Evaluation of activity and combination strategies with the microtubule-targeting drug sagopilone in breast cancer cell lines

Frontiers in Oncology

Volumn 1, Issue NOV, 2011, Pages

  Eschenbrenner, Julia ^a,b   Winsel, Sebastian ^a,c,d   Hammer, Stefanie ^a   Sommer, Anette ^a   Mittelstaedt, Kevin ^a,c,e   Drosch, Michael ^a,f   Klar, Ulrich ^a   Sachse, Christoph ^g   Hannus, Michael ^g   Seidel, Monika ^g   Weiss, Bertram ^a   Merz, Claudia ^a   Siemeister, Gerhard ^a   Hoffmann, Jens ^a,h  

^a BAYER PHARMA AG   (Germany)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f UNIVERSITY OF BREMEN   (Germany)

^g Cenix BioScience GmbH   (Germany)

^h Experimentelle Pharmakologie und Onkologie Berlin Buch GmbH   (Germany)

Author keywords

Breast cancer; Epothilone; Microtubule stabilizing agent; Mitotic kinesins; RNAi screening; Sagopilone; Spindle assembly checkpoint; Translational cancer research

Indexed keywords

EID: 84873444775     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2011.00044     Document Type: Article

References (54)

1. Aoki, S., Ohta, K., Yamazaki, T., Sugawara, F., and Sakaguchi, K. (2005). Mammalian mitotic centromere-associated kinesin (MCAK): a new molecular target of sulfoquinovosylacylglycerols novel antitumor and immunosuppressive agents. FEBS J. 272, 2132-2140.
2. Bergstralh, D. T., and Ting, J. P.-Y. (2006). Microtubule stabilizing agents: their molecular signaling consequences and the potential for enhancement by drug combination. Cancer Treat. Rev. 32, 166-179.
3. Blagden, S. P., Molife, L. R., Seebaran, A., Payne, M., Reid, A. H., Protheroe, A. S., Vasist, L. S., Williams, D. D., Bowen, C., Kathman, S. J., Hodge, J. P., Dar, M. M., de Bono, J. S., and Middleton, M. R. (2008). A phase I trial of ispinesib, a kinesin spindle protein inhibitor, with docetaxel in patients with advanced solid tumours. Br. J. Cancer 98, 894-899.
4. Brendle, A., Brandt, A., Johansson, R., Enquist, K., Hallmans, G., Hemminki, K., Lenner, P., and Forsti, A. (2008). Single nucleotide polymorphisms in chromosomal instability genes and risk and clinical outcome of breast cancer: a Swedish prospective case-control study. Eur. J. Cancer 45, 435-442.
5. Cailleau, R., Olivé, M., and Cruciger, Q. V. (1978). Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In vitro 14, 911-915.
6. Carvalho, A., Carmena, M., Sambade, C., Earnshaw, W. C., and Wheatley, S. P. (2003). Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J. Cell. Sci. 116, 2987-2998.
7. Castedo, M., Ferri, K., Roumier, T., Metivier, D., Zamzami, N., and Kroemer, G. (2002). Quantitation of mitochondrial alterations associated with apoptosis. J. Immunol. Methods 265, 39-47.
8. Chambers, A. F. (2009). MDA-MB-435 and M14 cell lines: identical but not M14 melanoma? Cancer Res. 69, 5292-5293.
9. Chen, J. G., Yang, C. P., Cammer, M., and Horwitz, S. B. (2003). Gene expression and mitotic exit induced by microtubule-stabilizing drugs. Cancer Res. 63, 7891-7899.
10. Chou, T. C. (2006). Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev. 58, 621-681.
11. Dimri, G. P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelly, C., Medrano, E. E., Linskens, M., and Rubelj, I. (1995). A biomarker that identifies senescent human cells in culture and aging skin. Proc. Natl. Acad. Sci. U.S.A. 92, 9363.
12. Eom, Y. W., Kim, M. A., Park, S. S., Goo, M. J., Kwon, H. J., Sohn, S., Kim, W. H., Yoon, G., and Choi, K. S. (2005). Two distinct modes of cell death induced by doxorubicin: apoptosis and cell death through mitotic catastrophe accompanied by senescence-like phenotype. Oncogene 24, 4765-4777.
13. Forozan, F., Veldman, R., Ammerman, C., Parsa, N., Kallioniemi, A., Kallioniemi, O., and Ethier, S. (1999). Molecular cytogenetic analysis of 11 new breast cancer cell lines. Br. J. Cancer 81, 1328-1334.
14. Gonzalez-Angulo, A., Morales-Vasquez, F., and Hortobagyi, G. (2007). Overview of resistance to systemic therapy in patients with breast cancer. Adv. Exp. Med. Biol. 608, 1-22.
15. Groth-Pedersen, L., Ostenfeld, M., Høyer-Hansen, M., Nylandsted, J., and Jäättelä, M. (2007). Vincristine induces dramatic lysosomal changes and sensitizes cancer cells to lysosomedestabilizing siramesine. Cancer Res. 67, 2217-2225.
16. Hammer, S., Sommer, A., Fichtner, I., Becker, M., Rolff, J., Merk, J., Klar, U., and Hoffmann, J. (2010). Comparative profiling of the novel epothilone, sagopilone, in xenografts derived from primary non-small cell lung cancer. Clin. Cancer Res. 16, 1452-1465.
17. Harrison, M., and Swanton, C. (2008). Epothilones and new analogues of the microtubule modulators in taxane-resistant disease. Expert Opin. Investig. Drugs 17, 523-546.
18. Hatake, K., Tokudome, N., and Ito, Y. (2007). Next generation molecular targeted agents for breast cancer: focus on egfr and vegfr pathways. Breast Cancer 14, 132-149.
19. Hedrick, D. G., Stout, J. R., and Walczak, C. E. (2008). Effects of anti-microtubule agents on microtubule organization in cells lacking the kinesin-13 MCAK. Cell Cycle 7, 2146-2156.
20. Hoffmann, J., Vitale, I., Buchmann, B., Galluzzi, L., Schwede, W., Senovilla, L., Skuballa, W., Vivet, S., Lichtner, R. B., Vicencio, J. M., Panaretakis, T., Siemeister, G., Lage, H., Nanty, L., Hammer, S., Mittelstaedt, K., Winsel, S., Eschenbrenner, J., Castedo, M., Demarche, C., Klar, U., and Kroemer, G. (2008). Improved cellular pharmacokinetics and pharmacodynamics underlie the wide anticancer activity of sagopilone. Cancer Res. 68, 5301-5308.
21. Hollestelle, A., Nagel, J. H., Smid, M., Lam, S., Elstrodt, F., Wasielewski, M., Ng, S. S., French, P. J., Peeters, J. K., Rozendaal, M. J., Riaz, M., Koopman, D. G., Ten Hagen, T. L., de Leeuw, B. H., Zwarthoff, E. C., Teunisse, A., van der Spek, P. J., Klijn, J. G., Dinjens, W. N., Ethier, S. P., Clevers, H., Jochemsen, A. G., den Bakker, M. A., Foekens, J. A., Martens, J. W., and Schutte, M. (2009). Distinct gene mutation profiles among luminal-type and basal-type breast cancer cell lines. Breast Cancer Res. Treat. 121, 53-64.
22. Hollestelle, A., and Schutte, M. (2009). Comment Re: MDA-MB-435 and M14 cell lines: identical but not M14 Melanoma? Cancer Res. 69, 7893.
23. Horwitz, S., Cohen, D., Rao, S., Ringel, I., Shen, H., and Yang, C. (1993). Taxol: mechanisms of action and resistance. J. Natl. Cancer Inst. Monogr. 15, 55-61.
24. Huang, J., Li, X., Hilf, R., Bambara, R., and Muyan, M. (2005). Molecular basis of therapeutic strategies for breast cancer. Curr. Drug Targets Immune Endocr. Metabol. Disord. 5, 379-396.
25. Jordan, M. A., Toso, R. J., Thrower, D., and Wilson, L. (1993). Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc. Natl. Acad. Sci. U.S.A. 90, 9552-9556.
26. Jordan, M. A., and Wilson, L. (2004). Microtubules as target for anticancer drugs. Nat. Rev. Cancer 4, 253-265.
27. Kim, H., Nam, S. W., Rhee, H., Shan Li, L., Ju Kang, H., Hye Koh, K., Kyu Kim, N., Song, J., Tak-Bun Liu, E., and Kim, H. (2004). Different gene expression profiles between microsatellite instability-high and microsatellite stable colorectal carcinomas. Oncogene 23, 6218-6225.
28. Klar, U., Buchmann, B., Schwede, W., Skuballa, W., Hoffmann, J., and Lichtner, R. B. (2006). Total synthesis and antitumor activity of ZK-EPO: the first fully synthetic epothilone in clinical development. Angew. Chem. Int. Ed. Engl. 45, 7942-7948.
29. Lichtner, R. B., Rotgeri, A., Bunte, T., Buchmann, B., Hoffmann, J., Schwede, W., Skuballa, W., and Klar, U. (2001). Subcellular distribution of epothilones in human tumor cells. Proc. Natl. Acad. Sci. U.S.A. 98, 11743-11748.
30. Maehara, Y., Emi, Y., Sakaguchi, Y., Kusumoto, T., Kakeji, Y., Kohnoe, S., and Sugimachi, K. (1990). Estrogen-receptor-negative breast cancer tissue is chemosensitive in vitro compared with estrogen-receptor-positive tissue. Eur. Surg. Res. 22, 50-55.
31. Musacchio, A., and Salmon, E. D. (2007). The spindle assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379-393.
32. National Comprehensive Cancer Network. (2008). NCCN Clinical Practice Guidelines in Oncology: Breast Cancer. Available at: http://www.nccn.org/professionals/physician_gls/PDF/breast.pdf
33. Parkin, D., Bray, F., Ferlay, J., and Pisani, P. (2005). Global cancer statistics, 2002. CA Cancer J. Clin. 55, 74-108.
34. Perou, C., Sørlie, T., Eisen, M., van de Rijn, M., Jeffrey, S., Rees, C., Pollack, J., Ross, D., Johnsen, H., Akslen, L., Fluge, Ø., Pergamenschikov, A., Williams, C., Zhu, S., Lønning, P., Børresen-Dale, A., Brown, P., and Botstein, D. (2000). Molecular portraits of human breast tumours. Nature 406, 747-752.
35. Potti, A., Dressman, H. K., Bild, A., Riedel, R. F., Chan, G., Sayer, R., Cragun, J., Cottrill, H., Kelley, M. J., Petersen, R., Harpole, D., Marks, J., Berchuck, A., Ginsburg, G. S., Febbo, P., Lancaster, J., and Nevins, J. R. (2006). Genomic signatures to guide the use of chemotherapeutics. Nat. Med. 12, 1294-1300.
36. Purcell, J. W., Davis, J., Reddy, M., Martin, S., Samayoa, K., Vo, H., Thomsen, K., Bean, P., Kuo, W. L., Ziyad, S., Billig, J., Feiler, H. S., Gray, J. W., Wood, K. W., and Cases, S. (2010). Activity of the kinesin spindle protein inhibitor ispinesib (SB-715992) in models of breast cancer. Clin. Cancer Res. 16, 566-576.
37. Pusztai, L. (2007). Markers predicting clinical benefit in breast cancer from microtubule-targeting agents. Ann. Oncol. 18(Suppl. 12), xii15-xii20.
38. Risinger, A. L., Giles, F. J., and Mooberry, S. L. (2009). Microtubule dynamics as a target in oncology. Cancer Treat. Rev. 35, 255-261.
39. Sakaushi, S., Nishida, K., Fukada, T., Senda-Murata, K., Oka, S., and Sugimoto, K. (2008). Differential responses of mitotic spindle pole formation to microtubule-stabilizing agents epothilones A and B at low concentrations. Cell Cycle 7, 477-483.
40. Shi, J., Orth, J. D., and Mitchison, T. (2008). Cell type variation in responses to antimitotic drugs that target microtubules and kinesin-5. Cancer Res. 68, 3269-3276.
41. Shimo, A., Tanikawa, C., Nishidate, T., Lin, M. L., Matsuda, K., Park, J. H., Ueki, T., Ohta, T., Hirata, K., Fukuda, M., Nakamura, Y., and Katagiri, T. (2008). Involvement of kinesin family member 2C/mitotic centromere-associated kinesin overexpression in mammary carcinogenesis. Cancer Sci. 99, 62-70.
42. Sørlie, T., Perou, C., Tibshirani, R., Aas, T., Geisler, S., Johnsen, H., Hastie, T., Eisen, M., van de Rijn, M., Jeffrey, S., Thorsen, T., Quist, H., Matese, J., Brown, P., Botstein, D., Lønning, P., and Børresen-Dale, A. (2001). Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. U.S.A. 98, 10869-10874.
43. Sudo, T., Nitta, M., Saya, H., and Ueno, N. T. (2004). Dependence of paclitaxel sensitivity on a functional spindle assembly checkpoint. Cancer Res. 64, 2502-2508.
44. Swanton, C., Marani, M., Pardo, O., Warne, P. H., Kelly, G., Sahai, E., Elustondo, F., Chang, J., Temple, J., Ahmed, A. A., Brenton, J. D., Downward, J., and Nicke, B. (2007). Regulators of mitotic arrest and ceramide metabolism are determinants of sensitivity to paclitaxel and other chemotherapeutic drugs. Cancer Cell 11, 498-512.
45. Swanton, C., Tomlinson, I., and Downward, J. (2006). Chromosomal instability, colorectal cancer and taxane resistance. Cell Cycle 5, 818-823.
46. Tao, W., South, V. J., Zhang, Y., Davide, J. P., Farrell, L., Kohl, N. E., Sepp-Lorenzino, L., and Lobell, R. B. (2005). Induction of apoptosis by an inhibitor of the mitotic kinesin KSP requires both activation of the spindle assembly checkpoint and mitotic slippage. Cancer Cell 8, 49-59.
47. Torres, K., and Horwitz, S. B. (1998). Mechanisms of Taxol-induced cell death are concentration dependent. Cancer Res. 58, 3620-3626.
48. Wahl, A. F., Donaldson, K. L., Fairchild, C., Lee, F. Y., Foster, S. A., Demers, G. W., and Galloway, D. A. (1996). Loss of normal p53 function confers sensitization to Taxol by increasing G2/M arrest and apoptosis. Nat. Med. 2, 72-79.
49. Wang, Y., Klijn, J., Zhang, Y., Sieuwerts, A., Look, M., Yang, F., Talantov, D., Timmermans, M., van Meijer, M. E., Yu, J., Jatkoe, T., Berns, E., Atkins, D., and Foekens, J. (2005). Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365, 671-679.
50. Weaver, B. A., and Cleveland, D. W. (2007). Aneuploidy: instigator and inhibitor of tumorigenesis. Cancer Res. 67, 10103-10105.
51. Whitehurst, A. W., Bodemann, B. O., Cardenas, J., Ferguson, D., Girard, L., Peyton, M., Minna, J. D., Michnoff, C., Hao, W., Roth, M. G., Xie, X. J., and White, M. A. (2007). Synthetic lethal screen identification of chemosensitizer loci in cancer cells. Nature 446, 825-829.
52. Winsel, S., Sommer, A., Eschenbrenner, J., Mittelstaedt, K., Klar, U., Hammer, S., and Hoffmann, J. (2011). Molecular mode of action and role of TP53 in the sensitivity to the novel epothilone sagopilone (ZK-EPO) in A549 non-small cell lung cancer cells. PLoS ONE 6, e19273. doi:10.1371/journal.pone.0019273
53. Zhou, J., Panda, D., Landen, J. W., Wilson, L., and Joshi, H. C. (2002). Minor alteration of microtubule dynamics causes loss of tension across kinetochore pairs and activates the spindle checkpoint. J. Biol. Chem. 277, 17200-17208.
54. Zhu, C., Zhao, J., Bibikova, M., Leverson, J. D., Bossy-Wetzel, E., Fan, J. B., Abraham, R. T., and Jiang, W. (2005). Functional analysis of human microtubule-based motor proteins, the kinesins and dyneins, in mitosis/cytokinesis using RNA interference. Mol. Biol. Cell 16, 3187-3199.