Epstein-Barr Virus_Encoded LMP1 Upregulates MicroRNA-21 to Promote the Resistance of Nasopharyngeal Carcinoma Cells to Cisplatin-Induced Apoptosis by Suppressing PDCD4 and Fas-L

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Yang, Guang Da ^a   Huang, Tie Jun ^c   Peng, Li Xia ^a   Yang, Chang Fu ^b   Liu, Ran Yi ^a   Huang, Hong Bing ^a   Chu, Qiao Qiao ^d   Yang, Hong Jie ^a   Huang, Jia Ling ^e   Zhu, Zhen Yu ^b   Qian, Chao Nan ^a   Huang, Bi Jun ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c SECOND PEOPLE S HOSPITAL OF SHENZHEN   (China)

^d SUN YAT SEN UNIVERSITY   (China)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CISPLATIN; FAS LIGAND; LATENT MEMBRANE PROTEIN 1; MICRORNA 21; PHOSPHATIDYLINOSITOL 3 KINASE; PROAPOPTOTIC FACTORS PROGRAMMED CELL DEATH 4; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; FASLG PROTEIN, HUMAN; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, HUMAN; LUCIFERASE; MATRIX PROTEIN; MICRORNA; MIRN21 MICRORNA, HUMAN; PDCD4 PROTEIN, HUMAN; RNA BINDING PROTEIN; TETRAZOLIUM; THIAZOLE DERIVATIVE; THIAZOLYL BLUE;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CARCINOMA CELL; CELL PROLIFERATION; CHEMOSENSITIVITY; COLONY FORMATION; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GENE EXPRESSION; GENE SILENCING; GENETIC REGULATION; GENETIC TRANSFECTION; HUMAN; IC 50; NASOPHARYNX CARCINOMA; NONHUMAN; PROTEIN RNA BINDING; SIGNAL TRANSDUCTION; UPREGULATION; ANTAGONISTS AND INHIBITORS; CELL LINE; CFU COUNTING; DRUG EFFECTS; DRUG RESISTANCE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; IC50; METABOLISM; NASOPHARYNGEAL NEOPLASMS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY; WESTERN BLOTTING;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CELL LINE; CISPLATIN; COLONY-FORMING UNITS ASSAY; DRUG RESISTANCE, NEOPLASM; FAS LIGAND PROTEIN; FLUORESCENT ANTIBODY TECHNIQUE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INHIBITORY CONCENTRATION 50; LUCIFERASES; MICRORNAS; NASOPHARYNGEAL NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TETRAZOLIUM SALTS; THIAZOLES; VIRAL MATRIX PROTEINS;

EID: 84885995312     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078355     Document Type: Article

References (60)

1. Wei WI, Sham JS, (2005) Nasopharyngeal carcinoma. Lancet 365: 2041-2054. doi:10.1016/S0140-6736(05)66698-6. PubMed: 15950718.
2. Cao SM, Simons MJ, Qian CN, (2011) The prevalence and prevention of nasopharyngeal carcinoma in China. Chin J Cancer 30: 114-119. doi:10.5732/cjc.010.10377. PubMed: 21272443.
3. Langendijk JA, Leemans CR, Buter J, Berkhof J, Slotman BJ, (2004) The additional value of chemotherapy to radiotherapy in locally advanced nasopharyngeal carcinoma: a meta-analysis of the published literature. J Clin Oncol 22: 4604-4612. doi:10.1200/JCO.2004.10.074. PubMed: 15542811.
4. Jin Y, Cai XY, Shi YX, Xia XY, Cai YC, et al. (2012) Comparison of five cisplatin-based regimens frequently used as the first-line protocols in metastatic nasopharyngeal carcinoma. J Cancer Res Clin Oncol 138: 1717-1725. doi:10.1007/s00432-012-1219-x. PubMed: 22684794.
5. Chan AT, Lo YM, Zee B, Chan LY, Ma BB, et al. (2002) Plasma Epstein-Barr virus DNA and residual disease after radiotherapy for undifferentiated nasopharyngeal carcinoma. J Natl Cancer Inst 94: 1614-1619. doi:10.1093/jnci/94.21.1614. PubMed: 12419787.
6. Lin JC, Wang WY, Chen KY, Wei YH, Liang WM, et al. (2004) Quantification of plasma Epstein-Barr virus DNA in patients with advanced nasopharyngeal carcinoma. N Engl J Med 350: 2461-2470. doi:10.1056/NEJMoa032260. PubMed: 15190138.
7. Pathmanathan R, Prasad U, Sadler R, Flynn K, Raab-Traub N, (1995) Clonal proliferations of cells infected with Epstein-Barr virus in preinvasive lesions related to nasopharyngeal carcinoma. N Engl J Med 333: 693-698. doi:10.1056/NEJM199509143331103. PubMed: 7637746.
8. Speck SH, Ganem D, (2010) Viral latency and its regulation: lessons from the gamma-herpesviruses. Cell Host Microbe 8: 100-115. doi:10.1016/j.chom.2010.06.014. PubMed: 20638646.
9. Dawson CW, Port RJ, Young LS, (2012) The role of the EBV-encoded latent membrane proteins LMP1 and LMP2 in the pathogenesis of nasopharyngeal carcinoma (NPC). Semin Cancer Biol 22: 144-153. doi:10.1016/j.semcancer.2012.01.004. PubMed: 22249143.
10. Li L, Li W, Xiao L, Xu J, Chen X, et al. (2012) Viral oncoprotein LMP1 disrupts p53-induced cell cycle arrest and apoptosis through modulating K63-linked ubiquitination of p53. Cell Cycle 11: 2327-2336. doi:10.4161/cc.20771. PubMed: 22684299.
11. Choy EY, Siu KL, Kok KH, Lung RW, Tsang CM, et al. (2008) An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J Exp Med 205: 2551-2560. doi:10.1084/jem.20072581. PubMed: 18838543.
12. Kim YS, Park GB, Lee HK, Song H, Choi IH, et al. (2008) Cross-linking of B7-H1 on EBV-transformed B cells induces apoptosis through reactive oxygen species production, JNK signaling activation, and fasL expression. J Immunol 181: 6158-6169. PubMed: 18941206.
13. Tsuruo T, Naito M, Tomida A, Fujita N, Mashima T, et al. (2003) Molecular targeting therapy of cancer: drug resistance, apoptosis and survival signal. Cancer Sci 94: 15-21. doi:10.1111/j.1349-7006.2003.tb01345.x. PubMed: 12708468.
14. Fu X, Han Y, Wu Y, Zhu X, Lu X, et al. (2011) Prognostic role of microRNA-21 in various carcinomas: a systematic review and meta-analysis. Eur J Clin Invest 41: 1245-1253. doi:10.1111/j.1365-2362.2011.02535.x. PubMed: 21521185.
15. Wang HY, Sun BY, Zhu ZH, Chang ET, To KF, et al. (2011) Eight-signature classifier for prediction of nasopharyngeal [corrected] carcinoma survival. J Clin Oncol 29: 4516-4525. doi:10.1200/JCO.2010.33.7741. PubMed: 22025164.
16. Chen J, Hu CF, Hou JH, Shao Q, Yan LX, et al. (2010) Epstein-Barr virus encoded latent membrane protein 1 regulates mTOR signaling pathway genes which predict poor prognosis of nasopharyngeal carcinoma. J Transl Med 8: 30. doi:10.1186/1479-5876-8-30. PubMed: 20338061.
17. Mosialos G, Birkenbach M, Yalamanchili R, VanArsdale T, Ware C, et al. (1995) The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell 80: 389-399. doi:10.1016/0092-8674(95)90489-1. PubMed: 7859281.
18. Zhao Y, Wang Y, Zeng S, Hu X, (2012) LMP1 expression is positively associated with metastasis of nasopharyngeal carcinoma: evidence from a meta-analysis. J Clin Pathol 65: 41-45. doi:10.1136/jclinpath-2011-200198. PubMed: 22039283.
19. Kondo S, Wakisaka N, Muramatsu M, Zen Y, Endo K, et al. (2011) Epstein-Barr virus latent membrane protein 1 induces cancer stem/progenitor-like cells in nasopharyngeal epithelial cell lines. J Virol 85: 11255-11264. doi:10.1128/JVI.00188-11. PubMed: 21849440.
20. Anastasiadou E, Boccellato F, Vincenti S, Rosato P, Bozzoni I, et al. (2010) Epstein-Barr virus encoded LMP1 downregulates TCL1 oncogene through miR-29b. Oncogene 29: 1316-1328. doi:10.1038/onc.2009.439. PubMed: 19966860.
21. Cameron JE, Yin Q, Fewell C, Lacey M, McBride J, et al. (2008) Epstein-Barr virus latent membrane protein 1 induces cellular MicroRNA miR-146a, a modulator of lymphocyte signaling pathways. J Virol 82: 1946-1958. doi:10.1128/JVI.02136-07. PubMed: 18057241.
22. Lu F, Weidmer A, Liu CG, Volinia S, Croce CM, et al. (2008) Epstein-Barr virus-induced miR-155 attenuates NF-kappaB signaling and stabilizes latent virus persistence. J Virol 82: 10436-10443. doi:10.1128/JVI.00752-08. PubMed: 18753206.
23. Yu H, Lu J, Zuo L, Yan Q, Yu Z, et al. (2012) Epstein-Barr virus downregulates microRNA 203 through the oncoprotein latent membrane protein 1: a contribution to increased tumor incidence in epithelial cells. J Virol 86: 3088-3099. doi:10.1128/JVI.05901-11. PubMed: 22205737.
24. Sotiropoulou G, Pampalakis G, Lianidou E, Mourelatos Z, (2009) Emerging roles of microRNAs as molecular switches in the integrated circuit of the cancer cell. RNA 15: 1443-1461. doi:10.1261/rna.1534709. PubMed: 19561119.
25. Rosato P, Anastasiadou E, Garg N, Lenze D, Boccellato F, et al. (2012) Differential regulation of miR-21 and miR-146a by Epstein-Barr virus-encoded EBNA2. Leukemia 26: 2343-2352. doi:10.1038/leu.2012.108. PubMed: 22614176.
26. Young LS, Rickinson AB, (2004) Epstein-Barr virus: 40 years on. Nat Rev 4: 757-768. doi:10.1038/nrc1452.
27. Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, et al. (2008) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27: 2128-2136. doi:10.1038/sj.onc.1210856. PubMed: 17968323.
28. Sayed D, He M, Hong C, Gao S, Rane S, et al. (2010) MicroRNA-21 is a downstream effector of AKT that mediates its antiapoptotic effects via suppression of Fas ligand. J Biol Chem 285: 20281-20290. doi:10.1074/jbc.M110.109207. PubMed: 20404348.
29. Zhang H, Ozaki I, Mizuta T, Hamajima H, Yasutake T, et al. (2006) Involvement of programmed cell death 4 in transforming growth factor-beta1-induced apoptosis in human hepatocellular carcinoma. Oncogene 25: 6101-6112. doi:10.1038/sj.onc.1209634. PubMed: 16682950.
30. Pan X, Wang ZX, Wang R, (2011) MicroRNA-21: a novel therapeutic target in human cancer. Cancer Biol Ther 10: 1224-1232. PubMed: 21139417.
31. Dubrovska A, Kim S, Salamone RJ, Walker JR, Maira SM, et al. (2009) The role of PTEN/Akt/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc Natl Acad Sci U S A 106: 268-273. doi:10.1073/pnas.0810956106. PubMed: 19116269.
32. Dawson CW, Tramountanis G, Eliopoulos AG, Young LS, (2003) 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 278: 3694-3704. doi:10.1074/jbc.M209840200. PubMed: 12446712.
33. Mainou BA, Everly DJ, Raab-Traub N, (2005) Epstein-Barr virus latent membrane protein 1 CTAR1 mediates rodent and human fibroblast transformation through activation of PI3K. Oncogene 24: 6917-6924. doi:10.1038/sj.onc.1208846. PubMed: 16007144.
34. Wang K, Li PF, (2010) Foxo3a regulates apoptosis by negatively targeting miR-21. J Biol Chem 285: 16958-16966. doi:10.1074/jbc.M109.093005. PubMed: 20371612.
35. Li JH, Shi W, Chia M, Sanchez-Sweatman O, Siatskas C, et al. (2003) Efficacy of targeted FasL in nasopharyngeal carcinoma. Mol Ther 8: 964-973. doi:10.1016/j.ymthe.2003.08.018. PubMed: 14664799.
36. Fang W, Li X, Jiang Q, Liu Z, Yang H, et al. (2008) Transcriptional patterns, biomarkers and pathways characterizing nasopharyngeal carcinoma of Southern China. J Transl Med 6: 32. doi:10.1186/1479-5876-6-32. PubMed: 18570662.
37. Cheung ST, Huang DP, Hui AB, Lo KW, Ko CW, et al. (1999) Nasopharyngeal carcinoma cell line (C666-1) consistently harbouring Epstein-Barr virus. Int J Cancer 83: 121-126. doi:10.1002/(SICI)1097-0215(19990924)83:1. PubMed: 10449618.
38. Tsao SW, Wang X, Liu Y, Cheung YC, Feng H, et al. (2002) Establishment of two immortalized nasopharyngeal epithelial cell lines using SV40 large T and HPV16E6/E7 viral oncogenes. Biochim Biophys Acta 1590: 150-158. doi:10.1016/S0167-4889(02)00208-2. PubMed: 12063178.
39. Sizhong Z, Xiukung G, Yi Z, (1983) Cytogenetic studies on an epithelial cell line derived from poorly differentiated nasopharyngeal carcinoma. Int J Cancer 31: 587-590. doi:10.1002/ijc.2910310509. PubMed: 6852976.
40. Glaser R, Zhang HY, Yao KT, Zhu HC, Wang FX, et al. (1989) Two epithelial tumor cell lines (HNE-1 and HONE-1) latently infected with Epstein-Barr virus that were derived from nasopharyngeal carcinomas. Proc Natl Acad Sci U S A 86: 9524-9528. doi:10.1073/pnas.86.23.9524. PubMed: 2556716.
41. Yang XY, Ren CP, Wang L, Li H, Jiang CJ, et al. (2005) Identification of differentially expressed genes in metastatic and non-metastatic nasopharyngeal carcinoma cells by suppression subtractive hybridization. Cell Oncol 27: 215-223. PubMed: 16308470.
42. Satoh T, Fukuda M, Sairenji T, (2002) Distinct patterns of mitogen-activated protein kinase phosphorylation and Epstein-Barr virus gene expression in Burkitt's lymphoma cell lines versus B lymphoblastoid cell lines. Virus Genes 25: 15-21. doi:10.1023/A:1020113906966. PubMed: 12206304.
43. Bourguignon LY, Spevak CC, Wong G, Xia W, Gilad E, (2009) Hyaluronan-CD44 interaction with protein kinase C(epsilon) promotes oncogenic signaling by the stem cell marker Nanog and the Production of microRNA-21, leading to down-regulation of the tumor suppressor protein PDCD4, anti-apoptosis, and chemotherapy resistance in breast tumor cells. J Biol Chem 284: 26533-26546. doi:10.1074/jbc.M109.027466. PubMed: 19633292.
44. Gong C, Yao Y, Wang Y, Liu B, Wu W, et al. (2011) Up-regulation of miR-21 mediates resistance to trastuzumab therapy for breast cancer. J Biol Chem 286: 19127-19137. doi:10.1074/jbc.M110.216887. PubMed: 21471222.
45. Zhang X, Wang X, Song X, Liu C, Shi Y, et al. (2010) Programmed cell death 4 enhances chemosensitivity of ovarian cancer cells by activating death receptor pathway in vitro and in vivo. Cancer Sci 101: 2163-2170. doi:10.1111/j.1349-7006.2010.01664.x. PubMed: 20735432.
46. Schneiderman D, Kim JM, Senterman M, Tsang BK, (1999) Sustained suppression of Fas ligand expression in cisplatin-resistant human ovarian surface epithelial cancer cells. Apoptosis 4: 271-281. doi:10.1023/A:1026456926754. PubMed: 14692397.
47. Hsu CL, Chang KP, Lin CY, Chang HK, Wang CH, et al. (2012) Plasma Epstein-Barr virus DNA concentration and clearance rate as novel prognostic factors for metastatic nasopharyngeal carcinoma. Head Neck 34: 1064-1070. doi:10.1002/hed.21890. PubMed: 22083949.
48. Riley KJ, Rabinowitz GS, Yario TA, Luna JM, Darnell RB, et al. (2012) EBV and human microRNAs co-target oncogenic and apoptotic viral and human genes during latency. EMBO J 31: 2207-2221. doi:10.1038/emboj.2012.63. PubMed: 22473208.
49. Cameron JE, Fewell C, Yin Q, McBride J, Wang X, et al. (2008) Epstein-Barr virus growth/latency III program alters cellular microRNA expression. Virology 382: 257-266. doi:10.1016/j.virol.2008.09.018. PubMed: 18950829.
50. Skalsky RL, Corcoran DL, Gottwein E, Frank CL, Kang D, et al. (2012) The viral and cellular microRNA targetome in lymphoblastoid cell lines. PLOS Pathog 8: e1002484. PubMed: 22291592.
51. Wei J, Gao W, Zhu CJ, Liu YQ, Mei Z, et al. (2011) Identification of plasma microRNA-21 as a biomarker for early detection and chemosensitivity of non-small cell lung cancer. Chin J Cancer 30: 407-414. doi:10.5732/cjc.010.10522. PubMed: 21627863.
52. Yang JY, Hung MC, (2009) A new fork for clinical application: targeting forkhead transcription factors in cancer. Clin Cancer Res 15: 752-757. doi:10.1158/1078-0432.CCR-08-0124. PubMed: 19188143.
53. Shou Z, Lin L, Liang J, Li JL, Chen HY, (2012) Expression and prognosis of FOXO3a and HIF-1alpha in nasopharyngeal carcinoma. J Cancer Res Clin Oncol 138: 585-593. doi:10.1007/s00432-011-1125-7. PubMed: 22209974.
54. Yang JY, Zong CS, Xia W, Yamaguchi H, Ding Q, et al. (2008) ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 10: 138-148. doi:10.1038/ncb1676. PubMed: 18204439.
55. Rebillard A, Tekpli X, Meurette O, Sergent O, LeMoigne-Muller G, et al. (2007) Cisplatin-induced apoptosis involves membrane fluidification via inhibition of NHE1 in human colon cancer cells. Cancer Res 67: 7865-7874. doi:10.1158/0008-5472.CAN-07-0353. PubMed: 17699793.
56. Lo AK, To KF, Lo KW, Lung RW, Hui JW, et al. (2007) Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc Natl Acad Sci U S A 104: 16164-16169. doi:10.1073/pnas.0702896104. PubMed: 17911266.
57. Le Clorennec C, Ouk TS, Youlyouz-Marfak I, Panteix S, Martin CC, et al. (2008) Molecular basis of cytotoxicity of Epstein-Barr virus (EBV) latent membrane protein 1 (LMP1) in EBV latency III B cells: LMP1 induces type II ligand-independent autoactivation of CD95/Fas with caspase 8-mediated apoptosis. J Virol 82: 6721-6733. doi:10.1128/JVI.02250-07. PubMed: 18448526.
58. Pratt ZL, Zhang J, Sugden B, (2012) The latent membrane protein 1 (LMP1) oncogene of Epstein-Barr virus can simultaneously induce and inhibit apoptosis in B cells. J Virol 86: 4380-4393. doi:10.1128/JVI.06966-11. PubMed: 22318153.
59. Chang PY, Wu ZZ, Sun NK, Chao CC, (2013) EBV-encoded LMP-1 sensitizes nasopharyngeal carcinoma cells to genotoxic drugs by down-regulating Cabin1 expression. J Cell Physiol. PubMed: 23939952.
60. Brocqueville G, Ndour PA, Ouk TS, Le Goff A, De Witte C, et al. (2013) LMP1-induced cell death may contribute to the emergency of its oncogenic property. PLOS ONE 8: e60743. PubMed: 23637765.