Targeting GD2 ganglioside and aurora A kinase as a dual strategy leading to cell death in cultures of human neuroblastoma cells

Cancer Letters

Volumn 341, Issue 2, 2013, Pages 248-264

  Horwacik, Irena ^a   Durbas, Małgorzata ^a   Boratyn, Elzbieta ^a   Wegrzyn, Paulina ^a   Rokita, Hanna ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Aurora kinases; GD2 ganglioside; Monoclonal antibody; Neuroblastoma; P53

Indexed keywords

AURORA A KINASE; AURORA KINASE INHIBITOR; GANGLIOSIDE GD2; HEAT SHOCK PROTEIN; MK 5108; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 14G2A; PROTEIN P53; UNCLASSIFIED DRUG; 4-(3-CHLORO-2-FLUOROPHENOXY)-1-((6-(1,3-THIAZOL-2-YLAMINO)PYRIDIN TO 2-YL)METHYL) CYCLOHEXANECARBOXYLIC ACID; CASPASE 3; CASPASE 7; CYCLOHEXANECARBOXYLIC ACID DERIVATIVE; GANGLIOSIDE; GANGLIOSIDE, GD2; MYCN PROTEIN, HUMAN; NUCLEAR PROTEIN; ONCOPROTEIN; PHLDA1 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; THIAZOLE DERIVATIVE; TP53 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG POTENTIATION; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; MYCN GENE; NEUROBLASTOMA CELL; PHLDA1 GENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE; NEUROBLASTOMA; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

CHANDIPURA VIRUS;

ANIMALS; ANTIBODIES, MONOCLONAL; AURORA KINASE A; CASPASE 3; CASPASE 7; CELL LINE, TUMOR; CELL SURVIVAL; CYCLOHEXANECARBOXYLIC ACIDS; FLOW CYTOMETRY; GANGLIOSIDES; GENE EXPRESSION; HUMANS; IMMUNOBLOTTING; MICE; NEUROBLASTOMA; NUCLEAR PROTEINS; ONCOGENE PROTEINS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THIAZOLES; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84887137092     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.08.018     Document Type: Article

References (44)

1. Kowalczyk A., Wierzbicki A., Gil M., Bambach B., Kaneko Y., Rokita H., Repasky E., Fenstermaker R., Brecher M., Ciesielski M., Kozbor D. Induction of protective immune responses against NXS2 neuroblastoma challenge in mice by immunotherapy with GD2 mimotope vaccine and IL-15 and IL-21 gene delivery. Cancer Immunol. Immunother. 2007, 56:1443-1458.
2. Modak S., Cheung N.-K. Neuroblastoma: therapeutic strategies for a clinical enigma. Cancer Treat. Rev. 2010, 36:307-317.
3. Ora I., Eggert A. Progress in treatment and risk stratification of neuroblastoma: impact on future clinical and basic research. Semin. Cancer Biol. 2011, 21:217-228.
4. Hara J. Development of treatment strategies for advanced neuroblastoma. Int. J. Clin. Oncol. 2012, 17:196-203.
5. Zeng Y., Fest S., Kunert R., Katinger H., Pistoia V., Michon J., Lewis G., Ladenstein R., Lode H.N. Anti-neuroblastoma effect of ch14.18 antibody produced in CHO cells is mediated by NK-cells in mice. Mol. Immunol. 2005, 42:1311-1319.
6. Aixinjueluo W., Furukawa K., Zhang Q., Hamamura K., Tokuda N., Yoshida S., Ueda R., Furukawa K. Mechanisms for the apoptosis of small cell lung cancer cells induced by anti-GD2 monoclonal antibodies. J. Biol. Chem. 2005, 280:29828-29836.
7. Yoshida S., Kawaguchi H., Sato S., Ueda R., Furukawa K. An anti-GD2 monoclonal antibody enhances apoptotic effects of anti-cancer drugs against small cell lung cancer cells via JNK (c-Jun terminal kinase) activation. Jpn. J. Cancer Res. 2002, 93:816-824.
8. Kowalczyk A., Gil M., Horwacik I., Odrowaz Z., Kozbor D., Rokita H. The GD2-specific 14G2a monoclonal antibody induces apoptosis and enhances cytotoxicity of chemotherapeutic drugs in IMR-32 human neuroblastoma cells. Cancer Lett. 2009, 281:171-182.
9. Lens S.M.A., Voest E.E., Medema R.H. Shared and separate functions of polo-like kinases and aurora kinases in cancer. Nat. Rev. Cancer 2010, 10:825-841.
10. Gautschi O., Heighway J., Mack P.C., Purnell P.R., Lara P.N., Gandara D.R. Aurora kinases as anticancer drug targets. Clin. Cancer Res. 2008, 14:1639-1648.
11. Morozova O., Vojvodic M., Grinshtein N., Hansford L.M., Balkely K.M., Maslova A., Hirst M., Cezard T., Morin R.D., Moore R., Smith K.M., Miller F., Taylor P., Thiessen N., Varhol R., Zhao Y., Jones S., Moffat J., Kislinger T., Moran M.F., Kaplan D.R., Marra M.A. System-level analysis of neuroblastoma tumor-initiating cells implicates AURKB as a novel drug target. Clin. Cancer Res. 2010, 16:4572-4582.
12. Faisal A., Vaughan L., Bavetsias V., Sun C., Atrash B., Avery S., Jamin Y., Robinson S.P., Workman P., Blagg J., Raynaud F.I., Eccles S.A., Chesler L., Linardopoulos S. The aurora kinase inhibitor CCT137690 downregulates MYCN and sensitizes MYCN-amplified neuroblastoma in vivo. Mol. Cancer Ther. 2011, 10:2115-2123.
13. Katayama H., Sen S. Aurora kinase inhibitors as anticancer molecules. Biochim. Biophys. Acta 2010, 1799:829-839.
14. Kollareddy M., Zheleva D., Dzubak P., Brahmkshatriya P.S., Lepsik M., Hajduch M. Aurora kinase inhibitors: progress toward the clinic. Invest. New Drugs 2012, 30:2411-2432.
15. Manfredi M.G., Ecsedy J.A., Meetze K.A., Balani S.K., Burenkova O., Chen W., Galvin K.M., Hoar K.M., Huck J.J., LeRoy P.J., Ray E.T., Sells T.B., Stringer B., Stroud S.G., Vos T.J., Weatherhead G.S., Wysong D.R., Zhang M., Bolen J.B., Claiborne C.F. Antitumor activity of MLN8054, an orally active small-molecule inhibitor of Aurora A kinase. Proc. Natl. Acad Sci. USA 2007, 104:4106-4111.
16. Katayama H., Sasai K., Kawai H., Yuan Z.M., Bondaruk J., Suzuki F., Fujii S., Arlinghaus R.B., Czerniak B.A., Sen S. Phosphorylation by aurora kinase A induces MDM1-mediated destabilization and inhibition of p53. Nat. Genet. 2004, 36:55-62.
17. Yan X., Cao L., Li Q., Wu Y., Zhang H., Saiyin H., Liu X., Zhang X., Shi Q., Yu L. Aurora C is directly associated with survivin and required for cytokinesis. Genes Cells 2005, 10:617-626.
18. Zhou H., Kuang J., Zhong L., Kuo W.L., Gray J.W., Sahin A., Brinkley B.R., Sen S. Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation. Nat. Genet. 1998, 20:189-193.
19. Shang X., Burlingame S.M., Okcu M.F., Ge N., Russell H.V., Egler R.A., David R.D., Vasudevan S.A., Yang J., Nuchtern J.G. Aurora A is a negative prognostic factor and a new therapeutic target in human neuroblastoma. Mol. Cancer Ther. 2009, 8:2461-2469.
20. Maris J.M. Unholy matrimony: Aurora A and N-Myc as malignant partners in neuroblastoma. Cancer Cell 2009, 15:5-6.
21. Liu Q., Kaneko S., Yang L., Feldman R.I., Nicosia S.V., Chen J., Cheng J.Q. Aurora-A abrogation of p53 DNA binding and transactivation activity by phosphorylation of serine 215. J. Biol. Chem. 2004, 279:52175-52182.
22. Johnson E.O., Chang K.H., de Pablo Y., Ghosh S., Mehta R., Badve S., Shah K. PHLDA1 is a crucial negative regulator and effector of Aurora A kinase in breast cancer. J. Cell Sci. 2011, 124:2711-2722.
23. Otto T., Horn S., Brockmann M., Eilers U., Schuttrumpf L., Popov N., Kenney A.M., Schulte J.H., Beijersbergen R., Christiansen H., Berwanger B., Eilers M. Stabilization of N-Myc is a critical function of aurora A in human neuroblastoma. Cancer Cell 2009, 15:67-78.
24. Nair J.S., Ho A.L., Schwartz G.K. The induction of polyploidy or apoptosis by the aurora A kinase inhibitor MK8745 is p53-dependent. Cell Cycle 2012, 11:807-817.
25. Hayashida N., Inouye S., Fujimoto M., Tanaka Y., Izu H., Takaki E., Ichikawa H., Rho J., Nakai A. A novel HSF1-mediated death pathway that is suppressed by heat shock proteins. EMBO J. 2006, 25:4773-4783.
26. Suzuki Y.J., Mizuno M., Packer L. Signal transduction for nuclear factor-kappa B activation. Proposed location of antioxidant-inhibitable step. J. Immunol. 1994, 153:5008-5015.
27. Shimomura T., Hasako S., Nakatsuru Y., Mita T., Ichikawa K., Kodera T., Sakai T., Nambu T., Miyamoto M., Takahashi I., Miki S., Kawanishi N., Ohkubo M., Kotani H., Iwasawa Y. MK-5108, a highly selective aurora-A kinase inhibitor, shows antitumor activity alone and in combination with docetaxel. Mol. Cancer Ther. 2010, 9:157-166.
28. Oda K., Arakawa H., Tanaka T., Matsuda K., Tanikawa C., Mori T., Nishimori H., Tamai K., Tokino T., Nakamura Y., Taya Y. P53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 2000, 102:849-862.
29. Bell E., Chen L., Liu T., Marshall G.M., Lunec J., Tweddle D.A. MYCN oncoprotein targets and their therapeutic potential. Cancer Lett. 2010, 293:144-157.
30. Chen L., Iraci N., Gherardi S., Gamble L.D., Wood K.M., Perini G., Lunec J., Tweddle D.A. P53 is a direct transcriptional target of MYCN in neuroblastoma. Cancer Res. 2010, 70:1377-1388.
31. Jaattela M. Heat shock proteins as cellular lifeguards. Ann. Med. 1999, 31:261-271.
32. Mosser D.D., Caron A.W., Bourget L., Merlin A.B., Sherman M.Y., Morimoto R.I., Massie B. The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol. Cell. Biol. 2000, 20:7146-7159.
33. Voellmy R., Boellmann F. Chaperone regulation of the heat shock protein response. Molecular Aspects of the Stress Response: Chaperons, Membranes and Networks 2007, 89-99. Landes Bioscience and Springer Science+Business Media. P. Csermely, L. Vigh (Eds.).
34. Yu A.L., Gilman A.L., Ozkaynak M.F., London W.B., Kreissman S.G., Chen H.X., Smith M., Anderson B., Villablanca J.G., Matthay K.K., Shimada H., Grupp S.A., Seeger R., Reynolds C.P., Buxton A., Reisfeld R.A., Gillies S.D., Cohn S.L., Maris J.M., Sondel P.M. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N. Engl. J. Med. 2010, 363:1324-1334.
35. Kretzner L., Scuto A., Dino P.M., Kowolik C.M., Wu J., Ventura P., Jove R., Forman S.J., Yen Y., Kirschbaum M.H. Combining histone deacetylase inhibitor vorinostat with aurora kinase inhibitors enhances lymphoma cell killing with repression of c-Myc, hTERT, and microRNA levels. Cancer Res. 2011, 71:3912-3920.
36. Cochonneau D., Terme M., Michaud A., Dorvillius M., Gautier N., Frikeche J., Alvarez-Rueda N., Bougras G., Aubry J., Paris F., Birkle S. Cell cycle arrest and apoptosis induced by O-acetyl-GD2-specific monoclonal antibody 8B6 inhibits tumor growth in vitro and in vivo. Cancer Lett. 2013, 333:194-204.
37. Brockmann M., Poon E., Berry T., Carstensen A., Deubzer H.E., Rycak L., Jamin Y., Thway K., Robinson S.P., Roels F., Witt O., Fischer M., Chesler L., Eilers M. Small molecule inhibitors of aurora-A induce proteasomal degradation of N-Myc in childhood neuroblastoma. Cancer Cell 2013, 24:75-89.
38. Carmo-Fonseca M. The contribution of nuclear compartmentalization to gene regulation. Cell 2002, 108:513-521.
39. Cheok C.F., Kua N., Kaldis P., Lane D.P. Combination of nutlin-3 and VX-680 selectively targets p53 mutant cells with reversible effects on cells expressing wild-type p53. Cell Death Differ. 2010, 17:1486-1500.
40. Ostermeyer A.G., Runko E., Winkfield B., Ahn B., Moll U.M. Cytoplasmically sequestered wild-type p53 protein in neuroblastoma is relocated to the nucleus by a C-terminal peptide. Proc. Natl. Acad. Sci. USA 1996, 93:15190-15194.
41. Tweddle D.A., Pearson A.D., Haber M., Norris M.D., Xue C., Flemming C., Lunec J. The p53 pathway and its inactivation in neuroblastoma. Cancer Lett. 2003, 197:93-98.
42. Kim E.-H., Lee Y.-J., Bae S., Lee J.S., Kim J., Lee Y.-S. Heat shock factor 1-mediated aneuploidy requires a defective function of p53. Cancer Res. 2009, 69:9404-9412.
43. Brodeur G.M. Neuroblastoma: biological insights into a clinical enigma. Nat. Rev. Cancer 2003, 3:203-216.
44. Maris J.M., Hogarty M.D., Bagatell R., Cohn S.L. Neuroblastoma. Lancet 2007, 369:2106-2120.