Structural Basis for Ubiquitin-Mediated Dimerization and Activation of the Ubiquitin Protein Ligase Cbl-b

Molecular Cell

Volumn 27, Issue 3, 2007, Pages 474-485

  Peschard, Pascal ^a,b   Kozlov, Guennadi ^a   Lin, Tong ^a,b   Mirza, I Ahmad ^a   Berghuis, Albert M ^a   Lipkowitz, Stanley ^c   Park, Morag ^a,b   Gehring, Kalle ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

PROTEINS

Indexed keywords

AMINO ACID; CBL PROTEIN; PROTEIN CBL B; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; HUMAN CELL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; BINDING SITES; CELL LINE; CRYSTALLIZATION; DIMERIZATION; ENZYME ACTIVATION; HELA CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; KIDNEY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTO-ONCOGENE PROTEINS C-CBL; SEQUENCE HOMOLOGY, AMINO ACID; TRANSFECTION; UBIQUITIN;

EID: 34547195241     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.06.023     Document Type: Article

References (42)

1. Balachandran P., Dragone L., Garrity-Ryan L., Lemus A., Weiss A., and Engel J. The ubiquitin ligase Cbl-b limits Pseudomonas aeruginosa exotoxin T-mediated virulence. J. Clin. Invest. 117 (2007) 419-427
2. Bartkiewicz M., Houghton A., and Baron R. Leucine zipper-mediated homodimerization of the adaptor protein c-Cbl. A role in c-Cbl's tyrosine phosphorylation and its association with epidermal growth factor receptor. J. Biol. Chem. 274 (1999) 30887-30895
3. Bayrer J.R., Zhang W., and Weiss M.A. Dimerization of doublesex is mediated by a cryptic ubiquitin-associated domain fold: implications for sex-specific gene regulation. J. Biol. Chem. 280 (2005) 32989-32996
4. Bertolaet B.L., Clarke D.J., Wolff M., Watson M.H., Henze M., Divita G., and Reed S.I. UBA domains mediate protein-protein interactions between two DNA damage-inducible proteins. J. Mol. Biol. 313 (2001) 955-963
5. Chang Y.G., Song A.X., Gao Y.G., Shi Y.H., Lin X.J., Cao X.T., Lin D.H., and Hu H.Y. Solution structure of the ubiquitin-associated domain of human BMSC-UbP and its complex with ubiquitin. Protein Sci. 15 (2006) 1248-1259
6. Chim N., Gall W.E., Xiao J., Harris M.P., Graham T.R., and Krezel A.M. Solution structure of the ubiquitin-binding domain in Swa2p from Saccharomyces cerevisiae. Proteins 54 (2004) 784-793
7. Ciani B., Layfield R., Cavey J.R., Sheppard P.W., and Searle M.S. Structure of the ubiquitin-associated domain of p62 (SQSTM1) and implications for mutations that cause Paget's disease of bone. J. Biol. Chem. 278 (2003) 37409-37412
8. Davies G.C., Ettenberg S.A., Coats A.O., Mussante M., Ravichandran S., Collins J., Nau M.M., and Lipkowitz S. Cbl-b interacts with ubiquitinated proteins; differential functions of the UBA domains of c-Cbl and Cbl-b. Oncogene 23 (2004) 7104-7115
9. Dieckmann T., Withers-Ward E.S., Jarosinski M.A., Liu C.F., Chen I.S., and Feigon J. Structure of a human DNA repair protein UBA domain that interacts with HIV-1 Vpr. Nat. Struct. Biol. 5 (1998) 1042-1047
10. Ettenberg S.A., Magnifico A., Cuello M., Nau M.M., Rubinstein Y.R., Yarden Y., Weissman A.M., and Lipkowitz S. Cbl-b-dependent coordinated degradation of the epidermal growth factor receptor signaling complex. J. Biol. Chem. 276 (2001) 27677-27684
11. Hofmann K., and Bucher P. The UBA domain: a sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends Biochem. Sci. 21 (1996) 172-173
12. Kang R.S., Daniels C.M., Francis S.A., Shih S.C., Salerno W.J., Hicke L., and Radhakrishnan I. Solution structure of a CUE-ubiquitin complex reveals a conserved mode of ubiquitin binding. Cell 113 (2003) 621-630
13. Lee S., Tsai Y.C., Mattera R., Smith W.J., Kostelansky M.S., Weissman A.M., Bonifacino J.S., and Hurley J.H. Structural basis for ubiquitin recognition and autoubiquitination by Rabex-5. Nat. Struct. Mol. Biol. 13 (2006) 264-271
14. Liu J., DeYoung S.M., Hwang J.B., O'Leary E.E., and Saltiel A.R. The roles of Cbl-b and c-Cbl in insulin-stimulated glucose transport. J. Biol. Chem. 278 (2003) 36754-36762
15. Lowe E.D., Hasan N., Trempe J.F., Fonso L., Noble M.E., Endicott J.A., Johnson L.N., and Brown N.R. Structures of the Dsk2 UBL and UBA domains and their complex. Acta Crystallogr. D Biol. Crystallogr. 62 (2006) 177-188
16. Magnifico A., Ettenberg S., Yang C., Mariano J., Tiwari S., Fang S., Lipkowitz S., and Weissman A.M. WW domain HECT E3s target Cbl RING finger E3s for proteasomal degradation. J. Biol. Chem. 278 (2003) 43169-43177
17. McRee D.E. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
18. Mueller T.D., and Feigon J. Solution structures of UBA domains reveal a conserved hydrophobic surface for protein-protein interactions. J. Mol. Biol. 319 (2002) 1243-1255
19. Mueller T.D., Kamionka M., and Feigon J. Specificity of the interaction between ubiquitin-associated domains and ubiquitin. J. Biol. Chem. 279 (2004) 11926-11936
20. Murshudov G.N., Vagin A.A., Lebedev A., Wilson K.S., and Dodson E.J. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D Biol. Crystallogr. 55 (1999) 247-255
21. Ohno A., Jee J., Fujiwara K., Tenno T., Goda N., Tochio H., Kobayashi H., Hiroaki H., and Shirakawa M. Structure of the UBA domain of Dsk2p in complex with ubiquitin molecular determinants for ubiquitin recognition. Structure 13 (2005) 521-532
22. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
23. Panneerselvam S., Marx A., Mandelkow E.M., and Mandelkow E. Structure of the catalytic and ubiquitin-associated domains of the protein kinase MARK/Par-1. Structure 14 (2006) 173-183
24. Penengo L., Mapelli M., Murachelli A.G., Confalonieri S., Magri L., Musacchio A., Di Fiore P.P., Polo S., and Schneider T.R. Crystal structure of the ubiquitin binding domains of rabex-5 reveals two modes of interaction with ubiquitin. Cell 124 (2006) 1183-1195
25. Peschard P., Fournier T.M., Lamorte L., Naujokas M.A., Band H., Langdon W.Y., and Park M. Mutation of the c-Cbl TKB domain binding site on the Met receptor tyrosine kinase converts it into a transforming protein. Mol. Cell 8 (2001) 995-1004
26. Peschard P., Ishiyama N., Lin T., Lipkowitz S., and Park M. A conserved DpYR motif in the juxtamembrane domain of the Met receptor family forms an atypical c-Cbl/Cbl-b tyrosine kinase binding domain binding site required for suppression of oncogenic activation. J. Biol. Chem. 279 (2004) 29565-29571
27. Prag G., Misra S., Jones E.A., Ghirlando R., Davies B.A., Horazdovsky B.F., and Hurley J.H. Mechanism of ubiquitin recognition by the CUE domain of Vps9p. Cell 113 (2003) 609-620
28. Raasi S., Varadan R., Fushman D., and Pickart C.M. Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat. Struct. Mol. Biol. 12 (2005) 708-714
29. Read R.J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D Biol. Crystallogr. 57 (2001) 1373-1382
30. Ryan P.E., Davies G.C., Nau M.M., and Lipkowitz S. Regulating the regulator: negative regulation of Cbl ubiquitin ligases. Trends Biochem. Sci. 31 (2006) 79-88
31. Ryu K.S., Lee K.J., Bae S.H., Kim B.K., Kim K.A., and Choi B.S. Binding surface mapping of intra- and interdomain interactions among hHR23B, ubiquitin, and polyubiquitin binding site 2 of S5a. J. Biol. Chem. 278 (2003) 36621-36627
32. Sasaki T., Funakoshi M., Endicott J.A., and Kobayashi H. Budding yeast Dsk2 protein forms a homodimer via its C-terminal UBA domain. Biochem. Biophys. Res. Commun. 336 (2005) 530-535
33. Schiering N., Casale E., Caccia P., Giordano P., and Battistini C. Dimer formation through domain swapping in the crystal structure of the Grb2-SH2-Ac-pYVNV complex. Biochemistry 39 (2000) 13376-13382
34. Shih S.C., Prag G., Francis S.A., Sutanto M.A., Hurley J.H., and Hicke L. A ubiquitin-binding motif required for intramolecular monoubiquitylation, the CUE domain. EMBO J. 22 (2003) 1273-1281
35. Swanson K.A., Hicke L., and Radhakrishnan I. Structural basis for monoubiquitin recognition by the Ede1 UBA domain. J. Mol. Biol. 358 (2006) 713-724
36. Thien C.B., and Langdon W.Y. c-Cbl and Cbl-b ubiquitin ligases: substrate diversity and the negative regulation of signalling responses. Biochem. J. 391 (2005) 153-166
37. Trempe J.F., Brown N.R., Lowe E.D., Gordon C., Campbell I.D., Noble M.E., and Endicott J.A. Mechanism of Lys48-linked polyubiquitin chain recognition by the Mud1 UBA domain. EMBO J. 24 (2005) 3178-3189
38. Varadan R., Assfalg M., Raasi S., Pickart C., and Fushman D. Structural determinants for selective recognition of a Lys48-linked polyubiquitin chain by a UBA domain. Mol. Cell 18 (2005) 687-698
39. Wang Q., Goh A.M., Howley P.M., and Walters K.J. Ubiquitin recognition by the DNA repair protein hHR23a. Biochemistry 42 (2003) 13529-13535
40. Waterman H., Katz M., Rubin C., Shtiegman K., Lavi S., Elson A., Jovin T., and Yarden Y. A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. EMBO J. 21 (2002) 303-313
41. Withers-Ward E.S., Mueller T.D., Chen I.S., and Feigon J. Biochemical and structural analysis of the interaction between the UBA(2) domain of the DNA repair protein HHR23A and HIV-1 Vpr. Biochemistry 39 (2000) 14103-14112
42. Yuan X., Simpson P., McKeown C., Kondo H., Uchiyama K., Wallis R., Dreveny I., Keetch C., Zhang X., Robinson C., et al. Structure, dynamics and interactions of p47, a major adaptor of the AAA ATPase, p97. EMBO J. 23 (2004) 1463-1473