NleG type 3 effectors from enterohaemorrhagic Escherichia coli are U-Box E3 ubiquitin ligases

PLoS Pathogens

Volumn 6, Issue 6, 2010, Pages

  Wu, Bin ^a,b   Skarina, Tatiana ^c   Yee, Adelinda ^a,b   Jobin, Marie Claude ^b,c   Dileo, Rosa ^c   Semesi, Anthony ^a,b   Fares, Christophe ^a,b   Lemak, Alexander ^a,b   Coombes, Brian K ^d   Arrowsmith, Cheryl H ^a,b,c   Singer, Alexander U ^b,c   Savchenko, Alexei ^b,c  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

RING FINGER PROTEIN; UBIQUITIN PROTEIN LIGASE E3; ESCHERICHIA COLI PROTEIN; UBE2D2 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

ARTICLE; BINDING AFFINITY; ENZYME ACTIVITY; ESCHERICHIA COLI; FLUORESCENCE; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLARIZATION; PROTEIN INTERACTION; UBIQUITINATION; AMINO ACID SEQUENCE; CHEMISTRY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; RING FINGER MOTIF; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

ESCHERICHIA COLI; EUKARYOTA;

AMINO ACID SEQUENCE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; RING FINGER DOMAINS; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES;

EID: 77954670354     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000960     Document Type: Article

References (59)

1. Galan JE (2009) Common themes in the design and function of bacterial effectors. Cell Host Microbe 5: 571-579.
2. Parsot C (2009) Shigella type III secretion effectors: how, where, when, for what purposes? Curr Opin Microbiol 12: 110-116.
3. Bhavsar AP, Guttman JA, Finlay BB (2007) Manipulation of host-cell pathways by bacterial pathogens. Nature 449: 827-834.
4. Sal-Man N, Biemans-Oldehinkel E, Finlay BB (2009) Structural microengineers: pathogenic Escherichia coli redesigns the actin cytoskeleton in host cells. Structure 17: 15-19.
5. Mounier J, Popoff MR, Enninga J, Frame MC, Sansonetti PJ, et al. (2009) The IpaC carboxyterminal effector domain mediates Src-dependent actin polymer- ization during Shigella invasion of epithelial cells. PLoS Pathog 5: e1000271.
6. Steele-Mortimer O (2008) The Salmonella-containing vacuole: moving with the times. Curr Opin Microbiol 11: 38-45.
7. Alto NM, Weflen AW, Rardin MJ, Yarar D, Lazar CS, 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.
8. Brodsky IE, Medzhitov R (2009) Targeting of immune signalling networks by bacterial pathogens. Nat Cell Biol 11: 521-526.
9. Navarro L, Alto NM, Dixon JE (2005) Functions of the Yersinia effector proteins in inhibiting host immune responses. Curr Opin Microbiol 8: 21-27.
10. Rytkonen A, Holden DW (2007) Bacterial interference of ubiquitination and deubiquitination. Cell Host Microbe 1: 13-22.
11. Angot A, Vergunst A, Genin S, 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.
12. Spallek T, Robatzek S, Gohre V (2009) How microbes utilize host ubiquitination. Cell Microbiol 11: 1425-1434.
13. Huibregtse JM, Scheffner M, Beaudenon S, Howley PM (1995) A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc Natl Acad Sci U S A 92: 2563-2567.
14. Schwarz SE, Rosa JL, Scheffner M (1998) Characterization of human HECT domain family members and their interaction with UbcH5 and UbcH7. J Biol Chem 273: 12148-12154.
15. Scheffner M, Nuber U, Huibregtse JM (1995) Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 373: 81-83.
16. Jackson PK, Eldridge AG, Freed E, Furstenthal L, Hsu JY, et al. (2000) The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol 10: 429-439.
17. Cyr DM, Hohfeld J, Patterson C (2002) Protein quality control: U-box- containing E3 ubiquitin ligases join the fold. Trends Biochem Sci 27: 368- 375.
18. Abramovitch RB, Martin GB (2005) AvrPtoB: a bacterial type III effector that both elicits and suppresses programmed cell death associated with plant immunity. FEMS Microbiol Lett 245: 1-8.
19. Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311: 222-226.
20. Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, et al. (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448: 370-374.
21. Angot A, Peeters N, Lechner E, Vailleau F, Baud C, et al. (2006) Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. Proc Natl Acad Sci U S A 103: 14620-14625.
22. Diao J, Zhang Y, Huibregtse JM, Zhou D, Chen J (2008) Crystal structure of SopA, a Salmonella effector protein mimicking a eukaryotic ubiquitin ligase. Nat Struct Mol Biol 15: 65-70.
23. Rohde JR, Breitkreutz A, Chenal A, Sansonetti PJ, Parsot C (2007) Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 1: 77-83.
24. Haraga A, Miller SI (2006) A Salmonella type III secretion effector interacts with the mammalian serine/threonine protein kinase PKN1. Cell Microbiol 8: 837-846.
25. Zhu Y, Li H, Hu L, Wang J, Zhou Y, et al. (2008) Structure of a Shigella effector reveals a new class of ubiquitin ligases. Nat Struct Mol Biol 15: 1302-1308.
26. Singer AU, Rohde JR, Lam R, Skarina T, Kagan O, et al. (2008) Structure of the Shigella T3SS effector IpaH defines a new class of E3 ubiquitin ligases. Nat Struct Mol Biol 15: 1293-1301.
27. Quezada CM, Hicks SW, Galan JE, Stebbins CE (2009) A family of Salmonella virulence factors functions as a distinct class of autoregulated E3 ubiquitin ligases. Proc Natl Acad Sci U S A 106: 4864-4869.
28. Kaper JB, McDaniel TK, Jarvis KG, Gomez-Duarte O (1997) Genetics of virulence of enteropathogenic E. coli. Adv Exp Med Biol 412: 279-287.
29. Dean P, Maresca M, Kenny B (2005) EPEC's weapons of mass subversion. Curr Opin Microbiol 8: 28-34.
30. Tobe T, Beatson SA, Taniguchi H, Abe H, Bailey CM, et al. (2006) An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc Natl Acad Sci U S A 103: 14941-14946.
31. Li M, Rosenshine I, Yu HB, Nadler C, Mills E, et al. (2006) Identification and characterization of NleI, a new non-LEE-encoded effector of enteropathogenic Escherichia coli (EPEC). Microbes Infect 8: 2890-2898.
32. Holm L, Kaariainen S, Rosenstrom P, Schenkel A (2008) Searching protein structure databases with DaliLite v.3. Bioinformatics 24: 2780-2781.
33. Capili AD, Edghill EL, Wu K, Borden KL (2004) Structure of the C-terminal RING finger from a RING-IBR-RING/TRIAD motif reveals a novel zinc- binding domain distinct from a RING. J Mol Biol 340: 1117-1129.
34. Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S, et al. (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci U S A 96: 11364-11369.
35. Xu Z, Kohli E, Devlin KI, Bold M, Nix JC, et al. (2008) Interactions between the quality control ubiquitin ligase CHIP and ubiquitin conjugating enzymes. BMC Struct Biol 8: 26.
36. Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78: 399-434.
37. Winkler GS, Albert TK, Dominguez C, Legtenberg YI, Boelens R, et al. (2004) An altered-specificity ubiquitin-conjugating enzyme/ubiquitin-protein ligase pair. J Mol Biol 337: 157-165.
38. Shembade N, Ma A, Harhaj EW Inhibition of NF-kB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 327: 1135-1139.
39. Zhang RG, Skarina T, Katz JE, Beasley S, Khachatryan A, et al. (2001) Structure of Thermotoga maritima stationary phase survival protein SurE: a novel acid phosphatase. Structure 9: 1095-1106.
40. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234.
41. 15N-NOESY-HSQC. J Biomol NMR 24: 191-201.
42. Luan T, Jaravine V, Yee A, Arrowsmith CH, Orekhov VY (2005) Optimization of resolution and sensitivity of 4D NOESY using multi-dimensional decompo- sition. J Biomol NMR 33: 1-14.
43. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
44. Bax A, Vuister GW, Grzesiek S, Delaglio F, Wang AC, et al. (1994) Measurement of homo- and heteronuclear J couplings from quantitative J correlation. Methods Enzymol 239: 79-105.
45. Kay LE (1997) NMR methods for the study of protein structure and dynamics. Biochem Cell Biol 75: 1-15.
46. 13C labeling. Biochemistry 28: 7510-7516.
47. Lescop E, Schanda P, Brutscher B (2007) A set of BEST triple-resonance experiments for time-optimized protein resonance assignment. J Magn Reson 187: 163-169.
48. Cornilescu G, Marquardt JL, Bax A (1998) Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J Am Chem Soc 120: 6836-6837.
49. Guntert P (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278: 353-378.
50. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289-302.
51. Huang YJ, Powers R, Montelione GT (2005) Protein NMR recall, precision, and F-measure scores (RPF scores): structure quality assessment measures based on information retrieval statistics. J Am Chem Soc 127: 1665-1674.
52. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
53. Linge JP, Williams MA, Spronk CA, Bonvin AM, Nilges M (2003) Refinement of protein structures in explicit solvent. Proteins 50: 496-506.
54. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486.
55. Lovell SC, Davis IW, Arendall WB, 3rd, de Bakker PI, Word JM, et al. (2003) Structure validation by Ca geometry: Q, y and Cb deviation. Proteins 50: 437-450.
56. Bhattacharya A, Tejero R, Montelione GT (2007) Evaluating protein structures determined by structural genomics consortia. Proteins 66: 778-795.
57. Koradi R, Billeter M, Wuthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55, 29-32.
58. Shen Y, Lange O, Delaglio F, Rossi P, Aramini JM, et al. (2008) Consistent blind protein structure generation from NMR chemical shift data. Proc Natl Acad Sci U S A 105: 4685-4690.
59. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.