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Chapter 21 : Trafficking of Cholera Toxin and Related Bacterial Enterotoxins: Pathways and Endpoints

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Abstract:

This chapter focuses on toxins of the cholera family as a paradigm for the opportunistic invasion of the mammalian intestine by exploitation of eukaryotic mechanisms of membrane trafficking, protein transport, and signal transduction. Cholera toxin (CT) enters epithelial cells of the human intestine after binding specific lipids on the host cell apical membrane. The mechanism of toxin entry is a near mirror image of protein biosynthesis in eukaryotic cells. CT represents one of the best-characterized virulence factors produced by pathogenic microorganisms, and its mode of action is discussed in detail. Labile toxins from that are antigenically similar to CT are classified as type I toxins. Montesano and coauthors first reported the localization of gold-labeled CT in non-clathrin-coated membrane invaginations of cultured liver cells and proposed the existence of at least two distinct pathways for internalization of surface-bound ligands. Human intestinal epithelial cells, however, express low levels of caveolin-1 and -2 and do not exhibit caveolae as assessed morphologically. In eukaryotic cells, translocation of nascent proteins into the endoplasmic reticulum (ER) occurs via the protein conducting channel Sec61, termed as the translocon. Recent studies indicate that protein translocation through the translocon and protein folding in the ER are reversible processes.

Citation: Rodighiero C, Lencer W. 2003. Trafficking of Cholera Toxin and Related Bacterial Enterotoxins: Pathways and Endpoints, p 385-402. In Hecht G (ed), Microbial Pathogenesis and the Intestinal Epithelial Cell. ASM Press, Washington, DC. doi: 10.1128/9781555817848.ch21

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Figures

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FIGURE 1

Schematic representation of the structural organization of some AB toxins. (Top, from left) CT together with heat-labile enterotoxins type I and II (LT); Shiga toxin (ShT) together with Shiga-like toxins (ShLTs); pertussis toxin (PT). (Bottom, from left) Ricin toxin (RT), PEA, and diphtheria toxin (DT). Identical shapes indicate conserved functional domains, where receptor-binding subunits are cylinders, ADP-ribosyltransferase catalytic subunits are triangles, -glycosidase catalytic subunits are ovals, and translocation domains are cubes. The A domain of C/LT and Shiga and Shiga-like toxins can also be divided into an N-terminal domain (A1) and a C-terminal domain (A2) that anchor domain A1 to the pentameric binding component. The pair of scissors indicates a proteolysis-sensitive loop, and disulfide bonds are also represented (S-S). The ER retention sequence at the C terminus of the A2 fragment of Ctx is KDEL (represented) and RDEL for LT (omitted), while for PEA the signal is REDLK (represented).

Citation: Rodighiero C, Lencer W. 2003. Trafficking of Cholera Toxin and Related Bacterial Enterotoxins: Pathways and Endpoints, p 385-402. In Hecht G (ed), Microbial Pathogenesis and the Intestinal Epithelial Cell. ASM Press, Washington, DC. doi: 10.1128/9781555817848.ch21
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Image of FIGURE 2
FIGURE 2

Trafficking model for CT. Toxin enters the cell by binding to the apical surface of the polarized epithelium via G and association with lipid rafts (1). Toxin moves via endosomes to the Golgi network (2), where the C-terminal KDEL motif facilitates retrograde movement of the CT-GM1 complex to the ER (3). Release and translocation of the A-subunit occur in the ER and is a process mediated by PDI (4), while the B-subunit undergoes Golgi/ER recycling prior to degradation (5). Once in the cytosol, the A-subunit is transported to the basolateral membrane where the Gs/adenylate cyclase complex is located (6). ADP-ribosylation of the heterotrimeric GTPase Gsα by the toxin, produces an increase of intracellular cyclic AMP (cAMP) (7) that causes an active secretion of chloride (8).

Citation: Rodighiero C, Lencer W. 2003. Trafficking of Cholera Toxin and Related Bacterial Enterotoxins: Pathways and Endpoints, p 385-402. In Hecht G (ed), Microbial Pathogenesis and the Intestinal Epithelial Cell. ASM Press, Washington, DC. doi: 10.1128/9781555817848.ch21
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Tables

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TABLE 1

Selection of AB enterotoxins

Citation: Rodighiero C, Lencer W. 2003. Trafficking of Cholera Toxin and Related Bacterial Enterotoxins: Pathways and Endpoints, p 385-402. In Hecht G (ed), Microbial Pathogenesis and the Intestinal Epithelial Cell. ASM Press, Washington, DC. doi: 10.1128/9781555817848.ch21

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