From fragment to clinical candidate--a historical perspective.

As recently as ten years ago few scientists had heard of fragment screening, let alone considered low molecular weight fragments (MW <300) with weak binding affinities to be attractive start points for drug discovery programmes. Today, however, there is widespread acceptance that these fragments can be progressed into lead series and on to become clinical candidates. Consequently, over the past three to four years, fragment-based drug discovery has become firmly established within the biotechnology and pharmaceutical industries as a complimentary strategy to high-throughput screening. In this review, we give a historical perspective of how rapidly fragment-based drug discovery has developed and describe a number of clinical compounds discovered using this approach.

[1]  T. J. R. Harris High throughput X-ray crystallography for Drug Discovery , 2000 .

[2]  David G Myszka,et al.  Structure-activity analysis of the purine binding site of human liver glycogen phosphorylase. , 2002, Chemistry & biology.

[3]  T. Blundell,et al.  Structural biology and drug discovery. , 2005, Drug discovery today.

[4]  Paul G Wyatt,et al.  Detection of ligands from a dynamic combinatorial library by X-ray crystallography. , 2003, Angewandte Chemie.

[5]  David J. Craik,et al.  FUNCTIONAL GROUP CONTRIBUTIONS TO DRUG-RECEPTOR INTERACTIONS , 1985 .

[6]  R. Stroud,et al.  Site-directed ligand discovery. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Saul H Rosenberg,et al.  Discovery of an orally bioavailable small molecule inhibitor of prosurvival B-cell lymphoma 2 proteins. , 2008, Journal of medicinal chemistry.

[8]  Gianni Chessari,et al.  Application of fragment-based lead generation to the discovery of novel, cyclic amidine beta-secretase inhibitors with nanomolar potency, cellular activity, and high ligand efficiency. , 2007, Journal of medicinal chemistry.

[9]  D. Fattori,et al.  The fragment-approach: An update , 2006 .

[10]  Gerard J Kleywegt,et al.  Application and limitations of X-ray crystallographic data in structure-based ligand and drug design. , 2003, Angewandte Chemie.

[11]  Phillip Gribbon,et al.  High-throughput drug discovery: what can we expect from HTS? , 2005, Drug discovery today.

[12]  P. Leeson,et al.  The influence of drug-like concepts on decision-making in medicinal chemistry , 2007, Nature Reviews Drug Discovery.

[13]  Tudor I. Oprea,et al.  The Design of Leadlike Combinatorial Libraries. , 1999, Angewandte Chemie.

[14]  M. Uesugi,et al.  [Discovering high-affinity ligands for proteins: SAR by NMR]. , 2007, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[15]  R. Hertzberg,et al.  High-throughput screening: new technology for the 21st century. , 2000, Current opinion in chemical biology.

[16]  Dustin J Maly,et al.  Combinatorial target-guided ligand assembly: identification of potent subtype-selective c-Src inhibitors. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Vicki L. Nienaber,et al.  Discovering novel ligands for macromolecules using X-ray crystallographic screening , 2000, Nature Biotechnology.

[18]  J. T. Metz,et al.  Ligand efficiency indices as guideposts for drug discovery. , 2005, Drug discovery today.

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

[20]  M. Congreve,et al.  A 'rule of three' for fragment-based lead discovery? , 2003, Drug discovery today.

[21]  T. Hesterkamp,et al.  Fragment based drug discovery using fluorescence correlation: spectroscopy techniques: challenges and solutions. , 2007, Current topics in medicinal chemistry.

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

[23]  J. Laurence,et al.  High-field solution NMR spectroscopy as a tool for assessing protein interactions with small molecule ligands. , 2008, Journal of Pharmacy and Science.

[24]  Christopher W. Murray,et al.  Entropic Consequences of Linking Ligands , 2006 .

[25]  Ajay,et al.  The SHAPES strategy: an NMR-based approach for lead generation in drug discovery. , 1999, Chemistry & biology.

[26]  Bohdan Waszkowycz,et al.  PRO_SELECT: combining structure-based drug design and array-based chemistry for rapid lead discovery. 2. The development of a series of highly potent and selective factor Xa inhibitors. , 2002, Journal of medicinal chemistry.

[27]  Christopher W Murray,et al.  Fragment-based lead discovery using X-ray crystallography. , 2005, Journal of medicinal chemistry.

[28]  Alexander A Alex,et al.  Fragment-based drug discovery: what has it achieved so far? , 2007, Current topics in medicinal chemistry.

[29]  Glyn Williams,et al.  Fragment-based screening using X-ray crystallography and NMR spectroscopy. , 2007, Current opinion in chemical biology.

[30]  W. Guida,et al.  The art and practice of structure‐based drug design: A molecular modeling perspective , 1996, Medicinal research reviews.

[31]  I. Kuntz,et al.  The maximal affinity of ligands. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Marcel L Verdonk,et al.  Automated Protein–Ligand Crystallography for Structure‐Based Drug Design , 2006, ChemMedChem.

[33]  Paul G Wyatt,et al.  Identification of N-(4-piperidinyl)-4-(2,6-dichlorobenzoylamino)-1H-pyrazole-3-carboxamide (AT7519), a novel cyclin dependent kinase inhibitor using fragment-based X-ray crystallography and structure based drug design. , 2008, Journal of medicinal chemistry.

[34]  Gebhard F. X. Schertler,et al.  Structure of a β1-adrenergic G-protein-coupled receptor , 2008, Nature.

[35]  Karl A. Walter,et al.  ChemInform Abstract: Discovery of Potent Nonpeptide Inhibitors of Stromelysin Using SAR by NMR. , 1997 .

[36]  David J. Newman Natural Products as Leads to Potential Drugs: An Old Process or the New Hope for Drug Discovery? , 2008 .

[37]  C L Verlinde,et al.  Structure-based drug design: progress, results and challenges. , 1994, Structure.

[38]  Leland J. Gershell,et al.  A brief history of novel drug discovery technologies , 2003, Nature Reviews Drug Discovery.

[39]  P. Goodford A computational procedure for determining energetically favorable binding sites on biologically important macromolecules. , 1985, Journal of medicinal chemistry.

[40]  Shenghua Shi,et al.  Scaffold-based discovery of indeglitazar, a PPAR pan-active anti-diabetic agent , 2009, Proceedings of the National Academy of Sciences.

[41]  Alan L Harvey,et al.  Natural products in drug discovery. , 2008, Drug discovery today.

[42]  M. Ziebell,et al.  Affinity selection-mass spectrometry screening techniques for small molecule drug discovery. , 2007, Current opinion in chemical biology.

[43]  D. Kostrewa,et al.  Novel inhibitors of DNA gyrase: 3D structure based biased needle screening, hit validation by biophysical methods, and 3D guided optimization. A promising alternative to random screening. , 2000, Journal of medicinal chemistry.

[44]  P. Hajduk,et al.  A decade of fragment-based drug design: strategic advances and lessons learned , 2007, Nature Reviews Drug Discovery.

[45]  Wim G. J. Hol,et al.  In search of new lead compounds for trypanosomiasis drug design: A protein structure-based linked-fragment approach , 1992, J. Comput. Aided Mol. Des..

[46]  Tom L. Blundell,et al.  Keynote review: Structural biology and drug discovery , 2005 .

[47]  Andrew R. Leach,et al.  Molecular Complexity and Its Impact on the Probability of Finding Leads for Drug Discovery , 2001, J. Chem. Inf. Comput. Sci..

[48]  T Neumann,et al.  SPR-based fragment screening: advantages and applications. , 2007, Current topics in medicinal chemistry.

[49]  Andrew J. Sharff HIGH THROUGHPUT CRYSTALLOGRAPHY ON AN IN-HOUSE SOURCE, USING ACTOR , 2003 .

[50]  A. Dmitrienko,et al.  A phase II study of the oral factor Xa inhibitor LY517717 for the prevention of venous thromboembolism after hip or knee replacement , 2007, Journal of thrombosis and haemostasis : JTH.

[51]  Alastair Binnie,et al.  Case study: impact of technology investment on lead discovery at Bristol-Myers Squibb, 1998-2006. , 2008, Drug discovery today.

[52]  P. Taylor,et al.  Click chemistry in situ: acetylcholinesterase as a reaction vessel for the selective assembly of a femtomolar inhibitor from an array of building blocks. , 2002, Angewandte Chemie.

[53]  Marcel L. Verdonk,et al.  The consequences of translational and rotational entropy lost by small molecules on binding to proteins , 2002, J. Comput. Aided Mol. Des..

[54]  Jean-Louis Reymond,et al.  Virtual exploration of the small-molecule chemical universe below 160 Daltons. , 2005, Angewandte Chemie.

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

[56]  W. Jencks,et al.  On the attribution and additivity of binding energies. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[57]  F. Lombardo,et al.  Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. , 2001, Advanced drug delivery reviews.

[58]  Tudor I. Oprea,et al.  Is There a Difference between Leads and Drugs? A Historical Perspective , 2001, J. Chem. Inf. Comput. Sci..

[59]  D. Erlanson Fragment-based lead discovery: a chemical update. , 2006, Current opinion in biotechnology.

[60]  Stefan Knapp,et al.  NMR-Based screening with competition water-ligand observed via gradient spectroscopy experiments: detection of high-affinity ligands. , 2002, Journal of medicinal chemistry.

[61]  Gerard J Kleywegt,et al.  Limitations and lessons in the use of X-ray structural information in drug design , 2008, Drug Discovery Today.