Complex Structure of OspI and Ubc13: The Molecular Basis of Ubc13 Deamidation and Convergence of Bacterial and Host E2 Recognition

PLoS Pathogens

Volumn 9, Issue 4, 2013, Pages

  Fu, Panhan ^a   Zhang, Xiaoqing ^a   Jin, Mengmeng ^a   Xu, Li ^a   Wang, Chong ^a   Xia, Zongping ^a   Zhu, Yongqun ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LUCIFERASE; OSPI PROTEIN; RECOMBINANT PROTEIN; UBIQUITIN CONJUGATING ENZYME 13; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DEAMINATION; INFECTION; INFORMATION PROCESSING; MUTAGENESIS; NONHUMAN; PLASMID; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; QUANTITATIVE ANALYSIS; RECOGNITION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SECRETION (PROCESS); UBIQUITINATION;

AMIDOHYDROLASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HEK293 CELLS; HUMANS; INFLAMMATION; MULTIPROTEIN COMPLEXES; NF-KAPPA B; PROTEIN BINDING; SEQUENCE ALIGNMENT; SHIGELLA FLEXNERI; TNF RECEPTOR-ASSOCIATED FACTOR 6; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

BACTERIA (MICROORGANISMS); SHIGELLA;

EID: 84876851948     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003322     Document Type: Article

References (48)

1. Kerscher O, Felberbaum R, Hochstrasser M, (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22: 159-180.
2. van Wijk SJ, Timmers HT, (2010) The family of ubiquitin-conjugating enzymes (E2s): deciding between life and death of proteins. FASEB J 24: 981-993.
3. Michelle C, Vourc'h P, Mignon L, Andres CR, (2009) What was the set of ubiquitin and ubiquitin-like conjugating enzymes in the eukaryote common ancestor? J Mol Evol 68: 616-628.
4. VanDemark AP, Hofmann RM, Tsui C, Pickart CM, Wolberger C, (2001) Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer. Cell 105: 711-720.
5. Hofmann RM, Pickart CM, (1999) Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96: 645-653.
6. Deng L, Wang C, Spencer E, Yang L, Braun A, et al. (2000) Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103: 351-361.
7. Xia ZP, Sun L, Chen X, Pineda G, Jiang X, et al. (2009) Direct activation of protein kinases by unanchored polyubiquitin chains. Nature 461: 114-119.
8. Ashida H, Ogawa M, Mimuro H, Kobayashi T, Sanada T, et al. (2011) Shigella are versatile mucosal pathogens that circumvent the host innate immune system. Curr Opin Immunol 23: 448-455.
9. Li H, Xu H, Zhou Y, Zhang J, Long C, et al. (2007) The phosphothreonine lyase activity of a bacterial type III effector family. Science 315: 1000-1003.
10. Zhu Y, Li H, Long C, Hu L, Xu H, et al. (2007) Structural insights into the enzymatic mechanism of the pathogenic MAPK phosphothreonine lyase. Mol Cell 28: 899-913.
11. 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.
12. 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.
13. 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.
14. 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.
15. Ashida H, Kim M, Schmidt-Supprian M, Ma A, Ogawa M, et al. (2010) A bacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKgamma to dampen the host NF-kappaB-mediated inflammatory response. Nat Cell Biol 12: 66-73; sup pp 61-69.
16. Wang F, Jiang Z, Li Y, He X, Zhao J, et al. (2013) Shigella flexneri T3SS effector IpaH4.5 modulates the host inflammatory response via interaction with NF-kappaB p65 protein. Cell Microbiol 15: 474-85.
17. Dong N, Zhu Y, Lu Q, Hu L, Zheng Y, et al. (2012) Structurally distinct bacterial TBC-like GAPs link Arf GTPase to Rab1 inactivation to counteract host defenses. Cell 150: 1029-1041.
18. Sanada T, Kim M, Mimuro H, Suzuki M, Ogawa M, et al. (2012) The Shigella flexneri effector OspI deamidates UBC13 to dampen the inflammatory response. Nature 483: 623-626.
19. Burroughs AM, Jaffee M, Iyer LM, Aravind L, (2008) Anatomy of the E2 ligase fold: implications for enzymology and evolution of ubiquitin/Ub-like protein conjugation. J Struct Biol 162: 205-218.
20. Yin Q, Lin SC, Lamothe B, Lu M, Lo YC, et al. (2009) E2 interaction and dimerization in the crystal structure of TRAF6. Nat Struct Mol Biol 16: 658-666.
21. Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, et al. (2005) Chaperoned ubiquitylation-crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol Cell 20: 525-538.
22. Holm L, Sander C, (1993) Protein structure comparison by alignment of distance matrices. J Mol Biol 233: 123-138.
23. Komander D, Lord CJ, Scheel H, Swift S, Hofmann K, et al. (2008) The structure of the CYLD USP domain explains its specificity for Lys63-linked polyubiquitin and reveals a B box module. Mol Cell 29: 451-464.
24. Hu M, Li P, Li M, Li W, Yao T, et al. (2002) Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 111: 1041-1054.
25. Hu M, Li P, Song L, Jeffrey PD, Chenova TA, et al. (2005) Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. EMBO J 24: 3747-3756.
26. Avvakumov GV, Walker JR, Xue S, Finerty PJ Jr, Mackenzie F, et al. (2006) Amino-terminal dimerization, NRDP1-rhodanese interaction, and inhibited catalytic domain conformation of the ubiquitin-specific protease 8 (USP8). J Biol Chem 281: 38061-38070.
27. Ye Y, Akutsu M, Reyes-Turcu F, Enchev RI, Wilkinson KD, et al. (2011) Polyubiquitin binding and cross-reactivity in the USP domain deubiquitinase USP21. EMBO Rep 12: 350-357.
28. Cui J, Yao Q, Li S, Ding X, Lu Q, et al. (2010) Glutamine deamidation and dysfunction of ubiquitin/NEDD8 induced by a bacterial effector family. Science 329: 1215-1218.
29. Hsu Y, Jubelin G, Taieb F, Nougayrede JP, Oswald E, et al. (2008) Structure of the cyclomodulin Cif from pathogenic Escherichia coli. J Mol Biol 384: 465-477.
30. Crow A, Hughes RK, Taieb F, Oswald E, Banfield MJ, (2012) The molecular basis of ubiquitin-like protein NEDD8 deamidation by the bacterial effector protein Cif. Proc Natl Acad Sci U S A 109: E1830-1838.
31. Zhu M, Shao F, Innes RW, Dixon JE, Xu Z, (2004) The crystal structure of Pseudomonas avirulence protein AvrPphB: a papain-like fold with a distinct substrate-binding site. Proc Natl Acad Sci U S A 101: 302-307.
32. Storer AC, Menard R, (1994) Catalytic mechanism in papain family of cysteine peptidases. Methods Enzymol 244: 486-500.
33. Slotman JA, da Silva Almeida AC, Hassink GC, van de Ven RH, van Kerkhof P, et al. (2012) Ubc13 and COOH terminus of Hsp70-interacting protein (CHIP) are required for growth hormone receptor endocytosis. J Biol Chem 287: 15533-15543.
34. Wiener R, Zhang X, Wang T, Wolberger C, (2012) The mechanism of OTUB1-mediated inhibition of ubiquitination. Nature 483: 618-622.
35. Nakada S, Tai I, Panier S, Al-Hakim A, Iemura S, et al. (2010) Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466: 941-946.
36. Buetow L, Flatau G, Chiu K, Boquet P, Ghosh P, (2001) Structure of the Rho-activating domain of Escherichia coli cytotoxic necrotizing factor 1. Nat Struct Biol 8: 584-588.
37. Cruz-Migoni A, Hautbergue GM, Artymiuk PJ, Baker PJ, Bokori-Brown M, et al. (2011) A Burkholderia pseudomallei toxin inhibits helicase activity of translation factor eIF4A. Science 334: 821-824.
38. Zhang L, Krachler AM, Broberg CA, Li Y, Mirzael H, et al. (2012) Type III effector VopC mediates invasion for Vibrio species. Cell Rep 1: 453-460.
39. Orth JH, Preuss I, Fester I, Schlosser A, Wilson BA, et al. (2009) Pasteurella multocida toxin activation of heterotrimeric G proteins by deamidation. Proc Natl Acad Sci U S A 106: 7179-7184.
40. Yao Q, Cui J, Zhu Y, Wang G, Hu L, et al. (2009) A bacterial type III effector family uses the papain-like hydrolytic activity to arrest the host cell cycle. Proc Natl Acad Sci U S A 106: 3716-3721.
41. Kitadokoro K, Kamitani S, Miyazawa M, Hanajima-Ozawa M, Fukui A, et al. (2007) Crystal structures reveal a thiol protease-like catalytic triad in the C-terminal region of Pasteurella multocida toxin. Proc Natl Acad Sci U S A 104: 5139-5144.
42. 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.
43. Shembade N, Ma A, Harhaj EW, (2010) Inhibition of NF-kappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 327: 1135-1139.
44. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
45. 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.
46. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
47. Laskowski AR, MacArthur WM, Moss SD, Thornton MJ, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993: 283-291.
48. Tamano K, Aizawa S, Katayama E, Nonaka T, Imajoh-Ohmi S, et al. (2000) Supramolecular structure of the Shigella type III secretion machinery: the needle part is changeable in length and essential for delivery of effectors. EMBO J 19: 3876-3887.