Structure of the DDB1-CRBN E3 ubiquitin ligase in complex with thalidomide

Nature

Volumn 512, Issue 1, 2014, Pages 49-53

  Fischer, Eric S ^a,b   Böhm, Kerstin ^a,b   Lydeard, John R ^c   Yang, Haidi ^d   Stadler, Michael B ^a,b,e   Cavadini, Simone ^a,b   Nagel, Jane ^d   Serluca, Fabrizio ^d   Acker, Vincent ^f   Lingaraju, Gondichatnahalli M ^a,b   Tichkule, Ritesh B ^d   Schebesta, Michael ^d   Forrester, William C ^d   Schirle, Markus ^d   Hassiepen, Ulrich ^f   Ottl, Johannes ^f   Hild, Marc ^d   Beckwith, Rohan E J ^d   Harper, J Wade ^c   Jenkins, Jeremy L ^d   Thomä, Nicolas H ^a,b   more..

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c HARVARD MEDICAL SCHOOL   (United States)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^e SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^f NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PEPTIDE HYDROLASES; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; THALIDOMIDE; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 84905568369     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13527     Document Type: Article

References (43)

1. Bartlett, J. B., Dredge, K. & Dalgleish, A. G. The evolution of thalidomide and its IMiD derivatives as anticancer agents. Nature Rev. Cancer 4, 314-322 (2004).
2. Shortt, J., Hsu, A. K. & Johnstone, R. W. Thalidomide-analogue biology: immunological, molecular and epigenetic targetsincancer therapy. Oncogene 32, 4191-4202 (2013).
3. Melchert, M. & List, A. The thalidomide saga. Int. J. Biochem. Cell Biol. 39, 1489-1499 (2007).
4. McBride, W. G. Thalidomide and congenital abnormalities. Lancet 278, 1358 (1961).
5. Lenz, W., Pfeiffer, R. A., Kosenow, W. & Hayman, D. J. Thalidomide and congenital abnormalities. Lancet 279, 45-46 (1962).
6. Sheskin, J. Thalidomideinthe treatmentoflepra reactions. Clin. Pharmacol. Ther. 6, 303-306 (1965).
7. D'Amato, R. J., Loughnan, M. S., Flynn, E. & Folkman, J. Thalidomide is an inhibitor of angiogenesis. Proc. Natl Acad. Sci. USA 91, 4082-4085 (1994).
8. Pan, B. & Lentzsch, S. The application and biology of immunomodulatory drugs (IMiDs) in cancer. Pharmacol. Ther. 136, 56-68 (2012).
9. Singhal, S. et al. Antitumor activity of thalidomide in refractory multiple myeloma. N. Engl. J. Med. 341, 1565-1571 (1999).
10. Ito, T. et al. Identification of a primary target of thalidomide teratogenicity. Science 327, 1345-1350 (2010).
11. Higgins, J. J., Pucilowska, J., Lombardi, R. Q. & Rooney, J. P. A mutation in a novel ATP-dependent Lon protease gene in a kindred with mild mental retardation. Neurology 63, 1927-1931 (2004).
12. Lopez-Girona, A. et al. Cereblon is a direct protein target for immunomodulatory and antiproliferative activities of lenalidomide and pomalidomide. Leukemia 26, 2326-2335 (2012).
13. Zhu, Y. X. et al. Cereblon expression is required for the antimyeloma activity of lenalidomide and pomalidomide. Blood 118, 4771-4779 (2011).
14. Lu, G. et al. The myeloma drug lenalidomide promotes the cereblon-dependent destruction of Ikaros proteins. Science 343, 305-309 (2014).
15. Kronke, J. et al. Lenalidomide causes selective degradation of IKZF1 and IKZF3 in multiple myeloma cells. Science 343, 301-305 (2014).
16. Gandhi, A. K. et al. Immunomodulatory agents lenalidomide and pomalidomide co-stimulate T cells by inducing degradation of T cell repressors Ikaros and Aiolos via modulation of the E3 ubiquitin ligase complex CRL4(CRBN.). Br. J. Haematol. 164, 811-821 (2014).
17. Li, T., Chen, X., Garbutt, K. C., Zhou, P. & Zheng, N. Structure of DDB1 in complex with a Paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 124, 105-117 (2006).
18. Scrima, A. et al. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135, 1213-1223 (2008).
19. Li, T., Robert, E. I., van Breugel, P. C., Strubin, M. & Zheng, N. A promiscuous alpha-helical motif anchors viral hijackers and substrate receptors to the CUL4-DDB1 ubiquitin ligase machinery. Nature Struct. Mol. Biol. 17, 105-111 (2010).
20. Scrima, A. et al. Detecting UV-lesionsin the genome: The modular CRL4 ubiquitin ligase does it best! FEBS Lett. 585, 2818-2825 (2011).
21. Hur, S., Stroud, R. M. & Finer-Moore, J. Substrate recognition by RNA 5-methyluridine methyltransferases and pseudouridine synthases: a structural perspective. J. Biol. Chem. 281, 38969-38973 (2006).
22. Ruchelman, A. L. et al. Isosteric analogs of lenalidomide and pomalidomide: Synthesis and biological activity. Bioorg. Med. Chem. Lett. 23, 360-365 (2013).
23. Jin, J., Arias, E., Chen, J., Harper, J. & Walter, J. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, whichis required forSphase destruction ofthe replication factor Cdt1. Mol. Cell 23, 709-721 (2006).
24. Angers, S. et al. Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443, 590-593 (2006).
25. Fischer, E. S. et al. The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 147, 1024-1039 (2011).
26. Hornbeck, P. V. et al. PhosphoSitePlus:acomprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 40, D261-D270 (2012).
27. Hofmeister, C. C. et al. Phase I trial of lenalidomide and CCI-779 in patients with relapsed multiple myeloma: evidence for lenalidomide-CCI-779 interaction via P-glycoprotein. J. Clin. Oncol. 29, 3427-3434 (2011).
28. Zhou, S. et al. Transport of thalidomide by the human intestinal caco-2 monolayers. Eur. J. Drug Metab. Pharmacokinet. 30, 49-61 (2005).
29. Roche, S. et al. Development, validation and application of a sensitive LC-MS/MS method for the quantification of thalidomide in human serum, cells and cell culture medium. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 902, 16-26 (2012).
30. Crowley, M. A. et al. Further evidence for the possible role of MEIS2 in the development of cleft palate and cardiac septum. Am. J. Med. Genet. A. 152A, 1326-1327 (2010).
31. Capdevila, J., Tsukui, T., Rodŕiquez Esteban, C., Zappavigna, V. & Izpisúa Belmonte, J. C. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol. Cell 4, 839-849 (1999).
32. Paige, S. L. et al. A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell 151, 221-232 (2012).
33. Skaar, J. R., Pagan, J. K. & Pagano, M. Mechanisms and function of substrate recruitment by F-box proteins. Nature Rev. Mol. Cell Biol. 14, 369-381 (2013).
34. Bennett, E. J., Rush, J., Gygi, S. P. & Harper, J. W. Dynamics of Cullin-RING Ubiquitin Ligase Network Revealed by Systematic Quantitative Proteomics. Cell 143, 951-965 (2010).
35. Tan, X. et al. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640-645 (2007).
36. Huai, Q. et al. Crystal structure of calcineurin-cyclophilin-cyclosporin shows common but distinct recognition of immunophilin-drug complexes. Proc. Natl Acad. Sci. USA 99, 12037-12042 (2002).
37. Kissinger, C. R. et al. Crystal structures of human calcineurin and the human FKBP12-FK506-calcineurin complex. Nature 378, 641-644 (1995).
38. Landau, M. et al. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33, W299-W302 (2005).
39. Li, T., Robert, E. I., van Breugel, P. C., Strubin, M. & Zheng, N. A promiscuous a-helical motif anchors viral hijackers and substrate receptors to the CUL4-DDB1 ubiquitin ligase machinery. Nature Struct. Mol. Biol. 17, 105-111 (2010).
40. Xu, G., Jiang, X. & Jaffrey, S. R. A mental retardation-linked nonsense mutation in cereblon isrescuedbyproteasome inhibition. J. Biol. Chem. 288, 29573-29585 (2013).
41. Zhang, L., Lubin, A., Chen, H., Sun, Z. & Gong, F. The deubiquitinating protein USP24 interacts with DDB2 and regulates DDB2 stability. Cell Cycle 11, 4378-4384 (2012).
42. Zhang, X. et al. Mutations in UVSSA cause UV-sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair. Nature Genet. 44, 593-597 (2012).
43. Forbes, S. A. S. et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 39, D945-D950 (2011).