Peptide pheromone-induced transfer of plasmid pCF10 in Enterococcus faecalis: probing the genetic and molecular basis for specificity of the pheromone response

Dunny, Gary M.; Antiporta, Michelle H.; Hirt, Helmut

doi:10.1016/s0196-9781(01)00489-2

Cited by 40 publications

(23 citation statements)

References 49 publications

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“…The specificity of the pCF10 plasmid transfer for cCF10 is remarkable. It has been demonstrated that the addition of pheromones cAD1 and cPD1, specific for the transfer of the plasmids pAD1 and pPD1, respectively, did not induce the transfer of pCF10 (13). Alterations in the cCF10 sequence, for example, replacing the second position valine with alanine, led to a drastic reduction in induction capacity (M. H. Antiporta and G. M. Dunny, personal communication).…”

Section: Resultsmentioning

confidence: 99%

“…In addition, specificity towards the pheromones is also striking. Mating induction experiments involving pCF10, pAD1, and pPD1 have shown that when donor cells carrying two of these plasmids are induced by one of the pheromones, only the cognate plasmid shows elevated transfer (13,19). The exclusivity and specificity of the sex pheromone system raised the question of how induction of AS can be achieved in vivo, especially in a complex system like plasma.…”

Section: ϫ2mentioning

confidence: 99%

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In Vivo Induction of Virulence and Antibiotic Resistance Transfer in Enterococcus faecalis Mediated by the Sex Pheromone-Sensing System of pCF10

2002

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Enterococcus faecalis has become one of the most notable nosocomial pathogens in the last decade. Aggregation substance (AS) on the sex pheromone plasmids of E. faecalis has been implicated as a virulence factor in several model systems. We investigated the AS-encoding plasmid pCF10 for its ability to increase virulence in a rabbit endocarditis model. Cells containing pCF10 increased the virulence in the model significantly, as assessed by an increase in aortic valve vegetation size. The results confirmed in vivo induction of the normally tightly controlled AS. In addition to the expression of AS when E. faecalis cells were in contact with plasma, plasmid transfer of the tetracycline resistance-carrying plasmid was also activated in vitro and in vivo. In vivo, plasmid transfer reached remarkable frequencies of 8 ؋ 10 ؊2 to 9 ؋ 10 ؊2 . These values are comparable to the highest frequencies ever observed in vitro. Cells harboring pCF10 had a significant survival advantage over plasmid-free cells indicated by pCF10 present in two-thirds of the recipient population. Plasma induction was dependent on the presence of the plasmid-encoded PrgZ protein, indicating the requirement of the pheromonesensing system in the induction process. The data suggested that the mechanism of in vivo induction may involve interference of plasma with the normal function of the pheromone peptide and its inhibitor. Aggregation substance (AS) is a 137-kDa surface protein encoded on sex pheromone plasmids of Enterococcus faecalis.This protein mediates strong binding between E. faecalis cells as manifested by the formation of visible cell aggregates preceding the conjugative transfer of a sex pheromone plasmid (14). The plasmid transfer response is initiated by 7-to 8-amino-acid-long hydrophobic peptides secreted by potential recipient cells (16,32). These peptides are part of signal sequences of chromosomally encoded lipoproteins (10) and lead to induction of AS expression.Asc10, the AS of the sex pheromone plasmid pCF10 (encoding tetracycline resistance) (17), is induced by the 7-aminoacid peptide cCF10 (32) encoded by the ccfA gene. The donor cell binds the peptide (37), employing a specific plasmid-encoded receptor, PrgZ, an OppA homologue (Fig. 1). The peptide is then transported into the cell via the oligopeptide permease system (29), leading to the expression of AS and subsequent plasmid transfer. Since expression of AS and the other plasmid transfer machinery is presumably a very energyconsuming process, it is not surprising that expression of AS is tightly regulated. This ensures that the nonmotile enterococcal cells expressing transfer functions are in close proximity for cell contact to occur between mating partners. pCF10 donor cells are faced with the dilemma that they secrete unaltered amounts of cCF10 (33), necessitating a complex scheme to prevent autoinduction by their own pheromones. A schematic overview of the events controlling AS expression is given in Fig. 1. Secreted cCF10 may accumulate to approximately 8 pg/ml (33). To...

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Section: Resultsmentioning

confidence: 99%

Section: ϫ2mentioning

confidence: 99%

In Vivo Induction of Virulence and Antibiotic Resistance Transfer in Enterococcus faecalis Mediated by the Sex Pheromone-Sensing System of pCF10

2002

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“…Transfer frequencies for conjugative plasmids in Enterococcus faecium can be as low ≥10 -6 per donor in laboratory experiments using broth mating, but the production of short peptides by some recipient cells which cause cell aggregation greatly increase transfer rates (≥10 -4 ) (Dunny et al, 2001). Plasmids play an important role in gene transfer in staphylococci, conjugative plasmids also being capable of mobilising small non-transferable plasmids (McDonnell et al, 1983).…”

Section: Mechanisms Of Horizontal Gene Transfermentioning

confidence: 99%

Antibiotic Resistance in the Environment, with Particular Reference to MRSA

Gaze

O’Neill

Wellington

et al. 2008

Advances in Applied Microbiology

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“…Conjugation systems involving plasmids and transposons are abundant in these organisms and contribute to the dissemination of both antibiotic resistance and virulence factors (6). In particular, the sex pheromone system of E. faecalis, first described by Dunny et al (9), involves the production of pheromones by recipient strains, each being specific for a particular plasmid or a group of related plasmids (11). Donor strains exposed to a pheromone are induced to synthesize a specific plasmid-encoded surface protein, designated "aggregation substance" (AS), which facilitates the initiation of mating pair formation (5).…”

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confidence: 99%

Sex Pheromone Response, Clumping, and Slime Production in Enterococcal Strains Isolated from Occluded Biliary Stents

et al. 2004

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Bile-resistant bacteria, particularly gram-positive Enterococcus faecalis and Enterococcus faecium, play an important role in biliary stent occlusion, because their sessile mode of growth protects them against host defenses and antimicrobial agents. Twelve E. faecalis and seven E. faecium strains isolated from occluded biliary stents have been investigated for slime production, presence of aggregation substance genes, and ability to adhere to Caco-2 cells. Ten isolates were strong producers of slime, and seven isolates produced clumps when exposed to pheromones of E. faecalis JH2-2 and/or OG1RF. The small E. faecium clumps differed from the large clumps of E. faecalis and were similar to those of E. faecium LS10(pBRG1) carrying a pheromone response plasmid. After induction with pheromones, the adhesion to Caco-2 cells of clumping-positive strains was found to increase from two-to fourfold. Amplicons of the expected size were detected in three clumpingpositive and three clumping-negative E. faecalis isolates by using primers (agg) internal to a highly conserved region of the E. faecalis pheromone response plasmids pAD1, pPD1, and pCF10 and primers internal to prgB of the E. faecalis plasmid pCF10. The agg/prgB-positive E. faecalis strains were also positive in Southern hybridization experiments with a prgB-specific probe. No PCR products were obtained with the same primers from four clumping-positive isolates (one E. faecalis and three E. faecium strains), which were also Southern hybridization negative. Our results demonstrate that slime production and pheromone response are both present in isolated enterococci, suggesting that clinical strains with these features might have a selective advantage in colonizing biliary stents.

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Peptide pheromone-induced transfer of plasmid pCF10 in Enterococcus faecalis: probing the genetic and molecular basis for specificity of the pheromone response

Cited by 40 publications

References 49 publications

In Vivo Induction of Virulence and Antibiotic Resistance Transfer in Enterococcus faecalis Mediated by the Sex Pheromone-Sensing System of pCF10

In Vivo Induction of Virulence and Antibiotic Resistance Transfer in Enterococcus faecalis Mediated by the Sex Pheromone-Sensing System of pCF10

Antibiotic Resistance in the Environment, with Particular Reference to MRSA

Sex Pheromone Response, Clumping, and Slime Production in Enterococcal Strains Isolated from Occluded Biliary Stents

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