Inhibitor of Aurora Kinase B Induces Differentially Cell Death and Polyploidy via DNA Damage Response Pathways in Neurological Malignancy: Shedding New Light on the Challenge of Resistance to AZD1152-HQPA

Molecular Neurobiology

Volumn 53, Issue 3, 2016, Pages 1808-1823

  Zekri, Ali ^a,b   Ghaffari, Seyed H ^a   Yaghmaie, Marjan ^a   Estiar, Mehrdad Asghari ^b   Alimoghaddam, Kamran ^a   Modarressi, Mohammad Hossein ^b   Ghavamzadeh, Ardeshir ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

AZD1152 HQPA; DNA damage response pathway; Mitotic catastrophe; Neurological malignancies; P53 p73 status

Indexed keywords

AURORA B KINASE; BARASERTIB; BREAST CANCER RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN P53; PROTEIN P73; 2-((3-((4-((5-(2-((3-FLUOROPHENYL)AMINO)-2-OXOETHYL)-1H-PYRAZOL-3-YL)AMINO)QUINAZOLIN-7-YL)OXY)PROPYL)(ETHYL)AMINO)ETHYL DIHYDROGEN PHOSPHATE; CASPASE 3; DNA; ORGANOPHOSPHATE; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE;

ANTINEOPLASTIC ACTIVITY; APAF1 GENE; ARTICLE; BAD GENE; BAX GENE; CANCER CELL DESTRUCTION; CANCER RESISTANCE; CELL CYCLE; CELL DIFFERENTIATION; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DRUG MECHANISM; ENDOREDUPLICATION; GENE; GENE MUTATION; GENE OVEREXPRESSION; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; NEUROBLASTOMA; NEUROBLASTOMA CELL LINE; POLYPLOIDY; PUMA GENE; UPREGULATION; WILD TYPE; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BRAIN NEOPLASMS; CELL DEATH; CELL DIVISION; CELL SHAPE; CELL SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GERMLINE MICRONUCLEUS; METABOLISM; MULTIDRUG RESISTANCE; MUTATION; PATHOLOGY; TUMOR CELL LINE; TUMOR STEM CELL ASSAY;

AURORA KINASE B; BRAIN NEOPLASMS; CASPASE 3; CELL CYCLE; CELL DEATH; CELL DIVISION; CELL LINE, TUMOR; CELL SHAPE; CELL SURVIVAL; DNA DAMAGE; DNA, NEOPLASM; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRONUCLEUS, GERMLINE; MUTATION; ORGANOPHOSPHATES; POLYPLOIDY; PROTEIN KINASE INHIBITORS; QUINAZOLINES; TRANSCRIPTION, GENETIC; TUMOR STEM CELL ASSAY;

EID: 84961116388     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9139-9     Document Type: Article

References (41)

1. Khasraw M, Lassman AB (2010) Advances in the treatment of malignant gliomas. Curr Oncol Rep 12(1):26–33. doi:10.1007/s11912-009-0077-4
2. Brodeur GM (2003) Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 3(3):203–216. doi:10.1038/nrc1014
3. Hontz AE, Li SA, Lingle WL, Negron V, Bruzek A, Salisbury JL, Li JJ (2007) Aurora A and B overexpression and centrosome amplification in early estrogen-induced tumor foci in the Syrian hamster kidney: implications for chromosomal instability, aneuploidy, and neoplasia. Cancer Res 67(7):2957–2963
4. Carmena M, Earnshaw WC (2003) The cellular geography of aurora kinases. Nat Rev 4(11):842–854
5. Zeng WF, Navaratne K, Prayson RA, Weil RJ (2007) Aurora B expression correlates with aggressive behaviour in glioblastoma multiforme. J Clin Pathol 60(2):218–221. doi:10.1136/jcp.2006.036806
6. Chieffi P, Cozzolino L, Kisslinger A, Libertini S, Staibano S, Mansueto G, De Rosa G, Villacci A et al (2006) Aurora B expression directly correlates with prostate cancer malignancy and influence prostate cell proliferation. Prostate 66(3):326–333. doi:10.1002/pros.20345
7. Li D, Zhu J, Firozi PF, Abbruzzese JL, Evans DB, Cleary K, Friess H, Sen S (2003) Overexpression of oncogenic STK15/BTAK/Aurora A kinase in human pancreatic cancer. Clin Cancer Res 9(3):991–997
8. Ulisse S, Delcros JG, Baldini E, Toller M, Curcio F, Giacomelli L, Prigent C, Ambesi-Impiombato FS et al (2006) Expression of Aurora kinases in human thyroid carcinoma cell lines and tissues. Int J Cancer 119(2):275–282. doi:10.1002/ijc.21842
9. Ikezoe T, Yang J, Nishioka C, Tasaka T, Taniguchi A, Kuwayama Y, Komatsu N, Bandobashi K et al (2007) A novel treatment strategy targeting Aurora kinases in acute myelogenous leukemia. Mol Cancer Ther 6(6):1851–1857. doi:10.1158/1535-7163.MCT-07-0067
10. Michaelis M, Selt F, Rothweiler F, Loschmann N, Nusse B, Dirks WG, Zehner R, Cinatl J Jr (2014) Aurora kinases as targets in drug-resistant neuroblastoma cells. PLoS One 9(9):e108758. doi:10.1371/journal.pone.0108758
11. Borges KS, Castro-Gamero AM, Moreno DA, da Silva SV, Brassesco MS, de Paula Queiroz RG, de Oliveira HF, Carlotti CG Jr et al (2012) Inhibition of Aurora kinases enhances chemosensitivity to temozolomide and causes radiosensitization in glioblastoma cells. J Cancer Res Clin Oncol 138(3):405–414. doi:10.1007/s00432-011-1111-0
12. Morozova O, Vojvodic M, Grinshtein N, Hansford LM, Blakely KM, Maslova A, Hirst M, Cezard T et al (2010) System-level analysis of neuroblastoma tumor-initiating cells implicates AURKB as a novel drug target for neuroblastoma. Clin Cancer Res 16(18):4572–4582. doi:10.1158/1078-0432.CCR-10-0627
13. Van Brocklyn JR, Wojton J, Meisen WH, Kellough DA, Ecsedy JA, Kaur B, Lehman NL (2014) Aurora-A inhibition offers a novel therapy effective against intracranial glioblastoma. Cancer Res 74(19):5364–5370. doi:10.1158/0008-5472.CAN-14-0386
14. Hong X, O’Donnell JP, Salazar CR, Van Brocklyn JR, Barnett KD, Pearl DK, deCarvalho AC, Ecsedy JA et al (2014) The selective Aurora-A kinase inhibitor MLN8237 (alisertib) potently inhibits proliferation of glioblastoma neurosphere tumor stem-like cells and potentiates the effects of temozolomide and ionizing radiation. Cancer Chemother Pharmacol 73(5):983–990. doi:10.1007/s00280-014-2430-z
15. Dennis M, Davies M, Oliver S, D’Souza R, Pike L, Stockman P (2012) Phase I study of the Aurora B kinase inhibitor barasertib (AZD1152) to assess the pharmacokinetics, metabolism and excretion in patients with acute myeloid leukemia. Cancer Chemother Pharmacol 70(3):461–469. doi:10.1007/s00280-012-1939-2
16. Schwartz GK, Carvajal RD, Midgley R, Rodig SJ, Stockman PK, Ataman O, Wilson D, Das S et al (2012) Phase I study of barasertib (AZD1152), a selective inhibitor of Aurora B kinase, in patients with advanced solid tumors. Invest New Drugs. doi:10.1007/s10637-012-9825-7
17. Zekri A, Ghaffari SH, Ghanizadeh-Vesali S, Yaghmaie M, Salmaninejad A, Alimoghaddam K, Modarressi MH, Ghavamzadeh A (2014) AZD1152-HQPA induces growth arrest and apoptosis in androgen-dependent prostate cancer cell line (LNCaP) via producing aneugenic micronuclei and polyploidy. Tumour Biol. doi:10.1007/s13277-014-2664-8
18. Pluim D, Beijnen JH, Schellens JH, van Tellingen O (2009) Simultaneous determination of AZD1152 (prodrug) and AZD1152-hydroxyquinazoline pyrazol anilide by reversed phase liquid chromatography. J Chromatogr B Anal Technol Biomed Life Sci 877(29):3549–3555. doi:10.1016/j.jchromb.2009.08.035
19. Talos F, Nemajerova A, Flores ER, Petrenko O, Moll UM (2007) p73 suppresses polyploidy and aneuploidy in the absence of functional p53. Mol Cell 27(4):647–659. doi:10.1016/j.molcel.2007.06.036
20. Aihara A, Tanaka S, Yasen M, Matsumura S, Mitsunori Y, Murakata A, Noguchi N, Kudo A et al (2010) The selective Aurora B kinase inhibitor AZD1152 as a novel treatment for hepatocellular carcinoma. J Hepatol 52(1):63–71. doi:10.1016/j.jhep.2009.10.013
21. Tao Y, Zhang P, Girdler F, Frascogna V, Castedo M, Bourhis J, Kroemer G, Deutsch E (2008) Enhancement of radiation response in p53-deficient cancer cells by the Aurora-B kinase inhibitor AZD1152. Oncogene 27(23):3244–3255. doi:10.1038/sj.onc.1210990
22. Freed-Pastor WA, Prives C (2012) Mutant p53: one name, many proteins. Genes Dev 26(12):1268–1286. doi:10.1101/gad.190678.112
23. Fenech M (2000) The in vitro micronucleus technique. Mutat Res 455(1–2):81–95
24. Davidoff AM, Pence JC, Shorter NA, Iglehart JD, Marks JR (1992) Expression of p53 in human neuroblastoma- and neuroepithelioma-derived cell lines. Oncogene 7(1):127–133
25. Gartel AL, Tyner AL (2002) The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol Cancer Ther 1(8):639–649
26. Kaghad M, Bonnet H, Yang A, Creancier L, Biscan JC, Valent A, Minty A, Chalon P et al (1997) Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers. Cell 90(4):809–819
27. Girdler F, Sessa F, Patercoli S, Villa F, Musacchio A, Taylor S (2008) Molecular basis of drug resistance in aurora kinases. Chem Biol 15(6):552–562. doi:10.1016/j.chembiol.2008.04.013
28. Walsby E, Walsh V, Pepper C, Burnett A, Mills K (2008) Effects of the aurora kinase inhibitors AZD1152-HQPA and ZM447439 on growth arrest and polyploidy in acute myeloid leukemia cell lines and primary blasts. Haematologica 93(5):662–669. doi:10.3324/haematol.12148
29. Sasai K, Katayama H, Stenoien DL, Fujii S, Honda R, Kimura M, Okano Y, Tatsuka M et al (2004) Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil Cytoskeleton 59(4):249–263. doi:10.1002/cm.20039
30. Guo J, Anderson MG, Tapang P, Palma JP, Rodriguez LE, Niquette A, Li J, Bouska JJ et al (2009) Identification of genes that confer tumor cell resistance to the aurora B kinase inhibitor, AZD1152. Pharmacogenomics J 9(2):90–102. doi:10.1038/tpj.2008.20
31. Talos F, Moll UM (2010) Role of the p53 family in stabilizing the genome and preventing polyploidization. Adv Exp Med Biol 676:73–91
32. Tsuiki H, Nitta M, Tada M, Inagaki M, Ushio Y, Saya H (2001) Mechanism of hyperploid cell formation induced by microtubule inhibiting drug in glioma cell lines. Oncogene 20(4):420–429
33. Tomasini R, Mak TW, Melino G (2008) The impact of p53 and p73 on aneuploidy and cancer. Trends Cell Biol 18(5):244–252. doi:10.1016/j.tcb.2008.03.003
34. Stukenberg PT (2004) Triggering p53 after cytokinesis failure. J Cell Biol 165(5):607–608. doi:10.1083/jcb.200405089
35. Sak A, Stuschke M, Groneberg M, Kubler D, Pottgen C, Eberhardt WE (2012) Inhibiting the aurora B kinase potently suppresses repopulation during fractionated irradiation of human lung cancer cell lines. Int J Radiat Oncol Biol Phys 84(2):492–499. doi:10.1016/j.ijrobp.2011.12.021
36. Diaz RJ, Golbourn B, Shekarforoush M, Smith CA, Rutka JT (2012) Aurora kinase B/C inhibition impairs malignant glioma growth in vivo. J Neurooncol 108(3):349–360. doi:10.1007/s11060-012-0835-2
37. Yu J, Zhang H, Gu J, Lin S, Li J, Lu W, Wang Y, Zhu J (2004) Methylation profiles of thirty four promoter-CpG islands and concordant methylation behaviours of sixteen genes that may contribute to carcinogenesis of astrocytoma. BMC Cancer 4:65. doi:10.1186/1471-2407-4-65
38. Stokes MP, Rush J, Macneill J, Ren JM, Sprott K, Nardone J, Yang V, Beausoleil SA et al (2007) Profiling of UV-induced ATM/ATR signaling pathways. Proc Natl Acad Sci U S A 104(50):19855–19860. doi:10.1073/pnas.0707579104
39. Vitale I, Galluzzi L, Castedo M, Kroemer G (2011) Mitotic catastrophe: a mechanism for avoiding genomic instability. Nat Rev Mol Cell Biol 12(6):385–392. doi:10.1038/nrm3115
40. Bassing CH, Alt FW (2004) The cellular response to general and programmed DNA double strand breaks. DNA Repair 3(8–9):781–796
41. Featherstone C, Jackson SP (1999) DNA double-strand break repair. Curr Biol 9(20):R759–R761