Aurora A is differentially expressed in gliomas, is associated with patient survival in glioblastoma, and is a potential chemotherapeutic target in gliomas

Cell Cycle

Volumn 11, Issue 3, 2012, Pages 489-502

  Lehman, Norman L ^a,b   O'Donnell, James P ^a   Whiteley, Lisa J ^a   Stapp, Robert T ^a   Lehman, Trang D ^a   Roszka, Kathleen M ^a   Schultz, Lonni R ^a,b   Williams, Caitlin J ^a   Mikkelsen, Tom ^a,b   Brown, Stephen L ^a   Ecsedy, Jeffrey A ^c   Poisson, Laila M ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MILLENNIUM PHARMACEUTICALS INC   (United States)

Author keywords

Aurora A; Differential expression; Diffuse astrocytoma; Ependymoma; Glioblastoma; MLN8237; Oligodendroglioma; Patient survival; Pilocytic astrocytoma; Radiation

Indexed keywords

ALISERTIB; AURORA A KINASE; MESSENGER RNA;

ARTICLE; BRAIN TISSUE; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER GRADING; CANCER SURVIVAL; CELL DIFFERENTIATION; CONTROLLED STUDY; DISEASE ASSOCIATION; EPENDYMOMA; EPILEPSY; FEMALE; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IC 50; IONIZING RADIATION; KAPLAN MEIER METHOD; MALE; MOUSE; NONHUMAN; OLIGODENDROGLIOMA; PILOCYTIC ASTROCYTOMA; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RETROSPECTIVE STUDY; SENESCENCE; WESTERN BLOTTING; WORLD HEALTH ORGANIZATION;

EID: 84857230742     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.11.3.18996     Document Type: Article

References (57)

1. Zhou H, Kuang J, Zhong L, Kuo WL, Gray JW, Sahin A, et al. Tumour amplified kinase STK15/ BTAK induces centrosome amplification, aneuploidy and transformation. Nat Genet 1998; 20:189-93; PMID:9771714; http://dx.doi.org/10. 1038/2496.
2. Marumoto T, Honda S, Hara T, Nitta M, Kohmura E, Saya H. Aurora A kinase maintains the fidelity of early and late mitotic events in HeLa cells. J Biol Chem 2003; 278:51786-95; PMID:14523000; http://dx.doi. org/10.1074/jbc. M306275200.
3. Seki A, Coppinger JA, Jang CY, Yates JR, Fang G. Bora and the kinase Aurora A cooperatively activate the kinase Plk1 and control mitotic entry. Science 2008; 320:1655-8; PMID:18566290; http://dx.doi. org/10.1126/science. 1157425.
4. Song SJ, Song MS, Kim SJ, Kim SY, Kwon SH, Kim JG, et al. Aurora A regulates prometaphase progression by inhibiting the ability of RASSF1A to suppress APC-Cdc20 activity. Cancer Res 2009; 69:2314-23; PMID:19276349; http://dx.doi.org/10.1158/0008-5472.CAN-08-3984.
5. Otto T, Horn S, Brockmann M, Eilers U, Schüttrumpf L, Popov N, et al. Stabilization of N-Myc is a critical function of Aurora A in human neuroblastoma. Cancer Cell 2009; 15:67-78; PMID:19111882; http://dx.doi. org/10.1016/j.ccr.2008.12.005.
6. Dar AA, Belkhiri A, El-Rifai W. The Aurora kinase A regulates GSK-3â in gastric cancer cells. Oncogene 2009; 28:866-75; PMID:19060929; http://dx.doi. org/10.1038/onc.2008.434.
7. Yang H, Ou CC, Feldman RI, Nicosia SV, Kruk PA, Cheng JQ. Aurora A kinase regulates telomerase activity through c-Myc in human ovarian and breast epithelial cells. Cancer Res 2004; 64:463-7; PMID:14744757; http://dx.doi.org/ 10.1158/0008-5472.CAN-03-2907.
8. Sasayama T, Marumoto T, Kunitoku N, Zhang D, Tamaki N, Kohmura E, et al. Overexpression of Aurora A targets cytoplasmic polyadenylation element binding protein and promotes mRNA polyadenylation of Cdk1 and Cyclin B1. Genes Cells 2005; 10:627-38; PMID:15966895; http://dx.doi.org/10.1111/j.1365- 2443.2005.00870.x.
9. Qin L, Tong T, Song Y, Xue L, Fan F, Zhan Q. Aurora A interacts with Cyclin B1 and enhances its stability. Cancer Lett 2009; 275:77-85; PMID:19028417; http://dx.doi.org/10.1016/j.canlet.2008.10.011.
10. Tomita M, Toyota M, Ishikawa C, Nakazato T, Okudaira T, Matsuda T, et al. Overexpression of Aurora A by loss of CHFR gene expression increases the growth and survival of HTLV-1-infected T cells through enhanced NFkappaB activity. Int J Cancer 2009; 124:2607-15; PMID:19230025; http://dx.doi. org/10.1002/ijc. 24257.
11. He L, Yang H, Ma Y, Pledger WJ, Cress WD, Cheng JQ. Identification of Aurora A as a direct target of E2F3 during G2/M cell cycle progression. J Biol Chem 2008; 283:31012-20; PMID:18776222; http://dx.doi. org/10.1074/jbc. M803547200.
12. Tanaka M, Ueda A, Kanamori H, Ideguchi H, Yang J, Kitajima S, et al. Cell cycle-dependent regulation of human Aurora A transcription is mediated by periodic repression of E4TF1. J Biol Chem 2002; 277:10719- 26; PMID:11790771; http://dx.doi.org/10.1074/jbc. M108252200.
13. Klein A, Flügel D, Kietzmann T. Transcriptional regulation of serine/threonine kinase-15 (STK15) expression by hypoxia and HIF-1. Mol Biol Cell 2008; 19:3667-75; PMID:18562694; http://dx.doi.org/10.1091/mbc. E08-01-0042.
14. den Hollander J, Rimpi S, Doherty JR, Rudelius M, Buck A, Hoellein A, et al. Aurora kinases A and B are upregulated by Myc and are essential for maintenance of the malignant state. Blood 2010; 116:1498-505; PMID:20519624; http://dx.doi.org/10.1182/blood- 2009-11-251074.
15. van Leuken R, Clijsters L, van Zon W, Lim D, Yao X, Wolthuis RM, et al. Polo-like kinase-1 controls Aurora A destruction by activating APC/C-Cdh1. PLoS ONE 2009; 4:5282; PMID:19390576; http:// dx.doi.org/10.1371/journal.pone. 0005282.
16. Fujii Y, Yada M, Nishiyama M, Kamura T, Takahashi H, Tsunematsu R, et al. Fbxw7 contributes to tumor suppression by targeting multiple proteins for ubiquitin- dependent degradation. Cancer Sci 2006; 97:729- 36; PMID:16863506; http://dx.doi.org/10.1111/ j.1349-7006.2006.00239.x.
17. Finkin S, Aylon Y, Anzi S, Oren M, Shaulian E. Fbw7 regulates the activity of endoreduplication mediators and the p53 pathway to prevent drug-induced polyploidy. Oncogene 2008; 27:4411-21; PMID:18391985; http://dx.doi.org/10.1038/onc.2008.77.
18. Hagedorn M, Delugin M, Abraldes I, Allain N, Belaud-Rotureau MA, Turmo M, et al. FBXW7/ hCDC4 controls glioma cell proliferation in vitro and is a prognostic marker for survival in glioblastoma patients. Cell Div 2007; 2:9; PMID:17326833; http:// dx.doi.org/10.1186/1747-1028-2-9.
19. Bischoff JR, Anderson L, Zhu Y, Mossie K, Ng L, Souza B, et al. A homologue of Drosophila Aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J 1998; 17:3052-65; PMID:9606188; http:// dx.doi.org/10.1093/emboj/17.11.3052.
20. Meraldi P, Honda R, Nig EA. Aurora A overexpression reveals tetraploidization as a major route to centrosome amplification in p53-/- cells. EMBO J 2002; 21:483- 92; PMID:11847097; http://dx.doi.org/10.1093/emboj/21.4. 483.
21. Hoar K, Chakravarty A, Rabino C, Wysong D, Bowman D, Roy N, et al. MLN8054, a small-molecule inhibitor of Aurora A, causes spindle pole and chromosome congression defects leading to aneuploidy. Mol Cell Biol 2007; 27:4513-25; PMID:17438137; http:// dx.doi.org/10.1128/MCB.02364-06.
22. Huck JJ, Zhang M, McDonald A, Bowman D, Hoar KM, Stringer B, et al. MLN8054, an inhibitor of Aurora A kinase, induces senescence in human tumor cells both in vitro and in vivo. Mol Cancer Res 2010; 8:373-84; PMID:20197380; http://dx.doi. org/10.1158/1541-7786.MCR-09-0300.
23. Cahill DP, Kinzler KM, Vogelstein B, Lengauer C. Genetic instability and darwinian selection in tumours. Trends Cell Biol 1999; 9:57-60; PMID:10611684; http://dx.doi.org/10.1016/S0962-8924(99)01661-X.
24. Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 2005; 437:1043-7; PMID:16222300; http://dx.doi. org/10.1038/nature04217.
25. Lehman NL, Verschuren EW, Hsu JY, Cherry Am, Jackson PK. Overexpression of the anaphase promoting complex/cyclosome inhibitor Emi1 leads to tetraploidy and genomic instability of p53-deficient cells. Cell Cycle 2006; 5:1569-73; PMID:16861914; http:// dx.doi.org/10.4161/cc.5.14.2925.
26. Gritsko TM, Coppola D, Paciga JE, Yang L, Sun M, Shelley SA, et al. Activation and overexpression of centrosome kinase BTAK/Aurora A in human ovarian cancer. Clin Cancer Res 2003; 9:1420-6; PMID:12684414.
27. Conte N, Delaval B, Ginestier C, Ferrand A, Isnardon D, Larroque C, et al. TACC1-chTOG-Aurora A protein complex in breast cancer. Oncogene 2003; 22:8102-16; PMID:14603251; http://dx.doi. org/10.1038/sj.onc.1206972.
28. Buschhorn HM, Klein RR, Chambers SM, Hardy MC, Green S, Bearss D, et al. Aurora A overexpression in high-grade PIN lesions and prostate cancer. Prostate 2005; 64:341-6; PMID:15754349; http:// dx.doi.org/10.1002/pros.20247.
29. Neben K, Korshunov A, Benner A, Wrobel G, Hahn M, Kokocinski F, et al. Microarray-based screening for molecular markers in medulloblastoma revealed STK15 as independent predictor for survival. Cancer Res 2004; 64:3103-11; PMID:15126347; http://dx.doi. org/10.1158/0008-5472.CAN-03-3968.
30. Shang X, Burlingame SM, Okcu MF, Ge N, Russell HV, Egler RA, et al. Aurora A is a negative prognostic factor and a new therapeutic target in human neuroblastoma. Mol Cancer Ther 2009; 8:2461-9; PMID:19671766; http://dx.doi.org/10.1158/1535-7163.MCT-08-0857.
31. Reichardt W, Jung V, Brunner C, Klein A, Wemmert S, Romeike BF, et al. The putative serine/threonine kinase gene STK15 on chromosome 20q13.2 is amplified in human gliomas. Oncol Rep 2003; 10:1275-9; PMID:12883693.
32. Klein A, Reichardt W, Jung V, Zang KD, Meese E, Urbschat S. Overexpression and amplification of STK15 in human gliomas. Int J Oncol 2004; 25:1789-94; PMID:15547718.
33. Lehman NL, Tibshirani R, Hsu JY, Natkunam Y, Harris BT, West RB, et al. Oncogenic regulators and substrates of the anaphase promoting complex/cyclosome are frequently overexpressed in malignant tumors. Am J Pathol 2007; 170:1793-805; PMID:17456782; http://dx.doi.org/10.2353/ajpath.2007.060767.
34. Samaras V, Stamatelli A, Samaras E, Arnaoutoglou C, Arnaoutoglou M, Stergiou I, et al. Comparative immunohistochemical analysis of Aurora A and Aurora B expression in human glioblastomas. Associations with proliferative activity and clinicopathological features. Pathol Res Pract 2009; 205:765-73; PMID:19616898; http://dx.doi.org/10.1016/j.prp.2009.06.011.
35. Barton VN, Foreman NK, Donson AM, Birks DK, Handler MH, Vibhakar R. Aurora kinase A as a rational target for therapy in glioblastoma. J Neurosurg Pediatr 2010; 6:98-105; PMID:20593995; http:// dx.doi.org/10.3171/2010.3. PEDS10120.
36. Li CC, Chu HY, Yang CW, Chou CK, Tsai TF. Aurora A overexpression in mouse liver causes p53-dependent premitotic arrest during liver regeneration. Mol Cancer Res 2009; 7:678-88; PMID:19435814; http://dx.doi. org/10.1158/1541-7786.MCR-08-0483.
37. Warner SL, Muñoz RM, Bearss DJ, Grippo P, Han H, Von Hoff DD. Pdx-1-driven overexpression of Aurora a kinase induces mild ductal dysplasia of pancreatic ducts near islets in transgenic mice. Pancreas 2008; 37:39-44; PMID:18815537; http://dx.doi.org/10.1097/MPA.0b013e318176b9ae.
38. Zhang D, Shimizu T, Araki N, Hirota T, Yoshie M, Ogawa K, et al. Aurora A overexpression induces cellular senescence in mammary gland hyperplastic tumors developed in p53-deficient mice. Oncogene 2008; 27:4305-14; PMID:18372918; http://dx.doi.org/10.1038/onc.2008.76.
39. Wang X, Zhou YX, Qiao W, Tominaga Y, Ouchi M, Ouchi T, et al. Overexpression of Aurora kinase A in mouse mammary epithelium induces genetic instability preceding mammary tumor formation. Oncogene 2006; 25:7148-58; PMID:16715125; http://dx.doi. org/10.1038/sj.onc.1209707.
40. Lu LY, Wood JL, Ye L, Minter-Dykhouse K, Saunders TL, Yu X, et al. Aurora A is essential for early embryonic development and tumor suppression. J Biol Chem 2008; 283:31785-90; PMID:18801727; http://dx.doi. org/10.1074/jbc. M805880200.
41. Harrington EA, Bebbington D, Moore J, Rasmussen RK, Ajose-Adeogun AO, Nakayama T, et al. VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat Med 2004; 10:262-7; PMID:14981513; http://dx.doi. org/10.1038/nm1003.
42. Cheung CH, Coumar MS, Hsieh HP, Chang JY. Aurora kinase inhibitors in preclinical and clinical testing. Expert Opin Investig Drugs 2009; 18:379-98; PMID:19335272; http://dx.doi. org/10.1517/13543780902806392.
43. 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 USA 2007; 104:4106-11; PMID:17360485; http://dx.doi. org/10.1073/pnas.0608798104.
44. Hose D, Rème T, Meissner T, Moreaux J, Seckinger A, Lewis J, et al. Inhibition of Aurora kinases for tailored risk-adapted treatment of multiple myeloma. Blood 2009; 113:4331-40; PMID:19171872; http://dx.doi. org/10.1182/blood-2008-09-178350.
45. VanderPorten EC, Taverna P, Hogan JN, Ballinger MD, Flanagan WM, Fucini RV. The Aurora kinase inhibitor SNS-314 shows broad therapeutic potential with chemotherapeutics and synergy with microtubule-targeted agents in a colon carcinoma model. Mol Cancer Ther 2009; 8:930-9; PMID:19372566; http:// dx.doi.org/10.1158/1535-7163.MCT-08-0754.
46. Macarulla T, Cervantes A, Elez E, Rodríguez-Braun E, Baselga J, Roselló S, et al. Phase I study of the selective Aurora A kinase inhibitor MLN8054 in patients with advanced solid tumors: safety, pharmacokinetics and pharmacodynamics. Mol Cancer Ther 2010; 9:2844-52; PMID:20724522; http://dx.doi.org/10.1158/1535-7163.MCT-10-0299.
47. Kelly KR, Ecsedy J, Medina E, Mahalingam D, Padmanabhan S, Nawrocki ST, et al. The novel Aurora A kinase inhibitor MLN8237 is active in resistant chronic myeloid leukemia and significantly increases the efficacy of nilotinib. J Cell Mol Med 2011; 15:2057-70; PMID:21091633; http://dx.doi.org/10.1111/j. 1582-4934.2010.01218.x.
48. Görgün G, Calabrese E, Hideshima T, Ecsedy J, Perrone G, Mani M, et al. A novel Aurora A kinase inhibitor MLN8237 induces cytotoxicity and cell cycle arrest in multiple myeloma. Blood 2010; 115:5202-13; PMID:20382844; http://dx.doi.org/10.1182/blood-2009-12-259523.
49. Carol H, Boehm I, Reynolds CP, Kang MH, Maris JM, Morton CL, et al. Efficacy and pharmacokinetic/pharmacodynamic evaluation of the Aurora kinase A inhibitor MLN8237 against preclinical models of pediatric cancer. Cancer Chemother Pharmacol 2011; 68:1291-304; PMID:21448591; http://dx.doi.org/10.1007/ s00280-011-1618-8.
50. Maris JM, Morton CL, Gorlick R, Kolb EA, Lock R, Carol H, et al. Initial testing of the Aurora kinase A inhibitor MLN8237 by the Pediatric Preclinical Testing Program (PPTP). Pediatr Blood Cancer 2010; 55:26-34; PMID:20108338.
51. Sells T, Ecsedy J, Stroud S, Janowick D, Hoar K, LeRoy P, et al. MLN8237: An orally active small molecule inhibitor of Aurora A kinase in Phase I clinical trials. Proceedings American Association for Cancer Research 2008.
52. Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455:1061-8; PMID:18772890; http://dx.doi.org/10.1038/nature07385.
53. Yang S, He S, Zhou X, Liu M, Zhu H, Wang Y, et al. Suppression of Aurora A oncogenic potential by c-Myc downregulation. Exp Mol Med 2010; 42:759-67; PMID:20890087; http://dx.doi.org/10.3858/ emm.2010.42.11.077.
54. El-Sheikh A, Fan R, Birks D, Donson A, Foreman NK, Vibhakar R. Inhibition of Aurora Kinase A enhances chemosensitivity of medulloblastoma cell lines. Pediatr Blood Cancer 2010; 55:35-41; PMID:20232424.
55. Smith SG, Lehman NL, Moran RG. Cytotoxicity of antifolate inhibitors of thymidylate and purine synthesis to WiDr colonic carcinoma cells. Cancer Res 1993; 53:5697-706; PMID:8242626.
56. Takeuchi H, Sato K, Ido K, Kubota T. Mitotic activity of multinucleated giant cells with glial fibrillary acidic protein immunoreactivity in glioblastomas: an immunohistochemical double labeling study. J Neurooncol 2006; 78:15-8; PMID:16718521; http://dx.doi.org/10.1007/s11060-005-9067-z.
57. Tao Y, Zhang P, Frascogna V, Lecluse Y, Auperin A, Bourhis J, et al. Enhancement of radiation response by inhibition of Aurora A kinase using siRNA or a selective Aurora kinase inhibitor PHA680632 in p53-deficient cancer cells. Br J Cancer 2007; 97:1664-72; PMID:18026198; http://dx.doi.org/10.1038/sj.bjc. 6604083.