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Mechanism of action of choleragen andE. coli heat-labile enterotoxin: activation of adenylate cyclase by ADP-ribosylation

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Summary

Choleragen exerts its effects on cells through the activation of adenylate cyclase. The initial event appears to be the binding of the B subunit of the toxin to ganglioside GM1 on the cell surface, following which there is a delay prior to activation of adenylate cyclase. Patching and capping of the toxin on the cell surface, perhaps involved in the internalization of the enzymatically active subunit, may be occuring during this time. The activation of adenylate cyclase, which is catalyzed by the A1 peptide of choleragen, does not require the B subunit or ganglioside GM1. The A1 peptide catalyzes the transfer of ADP-ribose from NAD to an amino acid, probably arginine, in a 42 000 dalton membrane protein. This protein appears to be the GTP-binding component (or G/F factor) of the adenylate cyclase system and is cruical to the regulation of cyclase activity by hormones such as epinephrine. ADP-ribosylation of the G/F factor is enhanced by GTP and, in some systems, by a cytosolic factor. GTP is also required for stabilization and optimal catalytic function of the choleragen-activated cyclase. Calmodulin, a calcium-binding protein, is necessary for expression of catalytic activity of the toxin-activated adenylate cyclase in brain and other tissues.

The ADP-ribosyltransferase activity required for activation of the cyclase is an intrinsic property of the A1 peptide of choleragen which is expressed only after the peptide is released from the holotoxin by reduction of a single disulfide bond. In the absence of cellular components, choleragen catalyzes the ADP-ribosylation of small guanidino compounds such as arginine as well as peptides and proteins that contain arginine. It is assumed, therefore, that the site of ADP-ribosylation in the natural acceptor protein is an arginine or similar amino acid. When guanidino compounds are not present as ADP-ribose acceptors, choleragen hydrolyzes NAD to ADP-ribose and nicotinamide at a considerably slower rate.

E. coli heat-labile enterotoxin (LT) is very similar to choleragen in structure and function. It consists of two types of subunits, A and B, with sizes comparable to those of the A and B subunits of choleragen. Binding of LT to the cell surface is enhanced by prior incorporation of GM1 but not other gangliosides; the oligosaccharide of GM1 specifically interacts with LT and its B subunit. The A subunit of LT exhibits ADP-ribosyltransferase activity following activation by thiol to release the A1 peptide. The A subunit of LT can be isolated in an ‘unnicked’ form and thus requires, in addition to reduction by a thiol, proteolytic cleavage to generate the active A1 peptide. Like choleragen, LT uses guanidino compounds as model ADP-ribose acceptors and catalyzes the ADP-ribosylation of a 42 000 dalton protein in cell membrane prepatations.

ADP-ribosyltransferases that use arginine as ADP-ribose acceptors are not restricted to bacterial systems; such an enzyme has been purified to apparent homogeneity (>500 000-fold) from turkey erythrocytes. Based on a subunit molecular weight of 28 000, its turnover number with arginine as the ADP-ribose acceptor is considerably higher than that of either toxin. Although with low molecular weight guanidino derivatives the substrate specificity of the enzyme is similar to that of choleragen, with protein substrates it clearly differs. The physiological role of the turkey erythrocyte transferase remains to be established.

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  1. Laboratory of Cellular Metabolism, National Heart, Lung, and Blood Institute, National Institutes of Health, 20205, Bethesda, MD, USA

    Joel Moss & Martha Vaughan

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Moss, J., Vaughan, M. Mechanism of action of choleragen andE. coli heat-labile enterotoxin: activation of adenylate cyclase by ADP-ribosylation. Mol Cell Biochem 37, 75–90 (1981). https://doi.org/10.1007/BF02354931

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