The MLLE domain of the ubiquitin ligase UBR5 binds to its catalytic domain to regulate substrate binding

Journal of Biological Chemistry

Volumn 290, Issue 37, 2015, Pages 22841-22850

  Muńoz Escobar, Juliana ^a   Matta Camacho, Edna ^a,b   Kozlov, Guennadi ^a   Gehring, Kalle ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CRYSTAL STRUCTURE; ENZYMES; PEPTIDES; SUBSTRATES;

BINDING PROPERTIES; DNA DAMAGE RESPONSE; E3 UBIQUITIN LIGASES; IONIC INTERACTION; SUBSTRATE BINDING; SUBSTRATE RECOGNITION; TRANSLATION REGULATION; UBIQUITIN LIGASES;

PROTEINS;

CELL PROTEIN; DNA; PABP INTERACTING MOTIF 2 PROTEIN; PABP INTERACTING PROTEIN 1; PROTEIN GW182; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE E3 UBR5; UNCLASSIFIED DRUG; INITIATION FACTOR; PAIP1 PROTEIN, HUMAN; PEPTIDE; PROTEIN BINDING; RNA BINDING PROTEIN; UBIQUITIN PROTEIN LIGASE; UBR5 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BIOCATALYSIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DAMAGE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GLUCONEOGENESIS; HECT DOMAIN; HUMAN; HUMAN CELL; HYDROPHOBICITY; MLLE DOMAIN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; TRANSLATION REGULATION; UBIQUITINATION; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; RAT; X RAY CRYSTALLOGRAPHY;

AMINO ACID MOTIFS; ANIMALS; CRYSTALLOGRAPHY, X-RAY; HUMANS; PEPTIDE INITIATION FACTORS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RATS; RNA-BINDING PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84941584669     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.672246     Document Type: Article

References (50)

1. Varshavsky, A. (2012) The ubiquitin system, an immense realm. Annu. Rev. Biochem. 81, 167-176
2. Pickart, C. M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533
3. Ciechanover, A., and Ben-Saadon, R. (2004) N-terminal ubiquitination: more protein substrates join in. Trends Cell Biol. 14, 103-106
4. Scheffner, M., and Kumar, S. (2014) Mammalian HECT ubiquitin-protein ligases: biological and pathophysiological aspects. Biochim. Biophys. Acta 1843, 61-74
5. Callaghan, M. J., Russell, A. J., Woollatt, E., Sutherland, G. R., Sutherland, R. L., and Watts, C. K. (1998) Identification of a human HECT family protein with homology to the Drosophila tumor suppressor gene hyperplastic discs. Oncogene 17, 3479-3491
6. Mansfield, E., Hersperger, E., Biggs, J., and Shearn, A. (1994) Genetic and molecular analysis of hyperplastic discs, a gene whose product is required for regulation of cell proliferation in Drosophila melanogaster imaginal discs and germ cells. Dev. Biol. 165, 507-526
7. Cojocaru, M., Bouchard, A., Cloutier, P., Cooper, J. J., Varzavand, K., Price, D. H., and Coulombe, B. (2011) Transcription factor IIS cooperates with the E3 ligase UBR5 to ubiquitinate the CDK9 subunit of the positive transcription elongation factor B. J. Biol. Chem. 286, 5012-5022
8. Hay-Koren, A., Caspi, M., Zilberberg, A., and Rosin-Arbesfeld, R. (2011) The EDD E3 ubiquitin ligase ubiquitinates and up-regulates β-catenin. Mol. Biol. Cell 22, 399-411
9. Honda, Y., Tojo, M., Matsuzaki, K., Anan, T., Matsumoto, M., Ando, M., Saya, H., and Nakao, M. (2002) Cooperation of HECT-domain ubiquitin ligase hHYD and DNA topoisomerase II-binding protein for DNA damage response. J. Biol. Chem. 277, 3599-3605
10. Jung, H. Y., Wang, X., Jun, S., and Park, J. I. (2013) Dyrk2-associated EDD-DDB1-VprBP E3 ligase inhibits telomerase by TERT degradation. J. Biol. Chem. 288, 7252-7262
11. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
12. Rutz, S., Kayagaki, N., Phung, Q. T., Eidenschenk, C., Noubade, R., Wang, X., Lesch, J., Lu, R., Newton, K., Huang, O. W., Cochran, A. G., Vasser, M., Fauber, B. P., DeVoss, J., Webster, J., et al. (2015) Deubiquitinase DUBA is a post-translational brake on interleukin-17 production in T cells. Nature 518, 417-421
13. Wang, X., Singh, S., Jung, H. Y., Yang, G., Jun, S., Sastry, K. J., and Park, J. I. (2013) HIV-1 Vpr protein inhibits telomerase activity via the EDD-DDB1-VPRBP E3 ligase complex. J. Biol. Chem. 288, 15474-15480
14. Yoshida, M., Yoshida, K., Kozlov, G., Lim, N. S., De Crescenzo, G., Pang, Z., Berlanga, J. J., Kahvejian, A., Gehring, K., Wing, S. S., and Sonenberg, N. (2006) Poly (A) binding protein (PABP) homeostasis is mediated by the stability of its inhibitor, Paip2. EMBO J. 25, 1934-1944
15. Zhang, T., Cronshaw, J., Kanu, N., Snijders, A. P., and Behrens, A. (2014) UBR5-mediated ubiquitination of ATMIN is required for ionizing radiationinduced ATM signaling and function. Proc. Natl. Acad. Sci. U. S. A. 111, 12091-12096
16. Bradley, A., Zheng, H., Ziebarth, A., Sakati, W., Branham-O'Connor, M., Blumer, J. B., Liu, Y., Kistner-Griffin, E., Rodriguez-Aguayo, C., Lopez-Berestein, G., Sood, A. K., Landen, C. N., Jr., and Eblen, S. T. (2014) EDD enhances cell survival and cisplatin resistance and is a therapeutic target for epithelial ovarian cancer. Carcinogenesis 35, 1100-1109
17. Fuja, T. J., Lin, F., Osann, K. E., and Bryant, P. J. (2004) Somatic mutations and altered expression of the candidate tumor suppressors CSNK1ε, DLG1, and EDD/hHYD in mammary ductal carcinoma. Cancer Res. 64, 942-951
18. Meissner, B., Kridel, R., Lim, R. S., Rogic, S., Tse, K., Scott, D. W., Moore, R., Mungall, A. J., Marra, M. A., Connors, J. M., Steidl, C., and Gascoyne, R. D. (2013) The E3 ubiquitin ligase UBR5 is recurrently mutated in mantle cell lymphoma. Blood 121, 3161-3164
19. Ohshima, R., Ohta, T., Wu, W., Koike, A., Iwatani, T., Henderson, M., Watts, C. K., and Otsubo, T. (2007) Putative tumor suppressor EDD interacts with and up-regulates APC. Genes Cells 12, 1339-1345
20. Henderson, M. J., Munoz, M. A., Saunders, D. N., Clancy, J. L., Russell, A. J., Williams, B., Pappin, D., Khanna, K. K., Jackson, S. P., Sutherland, R. L., and Watts, C. K. (2006) EDD mediates DNA damage-induced activation of CHK2. J. Biol. Chem. 281, 39990-40000
21. Ling, S., and Lin, W. C. (2011) EDD inhibits ATM-mediated phosphorylation of p53. J. Biol. Chem. 286, 14972-14982
22. Smits, V. A. (2012) EDD induces cell cycle arrest by increasing p53 levels. Cell Cycle 11, 715-720
23. Su, H., Meng, S., Lu, Y., Trombly, M. I., Chen, J., Lin, C., Turk, A., and Wang, X. (2011) Mammalian hyperplastic discs homolog EDD regulates miRNA-mediated gene silencing. Mol. Cell 43, 97-109
24. Kozlov, G., Nguyen, L., Lin, T., De Crescenzo, G., Park, M., and Gehring, K. (2007) Structural basis of ubiquitin recognition by the ubiquitin-associated (UBA) domain of the ubiquitin ligase EDD. J. Biol. Chem. 282, 35787-35795
25. Kozlov, G., Trempe, J. F., Khaleghpour, K., Kahvejian, A., Ekiel, I., and Gehring, K. (2001) Structure and function of the C-terminal PABC domain of human poly (A)-binding protein. Proc. Natl. Acad. Sci. U. S. A. 98, 4409-4413
26. Matta-Camacho, E., Kozlov, G., Menade, M., and Gehring, K. (2012) Structure of the HECT C-lobe of the UBR5 E3 ubiquitin ligase. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68, 1158-1163
27. Deo, R. C., Sonenberg, N., and Burley, S. K. (2001) X-ray structure of the human hyperplastic discs protein: an ortholog of the C-terminal domain of poly (A)-binding protein. Proc. Natl. Acad. Sci. U. S. A. 98, 4414-4419
28. Xie, J., Kozlov, G., and Gehring, K. (2014) The "tale" of poly (A) binding protein: the MLLE domain and PAM2-containing proteins. Biochim. Biophys. Acta 1839, 1062-1068
29. Albrecht, M., and Lengauer, T. (2004) Survey on the PABC recognition motif PAM2. Biochem. Biophys. Res. Commun. 316, 129-138
30. Kozlov, G., De Crescenzo, G., Lim, N. S., Siddiqui, N., Fantus, D., Kahvejian, A., Trempe, J. F., Elias, D., Ekiel, I., Sonenberg, N., O'Connor-McCourt, M., and Gehring, K. (2004) Structural basis of ligand recognition by PABC, a highly specific peptide-binding domain found in poly (A)-binding protein and a HECT ubiquitin ligase. EMBO J. 23, 272-281
31. Kozlov, G., Ménade, M., Rosenauer, A., Nguyen, L., and Gehring, K. (2010) Molecular determinants of PAM2 recognition by the MLLE domain of poly (A)-binding protein. J. Mol. Biol. 397, 397-407
32. Lim, N. S., Kozlov, G., Chang, T. C., Groover, O., Siddiqui, N., Volpon, L., De Crescenzo, G., Shyu, A. B., and Gehring, K. (2006) Comparative peptide binding studies of the PABC domains from the ubiquitin-protein isopeptide ligaseHYDand poly (A)-binding protein. Implications forHYD function. J. Biol. Chem. 281, 14376-14382
33. Kozlov, G., Safaee, N., Rosenauer, A., and Gehring, K. (2010) Structural basis of binding of P-body-associated proteins GW182 and ataxin-2 by the Mlle domain of poly (A)-binding protein. J. Biol. Chem. 285, 13599-13606
34. Jinek, M., Fabian, M. R., Coyle, S. M., Sonenberg, N., and Doudna, J. A. (2010) Structural insights into the human GW182-PABC interaction in microRNA-mediated deadenylation. Nat. Struct. Mol. Biol. 17, 238-240
35. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
36. McRee, D. E. (1999) XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125, 156-165
37. Murshudov, G. N., Vagin, A. A., Lebedev, A., Wilson, K. S., and Dodson, E. J. (1999) Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D Biol. Crystallogr. 55, 247-255
38. Winn, M. D., Murshudov, G. N., and Papiz, M. Z. (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 374, 300-321
39. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
40. Vriend, G. (1990) WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8, 52-56
41. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol. NMR 6, 277-293
42. Bartels, C., Xia, T. H., Billeter, M., Güntert, P., and Wüthrich, K. (1995) The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR 6, 1-10
43. Gallagher, E., Gao, M., Liu, Y. C., and Karin, M. (2006) Activation of the E3 ubiquitin ligase Itch through a phosphorylation-induced conformational change. Proc. Natl. Acad. Sci. U. S. A. 103, 1717-1722
44. Mari, S., Ruetalo, N., Maspero, E., Stoffregen, M. C., Pasqualato, S., Polo, S., and Wiesner, S. (2014) Structural and functional framework for the autoinhibition of Nedd4-family ubiquitin ligases. Structure 22, 1639-1649
45. Wiesner, S., Ogunjimi, A. A., Wang, H. R., Rotin, D., Sicheri, F., Wrana, J. L., and Forman-Kay, J. D. (2007) Autoinhibition of the HECT-type ubiquitin ligase Smurf2 through its C2 domain. Cell 130, 651-662
46. Ichimura, T., Yamamura, H., Sasamoto, K., Tominaga, Y., Taoka, M., Kakiuchi, K., Shinkawa, T., Takahashi, N., Shimada, S., and Isobe, T. (2005) 14-3-3 proteins modulate the expression of epithelial Na+ channels by phosphorylation-dependent interaction with Nedd4-2 ubiquitin ligase. J. Biol. Chem. 280, 13187-13194
47. Shea, F. F., Rowell, J. L., Li, Y., Chang, T. H., and Alvarez, C. E. (2012) Mammalian α-arrestins link activated seven transmembrane receptors to Nedd4 family E3 ubiquitin ligases and interact with β-arrestins. PLoS ONE 7, e50557
48. Shearwin-Whyatt, L., Dalton, H. E., Foot, N., and Kumar, S. (2006) Regulation of functional diversity within the Nedd4 family by accessory and adaptor proteins. Bioessays 28, 617-628
49. Pandya, R. K., Partridge, J. R., Love, K. R., Schwartz, T. U., and Ploegh, H. L. (2010) Astructural element within the HUWE1HECT domain modulates self-ubiquitination and substrate ubiquitination activities. J. Biol. Chem. 285, 5664-5673
50. Bethard, J. R., Zheng, H., Roberts, L., and Eblen, S. T. (2011) Identification of phosphorylation sites on the E3 ubiquitin ligase UBR5/EDD. J. Proteomics 75, 603-609