HaloPROTACS: Use of Small Molecule PROTACs to Induce Degradation of HaloTag Fusion Proteins

ACS Chemical Biology

Volumn 10, Issue 8, 2015, Pages 1831-1837

  Buckley, Dennis L ^a,d   Raina, Kanak ^a   Darricarrere, Nicole ^a   Hines, John ^a   Gustafson, Jeffrey L ^a   Smith, Ian E ^c   Miah, Afjal H ^c   Harling, John D ^c   Crews, Craig M ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GLAXOSMITHKLINE   (United Kingdom)

^d DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMETHYL SULFOXIDE; EPOXOMICIN; HYBRID PROTEIN; LIGAND; UBIQUITIN PROTEIN LIGASE E3; MOLECULAR LIBRARY; PROTEIN BINDING; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CELL MEMBRANE PERMEABILITY; CHEMICAL GENETICS; COMPARATIVE STUDY; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HEK293 CELL LINE; HUMAN; HUMAN CELL; HYDROPHOBICITY; IMMUNOBLOTTING; MOLECULE; PRIORITY JOURNAL; PROTEIN DEGRADATION; CHEMISTRY; METABOLISM; MOLECULAR LIBRARY;

HEK293 CELLS; HUMANS; LIGANDS; PROTEIN BINDING; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; SMALL MOLECULE LIBRARIES; UBIQUITIN-PROTEIN LIGASES;

EID: 84939794726     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00442     Document Type: Article

References (39)

1. 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
2. Sakamoto, K. M. (2010) Protacs for treatment of cancer Pediatr. Res. 67, 505-508
3. Banaszynski, L. A. and Wandless, T. J. (2006) Conditional control of protein function Chem. Biol. 13, 11-21
4. Sakamoto, K., Kim, K.-B., Kumagai, A., Mercurio, F., Crews, C. M., and Deshaies, R. J. (2001) Protacs: chimeric molecules that target proteins to the Skp1-Cullin-F box complex for ubiquitination and degradation Proc. Natl. Acad. Sci. U.S.A. 98, 8554-8559
5. Schneekloth, J. S., Jr., Fonseca, F. N., Koldobskiy, M., Mandal, A. K., Deshaies, R. J., Sakamoto, K., and Crews, C. M. (2004) Chemical genetic control of protein levels: selective in vivo targeted degradation J. Am. Chem. Soc. 126, 3748-3754
6. Sakamoto, K., Kim, K.-B., Verma, R., Ransick, A., Stein, B., Crews, C. M., and Deshaies, R. J. (2003) Development of Protacs to target cancer-promoting proteins for ubiquitination and degradation Mol. Cell. Proteomics 2, 1350
7. Lee, H., Puppala, D., Choi, E.-Y., Swanson, H., and Kim, K.-B. (2007) Targeted Degradation of the Aryl Hydrocarbon Receptor by the PROTAC Approach: A Useful Chemical Genetic Tool ChemBioChem. 8, 2058-2062
8. Rodriguez-Gonzalez, A., Cyrus, K., Salcius, M., Kim, K.-B., Crews, C. M., Deshaies, R. J., and Sakamoto, K. M. (2008) Targeting steroid hormone receptors for ubiquitination and degradation in breast and prostate cancer Oncogene 27, 7201-7211
9. Cyrus, K., Wehenkel, M., Choi, E.-Y., Swanson, H., and Kim, K.-B. (2010) Two-Headed PROTAC: An Effective New Tool for Targeted Protein Degradation ChemBioChem. 11, 1531-1534
10. Cyrus, K., Wehenkel, M., Choi, E.-Y., Han, H.-J., Lee, H., Swanson, H., and Kim, K.-B. (2011) Impact of linker length on the activity of PROTACs Mol. BioSyst. 7, 359-364
11. Hines, J., Gough, J. D., Corson, T. W., and Crews, C. M. (2013) Posttranslational protein knockdown coupled to receptor tyrosine kinase activation with phosphoPROTACs Proc. Natl. Acad. Sci. U.S.A. 110, 8942-8947
12. Vassilev, L. T., Vu, B. T., Graves, B., Carvajal, D., Podlaski, F., Filipovic, Z., Kong, N., Kammlott, U., Lukacs, C., Klein, C., Fotouhi, N., and Liu, E. A. (2004) In vivo activation of the p53 pathway by small-molecule antagonists of MDM2 Science 303, 844-848
13. Schneekloth, A. R., Pucheault, M., Tae, H. S., and Crews, C. M. (2008) Targeted intracellular protein degradation induced by a small molecule: En route to chemical proteomics Bioorg. Med. Chem. Lett. 18, 5904-5908
14. Itoh, Y., Ishikawa, M., Kitaguchi, R., Okuhira, K., Naito, M., and Hashimoto, Y. (2012) Double protein knockdown of cIAP1 and CRABP-II using a hybrid molecule consisting of ATRA and IAPs antagonist Bioorg. Med. Chem. Lett. 22, 4453-4457
15. Itoh, Y., Ishikawa, M., Kitaguchi, R., Sato, S., Naito, M., and Hashimoto, Y. (2011) Development of target protein-selective degradation inducer for protein knockdown Bioorg. Med. Chem. 19, 3229-3241
16. 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
17. Okuhira, K., Ohoka, N., Sai, K., Nishimaki-Mogami, T., Itoh, Y., Ishikawa, M., Hashimoto, Y., and Naito, M. (2011) Specific degradation of CRABP-II via cIAP1-mediated ubiquitylation induced by hybrid molecules that crosslink cIAP1 and the target protein FEBS Lett. 585, 1147-1152
18. Umezawa, H., Aoyagi, T., Suda, H., Hamada, M., and Takeuchi, T. (1976) Bestatin, an inhibitor of aminopeptidase B, produced by actinomycetes J. Antibiot. 29, 97-99
19. Fulda, S. and Vucic, D. (2012) Targeting IAP proteins for therapeutic intervention in cancer Nat. Rev. Drug Discovery 11, 109-124
20. Varfolomeev, E., Blankenship, J. W., Wayson, S. M., Fedorova, A. V., Kayagaki, N., Garg, P., Zobel, K., Dynek, J. N., Elliott, L. O., Wallweber, H. J. A., Flygare, J. A., Fairbrother, W. J., Deshayes, K., Dixit, V. M., and Vucic, D. (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis Cell 131, 669-681
21. Buckley, D. L., Gustafson, J. L., Van Molle, I., Roth, A. G., Tae, H. S., Gareiss, P. C., Jorgensen, W. L., Ciulli, A., and Crews, C. M. (2012) Small-molecule inhibitors of the interaction between the E3 ligase VHL and HIF1α Angew. Chem., Int. Ed. 51, 11463-11467
22. Buckley, D. L., Van Molle, I., Gareiss, P. C., Tae, H. S., Michel, J., Noblin, D. J., Jorgensen, W. L., Ciulli, A., and Crews, C. M. (2012) Targeting the von Hippel-Lindau E3 Ubiquitin Ligase Using Small Molecules To Disrupt the VHL/HIF-1α Interaction J. Am. Chem. Soc. 134, 4465-4468
23. Van Molle, I., Thomann, A., Buckley, D. L., So, E. C., Lang, S., Crews, C. M., and Ciulli, A. (2012) Dissecting Fragment-Based Lead Discovery at the von Hippel-Lindau Protein:Hypoxia Inducible Factor 1α Protein-Protein Interface Chem. Biol. 19, 1300-1312
24. Los, G. V., Encell, L. P., McDougall, M. G., Hartzell, D. D., Karassina, N., Zimprich, C., Wood, M. G., Learish, R., Ohana, R. F., Urh, M., Simpson, D., Mendez, J., Zimmerman, K., Otto, P., Vidugiris, G., Zhu, J., Darzins, A., Klaubert, D. H., Bulleit, R. F., and Wood, K. V. (2008) HaloTag: a novel protein labeling technology for cell imaging and protein analysis ACS Chem. Biol. 3, 373-382
25. 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
26. 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
27. Ohana, R. F., Encell, L. P., Zhao, K., Simpson, D., Slater, M. R., Urh, M., and Wood, K. V. (2009) HaloTag7: a genetically engineered tag that enhances bacterial expression of soluble proteins and improves protein purification Protein Expression Purif. 68, 110-120
28. Douglass, E. F., Miller, C. J., Sparer, G., Shapiro, H., and Spiegel, D. A. (2013) A comprehensive mathematical model for three-body binding Am. Chem. Soc. 135, 6092-6099
29. Meng, L., Mohan, R., Kwok, B. H., Elofsson, M., Sin, N., and Crews, C. M. (1999) Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity Proc. Natl. Acad. Sci. U.S.A. 96, 10403-10408
30. Sin, N., Kim, K.-B., Elofsson, M., Meng, L., Auth, H., Kwok, B. H., and Crews, C. M. (1999) Total synthesis of the potent proteasome inhibitor epoxomicin: a useful tool for understanding proteasome biology Bioorg. Med. Chem. Lett. 9, 2283-2288
31. Banaszynski, L. A., Chen, L.-C., Maynard-Smith, L. A., Ooi, A. G. L., and Wandless, T. J. (2006) A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules Cell 126, 995-1004
32. Banaszynski, L. A., Sellmyer, M. A., Contag, C. H., Wandless, T. J., and Thorne, S. H. (2008) Chemical control of protein stability and function in living mice Nature Med. 14, 1123-1127
33. Lau, H. D., Yaegashi, J., Zaro, B. W., and Pratt, M. R. (2010) Precise control of protein concentration in living cells Angew. Chem., Int. Ed. 49, 8458-8461
34. Shoulders, M. D., Ryno, L. M., Cooley, C. B., and Wiseman, R. L. (2013) Broadly Applicable Methodology for the Rapid and Dosable Small Molecule-Mediated Regulation of Transcription Factors in Human Cells J. Am. Chem. Soc. 135, 8129-8132
35. Shoulders, M. D., Ryno, L. M., Genereux, J. C., Moresco, J. J., Tu, P. G., Wu, C., Yates, J. R., Su, A. I., Kelly, J. W., and Wiseman, R. L. (2013) Stress-Independent Activation of XBP1s and/or ATF6 Reveals Three Functionally Diverse ER Proteostasis Environments Cell Reports 3, 1279-1292
36. Bonger, K. M., Chen, L.-C., Liu, C. W., and Wandless, T. J. (2011) Small-molecule displacement of a cryptic degron causes conditional protein degradation Nat. Chem. Biol. 7, 531-537
37. HaloTag Technology, Expression-ready ORF cDNA Clone Collection|GeneCopeia. http://www.genecopoeia.com/tech/halo-tag/.
38. Santarpia, L., Lippman, S. M., and El-Naggar, A. K. (2012) Targeting the MAPK-RAS-RAF signaling pathway in cancer therapy Expert Opin. Ther. Targets 16, 103-119
39. Downward, J. (2003) Targeting RAS signalling pathways in cancer therapy Nat. Rev. Cancer 3, 11-22