Expression and cytoprotective activity of the small GTPase RhoB induced by the Escherichia coli cytotoxic necrotizing factor 1

Int J Biochem Cell Biol. 2013 Aug;45(8):1767-75. doi: 10.1016/j.biocel.2013.05.020. Epub 2013 May 31.

Abstract

RhoB is the only member of the Rho subfamily of small GTPases, which is classified as an immediate early gene product. RhoB is up-regulated in response to growth factors as well as cytotoxic and genotoxic agents. Clostridial glucosylating toxins have been reported to evoke pronounced RhoB expression, based on the inactivation of Rho/Ras proteins. In this study, we report on a long lasting expression of RhoB in cultured cells upon activation of Rho proteins by the cytotoxic necrotizing factor 1 (CNF1) from Escherichia coli. The observations of this study highlight a new pathway involving Rac1, which positively regulates the activity of the rhoB promoter and RhoB expression. Conversely, the isomeric cytotoxic necrotizing factor from Yersinia pseudotuberculosis (CNFy) drives GTP-loading of basal RhoB but fails to cause activation of the rhoB promoter and thus its expression. CNF1 inhibits cytokinesis and induces the formation of bi-nucleated (tetraploid) cells. Upon long term treatment with CNF1, RhoB(-/-) mouse embryonic fibroblasts (MEFs) exhibit DNA fragmentation, phosphatidylserine exposure, and loss of membrane integrity, while RhoB(+/-) MEFs persist as bi-nucleated (tetraploid) cells without any signs of cell death. In conclusion, the cytoprotective RhoB response is not only evoked by bacterial protein toxins inactivating Rho/Ras proteins but also by the Rac1-activating toxin CNF1.

Keywords: Apoptosis; CNF1; Clostridium difficile Toxin B; Cytokinesis; Deamidation; Glucosylation; Lethal Toxin from C. sordellii; Multi-nucleation; Ras; Rho; TcdA; TcdB; TcsL; Toxin A from C. difficile strain; Toxin B from C. difficile strain; cytotoxic necrotizing factor from E. coli; cytotoxic necrotizing factor from Y. pseudotuberculosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Toxins / pharmacology*
  • Cell Death / drug effects
  • Cell Shape / drug effects
  • Cytoprotection / drug effects*
  • Enzyme Activation / drug effects
  • Escherichia coli / metabolism*
  • Escherichia coli Proteins / pharmacology*
  • Gene Expression Regulation / drug effects
  • HT29 Cells
  • HeLa Cells
  • Humans
  • Mice
  • NIH 3T3 Cells
  • Polyploidy
  • Promoter Regions, Genetic / genetics
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Transcriptional Activation / drug effects
  • Yersinia pseudotuberculosis / metabolism
  • rac1 GTP-Binding Protein / metabolism
  • rhoB GTP-Binding Protein / genetics
  • rhoB GTP-Binding Protein / metabolism*

Substances

  • Bacterial Toxins
  • Escherichia coli Proteins
  • RNA, Messenger
  • cytotoxic necrotizing factor type 1
  • rac1 GTP-Binding Protein
  • rhoB GTP-Binding Protein