Escherichia coli Producing CNF1 Toxin Hijacks Tollip to Trigger Rac1-Dependent Cell Invasion

Traffic

Volumn 12, Issue 5, 2011, Pages 579-590

  Visvikis, Orane ^a,b,c   Boyer, Laurent ^a,b   Torrino, Stéphanie ^a,b   Doye, Anne ^a,b   Lemonnier, Marc ^a,b   Lorès, Patrick ^c   Rolando, Monica ^a,b   Flatau, Gilles ^a,b   Mettouchi, Amel ^b,d   Bouvard, Daniel ^d   Veiga, Esteban ^e   Gacon, Gérard ^c   Cossart, Pascale ^e   Lemichez, Emmanuel ^a,b  

^a CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c INSTITUT COCHIN   (France)

^d INSERM   (France)

^e INSTITUT PASTEUR   (France)

Author keywords

Bacterial invasion; Bacterial toxin; Clathrin; CNF1; Rac1; Rho GTPases; Tollip; Ubiquitination; UPEC

Indexed keywords

BACTERIAL PROTEIN; CLATHRIN; CYTOTOXIC NECROTIZING FACTOR 1; PROTEIN INIB; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TOLL INTERACTING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL VIRULENCE; CELL INVASION; CYTOSKELETON; HOST CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; INTERNALIZATION; LISTERIA MONOCYTOGENES; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UBIQUITINATION; UROPATHOGENIC ESCHERICHIA COLI;

ANIMALS; BACTERIAL INFECTIONS; BACTERIAL TOXINS; CELL LINE; ENDOCYTOSIS; ESCHERICHIA COLI PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; PROTEINS; RAC1 GTP-BINDING PROTEIN; UROPATHOGENIC ESCHERICHIA COLI;

EID: 79953732721     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01174.x     Document Type: Article

References (50)

1. Anitei M, Stange C, Parshina I, Baust T, Schenck A, Raposo G, Kirchhausen T, Hoflack B. Protein complexes containing CYFIP/Sra/PIR121 coordinate Arf1 and Rac1 signalling during clathrin-AP-1-coated carrier biogenesis at the TGN. Nat Cell Biol 2010;12:330-340.
2. Merrifield CJ, Perrais D, Zenisek D. Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 2005;121:593-606.
3. 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.
4. Ridley AJ. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 2006;16:522-529.
5. Kaksonen M, Toret CP, Drubin DG. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 2006;7:404-414.
6. Jaffe AB, Hall A. RHO GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005;21:247-269.
7. Boquet P, Lemichez E. Bacterial virulence factors targeting Rho GTPases: parasitism or symbiosis? Trends Cell Biol 2003;13:238-246.
8. Aktories K, Barbieri JT. Bacterial cytotoxins: targeting eukaryotic switches. Nat Rev Microbiol 2005;3:397-410.
9. Patel JC, Galan JE. Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J Cell Biol 2006;175:453-463.
10. Lemonnier M, Landraud L, Lemichez E. Rho GTPase-activating bacterial toxins: from bacterial virulence regulation to eukaryotic cell biology. FEMS Microbiol Rev 2007;31:515-534.
11. Dhakal BK, Kulesus RR, Mulvey MA. Mechanisms and consequences of bladder cell invasion by uropathogenic Escherichia coli. Eur J Clin Invest 2008;38(Suppl. 2):2-11.
12. Falzano L, Fiorentini C, Donelli G, Michel E, Kocks C, Cossart P, Cabanie L, Oswald E, Boquet P. Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor type 1. Mol Microbiol 1993;9:1247-1254.
13. Doye A, Mettouchi A, Bossis G, Clement R, Buisson-Touati C, Flatau G, Gagnoux L, Piechaczyk M, Boquet P, Lemichez E. CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 2002;111:553-564.
14. Lemichez E, Flatau G, Bruzzone M, Boquet P, Gauthier M. Molecular localization of the Escherichia coli cytotoxic necrotizing factor CNF1 cell-binding and catalytic domains. Mol Microbiol 1997;24:1061-1070.
15. Contamin S, Galmiche A, Doye A, Flatau G, Benmerah A, Boquet P. The p21 Rho-activating toxin cytotoxic necrotizing factor 1 is endocytosed by a clathrin-independent mechanism and enters the cytosol by an acidic-dependent membrane translocation step. Mol Biol Cell 2000;11:1775-1787.
16. Pei S, Doye A, Boquet P. Mutation of specific acidic residues of the CNF1 T domain into lysine alters cell membrane translocation of the toxin. Mol Microbiol 2001;41:1237-1247.
17. Kim KJ, Chung JW, Kim KS. 67-kDa laminin receptor promotes internalization of cytotoxic necrotizing factor 1-expressing Escherichia coli K1 into human brain microvascular endothelial cells. J Biol Chem 2005;280:1360-1368.
18. Knust Z, Blumenthal B, Aktories K, Schmidt G. Cleavage of Escherichia coli cytotoxic necrotizing factor 1 is required for full biologic activity. Infect Immun 2009;77:1835-1841.
19. Flatau G, Lemichez E, Gauthier M, Chardin P, Paris S, Fiorentini C, Boquet P. Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 1997;387:729-733.
20. Schmidt G, Sehr P, Wilm M, Selzer J, Mann M, Aktories K. Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 1997;387:725-729.
21. Lerm M, Selzer J, Hoffmeyer A, Rapp UR, Aktories K, Schmidt G. Deamidation of Cdc42 and Rac by Escherichia coli cytotoxic necrotizing factor 1: activation of c-Jun N-terminal kinase in HeLa cells. Infect Immun 1999;67:496-503.
22. Lerm M, Pop M, Fritz G, Aktories K, Schmidt G. Proteasomal degradation of cytotoxic necrotizing factor 1-activated rac. Infect Immun 2002;70:4053-4058.
23. Lynch EA, Stall J, Schmidt G, Chavrier P, D'Souza-Schorey C. Proteasome-mediated degradation of Rac1-GTP during epithelial cell scattering. Mol Biol Cell 2006;17:2236-2242.
24. Visvikis O, Maddugoda MP, Lemichez E. Direct modifications of Rho proteins: deconstructing GTPase regulation. Biol Cell 2010;102: 377-389.
25. Boyer L, Turchi L, Desnues B, Doye A, Ponzio G, Mege JL, Yamashita M, Zhang YE, Bertoglio J, Flatau G, Boquet P, Lemichez E. CNF1-induced ubiquitylation and proteasome destruction of activated RhoA is impaired in Smurf1-/- cells. Mol Biol Cell 2006;17: 2489-2497.
26. Harper JW, Schulman BA. Structural complexity in ubiquitin recognition. Cell 2006;124:1133-1136.
27. Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007;315:201-205.
28. Jura N, Scotto-Lavino E, Sobczyk A, Bar-Sagi D. Differential modification of Ras proteins by ubiquitination. Mol Cell 2006;21:679-687.
29. Nethe M, Anthony EC, Fernandez-Borja M, Dee R, Geerts D, Hensbergen PJ, Deelder AM, Schmidt G, Hordijk PL. Focal-adhesion targeting links caveolin-1 to a Rac1-degradation pathway. J Cell Sci 2010;123:1948-1958.
30. Blum G, Falbo V, Caprioli A, Hacker J. Gene clusters encoding the cytotoxic necrotizing factor type 1, Prs-fimbriae and alpha-hemolysin form the pathogenicity island II of the uropathogenic Escherichia coli strain J96. FEMS Microbiol Lett 1995;126:189-195.
31. Falkow S, Small P, Isberg R, Hayes SF, Corwin D. A molecular strategy for the study of bacterial invasion. Rev Infect Dis 1987; 9(Suppl. 5):S450-S455.
32. Eto DS, Jones TA, Sundsbak JL, Mulvey MA. Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog 2007;3:e100.
33. Burns K, Clatworthy J, Martin L, Martinon F, Plumpton C, Maschera B, Lewis A, Ray K, Tschopp J, Volpe F. Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor. Nat Cell Biol 2000;2:346-351.
34. Katoh Y, Shiba Y, Mitsuhashi H, Yanagida Y, Takatsu H, Nakayama K. Tollip and Tom1 form a complex and recruit ubiquitin-conjugated proteins onto early endosomes. J Biol Chem 2004;279:24435-24443.
35. Yamakami M, Yoshimori T, Yokosawa H. Tom1, a VHS domain-containing protein, interacts with Tollip, ubiquitin, and clathrin. J Biol Chem 2003;278:52865-52872.
36. Katoh Y, Imakagura H, Futatsumori M, Nakayama K. Recruitment of clathrin onto endosomes by the Tom1-Tollip complex. Biochem Biophys Res Commun 2006;341:143-149.
37. Brissoni B, Agostini L, Kropf M, Martinon F, Swoboda V, Lippens S, Everett H, Aebi N, Janssens S, Meylan E, Felberbaum-Corti M, Hirling H, Gruenberg J, Tschopp J, Burns K. Intracellular trafficking of interleukin-1 receptor I requires Tollip. Curr Biol 2006;16:2265-2270.
38. Martinez JJ, Hultgren SJ. Requirement of Rho-family GTPases in the invasion of type 1-piliated uropathogenic Escherichia coli. Cell Microbiol 2002;4:19-28.
39. Eto DS, Gordon HB, Dhakal BK, Jones TA, Mulvey MA. Clathrin, AP-2, and the NPXY-binding subset of alternate endocytic adaptors facilitate FimH-mediated bacterial invasion of host cells. Cell Microbiol 2008;10:2553-2567.
40. Shen Y, Naujokas M, Park M, Ireton K. InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 2000;103:501-510.
41. Seveau S, Tham TN, Payrastre B, Hoppe AD, Swanson JA, Cossart P. A FRET analysis to unravel the role of cholesterol in Rac1 and PI 3-kinase activation in the InlB/Met signalling pathway. Cell Microbiol 2007;9:790-803.
42. Veiga E, Cossart P. Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nat Cell Biol 2005;7:894-900.
43. Petrelli A, Gilestro GF, Lanzardo S, Comoglio PM, Migone N, Giordano S. The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature 2002;416:187-190.
44. 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.
45. Dramsi S, Biswas I, Maguin E, Braun L, Mastroeni P, Cossart P. Entry of Listeria monocytogenes into hepatocytes requires expression of inIB, a surface protein of the internalin multigene family. Mol Microbiol 1995;16:251-261.
46. Doye A, Boyer L, Mettouchi A, Lemichez E. Ubiquitin-mediated proteasomal degradation of Rho proteins by the CNF1 toxin. Methods Enzymol 2006;406:447-456.
47. Bouvard D, Aszodi A, Kostka G, Block MR, Albiges-Rizo C, Fassler R. Defective osteoblast function in ICAP-1-deficient mice. Development 2007;134:2615-2625.
48. Millon-Fremillon A, Bouvard D, Grichine A, Manet-Dupe S, Block MR, Albiges-Rizo C. Cell adaptive response to extracellular matrix density is controlled by ICAP-1-dependent beta1-integrin affinity. J Cell Biol 2008;180:427-441.
49. Rudert F, Visser E, Gradl G, Grandison P, Shemshedini L, Wang Y, Grierson A, Watson J. pLEF, a novel vector for expression of glutathione S-transferase fusion proteins in mammalian cells. Gene 1996;169:281-282.
50. Lemonnier M, Ziegelin G, Reick T, Munoz Gomez A, Diaz-Orejas R, Lanka E. Bacteriophage P1 Ban protein is a hexameric DNA helicase that interacts with and substitutes for Escherichia coli DnaB. Nucleic Acids Res 2003;31:3918-3928.