Advantages of crystallographic fragment screening: Functional and mechanistic insights from a powerful platform for efficient drug discovery

Progress in Biophysics and Molecular Biology

Volumn 116, Issue 2-3, 2014, Pages 92-100

  Patel, Disha ^a   Bauman, Joseph D ^a   Arnold, Eddy ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

BpGCDH; DHNA; DMSO; FBDD; Fragment screening; HCV; HIV; Influenza; NMR; NNRTI; PAN; PR; RT; TMAO; TS; X ray crystallography

Indexed keywords

HEPATITIS C VIRUS;

PROTEIN;

CHEMISTRY; DRUG SCREENING; METABOLISM; PROCEDURES; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; DRUG EVALUATION, PRECLINICAL; PROTEINS;

EID: 84924040633     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2014.08.004     Document Type: Article

References (44)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., McCoy A.J., Moriarty N.W., Oeffner R., Read R.J., Richardson D.C., Richardson J.S., Terwilliger T.C., Zwart P.H. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr. Sect. D. Biol. Crystallogr. 2010, 66:213-221.
2. Allen K.N., Bellamacina C.R., Ding X., Jeffery C.J., Mattos C., Petsko G.A., Ringe D. An experimental approach to mapping the binding surfaces of crystalline proteins. J.Phys. Chem. 1996, 100:2605-2611.
3. Atwell S., Brouillette C.G., Conners K., Emtage S., Gheyi T., Guggino W.B., et al. Structures of a minimal human CFTR first nucleotide-binding domain as a monomer, head-to-tail homodimer, and pathogenic mutant. Protein Eng. Des. Sel. 2010, 23:375-384.
4. Bauman J.D., Das K., Ho W.C., Baweja M., Himmel D.M., Clark A.D., Oren D.A., Boyer P.L., Hughes S.H., Shatkin A.J., Arnold E. Crystal engineering of HIV-1 reverse transcriptase for structure-based drug design. Nucleic Acids Res. 2008, 36:5083-5092.
5. Bauman J.D., Patel D., Baker S., Vijayan R.S.K., Xiang A., Parhi A., Martinez-Sobrido L., LaVoie E.J., Das K., Arnold E. Crystallographic fragment screening and structure-based optimization yields a new class of influenza endonuclease inhibitors. ACS Chem. Biol. 2013, 8:2501-2508.
6. Bauman J., Patel D., Dharia C., Fromer M.W., Ahmed S., Frenkel Y., Vijayan R.S.K., Eck T.J., Ho W.C., Das K., Shatkin A.J., Arnold E. Detecting allosteric sites of HIV-1 reverse transcriptase by X-ray crystallographic fragment screening. J.Med. Chem. 2013, 56:2738-2746.
7. Begley D.W., Davies D.R., Hartley R.C., Hewitt S.N., Rychel A.L., Myler P.J., Van Voorhis W.C., Staker B.L., Stewart L.J. Probing conformation stats of glutaryl-CoA dehydrogenase by fragment screening. Acta Crystallogr. Sect. F. 2011, 67:1060-1069.
8. Behnen J., Köster H., Neudert G., Craan T., Heine A., Klebe G. Experimental and computational active site mapping as a starting point to fragment-based lead discovery. ChemMedChem 2012, 7:248-261.
9. Blaney J., Nienaber V., Burley S.K. Fragment-based lead discovery and optimisation using X- ray crystallography, computational chemistry, and high-throughput organic synthesis. Methods and Principles in Medicinal Chemistry 2006, 215-248. Wiley-VCH, Weinheim, Germany. W. Jahnke, D.A. Erlanson (Eds.).
10. Blundell T.L., Jhoti H., Abell C. High-throughput crystallography for lead discovery in drug design. Nat. Rev. Drug. Discov. 2002, 1:45-54.
11. Dalvit C., Flocco M., Veronesi M., Stockman B.J. Fluorine-NMR competition binding experiments for high-throughput screening of large compound mixtures. Comb. Chem. High. Throughput Screen. 2002, 5:605-611.
12. Davies T.G., Tickle I.J. Fragment screening using X-ray crystallography. Top. Curr. Chem. 2012, 317:33-59.
13. Dias A., Bouvier D., Crepin T., McCarthy A.A., Hart D.J., Baudin F., Cusack S., Ruigrok R.W. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 2009, 458:914-918.
14. English A.C., Done S.H., Caves L.S., Groom C.R., Hubbard R.E. Locating interaction sites on proteins: the crystal structure of thermolysin soaked in 2% to 100% isopropanol. Proteins: Struct. Funct. Genet. 1999, 37:628-640.
15. Erlanson D.A., Wells J.A., Braisted A.C. Tethering: fragment-based drug discovery. Annu. Rev. Biophys. Biomol. Struct. 2004, 33:199-223.
16. Flocco M.M., Mowbray S.L. Planar stacking interactions of arginine and aromatic-side chains in proteins. J.Mol. Biol. 1994, 235:709-717.
17. Hadjuk P.J., Greer J. Adecade of fragment-based drug design: strategic advances and lessons learned. Nat. Rev. Drug. Discov. 2007, 6:211-219.
18. Hartshorn M.J., Murray C.W., Cleasby A., Frederickson M., Tickle I.J., Jhoti H. Fragment-based lead discovery using X-ray crystallography. J.Med. Chem. 2005, 48:403-413.
19. Henrich B., Bergamaschi A., Broennimann C., Dinapoli R., Eikenberry E.F., Johnson I., Kobas M., Kraft P., Mozzanica A., Schmitt B. PILATUS: a single photon counting pixel detector for X-ray applications. Nucl. Instrum. Methods Phys. Res. Sect. 2009, 607:247-249.
20. Hesterkamp T., Whittaker M. Fragment-based activity space: smaller is better. Curr. Opin. Chem. Biol. 2008, 12:260-268.
21. Horton N.C., Perona J.J. DNA cleavage by EcoRV endonuclease: two metal ions in three metal ion binding sites. Biochemistry 2004, 43:6841-6857.
22. Kuroda D.G., Bauman J.D., Challa R., Patel D., Troxler T., Das K., Arnold E., Hochstrasser R.M. Snapshot of the equilibrium dynamics of a drug bound to HIV-1 reverse transcriptase. Nat. Chem. 2013, 5:174-181.
23. Lin T.Y., Timasheff S.N. Why do some organisms use a urea-methylamine mixture as osmolyte? Thermodynamic compensation of urea and trimethylamine N-oxide interactions with protein. Biochemistry 1994, 33:12695-12701.
24. Mattos C., Bellamacina C.R., Peisach E., Pereira A., Vitkup D., Petsko G.A., Ringe D. Multiple solvent crystal structures: probing binding sites, plasticity, and hydration. J.Mol. Biol. 2006, 57:1471-1482.
25. Mattos C., Ringe D. Locating and characterizing binding sites on proteins. Nat. Biotechnol. 1996, 14:595-599.
26. Mueller-Dieckmann C., Kauffmann B., Weiss M.S. Trimethylamine N-oxide as a versatile cryoprotective agent in macromolecular crystallography. J.Appl. Crystallogr. 2011, 44:433-436.
27. Nienaber V.L., Richardson P.L., Klighofer V., Bouska J.J., Giranda V.L., Greer J. Discovering novel ligands for macromolecules using X-ray crystallographic screening. Nat. Biotechnol. 2000, 18:1105-1108.
28. Perryman A.L., Zhang Q., Soutter H.H., Rosenfeld R., McRee D.E., Olson A.J., Elder J.E., Stout C.D. Fragment-based screen against HIV protease. Chem. Biol. Drug. Des. 2010, 75:257-268.
29. Saalau-Bethell S., Woodhead A.J., Chessari G., Carr M.G., Coyle J., Graham B., Hiscock S.D., Murray C.W., Pathuri P., Rich S.J., Richardson C.J., Williams P.A., Jhoti H. Discovery of an allosteric mechanism for the regulation of HCV NS3 protein function. Nat. Chem. Biol. 2012, 8:920-925.
30. Sanders W.J., Nienaber V.L., Lerner C.G., McCall J.O., Merrick S.M., Swanson S.J., Harlan J.E., Stoll V.S., Stamper G.F., Betz S.F., Condroski K.R., Meadows R.P., Severin J.M., Walter K.A., Magdalinos P., Jakob C.G., Wagner R., Beutel B.A. Discovery of potent inhibitors of dihydroneopterin aldolase using CrystaLEAD high-throughput X-ray crystallographic screening and structure-directed lead optimization. J.Med. Chem. 2004, 47:1709-1718.
31. Shin G., Yost S.A., Miller M.T., Elrod E.J., Grakoui A., Marcotrigiano J. Structural and functional insights into alphavirus polyprotein processing and pathogenesis. Proc. Natl. Acad. Sci. USA 2012, 109:16534-16539.
32. Shumlin I.A., Cymborowski M., Chertihin O., Jha K.N., Herr J.C., Lesley S.A., Joachimiak A., Minor W. Identification of unknown protein function using metabolite cocktail screening. Structure 2012, 20:1715-1725.
33. Spurlino J.C. Fragment screening purely with protein crystallography. Methods Enzym. 2011, 493:321-356.
34. Stout T.J., Schellenber U., Santi D.V., Stroud R.M. Crystal structures of a unique thermal-stable thymidylate synthase from Bacillus subtilis. Biochemistry 1998, 37:14736-14747.
35. Tiefenbrunn T., Forli S., Happer M., Gonzalez A., Tsai Y., Soltis M., Elder J.H., Olson A.J., Stout C.D. Crystallographic fragment-based drug discovery: use of a brominated fragment library targeting HIV protease. Chem. Biol. Drug. Des. 2013, 83:141-148.
36. Verlinde C.L.M.J., Fan E., Shibata S., Zhang Z., Sun Z., Deng W., Ross J., Kim J., Xiao L., Arakaki T., Bosch J., Caruthers J.M., Larson E.T., LeTrong I., Napuli A., Kelley A., Mueller N., Zucker F., Van Voorhis W.C., Buckner F.S., Merritt E.A., Hol W.G.J. Fragment-based cocktail crystallography by the medical structural genomics of pathogenic protozoa consortium. Curr. Top. Med. Chem. 2009, 9:1678-1687.
37. Verlinde C., Kim H., Bernstein B.E., Mande S.C., Hol W.G.J. Antitrypanosomiasis drug development based on structures of glycolytic enzymes. Structure-based Drug Design 1997, 365-394. Marcel Dekker, Inc. P. Veerapandian (Ed.).
38. Wang A., Bolen D.W. Anaturally occurring protective system in urea-rich cells: mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry 1997, 36:9101-9108.
39. Wilcken R., Liu X., Zimmermann M.O., Rutherford T.J., Fersht A.R., Joerger A.C., Boeckler F.M. Halogenated-enriched fragment libraries as leads for drug rescue of mutant p53. J.Am. Chem. Soc. 2012, 134:6810-6818.
40. Winn M.D., Ballard C.C., Cowtan K.D., Dodson E.J., Emsley P., Evans P.R., et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. Sect. D. Biol. Crystallogr. 2011, 67:235-242.
41. Yancey P.H., Clark M.E., Hand S.C., Bowlus R.D., Somero G.N. Living with water stress: evolution of osmolyte systems. Science 1982, 217:1214-1222.
42. Yancey P.H., Somero G.N. Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes. Biochem. J. 1979, 183:317-323.
43. Yuan P., Bartlam M., Lou Z., Chen S., Zhou J., He X., Lv Z., Ge R., Li X., Deng T., Fodor E., Rao Z., Liu Y. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 2009, 458:909-913.
44. Zou Q., Bennion B.J., Daggett V., Murphy K.P. The molecular mechanism of stabilization of proteins by TMAO and its ability to counteract the effects of urea. J.Am. Chem. Soc. 2002, 124:1192-1202.