, Norgren M. Cleavage of antigen-bound immunoglobulin G by SpeB contributes to streptococcal persistence in opsonizing blood. Infect Immun 2003; 71: 211–7.
- 44 Virtaneva K, Porcella SF, Graham MR, Ireland RM, Johnson CA, Ricklefs SM, et al. Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc Natl Acad Sci USA 2005; 102: 9014–9.
- 45 Dalton TL, Scott JR. CovS inactivates CovR and is required for growth under conditions of general stress in Streptococcus pyogenes. J Bacteriol 2004; 186: 3928–37.
- 46 Froehlich BJ, Bates C, Scott JR. Streptococcus pyogenes CovRS mediates growth in iron starvation and in the presence of the human cationic antimicrobial peptide LL-37. J Bacteriol 2009; 191: 673–7.
- 47 Gryllos I, Levin JC, Wessels MR. The CsrR/CsrS two-component system of group A Streptococcus responds to environmental Mg2+. Proc Natl Acad Sci USA 2003; 100: 4227–32.
