Design, synthesis, biological evaluation, and Structure - Activity relationships of substituted phenyl 4-(2-oxoimidazolidin-1-yl)benzenesulfonates as new tubulin inhibitors mimicking combretastatin A-4

Journal of Medicinal Chemistry

Volumn 54, Issue 13, 2011, Pages 4559-4580

  Fortin, Sébastien ^a,b   Wei, Lianhu ^c   Moreau, Emmanuel ^d   Lacroix, Jacques ^a   Côté, Marie France ^a   Petitclerc, Éric ^a,f   Kotra, Lakshmi P ^c,e   C Gaudreault, René ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d UNIVERSITÉ CLERMONT AUVERGNE   (France)

^e UNIVERSITY OF TORONTO   (Canada)

^f HÉMA QUÉBEC   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 CHLOROPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2 ETHOXYPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2 ETHYLPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2 FLUOROPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2 IODOPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2 METHOXYPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2 NITROPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2 PROPYLPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2 TOLYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2,3 DIMETHYLPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2,4 DIMETHYLPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2,4,5 TRIMETHYLPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 2,5 DIMETHYLPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 3 TOLYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 4 (DIMETHYLAMINO)PHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 4 HYDROXYPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 4 METHOXYPHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; 4 TOLYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; ANTINEOPLASTIC AGENT; BENZENE DERIVATIVE; BETA TUBULIN; COLCHICINE; COMBRETASTATIN A4; GLYCOPROTEIN P; IMIDAZOLE DERIVATIVE; PACLITAXEL; PHENYL 4 (2 OXOIMIDAZOLIDIN 1 YL)BENZENESULFONATE; TUBULIN INHIBITOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; VINBLASTINE;

ANIMAL CELL; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CHICK EMBRYO; CONTROLLED STUDY; CYTOSKELETON; DRUG BINDING SITE; DRUG DESIGN; DRUG SYNTHESIS; EMBRYO; HUMAN; HUMAN CELL; IC 50; NONHUMAN; QUANTITATIVE STRUCTURE ACTIVITY RELATION;

EID: 79960156265     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm200488a     Document Type: Article

References (64)

1. Jordan, M. A.; Wilson, L. Microtubules as a target for anticancer drugs Nat. Rev. Cancer 2004, 4, 253-265 (Pubitemid 38525281)
2. Teicher, B. A. Newer cytotoxic agents: attacking cancer broadly Clin. Cancer Res. 2008, 14, 1610-1617 (Pubitemid 351469444)
3. Spencer, C. M.; Faulds, D. Paclitaxel. A review of its pharmacodynamic and pharmacokinetic properties and therapeutic potential in the treatment of cancer Drugs 1994, 48, 794-847 (Pubitemid 24304427)
4. Trivedi, M.; Budihardjo, I.; Loureiro, K.; Reid, T. R.; Ma, J. D. Epothilones: a novel class of microtubule-stabilizing drugs for the treatment of cancer Future Oncol. 2008, 4, 483-500
5. Robinson, H. M. Vinca revisited-another happenstance in the discovery of vinblastine Biochem. Cell Biol. 1991, 69, 581-582
6. Griggs, J.; Metcalfe, J. C.; Hesketh, R. Targeting tumour vasculature: the development of combretastatin A4 Lancet Oncol. 2001, 2, 82-87 (Pubitemid 33585919)
7. Rowinsky, E. K.; Donehower, R. C. The clinical pharmacology and use of antimicrotubule agents in cancer chemotherapeutics Pharmacol. Ther. 1991, 52, 35-84
8. Attard, G.; Greystoke, A.; Kaye, S.; De Bono, J. Update on tubulin-binding agents Pathol. Biol. (Paris) 2006, 54, 72-84
9. Checchi, P. M.; Nettles, J. H.; Zhou, J.; Snyder, J. P.; Joshi, H. C. Microtubule-interacting drugs for cancer treatment Trends Pharmacol. Sci. 2003, 24, 361-365 (Pubitemid 37315528)
10. Sridhare, M.; Macapinlac, M. J.; Goel, S.; Verdier-Pinard, D.; Fojo, T.; Rothenberg, M.; Colevas, D. The clinical development of new mitotic inhibitors that stabilize the microtubule Anti-Cancer Drugs 2004, 15, 553-555
11. Islam, M. N.; Song, Y.; Iskander, M. N. Investigation of structural requirements of anticancer activity at the paclitaxel/tubulin binding site using CoMFA and CoMSIA J. Mol. Graphics Modell. 2003, 21, 263-272 (Pubitemid 35441324)
12. Pettit, G. R.; Singh, S. B.; Hamel, E.; Lin, C. M.; Alberts, D. S.; Garcia-Kendall, D. Isolation and structure of the strong cell growth and tubulin inhibitor combretastatin A-4 Experientia 1989, 45, 209-211 (Pubitemid 19062390)
13. Young, S. L.; Chaplin, D. J. Combretastatin A4 phosphate: background and current clinical status Expert Opin. Invest. Drugs 2004, 13, 1171-1182 (Pubitemid 39242740)
14. Delmonte, A.; Sessa, C. AVE8062: a new combretastatin derivative vascular disrupting agent Expert Opin. Invest. Drugs 2009, 18, 1541-1548
15. Anderson, H. L.; Yap, J. T.; Miller, M. P.; Robbins, A.; Jones, T.; Price, P. M. Assessment of pharmacodynamic vascular response in a phase I trial of combretastatin A4 phosphate J. Clin. Oncol. 2003, 21, 2823-2830 (Pubitemid 46621829)
16. Patterson, D. M.; Rustin, G. J. Vascular damaging agents Clin. Oncol. (R. Coll. Radiol.) 2007, 19, 443-456 (Pubitemid 46995617)
17. Simoni, D.; Romagnoli, R.; Baruchello, R.; Rondanin, R.; Rizzi, M.; Pavani, M. G.; Alloatti, D.; Giannini, G.; Marcellini, M.; Riccioni, T.; Castorina, M.; Guglielmi, M. B.; Bucci, F.; Carminati, P.; Pisano, C. Novel combretastatin analogues endowed with antitumor activity J. Med. Chem. 2006, 49, 3143-3152 (Pubitemid 43830513)
18. Stevenson, J. P.; Rosen, M.; Sun, W.; Gallagher, M.; Haller, D. G.; Vaughn, D.; Giantonio, B.; Zimmer, R.; Petros, W. P.; Stratford, M.; Chaplin, D.; Young, S. L.; Schnall, M.; O'Dwyer, P. J. Phase I trial of the antivascular agent combretastatin A4 phosphate on a 5-day schedule to patients with cancer: magnetic resonance imaging evidence for altered tumor blood flow J. Clin. Oncol. 2003, 21, 4428-4438 (Pubitemid 46621821)
19. Aprile, S.; Del Grosso, E.; Tron, G. C.; Grosa, G. In vitro metabolism study of combretastatin A-4 in rat and human liver microsomes Drug Metab. Dispos. 2007, 35, 2252-2261 (Pubitemid 350146212)
20. Pettit, G. R.; Toki, B.; Herald, D. L.; Verdier-Pinard, P.; Boyd, M. R.; Hamel, E.; Pettit, R. K. Antineoplastic agents. 379. Synthesis of phenstatin phosphate J. Med. Chem. 1998, 41, 1688-1695 (Pubitemid 28221962)
21. La Regina, G.; Sarkar, T.; Bai, R.; Edler, M. C.; Saletti, R.; Coluccia, A.; Piscitelli, F.; Minelli, L.; Gatti, V.; Mazzoccoli, C.; Palermo, V.; Mazzoni, C.; Falcone, C.; Scovassi, A. I.; Giansanti, V.; Campiglia, P.; Porta, A.; Maresca, B.; Hamel, E.; Brancale, A.; Novellino, E.; Silvestri, R. New arylthioindoles and related bioisosteres at the sulfur bridging group. 4. Synthesis, tubulin polymerization, cell growth inhibition, and molecular modeling studies J. Med. Chem. 2009, 52, 7512-7527
22. Tron, G. C.; Pirali, T.; Sorba, G.; Pagliai, F.; Busacca, S.; Genazzani, A. A. Medicinal chemistry of combretastatin A4: present and future directions J. Med. Chem. 2006, 49, 3033-3044 (Pubitemid 43830499)
23. Gwaltney, S. L.; Imade, H. M.; Barr, K. J.; Li, Q.; Gehrke, L.; Credo, R. B.; Warner, R. B.; Lee, J. Y.; Kovar, P.; Wang, J.; Nukkala, M. A.; Zielinski, N. A.; Frost, D.; Ng, S. C.; Sham, H. L. Novel sulfonate analogues of combretastatin A-4: potent antimitotic agents Bioorg. Med. Chem. Lett. 2001, 11, 871-874 (Pubitemid 32226204)
24. Deschesnes, R. G.; Patenaude, A.; Rousseau, J. L.; Fortin, J. S.; Ricard, C.; Cote, M.-F.; Huot, J.; C.-Gaudreault, R.; Petitclerc, E. Microtubule-destabilizing agents induce focal adhesion structure disorganization and anoikis in cancer cells J. Pharmacol. Exp. Ther. 2007, 320, 853-864 (Pubitemid 46147968)
25. Petitclerc, E.; Deschesnes, R. G.; Cote, M.-F.; Marquis, C.; Janvier, R.; Lacroix, J.; Miot-Noirault, E.; Legault, J.; Mounetou, E.; Madelmont, J.-C.; C.-Gaudreault, R. Antiangiogenic and antitumoral activity of phenyl-3-(2-chloroethyl)ureas: a class of soft alkylating agents disrupting microtubules that are unaffected by cell adhesion-mediated drug resistance Cancer Res. 2004, 64, 4654-4663 (Pubitemid 38856940)
26. Mounetou, E.; Legault, J.; Lacroix, J.; C.-Gaudreault, R. Antimitotic antitumor agents: synthesis, structure-activity relationships, and biological characterization of N -aryl- N ′-(2-chloroethyl)ureas as new selective alkylating agents J. Med. Chem. 2001, 44, 694-702 (Pubitemid 32171666)
27. Mounetou, E.; Legault, J.; Lacroix, J.; C.-Gaudreault, R. A new generation of N -aryl- N ′-(1-alkyl-2-chloroethyl)ureas as microtubule disrupters: synthesis, antiproliferative activity, and β-tubulin alkylation kinetics J. Med. Chem. 2003, 46, 5055-5063 (Pubitemid 37352042)
28. Poyet, P.; Ritchot, N.; Bechard, P.; C.-Gaudreault, R. Effect of an aryl chloroethyl urea on tubulin and vimentin syntheses in a human breast cancer cell line Anticancer Res. 1993, 13, 1447-1452 (Pubitemid 23334773)
29. Fortin, S.; Moreau, E.; Patenaude, A.; Desjardins, M.; Lacroix, J.; Rousseau, J. L.; C.-Gaudreault, R. N -Phenyl- N ′-(2-chloroethyl)ureas (CEU) as potential antineoplastic agents. Part 2: Role of ω-hydroxyl group in the covalent binding to β-tubulin Bioorg. Med. Chem. 2007, 15, 1430-1438 (Pubitemid 46043436)
30. Moreau, E.; Fortin, S.; Desjardins, M.; Rousseau, J. L.; Petitclerc, E.; C.-Gaudreault, R. Optimized N -phenyl- N ′-(2-chloroethyl)ureas as potential antineoplastic agents: synthesis and growth inhibition activity Bioorg. Med. Chem. 2005, 13, 6703-6712 (Pubitemid 41571214)
31. Moreau, E.; Fortin, S.; Lacroix, J.; Patenaude, A.; Rousseau, J. L.; C.-Gaudreault, R. N -Phenyl- N ′-(2-chloroethyl)ureas (CEUs) as potential antineoplastic agents. Part 3: role of carbonyl groups in the covalent binding to the colchicine-binding site Bioorg. Med. Chem. 2008, 16, 1206-1217 (Pubitemid 351200485)
32. 14C]ethyl)ureido benzene J. Labelled Compd. Radiopharm. 1997, 39, 559-566
33. Maurizis, J. C.; Rapp, M.; Azim, E. M.; C.-Gaudreault, R.; Veyre, A.; Madelmont, J.-C. Disposition and metabolism of a novel antineoplastic agent, 4- tert -butyl-[3-(2-chloroethyl)ureido]benzene, in mice Drug Metab. Dispos. 1998, 26, 146-151 (Pubitemid 28104082)
34. II-tubulin and thioredoxin-1 by structurally related subsets of aryl chloroethylureas leading to either anti-microtubules or redox modulating agents Bioorg. Med. Chem. 2008, 16, 7277-7290
35. 1 phase and thioredoxin-1 nuclear translocation Bioorg. Med. Chem. Lett. 2008, 18, 3526-3531 (Pubitemid 351787570)
36. Fortin, J. S.; Cote, M.-F.; Lacroix, J.; Petitclerc, E.; C.-Gaudreault, R. Aromatic 2-chloroethyl urea derivatives and bioisosteres. Part 2: Cytocidal activity and effects on the nuclear translocation of thioredoxin-1, and the cell cycle progression Bioorg. Med. Chem. 2008, 16, 7477-7488
37. 1 arrest in B16 cells Br. J. Pharmacol. 2007, 152, 449-455 (Pubitemid 47585042)
38. Patenaude, A.; Deschesnes, R. G.; Rousseau, J. L.; Petitclerc, E.; Lacroix, J.; Cote, M.-F.; C.-Gaudreault, R. New soft alkylating agents with enhanced cytotoxicity against cancer cells resistant to chemotherapeutics and hypoxia Cancer Res. 2007, 67, 2306-2316 (Pubitemid 46424251)
39. Fortin, S.; Labrie, P.; Moreau, E.; Wei, L.; Kotra, L. P.; C.-Gaudreault, R. A comparative molecular field and comparative molecular similarity indices analyses (CoMFA and CoMSIA) of N -phenyl- N ′-(2-chloroethyl)ureas targeting the colchicine-binding site as anticancer agents Bioorg. Med. Chem. 2008, 16, 1914-1926 (Pubitemid 351233041)
40. Fortin, S.; Wei, L.; Moreau, E.; Labrie, P.; Petitclerc, E.; Kotra, L. P.; C.-Gaudreault, R. Mechanism of action of N -phenyl- N ′-(2- chloroethyl)ureas in the colchicine-binding site at the interface between α- and β-tubulin Bioorg. Med. Chem. 2009, 17, 3690-3697
41. Fortin, S.; Moreau, E.; Lacroix, J.; Teulade, J. C.; Patenaude, A.; C.-Gaudreault, R. N -Phenyl- N ′-(2-chloroethyl)urea analogues of combretastatin A-4: Is the N -phenyl- N ′-(2-chloroethyl)urea pharmacophore mimicking the trimethoxy phenyl moiety? Bioorg. Med. Chem. Lett. 2007, 17, 2000-2004 (Pubitemid 46389583)
42. Fortin, J. S.; Lacroix, J.; Desjardins, M.; Patenaude, A.; Petitclerc, E.; C.-Gaudreault, R. Alkylation potency and protein specificity of aromatic urea derivatives and bioisosteres as potential irreversible antagonists of the colchicine-binding site Bioorg. Med. Chem. 2007, 15, 4456-4469 (Pubitemid 46777295)
43. 3 adrenergic receptor agonists containing cyclic ureidobenzenesulfonamides Bioorg. Med. Chem. Lett. 1999, 9, 749-754 (Pubitemid 29130282)
44. Anthony, N. J.; Lim, J. J.; Su, D.-S.; Wood, M. R. Arylsulfonamide Derivatives. Patent WO/2005/004810, 2005; Merck & Co., Inc.
45. National Cancer Institute (NCI/NIH), Developmental Therapeutics Program Human Tumor Cell Line Screen. http://dtp.nci.nih.gov/branches/btb/ivclsp.html (accessed February 2, 2011).
46. Fortin, S.; Lacroix, J.; Côté, M.-F.; Moreau, E.; Petitclerc, E.; C.-Gaudreault, R. Quick and simple detection technique to assess the binding of antimicrotubule agents to the colchicine-binding site Biol. Proced. Online 2010, 12, 113-117
47. Schibler, M. J.; Cabral, F. Taxol-dependent mutants of Chinese hamster ovary cells with alterations in α- and β-tubulin J. Cell Biol. 1986, 102, 1522-1531 (Pubitemid 16038095)
48. Cabral, F.; Sobel, M. E.; Gottesman, M. M. CHO mutants resistant to colchicine, colcemid or griseofulvin have an altered β-tubulin Cell 1980, 20, 29-36 (Pubitemid 10117297)
49. Beck, W. T.; Mueller, T. J.; Tanzer, L. R. Altered surface membrane glycoproteins in Vinca alkaloid-resistant human leukemic lymphoblasts Cancer Res. 1979, 39, 2070-2076 (Pubitemid 9185002)
50. Hu, X. F.; Martin, T. J.; Bell, D. R.; de Luise, M.; Zalcberg, J. R. Combined use of cyclosporin A and verapamil in modulating multidrug resistance in human leukemia cell lines Cancer Res. 1990, 50, 2953-2957 (Pubitemid 20170744)
51. Levy, M.; Spino, M.; Read, S. E. Colchicine: a state-of-the-art review Pharmacotherapy 1991, 11, 196-211
52. Jain, A. N. Morphological similarity: a 3D molecular similarity method correlated with protein-ligand recognition J. Comput.-Aided Mol. Des. 2000, 14, 199-213 (Pubitemid 30110675)
53. Struski, S.; Cornillet-Lefebvre, P.; Doco-Fenzy, M.; Dufer, J.; Ulrich, E.; Masson, L.; Michel, N.; Gruson, N.; Potron, G. Cytogenetic characterization of chromosomal rearrangement in a human vinblastine-resistant CEM cell line: use of comparative genomic hybridization and fluorescence in situ hybridization Cancer Genet. Cytogenet. 2002, 132, 51-54 (Pubitemid 34136051)
54. Ueda, K.; Cardarelli, C.; Gottesman, M. M.; Pastan, I. Expression of a full-length cDNA for the human "MDR1" gene confers resistance to colchicine, doxorubicin, and vinblastine Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 3004-3008 (Pubitemid 17064766)
55. Desbene, S.; Giorgi-Renault, S. Drugs that inhibit tubulin polymerization: the particular case of podophyllotoxin and analogues Curr. Med. Chem.: Anti-Cancer Agents 2002, 2, 71-90 (Pubitemid 34649869)
56. Mooberry, S. L. Mechanism of action of 2-methoxyestradiol: new developments Drug Resist. Updates 2003, 6, 355-361 (Pubitemid 38173586)
57. Verenich, S.; Gerk, P. M. Therapeutic promises of 2-methoxyestradiol and its drug disposition challenges Mol. Pharmaceutics 2010, 7, 2030-2039
58. Petitclerc, E.; Boutaud, A.; Prestayko, A.; Xu, J.; Sado, Y.; Ninomiya, Y.; Sarras, M. P., Jr.; Hudson, B. G.; Brooks, P. C. New functions for non-collagenous domains of human collagen type IV. Novel integrin ligands inhibiting angiogenesis and tumor growth in vivo J. Biol. Chem. 2000, 275, 8051-8061 (Pubitemid 30159718)
59. Kim, J.; Yu, W.; Kovalski, K.; Ossowski, L. Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay Cell 1998, 94, 353-362 (Pubitemid 28376079)
60. Uchibayashi, T.; Lee, S. W.; Kunimi, K.; Ohkawa, M.; Endo, Y.; Noguchi, M.; Sasaki, T. Studies of effects of anticancer agents in combination with/without hyperthermia on metastasized human bladder cancer cells in chick embryos using the polymerase chain reaction technique Cancer Chemother. Pharmacol. 1994, 35 (Suppl.) S84-S87
61. Brooks, P. C.; Silletti, S.; von Schalscha, T. L.; Friedlander, M.; Cheresh, D. A. Disruption of angiogenesis by PEX, a noncatalytic metalloproteinase fragment with integrin binding activity Cell 1998, 92, 391-400 (Pubitemid 28093016)
62. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 1970, 227, 680-685
63. Lyu, M. A.; Choi, Y. K.; Park, B. N.; Kim, B. J.; Park, I. K.; Hyun, B. H.; Kook, Y. H. Over-expression of urokinase receptor in human epidermoid-carcinoma cell line (HEp3) increases tumorigenicity on chorio-allantoic membrane and in severe-combined-immunodeficient mice Int. J. Cancer 1998, 77, 257-263
64. SYBYL, version 8.1; Tripos International (1699 South Hanley Rd, St. Louis, MO, 63144, U.S.).