Ubiquitin and ubiquitin-modified proteins activate the Pseudomonas aeruginosa T3SS cytotoxin, ExoU

Molecular Microbiology

Volumn 82, Issue 6, 2011, Pages 1454-1467

  Anderson, David M ^a   Schmalzer, Katherine M ^a   Sato, Hiromi ^a   Casey, Monika ^a   Terhune, Scott S ^a   Haas, Arthur L ^b   Feix, Jimmy B ^a   Frank, Dara W ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOTOXIN; EXOU PROTEIN; PHOSPHOLIPASE; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL TRANSMISSION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION SYSTEM; GENETIC ENGINEERING; GENETIC MANIPULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; STRUCTURE ACTIVITY RELATION; TYPE III SECRETION SYSTEM; UBIQUITINATION;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CATTLE; CELL LINE; ENZYME ACTIVATORS; HUMANS; LEUKOCIDINS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SUPEROXIDE DISMUTASE; UBIQUITIN;

BACTERIA (MICROORGANISMS); EUKARYOTA; MAMMALIA; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 83355166268     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07904.x     Document Type: Article

References (51)

1. Angot, A., Vergunst, A., Genin, S., and Peeters, N. (2007) Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog 3: e3.
2. Baboshina, O.V., and Haas, A.L. (1996) Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26 S proteasome subunit 5. J Biol Chem 271: 2823-2831.
3. Benson, M.A., Schmalzer, K.M., and Frank, D.W. (2010) A sensitive fluorescence-based assay for the detection of ExoU-mediated PLA2 activity. Clin Chim Acta 411: 190-197.
4. Benson, M.A., Komas, S.M., Schmalzer, K.M., Casey, M.S., Frank, D.W., and Feix, J.B. (2011) Induced conformational changes in the activation of the Pseudomonas aeruginosa type III toxin, ExoU. Biophys J 100: 1335-1343.
5. Bohnsack, R.N., and Haas, A.L. (2003) Conservation in the mechanism of Nedd8 activation by the human AppBp1-Uba3 heterodimer. J Biol Chem 278: 26823-26830.
6. Catic, A., Misaghi, S., Korbel, G.A., and Ploegh, H.L. (2007) ElaD, a deubiquitinating protease expressed by E. coli. PLoS ONE 2: e381.
7. Collins, C.A., and Brown, E.J. (2010) Cytosol as battleground: ubiquitin as a weapon for both host and pathogen. Trends Cell Biol 20: 205-213.
8. Dupont, N., Temime-Smaali, N., and Lafont, F. (2010) How ubiquitination and autophagy participate in the regulation of the cell response to bacterial infection. Biol Cell 102: 621-634.
9. Finck-Barbançon, V., and Frank, D.W. (2001) Multiple domains are required for the toxic activity of Pseudomonas aeruginosa ExoU. J Bacteriol 183: 4330-4344.
10. Frank, D.W., Vallis, A., Wiener-Kronish, J.P., Roy-Burman, A., Spack, E.G., Mullaney, B.P., etal. (2002) Generation and characterization of a protective monoclonal antibody to Pseudomonas aeruginosa PcrV. J Infect Dis 186: 64-73.
11. Frithz-Lindsten, E., Du, Y., Rosqvist, R., and Forsberg, A. (1997) Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Mol Microbiol 25: 1125-1139.
12. Fu, H., Coburn, J., and Collier, R.J. (1993) The eukaryotic host factor that activates exoenzyme S of Pseudomonas aeruginosa is a member of the 14-3-3 protein family. Proc Natl Acad Sci USA 90: 2320-2324.
13. Ganesan, A.K., Vincent, T.S., Olson, J.C., and Barbieri, J.T. (1999) Pseudomonas aeruginosa exoenzyme S disrupts Ras-mediated signal transduction by inhibiting guanine nucleotide exchange factor-catalyzed nucleotide exchange. J Biol Chem 274: 21823-21829.
14. Giamarellou, H. (2000) Therapeutic guidelines for Pseudomonas aeruginosa infections. Int J Antimicrob Agents 16: 103-106.
15. 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.
16. Haas, A.L., and Bright, P.M. (1987) The dynamics of ubiquitin pools within cultured human lung fibroblasts. J Biol Chem 262: 345-351.
17. Haraga, A., and Miller, S.I. (2006) A Salmonella type III secretion effector interacts with the mammalian serine/threonine protein kinase PKN1. Cell Microbiol 5: 837-846.
18. Hauser, A.R., Jain, M., Bar-Meir, M., and McColley, S.A. (2011) Clinical significance of microbial infection and adaptation in cystic fibrosis. Clin Microbiol Rev 24: 29-70.
19. Janjusevic, R., Abramovitch, R.B., Martin, G.B., and Stebbins, C.E. (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311: 222-226.
20. Jubelin, G., Taieb, F., Duda, D.M., Hsu, Y., Samba-Louaka, A., Nobe, R., etal. (2010) Pathogens bacteria target NEDD8-conujgated cullins to hijack host-cell signaling pathways. PLoS Pathog 6: e1001128.
21. Kim, D.W., Lenzen, G., Page, A.L., Legrain, P., Sansonetti, P.J., and Parsot, C. (2005) The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci USA 102: 14046-14051.
22. Koth, C.M., Orlicky, S.M., Larson, S.M., and Edwards, A.M. (2003) Use of limited proteolysis to identify protein domains suitable for structural analysis. Meth Enzymol 368: 77-84.
23. Kubori, T., and Galan, J.E. (2003) Temporal regulation of Salmonella virulence effector function by proteosome-dependent protein degradation. Cell 115: 333-342.
24. Kubori, T., Hyakutake, A., and Nagai, H. (2008) Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol Microbiol 67: 1307-1319.
25. Le Negrate, G., Faustin, B., Welsh, K., Loeffler, M., Krajewska, M., Hasegawa, P., etal. (2008) Salmonella secreted factor L deubiquitinase of Salmonella typhimurium inhibits NF-kappaB, suppresses IkappaBalpha ubiquitinated and modulates innate immune responses. J Immunol 180: 5045-5056.
26. Lee, V.T., Smith, R.S., Tummler, B., and Lory, S. (2005) Activities of Pseudomonas aeruginosa effectors secreted by the type III secretion system in vitro and during infection. Infect Immun 73: 1695-1705.
27. Misaghi, S., Balsara, Z.R., Catic, A., Spooner, E., Ploegh, H.L., and Starnbach, M.N. (2006) Chlamydia trachomatis-derived deubiquitinating enzymes in mammalian cells during infection. Mol Microbiol 61: 142-150.
28. Narasimhan, J., Wang, M., Fu, Z., Klein, J.M., Haas, A.L., and Kim, J.J. (2005) Crystal structure of the interferon-induced ubiquitin-like protein ISG15. J Biol Chem 280: 20365-20374.
29. Nomura, K., DebRoy, S., Lee, Y.H., Pumplin, N., Jones, J., and He, S.Y. (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 31: 220-223.
30. Orth, K., Xu, Z., Mudgett, M.B., Bao, Z.Q., Palmer, L.E., Bliska, J.B., etal. (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594-1597.
31. Patel, J.C., Hueffer, K., Lam, T.T., and Galan, J.E. (2009) Diversification of a Salmonella virulence protein function by ubiquitin differential localization. Cell 137: 283-294.
32. Phillips, R.M., Six, D.A., Dennis, E.A., and Ghosh, P. (2003) In vivo phospholipase activity of the Pseudomonas aeruginosa cytotoxin ExoU and protection of mammalian cells with phospholipase A2 inhibitors. J Biol Chem 278: 41326-41332.
33. Pier, G.B., and Ramphal, R. (2005) Pseudomonas aeruginosa. In Principles and Practice of Infectious Diseases, 6th edn. Mandell, G.L., Bennett, J.E., and Dolin, R. (eds). Philadelphia: Elsevier Churchill Livingstone, pp. 2587-2615.
34. Rohde, J.R., Breitkreutz, A., Chenal, A., Sansonetti, P.J., and Parsot, C. (2007) Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 1: 77-83.
35. Rytkonen, A., Poh, J., Garmendia, J., Boyle, C., Thompson, A., Liu, M., etal. (2007) SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc Natl Acad Sci USA 104: 3502-3507.
36. Sato, H., and Frank, D.W. (2004) ExoU is a potent intracellular phospholipase. Mol Microbiol 53: 1279-1290.
37. Sato, H., Frank, D.W., Hillard, C.J., Feix, J., Pankhaniya, R., Moriyama, K., etal. (2003) The mechanism of action of the Pseudomonas aeruginosa-encoded type III cytotoxin, ExoU. EMBO J 22: 2959-2969.
38. Sato, H., Feix, J.B., Hillard, C.J., and Frank, D.W. (2005) Characterization of phospholipase activity of the Pseudomonas aeruginosa type III cytotoxin, ExoU. J Bacteriol 187: 1192-1195.
39. Sato, H., Feix, J.B., and Frank, D.W. (2006) Identification of superoxide dismutase as a cofactor for the Pseudomonas type III toxin, ExoU. Biochemistry 45: 10368-10375.
40. Sayner, S.L., Frank, D., King, J., VandeWaa, J., and Stevens, T. (2004) Paradoxical cAMPinduced endothelial hyperpermeability. Circ Res 95: 196-203.
41. Schmalzer, K.M., Benson, M.A., and Frank, D.W. (2010) Activation of ExoU phospholipase activity requires specific C-terminal regions. J Bacteriol 192: 1801-1812.
42. Schnupf, P., Portnoy, D.A., and Decatur, A.L. (2006) Phosphorylation, ubiquitination and degradation of listeriolysin O in mammalian cells:role of the PEST-like sequence. Cell Microbiol 8: 353-364.
43. Shames, S.R., Auweter, S.D., and Finlay, B.B. (2009) Co-evolution and exploitation of host signaling pathways by bacterial pathogens. Int J Biochem Cell Biol 41: 380-389.
44. Stirling, F.R., Cuzick, A., Kelly, S.M., Oxley, D., and Evans, T.J. (2006) Eukaryotic localization, activation and ubiquitinylation of a bacterial type III secreted toxin. Cell Microbiol 8: 1294-1309.
45. Sun, J., and Barbieri, J.T. (2003) Pseudomonas aeruginosa ExoT ADP-ribosylates CT10 regulator of kinase (Crk) proteins. J Biol Chem 278: 32794-32800.
46. Sweet, C.R., Conlon, J., Golenbock, D.T., Goguen, J., and Sliverman, N. (2007) YopJ targets TRAF proteins to inhibit TLR-mediated NF-kappaB, MAPK and IRF3 signal transduction. Cell Microbiol 9: 2700-2715.
47. Yahr, T.L., Mende-Mueller, L.M., Friese, M.B., and Frank, D.W. (1997) Identification of type III secreted products of the Pseudomonas aeruginosa exoenzyme S regulon. J Bacteriol 179: 7165-7168.
48. Yahr, T.L., Vallis, A.J., Hancock, M.K., Barbieri, J.T., and Frank, D.W. (1998) ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc Natl Acad Sci USA 95: 13899-13904.
49. Ye, Z., Petrof, E.O., Boone, D., Claud, E.C., and Sun, J. (2007) Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am J Pathol 171: 882-892.
50. Zhang, Y., Higashide, W.M., McCormick, B.A., Chen, J., and Zhou, D. (2006) The inflammation-associated Salmonella SopA HECT-like E3 ubiquitin ligase. Mol Microbiol 62: 786-793.
51. Zhou, H., Monack, D.M., Kayagaki, N., Wertz, I., Yin, J., Wolf, B., and Dixit, V.M. (2005) Yersinia virulence factor YopJ acts as a deubiquitinase to ihibiti NF-kappa B activation. J Exp Med 202: 1327-1332.