MicroRNA-211 enhances the oncogenicity of carcinogen-induced oral carcinoma by repressing TCF12 and increasing antioxidant activity

Cancer Research

Volumn 76, Issue 16, 2016, Pages 4872-4886

  Chen, Yi Fen ^a   Yang, Cheng Chieh ^a,b   Kao, Shou Yen ^a,b   Liu, Chung Ji ^a,c   Lin, Shu Chun ^a,b   Chang, Kuo Wei ^a,b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^c MACKAY MEMORIAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

4 NITROQUINOLINE 1 OXIDE; CARCINOGEN; MICRORNA; MICRORNA 211; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 12; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; MIRN211 MICRORNA, MOUSE; TCF12 PROTEIN, MOUSE;

ALGORITHM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BINDING SITE; CANCER TISSUE; CARCINOGENICITY; CARCINOMA CELL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; PHENOTYPE; PLASMID; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA CELL LINE; TISSUE MICROARRAY; TRANSGENIC MOUSE; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CARCINOGENESIS; CELL LINE; DISEASE MODEL; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; HEAD AND NECK TUMOR; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; MOUTH TUMOR; PATHOLOGY; SQUAMOUS CELL CARCINOMA; WESTERN BLOTTING; XENOGRAFT;

4-NITROQUINOLINE-1-OXIDE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; CARCINOGENESIS; CARCINOGENS; CARCINOMA, SQUAMOUS CELL; CELL LINE; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; MOUTH NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TISSUE ARRAY ANALYSIS;

EID: 84982165918     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-1664     Document Type: Article

References (50)

1. Liao CT, Wallace CG, Lee LY, Hsueh C, Lin CY, Fan KH, et al. Clinical evidence of field cancerization in patients with oral cavity cancer in a betel quid chewing area. Oral Oncol 2014;50:721-31.
2. Benson E, Li R, Eisele D, Fakhry C. The clinical impact of HPV tumor status upon head and neck squamous cell carcinomas. Oral Oncol 2014;50:565-74.
3. Li WC, Lee PL, Chou IC, Chang WJ, Lin SC, Chang KW. Molecular and cellular cues of diet-associated oral carcinogenesis-with an emphasis on areca-nut-induced oral cancer development. J Oral Pathol Med 2015;44:167-77.
4. Ganci F, Sacconi A, Manciocco V, Sperduti I, Battaglia P, Covello R, et al. microRNAs expression predicts local recurrence risk in oral squamous cell carcinoma. Head Neck 2016;38 Suppl 1:E189-97.
5. Leemans CR, Braakhuis BJ, Brakenhoff RH. The molecular biology of head and neck cancer. Nat Rev Cancer 2011;11:9-22.
6. Tu HF, Lin SC, Chang KW. MicroRNA aberrances in head and neck cancer: pathogenetic and clinical significance. Curr Opin Otolaryngol Head Neck Surg 2013;21:104-11.
7. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell 2012;148:1172-87.
8. Liu CJ, Shen WG, Peng SY, Cheng HW, Kao SY, Lin SC, et al. miR-134 induces oncogenicity and metastasis in head and neck carcinoma through targeting WWOX gene. Int J Cancer 2014;134:811-21.
9. Kinoshita T, Hanazawa T, Nohata N, Kikkawa N, Enokida H, Yoshino H, et al. Tumor suppressive microRNA-218 inhibits cancer cell migration and invasion through targeting laminin-332 in head and neck squamous cell carcinoma. Oncotarget 2012;3:1386-400.
10. Bourguignon LY, Earle C, Wong G, Spevak CC, Krueger K. Stem cell marker (Nanog) and Stat-3 signaling promote MicroRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cells. Oncogene 2012;31:149-60.
11. Liu CJ, Tsai MM, Hung PS, Kao SY, Liu TY, Wu KJ, et al. miR-31 ablates expression of the HIF regulatory factor FIH to activate the HIF pathway in head and neck carcinoma. Cancer Res 2010;70:1635-44.
12. Gao L, Wang X, Wang X, Zhang L, Qiang C, Chang S, et al. IGF-1R, a target of let-7b, mediates crosstalk between IRS-2/Akt and MAPK pathways to promote proliferation of oral squamous cell carcinoma. Oncotarget 2014;5:2562-74.
13. Tseng SH, Yang CC, Yu EH, Chang C, Lee YS, Liu CJ, et al. K14-EGFP-miR-31 transgenic mice have high susceptibilitytochemical-induced squamous cell tumorigenesis that is associating with Ku80 repression. Int J Cancer 2015;136:1263-75.
14. Chang KW, Liu CJ, Chu TH, Cheng HW, Hung PS, Hu WY, et al. Association between high miR-211 microRNA expression and the poor prognosis of oral carcinoma. J Dent Res 2008;87:1063-68.
15. Chu TH, Yang CC, Liu CJ, Lui MT, Lin SC, Chang KW. miR-211 promotes the progression of head and neck carcinomas by targeting TGFbetaRII. Cancer Lett 2013;337:115-24.
16. Cai C, Ashktorab H, Pang X, Zhao Y, Sha W, Liu Y, et al. MicroRNA-211 expression promotes colorectal cancer cell growth in vitro and in vivo by targeting tumor suppressor CHD5. PLoS One 2012;7:e29750.
17. Liu Q, Huang J, Zhou N, Zhang Z, Zhang A, Lu Z, et al. LncRNA loc285194 is a p53-regulated tumor suppressor. Nucleic Acids Res 2013;41:4976-87.
18. Chitnis NS, Pytel D, Bobrovnikova-Marjon E, Pant D, Zheng H, Maas NL, et al. miR-211 is a prosurvival microRNA that regulates chop expression in a PERK-dependent manner. Mol Cell 2012;48:353-64.
19. Margue C, Philippidou D, Reinsbach SE, Schmitt M, Behrmann I, Kreis S. Newtargetgenes of MITF-Induced microRNA-211 contributetomelanoma cell invasion. PLoS One 2013;8:e73473.
20. Mazar J, DeYoung K, Khaitan D, Meister E, Almodovar A, Goydos J, et al. The regulation of miRNA-211 expression and its role in melanoma cell invasiveness. PLoS One 2010;5:e13779.
21. Asuthkar S, Velpula KK, Chetty C, Gorantla B, Rao JS. Epigenetic regulation of miRNA-211 by MMP-9 governs glioma cell apoptosis, chemosensitivity and radiosensitivity. Oncotarget 2012;3:1439-54.
22. Lee CC, Chen WS, Chen CC, Chen LL, Lin YS, Fan CS, et al. TCF12 protein functions as transcriptional repressor of E-cadherin, and Its overexpression is correlated with metastasis of colorectal cancer. J Biol Chem 2011;287:2798-809.
23. Massari ME, Murre C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 2000;20:429-40.
24. Hu JS, Olson EN, Kingston RE. HEB, a helix-loop-helix protein related to E2A and ITF2 that can modulate the DNA-binding ability of myogenic regulatory factors. Mol Cell Biol 1992;12:1031-42.
25. Uittenbogaard M, Chiaramello A. Expression of the bHLH transcription factor Tcf12 (ME1) gene is linked to the expansion of precursor cell populations during neurogenesis. Brain Res Gene Expr Patterns 2002;1:115-21.
26. Zhao P, Hoffman EP. Embryonic myogenesis pathways in muscle regeneration. Dev Dyn 2004;229:380-92.
27. Quong MW, Romanow WJ, Murre C. E protein function in lymphocyte development. Annu Rev Immunol 2002;20:301-22.
28. Tanigawa Y, Yakura R, Komiya T. The bHLH transcription factor Tcf12 (ME1) mRNA is abundantly expressed in Paneth cells of mouse intestine. Gene Expr Patterns 2007;7:709-13.
29. Sharma VP, Fenwick AL, Brockop MS, McGowan SJ, Goos JA, Hoogeboom AJ, et al. Mutations in TCF12, encoding a basic helix-loop-helix partner of TWIST1, are a frequent cause of coronal craniosynostosis. Nat Genet 2013;45:304-7.
30. Broehm CJ, Wu J, Gullapalli RR, Bocklage T. Extraskeletal myxoid chondrosarcoma with at (9;16) (q22;p11.2) resulting in a NR4A3-FUS fusion. Cancer Genet 2014;207:276-80.
31. Adijanto J, Castorino JJ, Wang ZX, Maminishkis A, Grunwald GB, Philp NJ. Microphthalmia-associated transcription factor (MITF) promotes differentiation of human retinal pigment epithelium (RPE) by regulating microRNAs-204/211 expression. J Biol Chem 2012;287:20491-503.
32. Wang P, Cui J, Zhao C, Zhou L, Guo X, Shen R, et al. Differential expression of microRNAs in 2-cell and 4-cell mouse embryos. Zygote 2014;22:455-61.
33. Glasauer A, Chandel NS. Targeting antioxidants for cancer therapy. Biochem Pharmacol 2014;92:90-101.
34. Wang XJ, Sun Z, Villeneuve NF, Zhang S, Zhao F, Li Y, et al. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 2008;29:1235-43.
35. Chang CW, Chen YS, Chou SH, Han CL, Chen YJ, Yang CC, et al. Distinct subpopulations of head and neck cancer cells with different levels of intracellular reactive oxygen species exhibit diverse stemness, proliferation, and chemosensitivity. Cancer Res 2014;74:6291-305.
36. Cui H, Wang Y, Wang Y, Qin S. Genome-wide analysis of putative peroxiredoxin in unicellular and filamentous cyanobacteria. BMC Evol Biol 2012;12:220.
37. Rhee SG, Woo HA, Kil IS, Bae SH. Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides. J Biol Chem 2012;287:4403-10.
38. Yu Y, Zhang C, Zhou G, Wu S, Qu X, Wei H, et al. Gene expression profiling in human fetal liver and identification of tissue- and developmental-stage-specific genes through compiled expression profiles and efficient cloning of full-length cDNAs. Genome Res 2001;11:1392-403.
39. Xu Y, Morse LR, da Silva RA, Odgren PR, Sasaki H, Stashenko P, et al. PAMM: a redox regulatory protein that modulates osteoclast differentiation. Antioxid Redox Signal 2010;13:27-37.
40. Valverde G, Zhou H, Lippold S, de Filippo C, Tang K, Lopez Herraez D, et al. A novel candidate region for genetic adaptation to high altitude in andean populations. PLoS One 2015;10:e0125444.
41. Kao YY, Tu HF, Kao SY, Chang KW, Lin SC. The increase of oncogenic miRNA expressionintongue carcinogenesisofamouse model. Oral Oncol 2015;51:1103-12.
42. Nunoshiba T, Demple B. Potent intracellular oxidative stress exerted by the carcinogen 4-nitroquinoline-N-oxide. Cancer Res 1993;53:3250-2.
43. Hung PS, Tu HF, Kao SY, Yang CC, Liu CJ, Huang TY, et al. miR-31 is upregulated in oral premalignant epithelium and contributes to the immortalization of normal oral keratinocytes. Carcinogenesis 2014;35:1162-71.
44. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1:555-67.
45. Lu WC, Kao SY, Yang CC, Tu HF, Wu CH, Chang KW, et al. EGF up-regulates miR-31 through the C/EBPbeta signal cascade in oral carcinoma. PLoS One 2014;9:e108049.
46. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, et al. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res 2014;42(Database issue):D142-7.
47. Gao R, Wang L, Sun J, Nie K, Jian H, Gao L, et al. MiR-204 promotes apoptosis in oxidative stress-induced rat Schwann cells by suppressing neuritin expression. FEBS Lett 2014;588:3225-32.
48. Wang L, Yang H, Abel EV, Ney GM, Palmbos PL, Bednar F, et al. ATDC induces an invasive switch in KRAS-induced pancreatic tumorigenesis. Genes Dev 2015;29:171-83.
49. Ai L, Kim WJ, Alpay M, Tang M, Pardo CE, Hatakeyama S, et al. TRIM29 suppresses TWIST1 and invasive breast cancer behavior. Cancer Res 2014;74:4875-87.
50. Piskounova E, Agathocleous M, Murphy MM, Hu Z, Huddlestun SE, Zhao Z, et al. Oxidative stress inhibits distant metastasis by human melanoma cells. Nature 2015;527:186-91.