A synthetic dolastatin 10 analogue suppresses microtubule dynamics, inhibits cell proliferation, and induces apoptotic cell death

Journal of Medicinal Chemistry

Volumn 56, Issue 6, 2013, Pages 2235-2245

  Gajula, Praveen Kumar ^a   Asthana, Jayant ^b   Panda, Dulal ^b   Chakraborty, Tushar Kanti ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

^b INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BUB1 RELATED PROTEIN; DOLASTATIN 10; PROTEIN MAD2; STRESS ACTIVATED PROTEIN KINASE; TUBULIN;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL PROLIFERATION; CELL STRAIN MCF 7; CENTROMERE; CONTROLLED STUDY; DEPOLYMERIZATION; G2 PHASE CELL CYCLE CHECKPOINT; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; M PHASE CELL CYCLE CHECKPOINT; MICROTUBULE ASSEMBLY;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 3; CELL PROLIFERATION; COLCHICINE; DEPSIPEPTIDES; DRUG INTERACTIONS; DRUG RESISTANCE, NEOPLASM; GTP PHOSPHOHYDROLASES; HELA CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KINETOCHORES; MCF-7 CELLS; MICROTUBULES; MITOSIS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; TUBULIN; VINBLASTINE;

EID: 84875726864     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm3009629     Document Type: Article

References (61)

1. Aherne, G. W.; Hardcastle, A.; Valenti, M.; Bryant, A.; Rogers, P.; Pettit, G. R.; Srirangam, J. K.; Kelland, L. R. Antitumour evaluation of dolastatins 10 and 15 and their measurement in plasma by radioimmunoassay Cancer Chemother. Pharmacol. 1996, 38, 225-232
2. Sato, M.; Sagawa, M.; Nakazato, T.; Ikeda, Y.; Kizaki, M. A natural peptide, dolastatin 15, induces G2/M cell cycle arrest and apoptosis of human multiple myeloma cells Int. J. Oncol. 2007, 30, 1453-1459
3. Verdier-Pinard, P.; Kepler, J. A.; Pettit, G. R.; Hamel, E. Sustained intracellular retention of dolastatin 10 causes its potent antimitotic activity Mol. Pharmacol. 2000, 57, 180-187
4. Maki, A.; Mohammad, R.; Raza, S.; Saleh, M.; Govindaraju, K. D.; Pettit, G. R.; al-Katib, A. Effect of dolastatin 10 on human non-Hodgkin's lymphoma cell lines Anticancer Drugs 1996, 7, 344-350
5. Fujita, F.; Koike, M.; Fujita, M.; Sakamoto, Y.; Tsukagoshi, S. Antitumor effects of TZT-1027, a novel dolastatin 10 derivative, on human tumor xenografts in nude mice Gan To Kagaku Ryoho 2000, 27, 451-458
6. Shnyder, S. D.; Cooper, P. A.; Millington, N. J.; Pettit, G. R.; Bibby, M. C. Auristatin PYE, a novel synthetic derivative of dolastatin 10, is highly effective in human colon tumour models Int. J. Oncol. 2007, 31, 353-360
7. Schöffski, P.; Thate, B.; Beutel, G.; Bolte, O.; Otto, D.; Hofmann, M.; Ganser, A.; Jenner, A.; Cheverton, P.; Wanders, J.; Oguma, T.; Atsumi, R.; Satomi, M. Phase I and pharmacokinetic study of TZT-1027, a novel synthetic dolastatin 10 derivative, administered as a 1-h intravenous infusion every 3 weeks in patients with advanced refractory cancer Ann. Oncol. 2004, 15, 671-679
8. Kalemkerian, G. P.; Ou, X.; Adil, M. R.; Rosati, R.; Khoulani, M. M.; Madan, S. K.; Pettit, G. R. Activity of dolastatin 10 against small-cell lung cancer in vitro and in vivo: induction of apoptosis and bcl-2 modification Cancer Chemother. Pharmacol. 1999, 43, 507-515
9. de Arruda, M.; Cocchiaro, C. A.; Nelson, C. M.; Grinnell, C. M.; Janssen, B.; Haupt, A.; Barlozzari, T. LU103793 (NSC D-669356): a synthetic peptide that interacts with microtubules and inhibits mitosis Cancer Res. 1995, 55, 3085-3092
10. Bai, R.; Friedman, S. J.; Pettit, G. R.; Hamel, E. Dolastatin 15, a potent antimitotic depsipeptide derived from Dolabella auricularia: interaction with tubulin and effects of cellular microtubules Biochem. Pharmacol. 1992, 43, 2637-2645
11. Bai, R.; Pettit, G. R.; Hamel, E. Binding of dolastatin 10 to tubulin at a distinct site for peptide antimitotic agents near the exchangeable nucleotide and vinca alkaloid sites J. Biol. Chem. 1990, 265, 17141-17149
12. Bai, R.; Pettit, G. R.; Hamel, E. Dolastatin 10, a powerful cytostatic peptide derived from a marine animal. Inhibition of tubulin polymerization mediated through the vinca alkaloid binding domain Biochem. Pharmacol. 1990, 39, 1941-1949
13. Mitra, A.; Sept, D. Localization of the antimitotic peptide and depsipeptide binding site on beta-tubulin Biochemistry 2004, 43, 13955-13962
14. Bai, R.; Covell, D. G.; Taylor, G. F.; Kepler, J. A.; Copeland, T. D.; Nguyen, N. Y.; Pettit, G. R.; Hamel, E. Direct photoaffinity labeling by dolastatin 10 of the amino-terminal peptide of beta-tubulin containing cysteine 12 J. Biol. Chem. 2004, 279, 30731-30740
15. de Jonge, M, J.; van der Gaast, A.; Planting, A. S.; van Doorn, L.; Lems, A.; Boot, I.; Wanders, J.; Satomi, M.; Verweij, J. Phase I and pharmacokinetic study of the dolastatin 10 analogue TZT-1027, given on days 1 and 8 of a 3-week cycle in patients with advanced solid tumors Clin. Cancer Res. 2005, 11, 3806-3813
16. Molinski, T. F.; Dalisay, D. S.; Lievens, S. L.; Saludes, J. P. Drug development from marine natural products Nature Rev. Drug Discovery 2009, 8, 69-85
17. Risseeuw, M. D. P.; Overhand, M.; Fleet, G. W. J.; Simone, M. I. A compendium of sugar amino acids (SAA): scaffolds, peptide- and glycol-mimetics Tetrahedron: Asymmetry 2007, 18, 2001-2010
18. Jensen, K. J.; Brask, J. Carbohydrates in peptide and protein design Pept. Sci. 2005, 80, 747-761
19. Chakraborty, T. K.; Srinivasu, P.; Tapadar, S.; Mohan, B. K. Sugar amino acids in designing new molecules Glycoconjugate J. 2005, 22, 83-93
20. Chakraborty, T. K.; Srinivasu, P.; Tapadar, S.; Mohan, B. K. Sugar amino acids and related molecules: some recent developments J. Chem. Sci. 2004, 116, 187-207
21. Gruner, S. A. W.; Locardi, E.; Lohof, E.; Kessler, H. Carbohydrate-Based Mimetics in Drug Design: Sugar Amino Acids and Carbohydrate Scaffolds Chem. Rev. 2002, 102, 491-514
22. Schweizer, F. Glycosamino Acids: Building Blocks for Combinatorial Synthesis-Implication for Drug Discovery Angew Chem. Int. Ed. 2002, 41, 230-253
23. Chakraborty, T. K.; Ghosh, S.; Jayaprakash, S. Sugar amino acids and their uses in designing bioactive molecules Curr. Med. Chem. 2002, 9, 421-435
24. Chakraborty, T. K.; Jayaprakash, S.; Ghosh, S. Sugar amino acid based scaffolds-novel peptidomimetics and their potential in combinatorial synthesis Comb. Chem. High Throughput Screening 2002, 5, 373-387
25. Peri, F.; Cipolla, L.; Forni, E.; La Ferla, B.; Nicotra, F. Sugar-derived amino acids: powerful secondary structure-inducing elements in the design of novel peptidomimetics Chemtracts: Org. Chem. 2001, 14, 481-499
26. Gervay-Hague, J.; Weathers, T. M., Jr. Pyranosyl sugar amino acid conjugates: their biological origins, synthetic preparations and structural characterisation. In Glycochemistry: Principles, Synthesis and Applications; Wang, P. G; Bertozzi, C. R., Eds.; Marcel Dekker: New York, 2001.
27. Alattiat, T.; Roux, F.; Poncet, J.; Cavét, A.; Jouin, P. Conformational study of dolastatin 10 Tetrahedron 1995, 51, 2593-2604
28. Bai, R.; Taylor, G. F.; Schmidt, J. M.; Williams, M. D.; Kepler, J. A.; Pettit, G. R.; Hamel, E. Interaction of dolastatin 10 with tubulin: induction of aggregation and binding and dissociation reactions Mol. Pharmacol. 1995, 47, 965-976
29. Jordan, M. A.; Wilson, L. Microtubules as a target for anticancer drugs Nature Rev. Cancer 2004, 4, 253-265
30. Dumontet, C.; Jordan, M. A. Microtubule-binding agents: a dynamic field of cancer therapeutics Nature Rev. Drug Discovery 2010, 9, 790-803
31. Singh, P.; Rathinasamy, K.; Mohan, R.; Panda, D. Microtubule assembly dynamics: an attractive target for anticancer drugs IUBMB Life 2008, 60, 368-375
32. Mohan, R.; Panda, D. Kinetic stabilization of microtubule dynamics by estramustine is associated with tubulin acetylation, spindle abnormalities, and mitotic arrest Cancer Res. 2008, 68, 6181-6189
33. Rathinasamy, K.; Jindal, B.; Asthana, J.; Singh, P.; Balaji, P. V.; Panda, D. Griseofulvin stabilizes microtubule dynamics activates p53 and inhibits the proliferation of MCF-7 cells synergistically with vinblastine BMC Cancer 2010, 19, 213-225
34. Rathinasamy, K.; Panda, D. Kinetic stabilization of microtubule dynamic instability by benomyl increases the nuclear transport of p53 Biochem. Pharmacol. 2008, 76, 1669-1680
35. Kamath, K.; Jordan, M. A. Suppression of microtubule dynamics by epothilone B is associated with mitotic arrest Cancer Res. 2003, 63, 6026-6031
36. Skoufias, D. A.; Andreassen, P. R.; Lacroix, F. B.; Wilson, L.; Margolis, R. L. Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 4492-4497
37. Zhou, J.; Yao, J.; Joshi, H. C. Attachment and tension in the spindle assembly checkpoint J. Cell Sci. 2002, 115, 3547-3555
38. Bai, R.; Roach, M. C.; Jayaram, S. K.; Barkoczy, J.; Pettit, G. R.; Ludueña, R. F.; Hamel, E. Differential effects of active isomers, segments, and analogs of dolastatin 10 on ligand interactions with tubulin. Correlation with cytotoxicity Biochem. Pharmacol. 1993, 45, 1503-1515
39. Bai, R. L.; Pettit, G. R.; Hamel, E. Structure-activity studies with chiral isomers and with segments of the antimitotic marine peptide dolastatin 10 Biochem. Pharmacol. 1990, 40, 1859-1864
40. Rebacz, B.; Larsen, T. O.; Clausen, M. H.; Rønnest, M. H.; Löffler, H.; Ho, A. D.; Kramer, A. Identification of griseofulvin as an inhibitor of centrosomal clustering in a phenotype-based screen Cancer Res. 2007, 67, 6342-6350
41. Hoyt, M. A.; Totis, L.; Roberts, B. T. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function Cell 1991, 66, 507-517
42. Meraldi, P.; Draviam, V. M.; Sorger, P. K. Timing and checkpoints in the regulation of mitotic progression Dev. Cell 2004, 7, 45-60
43. Chan, G. K.; Jablonski, S. A.; Sudakin, V.; Hittle, J. C.; Yen, T. J. Human BUBR1 is a mitotic checkpoint kinase that monitors CENP-E functions at kinetochores and binds the cyclosome/APC J. Cell Biol. 1999, 146, 941-954
44. Chen, Y.; Wu, Q.; Song, S. Y.; Su, W. J. Activation of JNK by TPA promotes apoptosis via PKC pathway in gastric cancer cells World J. Gastroenterol. 2002, 8, 1014-1018
45. Kuan, C. Y.; Yang, D. D.; Samanta, Roy, D. R.; Davis, R. J.; Rakic, P.; Flavell, R. A. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development Neuron 1999, 22, 667-676
46. Dziadyk, J. M.; Sui, M.; Zhu, X.; Fan, W. Paclitaxel-induced apoptosis may occur without a prior G2/M-phase arrest Anticancer Res. 2004, 24, 27-36
47. Pourroy, B.; Carré, M.; Honoré, S.; Bourgarel-Rey, V.; Kruczynski, A.; Briand, C.; Braguer, D. Low concentrations of vinflunine induce apoptosis in human SK-N-SH neuroblastoma cells through a post mitotic G1 arrest and a mitochondrial pathway Mol. Pharmacol. 2004, 66, 580-591
48. Yvon, A. M.; Wadsworth, P.; Jordan, M. A. Taxol suppresses dynamics of individual microtubules in living human tumor cells Mol. Biol. Cell 1999, 10, 947-959
49. Turner, T.; Jackson, W. H.; Pettit, G. R.; Wells, A.; Kraft, A. S. Treatment of human prostate cancer cells with dolastatin 10, a peptide isolated from a marine shell-less mollusc Prostate 1998, 34, 175-181
50. Panda, D.; Rathinasamy, K.; Santra, M. K.; 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
51. Rathinasamy, K.; Panda, D. Suppression of microtubule dynamics by benomyl decreases tension across kinetochore pairs and induces apoptosis in cancer cells FEBS J. 2006, 273, 4114-4128
52. Srivastava, P.; Panda, D. Rotenone inhibits mammalian cell proliferation by inhibiting microtubule assembly through tubulin binding FEBS J. 2007, 274, 4788-4801
53. Zhu, N.; Wang, Z. An assay for DNA fragmentation in apoptosis without phenol/chloroform extraction and ethanol precipitation Anal. Biochem. 1997, 246, 155-158
54. Gupta, K.; Panda, D. Perturbation of microtubule polymerization by quercetin through tubulin binding: a novel mechanism of its antiproliferative activity Biochemistry 2002, 41, 13029-13038
55. Gupta, K. K.; Bharne, S. S.; Rathinasamy, K.; Naik, N. R.; Panda, D. Dietary antioxidant curcumin inhibits microtubule assembly through tubulin binding FEBS J. 2006, 273, 5320-5332
56. Geladopoulos, T. P.; Sotiroudis, T. G.; Evangelopoulos, A. E. A malachite green colorimetric assay for protein phosphatase activity Anal. Biochem. 1991, 192, 112-116
57. Tnimov, Z.; Guo, Z.; Gambin, Y.; Nguyen, U. T.; Wu, Y. W.; Abankwa, D.; Stigter, A.; Collins, B. M.; Waldmann, H.; Goody, R. S.; Alexandrov, K. Quantitative analysis of prenylated RhoA interaction with its chaperone, RhoGDI J. Biol. Chem. 2012, 287, 26549-26562
58. Otto-Bruc, A.; Antonny, B.; Vuong, T. M.; Chardin, P.; Chabre, M. Interaction between the retinal cyclic GMP phosphodiesterase inhibitor and transducin. Kinetics and affinity studies Biochemistry 1993, 32, 8636-8645
59. Chou, T. C.; Talalay, P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors Adv. Enzyme Regul. 1984, 22, 27-55
60. Chou, T. C.; Talalay, P. Analysis of Combined Drug Effects-A New Look at A Very Old Problem Trends Pharmacol. Sci. 1983, 4, 450-454
61. Clement, M. J.; Rathinasamy, K.; Adjadj, E.; Toma, F.; Curmi, P. A.; Panda, D. Benomyl and colchicine synergistically inhibit cell proliferation and mitosis: evidence of distinct binding sites for these agents in tubulin Biochemistry 2008, 47, 13016-13025