Discovery of a Hepatitis C Virus NS5B Replicase Palm Site Allosteric Inhibitor (BMS-929075) Advanced to Phase 1 Clinical Studies.

The hepatitis C virus (HCV) NS5B replicase is a prime target for the development of direct-acting antiviral drugs for the treatment of chronic HCV infection. Inspired by the overlay of bound structures of three structurally distinct NS5B palm site allosteric inhibitors, the high-throughput screening hit anthranilic acid 4, the known benzofuran analogue 5, and the benzothiadiazine derivative 6, an optimization process utilizing the simple benzofuran template 7 as a starting point for a fragment growing approach was pursued. A delicate balance of molecular properties achieved via disciplined lipophilicity changes was essential to achieve both high affinity binding and a stringent targeted absorption, distribution, metabolism, and excretion profile. These efforts led to the discovery of BMS-929075 (37), which maintained ligand efficiency relative to early leads, demonstrated efficacy in a triple combination regimen in HCV replicon cells, and exhibited consistently high oral bioavailability and pharmacokinetic parameters across preclinical animal species. The human PK properties from the Phase I clinical studies of 37 were better than anticipated and suggest promising potential for QD administration.

[1]  N. Habuka,et al.  Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus. , 1999, Structure.

[2]  Brett A Tounge,et al.  The role of molecular size in ligand efficiency. , 2007, Bioorganic & medicinal chemistry letters.

[3]  F. Rey,et al.  Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Jennifer L. Knight,et al.  OPLS3: A Force Field Providing Broad Coverage of Drug-like Small Molecules and Proteins. , 2016, Journal of chemical theory and computation.

[5]  F. Kesisoglou,et al.  Amorphous Solid Dispersions or Prodrugs: Complementary Strategies to Increase Drug Absorption. , 2016, Journal of pharmaceutical sciences.

[6]  J. Feld,et al.  Direct-acting antiviral agents for hepatitis C: structural and mechanistic insights , 2016, Nature Reviews Gastroenterology &Hepatology.

[7]  Nicholas A Meanwell,et al.  2015 Philip S. Portoghese Medicinal Chemistry Lectureship. Curing Hepatitis C Virus Infection with Direct-Acting Antiviral Agents: The Arc of a Medicinal Chemistry Triumph. , 2016, Journal of medicinal chemistry.

[8]  M. Waring,et al.  A quantitative assessment of hERG liability as a function of lipophilicity. , 2007, Bioorganic & medicinal chemistry letters.

[9]  C. Rice,et al.  Understanding the hepatitis C virus life cycle paves the way for highly effective therapies , 2013, Nature Medicine.

[10]  Qi Gao,et al.  The discovery of asunaprevir (BMS-650032), an orally efficacious NS3 protease inhibitor for the treatment of hepatitis C virus infection. , 2014, Journal of medicinal chemistry.

[11]  M. Houghton,et al.  Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. , 1989, Science.

[12]  Wonsuk Chang,et al.  Nucleoside, nucleotide, and non-nucleoside inhibitors of hepatitis C virus NS5B RNA-dependent RNA-polymerase. , 2012, Journal of medicinal chemistry.

[13]  Christian Laurence,et al.  The pK(BHX) database: toward a better understanding of hydrogen-bond basicity for medicinal chemists. , 2009, Journal of medicinal chemistry.

[14]  Emanuele Perola,et al.  An analysis of the binding efficiencies of drugs and their leads in successful drug discovery programs. , 2010, Journal of medicinal chemistry.

[15]  M. Congreve,et al.  Recent developments in fragment-based drug discovery. , 2008, Journal of medicinal chemistry.

[16]  N. Meanwell,et al.  Discovery of daclatasvir, a pan-genotypic hepatitis C virus NS5A replication complex inhibitor with potent clinical effect. , 2014, Journal of medicinal chemistry.

[17]  J. Lemm,et al.  Potency and Resistance Analysis of Hepatitis C Virus NS5B Polymerase Inhibitor BMS-791325 on All Major Genotypes , 2014, Antimicrobial Agents and Chemotherapy.

[18]  N. Meanwell A Synopsis of the Properties and Applications of Heteroaromatic Rings in Medicinal Chemistry , 2017 .

[19]  B. Beno,et al.  Discovery and initial optimization of alkoxyanthranilic acid derivatives as inhibitors of HCV NS5B polymerase. , 2017, Bioorganic & medicinal chemistry letters.

[20]  M. D. Hill,et al.  Applications of Fluorine in Medicinal Chemistry. , 2015, Journal of medicinal chemistry.

[21]  C. Rice,et al.  Expanded Classification of Hepatitis C Virus Into 7 Genotypes and 67 Subtypes: Updated Criteria and Genotype Assignment Web Resource , 2013, Hepatology.

[22]  Paul Seiler,et al.  A fluorine scan of thrombin inhibitors to map the fluorophilicity/fluorophobicity of an enzyme active site: evidence for C-F...C=O interactions. , 2003, Angewandte Chemie.

[23]  Julian E. Fuchs,et al.  Matched molecular pair analysis: significance and the impact of experimental uncertainty. , 2014, Journal of medicinal chemistry.

[24]  Daniel M. Lowe,et al.  ADMET rules of thumb II: A comparison of the effects of common substituents on a range of ADMET parameters. , 2009, Bioorganic & medicinal chemistry.

[25]  A. Hopkins,et al.  The role of ligand efficiency metrics in drug discovery , 2014, Nature Reviews Drug Discovery.

[26]  B. Beno,et al.  The discovery of a pan-genotypic, primer grip inhibitor of HCV NS5B polymerase. , 2017, MedChemComm.

[27]  S. Bembenek,et al.  Ligand binding efficiency: trends, physical basis, and implications. , 2008, Journal of medicinal chemistry.

[28]  T. Ritchie,et al.  Heterocyclic replacements for benzene: Maximising ADME benefits by considering individual ring isomers. , 2016, European journal of medicinal chemistry.

[29]  Stephen R. Johnson,et al.  Estimation of hERG inhibition of drug candidates using multivariate property and pharmacophore SAR. , 2007, Bioorganic & medicinal chemistry.

[30]  R. Chopra,et al.  Molecular Mechanism of Hepatitis C Virus Replicon Variants with Reduced Susceptibility to a Benzofuran Inhibitor, HCV-796 , 2008, Antimicrobial Agents and Chemotherapy.

[31]  D. Douglas,et al.  HCV796: A selective nonstructural protein 5B polymerase inhibitor with potent anti‐hepatitis C virus activity In Vitro, in mice with chimeric human livers, and in humans infected with hepatitis C virus , 2009, Hepatology.

[32]  R. Hamatake,et al.  Discovery of a potent boronic acid derived inhibitor of the HCV RNA-dependent RNA polymerase. , 2014, Journal of medicinal chemistry.

[33]  P. Beaulieu,et al.  Non-nucleoside inhibitors of the HCV NS5B polymerase: progress in the discovery and development of novel agents for the treatment of HCV infections. , 2007, Current opinion in investigational drugs.

[34]  A. Hopkins,et al.  Ligand efficiency: a useful metric for lead selection. , 2004, Drug discovery today.

[35]  Dashyant Dhanak,et al.  Substituted benzothiadizine inhibitors of Hepatitis C virus polymerase. , 2009, Bioorganic & medicinal chemistry letters.

[36]  P. Lam,et al.  Achieving structural diversity using the perpendicular conformation of alpha-substituted phenylcyclopropanes to mimic the bioactive conformation of ortho-substituted biphenyl P4 moieties: discovery of novel, highly potent inhibitors of Factor Xa. , 2008, Bioorganic & medicinal chemistry letters.

[37]  N. Meanwell Improving drug candidates by design: a focus on physicochemical properties as a means of improving compound disposition and safety. , 2011, Chemical research in toxicology.

[38]  Ralf Bartenschlager,et al.  The molecular and structural basis of advanced antiviral therapy for hepatitis C virus infection , 2013, Nature Reviews Microbiology.

[39]  J. Tomasi,et al.  Quantum mechanical continuum solvation models. , 2005, Chemical reviews.

[40]  Christopher E. Keefer,et al.  Fluorine multipolar interaction: Toward elucidating its energetics in binding recognition , 2017 .

[41]  P. Hajduk Fragment-based drug design: how big is too big? , 2006, Journal of medicinal chemistry.

[42]  Charles A. Lesburg,et al.  Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site , 1999, Nature Structural Biology.

[43]  April Wong,et al.  Slow Binding Inhibition and Mechanism of Resistance of Non-nucleoside Polymerase Inhibitors of Hepatitis C Virus , 2009, The Journal of Biological Chemistry.