Therapeutic targeting of CBP/β-catenin signaling reduces cancer stem-like population and synergistically suppresses growth of EBV-positive nasopharyngeal carcinoma cells with cisplatin

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Chan, King Chi ^a   Chan, Lai Sheung ^a   Ip, Joseph Chok Yan ^b   Lo, Carman ^c   Yip, Timothy Tak Chun ^b,d   Ngan, Roger Kai Cheong ^b,d   Wong, Ricky Ngok Shun ^a,b   Lo, Kwok Wai ^c   Ng, Wai Tong ^b,e   Lee, Anne Wing Mui ^b,e   Tsao, George Sai Wah ^b   Kahn, Michael ^f   Lung, Maria Li ^b   Mak, Nai Ki ^a,b  

^a HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d QUEEN ELIZABETH HOSPITAL   (Hong Kong)

^e PAMELA YOUDE NETHERSOLE EASTERN HOSPITAL   (Hong Kong)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BETA CATENIN; CISPLATIN; FUSED HETEROCYCLIC RINGS; HERMES ANTIGEN; HISTONE ACETYLTRANSFERASE PCAF; MICRORNA; MIRN145 MICRORNA, HUMAN; N BENZYL 1,2,3,4,8,9 HEXAHYDRO 6 (4 HYDROXYBENZYL) 8 (1 NAPHTHYLMETHYL) 4,7 DIOXO 2H PYRAZINO[1,2 A]PYRIMIDINE 1(6H) CARBOXAMIDE; PYRIMIDINONE DERIVATIVE; SMALL INTERFERING RNA; SOX2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX;

ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER STEM CELL; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG EFFECTS; DRUG POTENTIATION; EPITHELIAL MESENCHYMAL TRANSITION; EPSTEIN BARR VIRUS; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MOUSE; NASOPHARYNGEAL NEOPLASMS; NUDE MOUSE; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VIROLOGY; XENOGRAFT;

ANIMALS; ANTIGENS, CD44; ANTINEOPLASTIC AGENTS; BETA CATENIN; BRIDGED BICYCLO COMPOUNDS, HETEROCYCLIC; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; DRUG SYNERGISM; EPITHELIAL-MESENCHYMAL TRANSITION; HERPESVIRUS 4, HUMAN; HUMANS; MICE; MICE, NUDE; MICRORNAS; MICROSCOPY, CONFOCAL; NASOPHARYNGEAL NEOPLASMS; NEOPLASTIC STEM CELLS; P300-CBP TRANSCRIPTION FACTORS; PYRIMIDINONES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84928382257     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09979     Document Type: Article

References (57)

1. Lo, K. W., To, K. F., Huang, D. P. Focus on nasopharyngeal carcinoma. Cancer Cell 5, 423-428 (2004).
2. Tsao, S. W. et al. Etiological factors of nasopharyngeal carcinoma. Oral Oncol. 50, 330-338 (2014).
3. Cheung, S. T. et al. Nasopharyngeal carcinoma cell line (C666-1) consistently harbouring Epstein-Barr virus. Int. J. Cancer 83, 121-126 (1999).
4. Razak, A. R. et al. Nasopharyngeal carcinoma: the next challenges. Eur. J. Cancer 46, 1967-1978 (2010).
5. Chan, A. T. Nasopharyngeal carcinoma. Ann. Oncol. 21 Suppl 7, vii308-vii312 (2010).
6. Reya, T., Morrison, S. J., Clarke, M. F., Weissman, I. L. Stem cells, cancer, and cancer stem cells. Nature 414, 105-111 (2001).
7. O'Brien, C. A., Kreso, A., Dick, J. E. Cancer stem cells in solid tumors: an overview. Semin. Radiat. Oncol. 19, 71-77 (2009).
8. Morrison, R. et al. Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis.J. Oncol. 2011, 941876 (2011).
9. Liu, H. G., Chen, C, Yang, H., Pan, Y. F., Zhang, X. H. Cancer stem cell subsets and their relationships. J. Transl. Med. 9, 50 (2011).
10. Takebe, N., Harris, P. J., Warren, R. Q., Ivy, S. P. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat. Rev. Clin. Oncol. 8, 97-106 (2011).
11. Takahashi-Yanaga, F., Kahn, M. Targeting Wnt signaling: can we safely eradicate cancer stem cells? Clin. Cancer Res. 16, 3153-3162 (2010).
12. Wang, F. L. et al. Expression and clinical significance of Wnt-1 and beta-catenin in nasopharyngeal carcinoma. Ai. Zheng 28, 72-75 (2009).
13. Zeng, Z. Y. et al. Gene expression profiling of nasopharyngeal carcinoma reveals the abnormally regulated Wnt signaling pathway. Hum. Pathol. 38, 120-133 (2007).
14. Xu, L. et al. Aberrant expression of beta-catenin and E-cadherin is correlated with poor prognosis of nasopharyngeal cancer. Hum. Pathol. 44, 1357-1364 (2013).
15. Chan, S. L. et al. The tumor suppressor Wnt inhibitory factor 1 is frequently methylated in nasopharyngeal and esophageal carcinomas. Lab. Invest. 87, 644-650 (2007).
16. Fendri, A. et al. Epigenetic alteration of the Wnt inhibitory factor-1 promoter is common and occurs in advanced stage of Tunisian nasopharyngeal carcinoma. Cancer Invest. 28, 896-903 (2010).
17. Cheng, Y. et al. Physiological beta-catenin signaling controls self-renewal networks and generation of stem-like cells from nasopharyngeal carcinoma. BMC Cell Biol. 14, 44 (2013).
18. Lenz, H. J., Kahn, M. Safely targeting cancer stem cells via selective catenin coactivator antagonism. Cancer Sci. 105, 1087-1092 (2014).
19. Kahn, M. Can we safely target the WNT pathway? Nat. Rev. Drug Discov. 13, 513-532 (2014).
20. Gang, E. J. et al. Small-molecule inhibition of CBP/catenin interactions eliminates drug-resistant clones in acute lymphoblastic leukemia. Oncogene 33, 2169-2178 (2014).
21. Wend, P. et al. Wnt/beta-catenin signalling induces MLL to create epigenetic changes in salivary gland tumours. Embo. J. 32, 1977-1989 (2013).
22. He, K. et al. Cancer cells acquire a drug resistant, highly tumorigenic, cancer stemlike phenotype through modulation of the PI3K/Akt/beta-catenin/CBP pathway. Int. J. Cancer 134, 43-54 (2014).
23. Lukaszewicz, A. I., McMillan, M. K., Kahn, M. Small molecules and stem cells. Potency and lineage commitment: the new quest for the fountainof youth. J. Med. Chem. 53, 3439-3453 (2010).
24. Teo, J. L., Kahn, M. The Wnt signaling pathway in cellular proliferation and differentiation: A tale of two coactivators. Adv. Drug Deliv. Rev. 62, 1149-1155 (2010).
25. Polyak, K., Weinberg, R. A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer 9, 265-273 (2009).
26. Pastrana, E., Silva-Vargas, V., Doetsch, F. Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 8, 486-498 (2011).
27. Lun, S. W. et al. CD441 cancer stem-like cells in EBV-associated nasopharyngeal carcinoma. PLoS One 7, e52426 (2012).
28. Takahashi, K., Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (2006).
29. Leis, O. et al. Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene 31, 1354-1365 (2012).
30. Xu, N., Papagiannakopoulos, T., Pan, G., Thomson, J.A., Kosik, K.S. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137, 647-658 (2009).
31. Chen, H. C. et al. MicroRNA deregulation and pathway alterations in nasopharyngeal carcinoma. Br. J. Cancer 100, 1002-1011 (2009).
32. Singh, S. K. et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 63, 5821-5828 (2003).
33. Liu, J. C., Deng, T., Lehal, R. S., Kim, J., Zacksenhaus, E. Identification of tumorsphere-and tumor-initiating cells in HER2/Neu-induced mammary tumors. Cancer Res. 67, 8671-8681 (2007).
34. Zhang, S. et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 68, 4311-4320 (2008).
35. Wang, J., Guo, L. P., Chen, L. Z., Zeng, Y. X., Lu, S. H. Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Res. 67, 3716-3724 (2007).
36. Smith, P. A., Merritt, D., Barr, L., Thorley-Lawson, D. A. An orthotopic model of metastatic nasopharyngeal carcinoma and its application in elucidating a therapeutic target that inhibits metastasis. Genes. Cancer 2, 1023-1033 (2011).
37. Wang, S. J., Bourguignon, L. Y. Role of hyaluronan-mediated CD44 signaling in head and neck squamous cell carcinoma progression and chemoresistance. Am. J. Pathol. 178, 956-963 (2011).
38. Ma, H., Nguyen, C., Lee, K. S., Kahn, M. Differential roles for the coactivators CBP and p300 on TCF/beta-catenin-mediated survivin gene expression. Oncogene. 24, 3619-3631 (2005).
39. Sung, F. L. et al. Antitumor effect and enhancement of cytotoxic drug activity by cetuximab in nasopharyngeal carcinoma cells. In Vivo 19, 237-245 (2005).
40. Wang, Z.etal. FoxM1in tumorigenicityofthe neuroblastoma cells and renewal of the neural progenitors. Cancer Res. 71, 4292-4302 (2011).
41. Lee, T. I. et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125, 301-313 (2006).
42. Wang, X. et al. Prognostic significance of SOX2 expression in nasopharyngeal carcinoma. Cancer Invest 30, 79-85 (2012).
43. Ma, B. et al. A phase II study of patients with metastatic or locoregionally recurrent nasopharyngeal carcinoma and evaluation of plasma Epstein-Barr virus DNAas a biomarker of efficacy. Cancer Chemother. Pharmacol. 62, 59-64 (2008).
44. Ma, B. B. et al. Preclinical activity of gefitinib in non-keratinizing nasopharyngeal carcinoma cell lines and biomarkers of response. Invest New Drugs 28, 326-333 (2010).
45. Chen, H. et al. Adenovirus-mediated RNA interference targeting FOXM1 transcription factor suppresses cell proliferation and tumor growth of nasopharyngeal carcinoma. J. Gene. Med. 14, 231-240 (2012).
46. Tong, Z. T. et al. EZH2 supports nasopharyngeal carcinoma cell aggressiveness by forming a co-repressor complex with HDAC1/HDAC2 and Snail to inhibit E-cadherin. Oncogene 31, 583-594 (2012).
47. Port, R. J. et al. Epstein-Barr virus induction of the Hedgehog signalling pathway imposes a stem cell phenotype on human epithelial cells. J. Pathol. 231, 367-377 (2013).
48. Tay, Y., Zhang, J., Thomson, A. M., Lim, B., Rigoutsos, I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455, 1124-1128 (2008).
49. Chivukula, R. R., Mendell, J. T. Abate and switch: miR-145 in stem cell differentiation. Cell 137, 606-608 (2009).
50. Ma, N., Gao X. beta-Actin is predicted as one of the potential targets of miR-145: choose internal control gene in verification of microRNA target. Carcinogenesis 34, 236 (2013).
51. Chen, L.etal. Concurrent chemoradiotherapy plus adjuvant chemotherapy versus concurrent chemoradiotherapy alone in patients with locoregionally advanced nasopharyngeal carcinoma: a phase 3 multicentre randomised controlled trial. The Lancet Oncology 13, 163-171 (2012).
52. Glaser, R. et al. Two epithelial tumor cell lines (HNE-1 and HONE-1) latently infected with Epstein-Barr virus that were derived from nasopharyngeal carcinomas. Proc Natl Acad Sci U S A 86, 9524-9528 (1989).
53. Huang, D. P. et al. Establishment of a cell line (NPC/HK1) from a differentiated squamous carcinoma of the nasopharynx. Int. J. Cancer 26, 127-132 (1980).
54. Huang, D. P., Ho, J. H., Chan, W. K., Lau, W. H., Lui, M. Cytogenetics of undifferentiated nasopharyngeal carcinoma xenografts from southern Chinese. Int. J. Cancer 43, 936-939 (1989).
55. Chan, K. C. et al. A novel Hsp90 inhibitor AT13387 induces senescence in EBV-positive nasopharyngeal carcinoma cells and suppresses tumor formation. Mol. Cancer 12, 128 (2013).
56. Ting, C. M. et al. Role of STAT3/5 and Bcl-2/xL in 2-methoxyestradiol-induced endoreduplication of nasopharyngeal carcinoma cells. Mol. Carcinog. 51, 963-972 (2012).
57. Chou, T.-C., Talalay, P. Analysis of combined drug effects: a new look at a very old problem. Trends Pharmacology Science 4, 450-454 (1983).