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Chapter 40 : Staphylococcal Sortases and Surface Proteins

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Abstract:

This chapter reviews what is known about surface proteins of , their mechanisms of anchoring to the cell wall envelope, and their contributions to the pathogenesis of staphylococcal infections. Protein A amino acid sequence, gene sequence, and three dimensional nuclear magnetic resonance and X-ray diffraction structures revealed a molecule comprised of five nearly identical Ig-binding domains as well as the molecular elements involved in binding Ig. strains clump in the presence of plasma; this phenomenon, which has been exploited for diagnostic purposes, is the product of a molecular interaction between two microbial surface components recognizing adhesive matrix molecules (MSCRAMMS), clumping factor A and B, with fibrinogen. Both and strains encode for multiple cell wall-anchored surface proteins with large serine-aspartate repeat (Sdr) domains. In addition to the subset of sortase-anchored cell wall surface proteins that are covalently attached to the cell wall, there are also a number of surface proteins that lack a C-terminal cell wall sorting signal, yet remain in one way or another cell wall associated. The current model for the uptake of heme-iron by the Isd proteins states that IsdA, IsdB, and IsdH would interact with host hemoproteins such as hemoglobin (Hb), haptoglobin (Hpt), and/or hemopexin, which are released after erythrocyte lysis. The study and characterization of these and other cell wall-associated proteins has provided much insight into the understanding of the interactions of with its environment.

Citation: Dedent A, Marraffini L, Schneewind O. 2006. Staphylococcal Sortases and Surface Proteins, p 486-495. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch40
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FIGURE 1

Sortase-mediated anchoring of staphylococcal surface proteins. In order to catalyze the covalent linkage of a polypeptide to the cell wall, the sortase enzyme must recognize and act on two substrates: the surface protein and the peptidoglycan. Sortase protein substrates are first synthesized in the cytoplasm as a full-length precursor (P1) containing an N-terminal signal peptide (SP) and a C-terminal sorting signal. The signal peptide directs the cellular export of the polypeptide through the Sec system and is cleaved by a signal peptidase upon secretion. This results in the generation of P2 precursor, a shorter protein containing only the sorting signal. During the export of this precursor the hydrophobic and positively charged sequences of the sorting signal act as a “stop transfer” element, leading to the retention of P2 in the bacterial membrane. Sortase contains a signal peptide/membrane anchor sequence that localizes the enzyme to the membrane. Hence the LPTG motif of the P2 precursor is accessible to the cysteine residue of the sortase active site. The thiol group attacks the peptide bond between the T and G of the LPTG motif, generating an acyl intermediate (i.e., sortase and the protein substrate linked through a thioester bond). Lipid II, the peptidoglycan synthesis precursor, constitutes the cell wall substrate of sortase. Lipid II contains a single peptidoglycan subunit (GlcNAc-MurNAc-l-Ala-d-iGln-l-Lys (-NH-Gly5)-d-Ala-d-Ala-COH) associated to the bacterial membrane through an undecaprenyl phosphate group. Its synthesis occurs in the cytoplasm by the successive enzymatic addition of -acetylmuramic acid (MN), the cell wall peptide residues (l-Ala, d-iGln, l-Lys, and d-Ala-d-Ala), -acetylglucosamine (GN), and each of the glycines of the cross bridge via a tRNA donor to a UDP carrier. The peptidoglycan subunit thus generated is transferred from UDP to undecaprenyl phosphate, which in turn is translocated to the outer side of the membrane. There, lipid II is subjected to the transglycosylase and transpeptidase activities of penicillin-binding proteins during peptidoglycan polymerization. In the sorting reaction, the free amino group of the pentaglycine cross bridge of lipid II attacks the acyl intermediate, linking the C-terminal threonine of the surface protein to lipid II (P3) and regenerating the sortase active site. This constitutes the mature (M) form of the surface protein. Incorporation of this modified peptidoglycan subunit into the growing cell wall subsequently positions the surface protein in the cell envelope (M, mature form).

Citation: Dedent A, Marraffini L, Schneewind O. 2006. Staphylococcal Sortases and Surface Proteins, p 486-495. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch40
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Image of FIGURE 2
FIGURE 2

Anchored Isd proteins facilitate the transport of heme-iron through the staphylococcal cell wall. The (iron-regulated surface determinants) locus in is composed of three transcriptional units, , and (, sortase B). IsdA and IsdB contain an LPXTG motif, are anchored to the cell wall by sortase A, and are exposed in the outside of the cell. IsdC contains an NPQTN motif and is anchored by sortase B. In contrast to sortase A substrates, IsdC is buried in the cell wall, and it is anchored to poorly cross-linked peptidoglycan. IsdD is an integral membrane protein, IsdE is a lipoprotein, and IsdF represents a subunit of an oligomeric ABC transporter. IsdG is a heme-oxygenase. The current model for the uptake of heme-iron by the Isd proteins states that IsdA, IsdB, and IsdH would interact with host hemoproteins such as hemoglobin (Hb), haptoglobin (Hpt), and/or hemopexin, which are released after erythrocyte lysis. The interaction would result in the sequestration of heme-iron by IsdA, IsdB, and IsdH. IsdC would serve as an intermediate heme-iron receptor between the outer cell surface and membrane components of the Isd system, thus occupying a central role in the passage of heme-iron across the staphylococcal cell wall. IsdEDF would facilitate the passage of heme through the bacterial membrane. In the cytoplasm, IsdG and IsdI would degrade the porphyrine ring and release the iron for use by the bacterium.

Citation: Dedent A, Marraffini L, Schneewind O. 2006. Staphylococcal Sortases and Surface Proteins, p 486-495. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch40
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Tables

Generic image for table
TABLE 1

Cell-wall-anchored surface proteins of

Surface protein, identified as containing a C-terminal cell-wall sorting signal.

AA, protein length in amino acids.

Ligand, molecular component(s) recognized and bound by protein.

Motif, consensus motif recognized by sortase and present in C-terminal cell-wall sorting signal.

Citation: Dedent A, Marraffini L, Schneewind O. 2006. Staphylococcal Sortases and Surface Proteins, p 486-495. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch40
Generic image for table
TABLE 2

Cell-wall-associated surface proteins of

Surface-associated protein, localization to cell wall, but lacking a C-terminal cell-wall sorting signal.

AA, protein length in amino acids.

Ligand, molecular component(s) recognized and bound by protein.

Cell wall association, interaction with and targeting to cell wall.

Signal peptide, presence or absence of an N-terminal leader peptide directing protein to SEC pathway.

Citation: Dedent A, Marraffini L, Schneewind O. 2006. Staphylococcal Sortases and Surface Proteins, p 486-495. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch40

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