A small-molecule inhibitor targeting the mitotic spindle checkpoint impairs the growth of uterine leiomyosarcoma

Clinical Cancer Research

Volumn 18, Issue 12, 2012, Pages 3352-3365

  Shan, Weiwei ^a   Akinfenwa, Patricia Y ^a   Savannah, Kari B ^b   Kolomeyevskaya, Nonna ^a,d   Laucirica, Rudolfo ^a   Thomas, Dafydd G ^c   Odunsi, Kunle ^d   Creighton, Chad J ^a   Lev, Dina C ^b   Anderson, Matthew L ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; AURORA A KINASE; AURORA B KINASE; CELL PROTEIN; DOCETAXEL; GEMCITABINE; HISTONE H3; MK 5108; POLO LIKE KINASE 1; PROTEIN TPX2; PROTEIN UBE2C; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER SIZE; CANCER TISSUE; CENTROSOME; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG POTENTIATION; DRUG TARGETING; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE PRODUCT; GENOME ANALYSIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LEIOMYOMA; LEIOMYOSARCOMA; M PHASE CELL CYCLE CHECKPOINT; MITOSIS SPINDLE; MOUSE; MYOMETRIUM; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR XENOGRAFT; UTERUS SARCOMA; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CENTROSOME; CYCLOHEXANECARBOXYLIC ACIDS; DEOXYCYTIDINE; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LEIOMYOMA; LEIOMYOSARCOMA; M PHASE CELL CYCLE CHECKPOINTS; MICE; MICE, NUDE; MYOMETRIUM; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; TAXOIDS; THIAZOLES; UTERINE NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84862557239     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-3058     Document Type: Article

References (51)

1. Musacchio A, Hardwick KG. The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 2002;3:731-41.
2. Yu H. Cdc20: a WD40 activator for a cell cycle degradation machine. Mol Cell 2007;27:3-16. (Pubitemid 46991390)
3. Schvartzman JM, Sotillo R, Benezra R. Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat Rev 2010;10:102-15.
4. Bernal JA, Luna R, Espina A, Lazaro I, Ramos-Morales F, Romero F, et al. Human securin interacts with p53 and modulates p53-mediated transcriptional activity and apoptosis. Nat Genet 2002;32:306-11.
5. Hein J, Boichuk S,WuJ, Cheng Y, Freire R, Jat PS, et al. Simian virus 40 large T antigen disrupts genome integrity and activates a DNA damage response via Bub1 binding. J Virol 2009;83:117-27.
6. Marumoto T, Zhang D, Saya H. Aurora-A - a guardian of poles. Nat Rev 2005;5:42-50. (Pubitemid 40052324)
7. Glover DM, Leibowitz MH, McLean DA, Parry H. Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 1995;81:95-105.
8. Giet R, Uzbekov R, Cubizolles F, Le Guellec K, Prigent C. The Xenopus laevis aurora-related protein kinase pEg2 associates with and phosphorylates the kinesin-related protein XlEg5. J Biol Chem 1999;274:15005-13.
9. Hannak E, Kirkham M, Hyman AA, Oegema K. Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans. J Cell Biol 2001;155:1109-16.
10. Vader G, Lens SM. The Aurora kinase family in cell division and cancer. Biochimica et Biophysica Acta 2008;1786:60-72.
11. Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, et al. The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 2003;161:281-94. (Pubitemid 36529847)
12. Gadea BB, Ruderman JV. Aurora kinase inhibitor ZM447439 blocks chromosome-induced spindle assembly, the completion of chromosome condensation, and the establishment of the spindle integrity checkpoint in Xenopus egg extracts. Mol Biol Cell 2005;16:1305-18. (Pubitemid 40349566)
13. Georgieva I, Koychev D, Wang Y, Holstein J, Hopfenmuller W, Zeitz M, et al. ZM447439, a novel promising aurora kinase inhibitor, provokes antiproliferative and proapoptotic effects alone andin combination with bio- and chemotherapeutic agents in gastroenteropancreatic neuroendocrine tumor cell lines. Neuroendocrinology 2010;91:121-30.
14. Li M, Jung A, Ganswindt U, Marini P, Friedl A, Daniel PT, et al. Aurora kinase inhibitor ZM447439 induces apoptosis via mitochondrial pathways. Biochem Pharmacol 2010;79:122-9.
15. Arlot-Bonnemains Y, Baldini E, Martin B, Delcros JG, Toller M, Curcio F, et al. Effects of the Aurora kinase inhibitor VX-680 on anaplastic thyroid cancer-derived cell lines. Endocr Relat Cancer 2008;15:559-68. (Pubitemid 351880843)
16. Harrington EA, Bebbington D, Moore J, Rasmussen RK, Ajose-Adeogun AO, Nakayama T, et al. VX-680, a potent and selective smallmolecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo . Nat Med 2004;10:262-7. (Pubitemid 38667616)
17. Huang XF, Luo SK, Xu J, Li J, Xu DR, Wang LH, et al. Aurora kinase inhibitory VX-680 increases Bax/Bcl-2 ratio and induces apoptosis in Aurora-A-high acute myeloid leukemia. Blood 2008;111:2854-65.
18. Tyler RK, Shpiro N, Marquez R, Eyers PA. VX-680 inhibits Aurora A and Aurora B kinase activity in human cells. Cell Cycle 2007;6:2846-54. (Pubitemid 350277179)
19. Lin JF, Slomovitz BM. Uterine sarcoma 2008. Curr Oncol Reports 2008;10:512-8.
20. Giuntoli RL II, Metzinger DS, DiMarco CS, Cha SS, Sloan JA, Keeney GL, et al. Retrospective review of 208 patients with leiomyosarcoma of the uterus: prognostic indicators, surgical management, and adjuvant therapy. Gynecol Oncol 2003;89:460-9. (Pubitemid 36687793)
21. Thigpen JT, Blessing JA, Beecham J, Homesley H, Yordan E. Phase II trial of cisplatin as first-line chemotherapy in patients with advanced or recurrent uterine sarcomas: a Gynecologic Oncology Group study. J Clin Oncol 1991;9:1962-6.
22. Gallup DG, Blessing JA, Andersen W, Morgan MA. Evaluation of paclitaxel in previously treated leiomyosarcoma of the uterus: a gynecologic oncology group study. Gynecol Oncol 2003;89:48-51. (Pubitemid 36403646)
23. Sutton G, Blessing JA, Ball H. Phase II trial of paclitaxel in leiomyosarcoma of the uterus: a gynecologic oncology group study. Gynecol Oncol 1999;74:346-9. (Pubitemid 29439871)
24. Omura GA, Major FJ, Blessing JA, Sedlacek TV, Thigpen JT, Creasman WT, et al. A randomized study of adriamycin with and without dimethyl triazenoimidazole carboxamide in advanced uterine sarcomas. Cancer 1983;52:626-32. (Pubitemid 13025913)
25. Look KY, Sandler A, Blessing JA, Lucci JA III, Rose PG. Phase II trial of gemcitabine as second-line chemotherapy of uterine leiomyosarcoma: a Gynecologic Oncology Group (GOG) Study. Gynecol Oncol 2004;92:644-7. (Pubitemid 38183157)
26. Hensley ML, Blessing JA, Mannel R, Rose PG. Fixed-dose rate gemcitabine plus docetaxel as first-line therapy for metastatic uterine leiomyosarcoma: a Gynecologic Oncology Group phase II trial. Gynecol Oncol 2008;109:329-34. (Pubitemid 351754961)
27. Hensley ML, Ishill N, Soslow R, Larkin J, Abu-Rustum N, Sabbatini P, et al. Adjuvant gemcitabine plus docetaxel for completely resected stages I-IV high grade uterine leiomyosarcoma: results of a prospective study. Gynecol Oncol 2009;112:563-7.
28. de Vos S, Wilczynski SP, Fleischhacker M, Koeffler P. p53 alterations in uterine leiomyosarcomas versus leiomyomas. Gynecol Oncol 1994;54:205-8.
29. O'Neill CJ, McBride HA, Connolly LE, McCluggage WG. Uterine leiomyosarcomas are characterized by high p16, p53 and MIB1 expression in comparison with usual leiomyomas, leiomyoma variants and smooth muscle tumours of uncertain malignant potential. Histopathology 2007;50:851-8. (Pubitemid 46850073)
30. Xing D, Scangas G, Nitta M, He L, Xu X, Ioffe YJ, et al. A role for BRCA1 in uterine leiomyosarcoma. Cancer Res 2009;69:8231-5.
31. Strizzi L, Bianco C, Hirota M, Watanabe K, Mancino M, Hamada S, et al. Development of leiomyosarcoma of the uterus in MMTV-CR-1 transgenic mice. J Pathol 2007;211:36-44. (Pubitemid 46092027)
32. Lahat G, Zhu QS, Huang KL,Wang S, Bolshakov S, Liu J, et al. Vimentin is a novel anti-cancer therapeutic target; insights from in vitro and in vivo mice xenograft studies. PloS One 2010;5:e10105.
33. Creighton CJ, Fountain MD, Yu Z, Nagaraja AK, Zhu H, Khan M, et al. Molecular profiling uncovers a p53-associated role for microRNA-31 in inhibiting the proliferation of serous ovarian carcinomas and other cancers. Cancer Res 2010;70:1906-15.
34. Duhan N, Sirohiwal D. Uterine myomas revisited. Eur J Obstet Gynecol Reprod Biol 2010;152:119-25.
35. Walter AO, Seghezzi W, Korver W, Sheung J, Lees E. The mitotic serine/threonine kinase Aurora2/AIK is regulated by phosphorylation and degradation. Oncogene 2000;19:4906-16.
36. Macurek L, Lindqvist A, Medema RH. Aurora-A and hBora join the game of Polo. Cancer Res 2009;69:4555-8.
37. Chan EH, Santamaria A, Sillje HH, Nigg EA. Plk1 regulates mitotic Aurora A function through betaTrCP-dependent degradation of hBora. Chromosoma 2008;117:457-69.
38. Shimomura T, Hasako S, Nakatsuru Y, Mita T, Ichikawa K, Kodera T, et al. MK-5108, a highly selective Aurora-A kinase inhibitor, shows antitumor activity alone and in combination with docetaxel. Mol Cancer Ther 2010;9:157-66.
39. Hensley ML, Blessing JA, Degeest K, Abulafia O, Rose PG, Homesley HD. Fixed-dose rate gemcitabine plus docetaxel as second-line therapy for metastatic uterine leiomyosarcoma: a Gynecologic Oncology Group phase II study. Gynecol Oncol 2008;109:323-8.
40. Amant F, Dorfling CM, Dreyer L, Vergote I, Lindeque BG, Van Rensburg EJ. Microsatellite instability in uterine sarcomas. Int J Gynecol Cancer 2001;11:218-23. (Pubitemid 32624385)
41. Laxman R, Currie JL, Kurman RJ, Dudzinski M, Griffin CA. Cytogenetic profile of uterine sarcomas. Cancer 1993;71:1283-8. (Pubitemid 23054920)
42. Packenham JP, du Manoir S, Schrock E, Risinger JI, Dixon D, Denz DN, et al. Analysis of genetic alterations in uterine leiomyomas and leiomyosarcomas by comparative genomic hybridization. Mol Carcinog 1997;19:273-9. (Pubitemid 27392007)
43. Keen N, Taylor S. Aurora-kinase inhibitors as anticancer agents. Nat Rev 2004;4:927-36. (Pubitemid 39626216)
44. Manfredi MG, Ecsedy JA, Meetze KA, Balani SK, Burenkova O, Chen W, et al. Antitumor activity of MLN8054, an orally active small-molecule inhibitor of Aurora A kinase. Proc Natl Acad Sci U S A 2007;104:4106- 11.
45. Tong Y, Ben-Shlomo A, Zhou C, Wawrowsky K, Melmed S. Pituitary tumor transforming gene 1 regulates Aurora kinase A activity. Oncogene 2008;27:6385-95.
46. Bayliss R, Sardon T, Vernos I, Conti E. Structural basis of Aurora-A activation by TPX2 at the mitotic spindle. Mol Cell 2003;12:851-62. (Pubitemid 37352779)
47. Lin YC, Sun SH, Wang FF. Suppression of Polo like kinase 1 (PLK1) by p21(Waf1) mediates the p53-dependent prevention of caspase-independent mitotic death. Cell Signal 2011;23:1816-23.
48. McKenzie L, King S, Marcar L, Nicol S, Dias SS, Schumm K, et al. p53- dependent repression of polo-like kinase-1 (PLK1). Cell Cycle 2010;9:4200-12.
49. Chen L, Yang B. Immunohistochemical analysis of p16, p53, and Ki-67 expression in uterine smooth muscle tumors. Int J Gynecol Pathol 2008;27:326-32.
50. Jeffers MD, Farquharson MA, Richmond JA, McNicol AM. p53 immunoreactivity and mutation of the p53 gene in smooth muscle tumours of the uterine corpus. J Pathol 1995;177:65-70.
51. Mittal K, Demopoulos RI. MIB-1 (Ki-67), p53, estrogen receptor, and progesterone receptor expression in uterine smooth muscle tumors. Hum Pathol 2001;32:984-7. (Pubitemid 32911322)