Modulation of host cell endocytosis by the type III cytotoxin, pseudomonas ExoS

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Volumn 9, Issue 11, 2008, Pages 1948-1957

  Deng, Qing ^a   Barbieri, Joseph T ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

EGF receptor; Endocytosis; ExoS; Fluid phase; Rab 5; Uptake

Indexed keywords

CLATHRIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EXOENZYME S; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; RAB PROTEIN; RAB4 PROTEIN; RAB5 PROTEIN; RAB9 PROTEIN; RHO GTPASE ACTIVATING PROTEIN; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; BACTERIAL VIRULENCE; CELL DISRUPTION; COATED VESICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; EPITHELIUM CELL; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; LYSOSOME; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PSEUDOMONAS AERUGINOSA;

ADENOSINE DIPHOSPHATE RIBOSE; ADP RIBOSE TRANSFERASES; BACTERIAL TOXINS; ENDOCYTOSIS; EPIDERMAL GROWTH FACTOR; HELA CELLS; HUMANS; LYSOSOMES; PSEUDOMONAS AERUGINOSA; RAB5 GTP-BINDING PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 53849135540     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00808.x     Document Type: Article

References (48)

1. Mendelson MH, Gurtman A, Szabo S, Neibart E, Meyers BR, Policar M, Cheung TW, Lillienfeld D, Hammer G, Reddy S, Hirschman SZ, Choi K. Pseudomonas aeruginosa bacteremia in patients with AIDS. Clin Infect Dis 1994; 18: 886-895.
2. Yahr TL, Mende-Mueller LM, Friese MB, Frank DW. Identification of type III secreted products of the Pseudomonas aeruginosa exoenzyme S regulon. J Bacteriol 1997; 179: 7165-7168.
3. Sato H, Frank DW, Hillard CJ, Feix JB, Pankhaniya RR, Moriyama K, Finck-Barbancon V, Buchaklian A, Lei M, Long RM, Wiener-Kronish J, Sawa T. The mechanism of action of the Pseudomonas aeruginosa-encoded type III cytotoxin, ExoU. EMBO J 2003; 22: 2959-2969.
4. Yahr TL, Vallis AJ, Hancock MK, Barbieri JT, Frank DW. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc Natl Acad Sci U S A 1998; 95: 13899-13904.
5. Barbieri JT. Pseudomonas aeruginosa exoenzyme S, a bifunctional type-III secreted cytotoxin. Int J Med Microbiol 2000; 290: 381-387.
6. Coburn J, Dillon ST, Iglewski BH, Gill DM. Exoenzyme S of Pseudomonas aeruginosa ADP-ribosylates the intermediate filament protein vimentin. Infect Immun 1989; 57: 996-998.
7. Coburn J, Gill DM. ADP-ribosylation of p21ras and related proteins by Pseudomonas aeruginosa exoenzyme S. Infect Immun 1991; 59: 4259-4262.
8. Maresso AW, Baldwin MR, Barbieri JT. Ezrin/radixin/moesin proteins are high affinity targets for ADP-ribosylation by Pseudomonas aeruginosa ExoS. J Biol Chem 2004; 279: 38402-38408.
9. DiNovo AA, Schey KL, Vachon WS, McGuffie EM, Olson JC, Vincent TS. ADP-ribosylation of cyclophilin A by Pseudomonas aeruginosa exoenzyme S. Biochemistry 2006; 45: 4664-4673.
10. Sun J, Barbieri JT. Pseudomonas aeruginosa ExoT ADP-ribosylates CT10 regulator of kinase (Crk) proteins. J Biol Chem 2003; 278: 32794-32800.
11. Deng Q, Sun J, Barbieri JT. Uncoupling Crk signal transduction by Pseudomonas exoenzyme T. J Biol Chem 2005; 280: 35953-35960.
12. Li G, Stahl PD. Structure-function relationship of the small GTPase rab5. J Biol Chem 1993; 268: 24475-24480.
13. van der Bliek AM. A sixth sense for Rab5. Nat Cell Biol 2005; 7: 548-550.
14. Fraylick JE, Rucks EA, Greene DM, Vincent TS, Olson JC. Eukaryotic cell determination of ExoS ADP-ribosyltransferase substrate specificity. Biochem Biophys Res Commun 2002; 291: 91-100.
15. Barbieri AM, Sha Q, Bette-Bobillo P, Stahl PD, Vidal M. ADP-ribosylation of Rab5 by ExoS of Pseudomonas aeruginosa affects endocytosis. Infect Immun 2001; 69: 5329-5334.
16. Reaves BJ, Banting G, Luzio JP. Lumenal and transmembrane domains play a role in sorting type I membrane proteins on endocytic pathways. Mol Biol Cell 1998; 9: 1107-1122.
17. Jorissen RN, Walker F, Pouliot N, Garrett TP, Ward CW, Burgess AW. Epidermal growth factor receptor: Mechanisms of activation and signalling. Exp Cell Res 2003; 284: 31-53.
18. Merrifield CJ, Feldman ME, Wan L, Almers W. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 2002; 4: 691-698.
19. Sorkin A, Waters CM. Endocytosis of growth factor receptors. Bioessays 1993; 15: 375-382.
20. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994; 127: 915-934.
21. Barbieri MA, Roberts RL, Gumusboga A, Highfield H, Alvarez-Dominguez C, Wells A, Stahl PD. Epidermal growth factor and membrane trafficking. EGF receptor activation of endocytosis requires Rab5a. J Cell Biol 2000; 151: 539-550.
22. Chen X, Wang Z. Regulation of intracellular trafficking of the EGF receptor by Rab5 in the absence of phosphatidylinositol 3-kinase activity. EMBO Rep 2001; 2: 68-74.
23. Ceresa BP, Bahr SJ. rab7 activity affects epidermal growth factor:ePidermal growth factor receptor degradation by regulating endocytic trafficking from the late endosome. J Biol Chem 2006; 281: 1099-1106.
24. Cullis DN, Philip B, Baleja JD, Feig LA. Rab11-FIP2, an adaptor protein connecting cellular components involved in internalization and recycling of epidermal growth factor receptors. J Biol Chem 2002; 277: 49158-49166.
25. Kornilova E, Sorkina T, Beguinot L, Sorkin A. Lysosomal targeting of epidermal growth factor receptors via a kinase-dependent pathway is mediated by the receptor carboxyl-terminal residues 1022-1123. J Biol Chem 1996; 271: 30340-30346.
26. Pederson KJ, Vallis AJ, Aktories K, Frank DW, Barbieri JT. The amino-terminal domain of Pseudomonas aeruginosa ExoS disrupts actin filaments via small-molecular-weight GTP-binding proteins. Mol Microbiol 1999; 32: 393-401.
27. Pederson KJ, Barbieri JT. Intracellular expression of the ADP-ribosyltransferase domain of Pseudomonas exoenzyme S is cytotoxic to eukaryotic cells. Mol Microbiol 1998; 30: 751-759.
28. Bar-Sagi D, Feramisco JR. Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins. Science 1986; 233: 1061-1068.
29. Raiborg C, Wesche J, Malerod L, Stenmark H. Flat clathrin coats on endosomes mediate degradative protein sorting by scaffolding Hrs in dynamic microdomains. J Cell Sci 2006; 119: 2414-2424.
30. Roberts RL, Barbieri MA, Ullrich J, Stahl PD. Dynamics of rab5 activation in endocytosis and phagocytosis. J Leukoc Biol 2000; 68: 627-632.
31. Garrity-Ryan L, Kazmierczak B, Kowal R, Comolli J, Hauser A, Engel JN. The arginine finger domain of ExoT contributes to actin cytoskeleton disruption and inhibition of internalization of Pseudomonas aeruginosa by epithelial cells and macrophages. Infect Immun 2000; 68: 7100-7113.
32. Black DS, Bliska JB. The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence. Mol Microbiol 2000; 37: 515-527.
33. Fu Y, Galan JE. A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 1999; 401: 293-297.
34. Frithz-Lindsten E, Du Y, Rosqvist R, Forsberg A. Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Mol Microbiol 1997; 25: 1125-1139.
35. Rocha CL, Coburn J, Rucks EA, Olson JC. Characterization of Pseudomonas aeruginosa exoenzyme S as a bifunctional enzyme in J774A.1 macrophages. Infect Immun 2003; 71: 5296-5305.
36. Feltman H, Schulert G, Khan S, Jain M, Peterson L, Hauser AR. Prevalence of type III secretion genes in clinical and environmental isolates of Pseudomonas aeruginosa. Microbiology 2001; 147: 2659-2669.
37. Galperin E, Sorkin A. Visualization of Rab5 activity in living cells by FRET microscopy and influence of plasma-membrane-targeted Rab5 on clathrin-dependent endocytosis. J Cell Sci 2003; 116: 4799-4810.
38. McLauchlan H, Newell J, Morrice N, Osborne A, West M, Smythe E. A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr Biol 1998; 8: 34-45.
39. Lanzetti L, Rybin V, Malabarba MG, Christoforidis S, Scita G, Zerial M, Di Fiore PP. The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5. Nature 2000; 408: 374-377.
40. Dinneen JL, Ceresa BP. Expression of dominant negative rab5 in HeLa cells regulates endocytic trafficking distal from the plasma membrane. Exp Cell Res 2004; 294: 509-522.
41. Rubino M, Miaczynska M, Lippe R, Zerial M. Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J Biol Chem 2000; 275: 3745-3748.
42. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 1992; 70: 715-728.
43. Sato M, Sato K, Fonarev P, Huang CJ, Liou W, Grant BD. Caenorhabditis elegans RME-6 is a novel regulator of RAB-5 at the clathrin-coated pit. Nat Cell Biol 2005; 7: 559-569.
44. Wiley HS, Cunningham DD. Epidermal growth factor stimulates fluid phase endocytosis in human fibroblasts through a signal generated at the cell surface. J Cell Biochem 1982; 19: 383-394.
45. Leiva N, Pavarotti M, Colombo MI, Damiani MT. Reconstitution of recycling from the phagosomal compartment in streptolysin O-permeabilized macrophages: Role of Rab11. Exp Cell Res 2006; 312: 1843-1855.
46. Alvarez-Dominguez C, Madrazo-Toca F, Fernandez-Prieto L, Vandekerckhove J, Pareja E, Tobes R, Gomez-Lopez MT, Del Cerro-Vadillo E, Fresno M, Leyva-Cobian F, Carrasco-Marin E. Characterization of a Listeria monocytogenes protein interfering with Rab5a. Traffic 2008; 9: 325-337.
47. Zhang Y, Deng Q, Barbieri JT. Intracellular localization of type III-delivered Pseudomonas ExoS with endosome vesicles. J Biol Chem 2007; 282: 13022-13032.
48. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, Stanley EF. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: Analysis by quantitative immunocolocalization. J Neurosci 2004; 24: 4070-4081.