Suppression of miR-204 enables oral squamous cell carcinomas to promote cancer stemness, EMT traits, and lymph node metastasis

Oncotarget

Volumn 7, Issue 15, 2016, Pages 20180-20192

  Yu, Cheng Chia ^a,b   Chen, Pei Ni ^a   Peng, Chih Yu ^a,b   Yu, Chuan Hang ^a,b   Chou, Ming Yung ^a,b  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

EMT; Metastasis; MiR 204; Oral squamous cell carcinomas; Stemness

Indexed keywords

MICRORNA; MICRORNA 204; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SOX4; UNCLASSIFIED DRUG; ALDEHYDE DEHYDROGENASE ISOENZYME 1; ISOENZYME; MIRN204 MICRORNA, HUMAN; RETINAL DEHYDROGENASE; SNAI1 PROTEIN, HUMAN; SOX4 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX; TUMOR MARKER;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INCIDENCE; CANCER INHIBITION; CANCER PROGNOSIS; CANCER STEM CELL; CANCER STEMNESS; CANCER SURVIVAL; CELL SELF-RENEWAL; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LYMPH NODE METASTASIS; MITOSIS INHIBITION; MOUSE; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; ONCOLOGICAL PARAMETERS; OVERALL SURVIVAL; PREDICTION; PROTEIN RNA BINDING; PROTEIN SYNTHESIS INHIBITION; PROTEIN TARGETING; UPREGULATION; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; CELL CYCLE; CELL MOTION; CELL PROLIFERATION; DOWN REGULATION; DRUG SCREENING; GENETICS; METABOLISM; MOUTH TUMOR; NUDE MOUSE; PATHOLOGY; PROGNOSIS; SECONDARY; SQUAMOUS CELL CARCINOMA; SURVIVAL RATE; TUMOR CELL CULTURE;

ANIMALS; APOPTOSIS; BIOMARKERS, TUMOR; CARCINOMA, SQUAMOUS CELL; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; ISOENZYMES; LYMPHATIC METASTASIS; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MOUTH NEOPLASMS; NEOPLASTIC STEM CELLS; PROGNOSIS; RETINAL DEHYDROGENASE; SNAIL FAMILY TRANSCRIPTION FACTORS; SOXC TRANSCRIPTION FACTORS; SURVIVAL RATE; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84964793179     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7745     Document Type: Article

References (41)

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. Chang YC, Jan CI, Peng CY, Lai YC, Hu FW and Yu CC. 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. 2015; 6:24002-24016. doi: 10.18632/oncotarget.4365.
3. 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.
4. Chou MY, Hu FW, Yu CH and Yu CC. Sox2 expression involvement in the oncogenicity and radiochemoresistance of oral cancer stem cells. Oral oncology. 2015; 51:31-39.
5. 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.
6. 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.
7. Clay MR, Tabor M, Owen JH, Carey TE, Bradford CR, Wolf GT, Wicha MS and Prince ME. Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase. Head & neck. 2010; 32:1195-1201.
8. Wu MJ, Jan CI, Tsay YG, Yu YH, Huang CY, Lin SC, Liu CJ, Chen YS, Lo JF and Yu CC. Elimination of head and neck cancer initiating cells through targeting glucose regulated protein78 signaling. Molecular cancer. 2010; 9:283.
9. Yu C, Hu F, Ph DC and Chou M. Targeting CD133 in the enhancement of chemosensitivity in oral squamous cell carcinomas-derived side population cancer stem cells. Head & neck. 2014.
10. Sun S and Wang Z. Head neck squamous cell carcinoma c-Met(+) cells display cancer stem cell properties and are responsible for cisplatin-resistance and metastasis. International journal of cancer Journal international du cancer. 2011; 129:2337-2348.
11. 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.
12. 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.
13. 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.
14. Xia Z, Liu F, Zhang J and Liu L. Decreased Expression of MiRNA-204-5p Contributes to Glioma Progression and Promotes Glioma Cell Growth, Migration and Invasion. PloS one. 2015; 10:e0132399.
15. Imam JS, Plyler JR, Bansal H, Prajapati S, Bansal S, Rebeles J, Chen HI, Chang YF, Panneerdoss S, Zoghi B, Buddavarapu KC, Broaddus R, Hornsby P, Tomlinson G, Dome J, Vadlamudi RK, et al. Genomic loss of tumor suppressor miRNA-204 promotes cancer cell migration and invasion by activating AKT/mTOR/Rac1 signaling and actin reorganization. PloS one. 2012; 7:e52397.
16. Sacconi A, Biagioni F, Canu V, Mori F, Di Benedetto A, Lorenzon L, Ercolani C, Di Agostino S, Cambria AM, Germoni S, Grasso G, Blandino R, Panebianco V, Ziparo V, Federici O, Muti P, et al. miR-204 targets Bcl-2 expression and enhances responsiveness of gastric cancer. Cell death & disease. 2012; 3:e423.
17. Yin Y, Zhang B, Wang W, Fei B, Quan C, Zhang J, Song M, Bian Z, Wang Q, Ni S, Hu Y, Mao Y, Zhou L, Wang Y, Yu J, Du X, et al. miR-204-5p inhibits proliferation and invasion and enhances chemotherapeutic sensitivity of colorectal cancer cells by downregulating RAB22A. Clinical cancer research: an official journal of the American Association for Cancer Research. 2014; 20:6187-6199.
18. Liu L, Wang J, Li X, Ma J, Shi C, Zhu H, Xi Q, Zhang J, Zhao X and Gu M. MiR-204-5p suppresses cell proliferation by inhibiting IGFBP5 in papillary thyroid carcinoma. Biochemical and biophysical research communications. 2015; 457:621-626.
19. Shi L, Zhang B, Sun X, Lu S, Liu Z, Liu Y, Li H, Wang L, Wang X and Zhao C. MiR-204 inhibits human NSCLC metastasis through suppression of NUAK1. British journal of cancer. 2014; 111:2316-2327.
20. Ying Z, Li Y, Wu J, Zhu X, Yang Y, Tian H, Li W, Hu B, Cheng SY and Li M. Loss of miR-204 expression enhances glioma migration and stem cell-like phenotype. Cancer research. 2013; 73:990-999.
21. 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.
22. Mineva ND, Paulson KE, Naber SP, Yee AS and Sonenshein GE. Epigallocatechin-3-gallate inhibits stemlike inflammatory breast cancer cells. PloS one. 2013; 8:e73464.
23. Li YJ, Wu SL, Lu SM, Chen F, Guo Y, Gan SM, Shi YL, Liu S and Li SL. (-)-Epigallocatechin-3-gallate inhibits nasopharyngeal cancer stem cell self-renewal and migration and reverses the epithelial-mesenchymal transition via NF-kappaB p65 inactivation. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine. 2015; 36:2747-2761.
24. Wang H, Bian S and Yang CS. Green tea polyphenol EGCG suppresses lung cancer cell growth through upregulating miR-210 expression caused by stabilizing HIF-1alpha. Carcinogenesis. 2011; 32:1881-1889.
25. Rybicka A, Mucha J, Majchrzak K, Taciak B, Hellmen E, Motyl T and Krol M. Analysis of microRNA expression in canine mammary cancer stem-like cells indicates epigenetic regulation of transforming growth factor-beta signaling. Journal of physiology and pharmacology: an official journal of the Polish Physiological Society. 2015; 66:29-37.
26. 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. doi: 10.18632/oncotarget.3052.
27. Liu T, Hu K, Zhao Z, Chen G, Ou X, Zhang H, Zhang X, Wei X, Wang D, Cui M and Liu C. MicroRNA-1 downregulates proliferation and migration of breast cancer stem cells by inhibiting the Wnt/beta-catenin pathway. Oncotarget. 2015. doi: 10.18632/oncotarget.5873.
28. Ye X and Weinberg RA. Epithelial-Mesenchymal Plasticity: A Central Regulator of Cancer Progression. Trends in cell biology. 2015.
29. Parvani JG and Schiemann WP. Sox4, EMT programs, and the metastatic progression of breast cancers: mastering the masters of EMT. Breast cancer research: BCR. 2013; 15:R72.
30. Zhang J, Liang Q, Lei Y, Yao M, Li L, Gao X, Feng J, Zhang Y, Gao H, Liu DX, Lu J and Huang B. SOX4 induces epithelial-mesenchymal transition and contributes to breast cancer progression. Cancer research. 2012; 72:4597-4608.
31. Tiwari N, Tiwari VK, Waldmeier L, Balwierz PJ, Arnold P, Pachkov M, Meyer-Schaller N, Schubeler D, van Nimwegen E and Christofori G. Sox4 is a master regulator of epithelial-mesenchymal transition by controlling Ezh2 expression and epigenetic reprogramming. Cancer cell. 2013; 23:768-783.
32. Nieto MA. The snail superfamily of zinc-finger transcription factors. Nature reviews Molecular cell biology. 2002; 3:155-166.
33. Zheng M, Jiang YP, Chen W, Li KD, Liu X, Gao SY, Feng H, Wang SS, Jiang J, Ma XR, Cen X, Tang YJ, Chen Y, et al. Snail and Slug collaborate on EMT and tumor metastasis through miR-101-mediated EZH2 axis in oral tongue squamous cell carcinoma. Oncotarget. 2015; 6:6797-6810. doi: 10.18632/oncotarget.3180.
34. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, Itzkovitz S, Noske A, Zurrer-Hardi U, Bell G, Tam WL, Mani SA, van Oudenaarden A and Weinberg RA. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell. 2012; 148:1015-1028.
35. Luanpitpong S, Li J, Manke A, Brundage K, Ellis E, McLaughlin SL, Angsutararux P, Chanthra N, Voronkova M, Chen YC, Wang L, Chanvorachote P, Pei M, Issaragrisil S and Rojanasakul Y. SLUG is required for SOX9 stabilization and functions to promote cancer stem cells and metastasis in human lung carcinoma. Oncogene. 2015.
36. Wubetu GY, Shimada M, Morine Y, Ikemoto T, Ishikawa D, Iwahashi S, Yamada S, Saito Y, Arakawa Y and Imura S. Epigallocatechin gallate hinders human hepatoma and colon cancer sphere formation. Journal of gastroenterology and hepatology. 2015.
37. Singh A and Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010; 29:4741-4751.
38. 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.
39. 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.
40. 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. The Journal of pathology. 2011; 223:482-495.
41. Ebert MS, Neilson JR and Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nature methods. 2007; 4:721-726.