Prevention of BMS-777607-induced polyploidy/senescence by mTOR inhibitor AZD8055 sensitizes breast cancer cells to cytotoxic chemotherapeutics

Molecular Oncology

Volumn 8, Issue 3, 2014, Pages 469-482

  Sharma, Sharad ^a   Yao, Hang Ping ^b   Zhou, Yong Qing ^b   Zhou, Jianwei ^c   Zhang, Ruiwen ^a   Wang, Ming Hai ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Breast cancer; Chemosensitivity; MTOR signaling; Polyploidy; Receptor tyrosine kinase; Senescence; Small molecule inhibitor

Indexed keywords

AZD 8055; BETA GALACTOSIDASE; BMS 777607; CELL DNA; CISPLATIN; DOXORUBICIN; PACLITAXEL; PROTEIN TYROSINE KINASE INHIBITOR; RETINOBLASTOMA PROTEIN; SEPANTRONIUM BROMIDE; SURVIVIN; UNCLASSIFIED DRUG; (5-(2,4-BIS((3S)-3-METHYLMORPHOLIN-4-YL)PYRIDO(2,3-D)PYRIMIDIN-7-YL)-2-METHOXYPHENYL)METHANOL; AMINOPYRIDINE DERIVATIVE; MORPHOLINE DERIVATIVE; N-(4-(2-AMINO-3-CHLOROPYRIDIN-4-YLOXY)-3-FLUOROPHENYL)-4-ETHOXY-1-(4-FLUOROPHENYL)-2-OXO-1,2-DIHYDROPYRIDINE-3-CARBOXAMIDE; PROTEIN KINASE INHIBITOR; PYRIDONE DERIVATIVE; TARGET OF RAPAMYCIN KINASE;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER RESISTANCE; CELL NUCLEUS; CELL SIZE; CELL STRUCTURE; CELL VIABILITY; CHEMOSENSITIVITY; CONTROLLED STUDY; CYTOPLASM; DISSOCIATION; DNA CONTENT; DRUG CYTOTOXICITY; DRUG POTENTIATION; ENZYME ACTIVITY; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; METAPHASE; MITOSIS SPINDLE; PHENOTYPE; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SENESCENCE; WESTERN BLOTTING; AGING; ANTAGONISTS AND INHIBITORS; BREAST; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AGING; AMINOPYRIDINES; BREAST; BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MORPHOLINES; POLYPLOIDY; PROTEIN KINASE INHIBITORS; PYRIDONES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84899484841     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2013.12.014     Document Type: Article

References (49)

1. Ahmed N., Abubaker K., Findlay J., Quinn M. Epithelial mesenchymal transition and cancer stem cell-like phenotypes facilitate chemoresistance in recurrent ovarian cancer. Curr. Cancer Drug Targets 2010, 10:268-278.
2. Belalcazar A., Azaña D., Perez C.A., Raez L.E., Santos E.S. Targeting the Met pathway in lung cancer. Expert Rev. Anticancer Ther. 2012, 12:519-528.
3. Berezov A., Cai Z., Freudenberg J.A., Zhang H., Cheng X., Thompson T., et al. Disabling the mitotic spindle and tumor growth by targeting a cavity-induced allosteric site of survivin. Oncogene 2012, 31:1938-1948.
4. Beviglia L., Matsumoto K., Lin C.S., Ziober B.L., Kramer R.H. Expression of the c-Met/HGF receptor in human breast carcinoma: correlation with tumor progression. Int. J. Cancer 1997, 74:301-309.
5. Blumenschein G.R., Mills G.B., Gonzalez-Angulo A.M. Targeting the hepatocyte growth factor-cMET axis in cancer therapy. J.Clin. Oncol. 2012, 30:3287-3296.
6. Campisi J. Aging, cellular senescence, and cancer. Annu. Rev. Physiol. 2013, 75:685-705.
7. Cepero V., Sierra J.R., Corso S., Ghiso E., Casorzo L., Perera T., Comoglio P.M., Giordano S. MET and KRAS gene amplification mediates acquired resistance to MET tyrosine kinase inhibitors. Cancer Res. 2010, 70:7580-7590.
8. Choueiri T.K., Vaishampayan U., Rosenberg J.E., Logan T.F., Harzstark A.L., Bukowski R.M., Rini B.I., Srinivas S., Stein M.N., Adams L.M., Ottesen L.H., Laubscher K.H., Sherman L., McDermott D.F., Haas N.B., Flaherty K.T., Ross R., Eisenberg P., Meltzer P.S., Merino M.J., Bottaro D.P., Linehan W.M., Srinivasan R. Phase II and biomarker study of the dual MET/VEGFR2 inhibitor foretinib in patients with papillary renal cell carcinoma. J.Clin. Oncol. 2013, 31:181-186.
9. Chresta C.M., Davies B.R., Hickson I., Harding T., Cosulich S., Critchlow S.E., Vincent J.P., Ellston R., Jones D., Sini P., James D., Howard Z., Dudley P., Hughes G., Smith L., Maguire S., Hummersone M., Malagu K., Menear K., Jenkins R., Jacobsen M., Smith G.C., Guichard S., Pass M. AZD8055 is a potent, selective, and orally bioavailable ATP-competitive mammalian target of rapamycin kinase inhibitor with invitro and invivo antitumor activity. Cancer Res. 2010, 70:288-298.
10. Cornu M., Albert V., Hall M.N. mTOR in aging, metabolism, and cancer. Curr. Opin. Genet. Dev. 2013, 23:53-62.
11. Crescenzi E., Raia Z., Pacifico F., Mellone S., Moscato F., Palumbo G., Leonardi A. Down-regulation of wild-type p53-induced phosphatase 1 (Wip1) plays a critical role in regulating several p53-dependent functions in premature senescent tumor cells. J.Biol. Chem. 2013, 288:16212-16224.
12. Dai Y., Siemann D.W. BMS-777607, a small-molecule met kinase inhibitor, suppresses hepatocyte growth factor-stimulated prostate cancer metastatic phenotype invitro. Mol. Cancer Ther. 2010, 9:1554-1561.
13. Davis E., Teng H., Bilican B., Parker M.I., Liu B., Carriera S., et al. Ectopic Tbx2 expression results in polyploidy and cisplatin resistance. Oncogene 2008, 27:976-984.
14. Diamond J.R., Salgia R., Varella-Garcia M., Kanteti R., LoRusso P.M., Clark J.W., et al. Initial clinical sensitivity and acquired resistance to MET inhibition in MET-mutated papillary renal cell carcinoma. J.Clin. Oncol. 2013, 31:e254-e258.
15. Dick F.A., Rubin S.M. Molecular mechanisms underlying RB protein function. Nat. Rev. Mol. Cell Biol. 2013, 14:297-306.
16. Eder J.P., Shapiro G.I., Appleman L.J., Zhu A.X., Miles D., Keer H., et al. A phase I study of foretinib, a multi-targeted inhibitor of c-Met and vascular endothelial growth factor receptor 2. Clin. Cancer Res. 2010, 16:3507-3516.
17. Engelman J.A., Jänne P.A. Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin. Cancer Res. 2008, 14:2895-2899.
18. Engelman J.A., Zejnullahu K., Mitsudomi T., Song Y., Hyland C., Park J.O., Lindeman N., Gale C.M., Zhao X., Christensen J., Kosaka T., Holmes A.J., Rogers A.M., Cappuzzo F., Mok T., Lee C., Johnson B.E., Cantley L.C., Jänne P.A. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007, 316:1039-1043.
19. Garraway L.A., Jänne P.A. Circumventing cancer drug resistance in the era of personalized medicine. Cancer Discov. 2012, 2:214-226.
20. Gherardi E., Birchmeier W., Birchmeier C., Vande Woude G. Targeting MET in cancer: rationale and progress. Nat. Rev. Cancer 2012, 12:89-103.
21. Glaros T.G., Stockwin L.H., Mullendore M.E., Smith B., Morrison B.L., Newton D.L. The "survivin suppressants" NSC 80467 and YM155 induce a DNA damage response. Cancer Chemother. Pharmacol. 2012, 70:207-212.
22. Henley S.A., Dick F.A. The retinoblastoma family of proteins and their regulatory functions in the mammalian cell division cycle. Cell Div. 2012, 7:10.
23. Kelly R.J., Lopez-Chavez A., Citrin D., Janik J.E., Morris J.C. Impacting tumor cell-fate by targeting the inhibitor of apoptosis protein survivin. Mol. Cancer 2011, 10:35-42.
24. Kim H.P., Han S.W., Song S.H., Jeong E.G., Lee M.Y., Hwang D., Im S.A., Bang Y.J., Kim T.Y. Testican-1-mediated epithelial-mesenchymal transition signaling confers acquired resistance to lapatinib in HER2-positive gastric cancer. Oncogene 2013 Jul 22, (Epub ahead of print). 10.1038/onc.2013.285.
25. Knight J.F., Lesurf R., Zhao H., Pinnaduwage D., Davis R.R., Saleh S.M., Zuo D., Naujokas M.A., Chughtai N., Herschkowitz J.I., Prat A., Mulligan A.M., Muller W.J., Cardiff R.D., Gregg J.P., Andrulis I.L., Hallett M.T., Park M. Met synergizes with p53 loss to induce mammary tumors that possess features of claudin-low breast cancer. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E1301-E1310.
26. Kretschmann K.L., Eyob H., Buys S.S., Welm A.L. The macrophage stimulating protein/Ron pathway as a potential therapeutic target to impede multiple mechanisms involved in breast cancer progression. Curr. Drug Targets 2010, 11:1157-1168.
27. Lee W.Y., Chen H.H., Chow N.H., Su W.C., Lin P.W., Guo H.R. Prognostic significance of co-expression of RON and MET receptors in node-negative breast cancer patients. Clin. Cancer Res. 2005, 11:2222-2228.
28. McDermott U., Pusapati R.V., Christensen J.G., Gray N.S., Settleman J. Acquired resistance of non-small cell lung cancer cells to MET kinase inhibition is mediated by a switch to epidermal growth factor receptor dependency. Cancer Res. 2010, 70:1625-1634.
29. Merchant M., Ma X., Maun H.R., Zheng Z., Peng J., Romero M., Huang A., Yang N.Y., Nishimura M., Greve J., Santell L., Zhang Y.W., Su Y., Kaufman D.W., Billeci K.L., Mai E., Moffat B., Lim A., Duenas E.T., Phillips H.S., Xiang H., Young J.C., Vande Woude G.F., Dennis M.S., Reilly D.E., Schwall R.H., Starovasnik M.A., Lazarus R.A., Yansura D.G. Monovalent antibody design and mechanism of action of onartuzumab, a MET antagonist with anti-tumor activity as a therapeutic agent. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E2987-E2996.
30. Nakahara T., Kita A., Yamanaka K., Mori M., Amino N., Takeuchi M., Tominaga F., Kinoyama I., Matsuhisa A., Kudou M., Sasamata M. Broad spectrum and potent antitumor activities of YM155, a novel small-molecule survivin suppressant, in a wide variety of human cancer cell lines and xenograft models. Cancer Sci. 2011, 102:614-621.
31. Northrup A.B., Katcher M.H., Altman M.D., Chenard M., Daniels M.H., Deshmukh S.V., Falcone D., Guerin D.J., Hatch H., Li C., Lu W., Lutterbach B., Allison T.J., Patel S.B., Reilly J.F., Reutershan M., Rickert K.W., Rosenstein C., Soisson S.M., Szewczak A.A., Walker D., Wilson K., Young J.R., Pan B.S., Dinsmore C.J. Discovery of 1-[3-(1-Methyl-1H-pyrazol-4-yl)-5-oxo-5H-benzo [4,5]cyclohepta[1,2-b]pyridin-7-yl]-N-(pyridin-2-ylmethyl)methanesul-fonamide (MK-8033): a Specific c-Met/Ron dual kinase inhibitor with preferential affinity for the activated state of c-Met. J.Med. Chem. 2013, 56:2294-2310.
32. Padhye S.S., Guin S., Yao H.P., Zhou Y.Q., Zhang R., Wang M.H. Sustained expression of the RON receptor tyrosine kinase by pancreatic cancer stem cells as a potential targeting moiety for antibody-directed chemotherapeutics. Mol. Pharm. 2011, 8:2310-2319.
33. Pare R., Yang T., Shin J.S., Lee C.S. The significance of the senescence pathway in breast cancer progression. J.Clin. Pathol. 2013, 66:491-495.
34. Potratz J.C., Saunders D.N., Wai D.H., Ng T.L., McKinney S.E., Carboni J.M., Gottardis M.M., Triche T.J., Jürgens H., Pollak M.N., Aparicio S.A., Sorensen P.H. Synthetic lethality screens reveal RPS6 and MST1R as 6modifiers of insulin-like growth factor-1 receptor inhibitor activity in childhood sarcomas. Cancer Res. 2010, 70:8770-8781.
35. Qi J., McTigue M.A., Rogers A., Lifshits E., Christensen J.G., Jänne P.A., et al. Multiple mutations and bypass mechanisms can contribute to development of acquired resistance to MET inhibitors. Cancer Res. 2011, 71:1081-1091.
36. Romanov V.S., Pospelov V.A., Pospelova T.V. Cyclin-dependent kinase inhibitor p21(Waf1): contemporary view on its role in senescence and oncogenesis. Biochemistry (Mosc.) 2012, 77:575-584.
37. Schroeder G.M., An Y., Cai Z.W., Chen X.T., Clark C., Cornelius L.A., Dai J., Gullo-Brown J., Gupta A., Henley B., Hunt J.T., Jeyaseelan R., Kamath A., Kim K., Lippy J., Lombardo L.J., Manne V., Oppenheimer S., Sack J.S., Schmidt R.J., Shen G., Stefanski K., Tokarski J.S., Trainor G.L., Wautlet B.S., Wei D., Williams D.K., Zhang Y., Zhang Y., Fargnoli J., Borzilleri R.M. Discovery of N-(4-(2-amino-3-chloropyridin-4-yloxy)-3-fluorophenyl)-4-ethoxy-1-(4-fluorophenyl)-2-oxo-1,2 dihy-dropyridine-3-carboxamide (BMS-777607), a selective and orally efficacious inhibitor of the Met kinase superfamily. J.Med. Chem. 2009, 52:1251-1258.
38. Sharma S., Zeng Z.J., Zhuang C.M., Zhou Y.Q., Yao H.P., Hu X., et al. Small-molecule inhibitor BMS-777607 induces breast cancer cell polyploidy with increased resistance to cytotoxic chemotherapy agents. Mol. Cancer Ther. 2013, 12:725-736.
39. Shien K., Toyooka S., Yamamoto H., Soh J., Jida M., Thu K.L., et al. Acquired resistance to EGFR inhibitors is associated with a manifestation of stem cell-like properties in cancer cells. Cancer Res. 2013, 73:3051-3061.
40. Wang M.H., Lee W., Luo Y.L., Weis M.T., Yao H.P. Altered expression of the RON receptor tyrosine kinase in various epithelial cancers and its contribution to tumorigenic phenotypes in thyroid cancer cells. J.Pathol. 2007, 213:402-411.
41. Wang M.H., Ronsin C., Gesnel M.C., Coupey L., Skeel A., Leonard E.J., Breathnach R. Identification of the ron gene product as the receptor for the human macrophage stimulating protein. Science 1994, 266:117-119.
42. Wang Q., Wu P.C., Roberson R.S., Luk B.V., Ivanova I., Chu E., Wu D.Y. Survivin and escaping in therapy-induced cellular senescence. Int. J. Cancer 2011, 128:1546-1558.
43. Wheeler D.L., Dunn E.F., Harari P.M. Understanding resistance to EGFR inhibitors-impact on future treatment strategies. Nat. Rev. Clin. Oncol. 2010, 7:493-507.
44. Yamauchi T., Nakamura N., Hiramoto M., Yuri M., Yokota H., Naitou M., Takeuchi M., Yamanaka K., Kita A., Nakahara T., Kinoyama I., Matsuhisa A., Kaneko N., Koutoku H., Sasamata M., Kobori M., Katou M., Tawara S., Kawabata S., Furuichi K. Sepantronium bromide (YM155) induces disruption of the ILF3/p54(nrb) complex, which is required for survivin expression. Biochem. Biophys. Res. Commun. 2012, 425:711-716.
45. Yao H.P., Luo Y.L., Feng L., Cheng L.F., Lu Y., Li W., Wang M.H. Agonistic monoclonal antibodies potentiate tumorigenic and invasive activities of splicing variant of the RON receptor tyrosine kinase. Cancer Biol. Ther. 2006, 5:1179-1186.
46. Yao H.P., Zhou Y.Q., Ma Q., Guin S., Padhye S.S., Zhang R.W., Wang M.H. The monoclonal antibody Zt/f2 targeting RON receptor tyrosine kinase as potential therapeutics against tumor growth-mediated by colon cancer cells. Mol. Cancer 2011, 10:82-93.
47. Yao H.P., Zhuang C.M., Zhou Y.Q., Zeng J.Y., Zhang R., Wang M.H. Oncogenic variant RON160 expression in breast cancer and its potential as a therapeutic target by small molecule tyrosine kinase inhibitor. Curr. Cancer Drug Targets 2013, 13:686-697.
48. Yao H.P., Zhou Y.Q., Zhang R., Wang M.H. MSP-RON signaling in cancer: pathogenesis and therapeutic potential. Nat. Rev. Cancer 2013, 13:466-481.
49. Zou Y., Howell G.M., Humphrey L.E., Wang J., Brattain M.G. Ron knockdown and ron monoclonal antibody IMC-RON8 sensitize pancreatic cancer to Histone Deacetylase inhibitors (HDACi). PLoS One 2013, 8:e69092-e69100.