Gelatinase-associated phenotypes and genotypes among clinical isolates of Enterococcus faecalis in Poland

• Autorzy: Strzelecki J. , Hryniewicz W. , Sadowy E.
• Języki publikacji: EN

Abstrakty

EN

Enterococcus faecalis is an important nosocomial pathogen causing serious invasive infections. One of the virulence factors of this pathogen, gelatinase GelE, is a protease whose gene expression is regulated by the Fsr quorum sensing system. In this study, we used a wellcharacterized collection of 153 clinical E. faecalis isolates to investigate the distribution of genes involved in gelatinase expression. Although 140 isolates (91% of the group) harbored the gelE gene, only 81 isolates (53%) produced active gelatinase. The gelatinase-negative phenotype was found in several unrelated clones, and appeared to be caused by various genetic events. Isolates of the hospital-adapted clonal complex 2 (CC2) and of CC40 were uniformly gelatinase-positive, while all the CC87 isolates contained the 23.9 kb deletion encompassing most of the fsr locus and were gelatinase-negative. No significant differences among isolates of different clinical origin and gelatinase activity or presence of the fsr genes were found with the exception of isolates from cerebrospinal fluid, which were more often gelatinase-positive than colonizing isolates.

Słowa kluczowe

EN

gelatinase-associated phenotype; genotype; clinical isolate; Enterococcus faecalis; Poland; pathogen; virulence factor; gene expression; urinary tract; surgical infection; human disease; polymerase chain reaction; phenotype

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2011
• Tom: 60
• Numer: 4
• Opis fizyczny: p.287-292,ref.

Twórcy

autor

Strzelecki J.

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

autor

Hryniewicz W.

autor

Sadowy E.

Bibliografia

• Arias C.A., G.A. Contreras and B.E. Murray. 2010. Management of multi-drug resistant enterococcal infections. Clin. Microbiol. Infect. 16: 555–562.
• Balaban N. and R.P. Novick. 1995. Autocrine regulation of toxin synthesis by Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 92: 1619–1623.
• Bittencourt de Marques E. and S. Suzart. 2004. Occurrence of virulence-associated genes in clinical Enterococcus faecalis strains isolated in Londrina, Brazil. J. Med. Microbiol. 53: 1069–1073.
• Coque T.M., J.E. Patterson, J.M. Steckelberg and B.E. Murray. 1995. Incidence of hemolysin, gelatinase, and aggregation substance among enterococci isolated from patients with endocarditis and other infections and from feces of hospitalized and community-based persons. J. Infect. Dis. 171: 1223–1229.
• Domann E., T. Hain, R. Ghai, A. Billion, C. Kuenne, K. Zimmermann and T. Chakraborty. 2007. Comparative genomic analysis for the presence of potential enterococcal virulence factors in the probiotic Enterococcus faecalis strain Symbioflor 1. Int. J. Med. Microbiol. 297: 533–539.
• Engelbert M., E. Mylonakis, F.M. Ausubel, S.B. Calderwood and M.S. Gilmore. 2004. Contribution of gelatinase, serine protease, and fsr to the pathogenesis of Enterococcus faecalis endophthalmitis. Infect. Immun. 72: 3628–3633.
• Feil E.J., B.C. Li, D.M. Aanensen, W.P. Hanage and B.G. Spratt. 2004. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 186: 1518–1530.
• Fisher K. and C. Phillips. 2009. The ecology, epidemiology and virulence of Enterococcus. Microbiology. 155: 1749–1757.
• Galloway-Pena J.R., A. Bourgogne, X. Qin and B.E. Murray. 2011. Diversity of the fsr-gelE region of Enterococcus faecalis but conservation in strains with partial deletion of the fsr operon. Appl. Environ. Microbiol. 77: 442–451.
• Gilmore M.S., P.S. Coburn, S.R. Nallapareddy and B.E. Murray. 2002. Enterococcal virulence. pp. 301–354. In: Gimore M.S. (ed.). The Enterococci: Pathogenesis, Molecular Biology and Antibiotic Resistance. ASM Press, Washington, D.C.
• Guiton P.S., C.S. Hung, L.E. Hancock, M.G. Caparon and S.J. Hultgren. 2010. Enterococcal biofilm formation and virulence in an optimized murine model of foreign body-associated urinary tract infections. Infect. Immun. 78: 4166–4175.
• Hancock L.E. and M. Perego. 2004. The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J. Bacteriol. 186: 5629–5639.
• Hendrickx A.P., R.J. Willems, M.J. Bonten and W. van Schaik. 2009. LPxTG surface proteins of enterococci. Trends Microbiol. 17: 423–430.
• Kawalec M., Z. Pietras, E. Danilowicz, A. Jakubczak, M. Gniadkowski, W. Hryniewicz and R.J. Willems. 2007. Clonal structure of Enterococcus faecalis isolated from Polish hospitals: characterization of epidemic clones. J. Clin. Microbiol. 45: 147–153.
• Kristich C.J., Y.H. Li, D.G. Cvitkovitch and G.M. Dunny. 2004. Esp-independent biofilm formation by Enterococcus faecalis. J. Bacteriol. 186: 154–163.
• Lopes M. de F., A.P. Simoes, R. Tenreiro, J.J. Marques and M.T. Crespo. 2006. Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int. J. Food Microbiol. 112: 208–214.
• Makinen P.L., D.B. Clewell, F. An and K.K. Makinen. 1989. Purification and substrate specificity of a strongly hydrophobic extracellular metalloendopeptidase (“gelatinase”) from Streptococcus faecalis (strain 0G1-10). J. Biol. Chem. 264: 3325–3334.
• Mohamed J.A., W. Huang, S.R. Nallapareddy, F.Teng and B.E. Murray. 2004. Influence of origin of isolates, especially endocarditis isolates, and various genes on biofilm formation by Enterococcus faecalis. Infect. Immun. 72: 3658–3663.
• Mohamed J.A. and B.E. Murray. 2005. Lack of correlation of gelatinase production and biofilm formation in a large collection of Enterococcus faecalis isolates. J. Clin. Microbiol. 43: 5405–5407.
• Nakayama J., Y. Cao, T. Horii, S. Sakuda, A.D. Akkermans, W.M. de Vos and H. Nagasawa. 2001. Gelatinase biosynthesis-activating pheromone: a peptide lactone that mediates a quorum sensing in Enterococcus faecalis. Mol. Microbiol. 41: 145–154.
• Nakayama J., S. Chen, N. Oyama, K. Nishiguchi, E.A. Azab, E. Tanaka, R. Kariyama and K. Sonomoto. 2006. Revised model for Enterococcus faecalis fsr quorum-sensing system: the small open reading frame fsrD encodes the gelatinase biosynthesis-activating pheromone propeptide corresponding to staphylococcal AgrD. J. Bacteriol. 188: 8321–8326.
• Nakayama J., R. Kariyama and H. Kumon. 2002. Description of a 23.9-kilobase chromosomal deletion containing a region encoding fsr genes which mainly determines the gelatinase-negative phenotype of clinical isolates of Enterococcus faecalis in urine. Appl. Environ. Microbiol. 68: 3152–3155.
• Piekarska K., R. Gierczyński, M. Ławrynowicz-Paciorek, M. Kochman and M. Jagielski. 2008. Novel gyrase mutations and characterization of ciprofloxacin-resistant clinical strains of Enterococcus faecalis isolated in Poland. Pol. J. Microbiol. 57: 121–124.
• Piekarska K. and M. Jagielski. 2007. Prevalence of virulence-associated genes of Enterococcus faecalis clinical strains isolated from patients and volunteers (in Polish). Med. Dosw. Mikrobiol. 59: 207–216.
• Pillai S.K., G. Sakoulas, H.S. Gold, C. Wennersten, G.M. Eliopoulos, R.C. Moellering, Jr. and R.T. Inouye. 2002. Prevalence of the fsr locus in Enterococcus faecalis infections. J. Clin. Microbiol. 40: 2651–2652.
• Qin X., K.V. Singh, G.M. Weinstock and B.E. Murray. 2000. Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect. Immun. 68: 2579–2586.
• Qin X., K.V. Singh, G.M. Weinstock and B.E. Murray. 2001. Characterization of fsr, a regulator controlling expression of gelatinase and serine protease in Enterococcus faecalis OG1RF. J. Bacteriol. 183: 3372–3382.
• Roberts J.C., K.V. Singh, P.C. Okhuysen and B.E. Murray. 2004. Molecular epidemiology of the fsr locus and of gelatinase production among different subsets of Enterococcus faecalis isolates. J. Clin. Microbiol. 42: 2317–2320.
• Rudy M., M. Zientara, T. Bek and G. Martirosian. 2005. Occurrence of Antibiotic Resistant Enterococci in Clinical Specimens from a Pediatric Hospital. Pol. J. Microbiol. 54: 77–80.
• Ruiz-Garbajosa P., M.J. Bonten, D.A. Robinson, J. Top, S.R. Nallapareddy, C. Torres, T.M. Coque, R. Canton, F. Baquero, B.E. Murray and others. 2006. Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J. Clin. Microbiol. 44: 2220–2228.
• Sedgley C.M., A. Molander, S.E. Flannagan, A.C. Nagel, O.K. Appelbe, D.B. Clewell and G. Dahlen. 2005. Virulence, phenotype and genotype characteristics of endodontic Enterococcus spp. Oral Microbiol. Immunol. 20: 10–19.
• Sifri C.D., E. Mylonakis, K.V. Singh, X. Qin, D. A. Garsin, B.E. Murray, F.M. Ausubel and S.B. Calderwood. 2002. Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect. Immun. 70: 5647–5650.
• Su Y. A., M.C. Sulavik, P. He, K.K. Makinen, P.L. Makinen, S. Fiedler, R. Wirth and D.B. Clewell. 1991. Nucleotide sequence of the gelatinase gene (gelE) from Enterococcus faecalis subsp. liquefaciens. Infect. Immun. 59: 415–420.
• Thomas V.C., Y. Hiromasa, N. Harms, L. Thurlow, J. Tomich and L.E. Hancock. 2009. A fratricidal mechanism is responsible for eDNA release and contributes to biofilm development of Enterococcus faecalis. Mol. Microbiol. 72: 1022–1036.
• Thomas V.C., L.R. Thurlow, D. Boyle and L.E. Hancock. 2008. Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J. Bacteriol. 190: 5690–5698.
• Thurlow L.R., V.C. Thomas, S. Narayanan, S. Olson, S.D. Fleming and L.E. Hancock. 2010. Gelatinase contributes to the pathogenesis of endocarditis caused by Enterococcus faecalis. Infect. Immun. 78: 4936–4943.
• Waters C.M., M.H. Antiporta, B.E. Murray and G.M. Dunny. 2003. Role of the Enterococcus faecalis GelE protease in determination of cellular chain length, supernatant pheromone levels, and degradation of fibrin and misfolded surface proteins. J. Bacteriol. 185: 3613–3623.
• Werner G., T.M. Coque, A.M. Hammerum, R. Hope, W. Hryniewicz, A. Johnson, I. Klare, K.G. Kristinsson, R. Leclercq, C.H. Lester and others. 2008. Emergence and spread of vancomycin resistance among enterococci in Europe. Euro. Surveill. 13: pii=19046.