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Gene Review

exoS  -  exoenzyme S

Pseudomonas aeruginosa PAO1

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Disease relevance of exoS

  • Expression of Pseudomonas aeruginosa exoS is controlled by quorum sensing and RpoS [1].
  • With the addition of exoS and exoT to the molecular arsenal, questions concerning in vivo toxicity and target specificities of exoenzyme S can be directly addressed [2].
  • The exoT open reading frame, cloned into a T7 expression system, produced a 53-kDa protein in Escherichia coli, termed Exo53, which reacted to antisera against exoenzyme S. A histidine-tagged derivative of recombinant Exo53 possessed approximately 0.2% of the ADP-ribosyltransferase activity of recombinant ExoS [3].
  • By using an approach in which exoS was expressed in different strains of Yersinia, including secretion and translocation mutants, we could demonstrate that ExoS was secreted and translocated into HeLa cells by a similar mechanism to that described previously for YopE [4].
  • There was no significant difference in exoU or exoS prevalence among the keratitis strains [5].

High impact information on exoS


Chemical compound and disease context of exoS


Biological context of exoS

  • Clinical isolates that injure lung epithelium in vivo and that are cytotoxic in vitro possess exoT but lack exoS, suggesting that ExoS is not the cytotoxin responsible for the pathology and cell death measured in these assays [13].
  • Evidence is provided for downregulation of exoS during biofilm formation of P. aeruginosa PAO1 [1].
  • Upregulation of exoS'-gfp in the PDO100 mutant could be repressed to normal level by adding C4-HSL autoinducer, indicating a negative regulatory effect of RhlR/C4-HSL on exoS expression [1].
  • The aim of this study was to develop a real time RT-PCR method for the direct quantification of the transcripts of three P. aeruginosa virulence genes: exoS, lasI and algD, during the first seven days of a rat lung infection [14].
  • Our results demonstrate correlations among exoU or exoS genotype, TTSS phenotype, and O serotype in bacteremic P. aeruginosa isolates [15].

Anatomical context of exoS


Associations of exoS with chemical compounds

  • Exoenzyme S modifies all of its substrates at arginine residues [21].
  • Exoenzyme S absolutely requires a soluble eukaryotic protein, which we have named FAS (Factor Activating exoenzyme S), in order to ADP-ribosylate all substrates [22].
  • Raf-1 kinase and exoenzyme S interact with 14-3-3zeta through a common site involving lysine 49 [23].
  • Exotoxin A, exoenzyme S, phospholipase C, elastase, and total protease activities were suppressed by antibiotics at concentrations as low as 1/20 of the MIC over a 24-h period in broth [24].
  • Exoenzyme S differs from toxin A and diphtheria toxin in that it does not adenosine diphosphate (ADP)-ribosylate elongation factor-2, but rather catalyzes the transfer of the ADP-ribose moiety of nicotinamide adenine dinucleotide to a number of different proteins in extracts of eucaryotic cells [25].

Other interactions of exoS

  • In contrast, the exoS, exoU and exoY genes were variable traits [26].
  • A fimV mutant was unable to induce the expression of exoS, exoT and exsA genes under type III inducing conditions, thus exhibiting a defect in type III protein secretion [27].
  • Hybridization with the toxA internal probe produced a 0.8-kb hybridizing fragment, whereas hybridization with the exoS internal probe produced either a 2.0- or a 2.3-kb hybridizing fragment [28].
  • The majority of isolates (59%) were PCR-positive for exoU rather than for exoS (38%), and carried a-type fliC genes (76%) rather than b-type (24%) [29].
  • In general, the rate of multidrug resistance in the exoU positive cytotoxic and serotype E (O:11) strains was significantly higher than in exoS positive invasive strains (p < 0.01) [5].

Analytical, diagnostic and therapeutic context of exoS

  • To determine the genetic relationship between the two forms of exoenzyme S, exoS (encoding the 49-kDa form) was used as a probe in Southern blot analyses of P. aeruginosa chromosomal digests [3].
  • The two P. aeruginosa strains used in these studies, 388 and 388delta exoS, maintained genetic identity, with the exception that strain 388delta exoS lacked production of the 49-kDa form of ExoS [30].
  • Combined data from mutagenesis, regulatory, expression, and sequence analyses provide strong evidence that P. aeruginosa possesses a type III secretion apparatus which is required for the export of exoenzyme S and potentially other co-ordinately regulated proteins [31].
  • The exoenzyme S (ExoS)-producing Pseudomonas aeruginosa strain, 388, and corresponding ExoS knock-out strain, 388deltaexoS, were used in a bacterial and mammalian co-culture system as a model for the contact-dependent delivery of ExoS into host cells [32].
  • Exoenzyme S expression was measured in parental and mutant derivatives by Western blot (immunoblot) analysis and ADP-ribosyltransferase activity measurement [33].


  1. Expression of Pseudomonas aeruginosa exoS is controlled by quorum sensing and RpoS. Hogardt, M., Roeder, M., Schreff, A.M., Eberl, L., Heesemann, J. Microbiology (Reading, Engl.) (2004) [Pubmed]
  2. Genetic analysis of exoenzyme S expression by Pseudomonas aeruginosa. Goranson, J., Frank, D.W. FEMS Microbiol. Lett. (1996) [Pubmed]
  3. Genetic relationship between the 53- and 49-kilodalton forms of exoenzyme S from Pseudomonas aeruginosa. Yahr, T.L., Barbieri, J.T., Frank, D.W. J. Bacteriol. (1996) [Pubmed]
  4. Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Frithz-Lindsten, E., Du, Y., Rosqvist, R., Forsberg, A. Mol. Microbiol. (1997) [Pubmed]
  5. Type III Secretion System-Associated Toxins, Proteases, Serotypes, and Antibiotic Resistance of Pseudomonas aeruginosa Isolates Associated with Keratitis. Zhu, H., Conibear, T.C., Bandara, R., Aliwarga, Y., Stapleton, F., Willcox, M.D. Curr. Eye Res. (2006) [Pubmed]
  6. The eukaryotic host factor that activates exoenzyme S of Pseudomonas aeruginosa is a member of the 14-3-3 protein family. Fu, H., Coburn, J., Collier, R.J. Proc. Natl. Acad. Sci. U.S.A. (1993) [Pubmed]
  7. Pseudomonas aeruginosa exoenzyme S: an adenosine diphosphate ribosyltransferase distinct from toxin A. Iglewski, B.H., Sadoff, J., Bjorn, M.J., Maxwell, E.S. Proc. Natl. Acad. Sci. U.S.A. (1978) [Pubmed]
  8. Pseudomonas aeruginosa exoenzyme S ADP-ribosylates Ras at multiple sites. Ganesan, A.K., Frank, D.W., Misra, R.P., Schmidt, G., Barbieri, J.T. J. Biol. Chem. (1998) [Pubmed]
  9. Pseudomonas aeruginosa exoenzyme S disrupts Ras-mediated signal transduction by inhibiting guanine nucleotide exchange factor-catalyzed nucleotide exchange. Ganesan, A.K., Vincent, T.S., Olson, J.C., Barbieri, J.T. J. Biol. Chem. (1999) [Pubmed]
  10. 14-3-3zeta binds a phosphorylated Raf peptide and an unphosphorylated peptide via its conserved amphipathic groove. Petosa, C., Masters, S.C., Bankston, L.A., Pohl, J., Wang, B., Fu, H., Liddington, R.C. J. Biol. Chem. (1998) [Pubmed]
  11. Purification of Pseudomonas aeruginosa exoenzyme S. Woods, D.E., Que, J.U. Infect. Immun. (1987) [Pubmed]
  12. The glycerolipid receptor for Helicobacter pylori (and exoenzyme S) is phosphatidylethanolamine. Lingwood, C.A., Huesca, M., Kuksis, A. Infect. Immun. (1992) [Pubmed]
  13. ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Finck-Barbançon, V., Goranson, J., Zhu, L., Sawa, T., Wiener-Kronish, J.P., Fleiszig, S.M., Wu, C., Mende-Mueller, L., Frank, D.W. Mol. Microbiol. (1997) [Pubmed]
  14. Relative expression of Pseudomonas aeruginosa virulence genes analyzed by a real time RT-PCR method during lung infection in rats. Joly, B., Béatrice, J., Pierre, M., Maud, P., Auvin, S., Stéphane, A., Colin, F., Franc Cois, C., Gottrand, F., Frédéric, G., Guery, B., Benoit, G., Husson, M.O. FEMS Microbiol. Lett. (2005) [Pubmed]
  15. Genotypic and phenotypic analysis of type III secretion system in a cohort of Pseudomonas aeruginosa bacteremia isolates: evidence for a possible association between O serotypes and exo genes. Berthelot, P., Attree, I., Plésiat, P., Chabert, J., de Bentzmann, S., Pozzetto, B., Grattard, F. J. Infect. Dis. (2003) [Pubmed]
  16. Exoenzyme S shows selective ADP-ribosylation and GTPase-activating protein (GAP) activities towards small GTPases in vivo. Henriksson, M.L., Sundin, C., Jansson, A.L., Forsberg, A., Palmer, R.H., Hallberg, B. Biochem. J. (2002) [Pubmed]
  17. Different domains of Pseudomonas aeruginosa exoenzyme S activate distinct TLRs. Epelman, S., Stack, D., Bell, C., Wong, E., Neely, G.G., Krutzik, S., Miyake, K., Kubes, P., Zbytnuik, L.D., Ma, L.L., Xie, X., Woods, D.E., Mody, C.H. J. Immunol. (2004) [Pubmed]
  18. Intracellular expression of the ADP-ribosyltransferase domain of Pseudomonas exoenzyme S is cytotoxic to eukaryotic cells. Pederson, K.J., Barbieri, J.T. Mol. Microbiol. (1998) [Pubmed]
  19. Pseudomonas aeruginosa exoenzyme S is a mitogen but not a superantigen for human T lymphocytes. Bruno, T.F., Buser, D.E., Syme, R.M., Woods, D.E., Mody, C.H. Infect. Immun. (1998) [Pubmed]
  20. Pseudomonas aeruginosa exoenzyme S stimulates murine lymphocyte proliferation in vitro. Barclay, N.G., Spurrell, J.C., Bruno, T.F., Storey, D.G., Woods, D.E., Mody, C.H. Infect. Immun. (1999) [Pubmed]
  21. Several GTP-binding proteins, including p21c-H-ras, are preferred substrates of Pseudomonas aeruginosa exoenzyme S. Coburn, J., Wyatt, R.T., Iglewski, B.H., Gill, D.M. J. Biol. Chem. (1989) [Pubmed]
  22. Pseudomonas aeruginosa exoenzyme S requires a eukaryotic protein for ADP-ribosyltransferase activity. Coburn, J., Kane, A.V., Feig, L., Gill, D.M. J. Biol. Chem. (1991) [Pubmed]
  23. Raf-1 kinase and exoenzyme S interact with 14-3-3zeta through a common site involving lysine 49. Zhang, L., Wang, H., Liu, D., Liddington, R., Fu, H. J. Biol. Chem. (1997) [Pubmed]
  24. Inhibition of Pseudomonas aeruginosa exoenzyme expression by subinhibitory antibiotic concentrations. Grimwood, K., To, M., Rabin, H.R., Woods, D.E. Antimicrob. Agents Chemother. (1989) [Pubmed]
  25. Production of exoenzyme S by clinical isolates of Pseudomonas aeruginosa. Sokol, P.A., Iglewski, B.H., Hager, T.A., Sadoff, J.C., Cross, A.S., McManus, A., Farber, B.F., Iglewski, W.J. Infect. Immun. (1981) [Pubmed]
  26. Prevalence of type III secretion genes in clinical and environmental isolates of Pseudomonas aeruginosa. Feltman, H., Schulert, G., Khan, S., Jain, M., Peterson, L., Hauser, A.R. Microbiology (Reading, Engl.) (2001) [Pubmed]
  27. The truA gene of Pseudomonas aeruginosa is required for the expression of type III secretory genes. Ahn, K.S., Ha, U., Jia, J., Wu, D., Jin, S. Microbiology (Reading, Engl.) (2004) [Pubmed]
  28. Analysis of Pseudomonas aeruginosa clinical isolates for possible variations within the virulence genes exotoxin A and exoenzyme S. Rumbaugh, K.P., Hamood, A.N., Griswold, J.A. J. Surg. Res. (1999) [Pubmed]
  29. Genotypic and phenotypic characteristics of Pseudomonas aeruginosa isolates associated with ulcerative keratitis. Winstanley, C., Kaye, S.B., Neal, T.J., Chilton, H.J., Miksch, S., Hart, C.A. J. Med. Microbiol. (2005) [Pubmed]
  30. Effects of differential expression of the 49-kilodalton exoenzyme S by Pseudomonas aeruginosa on cultured eukaryotic cells. Olson, J.C., McGuffie, E.M., Frank, D.W. Infect. Immun. (1997) [Pubmed]
  31. Exoenzyme S of Pseudomonas aeruginosa is secreted by a type III pathway. Yahr, T.L., Goranson, J., Frank, D.W. Mol. Microbiol. (1996) [Pubmed]
  32. ADP-ribosylation of oncogenic Ras proteins by pseudomonas aeruginosa exoenzyme S in vivo. Vincent, T.S., Fraylick, J.E., McGuffie, E.M., Olson, J.C. Mol. Microbiol. (1999) [Pubmed]
  33. Construction and characterization of chromosomal insertional mutations of the Pseudomonas aeruginosa exoenzyme S trans-regulatory locus. Frank, D.W., Nair, G., Schweizer, H.P. Infect. Immun. (1994) [Pubmed]
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