Activation of microRNA-494-targeting Bmi1 and ADAM10 by silibinin ablates cancer stemness and predicts favourable prognostic value in head and neck squamous cell carcinomas

Oncotarget

Volumn 6, Issue 27, 2015, Pages 24002-24016

  Chang, Yu Chao ^a,b   Jan, Chia Ing ^c,d   Peng, Chih Yu ^a,b   Lai, Yu Chi ^a   Hu, Fang Wei ^a,b   Yu, Cheng Chia ^a,b  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d CHINA MEDICAL UNIVERSITY BEIGANG HOSPITAL   (Taiwan)

Author keywords

Head and neck squamous cell carcinomas; MicroRNA 494; Silibinin; Tumor initiating cells

Indexed keywords

ADAM10 ENDOPEPTIDASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; BMI1 PROTEIN; CD133 ANTIGEN; MICRORNA; MICRORNA 494; SILIBININ; UNCLASSIFIED DRUG; ADAM PROTEIN; ADAM10 PROTEIN, HUMAN; BMI1 PROTEIN, HUMAN; CD44 PROTEIN, HUMAN; GLYCOPROTEIN; HERMES ANTIGEN; ISOENZYME; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN; MIRN494 MICRORNA, HUMAN; PEPTIDE; PROM1 PROTEIN, HUMAN; PROM1 PROTEIN, MOUSE; RETINAL DEHYDROGENASE; SECRETASE; SILYMARIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PROGNOSIS; CANCER STEMNESS; CARCINOGENICITY; CELL PROLIFERATION; CELL RENEWAL; CHEMOSENSITIVITY; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG RESISTANCE; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; HEAD AND NECK SQUAMOUS CELL CARCINOMA; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; ONCOLOGICAL PARAMETERS; PROTEIN EXPRESSION; PROTEIN TARGETING; SURVIVAL TIME; TUMOR CELL; TUMOR GROWTH; TUMOR INITIATING CELL; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CANCER STEM CELL; CANCER TRANSPLANTATION; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; GENETICS; HEAD AND NECK TUMOR; HUMAN; INCIDENCE; METABOLISM; METASTASIS; NUDE MOUSE; PHENOTYPE; PROGNOSIS; SQUAMOUS CELL CARCINOMA; TUMOR INVASION;

AC133 ANTIGEN; ADAM PROTEINS; ADAM10 PROTEIN; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTIGENS, CD; ANTIGENS, CD44; CARCINOMA, SQUAMOUS CELL; CELL PROLIFERATION; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; GLYCOPROTEINS; HEAD AND NECK NEOPLASMS; HUMANS; INCIDENCE; ISOENZYMES; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PEPTIDES; PHENOTYPE; POLYCOMB REPRESSIVE COMPLEX 1; PROGNOSIS; RETINAL DEHYDROGENASE; SILYMARIN;

EID: 84943399497     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4365     Document Type: Article

References (56)

1. Kamangar F, Dores GM and Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents:defining priorities to reduce cancer disparities in different geographic regions of the world. Journal of clinical oncology :official journal of the American Society of Clinical Oncology. 2006;24:2137-2150.
2. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA:a cancer journal for clinicians. 2014;64:9-29.
3. Gibson MK and Forastiere AA. Reassessment of the role of induction chemotherapy for head and neck cancer. The Lancet Oncology. 2006;7:565-574.
4. Medema JP. Cancer stem cells:the challenges ahead. Nature cell biology. 2013;15:338-344.
5. Rosen JM and Jordan CT. The increasing complexity of the cancer stem cell paradigm. Science. 2009;324:1670-1673.
6. Visvader JE and Lindeman GJ. Cancer stem cells:current status and evolving complexities. Cell stem cell. 2012; 10:717-728.
7. Yu CC, Tsai LL, Wang ML, Yu CH, Lo WL, Chang YC, Chiou GY, Chou MY and Chiou SH. miR145 targets the SOX9/ADAM17 axis to inhibit tumor-initiating cells and IL-6-mediated paracrine effects in head and neck cancer. Cancer research. 2013;73:3425-3440.
8. Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, Tsai TH, Chou SH, Chien CS, Ku HH and Lo JF. Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clinical cancer research :an official journal of the American Association for Cancer Research. 2008;14:4085-4095.
9. Lo WL, Yu CC, Chiou GY, Chen YW, Huang PI, Chien CS, Tseng LM, Chu PY, Lu KH, Chang KW, Kao SY and Chiou SH. MicroRNA-200c attenuates tumour growth and metastasis of presumptive head and neck squamous cell carcinoma stem cells. J Pathol. 2011;223:482-495.
10. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, Weissman IL, Clarke MF and Ailles LE. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proceedings of the National Academy of Sciences of the United States of America. 2007;104:973-978.
11. Chen PN, Hsieh YS, Chiang CL, Chiou HL, Yang SF and Chu SC. Silibinin inhibits invasion of oral cancer cells by suppressing the MAPK pathway. Journal of dental research. 2006;85:220-225.
12. Zeng J, Sun Y, Wu K, Li L, Zhang G, Yang Z, Wang Z, Zhang D, Xue Y, Chen Y, Zhu G, Wang X and He D. Chemopreventive and chemotherapeutic effects of intravesical silibinin against bladder cancer by acting on mitochondria. Molecular cancer therapeutics. 2011;10:104-116.
13. Chang HR, Chen PN, Yang SF, Sun YS, Wu SW, Hung TW, Lian JD, Chu SC and Hsieh YS. Silibinin inhibits the invasion and migration of renal carcinoma 786-O cells in vitro, inhibits the growth of xenografts in vivo and enhances chemosensitivity to 5-fluorouracil and paclitaxel. Molecular carcinogenesis. 2011;50:811-823.
14. Zhang S, Yang Y, Liang Z, Duan W, Yang J, Yan J, Wang N, Feng W, Ding M, Nie Y and Jin Z. Silybin-mediated inhibition of Notch signaling exerts antitumor activity in human hepatocellular carcinoma cells. PloS one. 2013; 8:e83699.
15. Lu W, Lin C, King TD, Chen H, Reynolds RC and Li Y. Silibinin inhibits Wnt/beta-catenin signaling by suppressing Wnt co-receptor LRP6 expression in human prostate and breast cancer cells. Cellular signalling. 2012;24:2291-2296.
16. Singh RP, Raina K, Deep G, Chan D and Agarwal R. Silibinin suppresses growth of human prostate carcinoma PC-3 orthotopic xenograft via activation of extracellular signal-regulated kinase 1/2 and inhibition of signal transducers and activators of transcription signaling. Clinical cancer research :an official journal of the American Association for Cancer Research. 2009;15:613-621.
17. Wu K, Ning Z, Zeng J, Fan J, Zhou J, Zhang T, Zhang L, Chen Y, Gao Y, Wang B, Guo P, Li L, Wang X and He D. Silibinin inhibits beta-catenin/ZEB1 signaling and suppresses bladder cancer metastasis via dual-blocking epithelial-mesenchymal transition and stemness. Cellular signalling. 2013;25:2625-2633.
18. Kumar S, Raina K, Agarwal C and Agarwal R. Silibinin strongly inhibits the growth kinetics of colon cancer stem cell-enriched spheroids by modulating interleukin 4/6-mediated survival signals. Oncotarget. 2014;5:4972-4989.
19. Yu SL, Chen HY, Chang GC, Chen CY, Chen HW, Singh S, Cheng CL, Yu CJ, Lee YC, Chen HS, Su TJ, Chiang CC, Li HN, Hong QS, Su HY, Chen CC, et al. MicroRNA signature predicts survival and relapse in lung cancer. Cancer Cell. 2008;13:48-57.
20. Seike M, Goto A, Okano T, Bowman ED, Schetter AJ, Horikawa I, Mathe EA, Jen J, Yang P, Sugimura H, Gemma A, Kudoh S, Croce CM and Harris CC. MiR-21 is an EGFR-regulated anti-apoptotic factor in lung cancer in never-smokers. Proc Natl Acad Sci U S A. 2009; 106:12085-12090.
21. Iorio MV, Casalini P, Tagliabue E, Menard S and Croce CM. MicroRNA profiling as a tool to understand prognosis, therapy response and resistance in breast cancer. Eur J Cancer. 2008;44:2753-2759.
22. Romano G, Acunzo M, Garofalo M, Di Leva G, Cascione L, Zanca C, Bolon B, Condorelli G and Croce CM. MiR-494 is regulated by ERK1/2 and modulates TRAIL-induced apoptosis in non-small-cell lung cancer through BIM down-regulation. Proceedings of the National Academy of Sciences of the United States of America. 2012;109:16570-16575.
23. Shen PF, Chen XQ, Liao YC, Chen N, Zhou Q, Wei Q, Li X, Wang J and Zeng H. MicroRNA-494-3p targets CXCR4 to suppress the proliferation, invasion, and migration of prostate cancer. The Prostate. 2014;74:756-767.
24. Kim WK, Park M, Kim YK, Tae YK, Yang HK, Lee JM and Kim H. MicroRNA-494 downregulates KIT and inhibits gastrointestinal stromal tumor cell proliferation. Clinical cancer research :an official journal of the American Association for Cancer Research. 2011;17:7584-7594.
25. Yamanaka S, Campbell NR, An F, Kuo SC, Potter JJ, Mezey E, Maitra A and Selaru FM. Coordinated effects of microRNA-494 induce G(2)/M arrest in human cholangiocarcinoma. Cell Cycle. 2012;11:2729-2738.
26. Sun HB, Chen X, Ji H, Wu T, Lu HW, Zhang Y, Li H and Li YM. miR494 is an independent prognostic factor and promotes cell migration and invasion in colorectal cancer by directly targeting PTEN. International journal of oncology. 2014;45:2486-2494.
27. Liu C and Tang DG. MicroRNA regulation of cancer stem cells. Cancer research. 2011;71:5950-5954.
28. Humphries B and Yang C. The microRNA-200 family: small molecules with novel roles in cancer development, progression and therapy. Oncotarget. 2015;6:6472-6498.
29. Ceppi P and Peter ME. MicroRNAs regulate both epithelialto-mesenchymal transition and cancer stem cells. Oncogene. 2014;33:269-278.
30. Xia H, Cheung WK, Sze J, Lu G, Jiang S, Yao H, Bian XW, Poon WS, Kung HF and Lin MC. miR-200a regulates epithelial-mesenchymal to stem-like transition via ZEB2 and beta-catenin signaling. The Journal of biological chemistry. 2010;285:36995-37004.
31. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D and Tang DG. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nature medicine. 2011;17:211-215.
32. Visus C, Ito D, Amoscato A, Maciejewska-Franczak M, Abdelsalem A, Dhir R, Shin DM, Donnenberg VS, Whiteside TL and DeLeo AB. Identification of human aldehyde dehydrogenase 1 family member A1 as a novel CD8+ T-cell-defined tumor antigen in squamous cell carcinoma of the head and neck. Cancer Res. 2007; 67:10538-10545.
33. Chen YC, Chen YW, Hsu HS, Tseng LM, Huang PI, Lu KH, Chen DT, Tai LK, Yung MC, Chang SC, Ku HH, Chiou SH and Lo WL. Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun. 2009; 385:307-313.
34. Hu FW, Tsai LL, Yu CH, Chen PN, Chou MY and Yu CC. Impairment of tumor-initiating stem-like property and reversal of epithelial-mesenchymal transdifferentiation in head and neck cancer by resveratrol treatment. Molecular nutrition & food research. 2012;56:1247-1258.
35. Chen YS, Wu MJ, Huang CY, Lin SC, Chuang TH, Yu CC and Lo JF. CD133/Src axis mediates tumor initiating property and epithelial-mesenchymal transition of head and neck cancer. PloS one. 2011;6:e28053.
36. Nguyen LV, Vanner R, Dirks P and Eaves CJ. Cancer stem cells:an evolving concept. Nature reviews Cancer. 2012; 12:133-143.
37. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C and Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 2010;468:829-833.
38. Alvero AB, Fu HH, Holmberg J, Visintin I, Mor L, Marquina CC, Oidtman J, Silasi DA and Mor G. Stemlike ovarian cancer cells can serve as tumor vascular progenitors. Stem Cells. 2009;27:2405-2413.
39. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J and Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704-715.
40. Asiedu MK, Ingle JN, Behrens MD, Radisky DC and Knutson KL. TGFbeta/TNF(alpha)-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype. Cancer research. 2011; 71:4707-4719.
41. Dean M, Fojo T and Bates S. Tumour stem cells and drug resistance. Nature reviews Cancer. 2005;5:275-284.
42. Cufi S, Bonavia R, Vazquez-Martin A, Oliveras-Ferraros C, Corominas-Faja B, Cuyas E, Martin-Castillo B, BarrajonCatalan E, Visa J, Segura-Carretero A, Joven J, BoschBarrera J, Micol V and Menendez JA. Silibinin suppresses EMT-driven erlotinib resistance by reversing the high miR-21/low miR-200c signature in vivo. Scientific reports. 2013; 3:2459.
43. Pirrotta V. Polycombing the genome:PcG, trxG, and chromatin silencing. Cell. 1998;93:333-336.
44. Allegra E, Trapasso S, Pisani D and Puzzo L. The role of BMI1 as a biomarker of cancer stem cells in head and neck cancer:a review. Oncology. 2014;86:199-205.
45. Yu CC, Lo WL, Chen YW, Huang PI, Hsu HS, Tseng LM, Hung SC, Kao SY, Chang CJ and Chiou SH. Bmi-1 Regulates Snail Expression and Promotes Metastasis Ability in Head and Neck Squamous Cancer-Derived ALDH1 Positive Cells. Journal of oncology. 2011;2011.
46. Murphy G. The ADAMs:signalling scissors in the tumour microenvironment. Nature reviews Cancer. 2008;8:929-941.
47. Tsai YH, VanDussen KL, Sawey ET, Wade AW, Kasper C, Rakshit S, Bhatt RG, Stoeck A, Maillard I, Crawford HC, Samuelson LC and Dempsey PJ. ADAM10 regulates Notch function in intestinal stem cells of mice. Gastroenterology. 2014;147:822-834 e813.
48. Wolpert F, Tritschler I, Steinle A, Weller M and Eisele G. A disintegrin and metalloproteinases 10 and 17 modulate the immunogenicity of glioblastoma-initiating cells. Neurooncology. 2014;16:382-391.
49. Jones AV, Lambert DW, Speight PM and Whawell SA. ADAM 10 is over expressed in oral squamous cell carcinoma and contributes to invasive behaviour through a functional association with alphavbeta6 integrin. FEBS letters. 2013;587:3529-3534.
50. Bai Y, Sun Y, Peng J, Liao H, Gao H, Guo Y and Guo L. Overexpression of secretagogin inhibits cell apoptosis and induces chemoresistance in small cell lung cancer under the regulation of miR-494. Oncotarget. 2014;5:7760-7775.
51. Kwak SY, Yang JS, Kim BY, Bae IH and Han YH. Ionizing radiation-inducible miR-494 promotes glioma cell invasion through EGFR stabilization by targeting p190B rhoGAP. Biochimica et biophysica acta. 2014;1843:508-516.
52. Li L, Li Z, Kong X, Xie D, Jia Z, Jiang W, Cui J, Du Y, Wei D, Huang S and Xie K. Down-regulation of microRNA-494 via loss of SMAD4 increases FOXM1 and beta-catenin signaling in pancreatic ductal adenocarcinoma cells. Gastroenterology. 2014;147:485-497 e418.
53. Singh RP, Mallikarjuna GU, Sharma G, Dhanalakshmi S, Tyagi AK, Chan DC, Agarwal C and Agarwal R. Oral silibinin inhibits lung tumor growth in athymic nude mice and forms a novel chemocombination with doxorubicin targeting nuclear factor kappaB-mediated inducible chemoresistance. Clinical cancer research :an official journal of the American Association for Cancer Research. 2004;10:8641-8647.
54. Kasten FH, Soileau K and Meffert RM. Quantitative evaluation of human gingival epithelial cell attachment to implant surfaces in vitro. The International journal of periodontics & restorative dentistry. 1990;10:68-79.
55. Chen SF, Chang YC, Nieh S, Liu CL, Yang CY and Lin YS. Nonadhesive culture system as a model of rapid sphere formation with cancer stem cell properties. PloS one. 2012; 7:e31864.
56. Ebert MS, Neilson JR and Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nature methods. 2007;4:721-726.