The Bordetella type III secretion system effector BteA contains a conserved N-terminal motif that guides bacterial virulence factors to lipid rafts

Cellular Microbiology

Volumn 11, Issue 12, 2009, Pages 1735-1749

  French, Christopher T ^a   Panina, Ekaterina M ^a   Yeh, Sylvia H ^a   Griffith, Natasha ^a   Arambulal, Diego G ^a,b   Miller, Jeff F ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL PROTEIN; BTEA PROTEIN; EZRIN; HYBRID PROTEIN; METHYL BETA CYCLODEXTRIN; SPHINGOLIPID ACTIVATOR PROTEIN 1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BORDETELLA; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; LIPID RAFT; NONHUMAN; PHOTORHABDUS LUMINESCENS; PRIORITY JOURNAL; TYPE III SECRETION SYSTEM;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BETA-CYCLODEXTRINS; BORDETELLA; BORDETELLA INFECTIONS; CELL LINE; CYTOSKELETAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; MEMBRANE MICRODOMAINS; MICE; MOLECULAR SEQUENCE DATA; RATS; SECRETORY PATHWAY; VIRULENCE FACTORS, BORDETELLA;

BACTERIA (MICROORGANISMS); BORDETELLA; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; MAMMALIA; PHOTORHABDUS LUMINESCENS;

EID: 72749103047     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01361.x     Document Type: Article

References (62)

1. Akerley, B.J., Cotter, P.A., and Miller, J.F. (1995) Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell 80: 611-620.
2. Allen-Vercoe, E., Waddell, B., Livingstone, S., Deans, J., and DeVinney, R. (2006) Enteropathogenic Escherichia coli Tir translocation and pedestal formation requires membrane cholesterol in the absence of bundle-forming pili. Cell Microbiol 8: 613-624.
3. Bretscher, A., Edwards, K., and Fehon, R.G. (2002) ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 3: 586-599.
4. Bryant, P.J. (1999) Filopodia: fickle fingers of cell fate? Curr Biol 9: R655-R657.
5. Chang, J.H., Urbach, J.M., Law, T.F., Arnold, L.W., Hu, A., Gombar, S., et al. (2005) A high-throughput, nearsaturating screen for type III effector genes from Pseudomonas syringae. Proc Natl Acad Sci USA 102: 2549-2554.
6. Chen, J., Chen, L., Wang, G., and Tang, H. (2007) Cholesterol-dependent and - independent CD40 internalization and signaling activation in cardiovascular endothelial cells. Arterioscler Thromb Vasc Biol 27: 2005- 2013.
7. Chichili, G.R., and Rodgers, W. (2009) Cytoskeleton- membrane interactions in membrane raft structure. Cell Mol Life Sci 66: 2319-2328.
8. Cotter, P.A., and Miller, J.F. (1994) BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect Immun 62: 3381-3390.
9. Derzelle, S., Turlin, E., Duchaud, E., Pages, S., Kunst, F., Givaudan, A., and Danchin, A. (2004) The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J Bacteriol 186: 1270-1279.
10. Dove, S.L., and Hochschild, A. (2004) A bacterial two-hybrid system based on transcription activation. Meth Mol Biol 261: 231-246.
11. Edidin, M. (2003) The state of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct 32: 257- 283.
12. Faix, J., Breitsprecher, D., Stradal, T.E., and Rottner, K. (2009) Filopodia: Complex models for simple rods. Int J Biochem Cell Biol 41: 1656-1664.
13. Fouts, D.E., Abramovitch, R.B., Alfano, J.R., Baldo, A.M., Buell, C.R., Cartinhour, S., et al. (2002) Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc Natl Acad Sci USA 99: 2275-2280.
14. Fullner, K.J., and Mekalanos, J.J. (2000) In vivo covalent cross-linking of cellular actin by the Vibrio cholerae RTX toxin. EMBO J 19: 5315-5323.
15. Gajate, C., and Mollinedo, F. (2005) Cytoskeleton-mediated death receptor and ligand concentration in lipid rafts forms apoptosis-promoting clusters in cancer chemotherapy. J Biol Chem 280: 11641-11647.
16. Gay, M., Renault, T., Pons, A.M., and Le Roux, F. (2004) Two vibrio splendidus related strains collaborate to kill Crassostrea gigas: taxonomy and host alterations. Dis Aquat Organ 62: 65-74.
17. Gekara, N.O., Jacobs, T., Chakraborty, T., and Weiss, S. (2005) The cholesterol-dependent cytolysin listeriolysin O aggregates rafts via oligomerization. Cell Microbiol 7: 1345-1356.
18. Halayko, A.J., and Stelmack, G.L. (2005) The association of caveolae, actin, and the dystrophin-glycoprotein complex: a role in smooth muscle phenotype and function? Can J Physiol Pharmacol 83: 877-891.
19. Hanzal-Bayer, M.F., and Hancock, J.F. (2007) Lipid rafts and membrane traffic. FEBS Lett 581: 2098-2104.
20. Harrington, A.T., Hearn, P.D., Picking, W.L., Barker, J.R., Wessel, A., and Picking, W.D. (2003) Structural characterization of the N terminus of IpaC from Shigella flexneri. Infect Immun 71: 1255-1264.
21. Hawkes, D.J., and Mak, J. (2006) Lipid membrane; a novel target for viral and bacterial pathogens. Curr Drug Targets 7: 1615-1621.
22. Hayward, R.D., Hume, P.J., Humphreys, D., Phillips, N., Smith, K., and Koronakis, V. (2009) Clustering transfers the translocated Escherichia coli receptor into lipid rafts to stimulate reversible activation of c-Fyn. Cell Microbiol 11: 433-441.
23. Hoeflich, K.P., and Ikura, M. (2004) Radixin: cytoskeletal adopter and signaling protein. Int J Biochem Cell Biol 36: 2131-2136.
24. Ignoul, S., Simaels, J., Hermans, D., Annaert, W., and Eggermont, J. (2007) Human ClC-6 is a late endosomal glycoprotein that associates with detergent-resistant lipid domains. PLoS ONE 2: e474.
25. Kozak, N.A., Mattoo, S., Foreman-Wykert, A.K., Whitelegge, J.P., and Miller, J.F. (2005) Interactions between partner switcher orthologs BtrW and BtrV regulate type III secretion in Bordetella. J Bacteriol 187: 5665-5676.
26. Kuwae, A., Matsuzawa, T., Ishikawa, N., Abe, H., Nonaka, T., Fukuda, H., et al. (2006) BopC is a novel type III effector secreted by Bordetella bronchiseptica and has a critical role in type III-dependent necrotic cell death. J Biol Chem 281: 6589-6600.
27. Lacoste, A., Jalabert, F., Malham, S.K., Cueff, A., and Poulet, S.A. (2001) Stress and stress-induced neuroendocrine changes increase the susceptibility of juvenile oysters (Crassostrea gigas) to Vibrio splendidus. Appl Environ Microbiol 67: 2304-2309
28. Ladwein, M., and Rottner, K. (2008) On the Rho'd: the regulation of membrane protrusions by Rho-GTPases. FEBS Lett 582: 2066-2074.
29. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
30. Lafont, F., Abrami, L., and van der Goot, F.G. (2004) Bacterial subversion of lipid rafts. Curr Opin Microbiol 7: 4-10. Lafont, F., and van der Goot, F.G. (2005a) Bacterial invasion via lipid rafts. Cell Microbiol 7: 613-620.
31. Lafont, F., and van der Goot, F.G. (2005a) Bacterial invasion via lipid rafts. Cell Microbiol 7: 613-620.
32. Lafont, F., and van der Goot, F.G. (2005b) Oiling the key hole. Mol Microbiol 56: 575-577.
33. Lappalainen, K., Jaaskelainen, I., Syrjanen, K., Urtti, A., and Syrjanen, S. (1994) Comparison of cell proliferation and toxicity assays using two cationic liposomes. Pharm Res 11: 1127-1131.
34. Laude, A.J., and Prior, I.A. (2004) Plasma membrane microdomains: organization, function and trafficking. Mol Membr Biol 21: 193-205.
35. Lencer, W.I., and Saslowsky, D. (2005) Raft trafficking of AB5 subunit bacterial toxins. Biochim Biophys Acta 1746: 314- 321.
36. Lidke, D.S., Lidke, K.A., Rieger, B., Jovin, T.M., and Arndt-Jovin, D.J. (2005) Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors. J Cell Biol 170: 619-626.
37. Lin, W., Fullner, K.J., Clayton, R., Sexton, J.A., Rogers, M.B., Calia, K.E., et al. (1999) Identification of a Vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. Proc Natl Acad Sci USA 96: 1071-1076.
38. Manes, S., del Real, G., and Martinez, A.C. (2003) Pathogens: raft hijackers. Nat Rev Immunol 3: 557-568.
39. Mattoo, S., Yuk, M.H., Huang, L.L., and Miller, J.F. (2004) Regulation of type III secretion in Bordetella. Mol Microbiol 52: 1201-1214.
40. Mejia, E., Bliska, J.B., and Viboud, G.I. (2008) Yersinia controls type III effector delivery into host cells by modulating Rho activity. PLoS Pathog 4: e3.
41. Munro, S. (2003) Lipid rafts: elusive or illusive? Cell 115: 377-388.
42. Panina, E.M., Mattoo, S., Griffith, N., Kozak, N.A., Yuk, M.H., and Miller, J.F. (2005) A genome-wide screen identifies a Bordetella type III secretion effector and candidate effectors in other species. Mol Microbiol 58: 267-279.
43. Parkhill, J., Sebaihia, M., Preston, A., Murphy, L.D., Thomson, N., Harris, D.E., et al. (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35: 32-40.
44. Pilione, M.R., and Harvill, E.T. (2006) The Bordetella bronchiseptica type III secretion system inhibits gamma interferon production that is required for efficient antibodymediated bacterial clearance. Infect Immun 74: 1043- 1049.
45. Prochazkova, K., and Satchell, K.J. (2008) Structure-function analysis of inositol hexakisphosphate-induced autoprocessing of the Vibrio cholerae multifunctional autoprocessing RTX toxin. J Biol Chem 283: 23656-23664.
46. Riff, J.D., Callahan, J.W., and Sherman, P.M. (2005) Cholesterol-enriched membrane microdomains are required for inducing host cell cytoskeleton rearrangements in response to attaching-effacing Escherichia coli. Infect Immun 73: 7113-7125.
47. Schon, A., and Freire, E. (1989) Thermodynamics of intersubunit interactions in cholera toxin upon binding to the oligosaccharide portion of its cell surface receptor, ganglioside GM1. Biochemistry 28: 5019-5024.
48. Shaw, A.S. (2006) Lipid rafts: now you see them, now you don't. Nat Immunol 7: 1139-1142.
49. Sheahan, K.L., Cordero, C.L., and Satchell, K.J. (2007) Autoprocessing of the Vibrio cholerae RTX toxin by the cysteine protease domain. EMBO J 26: 2552-2561.
50. Shrivastava, R., and Miller, J.F. (2009) Virulence factor secretion and translocation by Bordetella species. Curr Opin Microbiol 12: 88-93.
51. Siciliano, N.A., Skinner, J.A., and Yuk, M.H. (2006) Bordetella bronchiseptica modulates macrophage phenotype leading to the inhibition of CD4+ T cell proliferation and the initiation of a Th17 immune response. J Immunol 177: 7131- 7138.
52. Simons, K., and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387: 569-572.
53. Skinner, J.A., Pilione, M.R., Shen, H., Harvill, E.T., and Yuk, M.H. (2005) Bordetella type III secretion modulates dendritic cell migration resulting in immunosuppression and bacterial persistence. J Immunol 175: 4647-4652.
54. Skwarek, M. (2004) Recent controversy surrounding lipid rafts. Arch Immunol Ther Exp (Warsz) 52: 427-431.
55. Small, J.V., Stradal, T., Vignal, E., and Rottner, K. (2002) The lamellipodium: where motility begins. Trends Cell Biol 12: 112-120.
56. Sommer, H., Schmitz, A., Schmeissner, U., and Miller, J.H. (1978) Genetic studies of the lac repressor. VI. The B116 repressor: an altered lac repressor containing amino acid specified by both the trp and lacI leader regions. J Mol Biol 123: 457-469.
57. Stockbauer, K.E., Foreman-Wykert, A.K., and Miller, J.F. (2003) Bordetella type III secretion induces caspase 1-independent necrosis. Cell Microbiol 5: 123-132.
58. Takenouchi, H., Kiyokawa, N., Taguchi, T., Matsui, J., Katagiri, Y.U., Okita, H., et al. (2004) Shiga toxin binding to globotriaosyl ceramide induces intracellular signals that mediate cytoskeleton remodeling in human renal carcinoma-derived cells. J Cell Sci 117: 3911-3922.
59. Viola, A., and Gupta, N. (2007) Tether and trap: regulation of membrane-raft dynamics by actin-binding proteins. Nat Rev Immunol 7: 889-896.
60. Xavier, R., Rabizadeh, S., Ishiguro, K., Andre, N., Ortiz, J.B., Wachtel, H., et al. (2004) Discs large (Dlg1) complexes in lymphocyte activation. J Cell Biol 166: 173-178.
61. Yuk, M.H., Harvill, E.T., and Miller, J.F. (1998) The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica. Mol Microbiol 28: 945-959.
62. Yuk, M.H., Harvill, E.T., Cotter, P.A., and Miller, J.F. 2000 Modulation of host immune responses, induction of apoptosis and inhibition of NF-kappaB activation by the Bordetella type III secretion system. Mol Microbiol 35: 991-1004.