Co-operative binding of human fibronectin to SfbI protein triggers streptococcal invasion into respiratory epithelial cells

Talay, Susanne R.; Zock, Angela; Rohde, Manfred; Molinari, Gabriella; Oggioni, Marco R.; Pozzi, Gianni; Guzmán, Carlos A.; Chhatwal, Gursharan S.

doi:10.1046/j.1462-5822.2000.00076.x

Cited by 107 publications

(136 citation statements)

References 53 publications

Supporting

Mentioning

131

Contrasting

Unclassified

Order By: Relevance

“…The GBD is known to associate with segments of these bacterial proteins (32,33) raising the possibility of competition with collagen for FN binding. Such binding could have significant functional implications for tissue changes induced during bacterial colonization.…”

Section: Discussionmentioning

confidence: 99%

Identification and structural analysis of type I collagen sites in complex with fibronectin fragments

Erat¹,

Slatter

Lowe

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

136

View full text Add to dashboard Cite

Collagen and fibronectin are major components of vertebrate extracellular matrices. Their association and distribution control the development and properties of diverse tissues, but thus far no structural information has been available for the complex formed. Here, we report binding of a peptide, derived from the ␣1 chain of type I collagen, to the gelatin-binding domain of human fibronectin and present the crystal structure of this peptide in complex with the 8 -9 FnI domain pair. Both gelatin-binding domain subfragments, 6 FnI 1-2 FnII 7 FnI and 8 -9 FnI, bind the same specific sequence on D-period 4 of collagen I ␣1, adjacent to the MMP-1 cleavage site. 8 -9 FnI also binds the equivalent sequence of the ␣2 chain. The collagen peptide adopts an antiparallel ␤-strand conformation, similar to structures of proteins from pathogenic bacteria bound to FnI domains. Analysis of the type I collagen sequence suggests multiple putative fibronectin-binding sites compatible with our structural model. We demonstrate, by kinetic unfolding experiments, that the triple-helical collagen state is destabilized by 8 -9 FnI. This finding suggests a role for fibronectin in collagen proteolysis and tissue remodeling.collagen destabilization ͉ extracellular matrix ͉ protein structure C ollagen is the most abundant protein in mammals, accounting for Ϸ25% of the body-protein content. It is crucial for effects as diverse as cell differentiation, cell migration, and mechanical properties of tissues. Many human diseases have their origin in mutations that affect interactions of collagen with other extracellular matrix (ECM) molecules and cell receptors (1). Type I collagen fibrils form spontaneously in vitro; in vivo, however, formation requires integrin receptors and fibronectin (FN) (2). FN is a large glycosylated protein composed of multiple copies of 3 classes of domains, FnI, FnII, and FnIII, that forms fibrils in the ECM (3). It plays a role in many important physiological processes, such as embryogenesis, wound healing, hemostasis, and thrombosis (4), and disruption of the FN gene is embryonic lethal in mice (5).The interaction of these 2 proteins has long been demonstrated in vitro by using denatured collagen (gelatin) (6, 7) and isolated collagen type I chains or chain fragments (8, 9). The collagen-binding site on FN has been localized to the 42-kDa gelatin-binding domain (GBD; for an overview of FN and collagen fragments see Fig. 1) (10, 11), and anti-GBD antibodies inhibit collagen organization in fibroblast cultures (12). Similarly, experiments in cultures have identified the collagenase/ MMP-1 (13) cleavage site in type I collagen as important for FN-mediated attachment of fibroblasts to collagen ECM (14). Peptides spanning that region (15) or MMP-1 cleavage at this site (6) inhibit attachment. However, attempts to reconstitute the FN-collagen interaction in vitro by using synthetic peptides failed to find strong, specific, interactions (8,9), and the precise sequence determinants for FN-binding to collagen remained unknown...

show abstract

Section: Discussionmentioning

confidence: 99%

Identification and structural analysis of type I collagen sites in complex with fibronectin fragments

Erat¹,

Slatter

Lowe

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

136

View full text Add to dashboard Cite

show abstract

“…In fact, interactions of S. suis with both fibronectin and plasminogen may play a role in some of these mechanisms. For example, fibronectinbinding proteins of streptococci and staphylococci have been reported to mediate bacterial adhesion to and invasion of host cells (Oehmcke et al, 2004;Talay et al, 2000;Valentin-Weigand et al, 1993). In the case of S. suis, it has been demonstrated recently that S. suis adhesion to and intracellular invasion of PBMEC increases more than 500 and 700 %, respectively, when bacteria are precoated with fibronectin (Vanier et al, 2007a).…”

Section: Discussionmentioning

confidence: 99%

Isolation and characterization of α-enolase, a novel fibronectin-binding protein from Streptococcus suis

et al. 2008

View full text Add to dashboard Cite

Streptococcus suis is an important swine pathogen that causes meningitis, endocarditis, arthritis and septicaemia. As a zoonotic agent, S. suis also causes similar diseases in humans. Binding of pathogenic bacteria to extracellular matrix components enhances their adhesion to and invasion of host cells. In the present study we isolated and identified a novel fibronectin-binding protein from S. suis. The native protein (designated SsEno) possessed not only high homology with other bacterial enolases but also enolase activity. We cloned, expressed and purified SsEno and showed that it is ubiquitously expressed by all S. suis serotypes and we identified its surface localization using immunoelectron microscopy. ELISA demonstrated that SsEno binds specifically to fibronectin and plasminogen in a lysine-dependent manner. Additional surface plasmon resonance assays demonstrated that SsEno binds to fibronectin or plasminogen with low nanomolar affinity. Inhibition experiments with anti-SsEno antibodies also showed that bacterial SsEno is important for the adhesion to and invasion of brain microvascular endothelial cells by S. suis. Overall, the present work is the first study, to our knowledge, to demonstrate a fibronectinbinding activity of a bacterial enolase, and shows that, similar to other bacterial fibronectin-binding proteins, SsEno may contribute to the virulence of S. suis. INTRODUCTIONStreptococcus suis is a major swine pathogen that causes septicaemia, meningitis, endocarditis and arthritis (Higgins & Gottschalk, 2005). Of the 35 known serotypes, serotype 2 is the most frequently isolated and associated with disease (Higgins & Gottschalk, 2005). It has been proposed that two serotypes (serotypes 32 and 34) be excluded from S. suis and redesignated Streptococcus orisratti (Hill et al., 2005). S. suis, especially serotype 2, has also been described as an important zoonotic agent that affects people in close contact with infected pigs or pork-derived products (Lun et al., 2007). Indeed, an important number of cases of human disease with a high rate of mortality in China were linked directly to a concurrent outbreak of S. suis infection in pigs (Ye et al., 2006).Little is known about S. suis virulence factors. The capsule polysaccharide (CPS) is a critical virulence factor, given that unencapsulated isogenic mutants are completely avirulent and rapidly cleared from the circulation in pig and mouse infection models (Charland et al., 2000;Smith et al., 1999). However, non-virulent strains are also encapsulated, indicating that the virulence of this pathogen is a multifactorial process . Other potential virulence factors have also been described in S. suis, including a haemolysin (suilysin), a 136 kDa muramidase-released protein (MRP), a 110 kDa extracellular factor (EF) protein, a hyaluronidase, a superoxide dismutase, various proteases, a serum opacity factor and different adhesins (Baums et al., 2006;.The pathogenesis of S. suis infection is not fully understood and likely involves many steps . Binding between b...

show abstract

“…However, the UR construct, as defined by Ozeri et al (39), contains, according to our definition of FnBRs, an almost complete FnBR (SfbI-1) that would bind to the NTD. Because the N-terminal region of this UR construct contains a GBF-binding site (40), this might explain the high affinity binding of this construct to Fn. Talay and co-workers (40) suggest an anti-parallel binding mode of SfbI to Fn where the FnBR region interacts with the NTD and activates binding of UR to GBF.…”

Section: Discussionmentioning

confidence: 99%

“…1). In previous definitions PyFF1 was included in the adjacent functional region of SfbI, the UR segment (see "Discussion") (39,40). (Fig.…”

Section: Dissection Approach-the Interactions Of Threementioning

confidence: 99%

High Affinity Streptococcal Binding to Human Fibronectin Requires Specific Recognition of Sequential F1 Modules

Schwarz‐Linek

Pilka

Pickford

et al. 2004

Journal of Biological Chemistry

View full text Add to dashboard Cite

Fibronectin (Fn) binding by the Streptococcus pyogenes protein SfbI has been shown to trigger integrindependent internalization of this pathogen by human epithelial and endothelial cells. Here, using nuclear magnetic resonance spectroscopy and isothermal titration calorimetry in a dissection approach, the basis for the specificity and high affinity of the interaction between the N-terminal domain of Fn and SfbI is revealed. Each of the five Fn type 1 modules is directly involved in the interaction and is recognized by short consecutive motifs within the repeat region of SfbI. Crucially, these motifs must be combined in the correct order to form a high affinity ligand for the N-terminal domain of Fn.

show abstract

Co-operative binding of human fibronectin to SfbI protein triggers streptococcal invasion into respiratory epithelial cells

Cited by 107 publications

References 53 publications

Identification and structural analysis of type I collagen sites in complex with fibronectin fragments

Identification and structural analysis of type I collagen sites in complex with fibronectin fragments

Isolation and characterization of α-enolase, a novel fibronectin-binding protein from Streptococcus suis

High Affinity Streptococcal Binding to Human Fibronectin Requires Specific Recognition of Sequential F1 Modules

Contact Info

Product

Resources

About