Virtual and Biophysical Screening Targeting the γ-Tubulin Complex - A New Target for the Inhibition of Microtubule Nucleation

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Cala, Olivier ^a   Remy, Marie Hélène ^a,b   Guillet, Valérie ^a   Merdes, Andreas ^a,b   Mourey, Lionel ^a   Milon, Alain ^a   Czaplicki, Georges ^a  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; GAMMA TUBULIN; GAMMA TUBULIN COMPLEX; GAMMA TUBULIN COMPLEX 4; GAMMA TUBULIN RING COMPLEX; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; COMPUTER MODEL; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIFFERENTIAL SCANNING CALORIMETRY; MICROTUBULE; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; SIMULATION;

BINDING SITES; BIOPHYSICAL PHENOMENA; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; TUBULIN;

EID: 84877751600     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063908     Document Type: Article

References (57)

1. Arkin MR, Wells JA, (2004) Small-molecule inhibitors of protein-protein interactions: progressing towards the dream. Nat Rev Drug Discov 3: 301-317.
2. Pieraccini S, De Gonda R, Sironi M, (2011) Molecular modeling of the inhibition of protein-protein interactions with small molecules: The IL2-IL2Rα case. Chemical Physics Letters 517: 217-222.
3. Barelier S, Krimm I, (2011) Ligand specificity, privileged substructures and protein druggability from fragment-based screening. Curr Opin Chem Biol 15: 469-474.
4. Bottegoni G, Favia AD, Recanatini M, Cavalli A, (2012) The role of fragment-based and computational methods in polypharmacology. Drug Discov Today 17: 23-34.
5. Hajduk PJ, Greer J, (2007) A decade of fragment-based drug design: strategic advances and lessons learned. Nat Rev Drug Discov 6: 211-219.
6. Congreve M, Carr R, Murray C, Jhoti H, (2003) A 'rule of three' for fragment-based lead discovery? Drug Discov Today 8: 876-877.
7. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ, (2012) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Advanced Drug Delivery Reviews 64Supplement: 4-17.
8. Jordan MA, Wilson L, (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4: 253-265.
9. Joshi HC, Palacios MJ, McNamara L, Cleveland DW, (1992) Gamma-tubulin is a centrosomal protein required for cell cycle-dependent microtubule nucleation. Nature 356: 80-83.
10. Oakley BR, Oakley CE, Yoon Y, Jung MK, (1990) Gamma-tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell 61: 1289-1301.
11. Oegema K, Wiese C, Martin OC, Milligan RA, Iwamatsu A, et al. (1999) Characterization of two related Drosophila gamma-tubulin complexes that differ in their ability to nucleate microtubules. J Cell Biol 144: 721-733.
12. Zheng Y, Wong ML, Alberts B, Mitchison T, (1995) Nucleation of microtubule assembly by a gamma-tubulin-containing ring complex. Nature 378: 578-583.
13. Gunawardane RN, Martin OC, Cao K, Zhang L, Dej K, et al. (2000) Characterization and reconstitution of Drosophila gamma-tubulin ring complex subunits. J Cell Biol 151: 1513-1524.
14. Moritz M, Braunfeld MB, Sedat JW, Alberts B, Agard DA, (1995) Microtubule nucleation by gamma-tubulin-containing rings in the centrosome. Nature 378: 638-640.
15. Murphy SM, Preble AM, Patel UK, O'Connell KL, Dias DP, et al. (2001) GCP5 and GCP6: two new members of the human gamma-tubulin complex. Mol Biol Cell 12: 3340-3352.
16. Kollman JM, Merdes A, Mourey L, Agard DA, (2011) Microtubule nucleation by gamma-tubulin complexes. Nat Rev Mol Cell Biol 12: 709-721.
17. Kollman JM, Polka JK, Zelter A, Davis TN, Agard DA, (2010) Microtubule nucleating gamma-TuSC assembles structures with 13-fold microtubule-like symmetry. Nature 466: 879-882.
18. Guillet V, Knibiehler M, Gregory-Pauron L, Remy MH, Chemin C, et al. (2011) Crystal structure of gamma-tubulin complex protein GCP4 provides insight into microtubule nucleation. Nat Struct Mol Biol 18: 915-919.
19. Kollman JM, Zelter A, Muller EG, Fox B, Rice LM, et al. (2008) The structure of the gamma-tubulin small complex: implications of its architecture and flexibility for microtubule nucleation. Mol Biol Cell 19: 207-215.
20. Friesen DE, Barakat KH, Semenchenko V, Perez-Pineiro R, Fenske BW, et al. (2012) Discovery of small molecule inhibitors that interact with gamma-tubulin. Chem Biol Drug Des 79: 639-652.
21. Bouissou A, Verollet C, Sousa A, Sampaio P, Wright M, et al. (2009) {gamma}-Tubulin ring complexes regulate microtubule plus end dynamics. J Cell Biol 187: 327-334.
22. Haren L, Remy MH, Bazin I, Callebaut I, Wright M, et al. (2006) NEDD1-dependent recruitment of the gamma-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J Cell Biol 172: 505-515.
23. Tillement V, Haren L, Roullet N, Etievant C, Merdes A, (2009) The centrosome protein NEDD1 as a potential pharmacological target to induce cell cycle arrest. Mol Cancer 8: 10.
24. Whitehurst AW, Bodemann BO, Cardenas J, Ferguson D, Girard L, et al. (2007) Synthetic lethal screen identification of chemosensitizer loci in cancer cells. Nature 446: 815-819.
25. Aldaz H, Rice LM, Stearns T, Agard DA, (2005) Insights into microtubule nucleation from the crystal structure of human gamma-tubulin. Nature 435: 523-527.
26. Rice LM, Montabana EA, Agard DA, (2008) The lattice as allosteric effector: structural studies of alphabeta- and gamma-tubulin clarify the role of GTP in microtubule assembly. Proc Natl Acad Sci U S A 105: 5378-5383.
27. Hildebrand PW, Goede A, Bauer RA, Gruening B, Ismer J, et al. (2009) SuperLooper-a prediction server for the modeling of loops in globular and membrane proteins. Nucleic Acids Res 37: W571-574.
28. Case DA, Cheatham TE, 3rd, Darden T, Gohlke H, Luo R, et al (2005) The Amber biomolecular simulation programs. Journal of computational chemistry 26: 1668-1688.
29. Ponder JW, Case DA, (2003) Force fields for protein simulations. Advances in protein chemistry 66: 27-85.
30. Jorgensen WL, Madura JD, (1983) Quantum and statistical mechanical studies of liquids. 25. Solvation and conformation of methanol in water. Journal of the American Chemical Society 105: 1407-1413.
31. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, et al. (2009) AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem 30: 2785-2791.
32. Trott O, Olson AJ, (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31: 455-461.
33. Guha R, Howard MT, Hutchison GR, Murray-Rust P, Rzepa H, et al. (2006) The Blue Obelisk-interoperability in chemical informatics. J Chem Inf Model 46: 991-998.
34. Guex N, Peitsch MC, (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
35. Studier FW, (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234.
36. Niesen FH, Berglund H, Vedadi M, (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat Protoc 2: 2212-2221.
37. Laurie AT, Jackson RM, (2005) Q-SiteFinder: an energy-based method for the prediction of protein-ligand binding sites. Bioinformatics 21: 1908-1916.
38. Strub C, Alies C, Lougarre A, Ladurantie C, Czaplicki J, et al. (2004) Mutation of exposed hydrophobic amino acids to arginine to increase protein stability. BMC Biochem 5: 9.
39. Dumontet C, Jordan MA, (2010) Microtubule-binding agents: a dynamic field of cancer therapeutics. Nat Rev Drug Discov 9: 790-803.
40. Zhou J, Giannakakou P, (2005) Targeting microtubules for cancer chemotherapy. Curr Med Chem Anticancer Agents 5: 65-71.
41. Cimmperman P, Baranauskiene L, Jachimoviciute S, Jachno J, Torresan J, et al. (2008) A quantitative model of thermal stabilization and destabilization of proteins by ligands. Biophys J 95: 3222-3231.
42. Barbosa V, Yamamoto RR, Henderson DS, Glover DM, (2000) Mutation of a Drosophila gamma tubulin ring complex subunit encoded by discs degenerate-4 differentially disrupts centrosomal protein localization. Genes Dev 14: 3126-3139.
43. Colombie N, Verollet C, Sampaio P, Moisand A, Sunkel C, et al. (2006) The Drosophila gamma-tubulin small complex subunit Dgrip84 is required for structural and functional integrity of the spindle apparatus. Mol Biol Cell 17: 272-282.
44. Geissler S, Pereira G, Spang A, Knop M, Soues S, et al. (1996) The spindle pole body component Spc98p interacts with the gamma-tubulin-like Tub4p of Saccharomyces cerevisiae at the sites of microtubule attachment. Embo J 15: 3899-3911.
45. Hendrickson TW, Yao J, Bhadury S, Corbett AH, Joshi HC, (2001) Conditional mutations in gamma-tubulin reveal its involvement in chromosome segregation and cytokinesis. Mol Biol Cell 12: 2469-2481.
46. Prigozhina NL, Oakley CE, Lewis AM, Nayak T, Osmani SA, et al. (2004) gamma-tubulin plays an essential role in the coordination of mitotic events. Mol Biol Cell 15: 1374-1386.
47. Sunkel CE, Gomes R, Sampaio P, Perdigao J, Gonzalez C, (1995) Gamma-tubulin is required for the structure and function of the microtubule organizing centre in Drosophila neuroblasts. Embo J 14: 28-36.
48. Verollet C, Colombie N, Daubon T, Bourbon HM, Wright M, et al. (2006) Drosophila melanogaster gamma-TuRC is dispensable for targeting gamma-tubulin to the centrosome and microtubule nucleation. J Cell Biol 172: 517-528.
49. Khodjakov A, Rieder CL, (1999) The sudden recruitment of gamma-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle, do not require microtubules. J Cell Biol 146: 585-596.
50. Moudjou M, Bordes N, Paintrand M, Bornens M, (1996) gamma-Tubulin in mammalian cells: the centrosomal and the cytosolic forms. J Cell Sci 109 (Pt 4): 875-887.
51. Cuschieri L, Miller R, Vogel J, (2006) Gamma-tubulin is required for proper recruitment and assembly of Kar9-Bim1 complexes in budding yeast. Mol Biol Cell 17: 4420-4434.
52. Masuda H, Miyamoto R, Haraguchi T, Hiraoka Y, (2006) The carboxy-terminus of Alp4 alters microtubule dynamics to induce oscillatory nuclear movement led by the spindle pole body in Schizosaccharomyces pombe. Genes Cells 11: 337-352.
53. Paluh JL, Nogales E, Oakley BR, McDonald K, Pidoux AL, et al. (2000) A mutation in gamma-tubulin alters microtubule dynamics and organization and is synthetically lethal with the kinesin-like protein pkl1p. Mol Biol Cell 11: 1225-1239.
54. Tange Y, Fujita A, Toda T, Niwa O, (2004) Functional dissection of the gamma-tubulin complex by suppressor analysis of gtb1 and alp4 mutations in Schizosaccharomyces pombe. Genetics 167: 1095-1107.
55. Zimmerman S, Chang F, (2005) Effects of gamma-tubulin complex proteins on microtubule nucleation and catastrophe in fission yeast. Mol Biol Cell 16: 2719-2733.
56. Law R, Barker O, Barker JJ, Hesterkamp T, Godemann R, et al. (2009) The multiple roles of computational chemistry in fragment-based drug design. J Comput Aided Mol Des 23: 459-473.
57. Wang YS, Strickland C, Voigt JH, Kennedy ME, Beyer BM, et al. (2010) Application of fragment-based NMR screening, X-ray crystallography, structure-based design, and focused chemical library design to identify novel microM leads for the development of nM BACE-1 (beta-site APP cleaving enzyme 1) inhibitors. J Med Chem 53: 942-950.