Cancer cell resistance to aurora kinase inhibitors: Identification of novel targets for cancer therapy

Journal of Proteome Research

Volumn 12, Issue 1, 2013, Pages 455-469

  Hrabakova, Rita ^a   Kollareddy, Madhu ^b   Tyleckova, Jirina ^a   Halada, Petr ^c   Hajduch, Marian ^b   Gadher, Suresh Jivan ^d   Kovarova, Hana ^a  

^a INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^b UNIVERSITY HOSPITAL OLOMOUC   (Czech Republic)

^c INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^d Life Technologies Inc   (United States)

Author keywords

Apoptosis; Aurora kinase inhibitors; Autophagy; Calretinin; P53; Platelet activating factor acetylhydrolase; Ran; Resistance; Serine hydroxymethyltransferase; Serpin B5

Indexed keywords

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; AURORA KINASE INHIBITOR; CALRETININ; CYC 116; GLYCINE HYDROXYMETHYLTRANSFERASE; N [4 [6 METHOXY 7 (3 MORPHOLINOPROPOXY) 4 QUINAZOLINYLAMINO]PHENYL]BENZAMIDE; PROTEIN P53; RAN PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CANCER RESISTANCE; CANCER THERAPY; CELL STRAIN HCT116; COLON CANCER; COMPUTER MODEL; ELECTROPHORESIS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; TUMOR GROWTH; WESTERN BLOTTING;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZAMIDES; DRUG RESISTANCE, NEOPLASM; GTP-BINDING PROTEINS; HCT116 CELLS; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASMS; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PYRIMIDINES; QUINAZOLINES; THIAZOLES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84874027283     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300819m     Document Type: Article

References (60)

1. Kollareddy, M.; Dzubak, P.; Zheleva, D.; Hajduch, M. Aurora kinases: Structure, functions and their association with cancer. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 2008, 152 (1), 27-33.
2. Kollareddy, M.; Zheleva, D.; Dzubak, P.; Brahmkshatriya, P. S.; Lepsik, M.; Hajduch, M. Aurora kinase inhibitors: Progress towards the clinic. Invest. New Drugs 2012, 30, 2411-2432.
3. Ditchfield, C.; Johnson, V. L.; Tighe, A.; Ellston, R.; Haworth, C.; Johnson, T.; Mortlock, A.; Keen, N.; Taylor, S. S. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 2003, 161 (2), 267-280.
4. Wang, S.; Midgley, C. A.; Scaerou, F.; Grabarek, J. B.; Griffiths, G.; Jackson, W.; Kontopidis, G.; McClue, S. J.; McInnes, C.; Meades, C.; Mezna, M.; Plater, A.; Stuart, I.; Thomas, M. P.; Wood, G.; Clarke, R. G.; Blake, D. G.; Zheleva, D. I.; Lane, D. P.; Jackson, R. C.; Glover, D. M.; Fischer, P. M. Discovery of N-phenyl-4-(thiazol-5-yl)pyrimidin-2-amine aurora kinase inhibitors. J. Med. Chem. 2010, 53 (11), 4367-4378.
5. Gottesman, M. M.; Fojo, T.; Bates, S. E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer 2002, 2 (1), 48-58.
6. Elsaleh, H.; Powell, B.; McCaul, K.; Grieu, F.; Grant, R.; Joseph, D.; Iacopetta, B. P53 alteration and microsatellite instability have predictive value for survival benefit from chemotherapy in stage III colorectal carcinoma. Clin. Cancer Res. 2001, 7 (5), 1343-1349.
7. Youn, C. K.; Kim, M. H.; Cho, H. J.; Kim, H. B.; Chang, I. Y.; Chung, M. H.; You, H. J. Oncogenic H-Ras up-regulates expression of ERCC1 to protect cells from platinum-based anti-cancer agents. Cancer Res. 2004, 64 (14), 4849-4857.
8. Dean, M. Cancer stem cells: Implications for cancer causation and therapy resistance. Discovery Med 2005, 5 (27), 278-82.
9. Glasspool, R. M.; Teodoridis, J. M.; Brown, R. Epigenetics as a mechanism driving polygenic clinical drug resistance. Br. J. Cancer 2006, 94 (8), 1087-92.
10. Hollstein, M.; Sidransky, D.; Vogelstein, B.; Harris, C. C. p53 mutations in human cancers. Science 1991, 253 (5015), 49-53.
11. Gasco, M.; Crook, T. p53 family members and chemoresistance in cancer: what we know and what we need to know. Drug Resist. Updates 2003, 6 (6), 323-328.
12. Vousden, K. H.; Lu, X. Live or let die: The cell's response to p53. Nat. Rev. Cancer 2002, 2 (8), 594-604.
13. Moll, U. M.; Wolff, S.; Speidel, D.; Deppert, W. Transcriptionindependent pro-apoptotic functions of p53. Curr. Opin. Cell Biol. 2005, 17 (6), 631-636.
14. Mao, J. H.; Wu, D.; Perez-Losada, J.; Jiang, T.; Li, Q.; Neve, R. M.; Gray, J. W.; Cai, W. W.; Balmain, A. Crosstalk between Aurora-A and p53: Frequent deletion or downregulation of Aurora-A in tumors from p53 null mice. Cancer Cell 2007, 11 (2), 161-173.
15. Chen, S. S.; Chang, P. C.; Cheng, Y. W.; Tang, F. M.; Lin, Y. S. Suppression of the STK15 oncogenic activity requires a transactivationindependent p53 function. EMBO J. 2002, 21 (17), 4491-4499.
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 Mdm2-mediated destabilization and inhibition of p53. Nat. Genet. 2004, 36 (1), 55-62.
17. Cheng, J.; Haas, M. Frequent mutations in the p53 tumor suppressor gene in human leukemia T-cell lines. Mol. Cell. Biol. 1990, 10 (10), 5502-5509.
18. Zhang, L.; Zhang, J.; Hu, C.; Cao, J.; Zhou, X.; Hu, Y.; He, Q.; Yang, B. Efficient activation of p53 pathway in A549 cells exposed to L2, a novel compound targeting p53-MDM2 interaction. Anticancer Drugs 2009, 20 (6), 416-424.
19. Dzubak, P.; Hajduch, M.; Gazak, R.; Svobodova, A.; Psotova, J.; Walterova, D.; Sedmera, P.; Kren, V. New derivatives of silybin and 2,3-dehydrosilybin and their cytotoxic and P-glycoprotein modulatory activity. Bioorg. Med. Chem. 2006, 14 (11), 3793-3810.
20. Noskova, V.; Dzubak, P.; Kuzmina, G.; Ludkova, A.; Stehlik, D.; Trojanec, R.; Janostakova, A.; Korinkova, G.; Mihal, V.; Hajduch, M. In vitro chemoresistance profile and expression/function of MDR associated proteins in resistant cell lines derived from CCRF-CEM, K562, A549 and MDA MB 231 parental cells. Neoplasma 2002, 49 (6), 418-425.
21. Hardy, E.; Castellanos-Serra, L. R. Reverse-staining of biomolecules in electrophoresis gels: analytical and micropreparative applications. Anal. Biochem. 2004, 328 (1), 1-13.
22. Stastna, M.; Behrens, A.; McDonnell, P. J.; Van Eyk, J. E. Analysis of protein composition of rabbit aqueous humor following two different cataract surgery incision procedures using 2-DE and LC-MS/MS. Proteome Sci. 2011, 9 (1), 8.
23. Gobom, J.; Nordhoff, E.; Mirgorodskaya, E.; Ekman, R.; Roepstorff, P. Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J. Mass Spectrom. 1999, 34 (2), 105-116.
24. Thomas, P. D.; Campbell, M. J.; Kejariwal, A.; Mi, H.; Karlak, B.; Daverman, R.; Diemer, K.; Muruganujan, A.; Narechania, A. PANTHER: A library of protein families and subfamilies indexed by function. Genome Res. 2003, 13 (9), 2129-2141.
25. Brown, K. R.; Jurisica, I. Online predicted human interaction database. Bioinformatics 2005, 21 (9), 2076-2082.
26. Agrawal, S.; Kumar, A.; Srivastava, V.; Mishra, B. N. Cloning, expression, activity and folding studies of serine hydroxymethyltransferase: A target enzyme for cancer chemotherapy. J. Mol. Microbiol. Biotechnol. 2003, 6 (2), 67-75.
27. Sorokin, A. V.; Kim, E. R.; Ovchinnikov, L. P. Nucleocytoplasmic transport of proteins. Biochemistry (Moscow) 2007, 72 (13), 1439-1457.
28. Payne, C. M.; Holubec, H.; Crowley-Skillicorn, C.; Nguyen, H.; Bernstein, H.; Wilcox, G.; Bernstein, C. Maspin is a deoxycholateinducible, anti-apoptotic stress-response protein differentially expressed during colon carcinogenesis. Clin. Exp. Gastroenterol. 2011, 4, 239-253.
29. Stevenson, L.; Allen, W. L.; Proutski, I.; Stewart, G.; Johnston, L.; McCloskey, K.; Wilson, P. M.; Longley, D. B.; Johnston, P. G. Calbindin 2 (CALB2) regulates 5-fluorouracil sensitivity in colorectal cancer by modulating the intrinsic apoptotic pathway. PLoS One 2011, 6 (5), e20276.
30. Roy, S. S.; Ehrlich, A. M.; Craigen, W. J.; Hajnoczky, G. VDAC2 is required for truncated BID-induced mitochondrial apoptosis by recruiting BAK to the mitochondria. EMBO Rep. 2009, 10 (12), 1341-1347.
31. Girdler, F.; Sessa, F.; Patercoli, S.; Villa, F.; Musacchio, A.; Taylor, S. Molecular basis of drug resistance in aurora kinases. Chem. Biol. 2008, 15 (6), 552-562.
32. Zhang, J. T.; Liu, Y. Use of comparative proteomics to identify potential resistance mechanisms in cancer treatment. Cancer Treat. Rev. 2007, 33 (8), 741-756.
33. Mizushima, N.; Klionsky, D. J. Protein turnover via autophagy: implications for metabolism. Annu. Rev. Nutr. 2007, 27, 19-40.
34. Han, W.; Sun, J.; Feng, L.; Wang, K.; Li, D.; Pan, Q.; Chen, Y.; Jin, W.; Wang, X.; Pan, H.; Jin, H. Autophagy inhibition enhances daunorubicin-induced apoptosis in K562 cells. PLoS One 2011, 6 (12), e28491.
35. Ma, X. H.; Piao, S.; Wang, D.; McAfee, Q. W.; Nathanson, K. L.; Lum, J. J.; Li, L. Z.; Amaravadi, R. K. Measurements of tumor cell autophagy predict invasiveness, resistance to chemotherapy, and survival in melanoma. Clin. Cancer Res. 2011, 17 (10), 3478-3489.
36. Qadir, M. A.; Kwok, B.; Dragowska, W. H.; Le, K. H.; Bally, D.; Gorski, M. B.; Macroautophagy, S. M. inhibition sensitizes tamoxifenresistant breast cancer cells and enhances mitochondrial depolarization. Breast Cancer Res. Treat. 2008, 112 (3), 389-403.
37. Yoon, J. H.; Ahn, S. G.; Lee, B. H.; Jung, S. H.; Oh, S. H. Role of autophagy in chemoresistance: regulation of the ATM-mediated DNAdamage signaling pathway through activation of DNA-PKcs and PARP-1. Biochem. Pharmacol. 2012, 83 (6), 747-757.
38. Dreier, M. R.; Grabovich, A. Z.; Katusin, J. D.; Taylor, W. R. Short and long-term tumor cell responses to Aurora kinase inhibitors. Exp. Cell Res. 2009, 315 (7), 1085-1099.
39. Yin, X.; Fontoura, B. M.; Morimoto, T.; Carroll, R. B. Cytoplasmic complex of p53 and eEF2. J. Cell Physiol. 2003, 196 (3), 474-482.
40. Liu, H.; Zheng, F.; Cao, Q.; Ren, B.; Zhu, L.; Striker, G.; Vlassara, H. Amelioration of oxidant stress by the defensin lysozyme. Am. J. Physiol. Endocrinol. Metab. 2006, 290 (5), E824-E832.
41. Chang, Y. J.; Huang, Y. P.; Li, Z. L.; Chen, C. H. GRP78 Knockdown Enhances Apoptosis via the Down-Regulation of Oxidative Stress and Akt Pathway after Epirubicin Treatment in Colon Cancer DLD-1 Cells. PLoS One 2012, 7 (4), e35123.
42. Zhang, L. H.; Zhang, X. Roles of GRP78 in physiology and cancer. J. Cell Biochem. 2010, 110 (6), 1299-1305.
43. Zhou, H.; Zhang, Y.; Fu, Y.; Chan, L.; Lee, A. S. Novel mechanism of anti-apoptotic function of 78-kDa glucose-regulated protein (GRP78): Endocrine resistance factor in breast cancer, through release of B-cell lymphoma 2 (BCL-2) from BCL-2-interacting killer (BIK). J. Biol. Chem. 2011, 286 (29), 25687-25696.
44. Tjoelker, L. W.; Stafforini, D. M. Platelet-activating factor acetylhydrolases in health and disease. Biochim. Biophys. Acta 2000, 1488 (1-2), 102-123.
45. Biancone, L.; Cantaluppi, V.; Del Sorbo, L.; Russo, S.; Tjoelker, L. W.; Camussi, G. Platelet-activating factor inactivation by local expression of platelet-activating factor acetyl-hydrolase modifies tumor vascularization and growth. Clin. Cancer Res. 2003, 9 (11), 4214-4220.
46. Denizot, Y.; Truffinet, V.; Bouvier, S.; Gainant, A.; Cubertafond, P.; Mathonnet, M. Elevated plasma phospholipase A2 and plateletactivating factor acetylhydrolase activity in colorectal cancer. Mediators Inflammation 2004, 13 (1), 53-54.
47. Clarke, P. R.; Zhang, C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat. Rev. Mol. Cell Biol. 2008, 9 (6), 464-477.
48. Honma, K.; Takemasa, I.; Matoba, R.; Yamamoto, Y.; Takeshita, F.; Mori, M.; Monden, M.; Matsubara, K.; Ochiya, T. Screening of potential molecular targets for colorectal cancer therapy. Int. J. Gen. Med. 2009, 2, 243-257.
49. Xia, F.; Lee, C. W.; Altieri, D. C. Tumor cell dependence on Ran-GTP-directed mitosis. Cancer Res. 2008, 68 (6), 1826-1833.
50. Thottassery, J. V.; Zambetti, G. P.; Arimori, K.; Schuetz, E. G.; Schuetz, J. D. p53-dependent regulation of MDR1 gene expression causes selective resistance to chemotherapeutic agents. Proc. Natl. Acad. Sci. U.S.A. 1997, 94 (20), 11037-11042.
51. Bush, J. A.; Li, G. Regulation of the Mdr1 isoforms in a p53-deficient mouse model. Carcinogenesis 2002, 23 (10), 1603-1607.
52. Pommier, Y.; Sordet, O.; Antony, S.; Hayward, R. L.; Kohn, K. W. Apoptosis defects and chemotherapy resistance: molecular interaction maps and networks. Oncogene 2004, 23 (16), 2934-2949.
53. Lovric, E.; Gatalica, Z.; Eyzaguirre, E.; Kruslin, B. Expression of maspin and glutathionine-S-transferase-pi in normal human prostate and prostatic carcinomas. Appl. Immunohistochem. Mol. Morphol. 2010, 18 (5), 429-432.
54. Yeom, S. Y.; Jang, H. L.; Lee, S. J.; Kim, E.; Son, H. J.; Kim, B. G.; Park, C. Interaction of testisin with maspin and its impact on invasion and cell death resistance of cervical cancer cells. FEBS Lett. 2010, 584 (8), 1469-1475.
55. Zou, Z.; Anisowicz, A.; Hendrix, M. J.; Thor, A.; Neveu, M.; Sheng, S.; Rafidi, K.; Seftor, E.; Sager, R. Maspin, a serpin with tumorsuppressing activity in human mammary epithelial cells. Science 1994, 263 (5146), 526-529.
56. Ben Shachar, B.; Feldstein, O.; Hacohen, D.; Ginsberg, D. The tumor suppressor maspin mediates E2F1-induced sensitivity of cancer cells to chemotherapy. Mol. Cancer Res. 2010, 8 (3), 363-372.
57. Feng, X. P.; Yi, H.; Li, M. Y.; Li, X. H.; Yi, B.; Zhang, P. F.; Li, C.; Peng, F.; Tang, C. E.; Li, J. L.; Chen, Z. C.; Xiao, Z. Q. Identification of biomarkers for predicting nasopharyngeal carcinoma response to radiotherapy by proteomics. Cancer Res. 2010, 70 (9), 3450-3462.
58. Nam, E.; Park, C. Maspin suppresses survival of lung cancer cells through modulation of Akt pathway. Cancer Res. Treat. 2010, 42 (1), 42-47.
59. Boyer, J.; Allen, W. L.; McLean, E. G.; Wilson, P. M.; McCulla, A.; Moore, S.; Longley, D. B.; Caldas, C.; Johnston, P. G. Pharmacogenomic identification of novel determinants of response to chemotherapy in colon cancer. Cancer Res. 2006, 66 (5), 2765-2777.
60. Haner, K.; Henzi, T.; Pfefferli, M.; Haner, K.; Salicio, V.; Schwaller, B. A bipartite butyrate-responsive element in the human calretinin (CALB2) promoter acts as a repressor in colon carcinoma cells but not in mesothelioma cells. J. Cell Biochem. 2010, 109 (3), 519-531.