Chapter 15 : Sortases, Surface Proteins, and Their Roles in Disease and Vaccine Development

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Prior to bacterial genome sequencing and the genetic analysis of pathogenesis, microbiologists identified molecules on microbial surfaces and studied their role in disease processes ( ). The ultimate goal of this research was the identification of molecular formulations inciting antibody responses in vaccine recipients that prevented disease yet would otherwise not cause harm ( ). Oswald Avery’s discovery of the pneumococcus capsule and the demonstration that capsular polysaccharide vaccine protects against pneumococcal pneumonia represent an important paradigm ( ). Another was Rebecca Lancefield’s characterization of M protein as the determinant of type-specific immunity against , the causative agent of streptococcal pharyngitis and rheumatic fever ( ). Lancefield and Sjöquist required proteases or peptidoglycan (murein) hydrolases, but not membrane detergents, to solubilize surface proteins of Gram-positive bacteria ( ). The underlying reason for this biochemical phenomenon is that surface proteins are covalently linked to peptidoglycan at their C-terminal ends ( ).

Citation: Schneewind O, Missiakas D. 2019. Sortases, Surface Proteins, and Their Roles in Disease and Vaccine Development, p 173-188. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0004-2018
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Figure 1

Sortase-mediated anchoring to the cell wall envelope of using SpA as a model substrate. Drawing to illustrate the primary structure of the SpA precursor with its N-terminal signal peptide and signal peptidase cleavage site, the five immunoglobulin binding domains (IgBDs), region X (Xr) LysM domain, and C-terminal LPXTG motif sorting signal with cleavage site for sortase A. Cell wall SpA is linked to peptidoglycan via an amide bond between the carboxyl group of the C-terminal threonine and the amino group of the pentaglycine cross bridge. Released SpA is liberated from the cell wall envelope via the action of several murein hydrolases. Drawing to illustrate secretion of SpA precursor, sortase-mediated cleavage of SpA precursor and acyl enzyme formation, resolution of the acyl enzyme by lipid II to generate SpA linked to lipid II, incorporation of SpA into the cell wall via the transpeptidation and transglycosylation reaction, and release of SpA from the cell wall envelope by murein hydrolases. Released SpA bears the overall structure -Ala–-iGln–-Lys(SpA-LPET-Gly)–-AlaGly.

Citation: Schneewind O, Missiakas D. 2019. Sortases, Surface Proteins, and Their Roles in Disease and Vaccine Development, p 173-188. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0004-2018
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Image of Figure 2
Figure 2

Biological functions of staphylococcal protein A (SpA). and its antibiotic-resistant isolates (MRSA) harbor SpA in the cell wall envelope or released into the extracellular milieu (released SpA). Cell wall SpA binds Fcγ of human and animal IgG (green segment within blue IgG) and blocks the effector functions of antibodies, thereby preventing opsonophagocytic killing (OPK) of MRSA by immune cells through interference with complement (CR1) and Fcγ receptors (FcγRs). Released SpA cross-links V3-clonal B cell receptors (V3-BCR on the surface of B cells), triggering B cell proliferation and secretion of V3-clonal IgM and IgG (pink segments within blue IgG) without antigen specificity for . This B cell superantigen activity (BCSA) of SpA produces irrelevant V3-clonal IgG and prevents the establishment of protective immunity against . Drawing to illustrate the primary structure of human IgG with variable (V and V) and conserved (C, C1, C2, and C3) light (L) and heavy (H) chains, their antigen-binding paratope (Ag), V3, and Fcγ domains. SpA binding sites at V3 heavy chains and Fcγ are in pink and green, respectively.

Citation: Schneewind O, Missiakas D. 2019. Sortases, Surface Proteins, and Their Roles in Disease and Vaccine Development, p 173-188. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0004-2018
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cell wall-anchored surface proteins

Citation: Schneewind O, Missiakas D. 2019. Sortases, Surface Proteins, and Their Roles in Disease and Vaccine Development, p 173-188. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0004-2018

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