Structural analysis of the uba domain of x-linked inhibitor of apoptosis protein reveals different surfaces for ubiquitin-binding and self-association

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Tse, Man Kit ^a,b   Hui, Sin Kam ^b   Yang, Yinhua ^c   Yin, Si Tao ^d   Hu, Hong Yu ^d   Zou, Bing ^e   Wong, Benjamin Chun Yu ^e   Sze, Kong Hung ^a,b  

^a THE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^e UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

UBIQUITINATED PROTEIN; X LINKED INHIBITOR OF APOPTOSIS; DIUBIQUITIN CONJUGATE; LYSINE; POLYUBIQUITIN; UBIQUITIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DIMERIZATION; HUMAN; HYDROPHOBICITY; MOLECULAR DOCKING; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN MOTIF; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SOLUTION AND SOLUBILITY; STRUCTURE ACTIVITY RELATION; SURFACE PROPERTY;

AMINO ACID SEQUENCE; BINDING SITES; HUMANS; LYSINE; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYUBIQUITIN; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SOLUTIONS; STRUCTURE-ACTIVITY RELATIONSHIP; SURFACE PROPERTIES; UBIQUITIN; UBIQUITINS; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 83455262533     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028511     Document Type: Article

References (67)

1. Deveraux QL, Reed JC, (1999) IAP family proteins-suppressors of apoptosis. Genes Dev 13: 239-252.
2. Salvesen GS, Abrams JM, (2004) Caspase activation- stepping on the gas or releasing the brakes? Lessons from humans and flies. Oncogene 23: 2774-2784.
3. Vucic D, (2008) Targeting IAP (inhibitor of apoptosis) proteins for therapeutic intervention in tumors. Curr Cancer Drug Targets 8: 110-117.
4. Hunter AM, LaCasse EC, Korneluk RG, (2007) The inhibitors of apoptosis (IAPs) as cancer targets. Apoptosis 12: 1543-1568.
5. Schimmer AD, Dalili S, Batey RA, Riedl SJ, (2006) Targeting XIAP for the treatment of malignancy. Cell Death Differ 13: 179-188.
6. Takahashi R, Deveraux Q, Tamm I, Welsh K, Assa-Munt N, et al. (1998) A single BIR domain of XIAP sufficient for inhibiting caspases. J Biol Chem 273: 7787-7790.
7. Sun C, Cai M, Meadows RP, Xu N, Gunasekera AH, et al. (2000) NMR structure and mutagenesis of the third Bir domain of the inhibitor of apoptosis protein XIAP. J Biol Chem 275: 33777-33781.
8. Lin SC, Huang Y, Lo YC, Lu M, Wu H, (2007) Crystal structure of the BIR1 domain of XIAP in two crystal forms. J Mol Biol 372: 847-854.
9. Galban S, Duckett CS, (2010) XIAP as a ubiquitin ligase in cellular signaling. Cell Death Differ 17: 54-60.
10. Srinivasula SM, Ashwell JD, (2008) IAPs: what's in a name? Mol Cell 30: 123-135.
11. Gyrd-Hansen M, Darding M, Miasari M, Santoro MM, Zender L, et al. (2008) IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-kappaB as well as cell survival and oncogenesis. Nat Cell Biol 10: 1309-1317.
12. Blankenship JW, Varfolomeev E, Goncharov T, Fedorova AV, Kirkpatrick DS, et al. (2009) Ubiquitin binding modulates IAP antagonist-stimulated proteasomal degradation of c-IAP1 and c-IAP2(1). Biochem J 417: 149-160.
13. Cook WJ, Jeffrey LC, Sullivan ML, Vierstra RD, (1992) Three-dimensional structure of a ubiquitin-conjugating enzyme (E2). J Biol Chem 267: 15116-15121.
14. Varadan R, Assfalg M, Haririnia A, Raasi S, Pickart C, et al. (2004) Solution conformation of Lys63-linked di-ubiquitin chain provides clues to functional diversity of polyubiquitin signaling. J Biol Chem 279: 7055-7063.
15. Komander D, Reyes-Turcu F, Licchesi JD, Odenwaelder P, Wilkinson KD, et al. (2009) Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep 10: 466-473.
16. Kirisako T, Kamei K, Murata S, Kato M, Fukumoto H, et al. (2006) A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J 25: 4877-4887.
17. Iwai K, Tokunaga F, (2009) Linear polyubiquitination: a new regulator of NF-kappaB activation. EMBO Rep 10: 706-713.
18. Kirkin V, Dikic I, (2007) Role of ubiquitin- and Ubl-binding proteins in cell signaling. Curr Opin Cell Biol 19: 199-205.
19. Chang YG, Song AX, Gao YG, Shi YH, Lin XJ, et al. (2006) Solution structure of the ubiquitin-associated domain of human BMSC-UbP and its complex with ubiquitin. Protein Sci 15: 1248-1259.
20. Chim N, Gall WE, Xiao J, Harris MP, Graham TR, et al. (2004) Solution structure of the ubiquitin-binding domain in Swa2p from Saccharomyces cerevisiae. Proteins 54: 784-793.
21. Ciani B, Layfield R, Cavey JR, Sheppard PW, Searle MS, (2003) Structure of the ubiquitin-associated domain of p62 (SQSTM1) and implications for mutations that cause Paget's disease of bone. J Biol Chem 278: 37409-37412.
22. Dieckmann T, Withers-Ward ES, Jarosinski MA, Liu CF, Chen IS, et al. (1998) Structure of a human DNA repair protein UBA domain that interacts with HIV-1 Vpr. Nat Struct Biol 5: 1042-1047.
23. Lowe ED, Hasan N, Trempe JF, Fonso L, Noble ME, et al. (2006) Structures of the Dsk2 UBL and UBA domains and their complex. Acta Crystallogr D Biol Crystallogr 62: 177-188.
24. Mueller TD, Feigon J, (2002) Solution structures of UBA domains reveal a conserved hydrophobic surface for protein-protein interactions. J Mol Biol 319: 1243-1255.
25. Panneerselvam S, Marx A, Mandelkow EM, Mandelkow E, (2006) Structure of the catalytic and ubiquitin-associated domains of the protein kinase MARK/Par-1. Structure 14: 173-183.
26. Trempe JF, Brown NR, Lowe ED, Gordon C, Campbell ID, et al. (2005) Mechanism of Lys48-linked polyubiquitin chain recognition by the Mud1 UBA domain. EMBO J 24: 3178-3189.
27. Withers-Ward ES, Mueller TD, Chen IS, Feigon J, (2000) Biochemical and structural analysis of the interaction between the UBA(2) domain of the DNA repair protein HHR23A and HIV-1 Vpr. Biochemistry 39: 14103-14112.
28. Yuan X, Simpson P, McKeown C, Kondo H, Uchiyama K, et al. (2004) Structure, dynamics and interactions of p47, a major adaptor of the AAA ATPase, p97. EMBO J 23: 1463-1473.
29. Swanson KA, Hicke L, Radhakrishnan I, (2006) Structural basis for monoubiquitin recognition by the Ede1 UBA domain. J Mol Biol 358: 713-724.
30. Ohno A, Jee J, Fujiwara K, Tenno T, Goda N, et al. (2005) Structure of the UBA domain of Dsk2p in complex with ubiquitin molecular determinants for ubiquitin recognition. Structure 13: 521-532.
31. Raasi S, Varadan R, Fushman D, Pickart CM, (2005) Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat Struct Mol Biol 12: 708-714.
32. Bayrer JR, Zhang W, Weiss MA, (2005) Dimerization of doublesex is mediated by a cryptic ubiquitin-associated domain fold: implications for sex-specific gene regulation. J Biol Chem 280: 32989-32996.
33. Bertolaet BL, Clarke DJ, Wolff M, Watson MH, Henze M, et al. (2001) UBA domains mediate protein-protein interactions between two DNA damage-inducible proteins. J Mol Biol 313: 955-963.
34. Kozlov G, Peschard P, Zimmerman B, Lin T, Moldoveanu T, et al. (2007) Structural basis for UBA-mediated dimerization of c-Cbl ubiquitin ligase. J Biol Chem 282: 27547-27555.
35. Peschard P, Kozlov G, Lin T, Mirza IA, Berghuis AM, et al. (2007) Structural basis for ubiquitin-mediated dimerization and activation of the ubiquitin protein ligase Cbl-b. Mol Cell 27: 474-485.
36. Long J, Garner TP, Pandya MJ, Craven CJ, Chen P, et al. (2010) Dimerisation of the UBA domain of p62 inhibits ubiquitin binding and regulates NF-kappaB signalling. J Mol Biol 396: 178-194.
37. Sasaki T, Funakoshi M, Endicott JA, Kobayashi H, (2005) Budding yeast Dsk2 protein forms a homodimer via its C-terminal UBA domain. Biochem Biophys Res Commun 336: 530-535.
38. Zhang D, Raasi S, Fushman D, (2008) Affinity makes the difference: nonselective interaction of the UBA domain of Ubiquilin-1 with monomeric ubiquitin and polyubiquitin chains. J Mol Biol 377: 162-180.
39. Sims JJ, Haririnia A, Dickinson BC, Fushman D, Cohen RE, (2009) Avid interactions underlie the Lys63-linked polyubiquitin binding specificities observed for UBA domains. Nat Struct Mol Biol 16: 883-889.
40. Dominguez C, Boelens R, Bonvin AM, (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125: 1731-1737.
41. de Vries SJ, van Dijk AD, Krzeminski M, van Dijk M, Thureau A, et al. (2007) HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets. Proteins 69: 726-733.
42. Dey S, Pal A, Chakrabarti P, Janin J, (2010) The subunit interfaces of weakly associated homodimeric proteins. J Mol Biol 398: 146-160.
43. Ogura K, Terasawa H, Inagaki F, (1996) An improved double-tuned and isotope-filtered pulse scheme based on a pulsed field gradient and a wide-band inversion shaped pulse. J Biomol NMR 8: 492-498.
44. Varadan R, Assfalg M, Raasi S, Pickart C, Fushman D, (2005) Structural determinants for selective recognition of a Lys48-linked polyubiquitin chain by a UBA domain. Mol Cell 18: 687-698.
45. Winget JM, Mayor T, (2010) The diversity of ubiquitin recognition: hot spots and varied specificity. Mol Cell 38: 627-635.
46. Reyes-Turcu FE, Horton JR, Mullally JE, Heroux A, Cheng X, et al. (2006) The ubiquitin binding domain ZnF UBP recognizes the C-terminal diglycine motif of unanchored ubiquitin. Cell 124: 1197-1208.
47. Mueller TD, Kamionka M, Feigon J, (2004) Specificity of the interaction between ubiquitin-associated domains and ubiquitin. J Biol Chem 279: 11926-11936.
48. Matta-Camacho E, Kozlov G, Trempe JF, Gehring K, (2009) Atypical binding of the Swa2p UBA domain to ubiquitin. J Mol Biol 386: 569-577.
49. Zhou ZR, Gao HC, Zhou CJ, Chang YG, Hong J, et al. (2008) Differential ubiquitin binding of the UBA domains from human c-Cbl and Cbl-b: NMR structural and biochemical insights. Protein Sci 17: 1805-1814.
50. Mace PD, Linke K, Feltham R, Schumacher FR, Smith CA, et al. (2008) Structures of the cIAP2 RING domain reveal conformational changes associated with ubiquitin-conjugating enzyme (E2) recruitment. J Biol Chem 283: 31633-31640.
51. Weeks SD, Grasty KC, Hernandez-Cuebas L, Loll PJ, (2009) Crystal structures of Lys-63-linked tri- and di-ubiquitin reveal a highly extended chain architecture. Proteins 77: 753-759.
52. Charbonnier S, Gallego O, Gavin A-C, (2008) The social network of a cell: Recent advances in interactome mapping. In: El-Gewely MR, editors. pp. 1-28 Biotechnology Annual Review: Elsevier.
53. Varadan R, Walker O, Pickart C, Fushman D, (2002) Structural properties of polyubiquitin chains in solution. J Mol Biol 324: 637-647.
54. Ryabov Y, Fushman D, (2006) Interdomain mobility in di-ubiquitin revealed by NMR. Proteins 63: 787-796.
55. Eddins MJ, Varadan R, Fushman D, Pickart CM, Wolberger C, (2007) Crystal structure and solution NMR studies of Lys48-linked tetraubiquitin at neutral pH. J Mol Biol 367: 204-211.
56. Hui SK, Tse MK, Yang Y, Wong BC, Sze KH, (2010) Backbone and side-chain 1H, 13C and 15N assignments of the ubiquitin-associated domain of human X-linked inhibitor of apoptosis protein. Biomol NMR Assign 4: 13-15.
57. Reyes-Turcu FE, Shanks JR, Komander D, Wilkinson KD, (2008) Recognition of polyubiquitin isoforms by the multiple ubiquitin binding modules of isopeptidase T. J Biol Chem 283: 19581-19592.
58. Goddard TD, Kneller DG, (1998) SPARKY 3.0. University of California, San Francisco.
59. Guntert P, (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278: 353-378.
60. 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.
61. Morris AL, MacArthur MW, Hutchinson EG, Thornton JM, (1992) Stereochemical quality of protein structure coordinates. Proteins 12: 345-364.
62. 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.
63. Holm L, Kaariainen S, Rosenstrom P, Schenkel A, (2008) Searching protein structure databases with DaliLite v.3. Bioinformatics 24: 2780-2781.
64. DeLano WL, (2002) Pymol. DeLano Scientific, South San Francisco, CA.
65. Jaravine VA, Zhuravleva AV, Permi P, Ibraghimov I, Orekhov VY, (2008) Hyperdimensional NMR spectroscopy with nonlinear sampling. J Am Chem Soc 130: 3927-3936.
66. French M, Swanson K, Shih SC, Radhakrishnan I, Hicke L, (2005) Identification and Characterization of Modular Domains That Bind Ubiquitin. In: Raymond JD, editors. pp. 135-157 Methods in Enzymology: Academic Press.
67. Kay LE, Torchia DA, Bax A, (1989) Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28: 8972-8979.