Covalent Ligand Screening Uncovers a RNF4 E3 Ligase Recruiter for Targeted Protein Degradation Applications

Targeted protein degradation has arisen as a powerful strategy for drug discovery allowing the targeting of undruggable proteins for proteasomal degradation. This approach most often employs heterobifunctional degraders consisting of a protein-targeting ligand linked to an E3 ligase recruiter to ubiquitinate and mark proteins of interest for proteasomal degradation. One challenge with this approach, however, is that only a few E3 ligase recruiters currently exist for targeted protein degradation applications, despite the hundreds of known E3 ligases in the human genome. Here, we utilized activity-based protein profiling (ABPP)-based covalent ligand screening approaches to identify cysteine-reactive small-molecules that react with the E3 ubiquitin ligase RNF4 and provide chemical starting points for the design of RNF4-based degraders. The hit covalent ligand from this screen reacted with either of two zinc-coordinating cysteines in the RING domain, C132 and C135, with no effect on RNF4 activity. We further optimized the potency of this hit and incorporated this potential RNF4 recruiter into a bifunctional degrader linked to JQ1, an inhibitor of the BET family of bromodomain proteins. We demonstrate that the resulting compound CCW 28-3 is capable of degrading BRD4 in a proteasome- and RNF4-dependent manner. In this study, we have shown the feasibility of using chemoproteomics-enabled covalent ligand screening platforms to expand the scope of E3 ligase recruiters that can be exploited for targeted protein degradation applications.

[1]  Keriann M. Backus Applications of Reactive Cysteine Profiling. , 2019, Current topics in microbiology and immunology.

[2]  John A. Tallarico,et al.  Harnessing the Anti-Cancer Natural Product Nimbolide for Targeted Protein Degradation , 2018, bioRxiv.

[3]  B. Cravatt,et al.  Electrophilic PROTACs that degrade nuclear proteins by engaging DCAF16 , 2018, bioRxiv.

[4]  D. Nomura,et al.  Chemoproteomics-Enabled Covalent Ligand Screening Reveals ALDH3A1 as a Lung Cancer Therapy Target. , 2018, ACS chemical biology.

[5]  P. Grandi,et al.  Multiplexed Proteome Dynamics Profiling Reveals Mechanisms Controlling Protein Homeostasis , 2018, Cell.

[6]  James E. Bradner,et al.  Plasticity in binding confers selectivity in ligand induced protein degradation , 2018, Nature Chemical Biology.

[7]  M. Rapé,et al.  Ubiquitylation at the crossroads of development and disease , 2017, Nature Reviews Molecular Cell Biology.

[8]  D. Nomura,et al.  Covalent Ligand Discovery against Druggable Hotspots Targeted by Anti-cancer Natural Products. , 2017, Cell chemical biology.

[9]  J. Olzmann,et al.  Chemoproteomics-Enabled Covalent Ligand Screening Reveals a Thioredoxin-Caspase 3 Interaction Disruptor That Impairs Breast Cancer Pathogenicity. , 2017, ACS chemical biology.

[10]  C. Crews,et al.  Small-Molecule Modulation of Protein Homeostasis. , 2017, Chemical reviews.

[11]  Stefano Forli,et al.  Global profiling of lysine reactivity and ligandability in the human proteome. , 2017, Nature chemistry.

[12]  C. Skibola,et al.  Chemoproteomics-enabled covalent ligand screen reveals a cysteine hotspot in reticulon 4 that impairs ER morphology and cancer pathogenicity. , 2017, Chemical communications.

[13]  S. Bilodeau,et al.  A CK2–RNF4 interplay coordinates non-canonical SUMOylation and degradation of nuclear receptor FXR , 2017, Journal of molecular cell biology.

[14]  C. Skibola,et al.  Chemoproteomic Screening of Covalent Ligands Reveals UBA5 As a Novel Pancreatic Cancer Target. , 2017, ACS chemical biology.

[15]  D. Lamont,et al.  Structural basis of PROTAC cooperative recognition for selective protein degradation , 2017, Nature chemical biology.

[16]  Craig M. Crews,et al.  Induced protein degradation: an emerging drug discovery paradigm , 2016, Nature Reviews Drug Discovery.

[17]  J. Staudinger,et al.  The Molecular Interface Between the SUMO and Ubiquitin Systems. , 2017, Advances in experimental medicine and biology.

[18]  M. Schirle,et al.  A Photoaffinity Labeling-Based Chemoproteomics Strategy for Unbiased Target Deconvolution of Small Molecule Drug Candidates. , 2017, Methods in molecular biology.

[19]  D. Nomura,et al.  GSTP1 Is a Driver of Triple-Negative Breast Cancer Cell Metabolism and Pathogenicity. , 2016, Cell chemical biology.

[20]  A. Olson,et al.  Proteome-wide covalent ligand discovery in native biological systems , 2016, Nature.

[21]  J. McCarter,et al.  Systematic Study of the Glutathione (GSH) Reactivity of N-Arylacrylamides: 1. Effects of Aryl Substitution. , 2015, Journal of medicinal chemistry.

[22]  John D. Venable,et al.  ProLuCID: An improved SEQUEST-like algorithm with enhanced sensitivity and specificity. , 2015, Journal of proteomics.

[23]  K. Fisher,et al.  Mapping Proteome-Wide Targets of Environmental Chemicals Using Reactivity-Based Chemoproteomic Platforms. , 2015, Chemistry & biology.

[24]  Hai-qing Tu,et al.  RNF4 negatively regulates NF‐κB signaling by down‐regulating TAB2 , 2015, FEBS letters.

[25]  James E. Bradner,et al.  Phthalimide conjugation as a strategy for in vivo target protein degradation , 2015, Science.

[26]  A. Ciulli,et al.  Selective Small Molecule Induced Degradation of the BET Bromodomain Protein BRD4 , 2015, ACS chemical biology.

[27]  J. Balzarini,et al.  Novel 5-Arylcarbamoyl-2-methylisoxazolidin-3-yl-3-phosphonates as Nucleotide Analogues , 2014, Nucleosides, nucleotides & nucleic acids.

[28]  Kai Zhu,et al.  Docking Covalent Inhibitors: A Parameter Free Approach To Pose Prediction and Scoring , 2014, J. Chem. Inf. Model..

[29]  D. Fera,et al.  Identification and Characterization of Small Molecule Human Papillomavirus E6 Inhibitors , 2014, ACS chemical biology.

[30]  J. Tainer,et al.  RNF4 interacts with both SUMO and nucleosomes to promote the DNA damage response , 2014, EMBO reports.

[31]  Benjamin F. Cravatt,et al.  A chemoproteomic platform to quantitatively map targets of lipid-derived electrophiles , 2013, Nature Methods.

[32]  R. Dohmen,et al.  SUMO-targeted ubiquitin ligases. , 2014, Biochimica et biophysica acta.

[33]  J. Tainer,et al.  RNF 4 interacts with both SUMO and nucleosomes to promote the DNA damage response , 2014 .

[34]  D. Fera,et al.  Identi fi cation and Characterization of Small Molecule Human Papillomavirus E 6 Inhibitors , 2014 .

[35]  O. J. Semmes,et al.  The Sumo-targeted ubiquitin ligase RNF4 regulates the localization and function of the HTLV-1 oncoprotein Tax. , 2012, Blood.

[36]  Ryan P. Dain,et al.  A study of fragmentation of protonated amides of some acylated amino acids by tandem mass spectrometry: observation of an unusual nitrilium ion. , 2011, Rapid communications in mass spectrometry : RCM.

[37]  William B. Smith,et al.  Selective inhibition of BET bromodomains , 2010, Nature.

[38]  David Baker,et al.  Quantitative reactivity profiling predicts functional cysteines in proteomes , 2010, Nature.

[39]  C. Crews,et al.  Targeted intracellular protein degradation induced by a small molecule: En route to chemical proteomics. , 2008, Bioorganic & medicinal chemistry letters.

[40]  M. Oikawa,et al.  Synthesis and domino metathesis of functionalized 7-oxanorbornene analogs toward cis-fused heterocycles , 2008 .

[41]  M. Kerr,et al.  Total synthesis of (+/-)-mersicarpine. , 2008, Organic letters.

[42]  J. Huddleston,et al.  Synthesis and preliminary evaluation of novel analogues of quindolines as potential stabilisers of telomeric G-quadruplex DNA , 2007 .

[43]  William Stafford Noble,et al.  Semi-supervised learning for peptide identification from shotgun proteomics datasets , 2007, Nature Methods.

[44]  John R Yates,et al.  Carcinoma and stromal enzyme activity profiles associated with breast tumor growth in vivo. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[45]  L. Vassilev,et al.  In Vivo Activation of the p53 Pathway by Small-Molecule Antagonists of MDM2 , 2004, Science.

[46]  J. Falck,et al.  A one-pot synthesis of pyrido[2,3-b][1,4]oxazin-2-ones. , 2003, The Journal of organic chemistry.

[47]  V. Timokhin,et al.  Rate constants for the beta-elimination of tosyl radical from a variety of substituted carbon-centered radicals. , 2003, The Journal of organic chemistry.

[48]  B. Cravatt,et al.  Activity-based protein profiling: the serine hydrolases. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[49]  P. K. Smith,et al.  Measurement of protein using bicinchoninic acid. , 1985, Analytical biochemistry.