Intracellular localization modulates targeting of ExoS, a type III cytotoxin, to eukaryotic signalling proteins

Molecular Microbiology

Volumn 46, Issue 5, 2002, Pages 1381-1390

  Pederson, Kristin J ^a,b   Krall, Rebecca ^a   Riese, Matthew J ^a   Barbieri, Joseph T ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Public Health Laboratory Division   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CYTOTOXIN; CYTOTOXIN TYPE 3; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE; HYBRID PROTEIN; MEMBRANE PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN EXOS; PROTEIN MLD; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; ACTIN; PHOTOPROTEIN; PROTEIN HISTIDINE KINASE; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE; RAS PROTEIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CYTOLOGY; CYTOSOL; CYTOTOXICITY; EUKARYOTIC CELL; GENE DELETION; GOLGI COMPLEX; MEMBRANE LOCALIZATION DOMAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN TARGETING; PSEUDOMONAS AERUGINOSA; RESIDUE ANALYSIS; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; CHO CELL; CYTOSKELETON; GENETICS; HAMSTER; METABOLISM; PATHOGENICITY;

ANIMALIA; EUKARYOTA; NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

ACTINS; ADP RIBOSE TRANSFERASES; ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CYTOSKELETON; CYTOTOXINS; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; PROTEIN KINASES; PSEUDOMONAS AERUGINOSA; RAS PROTEINS; RECOMBINANT FUSION PROTEINS;

EID: 0036887054     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2002.03256.x     Document Type: Article

References (52)

1. Ahnert-Hilger, G., Wegenhorst, U., Stecher, B., Spicher, K., Rosenthal, W., and Gratz, M. (1992) Exocytosis from permeabilized bovine adrenal chromaffin cells is differently modulated by guanosine 5′-[gamma-thio]triphosphate and guanosine 5′-[beta gamma-imido]triphosphate. Evidence for the involvement of various guanine nucleotide-binding proteins. Biochem J 284: 321-326.
2. Aktories, K. (1997) Rho proteins: targets for bacterial toxins. Trends Microbiol 5: 282-288.
3. Barbieri, J.T. (2000) Pseudomonas aeruginosa exoenzyme S, a bifunctional type-III secreted cytotoxin. Int J Med Microbiol 290: 381-387.
4. Barz, C., Abahji, T.N., Trulzsch, K., and Heesemann, J. (2000) The Yersinia Ser/Thr protein kinase YpkA/YopO directly interacts with the small GTPases RhoA and Rac1. FEBS Lett 482: 139-143.
5. Black, D.S., and Bliska, J.B. (2000) The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence. Mol Microbiol 37: 515-527.
6. Bliska, J.B., Clemens, J.C., Dixon, J.E., and Falkow, S. (1992) The Yersinia tyrosine phosphatase: specificity of a bacterial virulence determinant for phosphoproteins in the J774A.1 macrophage. J Exp Med 176: 1625-1630.
7. Boyd, A.P., Lambermont, I., and Cornelis, G.R. (2000) Competition between the Yops of Yersinia enterocolitica for delivery into eukaryotic cells: role of the SycE chaperone binding domain of YopE. J Bacteriol 182: 4811-4821.
8. Buss, J.E., Quilliam, L.A., Kato, K., Casey, P.J., Solski, P.A., Wong, G., et al. (1991) The COOH-terminal domain of the Rap1A (Krev-1) protein is isoprenylated and supports transformation by an H-Ras:Rap1A chimeric protein. Mol Cell Biol 11: 1523-1530.
9. Coburn, J., Dillon, S.T., Iglewski, B.H., and Gill, D.M. (1989) Exoenzyme S of Pseudomonas aeruginosa ADP-ribosylates the intermediate filament protein vimentin. Infect Immun 57: 996-998.
10. Evdokimov, A.G., Tropea, J.E., Routzahn, K.M., and Waugh, D.S. (2002) Crystal structure of the Yersinia pestis GTPase activator YopE. Protein Sci 11: 401-408.
11. Fields, K.A., and Straley, S.C. (1999) LcrV of Yersinia pestis enters infected eukaryotic cells by a virulence plasmid-independent mechanism. Infect Immun 67: 4801-4813.
12. Fleming, I.N., Elliott, C.M., and Exton, J.H. (1996) Differential translocation of rho family GTPases by lysophosphatidic acid, endothelin-1, and platelet-derived growth factor. J Biol Chem 271: 33067-33073.
13. Frank, D.W. (1997) The exoenzyme S regulon of Pseudomonas aeruginosa. Mol Microbiol 26: 621-629.
14. Fu, Y., and Galan, J.E. (1998) The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol Microbiol 27: 359-368.
15. Fu, Y., and Galan, J.E. (1999) A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion (in process citation). Nature 401: 293-297.
16. Ganesan, A.K., Frank, D.W., Misra, R.P., Schmidt, G., and Barbieri, J.T. (1998) Pseudomonas aeruginosa exoenzyme S ADP-ribosylates Ras at multiple sites. J Biol Chem 273: 7332-7337.
17. Ganesan, A.K., Mende-Mueller, L., Seizer, J., and Barbieri, J.T. (1999a) Pseudomonas aeruginosa exoenzyme S, a double ADP-ribosyltransferase, resembles vertebrate mono-ADP-ribosyltransferases. J Biol Chem 274: 9503-9508.
18. Ganesan, A.K., Vincent, T.S., Olson, J.C., and Barbieri, J.T. (1999b) Pseudomonas aeruginosa exoenzyme S disrupts Ras-mediated signal transduction by inhibiting guanine nucleotide exchange factor-catalyzed nucleotide exchange. J Biol Chem 274: 21823-21829.
19. Giamarellou, H. (2000) Therapeutic guidelines for Pseudomonas aeruginosa infections. Int J Antimicrob Agents 16: 103-106.
20. Goehring, U.M., Schmidt, G., Pederson, K.J., Aktories, K., and Barbieri, J.T. (1999) The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating Protein for Rho GTPases. J Biol Chem 274: 36369-36372.
21. Hakansson, S., Galyov, E.E., Rosqvist, R., and Wolf-Watz, H. (1996) The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane. Mol Microbiol 20: 593-603.
22. Hancock, J.F., Cadwallader, K., and Marshall, C.J. (1991a) Methylation and proteolysis are essential for efficient membrane binding of prenylated p21K-ras (B). EMBO J 10: 641-646.
23. Hancock, J.F., Cadwallader, K., Paterson, H., and Marshall, C.J. (1991b) A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO J 10: 4033-4039.
24. Hart, M.J., Jiang, X., Kozasa, T., Roscoe, W., Singer, W.D., Gilman, A.G., et al. (1998) Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by Galpha13. Science 280: 2112-2114.
25. Hori, Y., Kikuchi, A., Isomura, M., Katayama, M., Miura, Y., Fujioka, H., et al. (1991) Post-translational modifications of the C-terminal region of the rho protein are important for its interaction with membranes and the stimulatory and inhibitory GDP/GTP exchange proteins. Oncogene 6: 515-522.
26. Igdoura, S.A., Herscovics, A., Lal, A., Moremen, K.W., Morales, C.R., and Hermo, L. (1999) Alpha-mannosidases involved in N-glycan processing show cell specificity and distinct subcompartmentalization within the Golgi apparatus of cells in the testis and epididymis. Eur J Cell Biol 78: 441-452.
27. Krall, R., Schmidt, G., Aktories, K., and Barbieri, J.T. (2000) Pseudomonas aeruginosa ExoT is a Rho GTPase-activating protein. Infect Immun 68: 6066-6068.
28. Krall, R., Sun, J., Pederson, K.J., and Barbieri, J.T. (2002) In vivo rho GTPase-activating protein activity of Pseudomonas aeruginosa cytotoxin ExoS. Infect Immun 70: 360-367.
29. Kulich, S.M., Frank, D.W., and Barbieri, J.T. (1993) Purification and characterization of exoenzyme S from Pseudomonas aeruginosa 388. Infect Immun 61: 307-313.
30. Kulich, S.M., Frank, D.W., and Barbieri, J.T. (1995) Expression of recombinant exoenzyme S of Pseudomonas aeruginosa. Infect Immun 63: 1-8.
31. McGuffie, E.M., Fraylick, J.E., Hazen-Martin, D.J., Vincent, T.S., and Olson, J.C. (1999) Differential sensitivity of human epithelial cells to Pseudomonas aeruginosa exoenzyme S. Infect Immun 67: 3494-3503.
32. Maresso, A.W., and Barbieri, J.T. (2002) (in press).
33. Mammoto, A., Takahashi, K., Sasaki, T., and Takai, Y. (2000) Stimulation of Rho GDI release by ERM proteins. Methods Enzymol 325: 91-101.
34. Michaelson, D., Silletti, J., Murphy, G., D'Eustachio, P., Rush, M., and Philips, M.R. (2001) Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol 152: 111-126.
35. Moremen, K.W., Touster, O., and Robbins, P.W. (1991) Novel purification of the catalytic domain of Golgi alpha-mannosidase II. Characterization and comparison with the intact enzyme. J Biol Chem 266: 16876-16885.
36. Nobes, C.D., and Hall, A. (1995) Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81: 53-62.
37. Nobes, C.D., and Hall, A. (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144: 1235-1244.
38. Oh-Eda, M., Nakagawa, H., Akama, T.O., Lowitz, K., Misago, M., Moremen, K.W., and Fukuda, M.N. (2001) Overexpression of the Golgi-localized enzyme alpha-mannosidase IIx in Chinese hamster ovary cells results in the conversion of hexamannosyl-N-acetylchitobiose to tetramannosyl-N-acetylchitobiose in the N-glycan- processing pathway. Eur J Biochem 268: 1280-1288.
39. Pederson, K.J., and Barbieri, J.T. (1998) Intracellular expression of the ADP-ribosyltransferase domain of ExoS is cytotoxic for eukaryotic cells. Mol Microbiol 30: 751-760.
40. Pederson, K.J., Vallis, A.J., Aktories, K., Frank, D.W., and Barbieri, J.T. (1999) The amino-terminal domain of Pseudomonas aeruginosa ExoS disrupts actin filaments via small-molecular-weight GTP-binding proteins. Mol Microbiol 32: 393-401.
41. Pederson, K.J., Pal, S., Vallis, A.J., Frank, D.W., and Barbieri, J.T. (2000) Intracellular localization and processing of Pseudomonas aeruginosa ExoS in eukaryotic cells. Mol Microbiol 37: 287-299.
42. Ridley, A.J. (1997) The GTP-binding protein Rho. Int J Biochem Cell Biol 29: 1225-1229.
43. Riese, M.J., and Barbieri, J.T. (2002) Membrane localization contributes to the in vivo ADP-ribosylation of Ras by Pseudomonas aeruginosa ExoS. Infect Immun 70: 2230-2232.
44. Riese, M.J., Goehring, U.M., Ehrmantraut, M.E., Moss, J., Barbieri, J.T., Aktories, K., and Schmidt, G. (2002) Auto-ADP-ribosylation of Pseudomonas aeruginosa ExoS. J Biol Chem 277: 12082-12088.
45. Rosqvist, R., Forsberg, A., and Wolf-Watz, H. (1991) Microinjection of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Biochem Soc Trans 19: 1131-1132.
46. Rosqvist, R., Magnusson, K.E., and Wolf-Watz, H. (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J 13: 964-972.
47. Scheffzek, K., Stephan, I., Jensen, O.N., Illenberger, D., and Gierschik, P. (2000) The Rac-RhoGDI complex and the structural basis for the regulation of Rho proteins by RhoGDI. Nature Struct Biol 7: 122-126.
48. Skrzypek, E., Cowan, C., and Straley, S.C. (1998) Targeting of the Yersinia pestis YopM protein into HeLa cells and intracellular trafficking to the nucleus (in process citation). Mol Microbiol 30: 1051-1065.
49. Stebbins, C.E., and Galan, J.E. (2000) Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol Cell 6: 1449-1460.
50. Von Pawel-Rammingen, U., Telepnev, M.V., Schmidt, G., Aktories, K., Wolf-Watz, H., and Rosqvist, R. (2000) GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol Microbiol 36: 737-748.
51. Wurtele, M., Wolf, E., Pederson, K.J., Buchwald, G., Ahmadian, M.R., Barbieri, J.T., and Wittinghofer, A. (2001) How the Pseudomonas aeruginosa ExoS toxin downregulates Rac. Nature Struct Biol 8: 23-26.
52. Zhou, D., and Galan, J. (2001) Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect 3: 1293-1298.