A ‘Collagen Hug’ Model for Staphylococcus aureus CNA binding to collagen

Zong, Yinong; Xu, Yi; Liang, Xiaowen; Keene, Douglas R.; Höök, Agneta; Gurusiddappa, Shivasankarappa; Höök, Magnus; Narayana, S.V.L.

doi:10.1038/sj.emboj.7600888

Cited by 205 publications

(281 citation statements)

References 40 publications

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“…In addition to the peptide structures, there are high resolution structures of complexes of a triple-helical peptide bound to the I domain of integrin 19 and one bound to a bacterial cell surface receptor. 20 The high-resolution structures of collagen-like peptides confirm the basic triple-helical model and show details of hydration, hydrogen bonding, and helical parameters.…”

Section: X-ray Crystallography Of Triple-helical Peptidesmentioning

confidence: 54%

Triple‐helical peptides: An approach to collagen conformation, stability, and self‐association

et al. 2008

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Peptides have been an integral part of the collagen triple‐helix structure story, and have continued to serve as useful models for biophysical studies and for establishing biologically important sequence‐structure‐function relationships. High resolution structures of triple‐helical peptides have confirmed the basic Ramachandran triple‐helix model and provided new insights into the hydration, hydrogen bonding, and sequence dependent helical parameters in collagen. The dependence of collagen triple‐helix stability on the residues in its (Gly‐X‐Y)n repeating sequence has been investigated by measuring melting temperatures of host‐guest peptides and an on‐line collagen stability calculator is now available. Although the presence of Gly as every third residue is essential for an undistorted structure, interruptions in the repeating (Gly‐X‐Y)n amino acid sequence pattern are found in the triple‐helical domains of all nonfibrillar collagens, and are likely to play a role in collagen binding and degradation. Peptide models indicate that small interruptions can be incorporated into a rod‐like triple‐helix with a highly localized effect, which perturbs hydrogen bonds and places the standard triple‐helices on both ends out of register. In contrast to natural interruptions, missense mutations which replace one Gly in a triple‐helix domain by a larger residue have pathological consequences, and studies on peptides containing such Gly substitutions clarify their effect on conformation, stability, and folding. Recent studies suggest peptides may also be useful in defining the basic principles of collagen self‐association to the supramolecular structures found in tissues. © 2008 Wiley Periodicals, Inc. Biopolymers 89: 345–353, 2008.This article was originally published online as an accepted preprint. The “Published Online” date corresponds to the preprint version. You can request a copy of the preprint by emailing the Biopolymers editorial office at biopolymers@wiley.com

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Section: X-ray Crystallography Of Triple-helical Peptidesmentioning

confidence: 54%

Triple‐helical peptides: An approach to collagen conformation, stability, and self‐association

et al. 2008

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“…Defective sortase recognition or failure to present the Lys residue of the pilin motif appropriately would explain the loss of pilus assembly when intramolecular isopeptide bonds in SpaA or BcpA are deleted by mutation of the catalytic Asp/Glu. The isopeptide bonds in CnaA and GBS52 may similarly influence the binding of partner molecules, because their isopeptide bond-containing domains are important for specific binding of collagen (CnaA) and capable of binding to human pulmonary epithelial cells (GBS52) (15,29).…”

Section: Discussionmentioning

confidence: 99%

The Corynebacterium diphtheriae shaft pilin SpaA is built of tandem Ig-like modules with stabilizing isopeptide and disulfide bonds

Kang

Paterson

Gaspar

et al. 2009

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

104

166

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Cell-surface pili are important virulence factors that enable bacterial pathogens to adhere to specific host tissues and modulate host immune response. Relatively little is known about the structure of Gram-positive bacterial pili, which are built by the sortase-catalyzed covalent crosslinking of individual pilin proteins. Here we report the 1.6-Å resolution crystal structure of the shaft pilin component SpaA from Corynebacterium diphtheriae , revealing both common and unique features. The SpaA pilin comprises 3 tandem Ig-like domains, with characteristic folds related to those typically found in non-pilus adhesins. Whereas both the middle and the C-terminal domains contain an intramolecular Lys–Asn isopeptide bond, previously detected in the shaft pilins of Streptococcus pyogenes and Bacillus cereus , the middle Ig-like domain also harbors a calcium ion, and the C-terminal domain contains a disulfide bond. By mass spectrometry, we show that the SpaA monomers are cross-linked in the assembled pili by a Lys–Thr isopeptide bond, as predicted by previous genetic studies. Together, our results reveal that despite profound dissimilarities in primary sequences, the shaft pilins of Gram-positive pathogens have strikingly similar tertiary structures, suggesting a modular backbone construction, including stabilizing intermolecular and intramolecular isopeptide bonds.

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“…The topology of the D1 domain in other LRC collagen-binding proteins appears to be more favorable to collagen binding and to make the D1 domain a more likely candidate collagen-binding site than it is in OSCAR. Furthermore, a large conformational change would be required for the D2 domain of these proteins to interact with collagen at the corresponding region, in a manner analogous to a collagen hug seen with the Staphylococcus aureus collagen binding adhesion CNA (31). It also is likely that such an interaction may be restricted because of the lack of a large D1-D2 domain linker in LRC proteins.…”

Section: Discussionmentioning

confidence: 99%

Structural basis of collagen recognition by human osteoclast-associated receptor and design of osteoclastogenesis inhibitors

Haywood

Chen

et al. 2016

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

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Human osteoclast-associated receptor (OSCAR) is an immunoglobulin (Ig)-like collagen receptor that is up-regulated on osteoclasts during osteoclastogenesis and is expressed in a range of myeloid cells. As a member of the leukocyte receptor complex family of proteins, OSCAR shares a high degree of sequence and structural homology with other collagen receptors of this family, including glycoprotein VI, leukocyte-associated Ig-like receptor-1, and leukocyte Ig-like receptor B4, but recognizes a unique collagen sequence. Here, we present the crystal structures of OSCAR in its free form and in complex with a triple-helical collagen-like peptide (CLP). These structures reveal that the CLP peptide binds only one of the two Ig-like domains, the membrane-proximal domain (domain 2) of OSCAR, with the middle and trailing chain burying a total of 661 Å 2 of solvent-accessible collagen surface. This binding mode is facilitated by the unusual topography of the OSCAR protein, which displays an obtuse interdomain angle and a rotation of domain 2 relative to the membrane-distal domain 1. Moreover, the binding of the CLP to OSCAR appears to be mediated largely by tyrosine residues and conformational changes at a shallow Phe pocket. Furthermore, we investigated CLP peptides as inhibitors of osteoclastogenesis and found that a peptide length of 40 amino acids is required to ensure adequate inhibition of osteoclastogenesis in vitro. These findings provide valuable structural insights into the mode of collagen recognition by OSCAR and into the use of synthetic peptide matrikines for osteoclastogenesis inhibition.C ollagen is a highly versatile family of proteins consisting of more than 28 members that achieve a high degree of complexity through association of different collagen types, the use of multiple transcription initiation sites, alternative splicing patterns, posttranslational modifications, and a wide range of expression patterns (1). Despite this heterogeneity, studies of collagen over the past 60 y have revealed that collagens are commonly found as large fibrillar structures consisting of varying lengths of righthanded triple-helical structures that are formed by association of three left-handed polyproline type II helices with a one-residue stagger (2, 3). Crucial to the formation of these triple helical structures are the repetitive amino acid triplet sequences G-X-Y, of which the most frequently observed triplet is G-P-O, with O representing 4-hydroxyproline (4). In these structures the obligate glycine of the triplet is buried toward the center of the helix and is solvent inaccessible, whereas the X and Y residues are solvent accessible with the latter providing crucial stability to collagen fibrils through interchain hydrogen bonding (3). The diversity of imino and amino acids within these X and Y repetitive sequences are thought to result in changes in the helical parameters of collagen, which vary from a tight left-handed 7 2 to a looser 10 3 helical symmetry, and could provide a more flexible and accessible motif fo...

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A ‘Collagen Hug’ Model for Staphylococcus aureus CNA binding to collagen

Cited by 205 publications

References 40 publications

Triple‐helical peptides: An approach to collagen conformation, stability, and self‐association

Triple‐helical peptides: An approach to collagen conformation, stability, and self‐association

The Corynebacterium diphtheriae shaft pilin SpaA is built of tandem Ig-like modules with stabilizing isopeptide and disulfide bonds

Structural basis of collagen recognition by human osteoclast-associated receptor and design of osteoclastogenesis inhibitors

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