Abstract
The antigenically distinct Shiga-like toxins (SLTs) SLT-1 and SLT-II are cytotoxic for both Vero and HeLa cells and use Gal alpha 1-4Gal beta 1-4Glc beta 1-1Cer (Gb3) molecules as functional receptors. SLT-II-related variants SLT-IIvp and SLT-IIvh, produced by a porcine isolate and a human isolate, respectively, are cytotoxic for Vero but not HeLa cells. To investigate the basis for these differences in cytotoxic specificity among SLTs, the nature of the receptor for the SLT-II variants was examined. First, the patterns of binding of SLT-II and the SLT-II variants to Gb3 receptor analogs Gal alpha 1-4Gal-bovine serum albumin and Gal alpha 1-4Gal beta 1-4Glc-bovine serum albumin were compared. SLT-IIvp bound the trisaccharide neoglycoprotein preferentially, while SLT-IIvh bound both analogs equally but with less affinity than did SLT-II. Next, the glycolipids to which the SLT-II variants bound in Vero and HeLa cells were identified by thin-layer chromatography. SLT-IIvp bound to Gb3, GalNAc beta 1-3Gal alpha 1-4Gal beta 1-4Glc beta 1-1Cer (Gb4), and Gal beta 1-3GalNAc beta 1-3Gal alpha 1-4Gal beta 1-4Glc beta 1-1Cer (Gb5) in Vero cells but only Gb3 in HeLa cells. However, SLT-IIvh bound to Gal alpha 1-4Gal beta 1-1Cer (Gb2) and Gb3 in HeLa cells but only Gb3 in Vero cells. In addition, hybrid toxins (SLT-IIvp subunit A with SLT-II subunit B or SLT-II subunit A with SLT-IIvp subunit B) were used to show that the receptor specificities of the SLTs was B subunit specific. These differences in receptor specificities are important in vivo, as evidenced by a 400-fold difference in the 50% lethal doses of purified SLT-IIvp and SLT-II (200 versus 0.5 ng, respectively) for mice. These data indicate that SLT-II-cytotoxic variants can occur as a consequence of differences in receptor specificity and affinity.
MeSH Terms
Animals
Bacterial Toxins/metabolism,toxicity
Enterotoxins/metabolism
Enzyme-Linked Immunosorbent Assay
Escherichia coli/pathogenicity
Female
Glycoconjugates/metabolism
Glycolipids/analysis,metabolism
Guanylate Cyclase
HeLa Cells
Lethal Dose 50
Mice
Mice, Inbred BALB C
Receptors, Cell Surface/analysis,metabolism
Receptors, Enterotoxin
Receptors, Guanylate Cyclase-Coupled
Receptors, Peptide
Shiga Toxin 1
Shiga Toxin 2
Vero Cells
Chemicals
Bacterial Toxins
Enterotoxins
Glycoconjugates
Glycolipids
Receptors, Cell Surface
Receptors, Peptide
Shiga Toxin 1
Shiga Toxin 2
Guanylate Cyclase
Receptors, Enterotoxin
Receptors, Guanylate Cyclase-Coupled
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Samuel J E
Department of Microbiology, Uniformed Services University of the Health Sciences, Bethesda, Maryland 20814.
Perera L P
Ward S
O'Brien A D
Ginsburg V
Krivan H C
References (32)
32 references, click to expand
-
Recognition of galactosylgloboside by monoclonal antibodies derived from patients with primary lung cancer.
Proc Natl Acad Sci U S A. 1988 Jun;85(12):4441-5
PMID: 2837767
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Escherichia coli K99 binds to N-glycolylsialoparagloboside and N-glycolyl-GM3 found in piglet small intestine.
Arch Biochem Biophys. 1989 Apr;270(1):391-7
PMID: 2648997
-
Glycolipid binding of purified and recombinant Escherichia coli produced verotoxin in vitro.
J Biol Chem. 1987 Jun 25;262(18):8834-9
PMID: 3298243
-
Ribonuclease activity associated with the 60S ribosome-inactivating proteins ricin A, phytolaccin and Shiga toxin.
Biochem Biophys Res Commun. 1985 Jul 31;130(2):879-84
PMID: 3839673
-
Pathogenesis of shigella diarrhea. XI. Isolation of a shigella toxin-binding glycolipid from rabbit jejunum and HeLa cells and its identification as globotriaosylceramide.
J Exp Med. 1986 Jun 1;163(6):1391-404
PMID: 3519828
-
Purification and characterization of a Shigella dysenteriae 1-like toxin produced by Escherichia coli.
Infect Immun. 1983 May;40(2):675-83
PMID: 6341244
-
Edema disease-like brain lesions in gnotobiotic piglets infected with Escherichia coli serotype O157:H7.
Infect Immun. 1989 Apr;57(4):1339-42
PMID: 2647636
-
Cloning and sequencing of a Shiga-like toxin type II variant from Escherichia coli strain responsible for edema disease of swine.
J Bacteriol. 1988 Sep;170(9):4223-30
PMID: 3045088
-
Gangliosides: structure, isolation, and analysis.
Methods Enzymol. 1982;83:139-91
PMID: 7047999
-
The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli.
J Infect Dis. 1985 May;151(5):775-82
PMID: 3886804
-
Detection of gangliosides that bind cholera toxin: direct binding of 125I-labeled toxin to thin-layer chromatograms.
Anal Biochem. 1980 Dec;109(2):399-402
PMID: 7224165
-
Pathogenesis of edema disease in swine: pathologic effects of hemolysin, autolysate, and endotoxin of Escherichia coli (O141).
Am J Vet Res. 1976 Jan;37(1):15-24
PMID: 1108715
-
Preparation of iodine-131 labelled human growth hormone of high specific activity.
Nature. 1962 May 5;194:495-6
PMID: 14450081
-
Cloning of genes for production of Escherichia coli Shiga-like toxin type II.
Infect Immun. 1987 Nov;55(11):2675-80
PMID: 2822579
-
Pathogenesis of Shigella diarrhea. XIV. Analysis of Shiga toxin receptors on cloned HeLa cells.
J Infect Dis. 1989 May;159(5):881-9
PMID: 2651533
-
Shiga and Shiga-like toxins.
Microbiol Rev. 1987 Jun;51(2):206-20
PMID: 3299029
-
Globotetraosylceramide is recognized by the pig edema disease toxin.
J Biol Chem. 1989 Jul 25;264(21):12520-5
PMID: 2663859
-
Isolation and characterization of glycosphingolipid from animal cells and their membranes.
Methods Enzymol. 1974;32:345-67
PMID: 4374628
-
Globotriosyl ceramide is specifically recognized by the Escherichia coli verocytotoxin 2.
Biochem Biophys Res Commun. 1988 Apr 29;152(2):674-9
PMID: 3284526
-
Pathogenesis of Shigella diarrhea: rabbit intestinal cell microvillus membrane binding site for Shigella toxin.
Infect Immun. 1986 Aug;53(2):372-7
PMID: 3755421
-
Quantitative microtiter cytotoxicity assay for Shigella toxin.
J Clin Microbiol. 1980 Sep;12(3):361-6
PMID: 7012172
-
Identification of the carbohydrate receptor for Shiga toxin produced by Shigella dysenteriae type 1.
J Biol Chem. 1987 Feb 5;262(4):1779-85
PMID: 3543013
-
In vivo formation of hybrid toxins comprising Shiga toxin and the Shiga-like toxins and role of the B subunit in localization and cytotoxic activity.
Infect Immun. 1989 Dec;57(12):3743-50
PMID: 2807546
-
Purification and some properties of a Vero toxin from a human strain of Escherichia coli that is immunologically related to Shiga-like toxin II (VT2).
Microb Pathog. 1989 Feb;6(2):113-22
PMID: 2654533
-
Pathogenesis of Shigella diarrhea. IX. Simplified high yield purification of Shigella toxin and characterization of subunit composition and function by the use of subunit-specific monoclonal and polyclonal antibodies.
J Exp Med. 1984 Dec 1;160(6):1767-81
PMID: 6392471
-
Interaction of Shigella shigae cytotoxin with receptors on sensitive and insensitive cells.
J Recept Res. 1980;1(2):199-213
PMID: 6895387
-
Affinity purification and characterization of Shiga-like toxin II and production of toxin-specific monoclonal antibodies.
Infect Immun. 1988 Aug;56(8):1926-33
PMID: 3294179
-
Shiga-like toxin converting phage of enterohemorrhagic Escherichia coli strain 933.
Microb Pathog. 1989 May;6(5):381-90
PMID: 2671581
-
Cloning and sequencing of the genes for Shiga toxin from Shigella dysenteriae type 1.
J Bacteriol. 1988 Mar;170(3):1116-22
PMID: 2830229
-
Production of Shigella dysenteriae type 1-like cytotoxin by Escherichia coli.
J Infect Dis. 1982 Dec;146(6):763-9
PMID: 6754826
-
Two toxin-converting phages from Escherichia coli O157:H7 strain 933 encode antigenically distinct toxins with similar biologic activities.
Infect Immun. 1986 Jul;53(1):135-40
PMID: 3522426