Molecular Understanding of USP7 Substrate Recognition and C-Terminal Activation

Structure

Volumn 24, Issue 8, 2016, Pages 1335-1345

  Rougé, Lionel ^a   Bainbridge, Travis W ^a   Kwok, Michael ^a   Tong, Raymond ^a,b   Di Lello, Paola ^a   Wertz, Ingrid E ^a   Maurer, Till ^a   Ernst, James A ^a   Murray, Jeremy ^a  

^a GENENTECH INC   (United States)

^b Denali Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; DEUBIQUITINASE; PEPTIDE; UBIQUITIN; UBIQUITIN SPECIFIC PROTEASE 7; UNCLASSIFIED DRUG; PROTEIN BINDING; RECOMBINANT PROTEIN; UBIQUITIN THIOLESTERASE; USP7 PROTEIN, HUMAN;

ARTICLE; BIOCHEMICAL ANALYSIS; BIOPHYSICS; CATALYSIS; CONFORMATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN BINDING; ALPHA HELIX; AMINO ACID SEQUENCE; BETA SHEET; CHEMISTRY; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; KINETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; KINETICS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; THERMODYNAMICS; UBIQUITIN; UBIQUITIN THIOLESTERASE;

EID: 84980009798     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2016.05.020     Document Type: Article

References (48)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.-W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 213–221.
2. Bartenschlager, R., Ahlborn-Laake, L., Mous, J., Jacobsen, H., Kinetic and structural analyses of hepatitis C virus polyprotein processing. J. Virol. 68 (1994), 5045–5055.
3. Bartenschlager, R., Lohmann, V., Wilkinson, T., Koch, J.O., Complex formation between the NS3 serine-type proteinase of the hepatitis C virus and NS4A and its importance for polyprotein maturation. J. Virol. 69 (1995), 7519–7528.
4. Bax, A., Ikura, M., Kay, L.E., Torchia, D.A., Comparison of different modes of two-dimensional reverse-correlation NMR for the study of proteins. J. Magn. 86 (1990), 304–318.
5. Borodovsky, A., Ovaa, H., Kolli, N., Gan-Erdene, T., Wilkinson, K.D., Ploegh, H.L., Kessler, B.M., Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 9 (2002), 1149–1159.
6. Brooks, C.L., Gu, W., p53 ubiquitination: Mdm2 and beyond. Mol. Cell 21 (2006), 307–315.
7. Cavanagh, J., Rance, M., Sensitivity improvement in isotropic mixing (TOCSY) experiments. J. Magn. Reson. 88 (1990), 72–85.
8. Cheng, Q., Cross, B., Li, B., Chen, L., Li, Z., Chen, J., Regulation of MDM2 E3 ligase activity by phosphorylation after DNA damage. Mol. Cell. Biol. 31 (2011), 4951–4963.
9. Cheng, J., Yang, H., Fang, J., Ma, L., Gong, R., Wang, P., Li, Z., Xu, Y., Molecular mechanism for USP7-mediated DNMT1 stabilization by acetylation. Nat. Commun., 6, 2015, 7023.
10. Cummins, J.M., Rago, C., Kohli, M., Kinzler, K.W., Lengauer, C., Vogelstein, B., Tumour suppression: disruption of HAUSP gene stabilizes p53. Nature, 428, 2004, 10.1038/nature02501.
11. Du, Z., Song, J., Wang, Y., Zhao, Y., Guda, K., Yang, S., Kao, H.-Y., Xu, Y., Willis, J., Markowitz, S.D., et al. DNMT1 stability is regulated by proteins coordinating deubiquitination and acetylation-driven ubiquitination. Sci. Signal., 3, 2010, ra80.
12. Emsley, P., Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 2126–2132.
13. Evans, P., Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62 (2006), 72–82.
14. Everett, R.D., Meredith, M., Orr, A., Cross, A., Kathoria, M., Parkinson, J., A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein. EMBO J. 16 (1997), 1519–1530.
15. Everett, R.D., Meredith, M., Orr, A., The ability of herpes simplex virus type 1 immediate-early protein Vmw110 to bind to a ubiquitin-specific protease contributes to its roles in the activation of gene expression and stimulation of virus replication. J. Virol. 73 (1999), 417–426.
16. Faesen, A.C., Dirac, A.M.G., Shanmugham, A., Ovaa, H., Perrakis, A., Sixma, T.K., Mechanism of USP7/HAUSP activation by its C-terminal ubiquitin-like domain and allosteric regulation by GMP-synthetase. Mol. Cell 44 (2011), 147–159.
17. Findeisen, M., Brand, T., Berger, S., A 1H-NMR thermometer suitable for cryoprobes. Magn. Reson. Chem. 45 (2007), 175–178.
18. Grzesiek, S., Bax, A., An efficient experiment for sequential backbone assignment of medium-sized isotopically enriched proteins. J. Magn. Reson. (1969) 99 (1992), 201–207.
19. Grzesiek, S., Bax, A., Amino acid type determination in the sequential assignment procedure of uniformly 13C/15N-enriched proteins. J. Biomol. NMR 3 (1993), 185–204.
20. Holowaty, M.N., Sheng, Y., Nguyen, T., Arrowsmith, C., Frappier, L., Protein interaction domains of the ubiquitin-specific protease, USP7/HAUSP. J. Biol. Chem. 278 (2003), 47753–47761.
21. Hu, M., Li, P., Li, M., Li, W., Yao, T., Wu, J.-W., Gu, W., Cohen, R.E., Shi, Y., Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 111 (2002), 1041–1054.
22. Hu, M., Gu, L., Li, M., Jeffrey, P.D., Gu, W., Shi, Y., Structural basis of competitive recognition of p53 and MDM2 by HAUSP/USP7: implications for the regulation of the p53-MDM2 pathway. PLos Biol., 4, 2006, e27.
23. Kabsch, W., Xds. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 125–132.
24. Kessler, B.M., Selective and reversible inhibitors of ubiquitin-specific protease 7: a patent evaluation (WO2013030218). Expert Opin. Ther. Pat. 24 (2014), 597–602.
25. Komander, D., Clague, M.J., Urbé, S., Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10 (2009), 550–563.
26. Laue, E.D., Mayger, M.R., Skilling, J., Staunton, J., Reconstruction of phase-sensitive two-dimensional NMR spectra by maximum entropy. J. Magn. Reson. 68 (1986), 14–29.
27. Li, M., Brooks, C.L., Kon, N., Gu, W., A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol. Cell 13 (2004), 879–886.
28. Ma, J., Martin, J.D., Xue, Y., Lor, L.A., Kennedy-Wilson, K.M., Sinnamon, R.H., Ho, T.F., Zhang, G., Schwartz, B., Tummino, P.J., et al. C-terminal region of USP7/HAUSP is critical for deubiquitination activity and contains a second mdm2/p53 binding site. Arch. Biochem. Biophys. 503 (2010), 207–212.
29. Maertens, G.N., Messaoudi-Aubert El, S., Elderkin, S., Hiom, K., Peters, G., Ubiquitin-specific proteases 7 and 11 modulate Polycomb regulation of the INK4a tumour suppressor. EMBO J. 29 (2010), 2553–2565.
30. Marion, D., Wüthrich, K., Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of 1H-1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 113 (1983), 967–974.
31. McCoy, A.J., Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr. 63 (2007), 32–41.
32. Pfoh, R., Lacdao, I.K., Georges, A.A., Capar, A., Zheng, H., Frappier, L., Saridakis, V., Crystal structure of USP7 ubiquitin-like domains with an ICP0 peptide reveals a novel mechanism used by viral and cellular proteins to target USP7. PLoS Pathog., 11, 2015, e1004950.
33. Pufall, M.A., Graves, B.J., Autoinhibitory domains: modular effectors of cellular regulation. Annu. Rev. Cell Dev. Biol. 18 (2002), 421–462.
34. Saridakis, V., Sheng, Y., Sarkari, F., Holowaty, M.N., Shire, K., Nguyen, T., Zhang, R.G., Liao, J., Lee, W., Edwards, A.M., et al. Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein-Barr nuclear antigen 1 implications for EBV-mediated immortalization. Mol. Cell 18 (2005), 25–36.
35. Sarkari, F., Sheng, Y., Frappier, L., USP7/HAUSP promotes the sequence-specific DNA binding activity of p53. PLoS One, 5, 2010, e13040.
36. Schleucher, J., Sattler, M., Coherence selection by gradients without signal attenuation: application to the three-dimensional HNCO experiment. Angew. Chem. 32 (1993), 1489–1491.
37. Sheng, Y., Saridakis, V., Sarkari, F., Duan, S., Wu, T., Arrowsmith, C.H., Frappier, L., Molecular recognition of p53 and MDM2 by USP7/HAUSP. Nat. Struct. Mol. Biol. 13 (2006), 285–291.
38. Song, M.S., Salmena, L., Carracedo, A., Egia, A., Lo-Coco, F., Teruya-Feldstein, J., Pandolfi, P.P., The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network. Nature 455 (2008), 813–817.
39. Sowa, M.E., Bennett, E.J., Gygi, S.P., Harper, J.W., Defining the human deubiquitinating enzyme interaction landscape. Cell 138 (2009), 389–403.
40. Stonehouse, J., Clowes, R.T., Shaw, G.L., Keeler, J., Laue, E.D., Minimisation of sensitivity losses due to the use of gradient pulses in triple-resonance NMR of proteins. J. Biomol. NMR 5 (1995), 226–232.
41. van der Horst, A., de Vries-Smits, A.M.M., Brenkman, A.B., van Triest, M.H., van den Broek, N., Colland, F., Maurice, M.M., Burgering, B.M.T., FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat. Cell Biol. 8 (2006), 1064–1073.
42. Vranken, W.F., Boucher, W., Stevens, T.J., Fogh, R.H., Pajon, A., Llinas, M., Ulrich, E.L., Markley, J.L., Ionides, J., Laue, E.D., The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59 (2005), 687–696.
43. Wilkinson, K.D., Gan-Erdene, T., Kolli, N., Derivitization of the C-terminus of ubiquitin and ubiquitin-like proteins using intein chemistry: methods and uses. Methods Enzymol. 399 (2005), 37–51.
44. Wishart, D.S., Bigam, C.G., Yao, J., Abildgaard, F., Dyson, H.J., Oldfield, E., Markley, J.L., Sykes, B.D., 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 6 (1995), 135–140.
45. Ye, Y., Scheel, H., Hofmann, K., Komander, D., Dissection of USP catalytic domains reveals five common insertion points. Mol. Biosyst. 5 (2009), 1797–1808.
46. Zapata, J.M., Martínez-García, V., Lefebvre, S., Phylogeny of the TRAF/MATH domain. Adv. Exp. Med. Biol. 597 (2007), 1–24.
47. Zhang, Z.-M., Rothbart, S.B., Allison, D.F., Cai, Q., Harrison, J.S., Li, L., Wang, Y., Strahl, B.D., Wang, G.G., Song, J., An allosteric interaction links USP7 to deubiquitination and chromatin targeting of UHRF1. Cell Rep. 12 (2015), 1400–1406.
48. Zhu, X., Ménard, R., Sulea, T., High incidence of ubiquitin-like domains in human ubiquitin-specific proteases. Proteins 69 (2007), 1–7.