Professor Swen Hoelder

Head of Chemistry: Medicinal Chemistry 4 (including Analytical Chemistry)

OrcID: 0000-0001-8636-1488

Phone: +44 20 8722 4353

Email: [email protected]

Also on:  swen-hoelder-b2453b7

Location: Sutton

Dr Swen Holder

OrcID: 0000-0001-8636-1488

Phone: +44 20 8722 4353

Email: [email protected]

Also on:  swen-hoelder-b2453b7

Location: Sutton

Biography

Professor Swen Hoelder leads the Medicinal Chemistry 4 group within the Centre for Cancer Drug Discovery (CCDD), formerly known as Cancer Research UK Cancer Therapeutics Unit, at The Institute of Cancer Research, London. In 2020 he was awarded a professorship in Medicinal Chemistry and Drug Design and in 2022 he became the Head of Chemistry within the CCDD. 

Medicinal chemistry plays a crucial role towards the generation of a new drug. Drug candidates are identified through creative design, chemical synthesis and systematic testing of chemical compounds. These drug candidates are then progressed to clinical trials. 

Professor Hoelder and his group apply their medicinal chemistry skills to discover novel cancer drugs in collaboration with other research groups both within the ICR and externally. A recent example is the discovery of a series of pyrimidopyridine inhibitors for the cancer target MPS1 and the chemical optimization of this series to yield the clinical candidate BOS172722. BOS172722 is currently undergoing Phase 1 clinical development for triple negative breast cancer.

Professor Hoelder studied chemistry at the University of Muenster (Germany). He completed his PhD in organic chemistry at the Technical University in Berlin in the team of Professor S. Blechert. Following his PhD, Professor Hoelder spent two years in the lab of Professor P.G. Schultz at the University of California, Berkeley establishing methods to identify novel enzymes through selection from large protein libraries. His Post-Doctoral research was supported by a Feodor Lynen Fellowship from the Alexander von Humboldt Foundation.

Professor Hoelder then joined the department of Medicinal Chemistry at Hoechst Marion Roussel (now Sanofi), a major pharmaceutical company, where he predominately worked on diabetes therapies. In addition, he led teams that were responsible for the creation of a kinase screening library and explored the application of Bio-NMR for kinase drug discovery in collaboration with the group of Professor H. Schwalbe at Frankfurt UniversityIn 2005, he joined Altana (now Takeda) to work on cancer therapies, where he led a team of chemists that discovered two pre-clinical candidates.

In October 2007, Professor Hoelder joined the faculty of the ICR applying his medicinal chemistry experience to discover novel drugs in the unique and collaborative environment of the Centre for Cancer Drug Discovery (formerly known as Cancer Research UK Cancer Therapeutics Unit).

In 2017, he was awarded a readership in Medicinal Chemistry and Drug Design and in 2018 took up the role as a senior tutor at the ICR.

In 2020, Swen was awarded Professorship in Medicinal Chemistry and Drug Design and in 2022 he became the Head of Chemistry within the Centre for Cancer Drug Discovery.

Qualifications

PhD Organic Chemistry, Technical University Berlin.

German Chemistry Diploma, University of Muenster, Germany.

Awards, Prizes or Honours

VCI PhD fellowship, Fonds der chemischen Industrie, 1993.

Feodor Lynen fellowship, Alexander von Humboldt Foundation, 1996.

Readership in Medicinal Chemistry and Drug Design, ICR, 2017.

External Committees

Scientific advisory board (SAB), SAB member, EU-Openscreen, 2019.

Scientific Advisory Board (SAB), SAB member, Sixth Element Capital, 2016-2018.

Drug Design board, External examiner, UCL, 2014-2018.

Types of Publications

Journal articles

Vidler, L.R. Brown, N. Knapp, S. Hoelder, S (2012) Druggability analysis and structural classification of bromodomain acetyl-lysine binding sites.. Show Abstract full text

Bromodomains are readers of the epigenetic code that specifically bind acetyl-lysine containing recognition sites on proteins. Recently the BET family of bromodomains has been demonstrated to be druggable through the discovery of potent inhibitors, sparking an interest in protein-protein interaction inhibitors that directly target gene transcription. Here, we assess the druggability of diverse members of the bromodomain family using SiteMap and show that there are significant differences in predicted druggability. Furthermore, we trace these differences in druggability back to unique amino acid signatures in the bromodomain acetyl-lysine binding sites. These signatures were then used to generate a new classification of the bromodomain family, visualized as a classification tree. This represents the first analysis of this type for the bromodomain family and can prove useful in the discovery of inhibitors, particularly for anticipating screening hit rates, identifying inhibitors that can be explored for lead hopping approaches, and selecting proteins for selectivity screening.

Drouin, L. McGrath, S. Vidler, L.R. Chaikuad, A. Monteiro, O. Tallant, C. Philpott, M. Rogers, C. Fedorov, O. Liu, M. Akhtar, W. Hayes, A. Raynaud, F. Müller, S. Knapp, S. Hoelder, S (2015) Structure enabled design of BAZ2-ICR, a chemical probe targeting the bromodomains of BAZ2A and BAZ2B.. Show Abstract full text

The bromodomain containing proteins BAZ2A/B play essential roles in chromatin remodeling and regulation of noncoding RNAs. We present the structure based discovery of a potent, selective, and cell active inhibitor 13 (BAZ2-ICR) of the BAZ2A/B bromodomains through rapid optimization of a weakly potent starting point. A key feature of the presented inhibitors is an intramolecular aromatic stacking interaction that efficiently occupies the shallow bromodomain pockets. 13 represents an excellent chemical probe for functional studies of the BAZ2 bromodomains in vitro and in vivo.

Gurden, M.D. Westwood, I.M. Faisal, A. Naud, S. Cheung, K.-.M.J. McAndrew, C. Wood, A. Schmitt, J. Boxall, K. Mak, G. Workman, P. Burke, R. Hoelder, S. Blagg, J. Van Montfort, R.L.M. Linardopoulos, S (2015) Naturally Occurring Mutations in the MPS1 Gene Predispose Cells to Kinase Inhibitor Drug Resistance.. Show Abstract full text

Acquired resistance to therapy is perhaps the greatest challenge to effective clinical management of cancer. With several inhibitors of the mitotic checkpoint kinase MPS1 in preclinical development, we sought to investigate how resistance against these inhibitors may arise so that mitigation or bypass strategies could be addressed as early as possible. Toward this end, we modeled acquired resistance to the MPS1 inhibitors AZ3146, NMS-P715, and CCT251455, identifying five point mutations in the kinase domain of MPS1 that confer resistance against multiple inhibitors. Structural studies showed how the MPS1 mutants conferred resistance by causing steric hindrance to inhibitor binding. Notably, we show that these mutations occur in nontreated cancer cell lines and primary tumor specimens, and that they also preexist in normal lymphoblast and breast tissues. In a parallel piece of work, we also show that the EGFR p.T790M mutation, the most common mutation conferring resistance to the EGFR inhibitor gefitinib, also preexists in cancer cells and normal tissue. Our results therefore suggest that mutations conferring resistance to targeted therapy occur naturally in normal and malignant cells and these mutations do not arise as a result of the increased mutagenic plasticity of cancer cells.

Innocenti, P. Woodward, H.L. Solanki, S. Naud, S. Westwood, I.M. Cronin, N. Hayes, A. Roberts, J. Henley, A.T. Baker, R. Faisal, A. Mak, G.W.-.Y. Box, G. Valenti, M. De Haven Brandon, A. O'Fee, L. Saville, H. Schmitt, J. Matijssen, B. Burke, R. van Montfort, R.L.M. Raynaud, F.I. Eccles, S.A. Linardopoulos, S. Blagg, J. Hoelder, S (2016) Rapid Discovery of Pyrido[3,4-d]pyrimidine Inhibitors of Monopolar Spindle Kinase 1 (MPS1) Using a Structure-Based Hybridization Approach.. Show Abstract full text

Monopolar spindle 1 (MPS1) plays a central role in the transition of cells from metaphase to anaphase and is one of the main components of the spindle assembly checkpoint. Chromosomally unstable cancer cells rely heavily on MPS1 to cope with the stress arising from abnormal numbers of chromosomes and centrosomes and are thus more sensitive to MPS1 inhibition than normal cells. We report the discovery and optimization of a series of new pyrido[3,4-d]pyrimidine based inhibitors via a structure-based hybridization approach from our previously reported inhibitor CCT251455 and a modestly potent screening hit. Compounds in this novel series display excellent potency and selectivity for MPS1, which translates into biomarker modulation in an in vivo human tumor xenograft model.

McGrath, S. Tortorici, M. Drouin, L. Solanki, S. Vidler, L. Westwood, I. Gimeson, P. Van Montfort, R. Hoelder, S (2017) Structure-Enabled Discovery of a Stapled Peptide Inhibitor to Target the Oncogenic Transcriptional Repressor TLE1.. Show Abstract full text

TLE1 is an oncogenic transcriptional co-repressor that exerts its repressive effects through binding of transcription factors. Inhibition of this protein-protein interaction represents a putative cancer target, but no small-molecule inhibitors have been published for this challenging interface. Herein, the structure-enabled design and synthesis of a constrained peptide inhibitor of TLE1 is reported. The design features the introduction of a four-carbon-atom linker into the peptide epitope found in many TLE1 binding partners. A concise synthetic route to a proof-of-concept peptide, cycFWRPW, has been developed. Biophysical testing by isothermal titration calorimetry and thermal shift assays showed that, although the constrained peptide bound potently, it had an approximately five-fold higher K<sub>d</sub> than that of the unconstrained peptide. The co-crystal structure suggested that the reduced affinity was likely to be due to a small shift of one side chain, relative to the otherwise well-conserved conformation of the acyclic peptide. This work describes a constrained peptide inhibitor that may serve as the basis for improved inhibitors.

Hudson, L. Mui, J. Vázquez, S. Carvalho, D.M. Williams, E. Jones, C. Bullock, A.N. Hoelder, S (2018) Novel Quinazolinone Inhibitors of ALK2 Flip between Alternate Binding Modes: Structure-Activity Relationship, Structural Characterization, Kinase Profiling, and Cellular Proof of Concept.. Show Abstract full text

Structure-activity relationship and crystallographic data revealed that quinazolinone-containing fragments flip between two distinct modes of binding to activin receptor-like kinase-2 (ALK2). We explored both binding modes to discover potent inhibitors and characterized the chemical modifications that triggered the flip in binding mode. We report kinase selectivity and demonstrate that compounds of this series modulate ALK2 in cancer cells. These inhibitors are attractive starting points for the discovery of more advanced ALK2 inhibitors.

Woodward, H.L. Innocenti, P. Cheung, K.-.M.J. Hayes, A. Roberts, J. Henley, A.T. Faisal, A. Mak, G.W.-.Y. Box, G. Westwood, I.M. Cronin, N. Carter, M. Valenti, M. De Haven Brandon, A. O'Fee, L. Saville, H. Schmitt, J. Burke, R. Broccatelli, F. van Montfort, R.L.M. Raynaud, F.I. Eccles, S.A. Linardopoulos, S. Blagg, J. Hoelder, S (2018) Introduction of a Methyl Group Curbs Metabolism of Pyrido[3,4- d]pyrimidine Monopolar Spindle 1 (MPS1) Inhibitors and Enables the Discovery of the Phase 1 Clinical Candidate N<sup>2</sup>-(2-Ethoxy-4-(4-methyl-4 H-1,2,4-triazol-3-yl)phenyl)-6-methyl- N<sup>8</sup>-neopentylpyrido[3,4- d]pyrimidine-2,8-diamine (BOS172722).. Show Abstract full text

Monopolar spindle 1 (MPS1) occupies a central role in mitosis and is one of the main components of the spindle assembly checkpoint. The MPS1 kinase is an attractive cancer target, and herein, we report the discovery of the clinical candidate BOS172722. The starting point for our work was a series of pyrido[3,4- d]pyrimidine inhibitors that demonstrated excellent potency and kinase selectivity but suffered from rapid turnover in human liver microsomes (HLM). Optimizing HLM stability proved challenging since it was not possible to identify a consistent site of metabolism and lowering lipophilicity proved unsuccessful. Key to overcoming this problem was the finding that introduction of a methyl group at the 6-position of the pyrido[3,4- d]pyrimidine core significantly improved HLM stability. Met ID studies suggested that the methyl group suppressed metabolism at the distant aniline portion of the molecule, likely by blocking the preferred pharmacophore through which P450 recognized the compound. This work ultimately led to the discovery of BOS172722 as a Phase 1 clinical candidate.

Watts, E. Heidenreich, D. Tucker, E. Raab, M. Strebhardt, K. Chesler, L. Knapp, S. Bellenie, B. Hoelder, S (2019) Designing Dual Inhibitors of Anaplastic Lymphoma Kinase (ALK) and Bromodomain-4 (BRD4) by Tuning Kinase Selectivity.. Show Abstract full text

Concomitant inhibition of anaplastic lymphoma kinase (ALK) and bromodomain-4 (BRD4) is a potential therapeutic strategy for targeting two key oncogenic drivers that co-segregate in a significant fraction of high-risk neuroblastoma patients, mutation of ALK and amplification of MYCN. Starting from known dual polo-like kinase (PLK)-1-BRD4 inhibitor BI-2536, we employed structure-based design to redesign this series toward compounds with a dual ALK-BRD4 profile. These efforts led to compound ( R)-2-((2-ethoxy-4-(1-methylpiperidin-4-yl)phenyl)amino)-7-ethyl-5-methyl-8-((4-methylthiophen-2-yl)methyl)-7,8-dihydropteridin-6(5 H)-one (16k) demonstrating improved ALK activity and significantly reduced PLK-1 activity, while maintaining BRD4 activity and overall kinome selectivity. We demonstrate the compounds' on-target engagement with ALK and BRD4 in cells as well as favorable broad kinase and bromodomain selectivity.

Innocenti, P. Woodward, H. O'Fee, L. Hoelder, S (2015) Expanding the scope of fused pyrimidines as kinase inhibitor scaffolds: synthesis and modification of pyrido[3,4-d]pyrimidines.. Show Abstract full text

Fused pyrimidine cores are privileged kinase scaffolds, yet few examples of the 2-amino-pyrido[3,4-d]pyrimidine chemotype have been disclosed in the context of kinase inhibitor programs. Furthermore, no general synthetic route has been reported to access 2-amino-pyrido[3,4-d]pyrimidine derivatives. Here we report a versatile and efficient chemical approach to this class of molecules. Our strategy involves the concise preparation of 8-chloro-2-(methylthio)pyrido[3,4-d]pyrimidine intermediates and their efficient derivatisation to give novel compounds with potential as kinase inhibitors.

Innocenti, P. Cheung, K.-.M.J. Solanki, S. Mas-Droux, C. Rowan, F. Yeoh, S. Boxall, K. Westlake, M. Pickard, L. Hardy, T. Baxter, J.E. Aherne, G.W. Bayliss, R. Fry, A.M. Hoelder, S (2012) Design of potent and selective hybrid inhibitors of the mitotic kinase Nek2: structure-activity relationship, structural biology, and cellular activity.. Show Abstract full text

We report herein a series of Nek2 inhibitors based on an aminopyridine scaffold. These compounds have been designed by combining key elements of two previously discovered chemical series. Structure based design led to aminopyridine (R)-21, a potent and selective inhibitor able to modulate Nek2 activity in cells.

Types of Publications

Journal articles

Vogtherr, M. Saxena, K. Hoelder, S. Grimme, S. Betz, M. Schieborr, U. Pescatore, B. Robin, M. Delarbre, L. Langer, T. Wendt, K.U. Schwalbe, H (2006) NMR characterization of kinase p38 dynamics in free and ligand-bound forms..
Richards, M.W. O'Regan, L. Mas-Droux, C. Blot, J.M.Y. Cheung, J. Hoelder, S. Fry, A.M. Bayliss, R (2009) An autoinhibitory tyrosine motif in the cell-cycle-regulated Nek7 kinase is released through binding of Nek9.. Show Abstract full text

Mitosis is controlled by multiple protein kinases, many of which are abnormally expressed in human cancers. Nek2, Nek6, Nek7, and Nek9 are NIMA-related kinases essential for proper mitotic progression. We determined the atomic structure of Nek7 and discovered an autoinhibited conformation that suggests a regulatory mechanism not previously described in kinases. Additionally, Nek2 adopts the same conformation when bound to a drug-like molecule. In both structures, a tyrosine side chain points into the active site, interacts with the activation loop, and blocks the alphaC helix. Tyrosine mutants of Nek7 and the related kinase Nek6 are constitutively active. The activity of Nek6 and Nek7, but not the tyrosine mutant, is increased by interaction with the Nek9 noncatalytic C-terminal domain, suggesting a mechanism in which the tyrosine is released from its autoinhibitory position. The autoinhibitory conformation is common to three Neks and provides a potential target for selective kinase inhibitors.

Whelligan, D.K. Thomson, D.W. Taylor, D. Hoelder, S (2010) Two-step synthesis of aza- and diazaindoles from chloroamino-N-heterocycles using ethoxyvinylborolane.. Show Abstract full text

An efficient two-step route to a broad range of aza- and diazaindoles was established, starting from chloroamino-N-heterocycles, without the need for protecting groups. The method involves an optimized Suzuki-Miyaura coupling with (2-ethoxyvinyl)borolane followed by acetic acid-catalyzed cyclization.

Whelligan, D.K. Solanki, S. Taylor, D. Thomson, D.W. Cheung, K.-.M.J. Boxall, K. Mas-Droux, C. Barillari, C. Burns, S. Grummitt, C.G. Collins, I. van Montfort, R.L.M. Aherne, G.W. Bayliss, R. Hoelder, S (2010) Aminopyrazine inhibitors binding to an unusual inactive conformation of the mitotic kinase Nek2: SAR and structural characterization.. Show Abstract full text

We report herein the first systematic exploration of inhibitors of the mitotic kinase Nek2. Starting from HTS hit aminopyrazine 2, compounds with improved activity were identified using structure-based design. Our structural biology investigations reveal two notable observations. First, 2 and related compounds bind to an unusual, inactive conformation of the kinase which to the best of our knowledge has not been reported for other types of kinase inhibitors. Second, a phenylalanine residue at the center of the ATP pocket strongly affects the ability of the inhibitor to bind to the protein. The implications of these observations are discussed, and the work described here defines key features for potent and selective Nek2 inhibition, which will aid the identification of more advanced inhibitors of Nek2.

Solanki, S. Innocenti, P. Mas-Droux, C. Boxall, K. Barillari, C. van Montfort, R.L.M. Aherne, G.W. Bayliss, R. Hoelder, S (2011) Benzimidazole inhibitors induce a DFG-out conformation of never in mitosis gene A-related kinase 2 (Nek2) without binding to the back pocket and reveal a nonlinear structure-activity relationship.. Show Abstract full text

We describe herein the structure-activity relationship (SAR) and cocrystal structures of a series of Nek2 inhibitors derived from the published polo-like kinase 1 (Plk1) inhibitor (R)-1. Our studies reveal a nonlinear SAR for Nek2 and our cocrystal structures show that compounds in this series bind to a DFG-out conformation of Nek2 without extending into the enlarged back pocket commonly found in this conformation. These observations were further investigated, and structure-based design led to Nek2 inhibitors derived from (R)-1 with more than a hundred-fold selectivity against Plk1.

Blechert, S. Brodschelm, W. Hölder, S. Kammerer, L. Kutchan, T.M. Mueller, M.J. Xia, Z.Q. Zenk, M.H (1995) The octadecanoic pathway: signal molecules for the regulation of secondary pathways.. Show Abstract full text

Plant defense against microbial pathogens and herbivores relies heavily on the induction of defense proteins and low molecular weight antibiotics. The signals between perception of the aggression, gene activation, and the subsequent biosynthesis of secondary compounds are assumed to be pentacylic oxylipin derivatives. The rapid, but transient, synthesis of cis-jasmonic acid was demonstrated after insect attack on a food plant and by microbial elicitor addition to plant suspension cultures. This effect is highly specific and not caused by a number of environmental stresses such as light, heavy metals, or cold or heat shock. Elicitation of Eschscholtzia cell cultures also led to a rapid alkalinization of the growth medium prior to jasmonate formation. Inhibition of this alkalinization process by the protein kinase inhibitor staurosporine also inhibited jasmonate formation. The induction of specific enzymes in the benzo[c]phenanthridine alkaloid pathway leading to the antimicrobial sanguinarine was induced to a qualitatively and quantitatively similar extent by fungal elicitor, methyl jasmonate, and its linolenic acid-derived precursor 12-oxophytodienoic acid. It is herein proposed that a second oxylipid cascade may exist in plants starting from linoleic acid via 15,16-dihydro-12-oxophytodienoic acid to 9,10-dihydrojasmonate. Experiments with synthetic trihomojasmonate demonstrated that beta-oxidation is not a prerequisite for biological activity and that 12-oxophytodienoic acid and derivatives are most likely fully active as signal transducers. Octadecanoic acid-derived compounds are essential elements in modulating the synthesis of antibiotic compounds and are thus integral to plant defense.

Pedersen, H. Hölder, S. Sutherlin, D.P. Schwitter, U. King, D.S. Schultz, P.G (1998) A method for directed evolution and functional cloning of enzymes.. Show Abstract full text

A general scheme is described for the in vitro evolution of protein catalysts in a biologically amplifiable system. Substrate is covalently and site specifically attached by a flexible tether to the pIII coat protein of a filamentous phage that also displays the catalyst. Intramolecular conversion of substrate to product provides a basis for selecting active catalysts from a library of mutants, either by release from or attachment to a solid support. This methodology has been developed with the enzyme staphylococcal nuclease as a model. An analysis of factors influencing the selection efficiency is presented, and it is shown that phage displaying staphylococcal nuclease can be enriched 100-fold in a single step from a library-like ensemble of phage displaying noncatalytic proteins. Additionally, this approach should allow one to functionally clone natural enzymes, based on their ability to catalyze specific reactions (e.g., glycosyl transfer, sequence-specific proteolysis or phosphorylation, polymerization, etc.) rather than their sequence- or structural homology to known enzymes.

Blechert, S. Bockelmann, C. Brummer, O. Fusslein, M. Gundlach, H. Haider, G. Holder, S. Kutchan, T.M. Weiler, E.W. Zenk, M.H (1997) Structural separation of biological activities of jasmonates and related compounds. full text
Holder, S. Blechert, S (1996) A concise synthesis of coronafacic acid via ring closing olefin metathesis. full text
Hoelder, S. Clarke, P.A. Workman, P (2012) Discovery of small molecule cancer drugs: successes, challenges and opportunities.. Show Abstract full text

The discovery and development of small molecule cancer drugs has been revolutionised over the last decade. Most notably, we have moved from a one-size-fits-all approach that emphasized cytotoxic chemotherapy to a personalised medicine strategy that focuses on the discovery and development of molecularly targeted drugs that exploit the particular genetic addictions, dependencies and vulnerabilities of cancer cells. These exploitable characteristics are increasingly being revealed by our expanding understanding of the abnormal biology and genetics of cancer cells, accelerated by cancer genome sequencing and other high-throughput genome-wide campaigns, including functional screens using RNA interference. In this review we provide an overview of contemporary approaches to the discovery of small molecule cancer drugs, highlighting successes, current challenges and future opportunities. We focus in particular on four key steps: Target validation and selection; chemical hit and lead generation; lead optimization to identify a clinical drug candidate; and finally hypothesis-driven, biomarker-led clinical trials. Although all of these steps are critical, we view target validation and selection and the conduct of biology-directed clinical trials as especially important areas upon which to focus to speed progress from gene to drug and to reduce the unacceptably high attrition rate during clinical development. Other challenges include expanding the envelope of druggability for less tractable targets, understanding and overcoming drug resistance, and designing intelligent and effective drug combinations. We discuss not only scientific and technical challenges, but also the assessment and mitigation of risks as well as organizational, cultural and funding problems for cancer drug discovery and development, together with solutions to overcome the 'Valley of Death' between basic research and approved medicines. We envisage a future in which addressing these challenges will enhance our rapid progress towards truly personalised medicine for cancer patients.

Wylie, L. Innocenti, P. Whelligan, D.K. Hoelder, S (2012) Synthesis of amino-substituted indoles using the Bartoli reaction.. Show Abstract full text

We report herein the concise preparation of a range of functionalised aminoindoles via a new application of the Bartoli reaction. Scope and limitations of the methodology have been extensively studied to reveal the importance of protecting groups and substitution patterns. The use of amino substituted nitroanilines for the Bartoli reaction is to our knowledge unprecedented. Our work thus represents a novel entry into substituted aminoindoles which are relevant building blocks for both the fine chemical and pharmaceutical industry.

Vidler, L.R. Brown, N. Knapp, S. Hoelder, S (2012) Druggability analysis and structural classification of bromodomain acetyl-lysine binding sites.. Show Abstract full text

Bromodomains are readers of the epigenetic code that specifically bind acetyl-lysine containing recognition sites on proteins. Recently the BET family of bromodomains has been demonstrated to be druggable through the discovery of potent inhibitors, sparking an interest in protein-protein interaction inhibitors that directly target gene transcription. Here, we assess the druggability of diverse members of the bromodomain family using SiteMap and show that there are significant differences in predicted druggability. Furthermore, we trace these differences in druggability back to unique amino acid signatures in the bromodomain acetyl-lysine binding sites. These signatures were then used to generate a new classification of the bromodomain family, visualized as a classification tree. This represents the first analysis of this type for the bromodomain family and can prove useful in the discovery of inhibitors, particularly for anticipating screening hit rates, identifying inhibitors that can be explored for lead hopping approaches, and selecting proteins for selectivity screening.

Silva-Santisteban, M.C. Westwood, I.M. Boxall, K. Brown, N. Peacock, S. McAndrew, C. Barrie, E. Richards, M. Mirza, A. Oliver, A.W. Burke, R. Hoelder, S. Jones, K. Aherne, G.W. Blagg, J. Collins, I. Garrett, M.D. van Montfort, R.L.M (2013) Fragment-based screening maps inhibitor interactions in the ATP-binding site of checkpoint kinase 2.. Show Abstract full text

Checkpoint kinase 2 (CHK2) is an important serine/threonine kinase in the cellular response to DNA damage. A fragment-based screening campaign using a combination of a high-concentration AlphaScreen™ kinase assay and a biophysical thermal shift assay, followed by X-ray crystallography, identified a number of chemically different ligand-efficient CHK2 hinge-binding scaffolds that have not been exploited in known CHK2 inhibitors. In addition, it showed that the use of these orthogonal techniques allowed efficient discrimination between genuine hit matter and false positives from each individual assay technology. Furthermore, the CHK2 crystal structures with a quinoxaline-based fragment and its follow-up compound highlight a hydrophobic area above the hinge region not previously explored in rational CHK2 inhibitor design, but which might be exploited to enhance both potency and selectivity of CHK2 inhibitors.

Vidler, L.R. Filippakopoulos, P. Fedorov, O. Picaud, S. Martin, S. Tomsett, M. Woodward, H. Brown, N. Knapp, S. Hoelder, S (2013) Discovery of novel small-molecule inhibitors of BRD4 using structure-based virtual screening.. Show Abstract full text

Bromodomains (BRDs) are epigenetic readers that recognize acetylated-lysine (KAc) on proteins and are implicated in a number of diseases. We describe a virtual screening approach to identify BRD inhibitors. Key elements of this approach are the extensive design and use of substructure queries to compile a set of commercially available compounds featuring novel putative KAc mimetics and docking this set for final compound selection. We describe the validation of this approach by applying it to the first BRD of BRD4. The selection and testing of 143 compounds lead to the discovery of six novel hits, including four unprecedented KAc mimetics. We solved the crystal structure of four hits, determined their binding mode, and improved their potency through synthesis and the purchase of derivatives. This work provides a validated virtual screening approach that is applicable to other BRDs and describes novel KAc mimetics that can be further explored to design more potent inhibitors.

Naud, S. Westwood, I.M. Faisal, A. Sheldrake, P. Bavetsias, V. Atrash, B. Cheung, K.M.J. Liu, M. Hayes, A. Schmitt, J. Wood, A. Choi, V. Boxall, K. Mak, G. Gurden, M. Valenti, M. de Haven Brandon, A. Henley, A. Baker, R. McAndrew, C. Matijssen, B. Burke, R. Hoelder, S. Eccles, S.A. Raynaud, F.I. Linardopoulos, S. Van Montfort, R.L.M. Blagg, J (2013) Structure-based design of orally bioavailable 1H-pyrrolo[3,2-c]pyridine inhibitors of the mitotic kinase monopolar spindle 1 (MPS1).
Drouin, L. McGrath, S. Vidler, L.R. Chaikuad, A. Monteiro, O. Tallant, C. Philpott, M. Rogers, C. Fedorov, O. Liu, M. Akhtar, W. Hayes, A. Raynaud, F. Müller, S. Knapp, S. Hoelder, S (2015) Structure enabled design of BAZ2-ICR, a chemical probe targeting the bromodomains of BAZ2A and BAZ2B.. Show Abstract full text

The bromodomain containing proteins BAZ2A/B play essential roles in chromatin remodeling and regulation of noncoding RNAs. We present the structure based discovery of a potent, selective, and cell active inhibitor 13 (BAZ2-ICR) of the BAZ2A/B bromodomains through rapid optimization of a weakly potent starting point. A key feature of the presented inhibitors is an intramolecular aromatic stacking interaction that efficiently occupies the shallow bromodomain pockets. 13 represents an excellent chemical probe for functional studies of the BAZ2 bromodomains in vitro and in vivo.

Gurden, M.D. Westwood, I.M. Faisal, A. Naud, S. Cheung, K.-.M.J. McAndrew, C. Wood, A. Schmitt, J. Boxall, K. Mak, G. Workman, P. Burke, R. Hoelder, S. Blagg, J. Van Montfort, R.L.M. Linardopoulos, S (2015) Naturally Occurring Mutations in the MPS1 Gene Predispose Cells to Kinase Inhibitor Drug Resistance.. Show Abstract full text

Acquired resistance to therapy is perhaps the greatest challenge to effective clinical management of cancer. With several inhibitors of the mitotic checkpoint kinase MPS1 in preclinical development, we sought to investigate how resistance against these inhibitors may arise so that mitigation or bypass strategies could be addressed as early as possible. Toward this end, we modeled acquired resistance to the MPS1 inhibitors AZ3146, NMS-P715, and CCT251455, identifying five point mutations in the kinase domain of MPS1 that confer resistance against multiple inhibitors. Structural studies showed how the MPS1 mutants conferred resistance by causing steric hindrance to inhibitor binding. Notably, we show that these mutations occur in nontreated cancer cell lines and primary tumor specimens, and that they also preexist in normal lymphoblast and breast tissues. In a parallel piece of work, we also show that the EGFR p.T790M mutation, the most common mutation conferring resistance to the EGFR inhibitor gefitinib, also preexists in cancer cells and normal tissue. Our results therefore suggest that mutations conferring resistance to targeted therapy occur naturally in normal and malignant cells and these mutations do not arise as a result of the increased mutagenic plasticity of cancer cells.

Innocenti, P. Woodward, H.L. Solanki, S. Naud, S. Westwood, I.M. Cronin, N. Hayes, A. Roberts, J. Henley, A.T. Baker, R. Faisal, A. Mak, G.W.-.Y. Box, G. Valenti, M. De Haven Brandon, A. O'Fee, L. Saville, H. Schmitt, J. Matijssen, B. Burke, R. van Montfort, R.L.M. Raynaud, F.I. Eccles, S.A. Linardopoulos, S. Blagg, J. Hoelder, S (2016) Rapid Discovery of Pyrido[3,4-d]pyrimidine Inhibitors of Monopolar Spindle Kinase 1 (MPS1) Using a Structure-Based Hybridization Approach.. Show Abstract full text

Monopolar spindle 1 (MPS1) plays a central role in the transition of cells from metaphase to anaphase and is one of the main components of the spindle assembly checkpoint. Chromosomally unstable cancer cells rely heavily on MPS1 to cope with the stress arising from abnormal numbers of chromosomes and centrosomes and are thus more sensitive to MPS1 inhibition than normal cells. We report the discovery and optimization of a series of new pyrido[3,4-d]pyrimidine based inhibitors via a structure-based hybridization approach from our previously reported inhibitor CCT251455 and a modestly potent screening hit. Compounds in this novel series display excellent potency and selectivity for MPS1, which translates into biomarker modulation in an in vivo human tumor xenograft model.

Faisal, A. Naud, S. Schmitt, J. Westwood, I. Hayes, A. Gurden, M. Bavetsias, V. Berry, T. Mak, G. Innocenti, P. Cheung, J. Sheldrake, P. Atrash, B. Sun, C. Matijssen, B. Burke, R. Baker, R. McAndrew, C. Rowlands, M. Workman, P. Eccles, S.A. Hoelder, S. Raynaud, F.I. vanMontfort, R. Biagg, J. Linardopoulos, S (2012) Characterisation of CCT251455, a novel, selective and highly potent Mps1 kinase inhibitor. full text
Tisi, D. Chiarparin, E. Tamanini, E. Pathuri, P. Coyle, J.E. Hold, A. Holding, F.P. Amin, N. Martin, A.C.L. Rich, S.J. Berdini, V. Yon, J. Acklam, P. Burke, R. Drouin, L. Harmer, J.E. Jeganathan, F. van Montfort, R.L.M. Newbatt, Y. Tortorici, M. Westlake, M. Wood, A. Hoelder, S. Heightman, T.D (2016) Structure of the Epigenetic Oncogene MMSET and Inhibition by N-Alkyl Sinefungin Derivatives.. Show Abstract full text

The members of the NSD subfamily of lysine methyl transferases are compelling oncology targets due to the recent characterization of gain-of-function mutations and translocations in several hematological cancers. To date, these proteins have proven intractable to small molecule inhibition. Here, we present initial efforts to identify inhibitors of MMSET (aka NSD2 or WHSC1) using solution phase and crystal structural methods. On the basis of 2D NMR experiments comparing NSD1 and MMSET structural mobility, we designed an MMSET construct with five point mutations in the N-terminal helix of its SET domain for crystallization experiments and elucidated the structure of the mutant MMSET SET domain at 2.1 Å resolution. Both NSD1 and MMSET crystal systems proved resistant to soaking or cocrystallography with inhibitors. However, use of the close homologue SETD2 as a structural surrogate supported the design and characterization of N-alkyl sinefungin derivatives, which showed low micromolar inhibition against both SETD2 and MMSET.

McGrath, S. Tortorici, M. Drouin, L. Solanki, S. Vidler, L. Westwood, I. Gimeson, P. Van Montfort, R. Hoelder, S (2017) Structure-Enabled Discovery of a Stapled Peptide Inhibitor to Target the Oncogenic Transcriptional Repressor TLE1.. Show Abstract full text

TLE1 is an oncogenic transcriptional co-repressor that exerts its repressive effects through binding of transcription factors. Inhibition of this protein-protein interaction represents a putative cancer target, but no small-molecule inhibitors have been published for this challenging interface. Herein, the structure-enabled design and synthesis of a constrained peptide inhibitor of TLE1 is reported. The design features the introduction of a four-carbon-atom linker into the peptide epitope found in many TLE1 binding partners. A concise synthetic route to a proof-of-concept peptide, cycFWRPW, has been developed. Biophysical testing by isothermal titration calorimetry and thermal shift assays showed that, although the constrained peptide bound potently, it had an approximately five-fold higher K<sub>d</sub> than that of the unconstrained peptide. The co-crystal structure suggested that the reduced affinity was likely to be due to a small shift of one side chain, relative to the otherwise well-conserved conformation of the acyclic peptide. This work describes a constrained peptide inhibitor that may serve as the basis for improved inhibitors.

Faisal, A. Mak, G.W.Y. Gurden, M.D. Xavier, C.P.R. Anderhub, S.J. Innocenti, P. Westwood, I.M. Naud, S. Hayes, A. Box, G. Valenti, M.R. De Haven Brandon, A.K. O'Fee, L. Schmitt, J. Woodward, H.L. Burke, R. vanMontfort, R.L.M. Blagg, J. Raynaud, F.I. Eccles, S.A. Hoelder, S. Linardopoulos, S (2017) Characterisation of CCT271850, a selective, oral and potent MPS1 inhibitor, used to directly measure in vivo MPS1 inhibition vs therapeutic efficacy.. Show Abstract full text

<h4>Background</h4>The main role of the cell cycle is to enable error-free DNA replication, chromosome segregation and cytokinesis. One of the best characterised checkpoint pathways is the spindle assembly checkpoint, which prevents anaphase onset until the appropriate attachment and tension across kinetochores is achieved. MPS1 kinase activity is essential for the activation of the spindle assembly checkpoint and has been shown to be deregulated in human tumours with chromosomal instability and aneuploidy. Therefore, MPS1 inhibition represents an attractive strategy to target cancers.<h4>Methods</h4>To evaluate CCT271850 cellular potency, two specific antibodies that recognise the activation sites of MPS1 were used and its antiproliferative activity was determined in 91 human cancer cell lines. DLD1 cells with induced GFP-MPS1 and HCT116 cells were used in in vivo studies to directly measure MPS1 inhibition and efficacy of CCT271850 treatment.<h4>Results</h4>CCT271850 selectively and potently inhibits MPS1 kinase activity in biochemical and cellular assays and in in vivo models. Mechanistically, tumour cells treated with CCT271850 acquire aberrant numbers of chromosomes and the majority of cells divide their chromosomes without proper alignment because of abrogation of the mitotic checkpoint, leading to cell death. We demonstrated a moderate level of efficacy of CCT271850 as a single agent in a human colorectal carcinoma xenograft model.<h4>Conclusions</h4>CCT271850 is a potent, selective and orally bioavailable MPS1 kinase inhibitor. On the basis of in vivo pharmacodynamic vs efficacy relationships, we predict that more than 80% inhibition of MPS1 activity for at least 24 h is required to achieve tumour stasis or regression by CCT271850.

Hudson, L. Mui, J. Vázquez, S. Carvalho, D.M. Williams, E. Jones, C. Bullock, A.N. Hoelder, S (2018) Novel Quinazolinone Inhibitors of ALK2 Flip between Alternate Binding Modes: Structure-Activity Relationship, Structural Characterization, Kinase Profiling, and Cellular Proof of Concept.. Show Abstract full text

Structure-activity relationship and crystallographic data revealed that quinazolinone-containing fragments flip between two distinct modes of binding to activin receptor-like kinase-2 (ALK2). We explored both binding modes to discover potent inhibitors and characterized the chemical modifications that triggered the flip in binding mode. We report kinase selectivity and demonstrate that compounds of this series modulate ALK2 in cancer cells. These inhibitors are attractive starting points for the discovery of more advanced ALK2 inhibitors.

Woodward, H.L. Innocenti, P. Cheung, K.-.M.J. Hayes, A. Roberts, J. Henley, A.T. Faisal, A. Mak, G.W.-.Y. Box, G. Westwood, I.M. Cronin, N. Carter, M. Valenti, M. De Haven Brandon, A. O'Fee, L. Saville, H. Schmitt, J. Burke, R. Broccatelli, F. van Montfort, R.L.M. Raynaud, F.I. Eccles, S.A. Linardopoulos, S. Blagg, J. Hoelder, S (2018) Introduction of a Methyl Group Curbs Metabolism of Pyrido[3,4- d]pyrimidine Monopolar Spindle 1 (MPS1) Inhibitors and Enables the Discovery of the Phase 1 Clinical Candidate N<sup>2</sup>-(2-Ethoxy-4-(4-methyl-4 H-1,2,4-triazol-3-yl)phenyl)-6-methyl- N<sup>8</sup>-neopentylpyrido[3,4- d]pyrimidine-2,8-diamine (BOS172722).. Show Abstract full text

Monopolar spindle 1 (MPS1) occupies a central role in mitosis and is one of the main components of the spindle assembly checkpoint. The MPS1 kinase is an attractive cancer target, and herein, we report the discovery of the clinical candidate BOS172722. The starting point for our work was a series of pyrido[3,4- d]pyrimidine inhibitors that demonstrated excellent potency and kinase selectivity but suffered from rapid turnover in human liver microsomes (HLM). Optimizing HLM stability proved challenging since it was not possible to identify a consistent site of metabolism and lowering lipophilicity proved unsuccessful. Key to overcoming this problem was the finding that introduction of a methyl group at the 6-position of the pyrido[3,4- d]pyrimidine core significantly improved HLM stability. Met ID studies suggested that the methyl group suppressed metabolism at the distant aniline portion of the molecule, likely by blocking the preferred pharmacophore through which P450 recognized the compound. This work ultimately led to the discovery of BOS172722 as a Phase 1 clinical candidate.

Watts, E. Heidenreich, D. Tucker, E. Raab, M. Strebhardt, K. Chesler, L. Knapp, S. Bellenie, B. Hoelder, S (2019) Designing Dual Inhibitors of Anaplastic Lymphoma Kinase (ALK) and Bromodomain-4 (BRD4) by Tuning Kinase Selectivity.. Show Abstract full text

Concomitant inhibition of anaplastic lymphoma kinase (ALK) and bromodomain-4 (BRD4) is a potential therapeutic strategy for targeting two key oncogenic drivers that co-segregate in a significant fraction of high-risk neuroblastoma patients, mutation of ALK and amplification of MYCN. Starting from known dual polo-like kinase (PLK)-1-BRD4 inhibitor BI-2536, we employed structure-based design to redesign this series toward compounds with a dual ALK-BRD4 profile. These efforts led to compound ( R)-2-((2-ethoxy-4-(1-methylpiperidin-4-yl)phenyl)amino)-7-ethyl-5-methyl-8-((4-methylthiophen-2-yl)methyl)-7,8-dihydropteridin-6(5 H)-one (16k) demonstrating improved ALK activity and significantly reduced PLK-1 activity, while maintaining BRD4 activity and overall kinome selectivity. We demonstrate the compounds' on-target engagement with ALK and BRD4 in cells as well as favorable broad kinase and bromodomain selectivity.

Bellenie, B.R. Cheung, K.-.M.J. Varela, A. Pierrat, O.A. Collie, G.W. Box, G.M. Bright, M.D. Gowan, S. Hayes, A. Rodrigues, M.J. Shetty, K.N. Carter, M. Davis, O.A. Henley, A.T. Innocenti, P. Johnson, L.D. Liu, M. de Klerk, S. Le Bihan, Y.-.V. Lloyd, M.G. McAndrew, P.C. Shehu, E. Talbot, R. Woodward, H.L. Burke, R. Kirkin, V. van Montfort, R.L.M. Raynaud, F.I. Rossanese, O.W. Hoelder, S (2020) Achieving <i>In Vivo</i> Target Depletion through the Discovery and Optimization of Benzimidazolone BCL6 Degraders.. Show Abstract full text

Deregulation of the transcriptional repressor BCL6 enables tumorigenesis of germinal center B-cells, and hence BCL6 has been proposed as a therapeutic target for the treatment of diffuse large B-cell lymphoma (DLBCL). Herein we report the discovery of a series of benzimidazolone inhibitors of the protein-protein interaction between BCL6 and its co-repressors. A subset of these inhibitors were found to cause rapid degradation of BCL6, and optimization of pharmacokinetic properties led to the discovery of 5-((5-chloro-2-((3<i>R</i>,5<i>S</i>)-4,4-difluoro-3,5-dimethylpiperidin-1-yl)pyrimidin-4-yl)amino)-3-(3-hydroxy-3-methylbutyl)-1-methyl-1,3-dihydro-2<i>H</i>-benzo[<i>d</i>]imidazol-2-one (CCT369260), which reduces BCL6 levels in a lymphoma xenograft mouse model following oral dosing.

Innocenti, P. Woodward, H. O'Fee, L. Hoelder, S (2015) Expanding the scope of fused pyrimidines as kinase inhibitor scaffolds: synthesis and modification of pyrido[3,4-d]pyrimidines.. Show Abstract full text

Fused pyrimidine cores are privileged kinase scaffolds, yet few examples of the 2-amino-pyrido[3,4-d]pyrimidine chemotype have been disclosed in the context of kinase inhibitor programs. Furthermore, no general synthetic route has been reported to access 2-amino-pyrido[3,4-d]pyrimidine derivatives. Here we report a versatile and efficient chemical approach to this class of molecules. Our strategy involves the concise preparation of 8-chloro-2-(methylthio)pyrido[3,4-d]pyrimidine intermediates and their efficient derivatisation to give novel compounds with potential as kinase inhibitors.

Innocenti, P. Cheung, K.-.M.J. Solanki, S. Mas-Droux, C. Rowan, F. Yeoh, S. Boxall, K. Westlake, M. Pickard, L. Hardy, T. Baxter, J.E. Aherne, G.W. Bayliss, R. Fry, A.M. Hoelder, S (2012) Design of potent and selective hybrid inhibitors of the mitotic kinase Nek2: structure-activity relationship, structural biology, and cellular activity.. Show Abstract full text

We report herein a series of Nek2 inhibitors based on an aminopyridine scaffold. These compounds have been designed by combining key elements of two previously discovered chemical series. Structure based design led to aminopyridine (R)-21, a potent and selective inhibitor able to modulate Nek2 activity in cells.

Darby, J.F. Vidler, L.R. Simpson, P.J. Al-Lazikani, B. Matthews, S.J. Sharp, S.Y. Pearl, L.H. Hoelder, S. Workman, P (2020) Solution structure of the Hop TPR2A domain and investigation of target druggability by NMR, biochemical and in silico approaches.. Show Abstract full text

Heat shock protein 90 (Hsp90) is a molecular chaperone that plays an important role in tumour biology by promoting the stabilisation and activity of oncogenic 'client' proteins. Inhibition of Hsp90 by small-molecule drugs, acting via its ATP hydrolysis site, has shown promise as a molecularly targeted cancer therapy. Owing to the importance of Hop and other tetratricopeptide repeat (TPR)-containing cochaperones in regulating Hsp90 activity, the Hsp90-TPR domain interface is an alternative site for inhibitors, which could result in effects distinct from ATP site binders. The TPR binding site of Hsp90 cochaperones includes a shallow, positively charged groove that poses a significant challenge for druggability. Herein, we report the apo, solution-state structure of Hop TPR2A which enables this target for NMR-based screening approaches. We have designed prototype TPR ligands that mimic key native 'carboxylate clamp' interactions between Hsp90 and its TPR cochaperones and show that they block binding between Hop TPR2A and the Hsp90 C-terminal MEEVD peptide. We confirm direct TPR-binding of these ligands by mapping <sup>1</sup>H-<sup>15</sup>N HSQC chemical shift perturbations to our new NMR structure. Our work provides a novel structure, a thorough assessment of druggability and robust screening approaches that may offer a potential route, albeit difficult, to address the chemically challenging nature of the Hop TPR2A target, with relevance to other TPR domain interactors.

Lloyd, M.G. Huckvale, R. Cheung, K.-.M.J. Rodrigues, M.J. Collie, G.W. Pierrat, O.A. Gatti Iou, M. Carter, M. Davis, O.A. McAndrew, P.C. Gunnell, E. Le Bihan, Y.-.V. Talbot, R. Henley, A.T. Johnson, L.D. Hayes, A. Bright, M.D. Raynaud, F.I. Meniconi, M. Burke, R. van Montfort, R.L.M. Rossanese, O.W. Bellenie, B.R. Hoelder, S (2021) Into Deep Water: Optimizing BCL6 Inhibitors by Growing into a Solvated Pocket.. Show Abstract full text

We describe the optimization of modestly active starting points to potent inhibitors of BCL6 by growing into a subpocket, which was occupied by a network of five stably bound water molecules. Identifying potent inhibitors required not only forming new interactions in the subpocket but also perturbing the water network in a productive, potency-increasing fashion while controlling the physicochemical properties. We achieved this goal in a sequential manner by systematically probing the pocket and the water network, ultimately achieving a 100-fold improvement of activity. The most potent compounds displaced three of the five initial water molecules and formed hydrogen bonds with the remaining two. Compound <b>25</b> showed a promising profile for a lead compound with submicromolar inhibition of BCL6 in cells and satisfactory pharmacokinetic (PK) properties. Our work highlights the importance of finding productive ways to perturb existing water networks when growing into solvent-filled protein pockets.

Huckvale, R. Harnden, A.C. Cheung, K.-.M.J. Pierrat, O.A. Talbot, R. Box, G.M. Henley, A.T. de Haven Brandon, A.K. Hallsworth, A.E. Bright, M.D. Akpinar, H.A. Miller, D.S.J. Tarantino, D. Gowan, S. Hayes, A. Gunnell, E.A. Brennan, A. Davis, O.A. Johnson, L.D. de Klerk, S. McAndrew, C. Le Bihan, Y.-.V. Meniconi, M. Burke, R. Kirkin, V. van Montfort, R.L.M. Raynaud, F.I. Rossanese, O.W. Bellenie, B.R. Hoelder, S (2022) Improved Binding Affinity and Pharmacokinetics Enable Sustained Degradation of BCL6 <i>In Vivo</i>.. Show Abstract full text

The transcriptional repressor BCL6 is an oncogenic driver found to be deregulated in lymphoid malignancies. Herein, we report the optimization of our previously reported benzimidazolone molecular glue-type degrader <b>CCT369260</b> to <b>CCT373566</b>, a highly potent probe suitable for sustained depletion of BCL6 <i>in vivo</i>. We observed a sharp degradation SAR, where subtle structural changes conveyed the ability to induce degradation of BCL6. <b>CCT373566</b> showed modest <i>in vivo</i> efficacy in a lymphoma xenograft mouse model following oral dosing.

Davis, O.A. Cheung, K.-.M.J. Brennan, A. Lloyd, M.G. Rodrigues, M.J. Pierrat, O.A. Collie, G.W. Le Bihan, Y.-.V. Huckvale, R. Harnden, A.C. Varela, A. Bright, M.D. Eve, P. Hayes, A. Henley, A.T. Carter, M.D. McAndrew, P.C. Talbot, R. Burke, R. van Montfort, R.L.M. Raynaud, F.I. Rossanese, O.W. Meniconi, M. Bellenie, B.R. Hoelder, S (2022) Optimizing Shape Complementarity Enables the Discovery of Potent Tricyclic BCL6 Inhibitors.. Show Abstract full text

To identify new chemical series with enhanced binding affinity to the BTB domain of B-cell lymphoma 6 protein, we targeted a subpocket adjacent to Val18. With no opportunities for strong polar interactions, we focused on attaining close shape complementarity by ring fusion onto our quinolinone lead series. Following exploration of different sized rings, we identified a conformationally restricted core which optimally filled the available space, leading to potent BCL6 inhibitors. Through X-ray structure-guided design, combined with efficient synthetic chemistry to make the resulting novel core structures, a >300-fold improvement in activity was obtained by the addition of seven heavy atoms.

Harnden, A.C. Davis, O.A. Box, G.M. Hayes, A. Johnson, L.D. Henley, A.T. de Haven Brandon, A.K. Valenti, M. Cheung, K.-.M.J. Brennan, A. Huckvale, R. Pierrat, O.A. Talbot, R. Bright, M.D. Akpinar, H.A. Miller, D.S.J. Tarantino, D. Gowan, S. de Klerk, S. McAndrew, P.C. Le Bihan, Y.-.V. Meniconi, M. Burke, R. Kirkin, V. van Montfort, R.L.M. Raynaud, F.I. Rossanese, O.W. Bellenie, B.R. Hoelder, S (2023) Discovery of an <i>In Vivo</i> Chemical Probe for BCL6 Inhibition by Optimization of Tricyclic Quinolinones.. Show Abstract full text

B-cell lymphoma 6 (BCL6) is a transcriptional repressor and oncogenic driver of diffuse large B-cell lymphoma (DLBCL). Here, we report the optimization of our previously reported tricyclic quinolinone series for the inhibition of BCL6. We sought to improve the cellular potency and <i>in vivo</i> exposure of the non-degrading isomer, <b>CCT373567</b>, of our recently published degrader, <b>CCT373566</b>. The major limitation of our inhibitors was their high topological polar surface areas (TPSA), leading to increased efflux ratios. Reducing the molecular weight allowed us to remove polarity and decrease TPSA without considerably reducing solubility. Careful optimization of these properties, as guided by pharmacokinetic studies, led to the discovery of <b>CCT374705</b>, a potent inhibitor of BCL6 with a good <i>in vivo</i> profile. Modest <i>in vivo</i> efficacy was achieved in a lymphoma xenograft mouse model after oral dosing.

Mannion, J. Gifford, V. Bellenie, B. Fernando, W. Ramos Garcia, L. Wilson, R. John, S.W. Udainiya, S. Patin, E.C. Tiu, C. Smith, A. Goicoechea, M. Craxton, A. Moraes de Vasconcelos, N. Guppy, N. Cheung, K.-.M.J. Cundy, N.J. Pierrat, O. Brennan, A. Roumeliotis, T.I. Benstead-Hume, G. Alexander, J. Muirhead, G. Layzell, S. Lyu, W. Roulstone, V. Allen, M. Baldock, H. Legrand, A. Gabel, F. Serrano-Aparicio, N. Starling, C. Guo, H. Upton, J. Gyrd-Hansen, M. MacFarlane, M. Seddon, B. Raynaud, F. Roxanis, I. Harrington, K. Haider, S. Choudhary, J.S. Hoelder, S. Tenev, T. Meier, P (2024) A RIPK1-specific PROTAC degrader achieves potent antitumor activity by enhancing immunogenic cell death.. Show Abstract full text

Receptor-interacting serine/threonine-protein kinase 1 (RIPK1) functions as a critical stress sentinel that coordinates cell survival, inflammation, and immunogenic cell death (ICD). Although the catalytic function of RIPK1 is required to trigger cell death, its non-catalytic scaffold function mediates strong pro-survival signaling. Accordingly, cancer cells can hijack RIPK1 to block necroptosis and evade immune detection. We generated a small-molecule proteolysis-targeting chimera (PROTAC) that selectively degraded human and murine RIPK1. PROTAC-mediated depletion of RIPK1 deregulated TNFR1 and TLR3/4 signaling hubs, accentuating the output of NF-κB, MAPK, and IFN signaling. Additionally, RIPK1 degradation simultaneously promoted RIPK3 activation and necroptosis induction. We further demonstrated that RIPK1 degradation enhanced the immunostimulatory effects of radio- and immunotherapy by sensitizing cancer cells to treatment-induced TNF and interferons. This promoted ICD, antitumor immunity, and durable treatment responses. Consequently, targeting RIPK1 by PROTACs emerges as a promising approach to overcome radio- or immunotherapy resistance and enhance anticancer therapies.

Liu, M. Mirza, A. McAndrew, P.C. Thapaliya, A. Pierrat, O.A. Stubbs, M. Hahner, T. Chessum, N.E.A. Innocenti, P. Caldwell, J. Cheeseman, M.D. Bellenie, B.R. van Montfort, R.L.M. Newton, G.K. Burke, R. Collins, I. Hoelder, S (2023) Determination of Ligand-Binding Affinity (<i>K</i><sub>d</sub>) Using Transverse Relaxation Rate (<i>R</i><sub>2</sub>) in the Ligand-Observed <sup>1</sup>H NMR Experiment and Applications to Fragment-Based Drug Discovery.. Show Abstract full text

High hit rates from initial ligand-observed NMR screening can make it challenging to prioritize which hits to follow up, especially in cases where there are no available crystal structures of these hits bound to the target proteins or other strategies to provide affinity ranking. Here, we report a reproducible, accurate, and versatile quantitative ligand-observed NMR assay, which can determine <i>K</i><sub>d</sub> values of fragments in the affinity range of low μM to low mM using transverse relaxation rate <i>R</i><sub>2</sub> as the observable parameter. In this study, we examined the theory and proposed a mathematical formulation to obtain <i>K</i><sub>d</sub> values using non-linear regression analysis. We designed an assay format with automated sample preparation and simplified data analysis. Using tool compounds, we explored the assay reproducibility, accuracy, and detection limits. Finally, we used this assay to triage fragment hits, yielded from fragment screening against the CRBN/DDB1 complex.

Pierrat, O.A. Liu, M. Collie, G.W. Shetty, K. Rodrigues, M.J. Le Bihan, Y.-.V. Gunnell, E.A. McAndrew, P.C. Stubbs, M. Rowlands, M.G. Yahya, N. Shehu, E. Talbot, R. Pickard, L. Bellenie, B.R. Cheung, K.-.M.J. Drouin, L. Innocenti, P. Woodward, H. Davis, O.A. Lloyd, M.G. Varela, A. Huckvale, R. Broccatelli, F. Carter, M. Galiwango, D. Hayes, A. Raynaud, F.I. Bryant, C. Whittaker, S. Rossanese, O.W. Hoelder, S. Burke, R. van Montfort, R.L.M (2022) Discovering cell-active BCL6 inhibitors: effectively combining biochemical HTS with multiple biophysical techniques, X-ray crystallography and cell-based assays.. Show Abstract full text

By suppressing gene transcription through the recruitment of corepressor proteins, B-cell lymphoma 6 (BCL6) protein controls a transcriptional network required for the formation and maintenance of B-cell germinal centres. As BCL6 deregulation is implicated in the development of Diffuse Large B-Cell Lymphoma, we sought to discover novel small molecule inhibitors that disrupt the BCL6-corepressor protein-protein interaction (PPI). Here we report our hit finding and compound optimisation strategies, which provide insight into the multi-faceted orthogonal approaches that are needed to tackle this challenging PPI with small molecule inhibitors. Using a 1536-well plate fluorescence polarisation high throughput screen we identified multiple hit series, which were followed up by hit confirmation using a thermal shift assay, surface plasmon resonance and ligand-observed NMR. We determined X-ray structures of BCL6 bound to compounds from nine different series, enabling a structure-based drug design approach to improve their weak biochemical potency. We developed a time-resolved fluorescence energy transfer biochemical assay and a nano bioluminescence resonance energy transfer cellular assay to monitor cellular activity during compound optimisation. This workflow led to the discovery of novel inhibitors with respective biochemical and cellular potencies (IC<sub>50s</sub>) in the sub-micromolar and low micromolar range.

Morley, A.D. Pugliese, A. Birchall, K. Bower, J. Brennan, P. Brown, N. Chapman, T. Drysdale, M. Gilbert, I.H. Hoelder, S. Jordan, A. Ley, S.V. Merritt, A. Miller, D. Swarbrick, M.E. Wyatt, P.G (2013) Fragment-based hit identification: thinking in 3D. full text