Boc3Arg-Linked Ligands Induce Degradation by Localizing Target Proteins to the 20S Proteasome

ACS Chemical Biology

Volumn 11, Issue 12, 2016, Pages 3328-3337

  Shi, Yuntao ^a   Long, Marcus J C ^a   Rosenberg, Masha M ^a   Li, Shican ^a   Kobjack, Aimee ^a   Lessans, Philip ^a   Coffey, Rory T ^a   Hedstrom, Lizbeth ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CARBAMIC ACID; PROTEASOME; UBIQUITIN PROTEIN LIGASE; ATP DEPENDENT 26S PROTEASE; CARBAMIC ACID DERIVATIVE; LIGAND; T-BUTYLCARBAMATE;

ARTICLE; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TARGETING; UBIQUITINATION; ANALOGS AND DERIVATIVES; CHEMISTRY; DRUG DESIGN; DRUG EFFECTS; HELA CELL LINE; HUMAN; METABOLISM;

ARGININE; CARBAMATES; DRUG DESIGN; HELA CELLS; HUMANS; LIGANDS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS;

EID: 85006459403     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.6b00656     Document Type: Article

References (51)

1. Toure, M. and Crews, C. M. ( 2016 ) Small-Molecule PROTACS: New Approaches to Protein Degradation Angew. Chem., Int. Ed. 55, 1966-1973 10.1002/anie.201507978
2. Buckley, D. L. and Crews, C. M. ( 2014 ) Small-molecule control of intracellular protein levels through modulation of the ubiquitin proteasome system Angew. Chem., Int. Ed. 53, 2312-2330 10.1002/anie.201307761
3. Wittmann, B. M., Sherk, A., and McDonnell, D. P. ( 2007 ) Definition of functionally important mechanistic differences among selective estrogen receptor down-regulators Cancer Res. 67, 9549-9560 10.1158/0008-5472.CAN-07-1590
4. Bill, A., Hall, M. L., Borawski, J., Hodgson, C., Jenkins, J., Piechon, P., Popa, O., Rothwell, C., Tranter, P., Tria, S., Wagner, T., Whitehead, L., and Gaither, L. A. ( 2014 ) Small molecule-facilitated degradation of ANO1 protein: a new targeting approach for anticancer therapeutics J. Biol. Chem. 289, 11029-11041 10.1074/jbc.M114.549188
5. Citri, A., Alroy, I., Lavi, S., Rubin, C., Xu, W., Grammatikakis, N., Patterson, C., Neckers, L., Fry, D. W., and Yarden, Y. ( 2002 ) Drug-induced ubiquitylation and degradation of ErbB receptor tyrosine kinases: implications for cancer therapy EMBO J. 21, 2407-2417 10.1093/emboj/21.10.2407
6. Waller, A. S., Sharrard, R. M., Berthon, P., and Maitland, N. J. ( 2000 ) Androgen receptor localisation and turnover in human prostate epithelium treated with the antiandrogen, casodex J. Mol. Endocrinol. 24, 339-351 10.1677/jme.0.0240339
7. Peltonen, K., Colis, L., Liu, H., Trivedi, R., Moubarek, M. S., Moore, H. M., Bai, B., Rudek, M. A., Bieberich, C. J., and Laiho, M. ( 2014 ) A targeting modality for destruction of RNA polymerase I that possesses anticancer activity Cancer Cell 25, 77-90 10.1016/j.ccr.2013.12.009
8. Itoh, Y., Ishikawa, M., Naito, M., and Hashimoto, Y. ( 2010 ) Protein knockdown using methyl bestatin-ligand hybrid molecules: design and synthesis of inducers of ubiquitination-mediated degradation of cellular retinoic acid-binding proteins J. Am. Chem. Soc. 132, 5820-5826 10.1021/ja100691p
9. Lu, J., Qian, Y., Altieri, M., Dong, H., Wang, J., Raina, K., Hines, J., Winkler, J. D., Crew, A. P., Coleman, K., and Crews, C. M. ( 2015 ) Hijacking the E3 Ubiquitin Ligase Cereblon to Efficiently Target BRD4 Chem. Biol. 22, 755-763 10.1016/j.chembiol.2015.05.009
10. Winter, G. E., Buckley, D. L., Paulk, J., Roberts, J. M., Souza, A., Dhe-Paganon, S., and Bradner, J. E. ( 2015 ) DRUG DEVELOPMENT. Phthalimide conjugation as a strategy for in vivo target protein degradation Science 348, 1376-1381 10.1126/science.aab1433
11. Zengerle, M., Chan, K. H., and Ciulli, A. ( 2015 ) Selective Small Molecule Induced Degradation of the BET Bromodomain Protein BRD4 ACS Chem. Biol. 10, 1770-1777 10.1021/acschembio.5b00216
12. Neklesa, T. K., Noblin, D. J., Kuzin, A., Lew, S., Seetharaman, J., Acton, T. B., Kornhaber, G., Xiao, R., Montelione, G. T., Tong, L., and Crews, C. M. ( 2013 ) A bidirectional system for the dynamic small molecule control of intracellular fusion proteins ACS Chem. Biol. 8, 2293-2300 10.1021/cb400569k
13. Neklesa, T. K. and Crews, C. M. ( 2012 ) Chemical biology: Greasy tags for protein removal Nature 487, 308-309 10.1038/487308a
14. Tae, H. S., Sundberg, T. B., Neklesa, T. K., Noblin, D. J., Gustafson, J. L., Roth, A. G., Raina, K., and Crews, C. M. ( 2012 ) Identification of hydrophobic tags for the degradation of stabilized proteins ChemBioChem 13, 538-541 10.1002/cbic.201100793
15. Neklesa, T. K., Tae, H. S., Schneekloth, A. R., Stulberg, M. J., Corson, T. W., Sundberg, T. B., Raina, K., Holley, S. A., and Crews, C. M. ( 2011 ) Small-molecule hydrophobic tagging-induced degradation of HaloTag fusion proteins Nat. Chem. Biol. 7, 538-543 10.1038/nchembio.597
16. Xie, T., Lim, S. M., Westover, K. D., Dodge, M. E., Ercan, D., Ficarro, S. B., Udayakumar, D., Gurbani, D., Tae, H. S., Riddle, S. M., Sim, T., Marto, J. A., Janne, P. A., Crews, C. M., and Gray, N. S. ( 2014 ) Pharmacological targeting of the pseudokinase Her3 Nat. Chem. Biol. 10, 1006-1012 10.1038/nchembio.1658
17. Gustafson, J. L., Neklesa, T. K., Cox, C. S., Roth, A. G., Buckley, D. L., Tae, H. S., Sundberg, T. B., Stagg, D. B., Hines, J., McDonnell, D. P., Norris, J. D., and Crews, C. M. ( 2015 ) Small-Molecule-Mediated Degradation of the Androgen Receptor through Hydrophobic Tagging Angew. Chem., Int. Ed. 54, 9659-9662 10.1002/anie.201503720
18. Raina, K., Noblin, D. J., Serebrenik, Y. V., Adams, A., Zhao, C., and Crews, C. M. ( 2014 ) Targeted protein destabilization reveals an estrogen-mediated ER stress response Nat. Chem. Biol. 10, 957-962 10.1038/nchembio.1638
19. Long, M. J., Gollapalli, D. R., and Hedstrom, L. ( 2012 ) Inhibitor mediated protein degradation Chem. Biol. 19, 629-637 10.1016/j.chembiol.2012.04.008
20. Coffey, R. T., Shi, Y., Long, M. J., Marr, M. T., 2nd, and Hedstrom, L. ( 2016 ) Ubiquilin Mediated Small Molecule Inhibition of Mammalian Target of Rapamycin Complex 1 (mTORC1) Signaling J. Biol. Chem. 291, 5221-5233 10.1074/jbc.M115.691584
21. Callis, J. and Ling, R. ( 2005 ) Preparation, characterization, and use of tagged ubiquitins Methods Enzymol. 399, 51-64 10.1016/S0076-6879(05)99004-6
22. Kapuria, V., Peterson, L. F., Fang, D., Bornmann, W. G., Talpaz, M., and Donato, N. J. ( 2010 ) Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis Cancer Res. 70, 9265-9276 10.1158/0008-5472.CAN-10-1530
23. Schulman, B. A. and Harper, J. W. ( 2009 ) Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways Nat. Rev. Mol. Cell Biol. 10, 319-331 10.1038/nrm2673
24. Yang, Y., Kitagaki, J., Dai, R. M., Tsai, Y. C., Lorick, K. L., Ludwig, R. L., Pierre, S. A., Jensen, J. P., Davydov, I. V., Oberoi, P., Li, C. C., Kenten, J. H., Beutler, J. A., Vousden, K. H., and Weissman, A. M. ( 2007 ) Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics Cancer Res. 67, 9472-9481 10.1158/0008-5472.CAN-07-0568
25. Mi, L., Gan, N., Cheema, A., Dakshanamurthy, S., Wang, X., Yang, D. C., and Chung, F. L. ( 2009 ) Cancer preventive isothiocyanates induce selective degradation of cellular alpha-and beta-tubulins by proteasomes J. Biol. Chem. 284, 17039-17051 10.1074/jbc.M901789200
26. Kapuria, V., Peterson, L. F., Showalter, H. D., Kirchhoff, P. D., Talpaz, M., and Donato, N. J. ( 2011 ) Protein cross-linking as a novel mechanism of action of a ubiquitin-activating enzyme inhibitor with anti-tumor activity Biochem. Pharmacol. 82, 341-349 10.1016/j.bcp.2011.05.012
27. D’Arcy, P., Brnjic, S., Olofsson, M. H., Fryknas, M., Lindsten, K., De Cesare, M., Perego, P., Sadeghi, B., Hassan, M., Larsson, R., and Linder, S. ( 2011 ) Inhibition of proteasome deubiquitinating activity as a new cancer therapy Nat. Med. 17, 1636-1640 10.1038/nm.2536
28. Schnell, J. R., Dyson, H. J., and Wright, P. E. ( 2004 ) Structure, dynamics, and catalytic function of dihydrofolate reductase Annu. Rev. Biophys. Biomol. Struct. 33, 119-140 10.1146/annurev.biophys.33.110502.133613
29. Tey, L. H., Loveridge, E. J., Swanwick, R. S., Flitsch, S. L., and Allemann, R. K. ( 2010 ) Highly site-selective stability increases by glycosylation of dihydrofolate reductase FEBS J. 277, 2171-2179 10.1111/j.1742-4658.2010.07634.x
30. Ionescu, R. M., Smith, V. F., O’Neill, J. C., Jr., and Matthews, C. R. ( 2000 ) Multistate equilibrium unfolding of Escherichia coli dihydrofolate reductase: thermodynamic and spectroscopic description of the native, intermediate, and unfolded ensembles Biochemistry 39, 9540-9550 10.1021/bi000511y
31. Huang, L. and Chen, C. H. ( 2009 ) Proteasome regulators: activators and inhibitors Curr. Med. Chem. 16, 931-939 10.2174/092986709787581860
32. Kisselev, A. F., Kaganovich, D., and Goldberg, A. L. ( 2002 ) Binding of hydrophobic peptides to several non-catalytic sites promotes peptide hydrolysis by all active sites of 20 S proteasomes. Evidence for peptide-induced channel opening in the alpha-rings J. Biol. Chem. 277, 22260-22270 10.1074/jbc.M112360200
33. Chu-Ping, M., Slaughter, C. A., and DeMartino, G. N. ( 1992 ) Purification and characterization of a protein inhibitor of the 20S proteasome (macropain) Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1119, 303-311 10.1016/0167-4838(92)90218-3
34. Cascio, P. ( 2014 ) PA28alphabeta: the enigmatic magic ring of the proteasome? Biomolecules 4, 566-584 10.3390/biom4020566
35. Huang, L., Ho, P., and Chen, C. H. ( 2007 ) Activation and inhibition of the proteasome by betulinic acid and its derivatives FEBS Lett. 581, 4955-4959 10.1016/j.febslet.2007.09.031
36. Moravec, R. A., O’Brien, M. A., Daily, W. J., Scurria, M. A., Bernad, L., and Riss, T. L. ( 2009 ) Cell-based bioluminescent assays for all three proteasome activities in a homogeneous format Anal. Biochem. 387, 294-302 10.1016/j.ab.2009.01.016
37. Dantuma, N. P., Lindsten, K., Glas, R., Jellne, M., and Masucci, M. G. ( 2000 ) Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells Nat. Biotechnol. 18, 538-543 10.1038/75406
38. Lawson, A. P., Long, M. J., Coffey, R. T., Qian, Y., Weerapana, E., El Oualid, F., and Hedstrom, L. ( 2015 ) Naturally Occurring Isothiocyanates Exert Anticancer Effects by Inhibiting Deubiquitinating Enzymes Cancer Res. 75, 5130-5142 10.1158/0008-5472.CAN-15-1544
39. Liu, G., Rogers, J., Murphy, C. T., and Rongo, C. ( 2011 ) EGF signalling activates the ubiquitin proteasome system to modulate C. elegans lifespan EMBO J. 30, 2990-3003 10.1038/emboj.2011.195
40. Olivares, A. O., Baker, T. A., and Sauer, R. T. ( 2016 ) Mechanistic insights into bacterial AAA+ proteases and protein-remodelling machines Nat. Rev. Microbiol. 14, 33-44 10.1038/nrmicro.2015.4
41. Baugh, J. M., Viktorova, E. G., and Pilipenko, E. V. ( 2009 ) Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitination J. Mol. Biol. 386, 814-827 10.1016/j.jmb.2008.12.081
42. Pickering, A. M. and Davies, K. J. ( 2012 ) Degradation of damaged proteins: the main function of the 20S proteasome Prog. Mol. Biol. Transl Sci. 109, 227-248 10.1016/B978-0-12-397863-9.00006-7
43. Tummino, P. J. and Copeland, R. A. ( 2008 ) Residence time of receptor-ligand complexes and its effect on biological function Biochemistry 47, 5481-5492 10.1021/bi8002023
44. Morphy, R., Kay, C., and Rankovic, Z. ( 2004 ) From magic bullets to designed multiple ligands Drug Discovery Today 9, 641-651 10.1016/S1359-6446(04)03163-0
45. Janse, D. M., Crosas, B., Finley, D., and Church, G. M. ( 2004 ) Localization to the proteasome is sufficient for degradation J. Biol. Chem. 279, 21415-21420 10.1074/jbc.M402954200
46. Ben-Nissan, G. and Sharon, M. ( 2014 ) Regulating the 20S proteasome ubiquitin-independent degradation pathway Biomolecules 4, 862-884 10.3390/biom4030862
47. Tanahashi, N., Murakami, Y., Minami, Y., Shimbara, N., Hendil, K. B., and Tanaka, K. ( 2000 ) Hybrid proteasomes. Induction by interferon-gamma and contribution to ATP-dependent proteolysis J. Biol. Chem. 275, 14336-14345 10.1074/jbc.275.19.14336
48. Brooks, P., Fuertes, G., Murray, R. Z., Bose, S., Knecht, E., Rechsteiner, M. C., Hendil, K. B., Tanaka, K., Dyson, J., and Rivett, J. ( 2000 ) Subcellular localization of proteasomes and their regulatory complexes in mammalian cells Biochem. J. 346 ( Pt 1 ) 155-161 10.1042/0264-6021:3460155
49. Babbitt, S. E., Kiss, A., Deffenbaugh, A. E., Chang, Y. H., Bailly, E., Erdjument-Bromage, H., Tempst, P., Buranda, T., Sklar, L. A., Baumler, J., Gogol, E., and Skowyra, D. ( 2005 ) ATP hydrolysis-dependent disassembly of the 26S proteasome is part of the catalytic cycle Cell 121, 553-565 10.1016/j.cell.2005.03.028
50. Fabre, B., Lambour, T., Delobel, J., Amalric, F., Monsarrat, B., Burlet-Schiltz, O., and Bousquet-Dubouch, M. P. ( 2013 ) Subcellular distribution and dynamics of active proteasome complexes unraveled by a workflow combining in vivo complex cross-linking and quantitative proteomics Mol. Cell. Proteomics 12, 687-699 10.1074/mcp.M112.023317
51. Jariel-Encontre, I., Bossis, G., and Piechaczyk, M. ( 2008 ) Ubiquitin-independent degradation of proteins by the proteasome Biochim. Biophys. Acta, Rev. Cancer 1786, 153-177 10.1016/j.bbcan.2008.05.004