Insulin receptor tyrosine kinase substrate links the E. coli O157:H7 actin assembly effectors Tir and EspF U during pedestal formation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 16, 2009, Pages 6754-6759

  Vingadassalom, Didier ^a   Kazlauskas, Arunas ^b,c   Skehan, Brian ^a   Cheng, Hui Chun ^d   Magoun, Loranne ^a   Robbins, Douglas ^a   Rosen, Michael K ^d   Saksela, Kalle ^b,c   Leong, John M ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Enterohemorrhagic Escherichia coli; IRSp53 MIM homology domain; IRTKS; N WASP; SH3 domain

Indexed keywords

ACTIN; INSULIN RECEPTOR; OUTER MEMBRANE PROTEIN; PROLINE; PROTEIN SH3; TRANSLOCATED INTIMIN RECEPTOR; TYROSINE; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; BACTERIOPHAGE RECEPTOR; CARRIER PROTEIN; CELL SURFACE RECEPTOR; ESCHERICHIA COLI PROTEIN; ESPFU PROTEIN, E COLI; HYBRID PROTEIN; INSULIN RECEPTOR SUBSTRATE; IRTKS PROTEIN, HUMAN; TIR PROTEIN, E COLI;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; ENZYME SUBSTRATE; ESCHERICHIA COLI O157; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; BACTERIUM ADHERENCE; CHEMISTRY; CYTOLOGY; GENE DELETION; HELA CELL; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT; PROLINE RICH PROTEIN DOMAIN; PROTEIN TRANSPORT; SRC HOMOLOGY DOMAIN;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; ESCHERICHIA COLI O157:H-; MAMMALIA;

ACTINS; AMINO ACID SEQUENCE; ATTACHMENT SITES, MICROBIOLOGICAL; BACTERIAL ADHESION; CARRIER PROTEINS; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; GENE DELETION; HELA CELLS; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PROLINE-RICH PROTEIN DOMAINS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE; RECOMBINANT FUSION PROTEINS; SRC HOMOLOGY DOMAINS;

EID: 66149131872     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0809131106     Document Type: Article

References (40)

1. Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2:123-140.
2. Donnenberg MS, et al. (1993) Role of the eaeA gene in experimental enteropathogenic Escherichia coli infection. J Clin Invest 92:1412-1417.
3. Ritchie JM, Thorpe CM, Rogers AB, Waldor MK (2003) Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli -induced diarrhea and intestinal inflammation in infant rabbits Infect Immun 71:7129-7139.
4. Frankel G, Phillips AD (2008) Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal. Cell Microbiol 10:549-556.
5. Hayward RD, Leong JM, Koronakis V, Campellone KG (2006) Exploiting pathogenic Escherichia coli to model transmembrane receptor signalling. Nat Rev Microbiol 4:358-370.
6. Deibel C, Kramer S, Chakraborty T, Ebel F (1998) EspE, a novel secreted protein of attaching and effacing bacteria, is directly translocated into infected host cells, where it appears as a tyrosine-phosphorylated 90 kDa protein. Mol Microbiol 28:463-474.
7. Kenny B, et al. (1997) Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511-520.
8. Campellone KG, Giese A, Tipper DJ, Leong JM (2002) A tyrosine- phosphorylated 12-amino-acid sequence of enteropathogenic Escherichia coli Tir binds the host adaptor protein Nck and is required for Nck localization to actin pedestals. Mol Microbiol 43:1227-1241.
9. Gruenheid S, et al. (2001) Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat Cell Biol 3:856-859.
10. Rohatgi R, et al. (2001) Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J Biol Chem 276:26448-26452.
11. Campellone KG, Leong JM (2003) Tails of two Tirs: actin pedestal formation by enteropathogenic E. coli and enterohemorrhagic E. coli O157:H7. Curr Opin Microbiol 6:82-90.
12. Allen-Vercoe E, Waddell B, Toh MC, DeVinney R (2006) Amino acid residues within enterohemorrhagic Escherichia coli O157:H7 Tir involved in phosphorylation, alpha-actinin recruitment, and Nck-independent pedestal formation. Infect Immun 74:6196-6205.
13. Brady MJ, Campellone KG, Ghildiyal M, Leong JM (2007) Enterohaemorrhagic and enteropathogenic Escherichia coli Tir proteins trigger a common Nck-independent actin assembly pathway. Cell Microbiol 9:2242-2253.
14. Campellone KG, et al. (2006) Enterohaemorrhagic Escherichia coli Tir requires a C-terminal 12-residue peptide to initiate EspFU-mediated actin assembly and harbours N-terminal sequences that influence pedestal length. Cell Microbiol 8:1488-1503.
15. Campellone KG, Robbins D, Leong JM (2004) EspFU is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev Cell 7:217-228.
16. Garmendia J, et al. (2004) TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton. Cell Microbiol 6:1167-1183.
17. Ritchie JM, et al. (2008) EspFU, a type III-translocated effector of actin assembly, fosters epithelial association and late-stage intestinal colonization by E. coli O157:H7. Cell Microbiol 10:836-847.
18. Cheng HC, et al. (2008) Structural mechanism of WASP activation by the enterohae-morrhagic E. coli effector EspF(U). Nature 454:1009-1013.
19. Garmendia J, et al. (2006) Characterization of TccP-mediated N-WASP activation during enterohaemorrhagic Escherichia coli infection. Cell Microbiol 8:1444-1455.
20. Sallee NA, et al. (2008) The pathogen protein EspF(U) hijacks actin polymerization using mimicry and multivalency. Nature 454:1005-1008.
21. Campellone KG, et al. (2008) Repetitive N-WASP-binding elements of the enterohe-morrhagic Escherichia coli effector EspF(U) synergistically activate actin assembly. PLoS Pathog 4:e1000191.
22. Mayer BJ, Saksela K (2004) SH3 domains. Structure and Function of Modular Protein Domains , ed Cesareni G, Gimona M, Sudol M, Yaffe M (Wiley-VCH, Weinheim, Germany), pp 37-58.
23. Karkkainen S, et al. (2006) Identification of preferred protein interactions by phage-display of the human Src homology-3 proteome. EMBO Rep 7:186-191.
24. Millard TH, Dawson J, Machesky LM (2007) Characterisation of IRTKS, a novel IRSp53/ MIM family actin regulator with distinct filament bundling properties. J Cell Sci 120:1663-1672.
25. Lim KB, et al. (2008) The Cdc42 effector IRSp53 generates filopodia by coupling membrane protrusion with actin dynamics. J Biol Chem 283:20454-20472.
26. Scita G, Confalonieri S, Lappalainen P, Suetsugu S (2008) IRSp53: crossing the road of membrane and actin dynamics in the formation of membrane protrusions. Trends Cell Biol 18:52-60.
27. Suetsugu S, et al. (2006) Optimization of WAVE2 complex-induced actin polymerization by membrane-bound IRSp53, PIP(3), and Rac. J Cell Biol 173:571-585.
28. Cory GO, Cullen PJ (2007) Membrane curvature: the power of bananas, zeppelins and boomerangs. Curr Biol 17:R455-457.
29. Alto NM, et al. (2007) The type III effector EspF coordinates membrane trafficking by the spatiotemporal activation of two eukaryotic signaling pathways. J Cell Biol 178:1265-1278.
30. Marches O, et al. (2006) EspF of enteropathogenic Escherichia coli binds sorting nexin 9. J Bacteriol 188:3110-3115.
31. Lundmark R, Carlsson SR (2003) Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. J Biol Chem 278:46772-46781.
32. Viswanathan VK, et al. (2004) Comparative analysis of EspF from enteropathogenic and enterohemorrhagic Escherichia coli in alteration of epithelial barrier function. Infect Immun 72:3218-3227.
33. Luo Y, et al. (2000) Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature 405:1073-1077.
34. Touze T, et al. (2004) Self-association of EPEC intimin mediated by the beta-barrel-containing anchor domain: a role in clustering of the Tir receptor. Mol Microbiol 51:73-87.
35. Padrick SB, et al. (2008) Hierarchical regulation of WASP/WAVE proteins. Mol Cell 32:426-438.
36. Liu H, et al. (2002) Point mutants of EHEC intimin that diminish Tir recognition and actin pedestal formation highlight a putative Tir binding pocket. Mol Microbiol 45:1557-1573.
37. Campellone KG, Leong JM (2005) Nck-independent actin assembly is mediated by two phosphorylated tyrosines within enteropathogenic Escherichia coli Tir. Mol Microbiol 56:416-432.
38. Campellone KG, et al. (2007) Increased adherence and actin pedestal formation by dam-deficient enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 63:1468-1481.
39. Weiss SM, et al. (2009) IRSp53 links the enterohemorrhagic E.Coli effectors Tir and EspFu for actin pedestal formation. Cell Host Microbe 5:244-258.
40. Jerse AE, Yu J, Tall BD, Kaper JB (1990) A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci USA 87:7839-7843.