Miniaturization and validation of a sensitive multiparametric cell-based assay for the concomitant detection of microtubule-destabilizing and microtubule-stabilizing agents

Journal of Biomolecular Screening

Volumn 11, Issue 4, 2006, Pages 377-389

  Vassal, Emilie ^a   Barette, Caroline ^b   Fonrose, Xavier ^a   Dupont, Raphaël ^a   Sans Soleilhac, Emmanuelle ^b   Lafanechère, Laurence ^b  

^a UNIV GRENOBLE ALPES   (France)

^b CEA GRENOBLE   (France)

Author keywords

Anticancer drugs; Cell based assay; High content screening; Microtubules; Tubulin post translational modifications

Indexed keywords

3 AMINOBENZAMIDE; ALPHA TUBULIN; APIGENIN; BENOMYL; BREFELDIN A; CAMPTOTHECIN; COLCHICINE; COMBRETASTATIN; COSTUNOLIDE; CYCLOHEXIMIDE; CYTOCHALASIN D; DACTINOMYCIN; DAIDZEIN; DAUNORUBICIN; DOCETAXEL; EPOTHILONE B; ETOPOSIDE; GRISEOFULVIN; NOCODAZOLE; NOSCAPINE; PACLITAXEL; PODOPHYLLOTOXIN; PROTEIN ANTIBODY; TUBULIN; TUBULIN CARBOYXPEPTIDASE; TUBULIN TYROSINE LIGASE; TYROSINE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VINBLASTINE; VINCRISTINE;

ADDITION REACTION; ANTIBODY SPECIFICITY; ARTICLE; AUTOMATION; CARBOXY TERMINAL SEQUENCE; CELL; CHEMICAL REACTION; CONTROLLED STUDY; DEPOLYMERIZATION; DEVICE; DRUG CYTOTOXICITY; DRUG DETERMINATION; DRUG EFFECT; DRUG SCREENING; DRUG SENSITIZATION; DRUG TARGETING; ELECTRONICS; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SUBSTRATE; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; SENSITIVITY ANALYSIS; STAINING; VALIDATION PROCESS;

EID: 33744930155     PISSN: 10870571     EISSN: 1552454X     Source Type: Journal    
DOI: 10.1177/1087057106286210     Document Type: Article

References (72)

1. Jordan MA, Wilson L: Microtubules as a target for anticancer drugs. Nat Rev Cancer 2004;4:253-265.
2. Wood KW, Cornwell WD, Jackson JR: Past and future of the mitotic spindle as an oncology target. Curr Opin Pharmacol 2001;1:370-377.
3. Giannakakou P, Sackett D, Fojo T: Tubulin/microtubules: still a promising target for new chemotherapeutic agents. J Natl Cancer Inst 2000;92:182-183.
4. Giannakakou P, Gussio R, Nogales E, Downing KH, Zaharevitz D, Bollbuck B, et al: A common pharmacophore for epothilone and taxanes: molecular basis for drug resistance conferred by tubulin mutations in human cancer cells. Proc Natl Acad Sci U S A 2000;97:2904-2909.
5. Honore S, Kamath K, Braguer D, Horwitz SB, Wilson L, Briand C, et al: Synergistic suppression of microtubule dynamics by discodermolide and paclitaxel in non-small cell lung carcinoma cells. Cancer Res 2004;64:4957-4964.
6. Jordan MA: Mechanism of action of antitumor drugs that interact with microtubules and tubulin. Curr Med Chem Anti-Canc Agents 2002;2:1-17.
7. Stachel SJ, Biswas K, Danishefsky SJ: The epothilones, eleutherobins, and related types of molecules. Curr Pharm Des 2001;7:1277-1290.
8. Helft PR, Schilsky RL, Hoke FJ, Williams D, Kindler HL, Sprague E, et al: A phase I study of cantuzumab mertansine administered as a single intravenous infusion once weekly in patients with advanced solid tumors. Clin Cancer Res 2004;10:4363-4368.
9. Henry MD, Wen S, Silva MD, Chandra S, Milton M, Worland PJ: A prostate-specific membrane antigen-targeted monoclonal antibody-chemotherapeutic conjugate designed for the treatment of prostate cancer. Cancer Res 2004;64:7995-8001.
10. Tolcher AW, Aylesworth C, Rizzo J, Izbicka E, Campbell E, Kuhn J, et al: A phase I study of rhizoxin (NSC 332598) by 72-hour continuous intravenous infusion in patients with advanced solid tumors. Ann Oncol 2000;11:333-338.
11. Perez EA, Hillman DW, Fishkin PA, Krook JE, Tan WW, Kuriakose PA, et al: Phase II trial of dolastatin-10 in patients with advanced breast cancer. Invest New Drugs 2005;23:257-261.
12. Simmons TL, Andrianasolo E, McPhail K, Flatt P, Gerwick WH: Marine natural products as anticancer drugs. Mol Cancer Ther 2005;4:333-342.
13. Andrieux A, Job D: A role for the cytoskeleton in mental diseases? [in French]. Med Sci (Paris) 2003;19:135-137.
14. Andrieux A, Salin PA, Vernet M, Kujala P, Baratier J, Gory-Faure S, et al: The suppression of brain cold-stable microtubules in mice induces synaptic defects associated with neuroleptic-sensitive behavioral disorders. Genes Dev 2002;16:2350-2364.
15. Zhang B, Maiti A, Shively S, Lakhani F, McDonald-Jones G, Bruce J, et al: Microtubule-binding drugs offset tau sequestration by stabilizing microtubules and reversing fast axonal transport deficits in a tauopathy model. Proc Natl Acad Sci U S A 2005;102:227-231.
16. Watts NR, Sackett DL, Ward RD, Miller MW, Wingfield PT, Stahl SS, et al: HIV-1 rev depolymerizes microtubules to form stable bilayered rings. J Cell Biol 2000;150:349-360.
17. Ruthel G, Demmin GL, Kallstrom G, Javid MR Badie SS, Will AB, et al: Association of Ebola virus matrix protein VP40 with microtubules. J Virol 2005;79:4709-4719.
18. Dohner K, Sodeik B: The role of the cytoskeleton during viral infection. Curr Top Microbiol Immunol 2005;285:67-108.
19. Rodriguez A, Samoff E, Rioult MG, Chung A, Andrews NW: Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport. J Cell Biol 1996;134:349-362.
20. Estes R, Vogel N, Mack D, McLeod R: Paclitaxel arrests growth of intracellular Toxoplasma gondii. Antimicrob Agents Chemother 1998;42:2036-2040.
21. Melo EJ, Carvalho TM, De Souza W: Behaviour of microtubules in cells infected with Toxoplasma gondii. Biocell 2001;25:53-59.
22. Morrissette NS, Sibley LD: Disruption of microtubules uncouples budding and nuclear division in Toxoplasma gondii. J Cell Sci 2002;115:1017-1025.
23. Shaw MK, Compton HL, Roos DS, Tilney LG: Microtubules, but not actin filaments, drive daughter cell budding and cell division in Toxoplasma gondii. J Cell Sci 2000;113(pt 7):1241-1254.
24. Fowler RE, Fookes RE, Lavin F, Bannister LH, Mitchell GH: Microtubules in Plasmodium falciparum merozoites and their importance for invasion of erythrocytes. Parasitology 1998;117(pt 5):425-433.
25. Peterson JR, Mitchison TJ: Small molecules, big impact: a history of chemical inhibitors and the cytoskeleton. Chem Biol 2002;9:1275-1285.
26. Valiron O, Caudron N, Job D: Microtubule dynamics. Cell Mol Life Sci 2001;58:2069-2084.
27. Barra HS, Rodriguez JA, Arce CA, Caputto R: A soluble preparation from rat brain that incorporates into its own proteins (14 C)arginine by a ribonuclease-sensitive system and (14 C)tyrosine by a ribonuclease-insensitive system. J Neurochem 1973;20:97-108.
28. Arce CA, Rodriguez JA, Barra HS, Caputo R: Incorporation of L-tyrosine, L-phenylalanine and L-3,4-dihydroxyphenylalanine as single units into rat brain tubulin. Eur J Biochem 1975;59:145-149.
29. Lafanechère L, Job D: The third tubulin pool. Neurochem Res 2000;25:11-18.
30. Barra HS, Arce CA, Argarana CE: Posttranslational tyrosination/ detyrosination of tubulin. Mol Neurobiol 1988;2:133-153.
31. MacRae TH: Tubulin post-translational modifications - enzymes and their mechanisms of action. Eur J Biochem 1997;244:265-278.
32. Preston SF, Deanin GG, Hanson RK, Gordon MW: The phylogenetic distribution of tubulin:tyrosine ligase. J Mol Evol 1979;13:233-244.
33. Sasse R, Gull K: Tubulin post-translational modifications and the construction of microtubular organelles in Trypanosoma brucei. J Cell Sci 1988;90(pt 4):577-589.
34. Alfa CE, Hyams JS: Microtubules in the fission yeast Schizosaccharomyces pombe contain only the tyrosinated form of alpha-tubulin. Cell Motil Cytoskeleton 1991;18:86-93.
35. Badin-Larcon AC, Boscheron C, Soleilhac JM, Piel M, Mann C, Denarier E, et al: Suppression of nuclear oscillations in Saccharomyces cerevisiae expressing Glu tubulin. Proc Natl Acad Sci U S A 2004;101:5577-5582.
36. Wehland J, Weber K: Tubulin-tyrosine ligase has a binding site on beta-tubulin: a two-domain structure of the enzyme. J Cell Biol 1987;104:1059-1067.
37. Wehland J, Weber K: Turnover of the carboxy-terminal tyrosine of alpha-tubulin and means of reaching elevated levels of detyrosination in living cells. J Cell Sci 1987;88(pt 2):185-203.
38. Arce CA, Hallak ME, Rodriguez JA, Barra HS, Caputto R: Capability of tubulin and microtubules to incorporate and to release tyrosine and phenylalanine and the effect of the incorporation of these amino acids on tubulin assembly. J Neurochem 1978;31:205-210.
39. Webster DR, Gundersen GG, Bulinski JC, Borisy GG: Assembly and turnover of detyrosinated tubulin in vivo. J Cell Biol 1987;105:265-276.
40. Gundersen GG, Khawaja S, Bulinski JC: Postpolymerization detyrosination of alpha-tubulin: a mechanism for subcellular differentiation of microtubules. J Cell Biol 1987;105:251-264.
41. Kreis TE: Microtubules containing detyrosinated tubulin are less dynamic. Embo J 1987;6:2597-2606.
42. Gundersen GG, Kalnoski MH, Bulinski JC: Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell 1984;38:779-789.
43. Schulze E, Asai DJ, Bulinski JC, Kirschner M: Posttranslational modification and microtubule stability. J Cell Biol 1987;105:2167-2177.
44. Bosc C, Cronk JD, Pirollet F, Watterson DM, Haiech J, Job D, et al: Cloning, expression, and properties of the microtubule-stabilizing protein STOP. Proc Natl Acad Sci U S A 1996;93:2125-2130.
45. Westermann S, Weber K: Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol 2003;4:938-947.
46. Paturle-Lafanechere L, Manier M, Trigault N, Pirollet F, Mazarguil H, Job D: Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stable microtubule assemblies. J Cell Sci 1994;107(pt 6):1529-1543.
47. Lieuvin A, Labbe JC, Doree M, Job D: Intrinsic microtubule stability in interphase cells. J Cell Biol 1994;124:985-996.
48. Daxhelet GA, Coene MM, Hoet PP, Cocito CG: Spectrofluorometry of dyes with DNAs of different base composition and conformation. Anal Biochem 1989;179:401-403.
49. Zhang JH, Chung TD, Oldenburg KR: A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screen 1999;4:67-73.
50. Johnston PA: Cellular platforms for HTS: three case studies. Drug Discov Today 2002;7:353-363.
51. Wall ME: Camptothecin and taxol: discovery to clinic. Med Res Rev 1998;18:299-314.
52. Falconer M, Smith F, Surah-Narwal S, Congrave G, Liu Z, Hayter P, et al: High-throughput screening for ion channel modulators. J Biomol Screen 2002;7:460-465.
53. Pettit GR, Singh SB, Hamel E, Lin CM, Alberts DS, Garcia-Kendall D: Isolation and structure of the strong cell growth and tubulin inhibitor combretastatin A-4. Experientia 1989;45:209-211.
54. Sackett DL: Podophyllotoxin, steganacin and combretastatin: natural products that bind at the colchicine site of tubulin. Pharmacol Ther 1993;59:163-228.
55. Davidse LC, Flach W: Differential binding of methyl benzimidazol-2-yl carbamate to fungal tubulin as a mechanism of resistance to this antimitotic agent in mutant strains of Aspergillus nidulans. J Cell Biol 1977;72:174-193.
56. Panda D, Rathinasamy K, Santra MK, Wilson L: Kinetic suppression of microtubule dynamic instability by griseofulvin: implications for its possible use in the treatment of cancer. Proc Natl Acad Sci U S A 2005;102:9878-9883.
57. Landen JW, Hau V, Wang M, Davis T, Ciliax B, Wainer BH, et al: Noscapine crosses the blood-brain barrier and inhibits glioblastoma growth. Clin Cancer Res 2004;10:5187-5201.
58. Ye K, Ke Y, Keshava N, Shanks J, Kapp JA, Tekmal RR, et al: Opium alkaloid noscapine is an antitumor agent that arrests metaphase and induces apoptosis in dividing cells. Proc Natl Acad Sci U S A 1998;95:1601-1606.
59. Saoudi Y, Rousseau B, Doussiere J, Charrasse S, Gauthier-Rouviere C, Morin N, et al: Calcium-independent cytoskeleton disassembly induced by BAPTA. Eur J Biochem 2004;271:3255-3264.
60. Na GC, Timasheff SN: In vitro vinblastine-induced tubulin paracrystals. J Biol Chem 1982;257:10387-10391.
61. Gigant B, Wang C, Ravelli RB, Roussi F, Steinmetz MO, Curmi PA, et al: Structural basis for the regulation of tubulin by vinblastine. Nature 2005;435:519-522.
62. Gupta K, Bishop J, Peck A, Brown J, Wilson L, Panda D: Antimitotic antifungal compound benomyl inhibits brain microtubule polymerization and dynamics and cancer cell proliferation at mitosis, by binding to a novel site in tubulin. Biochemistry 2004;43:6645-6655.
63. Wehland J, Herzog W, Weber K: Interaction of griseofulvin with microtubules, microtubule protein and tubulin. J Mol Biol 1977;111:329-342.
64. Monneret C: Recent developments in the field of antitumour anthracyclines. Eur J Med Chem 2001;36:483-493.
65. Di Marco A, Cassinelli G, Arcamone F: The discovery of daunorubicin. Cancer Treat Rep 1981;65(4 Suppl):3-8.
66. Roberge M, Cinel B, Anderson HJ, Lim L, Jiang X, Xu L, et al: Cell-based screen for antimitotic agents and identification of analogues of rhizoxin, eleutherobin, and paclitaxel in natural extracts. Cancer Res 2000;60:5052-5058.
67. Wani MC, Taylor HL, Wall ME, Coggon P, McPhail AT: Plant antitumor agents. VI. The isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc 1971;93:2325-2327.
68. Noble RL: The discovery of the vinca alkaloids - chemotherapeutic agents against cancer. Biochem Cell Biol 1990;68:1344-1351.
69. Mayer TU, Kapoor TM, Haggarty SJ, King RW, Schreiber SL, Mitchison TJ: Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 1999;286:971-974.
70. Gupta S, Bhattacharyya B: Antimicrotubular drugs binding to vinca domain of tubulin. Mol Cell Biochem 2003;253:41-47.
71. Perlman ZE, Slack MD, Feng Y, Mitchison TJ, Wu LF, Altschuler SJ: Multi-dimensional drug profiling by automated microscopy. Science 2004;306:1194-1198.
72. Begley TJ, Rosenbach AS, Ideker T, Samson LD: Hot spots for modulating toxicity identified by genomic phenotyping and localization mapping. Mol Cell 2004;16:117-125.