EBV-miR-BART7-3p promotes the EMT and metastasis of nasopharyngeal carcinoma cells by suppressing the tumor suppressor PTEN

Oncogene

Volumn 34, Issue 17, 2015, Pages 2156-2166

  Cai, L M ^a   Lyu, X M ^a,b   Luo, W R ^a   Cui, X F ^c   Ye, Y F ^a   Yuan, C C ^a   Peng, Q X ^a   Wu, D H ^a   Liu, T F ^a   Wang, E ^d   Marincola, F M ^d   Yao, K T ^a   Fang, W Y ^a   Cai, H B ^a   Li, X ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b THE THIRD AFFILIATED HOSPITAL OF SOUTHERN MEDICAL UNIVERSITY   (China)

^c Department of ENT   (China)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PTEN PROTEIN, HUMAN; RNA; VIRUS RNA;

BIOSYNTHESIS; CELL LINE; CELL NUCLEUS; EPITHELIAL MESENCHYMAL TRANSITION; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; FEMALE; GENETICS; HUMAN; METABOLISM; METASTASIS; NASOPHARYNX TUMOR; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR INVASION; VIROLOGY;

CELL LINE; CELL NUCLEUS; EPITHELIAL-MESENCHYMAL TRANSITION; EPSTEIN-BARR VIRUS INFECTIONS; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HERPESVIRUS 4, HUMAN; HUMANS; NASOPHARYNGEAL NEOPLASMS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RNA, NEOPLASM; RNA, VIRAL; SIGNAL TRANSDUCTION;

EID: 84933499288     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.341     Document Type: Article

References (63)

1. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
2. Brabletz T. EMT and MET in metastasis: where are the cancer stem cells? Cancer Cell 2012; 22: 699-701.
3. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 2014; 15: 178-196.
4. Talbot LJ, Bhattacharya SD, Kuo PC. Epithelial-mesenchymal transition, the tumor microenvironment, and metastatic behavior of epithelial malignancies. Int J Biochem Mol Biol 2012; 3: 117-136.
5. Villarejo A, Cortes-Cabrera A, Molina-Ortiz P, Portillo F, Cano A. Differential role of Snail1 and Snail2 zinc fingers in E-cadherin repression and epithelial to mesenchymal transition. J Biol Chem 2013; 289: 930-941.
6. Lim SO, Gu JM, Kim MS, Kim HS, Park YN, Park CK et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology 2008; 135: 2128-2140, 2140-2141.
7. Zhang J, Ma L. MicroRNA control of epithelial-mesenchymal transition and metastasis. Cancer Metastasis Rev 2012; 31: 653-662.
8. Zhang JP, Zeng C, Xu L, Gong J, Fang JH, Zhuang SM. MicroRNA-148a suppresses the epithelial-mesenchymal transition and metastasis of hepatoma cells by targeting Met/Snail signaling. Oncogene 2013; 33: 4069-4076.
9. Johansson J, Berg T, Kurzejamska E, Pang MF, Tabor V, Jansson M et al. MiR-155-mediated loss of C/EBPbeta shifts the TGF-beta response from growth inhibition to epithelial-mesenchymal transition, invasion and metastasis in breast cancer. Oncogene 2013; 32: 5614-5624.
10. Formosa A, Markert EK, Lena AM, Italiano D, Finazzi-Agro' E, Levine AJ et al. MicroRNAs, miR-154, miR-299-5p, miR-376a, miR-376c, miR-377, miR-381, miR-487b, miR-485-3p, miR-495 and miR-654-3p, mapped to the 14q32.31 locus, regulate proliferation, apoptosis, migration and invasion in metastatic prostate cancer cells. Oncogene 2014; 33: 5173-5182.
11. Zhang G, Zhou H, Xiao H, Liu Z, Tian H, Zhou T. MicroRNA-92a functions as an oncogene in colorectal cancer by targeting PTEN. Dig Dis Sci 2014; 59: 98-107.
12. Chen D, Zhang Y, Wang J, Chen J, Yang C, Cai K et al. MicroRNA-200c overexpression inhibits tumorigenicity and metastasis of CD117+CD44+ ovarian cancer stem cells by regulating epithelial-mesenchymal transition. J Ovarian Res 2013; 6: 50.
13. Cao M, Seike M, Soeno C, Mizutani H, Kitamura K, Minegishi Y et al. MiR-23a regulates TGF-beta-induced epithelial-mesenchymal transition by targeting E-cadherin in lung cancer cells. Int J Oncol 2012; 41: 869-875.
14. Colangelo T, Fucci A, Votino C, Sabatino L, Pancione M, Laudanna C et al. MicroRNA-130b promotes tumor development and is associated with poor prognosis in colorectal cancer. Neoplasia 2013; 15: 1218-1231.
15. Kumarswamy R, Mudduluru G, Ceppi P, Muppala S, Kozlowski M, Niklinski J et al. MicroRNA-30a inhibits epithelial-to-mesenchymal transition by targeting Snai1 and is downregulated in non-small cell lung cancer. Int J Cancer 2012; 130: 2044-2053.
16. Ke Y, Zhao W, Xiong J, Cao R. miR-149 inhibits non-small-cell lung cancer cells EMT by targeting FOXM1. Biochem Res Int 2013; 2013: 506731.
17. Lyu X, Fang W, Cai L, Zheng H, Ye Y, Zhang L et al. TGFbetaR2 is a major target of miR-93 in nasopharyngeal carcinoma aggressiveness. Mol Cancer 2014; 13: 51.
18. Luo Z, Zhang L, Li Z, Jiang C, Dai Y, Liu X et al. miR-149 promotes epithelial-mesenchymal transition and invasion in nasopharyngeal carcinoma cells. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2011; 36: 604-609.
19. Luo Z, Dai Y, Zhang L, Jiang C, Li Z, Yang J et al. miR-18a promotes malignant progression by impairing microRNA biogenesis in nasopharyngeal carcinoma. Carcinogenesis 2013; 34: 415-425.
20. Zur HH. Viruses in human cancers. Science 1991; 254: 1167-1173.
21. McLaughlin-Drubin ME, Munger K. Viruses associated with human cancer. Biochim Biophys Acta 2008; 1782: 127-150.
22. Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer 2006; 118: 3030-3044.
23. Kim DN, Chae HS, Oh ST, Kang JH, Park CH, Park WS et al. Expression of viral microRNAs in Epstein-Barr virus-associated gastric carcinoma. J Virol 2007; 81: 1033-1036.
24. Ramakrishnan R, Donahue H, Garcia D, Tan J, Shimizu N, Rice AP et al. Epstein-Barr virus BART9 miRNA modulates LMP1 levels and affects growth rate of nasal NK T cell lymphomas. PLoS One 2011; 6: e27271.
25. Yang HJ, Huang TJ, Yang CF, Peng LX, Liu RY, Yang GD et al. Comprehensive pro filing of Epstein-Barr virus-encoded miRNA species associated with specific latency types in tumor cells. Virol J 2013; 10: 314.
26. Lei T, Yuen KS, Xu R, Tsao SW, Chen H, Li M et al. Targeting of DICE1 tumor suppressor by Epstein-Barr virus-encoded miR-BART3∗microRNA in nasopharyngeal carcinoma. Int J Cancer 2013; 133: 79-87.
27. Lo AK, Dawson CW, Jin DY, Lo KW. The pathological roles of BART miRNAs in nasopharyngeal carcinoma. J Pathol 2012; 227: 392-403.
28. Barth S, Pfuhl T, Mamiani A, Ehses C, Roemer K, Kremmer E et al. Epstein-Barr virus-encoded microRNA miR-BART2 down-regulates the viral DNA polymerase BALF5. Nucleic Acids Res 2008; 36: 666-675.
29. Lo AK, To KF, Lo KW, Lung RW, Hui JW, Liao G et al. Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc Natl Acad Sci USA 2007; 104: 16164-16169.
30. Lung RW, Tong JH, Sung YM, Leung PS, Ng DC, Chau SL et al. Modulation of LMP2A expression by a newly identified Epstein-Barr virus-encoded microRNA miR-BART22. Neoplasia 2009; 11: 1174-1184.
31. Choy EY, Siu KL, Kok KH, Lung RW, Tsang CM, To KF et al. An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J Exp Med 2008; 205: 2551-2560.
32. Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 2009; 5: 376-385.
33. Chan JY, Gao W, Ho WK, Wei WI, Wong TS. Overexpression of Epstein-Barr virus-encoded microRNA-BART7 in undifferentiated nasopharyngeal carcinoma. Anticancer Res 2012; 32: 3201-3210.
34. Choi H, Lee H, Kim SR, Gho YS, Lee SK. Epstein-Barr virus-encoded microRNA BART15-3p promotes cell apoptosis partially by targeting BRUCE. J Virol 2013; 87: 8135-8144.
35. Ye Y, Zhou Y, Zhang L, Chen Y, Lyu X, Cai L et al. EBV-miR-BART1 is involved in regulating metabolism-associated genes in nasopharyngeal carcinoma. Biochem Biophys Res Commun 2013; 436: 19-24.
36. Wong AM, Kong KL, Tsang JW, Kwong DL, Guan XY. Profi ling of Epstein-Barr virus-encoded microRNAs in nasopharyngeal carcinoma reveals potential biomarkers and oncomirs. Cancer 2012; 118: 698-710.
37. Zheng H, Li W, Wang Y, Liu Z, Cai Y, Xie T et al. Glycogen synthase kinase-3 beta regulates Snail and beta-catenin expression during Fas-induced epithelial-mesenchymal transition in gastrointestinal cancer. Eur J Cancer 2013; 49: 2734-2746.
38. Qiu J, Cosmopoulos K, Pegtel M, Hopmans E, Murray P, Middeldorp J et al. A novel persistence associated EBV miRNA expression profile is disrupted in neoplasia. PLoS Pathog 2011; 7: e1002193.
39. Cai X, Schafer A, Lu S, Bilello JP, Desrosiers RC, Edwards R et al. Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog 2006; 2: e23.
40. Dawson CW, Tramountanis G, Eliopoulos AG, Young LS. Epstein-Barr virus latent membrane protein 1 (LMP1) activates the phosphatidylinositol 3-kinase/Akt pathway to promote cell survival and induce actin filament remodeling. J Biol Chem 2003; 278: 3694-3704.
41. Portis T, Longnecker R. Epstein-Barr virus (EBV) LMP2A mediates B-lymphocyte survival through constitutive activation of the Ras/PI3K/Akt pathway. Oncogene 2004; 23: 8619-8628.
42. Pan YR, Vatsyayan J, Chang YS, Chang HY. Epstein-Barr virus latent membrane protein 2A upregulates UDP-glucose dehydrogenase gene expression via ERK and PI3K/Akt pathway. Cell Microbiol 2008; 10: 2447-2460.
43. Iwakiri D, Sheen TS, Chen JY, Huang DP, Takada K. Epstein-Barr virus-encoded small RNA induces insulin-like growth factor 1 and supports growth of nasopharyngeal carcinoma-derived cell lines. Oncogene 2005; 24: 1767-1773.
44. Ikeda A, Caldwell RG, Longnecker R, Ikeda M. Itchy, a Nedd4 ubiquitin ligase, downregulates latent membrane protein 2A activity in B-cell signaling. J Virol 2003; 77: 5529-5534.
45. Song LB, Li J, Liao WT, Feng Y, Yu CP, Hu LJ et al. The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells. J Clin Invest 2009; 119: 3626-3636.
46. Pagano JS. Epstein-Barr virus: the first human tumor virus and its role in cancer. Proc Assoc Am Physicians 1999; 111: 573-580.
47. Chen SJ, Chen GH, Chen YH, Liu CY, Chang KP, Chang YS et al. Characterization of Epstein-Barr virus miRNAome in nasopharyngeal carcinoma by deep sequencing. PLoS ONE 2010; 5: e12745.
48. Hsu CY, Yi YH, Chang KP, Chang YS, Chen SJ, Chen HC. The Epstein-Barr virus-encoded microRNA MiR-BART9 promotes tumor metastasis by targeting E-cadherin in nasopharyngeal carcinoma. PLoS Pathog 2014; 10: e1003974.
49. Qu C, Liang Z, Huang J, Zhao R, Su C, Wang S et al. MiR-205 determines the radioresistance of human nasopharyngeal carcinoma by directly targeting PTEN. Cell Cycle 2012; 11: 785-796.
50. Chen P, Guo X, Zhou H, Zhang W, Zeng Z, Liao Q et al. SPLUNC1 regulates cell progression and apoptosis through the miR-141-PTEN/p27 pathway, but is hindered by LMP1. PLoS ONE 2013; 8: e56929.
51. Zhang LY, Ho-Fun LV, Wong AM, Kwong DL, Zhu YH, Dong SS et al. MicroRNA-144 promotes cell proliferation, migration and invasion in nasopharyngeal carcinoma through repression of PTEN. Carcinogenesis 2013; 34: 454-463.
52. Wang X, Jiang X. Post-translational regulation of PTEN. Oncogene 2008; 27: 5454-5463.
53. Song MS, Salmena L, Pandolfi PP. The functions and regulation of the PTEN tumour suppressor. Nat Rev Mol Cell Biol 2012; 13: 283-296.
54. Ho FC, Tham IW, Earnest A, Lee KM, Lu JJ. Patterns of regional lymph node metastasis of nasopharyngeal carcinoma: a meta-analysis of clinical evidence. Bmc Cancer 2012; 12: 98.
55. Larue L, Bellacosa A. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3' kinase/AKT pathways. Oncogene 2005; 24: 7443-7454.
56. Ding VW, Chen RH, McCormick F. Differential regulation of glycogen synthase kinase 3beta by insulin and Wnt signaling. J Biol Chem 2000; 275: 32475-32481.
57. Ho MY, Tang SJ, Chuang MJ, Cha TL, Li JY, Sun GH et al. TNF-alpha induces epithelial-mesenchymal transition of renal cell carcinoma cells via a GSK3beta-dependent mechanism. Mol Cancer Res 2012; 10: 1109-1119.
58. Mishra P, Senthivinayagam S, Rana A, Rana B. Glycogen Synthase Kinase-3beta regulates Snail and beta-catenin during gastrin-induced migration of gastric cancer cells. J Mol Signal 2010; 5: 9.
59. Liu H, Xu L, He H, Zhu Y, Liu J, Wang S et al. Hepatitis B virus X protein promotes hepatoma cell invasion and metastasis by stabilizing Snail protein. Cancer Sci 2012; 103: 2072-2081.
60. Rosano L, Spinella F, Di Castro V, Nicotra MR, Dedhar S, de Herreros AG et al. Endothelin-1 promotes epithelial-to-mesenchymal transition in human ovarian cancer cells. Cancer Res 2005; 65: 11649-11657.
61. Jorda M, Olmeda D, Vinyals A, Valero E, Cubillo E, Llorens A et al. Upregulation of MMP-9 in MDCK epithelial cell line in response to expression of the Snail transcription factor. J Cell Sci 2005; 118: 3371-3385.
62. Dave N, Guaita-Esteruelas S, Gutarra S, Frias A, Beltran M, Peiro S et al. Functional cooperation between Snail1 and twist in the regulation of ZEB1 expression during epithelial to mesenchymal transition. J Biol Chem 2011; 286: 12024-12032.
63. Min H, Hong M, Ma J, Zhang E, Zheng Q, Zhang J et al. A new staging system for nasopharyngeal carcinoma in China. Int J Radiat Oncol Biol Phys 1994; 30: 1037-1042.