Silencing of miRNA-148a by hypermethylation activates the integrin-mediated signaling pathway in nasopharyngeal carcinoma

Oncotarget

Volumn 5, Issue 17, 2014, Pages 7610-7624

  Li, Hsin Pai ^a,b   Huang, Hsin Yi ^a   Lai, Yi Ru ^a   Huang, Jing Xuan ^a   Chang, Kai Ping ^c   Hsueh, Chuen ^a,c   Chang, Yu Sun ^a,b  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

DNA methylation; Integrin signaling pathway; Migration; miR 148a; Nasopharyngeal carcinoma

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; INTEGRIN; MICRORNA; MICRORNA 148A; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; UNCLASSIFIED DRUG; UPSTREAM STIMULATORY FACTOR 1; MIRN148 MICRORNA, HUMAN;

ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; GENE; GENE ACTIVATION; GENE ACTIVITY; GENE FUNCTION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTRACELLULAR SIGNALING; MIGRATION INHIBITION; NASOPHARYNX CARCINOMA; PROMOTER REGION; PROTEIN DNA BINDING; ROCK1 GENE; TUMOR BIOPSY; TUMOR SUPPRESSOR GENE; VAV2 GENE; WASL GENE; WESTERN BLOTTING; CELL MOTION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; NASOPHARYNX TUMOR; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

BLOTTING, WESTERN; CELL MOVEMENT; DNA METHYLATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, TUMOR SUPPRESSOR; HUMANS; IMMUNOHISTOCHEMISTRY; INTEGRINS; MICRORNAS; NASOPHARYNGEAL NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84907494467     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2282     Document Type: Article

References (49)

1. Baumforth KR, Young LS, Flavell KJ, Constandinou C and Murray PG. The Epstein-Barr virus and its association with human cancers. Mol Pathol. 1999; 52(6):307-322.
2. Tsai CL, Li HP, Lu YJ, Hsueh C, Liang Y, Chen CL, Tsao SW, Tse KP, Yu JS and Chang YS. Activation of DNA methyltransferase 1 by EBV LMP1 Involves c-Jun NH(2)-terminal kinase signaling. Cancer Res. 2006; 66(24):11668-11676.
3. Dawson CW, Port RJ and Young LS. The role of the EBV-encoded latent membrane proteins LMP1 and LMP2 in the pathogenesis of nasopharyngeal carcinoma (NPC). Seminars in cancer biology. 2012; 22(2):144-153.
4. Li HP and Chang YS. Epstein-Barr virus latent membrane protein 1: structure and functions. Journal of biomedical science. 2003; 10(5):490-504.
5. Tsai CL, Li HP, Lu YJ, Hsueh C, Liang Y, Chen CL, Tsao SW, Tse KP, Yu JS and Chang YS. Activation of DNA methyltransferase 1 by EBV LMP1 Involves c-Jun NH(2)-terminal kinase signaling. Cancer research. 2006; 66(24):11668-11676.
6. Wang T, Liu H, Chen Y, Liu W, Yu J and Wu G. Methylation associated inactivation of RASSF1A and its synergistic effect with activated K-Ras in nasopharyngeal carcinoma. J Exp Clin Cancer Res. 2009; 28:160.
7. Huang YC, Hung WC, Chen WT, Jiang WH, Yu HS and Chai CY. Effects of MEK and DNMT inhibitors on arsenic-treated human uroepithelial cells in relation to Cyclin-D1 and p16. Toxicology letters. 2011; 200(1-2):59-66.
8. Aprelikova O, Palla J, Hibler B, Yu X, Greer YE, Yi M, Stephens R, Maxwell GL, Jazaeri A, Risinger JI, Rubin JS and Niederhuber J. Silencing of miR-148a in cancer-associated fibroblasts results in WNT10B-mediated stimulation of tumor cell motility. Oncogene. 2013; 32(27):3246-3253.
9. Lopez-Serra P and Esteller M. DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene. 2012; 31(13):1609-1622.
10. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP and Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Molecular cell. 2007; 27(1):91-105.
11. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116(2):281-297.
12. Chen HC, Chen GH, Chen YH, Liao WL, Liu CY, Chang KP, Chang YS and Chen SJ. MicroRNA deregulation and pathway alterations in nasopharyngeal carcinoma. British journal of cancer. 2009; 100(6):1002-1011.
13. Suzuki H, Maruyama R, Yamamoto E and Kai M. Epigenetic alteration and microRNA dysregulation in cancer. Frontiers in genetics. 2013; 4:258.
14. Yi B, Piazza GA, Su X and Xi Y. MicroRNA and cancer chemoprevention. Cancer prevention research. 2013; 6(5):401-409.
15. Gailhouste L, Gomez-Santos L, Hagiwara K, Hatada I, Kitagawa N, Kawaharada K, Thirion M, Kosaka N, Takahashi RU, Shibata T, Miyajima A and Ochiya T. miR-148a plays a pivotal role in the liver by promoting the hepatospecific phenotype and suppressing the invasiveness of transformed cells. Hepatology. 2013; 58(3):1153-1165.
16. Liffers ST, Munding JB, Vogt M, Kuhlmann JD, Verdoodt B, Nambiar S, Maghnouj A, Mirmohammadsadegh A, Hahn SA and Tannapfel A. MicroRNA-148a is down-regulated in human pancreatic ductal adenocarcinomas and regulates cell survival by targeting CDC25B. Lab Invest. 2011; 91(10):1472-1479.
17. Zhu A, Xia J, Zuo J, Jin S, Zhou H, Yao L, Huang H and Han Z. MicroRNA-148a is silenced by hypermethylation and interacts with DNA methyltransferase 1 in gastric cancer. Med Oncol. 2012; 29(4):2701-2709.
18. Zhou X, Zhao F, Wang ZN, Song YX, Chang H, Chiang Y and Xu HM. Altered expression of miR-152 and miR-148a in ovarian cancer is related to cell proliferation. Oncol Rep. 2012; 27(2):447-454.
19. Xu Q, Jiang Y, Yin Y, Li Q, He J, Jing Y, Qi YT, Li W, Lu B, Peiper SS, Jiang BH and Liu LZ. A regulatory circuit of miR-148a/152 and DNMT1 in modulating cell transformation and tumor angiogenesis through IGF-IR and IRS1. J Mol Cell Biol. 2013; 5(1):3-13.
20. Chen Y, Min L, Zhang X, Hu S, Wang B, Liu W, Wang R, Gu X, Shen W, Lv H, Zou J, Xu X and Chen L. Decreased miRNA-148a is associated with lymph node metastasis and poor clinical outcomes and functions as a suppressor of tumor metastasis in non-small cell lung cancer. Oncol Rep. 2013; 30(4):1832-1840.
21. Zhang H, Li Y, Huang Q, Ren X, Hu H, Sheng H and Lai M. MiR-148a promotes apoptosis by targeting Bcl-2 in colorectal cancer. Cell Death Differ. 2011; 18(11):1702-1710.
22. Zhang H, Tsao SW, Jin C, Strombeck B, Yuen PW, Kwong YL and Jin Y. Sequential cytogenetic and molecular cytogenetic characterization of an SV40T-immortalized nasopharyngeal cell line transformed by Epstein-Barr virus latent membrane protein-1 gene. Cancer genetics and cytogenetics. 2004; 150(2):144-152.
23. Hanoun N, Delpu Y, Suriawinata AA, Bournet B, Bureau C, Selves J, Tsongalis GJ, Dufresne M, Buscail L, Cordelier P and Torrisani J. The silencing of microRNA 148a production by DNA hypermethylation is an early event in pancreatic carcinogenesis. Clin Chem. 2010; 56(7):1107-1118.
24. Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP and Lai EC. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome research. 2007; 17(12):1850-1864.
25. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136(2):215-233.
26. Guo W and Giancotti FG. Integrin signalling during tumour progression. Nature reviews Molecular cell biology. 2004; 5(10):816-826.
27. Jones PA and Baylin SB. The epigenomics of cancer. Cell. 2007; 128(4):683-692.
28. Ellis L, Atadja PW and Johnstone RW. Epigenetics in cancer: targeting chromatin modifications. Molecular cancer therapeutics. 2009; 8(6):1409-1420.
29. Chen Y, Song Y, Wang Z, Yue Z, Xu H, Xing C and Liu Z. Altered expression of MiR-148a and MiR-152 in gastrointestinal cancers and its clinical significance. J Gastrointest Surg. 2010; 14(7):1170-1179.
30. Li HP, Peng CC, Chung IC, Huang MY, Huang ST, Chen CC, Chang KP, Hsu CL and Chang YS. Aberrantly hypermethylated Homeobox A2 derepresses metalloproteinase-9 through TBP and promotes invasion in Nasopharyngeal carcinoma. Oncotarget. 2013; 4(11):2154-2165.
31. Zheng B, Liang L, Wang C, Huang S, Cao X, Zha R, Liu L, Jia D, Tian Q, Wu J, Ye Y, Wang Q, Long Z, Zhou Y, Du C, He X, et al. MicroRNA-148a suppresses tumor cell invasion and metastasis by downregulating ROCK1 in gastric cancer. Clin Cancer Res. 2011; 17(24):7574-7583.
32. Schwartz MA, Schaller MD and Ginsberg MH. Integrins: emerging paradigms of signal transduction. Annual review of cell and developmental biology. 1995; 11:549-599.
33. Giancotti FG and Ruoslahti E. Integrin signaling. Science. 1999; 285(5430):1028-1032.
34. Danen EH, van Rheenen J, Franken W, Huveneers S, Sonneveld P, Jalink K and Sonnenberg A. Integrins control motile strategy through a Rho-cofilin pathway. The Journal of cell biology. 2005; 169(3):515-526.
35. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT and Horwitz AF. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nature cell biology. 2004; 6(2):154-161.
36. Raftopoulou M and Hall A. Cell migration: Rho GTPases lead the way. Developmental biology. 2004; 265(1):23-32.
37. Chong IW, Chang MY, Chang HC, Yu YP, Sheu CC, Tsai JR, Hung JY, Chou SH, Tsai MS, Hwang JJ and Lin SR. Great potential of a panel of multiple hMTH1, SPD, ITGA11 and COL11A1 markers for diagnosis of patients with non-small cell lung cancer. Oncol Rep. 2006; 16(5):981-988.
38. Tchaicha JH, Reyes SB, Shin J, Hossain MG, Lang FF and McCarty JH. Glioblastoma angiogenesis and tumor cell invasiveness are differentially regulated by beta8 integrin. Cancer Res. 2011; 71(20):6371-6381.
39. Lai SY, Ziober AF, Lee MN, Cohen NA, Falls EM and Ziober BL. Activated Vav2 modulates cellular invasion through Rac1 and Cdc42 in oral squamous cell carcinoma. Oral Oncol. 2008; 44(7):683-688.
40. Patel V, Rosenfeldt HM, Lyons R, Servitja JM, Bustelo XR, Siroff M and Gutkind JS. Persistent activation of Rac1 in squamous carcinomas of the head and neck: evidence for an EGFR/Vav2 signaling axis involved in cell invasion. Carcinogenesis. 2007; 28(6):1145-1152.
41. Miki H, Sasaki T, Takai Y and Takenawa T. Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature. 1998; 391(6662):93-96.
42. Jin KM, Lu M, Liu FF, Gu J, Du XJ and Xing BC. N-WASP is highly expressed in hepatocellular carcinoma and associated with poor prognosis. Surgery. 2013; 153(4):518-525.
43. Li J, Song Y, Wang Y, Luo J and Yu W. MicroRNA-148a suppresses epithelial-to-mesenchymal transition by targeting ROCK1 in non-small cell lung cancer cells. Mol Cell Biochem. 2013; 380(1-2):277-282.
44. Graham FL, Smiley J, Russell WC and Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. The Journal of general virology. 1977; 36(1):59-74.
45. Huang DP, Ho JH, Poon YF, Chew EC, Saw D, Lui M, Li CL, Mak LS, Lai SH and Lau WH. Establishment of a cell line (NPC/HK1) from a differentiated squamous carcinoma of the nasopharynx. International journal of cancer. 1980; 26(2):127-132.
46. Cheung ST, Huang DP, Hui AB, Lo KW, Ko CW, Tsang YS, Wong N, Whitney BM and Lee JC. Nasopharyngeal carcinoma cell line (C666-1) consistently harbouring Epstein-Barr virus. International journal of cancer. 1999; 83(1):121-126.
47. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ and Guegler KJ. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic acids research. 2005; 33(20):e179.
48. Wang LJ, Hsu CW, Chen CC, Liang Y, Chen LC, Ojcius DM, Tsang NM, Hsueh C, Wu CC and Chang YS. Interactome-wide analysis identifies end-binding protein 1 as a crucial component for the speck-like particle formation of activated absence in melanoma 2 (AIM2) inflammasomes. Molecular & cellular proteomics: MCP. 2012; 11(11):1230-1244.
49. Chang YT, Wu CC, Shyr YM, Chen TC, Hwang TL, Yeh TS, Chang KP, Liu HP, Liu YL, Tsai MH, Chang YS and Yu JS. Secretome-based identification of ULBP2 as a novel serum marker for pancreatic cancer detection. PloS one. 2011; 6(5):e20029.