The ancillary protein 1 of <i>Streptococcus pyogenes</i> FCT‐1 pili mediates cell adhesion and biofilm formation through heterophilic as well as homophilic interactions

Becherelli, Marco; Manetti, Andrea G. O.; Buccato, Scilla; Viciani, Elisa; Ciucchi, Laura; Mollica, Giulia; Grandi, Guido; Margarit, I.

doi:10.1111/j.1365-2958.2012.07987.x

Cited by 42 publications

(37 citation statements)

References 44 publications

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“…Pili are known to be involved in biofilm formation in both Gram-positive and Gram-negative bacteria [89], [90]. Pili, by their adhesive properties can mediate early attachment to surfaces and cell to cell interaction leading to auto-aggregation and ultimately to biofilm formation [91]. In this study, we have shown that L. lactis cells that display pili induce auto-aggregation in liquid cultures and formation of thicker biofilms than the wild-type strain.…”

Section: Discussionmentioning

confidence: 60%

Pilus Biogenesis in Lactococcus lactis: Molecular Characterization and Role in Aggregation and Biofilm Formation

et al. 2012

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The genome of Lactococcus lactis strain IL1403 harbors a putative pilus biogenesis cluster consisting of a sortase C gene flanked by 3 LPxTG protein encoding genes (yhgD, yhgE, and yhhB), called here pil. However, pili were not detected under standard growth conditions. Over-expression of the pil operon resulted in production and display of pili on the surface of lactococci. Functional analysis of the pilus biogenesis machinery indicated that the pilus shaft is formed by oligomers of the YhgE pilin, that the pilus cap is formed by the YhgD pilin and that YhhB is the basal pilin allowing the tethering of the pilus fibers to the cell wall. Oligomerization of pilin subunits was catalyzed by sortase C while anchoring of pili to the cell wall was mediated by sortase A. Piliated L. lactis cells exhibited an auto-aggregation phenotype in liquid cultures, which was attributed to the polymerization of major pilin, YhgE. The piliated lactococci formed thicker, more aerial biofilms compared to those produced by non-piliated bacteria. This phenotype was attributed to oligomers of YhgE. This study provides the first dissection of the pilus biogenesis machinery in a non-pathogenic Gram-positive bacterium. Analysis of natural lactococci isolates from clinical and vegetal environments showed pili production under standard growth conditions. The identification of functional pili in lactococci suggests that the changes they promote in aggregation and biofilm formation may be important for the natural lifestyle as well as for applications in which these bacteria are used.

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Section: Discussionmentioning

confidence: 60%

Pilus Biogenesis in Lactococcus lactis: Molecular Characterization and Role in Aggregation and Biofilm Formation

et al. 2012

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“…Pili are often described as ‘adhesins on a stalk’ due to their specific architecture with an adhesive molecule located at the tip of an extended fibrilar structure (Kang and Baker, ; Kang et al ., ). For the well‐studied GAS pilus types encoded within the FCT‐2, FCT‐3 and FCT‐4 regions, the tip molecule was found to play an important role in host cell adhesion, and binds to the extracellular matrix component collagen (Kreikemeyer, ; Smith et al ., ; Becherelli et al ., ). In this study, we show that the GAS serotype M2 pilus encoded within the FCT‐6 region is not only genetically, but also functionally different from the classical pilus types.…”

Section: Discussionmentioning

confidence: 97%

The Group A Streptococcus serotype M2 pilus plays a role in host cell adhesion and immune evasion

Tsai

Loh

Clow³

et al. 2016

Molecular Microbiology

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Group A Streptococcus (GAS), or Streptococcus pyogenes, is a human pathogen that causes diseases ranging from skin and soft tissue infections to severe invasive diseases, such as toxic shock syndrome. Each GAS strain carries a particular pilus type encoded in the variable fibronectin-binding, collagen-binding, T antigen (FCT) genomic region. Here, we describe the functional analysis of the serotype M2 pilus encoded in the FCT-6 region. We found that, in contrast to other investigated GAS pili, the ancillary pilin 1 lacks adhesive properties. Instead, the backbone pilin is important for host cell adhesion and binds several host factors, including fibronectin and fibrinogen. Using a panel of recombinant pilus proteins, GAS gene deletion mutants and Lactococcus lactis gain-of-function mutants we show that, unlike other GAS pili, the FCT-6 pilus also contributes to immune evasion. This was demonstrated by a delay in blood clotting, increased intracellular survival of the bacteria in macrophages, higher bacterial survival rates in human whole blood and greater virulence in a Galleria mellonella infection model in the presence of fully assembled FCT-6 pili.

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“…Sortase-assembled pili have been implicated as virulence factors in models of infections caused by many Gram-positive pathogens, including GAS (46,47), GBS (48)(49)(50), and S. pneumoniae (51). Significant advances in the understanding of sortase-assembled pilus biogenesis have accompanied functional studies in these organisms and in the prototypical C. diphtheriae pilus systems.…”

Section: Discussionmentioning

confidence: 99%

Pilin and Sortase Residues Critical for Endocarditis- and Biofilm-Associated Pilus Biogenesis in Enterococcus faecalis

et al. 2013

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bEnterococci commonly cause hospital-acquired infections, such as infective endocarditis and catheter-associated urinary tract infections. In animal models of these infections, a long hairlike extracellular protein fiber known as the endocarditis-and biofilm-associated (Ebp) pilus is an important virulence factor for Enterococcus faecalis. For Ebp and other sortase-assembled pili, the pilus-associated sortases are essential for fiber formation as they create covalent isopeptide bonds between the sortase recognition motif and the pilin-like motif of the pilus subunits. However, the molecular requirements governing the incorporation of the three pilus subunits (EbpA, EbpB, and EbpC) have not been investigated in E. faecalis. Here, we show that a Lys residue within the pilin-like motif of the EbpC subunit was necessary for EbpC polymerization. However, incorporation of EbpA into the pilus fiber only required its sortase recognition motif (LPXTG), while incorporation of EbpB only required its pilin-like motif. Only the sortase recognition motif would be required for incorporation of the pilus tip subunit, while incorporation of the base subunit would only require the pilin recognition motif. Thus, these data support a model with EbpA at the tip and EbpB at the base of an EbpC polymer. In addition, the housekeeping sortase, SrtA, was found to process EbpB and its predicted catalytic Cys residue was required for efficient cell wall anchoring of mature Ebp pili. Thus, we have defined molecular interactions involved in fiber polymerization, minor subunit organization, and pilus subcellular compartmentalization in the E. faecalis Ebp pilus system. These studies advance our understanding of unique molecular mechanisms of sortase-assembled pilus biogenesis.

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The ancillary protein 1 of Streptococcus pyogenes FCT‐1 pili mediates cell adhesion and biofilm formation through heterophilic as well as homophilic interactions

Cited by 42 publications

References 44 publications

Pilus Biogenesis in Lactococcus lactis: Molecular Characterization and Role in Aggregation and Biofilm Formation

Pilus Biogenesis in Lactococcus lactis: Molecular Characterization and Role in Aggregation and Biofilm Formation

The Group A Streptococcus serotype M2 pilus plays a role in host cell adhesion and immune evasion

Pilin and Sortase Residues Critical for Endocarditis- and Biofilm-Associated Pilus Biogenesis in Enterococcus faecalis

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