A new rapid and cost-effective method for detection of phages, ICEs and virulence factors encoded by Streptococcus pyogenes

• Autorzy: Borek A.L. , Wilemska J. , Izdebski R. , Hryniewicz W. , Sitkiewicz I.
• Języki publikacji: EN

Abstrakty

EN

Streptococcus pyogenes (group A Streptococcus, GAS) is a human pathogen that causes diseases of various intensity, from mild strep throat to life threatening invasive infections and postinfectional sequelae. S. pyogenes encodes multiple, often phage encoded, virulence factors and their presence is related to severity of the disease. Acquisition of mobile genetic elements, carrying virulence factors, as phages or ICEs (integrative and cojugative elements) has been shown previously to promote selection of virulent clones. We designed the system of eight low volume multi- and one singleplex PCR reactions to detect genes encoding twenty virulence factors (spd3, sdc, sdaB, sdaD, speB, spyCEP, scpA, mac, sic, speL, K, M, C, I, A, H, G, J, smeZ and ssa) and twenty one phage and ICE integration sites described so far for S. pyogenes. Classification of strains based on the phage and virulence factors absence or presence, correlates with PFGE MLST and emm typing results. We developed a novel, fast and cost effective system that can be used to detect GAS virulence factors. Moreover, this system may become an alternative and effective system to differentiate between GAS strains.

Słowa kluczowe

EN

virulence factor; detection; phage; Streptococcus pyogenes; superantigen; human pathogen; human disease; strain classification; polymerase chain reaction; gene encoding; genome

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2011
• Tom: 60
• Numer: 3
• Opis fizyczny: p.187-201,fig.,ref.

Twórcy

autor

Borek A.L.

• Department of Epidemiology and Clinical Microbiology, National Medicines Institute, Chelmska 30/34, 00-725 Warsaw, Poland

autor

Wilemska J.

autor

Izdebski R.

autor

Hryniewicz W.

autor

Sitkiewicz I.

Bibliografia

• Beall B., R. Facklam and T. Thompson. 1996. Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci. J. Clin. Microbiol. 34: 953–958.
• Beall B., G. Gherardi, M. Lovgren, R.R. Facklam, B.A. Forwick and G.J. Tyrrell. 2000. emm and sof gene sequence variation in relation to serological typing of opacity-factor-positive group A streptococci. Microbiology 146: 1195–1209.
• Beres S.B., R.K. Carroll, P.R. Shea, I. Sitkiewicz, J.C. Martinez-Gutierrez, D.E. Low, A. McGeer, B.M. Willey, K. Green, G.J. Tyrrell, et al. 2010. Molecular complexity of successive bacterial epidemics deconvoluted by comparative pathogenomics. Proc. Natl. Acad. Sci. USA 107: 4371–4376.
• Beres S.B. and J.M. Musser. 2007. Contribution of exogenous genetic elements to the group A Streptococcus metagenome. PLoS One. 2: e800.
• Beres S.B., G.L. Sylva, D.E. Sturdevant, C.N. Granville, M. Liu, S.M. Ricklefs, A.R. Whitney, L.D. Parkins, N.P. Hoe, G.J. Adams, et al. 2004. Genome-wide molecular dissection of serotype M3 group A Streptococcus strains causing two epidemics of invasive infections. Proc. Natl. Acad. Sci. USA. 101: 11833–11838.
• Bernal A., T. Proft, J.D. Fraser and D.N. Posnett. 1999. Superantigens in human disease. J. Clin. Immunol. 19: 149–157.
• Bert F., C. Branger and N. Lambert-Zechovsky. 1997. Pulsed-field gel electrophoresis is more discriminating than multilocus enzyme electrophoresis and random amplified polymorphic DNA analysis for typing pyogenic streptococci. Curr. Microbiol. 34: 226–229.
• Carapetis J.R., A.C. Steer, E.K. Mulholland and M. Weber. 2005. The global burden of group A streptococcal diseases. Lancet. Infect. Dis. 5: 685–694.
• Carrico J.A., C. Silva-Costa, J. Melo-Cristino, F.R. Pinto, H. de Lencastre, J.S. Almeida and M. Ramirez. 2006. Illustration of a common framework for relating multiple typing methods by application to macrolide-resistant Streptococcus pyogenes. J. Clin. Microbiol. 44: 2524–2532.
• Chiang-Ni C. and J.J. Wu. 2008. Effects of streptococcal pyrogenic exotoxin B on pathogenesis of Streptococcus pyogenes. J. Formos. Med. Assoc. 107: 677–685.
• Cleary P.P., E.L. Kaplan, C. Livdahl and S. Skjold. 1988. DNA fingerprints of Streptococcus pyogenes are M type specific. J. Infect. Dis. 158: 1317–1323.
• Cleary P.P., U. Prahbu, J.B. Dale, D.E. Wexler and J. Handley. 1992. Streptococcal C5a peptidase is a highly specific endopeptidase. Infect. Immun. 60: 5219–5223.
• Commons R., S. Rogers, T. Gooding, M. Danchin, J. Carapetis, R. Robins-Browne and N. Curtis. 2008. Superantigen genes in group A streptococcal isolates and their relationship with emm types. J. Med. Microbiol. 57: 1238–1246.
• Courtney H.S., D.L. Hasty and J.B. Dale. 2002. Molecular mechanisms of adhesion, colonization, and invasion of group A streptococci. Ann. Med. 34: 77–87.
• Cunningham M.W. 2000. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13: 470–511.
• Edwards R.J., G.W. Taylor, M. Ferguson, S. Murray, N. Rendell, A. Wrigley, Z. Bai, J. Boyle, S.J. Finney, A. Jones, et al. 2005. Specific C-terminal cleavage and inactivation of interleukin-8 by invasive disease isolates of Streptococcus pyogenes. J. Infect. Dis. 192: 783–790.
• Enright M.C., B.G. Spratt, A. Kalia., J.H. Cross and D.E. Bessen. 2001. Multilocus sequence typing of Streptococcus pyogenes and the relationships between emm type and clone. Infect. Immun. 69: 2416–2427.
• Facklam R., B. Beall, A. Efstratiou, V. Fischetti, D. Johnson, E. Kaplan, P. Kriz, M. Lovgren, D. Martin, B. Schwartz, et al. 1999. Emm typing and validation of provisional M types for group A streptococci. Emerg. Infect. Dis. 5: 247–253.
• Ferretti J.J., W.M. McShan, D. Ajdic, D.J. Savic, G. Savic, K. Lyon, C. Primeaux, S. Sezate, A.N. Suvorov, S. Kenton, et al. 2001. Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc. Natl. Acad. Sci. USA 98: 4658–4663.
• Fraser J., V. Arcus, P. Kong, E. Baker and T. Proft. 2000. Superantigens – powerful modifiers of the immune system. Mol. Med. Today 6: 125–132.
• Green N.M., S. Zhang, S.F. Porcella, M.J. Nagiec, K.D. Barbian, S.B. Beres, R.B. LeFebvre and J.M. Musser. 2005. Genome sequence of a serotype M28 strain of group a streptococcus: potential new insights into puerperal sepsis and bacterial disease specificity. J. Infect. Dis. 192: 760–770.
• Hartas J., M. Hibble and K.S. Sriprakash. 1998. Simplification of a locus-specific DNA typing method (Vir typing) for Streptococcus pyogenes. J. Clin. Microbiol. 36: 1428–1429.
• Hauser A.R., D.L. Stevens, E.L. Kaplan and P.M. Schlievert. 1991. Molecular analysis of pyrogenic exotoxins from Streptococcus pyogenes isolates associated with toxic shock-like syndrome. J. Clin. Microbiol. 29: 1562–1567.
• Herschleb J., G. Ananiev and D.C. Schwartz. 2007. Pulsed-field gel electrophoresis. Nat. Protoc. 2: 677–684.
• Hoe N., K. Nakashima, D. Grigsby, X. Pan, S.J. Dou, S. Naidich, M. Garcia, E. Kahn, D. Bergmire-Sweat and J.M. Musser. 1999. Rapid molecular genetic subtyping of serotype M1 group A Streptococcus strains. Emerg. Infect. Dis. 5: 254–263.
• Koller T., A.G. Manetti, B. Kreikemeyer, C. Lembke, I. Margarit, G. Grandi and A. Podbielski. 2010. Typing of the pilus-proteinencoding FCT region and biofilm formation as novel parameters in epidemiological investigations of Streptococcus pyogenes isolates from various infection sites. J. Med. Microbiol. 59: 442–452.
• Kurupati P., C.E. Turner, I. Tziona, R.A. Lawrenson, F.M. Alam, M. Nohadani, G.W. Stamp, A.S. Zinkernagel, V. Nizet, R.J. Edward, et al. 2010. Chemokine-cleaving Streptococcus pyogenes protease SpyCEP is necessary and sufficient for bacterial dissemination within soft tissues and the respiratory tract. Mol. Microbiol. 76: 1387–1397.
• Lintges M., S. Arlt, P. Uciechowski, B. Plumakers, R.R. Reinert, A. Al-Lahham, R. Lutticken and L. Rink. 2007. A new closed-tube multiplex real-time PCR to detect eleven superantigens of Streptococcus pyogenes identifies a strain without superantigen activity. Int. J. Med. Microbiol. 297: 471–478.
• Matsumoto M., N.P. Hoe, M. Liu, S.B. Beres, G.L. Sylva, C.M. Brandt, G. Haase and J.M. Musser. 2003. Intrahost sequence variation in the streptococcal inhibitor of complement gene in patients with human pharyngitis. J. Infect. Dis. 187: 604–612.
• Maxted W.R., J.P. Widdowson, C.A. Fraser, L.C. Ball and D.C. Bassett. 1973. The use of the serum opacity reaction in the typing of group-A streptococci. J. Med. Microbiol. 6: 83–90.
• Moody M.D., J. Padula, D. Lizana and C.T. Hall. 1965. Epidemiologic Characterization of Group A streptococci by T-Agglutination and M-Precipitation Tests in the Public Health Laboratory. Health. Lab. Sci. 2: 149–162.
• Musser J.M., A.R. Hauser, M.H. Kim, P.M. Schlievert, K. Nelson and R.K. Selander. 1991. Streptococcus pyogenes causing toxic-shock-like syndrome and other invasive diseases: clonal diversity and pyrogenic exotoxin expression. Proc. Natl. Acad. Sci. USA 88: 2668–2672.
• Nandi S., N.K. Ganguly, R. Kumar, D.K. Bakshi, V.S. Vivek Sagar and A. Chakraborti. 2008. Genotyping of group A Streptococcus by various molecular methods. Indian. J. Med. Res. 127: 71–77.
• Oehmcke S., O. Shannon, M. Morgelin and H. Herwald. 2010. Streptococcal M proteins and their role as virulence determinants. Clin. Chim. Acta 411: 1172–1180.
• Perez-Caballero D., I. Garcia-Laorden, G. Cortes, M.R. Wessels, S.R. de Cordoba and S. Alberti. 2004. Interaction between complement regulators and Streptococcus pyogenes: binding of C4b-binding protein and factor H/factor H-like protein 1 to M18 strains involves two different cell surface molecules. J. Immunol. 173: 6899–6904.
• Pinto F.R., J. Melo-Cristino and M. Ramirez. 2008. A confidence interval for the wallace coefficient of concordance and its application to microbial typing methods. PLoS One. 3: e3696.
• Proft T., S.L. Moffatt, K.D. Weller, A. Paterson, D. Martin and J.D. Fraser. 2000. The streptococcal superantigen SMEZ exhibits wide allelic variation, mosaic structure, and significant antigenic variation. J. Exp. Med. 191: 1765–1776.
• Richardson L.J., S.Y. Tong, R.J. Towers, F. Huygens, K. McGregor, P.K. Fagan, B.J. Currie, J.R. Carapetis and P.M. Giffard. 2010. Preliminary validation of a novel high resolution melt-based typing method based on the multilocus sequence typing scheme of Streptococcus pyogenes. Clin. Microbiol. Infect. in press.
• Schmitz F.J., A. Beyer, E. Charpentier, B.H. Normark, M. Schade, A.C. Fluit, D. Hafner and R. Novak. 2003. Toxin-gene profile hetero geneity among endemic invasive European group A streptococcal isolates. J. Infect. Dis. 188: 1578–1586.
• Seppala H., J. Vuopio-Varkila, M. Osterblad, M. Jahkola, M. Rummukainen, S.E. Holm and P. Huovinen. 1994. Evaluation of methods for epidemiologic typing of group A streptococci. J. Infect. Dis. 169: 519–525.
• Slater G.W. 2009. DNA gel electrophoresis: the reptation model(s). Electrophoresis 30 Suppl. 1: S181–187.
• Smeesters P. R., D.J. McMillan and K.S. Sriprakash. 2010. The streptococcal M protein: a highly versatile molecule. Trends. Microbiol. 18: 275–282.
• Stanley J., D. Linton, M. Desai, A. Efstratiou and R. George. 1995. Molecular subtyping of prevalent M serotypes of Streptococcus pyogenes causing invasive disease. J. Clin. Microbiol. 33: 2850–2855.
• Stevens D.L., M.H. Tanner, J. Winship, R. Swarts, K.M. Ries, P.M. Schlievert and E. Kaplan. 1989. Severe group A streptococcal infections associated with a toxic shock-like syndrome and scarlet fever toxin A. N. Engl. J. Med. 321: 1–7.
• Sumby P., K.D. Barbian, D.J. Gardner, A.R. Whitney, D.M. Welty, R.D. Long, J.R. Bailey, M.J. Parnell, N.P. Hoe, G.G. Adams, et al. 2005. Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc. Natl. Acad. Sci. USA 102: 1679–1684.
• Sumby P., S. Zhang, A.R. Whitney, F. Falugi, G. Grandi, E.A. Graviss, F.R. Deleo and J.M. Musser. 2008. A chemokinedegrading extracellular protease made by group A Streptococcus alters pathogenesis by enhancing evasion of the innate immune response. Infect. Immun. 76: 978–985.
• Swift H.F., A.T. Wilson and R.C. Lancefield. 1943. Typing Group A Hemolytic streptococci by M precipitin reactions in capillary pipettes. J. Exp. Med. 78: 127–133.
• Szczypa K., E. Sadowy, R. Izdebski and W. Hryniewicz. 2004. A rapid increase in macrolide resistance in Streptococcus pyogenes isolated in Poland during 1996–2002. J. Antimicrob. Chemother. 54: 828–831.
• Tart A.H., M.J. Walker and J.M. Musser. 2007. New understanding of the group A Streptococcus pathogenesis cycle. Trends. Microbiol. 15: 318–325.
• Tenover F.C., R.D. Arbeit, R.V. Goering, P.A. Mickelsen, B.E. Murray, D.H. Persing and B. Swaminathan. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33: 2233–2239.
• Terao Y., Y. Mori, M. Yamaguchi, Y. Shimizu, K. Ooe, S. Hamada and S. Kawabata. 2008. Group A streptococcal cysteine protease degrades C3 (C3b) and contributes to evasion of innate immunity. J. Biol. Chem. 283: 6253–6260.
• Unnikrishnan M., D.M. Altmann, T. Proft, F. Wahid, J. Cohen, J.D. Fraser and S. Sriskandan. 2002. The bacterial superantigen streptococcal mitogenic exotoxin Z is the major immunoactive agent of Streptococcus pyogenes. J. Immunol. 169: 2561–2569.
• von U. Pawel-Rammingen, B.P. Johansson and L. Bjorck. 2002. IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. Embo. J. 21: 1607–1615.
• Walker M.J., A. Hollands, M.L. Sanderson-Smith, J.N. Cole, J.K. Kirk, A. Henningham, J.D. McArthur, K. Dinkla, R.K. Aziz, R.G. Kansal, et al. 2007. DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat. Med. 13: 981–985.
• C.E. Yu and J.J. Ferretti. 1989. Molecular epidemiologic analysis of the type A streptococcal exotoxin (erythrogenic toxin) gene (speA) in clinical Streptococcus pyogenes strains. Infect. Immun. 57: 3715–3719.
• Zinkernagel A.S., A.M. Timmer, M.A. Pence, J.B. Locke, J.T. Buchanan, C.E. Turner, I. Mishalian, S. Sriskandan, E. Hanski, and V. Nizet. 2008. The IL-8 protease SpyCEP/ScpC of group A Streptococcus promotes resistance to neutrophil killing. Cell. Host. Microbe. 4: 170–178.