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Volume 270, Number 23, Issue of June 9, pp. 13932-13936, 1995
©1995 by The American Society for Biochemistry and Molecular Biology, Inc.
The Enterotoxin from Clostridium difficile (ToxA) Monoglucosylates the Rho Proteins

Ingo Just , Matthias Wilm , Jörg Selzer , Gundula Rex , Christoph von Eichel-Streiber , Matthias Mann , Klaus Aktories

The enterotoxin from Clostridium difficile (ToxA) is one of the causative agents of the antibiotic-associated pseudomembranous colitis. In cultured monolayer cells ToxA exhibits cytotoxic activity to induce disassembly of the actin cytoskeleton, which is accompanied by morphological changes. ToxA-induced depolymerization of actin filaments is correlated with a decrease in the ADP-ribosylation of the low molecular mass GTP-binding Rho proteins (Just, I., Selzer, J., von Eichel-Streiber, C., and Aktories, K.(1995) J. Clin. Invest. 95, 1026-1031). Here we report on the identification of the ToxA-induced modification of Rho. Applying electrospray mass spectrometry, the mass of the modification was determined as 162 Da, which is consistent with the incorporation of a hexose into Rho. From several hexoses tested UDP-glucose selectively served as cosubstrate for ToxA-catalyzed modification. The acceptor amino acid of glucosylation was identified from a Lys-C-generated peptide by tandem mass spectrometry as Thr-37. Mutation of Thr-37 to Ala completely abolished glucosylation. The members of the Rho family (RhoA, Rac1, and Cdc42Hs) were substrates for ToxA, whereas H-Ras, Rab5, and Arf1 were not glucosylated. ToxA-catalyzed glucosylation of lysates from ToxA-pretreated rat basophilic leukemia (RBL) cells resulted in a decreased incorporation of [C]glucose, indicating previous glucosylation in the intact cell. Glucosylation of the Rho subtype proteins appears to be the molecular mechanism by which C. difficile ToxA mediates its cytotoxic effects on cells.



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Infect. Immun., June 1, 1998; 66(6): 2755 - 2761.
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J. A. Kink and J. A. Williams
Antibodies to Recombinant Clostridium difficile Toxins A and B Are an Effective Treatment and Prevent Relapse of C. difficile-Associated Disease in a Hamster Model of Infection
Infect. Immun., May 1, 1998; 66(5): 2018 - 2025.
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F. Hofmann, C. Busch, and K. Aktories
Chimeric Clostridial Cytotoxins: Identification of the N-Terminal Region Involved in Protein Substrate Recognition
Infect. Immun., March 1, 1998; 66(3): 1076 - 1081.
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J. K. Linevsky, C. Pothoulakis, S. Keates, M. Warny, A. C. Keates, J. T. Lamont, and C. P. Kelly
IL-8 release and neutrophil activation by Clostridium difficile toxin-exposed human monocytes
Am J Physiol Gastrointest Liver Physiol, December 1, 1997; 273(6): G1333 - G1340.
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E Johansson, E Jennische, S Lange, and I Lonnroth
Antisecretory factor suppresses intestinal inflammation and hypersecretion
Gut, November 1, 1997; 41(5): 642 - 645.
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J Salcedo, S Keates, C Pothoulakis, M Warny, I Castagliuolo, J T LaMont, and C P Kelly
Intravenous immunoglobulin therapy for severe Clostridium difficile colitis
Gut, September 1, 1997; 41(3): 366 - 370.
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C. Fiorentini, A. Fabbri, G. Flatau, G. Donelli, P. Matarrese, E. Lemichez, L. Falzano, and P. Boquet
Escherichia coli Cytotoxic Necrotizing Factor 1 (CNF1), a Toxin That Activates the Rho GTPase
J. Biol. Chem., August 1, 1997; 272(31): 19532 - 19537.
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S. Wesselborg, M. K. A. Bauer, M. Vogt, M. L. Schmitz, and K. Schulze-Osthoff
Activation of Transcription Factor NF-kappa B and p38 Mitogen-activated Protein Kinase Is Mediated by Distinct and Separate Stress Effector Pathways
J. Biol. Chem., May 9, 1997; 272(19): 12422 - 12429.
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B. B. Finlay and P. Cossart
Exploitation of Mammalian Host Cell Functions by Bacterial Pathogens
Science, May 2, 1997; 276(5313): 718 - 725.
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F. Hofmann, C. Busch, U. Prepens, I. Just, and K. Aktories
Localization of the Glucosyltransferase Activity of Clostridium difficile Toxin B to the N-terminal Part of the Holotoxin
J. Biol. Chem., April 25, 1997; 272(17): 11074 - 11078.
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H. M. Lacerda, G. D. Pullinger, A. J. Lax, and E. Rozengurt
Cytotoxic Necrotizing Factor 1from Escherichia coli and Dermonecrotic Toxin from Bordetella bronchiseptica Induce p21rho-dependent Tyrosine Phosphorylation of Focal Adhesion Kinase and Paxillin in Swiss 3T3 Cells
J. Biol. Chem., April 4, 1997; 272(14): 9587 - 9596.
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J. Selzer, F. Hofmann, G. Rex, M. Wilm, M. Mann, I. Just, and K. Aktories
Clostridium novyi alpha -Toxin-catalyzed Incorporation of GlcNAc into Rho Subfamily Proteins
J. Biol. Chem., October 11, 1996; 271(41): 25173 - 25177.
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I. Just, Jör. Selzer, F. Hofmann, G. A. Green, and K. Aktories
Inactivation of Ras by Clostridium sordellii Lethal Toxin-catalyzed Glucosylation
J. Biol. Chem., April 26, 1996; 271(17): 10149 - 10153.
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M. R. Popoff, E. Chaves-Olarte, E. Lemichez, C. von Eichel-Streiber, M. Thelestam, P. Chardin, D. Cussac, B. Antonny, P. Chavrier, G. Flatau, et al.
Ras, Rap, and Rac Small GTP-binding Proteins Are Targets for Clostridium sordellii Lethal Toxin Glucosylation
J. Biol. Chem., April 26, 1996; 271(17): 10217 - 10224.
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U. Prepens, I. Just, C. von Eichel-Streiber, and K. Aktories
Inhibition of Fc[IMAGE]RI-mediated Activation of Rat Basophilic Leukemia Cells by Clostridium difficile Toxin B (Monoglucosyltransferase)
J. Biol. Chem., March 29, 1996; 271(13): 7324 - 7329.
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E. Chaves-Olarte, I. Florin, P. Boquet, M. Popoff, C. von Eichel-Streiber, and M. Thelestam
UDP-Glucose Deficiency in a Mutant Cell Line Protects against Glucosyltransferase Toxins from Clostridium difficile and Clostridium sordellii
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H. Barth, G. Pfeifer, F. Hofmann, E. Maier, R. Benz, and K. Aktories
Low pH-induced Formation of Ion Channels by Clostridium difficile Toxin B in Target Cells
J. Biol. Chem., March 30, 2001; 276(14): 10670 - 10676.
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D. Gineitis and R. Treisman
Differential Usage of Signal Transduction Pathways Defines Two Types of Serum Response Factor Target Gene
J. Biol. Chem., June 29, 2001; 276(27): 24531 - 24539.
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C. Wilde, H. Genth, K. Aktories, and I. Just
Recognition of RhoA by Clostridium botulinum C3 Exoenzyme
J. Biol. Chem., May 26, 2000; 275(22): 16478 - 16483.
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N. Mani and B. Dupuy
Regulation of toxin synthesis in Clostridium difficile by an alternative RNA polymerase sigma factor
PNAS, May 8, 2001; 98(10): 5844 - 5849.
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