Protein crystallography and fragment-based drug design

Future Medicinal Chemistry

Volumn 5, Issue 10, 2013, Pages 1121-1140

  Caliandro, Rocco ^a   Belviso, Danilo Benny ^a   Aresta, Brunella Maria ^a   De Candia, Modesto ^b   Altomare, Cosimo Damiano ^a  

^a CNR   (Italy)

^b UNIVERSITY OF BARI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; CYSTEINE; GALECTIN; MEMBRANE PROTEIN; MOLECULAR SCAFFOLD; SILICON; VEMURAFENIB;

BINDING AFFINITY; COCKTAIL CRYSTALLOGRAPHY; COMPUTER PROGRAM; CONFORMATIONAL TRANSITION; CRYSTALLIZATION; CRYSTALLOGRAPHY; DIFFRACTION; DISULFIDE BOND; DRUG DESIGN; ELECTRON TRANSPORT; FOURIER TRANSFORMATION; HIGH THROUGHPUT SCREENING; HYDROGEN BOND; INFORMATION PROCESSING; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MATHEMATICAL COMPUTING; PH; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN STRUCTURE; REPRODUCIBILITY; REVIEW; SOLUBILITY; SYNCHROTRON; TEMPERATURE; WATER TRANSPORT; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

BINDING SITES; CARBOHYDRATES; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; ENZYME INHIBITORS; FRUCTOKINASES; HUMANS; MOLECULAR DYNAMICS SIMULATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEINS; TRYPSIN;

EID: 84879676139     PISSN: 17568919     EISSN: 17568927     Source Type: Journal    
DOI: 10.4155/fmc.13.84     Document Type: Review

References (95)

1. Newby ZE, O'Connell JD, Gruswitz F et al. A general protocol for the crystallization of membrane proteins for X-ray structural investigation. Nat. Protoc. 4, 619-637 (2009).
2. Snook CF, Purdy MD, Wiener MC. Use of a crystallization robot to set up sitting-drop vapor-diffusion crystallization and in situ crystallization screens. J. Appl. Crystallogr. 33, 344-349 (2000). (Pubitemid 32142139)
3. Hazes B, Price L. A nanovolume crystallization robot that creates its crystallization screens on-the-fly. Acta Crystallogr. D Biol. Crystallogr. 61, 1165-1171 (2005). (Pubitemid 43951499)
4. Di Profio G, Grosso V, Caridi A et al. Direct production of carbamazepine-saccharin cocrystals from water/ethanol solvent mixtures by membrane-based crystallization technology CrystEngComm. 13, 5670-5673 (2011).
5. Shah Umang V, Allenby MC, Williams DR et al. Crystallization of proteins at ultralow supersaturations using novel three-dimensional nanotemplates. Cryst. Growth Des. 12(4), 1772-1777 (2012).
6. Gil-Alvaradejo G, Ruiz-Arellano RR, Owen C et al. Novel protein crystal growth electrochemical cell for applications in X-ray diffraction and atomic force microscopy. Cryst. Growth Des. 11, 3917-3922 (2011).
7. Koizumi H, Uda S, Fujiwara K et al. Control of effect on the nucleation rate for hen egg white lysozyme crystals under application of an external ac electric field Langmuir. 27 (13), 8333-8338 (2011).
8. Henrich B, Bergamaschi A, Broennimann C et al. PILATUS: a single photon counting pixel detector for X-ray applications. Nucl. Instrum. Methods Phys. Res. A 607(1), 247-249 (2009).
9. Trueb P, Sobott BA, Schnyder R et al. Improved count rate corrections for highest data quality with PILATUS detectors. J. Synchrotron Radiat. 19, 347-351 (2012).
10. Rajendran C, Dworkowski FS, Wang M, Schulze-Briese C. Radiation damage in room-temperature data acquisition with the PILATUS 6M pixel detector. J. Synchrotron Radiat. 18, 318-328 (2011).
11. Fodje M, Janzen K, Berg R et al. MxDC and MxLIVE: software for data acquisition, information management and remote access to macromolecular crystallography beamlines. J. Synchrotron Radiat. 19, 274-280 (2012).
12. Giacovazzo C. Direct Phasing in Crystallography, Fundamentals and Applications. Oxford University Press, Oxford, UK (1998).
13. Rossmann MG, Blow DM. The detection of sub-units within the crystallographic asymmetric unit. Acta Crystallogr. 15, 24-31 (1962).
14. Hoppe W, Gassman J. Phase correction, a new method to solve partially known structures. Acta Crystallogr. B 24, 97-107 (1968).
15. Podjarny AD, Rees B. Density modification: theory and practice. In: Crystallographic Computing 5: From Chemistry to Biology. Moras D, Podjarny AD, Thierry JC (Eds). Oxford University Press, Oxford, UK, 361-371 (1991).
16. Arnold E, Rossmann MG. Effect of errors, redundancy, and solvent content in the molecular replacement procedure for the structure determination of biological macromolecules. Proc. Natl Acad. Sci. USA 83, 5489-5493 (1986).
17. Zhang KYJ, Main P. Histogram matching as a new density modification technique for phase refinement and extension of protein molecules. Acta Crystallogr. A 46, 41-46 (1990).
18. Burla MC, Caliandro R, Giacovazzo C et al. The difference electron density: a probabilistic reformulation. Acta Crystallogr. A 66, 347-361 (2010).
19. Debreczeni JE, Emsley P. Handling ligands with Coot. Acta Crystallogr. D Biol. Crystallogr. 68, 425-430 (2012).
20. Terwilliger TC, Klei H, Adams PD et al. Automated ligand fitting by core-fragment fitting and extension into density. Acta Crystallogr. D Biol. Crystallogr. 62, 915-922 (2006). (Pubitemid 44125669)
21. Mooij WT, Hartshorn MJ, Tickle IJ, Sharff AJ, Verdonk ML, Jhoti H. Automated protein-ligand crystallography for structure-based drug design. ChemMedChem 1, 827-838 (2006). (Pubitemid 44384544)
22. Caliandro R, Carrozzini B, Cascarano GL et al. Advances in the EDM-DEDM procedure. Acta Crystallogr. D Biol. Crystallogr. 65, 249-256 (2009).
23. Giacovazzo C, Mazzone A. A practical study of the electron-density-map variance. Acta Crystallogr. A 68, 464-469 (2012).
24. Blundell TL, Patel S. High-throughput X-ray crystallography for drug discovery. Curr. Opin. Pharmacol. 4, 490-496 (2004). (Pubitemid 40533010)
25. Nienaber VL, Richardson PL, Klighofer Vet al. Discovering novel ligands for macromolecules using X-ray crystallographic screening. Nat. Biotechnol. 18, 1105-1108 (2000).
26. Congreve M, Chessari G, Tisi D, Woodhead AJ. Recent development in fragment-based drug discovery. J. Med. Chem. 51, 3661-3680 (2008). (Pubitemid 351956496)
27. Congreve M, Carr R, Murray C, Jhoti H. A 'rule of three' for fragment-based lead discovery? Drug Discov. Today 8, 876-877 (2003). (Pubitemid 37194496)
28. Jhoti H, Cleasby A, Verdonk M, Williams G. Fragment-based screening using X-ray crystallography and NMR spectroscopy. Curr. Opin. Chem. Biol. 11, 485-493 (2007). (Pubitemid 47588996)
29. Schuffenhauer A, Ruedisser S, Marzinzik A, Jahnke W, Selzer P, Jacoby E. Library design for fragment based screening. Curr. Top. Med. Chem. 5, 751-762 (2005). (Pubitemid 41179715)
30. Sharff A, Jhoti H. High-throughput crystallography to enhance drug discovery Curr. Opin. Chem. Biol. 27, 340-345 (2003). (Pubitemid 36782360)
31. Caliandro R, Carrozzini B, Cascarano GL et al. Ab initio phasing of proteins with heavy atoms at non-atomic resolution: pushing the size limit of solvable structures up to 7800 non-H atoms in the asymmetric unit. J. Appl. Crystallogr. 41, 548-553 (2008). (Pubitemid 351693883)
32. Hajduk PJ, Greer J. A decade of fragment-based drug design: strategic advances and lessons learned. Nat. Rev. Drug Discov. 6, 211-219, (2007). (Pubitemid 46344625)
33. Klinac D, Gray ES, Millward M, Ziman M. Advances in personalized targeted treatment of metastatic melanoma and non-invasive tumor monitoring. Front. Oncol. 3, 54 (2013).
34. Heakal Y, Kester M, Savage S. Vemurafenib (PLX4032): an orally available inhibitor of mutated BRAF for the treatment of metastatic melanoma. Ann. Pharmacother. 45, 1399-1405 (2011).
35. Chilingaryan Z, Yin Z, Oakley AJ. Fragment-based screening by protein crystallography: Successes and pitfalls. Int. J. Mol. Sci. 13, 12857-12879 (2012).
36. Ward RA, Brassington C, Breeze AL et al. Design and synthesis of novel lactate dehydrogenase A inhibitors by fragment-based lead generation. J. Med. Chem. 55, 3285-3306 (2012).
37. Good AC, Liu J, Hirth B et al. Implications of promiscuous Pim-1 kinase fragment inhibitor hydrophobic interactions for fragment-based drug design. J. Med. Chem. 55, 2641-2648 (2012).
38. Chung CW, Dean AW, Woolven JM, Bamborough P. Fragment-based discovery of bromodomain inhibitors part 1: inhibitor binding modes and implications for lead discovery. J. Med. Chem. 55, 576-586 (2012).
39. Bamborough P, Diallo H, Goodacre JD et al. Fragment-based discovery of bromodomain inhibitors part 2: optimization of phenylisoxazole sulfonamides. J. Med. Chem. 55, 587-596 (2012).
40. Li R, Martin MP, Liu Y, Wang B et al. Fragment-based and structure-guided discovery and optimization of Rho kinase inhibitors. J. Med. Chem. 55, 2474-2478 (2012).
41. Murray CW, Carr MG, Callaghan O et al. Fragment-based drug discovery applied to Hsp90. discovery of two lead series with high ligand efficiency. J. Med. Chem. 53, 5942-5955 (2010).
42. Brough PA, Barril X, Borgognoni J et al. Combining hit identification strategies: fragment-based and in silico approaches to orally active 2-aminothieno[2,3-d]pyrimidine inhibitors of the Hsp90 molecular chaperone. .J. Med. Chem. 52, 4794-4809 (2009).
43. Buchstaller H-P, Eggenweiler H-M, Sirrenberg C et al. Fragment-based discovery of hydroxy-indazole-carboxamides as novel small molecule inhibitors of Hsp90. Bioorg. Med. Chem. Lett. 22, 4396-4403 (2012).
44. Saraboji K, Håkansson M, Genheden S et al. The carbohydrate-binding site in galectin-3 is preorganized to recognize a sugarlike framework of oxygens: ultra-high-resolution structures and water dynamics. Biochemistry 51, 296-306 (2012).
45. Hao G-F, Wang F, Li H et al. Computational discovery of picomolar Q(o) site inhibitors of cytochrome bc1 complex. J. Am. Chem. Soc. 134, 11168-11176 (2012).
46. Recht MI, Sridhar V, Badger J et al. Fragment-based screening for inhibitors of PDE4A using enthalpy arrays and X-ray crystallography. J. Biomol. Screen. 17, 469-480 (2012).
47. Erlanson DA, Arndt JW, Cancilla MT et al. Discovery of a potent and highly selective PDK1 inhibitor via fragment-based drug discovery. Bioorg. Med. Chem. Lett. 21, 3078-3083 (2011).
48. Johnson MC, Hu Q, Lingardo L et al. Novel isoquinolone PDK1 inhibitors discovered through fragment-based lead discovery. J. Comput. Aided Mol. Des. 25, 689-698 (2011).
49. Moffett K, Konteatis Z, Nguyen D et al. Discovery of a novel class of non-ATP site DFG-out state p38 inhibitors utilizing computationally assisted virtual fragment-based drug design (vFBDD). Bioorg. Med. Chem. Lett. 21, 7155-7165 (2011).
50. Behnen J, Köster H, Neudert G et al. Experimental and computational active site mapping as a starting point to fragment-based lead discovery. ChemMedChem 7, 248-261 (2012).
51. Gibbs AC, Abad MC, Zhang X et al. Electron density guided fragment-based lead discovery of ketohexokinase inhibitors. J. Med. Chem. 53, 7979-7991 (2010).
52. Zhang X, Song F, Kuo G-H et al. Optimization of a pyrazole hit from FBDD into a novel series of indazoles as ketohexokinase inhibitors. Bioorg. Med. Chem. Lett. 21, 4762-4767 (2011).
53. Edink E, Rucktooa P, Retra K et al. Fragment growing induces conformational changes in acetylcholine-binding protein: a structural and thermodynamic analysis. J. Am. Chem. Soc. 133, 5363-5371 (2011).
54. Yamane J, Yao M, Zhou Y et al. In-crystal affinity ranking of fragment hit compounds reveals a relationship with their inhibitory activities. J. Appl. Crystallogr. 44, 798-804 (2011).
55. Vulpetti A, Schiering N, Dalvit C. Combined use of computational chemistry, NMR screening, and X-ray crystallography for identification and characterization of fluorophilic protein environments. Proteins 78, 3281-3291 (2010).
56. Davies DR, Mamat B, Magnusson OT et al. Discovery of leukotriene A4 hydrolase inhibitors using metabolomics biased fragment crystallography. J. Med. Chem. 52, 4694-4715 (2009).
57. Sandanayaka V, Mamat B, Mishra RK et al. Discovery of 4-[(2S)-2-{[4-(4-chlorophenoxy)phenoxy]methyl}-1-pyrrolidinyl]butanoic acid (DG-051) as a novelleukotriene A4 hydrolase inhibitor of leukotriene B4 biosynthesis. J. Med. Chem. 53, 573-585 (2010).
58. Drinkwater N, Vu H, Lovell KM, Criscione KR et al. Fragment-based screening by X-ray crystallography, MS and isothermal titration calorimetry to identify PNMT (phenylethanolamineN-methyltransferase) inhibitors. Biochem. J. 431, 51-61 (2010).
59. Godemann R, Madden J, Kramer J et al. Fragment-based discovery of BACE1 inhibitors using functional assays. Biochemistry 48, 10743-10751 (2009).
60. Chen Y, Shoichet BK. Molecular docking and ligand specificity in fragment-based inhibitor discovery. Nat. Chem. Biol. 5, 358-363 (2009).
61. Antonysamy S, Hirst G, Park F et al. Fragment-based discovery of JAK-2 inhibitors. Bioorg. Med. Chem. Lett. 19, 279-282 (2009).
62. Frederickson M, Callaghan O, Chessari G et al. Fragment-based discovery of mexiletine derivatives as orally bioavailable inhibitors of urokinase-type plasminogen activator. J. Med. Chem. 51, 183-186 (2008).
63. Hansen JD, Grina J, Newhouse B et al. Potent and selective pyrazole-based inhibitors of B-Raf kinase. Bioorg. Med. Chem. Lett. 18, 4692-4695 (2008).
64. Tsai J, Lee JT, Wang W et al. Discovery of selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc. Natl Acad. Sci. USA 105, 3041-3046 (2008). (Pubitemid 351723664)
65. Bollag G, Hirth P, Tsai J et al. Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature 467, 596-599 (2010).
66. Wallace MB, Feng J, Zhang Z et al. Structure-based design and synthesis of benzimidazole derivatives as dipeptidyl peptidase IV inhibitors. Bioorg. Med. Chem. Lett. 18, 2362-2367 (2008). (Pubitemid 351447287)
67. Hohwy M, Spadola L, Lundquist B et al. Novel prostaglandin D synthase inhibitors generated by fragment-based drug design. J. Med. Chem. 51, 2178-2186 (2008). (Pubitemid 351503273)
68. MacKinnon AC, Farnworth SL, Hodkinson PS et al. Regulation of alternative macrophage activation by galectin-3. J. Immunol. 180, 2650-2658 (2008).
69. Yang RY, Rabinovich GA, Liu FT. Galectins: structure, function and therapeutic potential. Expert Rev. Mol. Med. 10, e17 (2008).
70. Wu MH, Hong TM, Cheng HW et al. Galectin-1-mediated tumor invasion and metastasis, up-regulated matrix metalloproteinase expression, and reorganized actin cytoskeletons. Mol. Cancer Res. 7, 311-318 (2009).
71. Delaine T, Cumpstey I, Ingrassia L et al. Galectin-inhibitory thiodigalactoside ester derivatives have antimigratory effects in cultured lung and prostate cancer cells. J. Med. Chem. 51, 8109-8114 (2008).
72. Lin CI, Whang EE, Donner DB et al. Galectin-3 targeted therapy with a small molecule inhibitor activates apoptosis and enhances both chemosensitivity and radiosensitivity in papillary thyroid cancer. Mol. Cancer Res. 7, 1655-1662 (2009).
73. Sörme P, Arnoux P, Kahl-Knutsson B, Leffler H, Rini JM, Nilsson UJ. Structural and thermodynamic studies on cation-p interactions in lectin-ligand complexes: high-affinity galectin-3 inhibitors through fine-tuning of an arginine-arene interaction. J. Am. Chem. Soc. 127, 1737-1743 (2005). (Pubitemid 40233025)
74. Seetharaman J, Kanigsberg A, Slaaby R, Leff ler H, Barondes SH, Rini JM. X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1-Å resolution. J. Biol. Chem. 273, 13047-13052 (1998). (Pubitemid 28246869)
75. Collins PM, Hidari KI, Blanchard H. Slow diffusion of lactose out of galectin-3 crystals monitored by X-ray crystallography: possible implications for ligand-exchange protocols. Acta Crystallogr. D 63, 415-419 (2007). (Pubitemid 46438535)
76. Henderson NC, Sethi T. The regulation of inf lammation by galectin-3. Immunol. Rev. 230, 160-171 (2009).
77. Von Itzstein M. The war against inf luenza: discovery and development of sialidase inhibitors. Nat. Rev. Drug Discov. 6, 967-974 (2007).
78. Ernst B, Magnani JL. From carbohydrate leads to glycomimetic drugs. Nat. Rev. Drug Discov. 8, 661-677 (2009).
79. Young CD, Lewis AS, Rudolph MC et al. Modulation of glucose transporter 1 (GLUT1) expression levels alters mouse mammary tumor cell growth in vitro and in vivo. PLoS ONE 6, e23205 (2011).
80. Lopopolo G, de Candia M, Panza L et al. b-d-glucosyl conjugates of highly potent inhibitors of blood coagulation factor Xa bearing 2-chorothiophene as P1 motif. ChemMedChem 7, 1669-1677 (2012).
81. Martin JL, Begun J, McLeish MJ, Caine JM, Grunewald GL. Getting the adrenaline going: crystal structure of the adrenaline-synthesizing enzyme PNMT. Structure 9, 977-985 (2001). (Pubitemid 32972163)
82. Drinkwater N, Gee CL, Puri M et al. Molecular recognition of physiological substrate noradrenaline by the adrenaline-synthesizing enzyme PNMT and factors influencing its methyltransferase activity. Biochem. J. 422, 463-471 (2009).
83. Nair PC, Malde AK, Drinkwater N, Mark AE. Missing fragments: cooperative binding in fragment-based drug design. ACS Med. Chem. Lett. 3, 322-326 (2012).
84. Flaherty KT, Yasothan U, Kirkpatrick P. Vemurafenib. Nat. Rev. Drug Discov. 10, 811-812 (2011).
85. Bollag G, Tsai J, Zhang J et al. Vemurafenib: the first drug approved for BRAF-mutant cancer. Nat. Rev. Drug Discov. 11, 873-886 (2012).
86. Navratilova I, Hopkins AL. Emerging role of surface plasmon resonance in fragment-based drug discovery. Future Med. Chem. 3(14), 1809-1820 (2011).
87. Torres FE, Recht MI, Coyle JE et al. Higher throughput calorimetry: opportunities, approaches and challenges. Curr. Opin. Chem. Biol. 20(5), 598-605 (2010).
88. Yang W, Fucini RV, Fahr BT et al. Fragment-based discovery of nonpeptidic BACE-1 inhibitors using tethering. Biochem. J. 48(21), 4488-4496 (2009).
89. Vajda S, Guarnieri F. Characterization of protein-ligand interaction sites using experimental and computational methods. Curr. Opin. Chem. Biol. 9, 354-362 (2006). (Pubitemid 43774164)
90. Adams PD, Afonine PV, Bunkoczi G et al. The Phenix software for automated determination of macromolecular structures. Methods 55, 94-106 (2011).
91. Bailey S. The CCP4 suite-programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
92. Burla MC, Caliandro R, Camalli M et al. IL MILIONE: a suite of computer programs for crystal structure solution of proteins. J. Appl. Crystallogr. 40, 609-613 (2007). (Pubitemid 46788575)
93. Caliandro R, Carrozzini B, Cascarano GL et al. Molecular replacement: the probabilistic approach of the program REMO09 and its applications. ActaCrystallogr. A 65, 512-527 (2009).
94. Read RJ, McCoy AJ. Using SAD data in Phaser. Acta Crystallogr. D 67, 338-344 (2011).
95. Bottegoni G, Favia AD, Recanatini M, Cavalli A. The role of fragment-based and computational methods in polypharmacology. Drug Discov. Today 17, 23-34 (2012).