Implication of viral microRNAs in the genesis and diagnosis of Epstein‑Barr virus‑associated tumors (Review)
- Authors:
- Xiangning Zhang
- Yudong Ye
- Ming Fu
- Biying Zheng
- Qianhui Qiu
- Zunnan Huang
-
Affiliations: Department of Pathophysiology, Chinese‑American Collaborative Cancer Institute, Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Guangdong Medical University, Dongguan, Guangdong 523808, P.R. China, Department of Otolaryngology, Dongguan City People's Hospital, Dongguan, Guangdong 523059, P.R. China, Department of Clinical Microbiology, College of Laboratory Medicine, Guangdong Medical University, Dongguan, Guangdong 523808, P.R. China, Department of Otolaryngology, Pearl River Hospital, Southern Medical University, Guangzhou, Guangdong 510280, P.R. China - Published online on: August 5, 2019 https://doi.org/10.3892/ol.2019.10713
- Pages: 3433-3442
This article is mentioned in:
Abstract
Kutok JL and Wang F: Spectrum of Epstein Barr virus associated diseases. Annu Rev Pathol. 1:375–404. 2006. View Article : Google Scholar : PubMed/NCBI | |
Williams H and Crawford DH: Epstein-Barr virus: The impact of scientific advances on clinical practice. Blood. 107:862–869. 2006. View Article : Google Scholar : PubMed/NCBI | |
Lo KW, To KF and Huang DP: Focus on nasopharyngeal carcinoma. Cancer Cell. 5:423–428. 2004. View Article : Google Scholar : PubMed/NCBI | |
Cesarman E: Gammaherpesvirus and lymphoproliferative disorders in immunocompromised patients. Cancer Lett. 305:163–174. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hsieh JJ and Hayward SD: Masking of the CBF1/RBPJ kappa transcriptional repression domain by Epstein-Barr virus EBNA2. Science. 268:560–563. 1995. View Article : Google Scholar : PubMed/NCBI | |
Yoshizaki T, Kondo S, Wakisaka N, Murono S, Endo K, Sugimoto H, Nakanishi S, Tsuji A and Ito M: Pathogenic role of Epstein-Barr virus latent membrane protein-1 in the development of nasopharyngeal carcinoma. Cancer Lett. 337:1–7. 2013. View Article : Google Scholar : PubMed/NCBI | |
Guasparri I, Bubman D and Cesarman E: EBV LMP2A affects LMP1-mediated NF-kappaB signaling and survival of lymphoma cells by regulating TRAF2 expression. Blood. 111:3813–3820. 2008. View Article : Google Scholar : PubMed/NCBI | |
Marquitz AR, Mathur A, Edwards RH and Raab-Traub N: Host gene expression is regulated by two types of noncoding RNAs transcribed from the Epstein-Barr virus BamHI A rightward transcript region. J Virol. 89:11256–11268. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bartel DP: MicroRNAs: Target recognition and regulatory functions. Cell. 136:215–233. 2009. View Article : Google Scholar : PubMed/NCBI | |
Winter J, Jung S, Keller S, Gregory RI and Diederichs S: Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol. 11:228–234. 2009. View Article : Google Scholar : PubMed/NCBI | |
Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK, Sohn SY, Cho Y, Zhang BT and Kim VN: Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell. 125:887–901. 2006. View Article : Google Scholar : PubMed/NCBI | |
Busson P, Keryer C, Ooka T and Corbex M: EBV-associated nasopharyngeal carcinomas: From epidemiology to virus-targeting strategies. Trends Microbiol. 12:356–360. 2004. View Article : Google Scholar : PubMed/NCBI | |
Pfeffer S, Zavolan M, Grässer FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C and Tuschl T: Identification of virus-encoded microRNAs. Science. 304:734–736. 2004. View Article : Google Scholar : PubMed/NCBI | |
Zhu JY, Pfuhl T, Motsch N, Barth S, Nicholls J, Grässer F and Meister G: Identification of novel Epstein-Barr virus microRNA genes from nasopharyngeal carcinomas. J Virol. 83:3333–3341. 2009. View Article : Google Scholar : PubMed/NCBI | |
Edwards RH, Marquitz AR and Raab-Traub N: Epstein-Barr virus BART microRNAs are produced from a large intron prior to splicing. J Virol. 82:9094–9106. 2008. View Article : Google Scholar : PubMed/NCBI | |
Qiu J, Cosmopoulos K, Pegtel M, Hopmans E, Murray P, Middeldorp J, Shapiro M and Thorley-Lawson DA: A novel persistence associated EBV miRNA expression profile is disrupted in neoplasia. PLoS Pathog. 7:e10021932011. View Article : Google Scholar : PubMed/NCBI | |
Tsai CY, Liu YY, Liu KH, Hsu JT, Chen TC, Chiu CT and Yeh TS: Comprehensive profiling of virus microRNAs of Epstein-Barr virus-associated gastric carcinoma: Highlighting the interactions of ebv-Bart9 and host tumor cells. J Gastroenterol Hepatol. 32:82–91. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sakamoto K, Sekizuka T, Uehara T, Hishima T, Mine S, Fukumoto H, Sato Y, Hasegawa H, Kuroda M and Katano H: Next-generation sequencing of miRNAs in clinical samples of Epstein-Barr virus-associated B-cell lymphomas. Cancer Med. 6:605–618. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lo AKF, Dawson CW, Jin DY and Lo KW: The pathological roles of BART miRNAs in nasopharyngeal carcinoma. J Pathol. 227:392–403. 2012. View Article : Google Scholar : PubMed/NCBI | |
Baer R, Bankier AT, Biggin MD, Deininger PL, Farrell PJ, Gibson TJ, Hatfull G, Hudson GS, Satchwell SC, Séguin C, et al: DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature. 310:207–211. 1984. View Article : Google Scholar : PubMed/NCBI | |
Pratt ZL, Kuzembayeva M, Sengupta S and Sugden B: The microRNAs of Epstein-Barr Virus are expressed at dramatically differing levels among cell lines. Virology. 386:387–397. 2009. View Article : Google Scholar : PubMed/NCBI | |
Xia T, O'Hara A, Araujo I, Barreto J, Carvalho E, Sapucaia JB, Ramos JC, Luz E, Pedroso C, Manrique M, et al: EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Res. 68:1436–1442. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kim DN, Chae HS, Oh ST, Kang JH, Park CH, Park WS, Takada K, Lee JM, Lee WK and Lee SK: Expression of viral microRNAs in Epstein-Barr virus-associated gastric carcinoma. J Virol. 81:1033–1036. 2007. View Article : Google Scholar : PubMed/NCBI | |
Cosmopoulos K, Pegtel M, Hawkins J, Moffett H, Novina C, Middeldorp J and Thorley-Lawson DA: Comprehensive profiling of Epstein-Barr virus microRNAs in nasopharyngeal carcinoma. J Virol. 83:2357–2367. 2009. View Article : Google Scholar : PubMed/NCBI | |
Chen SJ, Chen GH, Chen YH, Liu CY, Chang KP, Chang YS and Chen HC: Characterization of Epstein-Barr virus miRNAome in nasopharyngeal carcinoma by deep sequencing. PLoS One. 5(pii): e127452010. View Article : Google Scholar : PubMed/NCBI | |
Motsch N, Alles J, Imig J, Zhu J, Barth S, Reineke T, Tinguely M, Cogliatti S, Dueck A, Meister G, et al: MicroRNA profiling of Epstein-Barr virus-associated NK/T-cell lymphomas by deep sequencing. PLoS One. 7:e421932012. View Article : Google Scholar : PubMed/NCBI | |
Jun SM, Hong YS, Seo JS, Ko YH, Yang CW and Lee SK: Viral microRNA profile in Epstein-Barr virus-associated peripheral T cell lymphoma. Brit J Haematol. 142:320–323. 2008. View Article : Google Scholar | |
Arikawa J, Tokunaga M, Tashiro Y, Tanaka S, Sato E, Haraguchi K, Yamamoto A, Toyohira O and Tsuchimochi A: Epstein-Barr virus-positive multiple early gastric cancers and dysplastic lesions: A case report. Pathol Int. 47:730–734. 1997. View Article : Google Scholar : PubMed/NCBI | |
Fukayama M: Epstein-Barr virus and gastric carcinoma. Pathol Int. 60:337–350. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wong AM, Kong KL, Tsang JW, Kwong DL and Guan XY: Profiling of Epstein-Barr virus-encoded microRNAs in nasopharyngeal carcinoma reveals potential biomarkers and oncomirs. Cancer. 118:698–710. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, et al: Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 33:e1792005. View Article : Google Scholar : PubMed/NCBI | |
Amoroso R, Fitzsimmons L, Thomas WA, Kelly GL, Rowe M and Bell AI: Quantitative studies of Epstein-Barr virus-encoded microRNAs provide novel insights into their regulation. J Virol. 85:996–1010. 2011. View Article : Google Scholar : PubMed/NCBI | |
Chan JY, Gao W, Ho WK, Wei WI and Wong TS: Overexpression of Epstein-Barr virus-encoded microRNA-BART7 in undifferentiated nasopharyngeal carcinoma. Anticancer Res. 32:3201–3210. 2012.PubMed/NCBI | |
Cai X, Schäfer A, Lu S, Bilello JP, Desrosiers RC, Edwards R, Raab-Traub N and Cullen BR: Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. 2:e232006. View Article : Google Scholar : PubMed/NCBI | |
Neuhierl B and Delecluse HJ: Molecular genetics of DNA viruses: Recombinant virus technology. Methods Mol Biol. 292:353–370. 2005.PubMed/NCBI | |
Feederle R, Linnstaedt SD, Bannert H, Lips H, Bencun M, Cullen BR and Delecluse HJ: A viral microRNA cluster strongly potentiates the transforming properties of a human herpesvirus. PLoS Pathog. 7:e10012942011. View Article : Google Scholar : PubMed/NCBI | |
Tsao SW, Tsang CM and Lo KW: Epstein-Barr virus infection and nasopharyngeal carcinoma. Philos Trans R Soc Lond B Biol Sci. 372(pii): 201602702017. View Article : Google Scholar : PubMed/NCBI | |
Young LS and Dawson CW: Epstein-Barr virus and nasopharyngeal carcinoma. Chin J Cancer. 33:581–590. 2014.PubMed/NCBI | |
Zheng X, Wang J, Wei L, Peng Q, Gao Y, Fu Y, Lu Y, Qin Z, Zhang X, Lu J, et al: Epstein-Barr virus MicroRNA miR-BART5-3p inhibits p53 expression. J Virol. 92(pii): e01022–18. 2018.PubMed/NCBI | |
Marquitz AR, Mathur A, Nam CS and Raab-Traub N: The Epstein-Barr virus BART microRNAs target the pro-apoptotic protein Bim. Virology. 412:392–400. 2011. View Article : Google Scholar : PubMed/NCBI | |
Choy EY, Siu KL, Kok KH, Lung RW, Tsang CM, To KF, Kwong DL, Tsao SW and Jin DY: An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J Exp Med. 205:2551–2560. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lei T, Yuen KS, Xu R, Tsao SW, Chen H, Li M, Kok KH and Jin DY: Targeting of DICE1 tumor suppressor by Epstein-Barr virus-encoded miR-BART3* microRNA in nasopharyngeal carcinoma. Int J Cancer. 133:79–87. 2013. View Article : Google Scholar : PubMed/NCBI | |
Cai L, Ye Y, Jiang Q, Chen Y, Lyu X, Li J, Wang S, Liu T, Cai H, Yao K, et al: Epstein-Barr virus-encoded microRNA BART1 induces tumour metastasis by regulating PTEN-dependent pathways in nasopharyngeal carcinoma. Nat Commun. 6:73532015. View Article : Google Scholar : PubMed/NCBI | |
Cai LM, Lyu XM, Luo WR, Cui XF, Ye YF, Yuan CC, Peng QX, Wu DH, Liu TF, Wang E, et al: EBV-miR-BART7-3p promotes the EMT and metastasis of nasopharyngeal carcinoma cells by suppressing the tumor suppressor PTEN. Oncogene. 34:2156–2166. 2015. View Article : Google Scholar : PubMed/NCBI | |
Hsu CY, Yi YH, Chang KP, Chang YS, Chen SJ and Chen HC: The Epstein-Barr virus-encoded microRNA MiR-BART9 promotes tumor metastasis by targeting E-cadherin in nasopharyngeal carcinoma. PLoS Pathog. 10:e10039742014. View Article : Google Scholar : PubMed/NCBI | |
Dölken L, Malterer G, Erhard F, Kothe S, Friedel CC, Suffert G, Marcinowski L, Motsch N, Barth S, Beitzinger M, et al: Systematic analysis of viral and cellular microRNA targets in cells latently infected with human gamma-herpesviruses by RISC immunoprecipitation assay. Cell Host Microbe. 7:324–334. 2010. View Article : Google Scholar : PubMed/NCBI | |
Iizasa H, Wulff BE, Alla NR, Maragkakis M, Megraw M, Hatzigeorgiou A, Iwakiri D, Takada K, Wiedmer A, Showe L, et al: Editing of Epstein-Barr virus-encoded BART6 microRNAs controls their dicer targeting and consequently affects viral latency. J Biol Chem. 285:33358–33370. 2010. View Article : Google Scholar : PubMed/NCBI | |
Nachmani D, Stern-Ginossar N, Sarid R and Mandelboim O: Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe. 5:376–385. 2009. View Article : Google Scholar : PubMed/NCBI | |
Lo AK, To KF, Lo KW, Lung RW, Hui JW, Liao G and Hayward SD: Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc Natl Acad Sci USA. 104:16164–16169. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lung RW, Tong JH, Sung YM, Leung PS, Ng DC, Chau SL, Chan AW, Ng EK, Lo KW and To KF: Modulation of LMP2A expression by a newly identified Epstein-Barr virus-encoded microRNA miR-BART22. Neoplasia. 11:1174–1184. 2009. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Dawson CW, He Z and Huang P: Immune evasion strategies of the human gamma-herpesviruses: Implications for viral tumorigenesis. J Med Virol. 84:272–281. 2012. View Article : Google Scholar : PubMed/NCBI | |
Seto E, Moosmann A, Gromminger S, Walz N, Grundhoff A and Hammerschmidt W: Micro RNAs of Epstein-Barr virus promote cell cycle progression and prevent apoptosis of primary human B cells. PLoS Pathog. 6:e10010632010. View Article : Google Scholar : PubMed/NCBI | |
Vereide DT, Seto E, Chiu YF, Hayes M, Tagawa T, Grundhoff A, Hammerschmidt W and Sugden B: Epstein-Barr virus maintains lymphomas via its miRNAs. Oncogene. 33:1258–1264. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ramalingam D, Kieffer-Kwon P and Ziegelbauer JM: Emerging themes from EBV and KSHV microRNA targets. Viruses. 4:1687–1710. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fernandes Q, Merhi M, Raza A, Inchakalody VP, Abdelouahab N, Zar Gul AR, Uddin S and Dermime S: Role of Epstein-Barr virus in the pathogenesis of head and neck cancers and its potential as an immunotherapeutic target. Front in Oncol. 8:2572018. View Article : Google Scholar | |
Albanese M, Tagawa T, Buschle A and Hammerschmidt W: MicroRNAs of Epstein-Barr virus control innate and adaptive antiviral immunity. J Virol. 91(pii): e01667–16. 2017.PubMed/NCBI | |
Poling BC, Price AM, Luftig MA and Cullen BR: The Epstein-Barr virus miR-BHRF1 microRNAs regulate viral gene expression in cis. Virology. 512:113–123. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kim Y, Lee S, Kim S, Kim D, Ahn JH and Ahn K: Human cytomegalovirus clinical strain-specific microRNA miR-UL148D targets the human chemokine RANTES during infection. PLoS Pathog. 8:e10025772012. View Article : Google Scholar : PubMed/NCBI | |
Haneklaus M, Gerlic M, Kurowska-Stolarska M, Rainey AA, Pich D, McInnes IB, Hammerschmidt W, O'Neill LA and Masters SL: Cutting edge: miR-223 and EBV miR-BART15 regulate the NLRP3 inflammasome and IL-1β production. J Immunol. 189:3795–3799. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kim S, Lee S, Shin J, Kim Y, Evnouchidou I, Kim D, Kim YK, Kim YE, Ahn JH, Riddell SR, et al: Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol. 12:984–991. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bauman Y, Nachmani D, Vitenshtein A, Tsukerman P, Drayman N, Stern-Ginossar N, Lankry D, Gruda R and Mandelboim O: An identical miRNA of the human JC and BK polyoma viruses targets the stress-induced ligand ULBP3 to escape immune elimination. Cell Host Microbe. 9:93–102. 2011. View Article : Google Scholar : PubMed/NCBI | |
Abend JR, Ramalingam D, Kieffer-Kwon P, Uldrick TS, Yarchoan R and Ziegelbauer JM: Kaposi's sarcoma-associated herpesvirus microRNAs target IRAK1 and MYD88, two components of the toll-like receptor/interleukin-1R signaling cascade, to reduce inflammatory-cytokine expression. J Virol. 86:11663–11674. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lei X, Bai Z, Ye F, Xie J, Kim CG, Huang Y and Gao SJ: Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA. Nat Cell Biol. 12:193–199. 2010. View Article : Google Scholar : PubMed/NCBI | |
Liang D, Gao Y, Lin X, He Z, Zhao Q, Deng Q and Lan K: A human herpesvirus miRNA attenuates interferon signaling and contributes to maintenance of viral latency by targeting IKKε. Cell Res. 21:793–806. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hooykaas MJG, van Gent M, Soppe JA, Kruse E, Boer IGJ, van Leenen D, Groot Koerkamp MJA, Holstege FCP, Ressing ME, Wiertz EJHJ and Lebbink RJ: EBV MicroRNA BART16 suppresses type I IFN signaling. J Immunol. 198:4062–4073. 2017. View Article : Google Scholar : PubMed/NCBI | |
Skinner CM, Ivanov NS, Barr SA, Chen Y and Skalsky RL: An Epstein-Barr virus microrna blocks interleukin-1 (IL-1) signaling by targeting IL-1 receptor 1. J Virol. 91(pii): e00530–17. 2017.PubMed/NCBI | |
Dillon CP and Green DR: Molecular cell biology of apoptosis and necroptosis in cancer. Adv Exp Med Biol. 930:1–23. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kvansakul M, Caria S and Hinds MG: The Bcl-2 family in host-virus interactions. Viruses. 9(pii): E2902017. View Article : Google Scholar : PubMed/NCBI | |
Kang D, Skalsky RL and Cullen BR: EBV BART microRNAs target multiple pro-apoptotic cellular genes to promote epithelial cell survival. PLoS Pathog. 11:e10049792015. View Article : Google Scholar : PubMed/NCBI | |
Kim H, Choi H and Lee SK: Epstein-Barr virus miR-BART20-5p regulates cell proliferation and apoptosis by targeting BAD. Cancer Lett. 356:733–742. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kim H, Choi H and Lee SK: Epstein-Barr virus MicroRNA miR-BART20-5p suppresses lytic induction by inhibiting BAD-mediated caspase-3-dependent apoptosis. J Virol. 90:1359–1368. 2015. View Article : Google Scholar : PubMed/NCBI | |
Marquitz AR, Mathur A, Shair KH and Raab-Traub N: Infection of Epstein-Barr virus in a gastric carcinoma cell line induces anchorage independence and global changes in gene expression. Proc Natl Acad Sci USA. 109:9593–9598. 2012. View Article : Google Scholar : PubMed/NCBI | |
Shinozaki-Ushiku A, Kunita A, Isogai M, Hibiya T, Ushiku T, Takada K and Fukayama M: Profiling of virus-encoded microRNAs in Epstein-Barr virus-associated gastric carcinoma and their roles in gastric carcinogenesis. J Virol. 89:5581–5591. 2015. View Article : Google Scholar : PubMed/NCBI | |
Harold C, Cox D and Riley KJ: Epstein-Barr viral microRNAs target caspase 3. Virol J. 13:1452016. View Article : Google Scholar : PubMed/NCBI | |
Choi H and Lee SK: TAX1BP1 downregulation by EBV-miR-BART15-3p enhances chemosensitivity of gastric cancer cells to 5-FU. Arch Virol. 162:369–377. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ma J, Nie K, Redmond D, Liu Y, Elemento O, Knowles DM and Tam W: EBV-miR-BHRF1-2 targets PRDM1/Blimp1: Potential role in EBV lymphomagenesis. Leukemia. 30:594–604. 2016. View Article : Google Scholar : PubMed/NCBI | |
Bernhardt K, Haar J, Tsai MH, Poirey R, Feederle R and Delecluse HJ: A viral microRNA cluster regulates the expression of PTEN, p27 and of a bcl-2 homolog. PLoS Pathog. 12:e10054052016. View Article : Google Scholar : PubMed/NCBI | |
Engelman JA, Luo J and Cantley LC: The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet. 7:606–619. 2006. View Article : Google Scholar : PubMed/NCBI | |
Zhang G, Zong J, Lin S, Verhoeven RJ, Tong S, Chen Y, Ji M, Cheng W, Tsao SW, Lung M, et al: Circulating Epstein-Barr virus microRNAs miR-BART7 and miR-BART13 as biomarkers for nasopharyngeal carcinoma diagnosis and treatment. Int J Cancer. 136:E301–E312. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ferrajoli A, Ivan C, Ciccone M, Shimizu M, Kita Y, Ohtsuka M, D'Abundo L, Qiang J, Lerner S, Nouraee N, et al: Epstein-Barr virus microRNAs are expressed in patients with chronic lymphocytic leukemia and correlate with overall survival. EBioMedicine. 2:572–582. 2015. View Article : Google Scholar : PubMed/NCBI | |
Nordström M, Hardell L, Lindström G, Wingfors H, Hardell K and Linde A: Concentrations of organochlorines related to titers to Epstein-Barr virus early antigen IgG as risk factors for hairy cell leukemia. Environ Health Perspect. 108:441–445. 2000. View Article : Google Scholar : PubMed/NCBI | |
Sempere LF: Tissue slide-based microRNA characterization of tumors: How detailed could diagnosis become for cancer medicine? Expert Rev Mol Diagn. 14:853–869. 2014. View Article : Google Scholar : PubMed/NCBI | |
Mishra PJ: MicroRNAs as promising biomarkers in cancer diagnostics. Biomark Res. 2:192014. View Article : Google Scholar : PubMed/NCBI | |
Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, Muramatsu K, Fukuda Y, Ogura S, Yamaguchi K and Mochizuki T: Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One. 5:e132472010. View Article : Google Scholar : PubMed/NCBI | |
Zhao H, Shen J, Medico L, Wang D, Ambrosone CB and Liu S: A pilot study of circulating miRNAs as potential biomarkers of early stage breast cancer. PLoS One. 5:e137352010. View Article : Google Scholar : PubMed/NCBI | |
Pigati L, Yaddanapudi SC, Iyengar R, Kim DJ, Hearn SA, Danforth D, Hastings ML and Duelli DM: Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS One. 5:e135152010. View Article : Google Scholar : PubMed/NCBI | |
Wei R, Huang GL, Zhang MY, Li BK, Zhang HZ, Shi M, Chen XQ, Huang L, Zhou QM, Jia WH, et al: Clinical significance and prognostic value of microRNA expression signatures in hepatocellular carcinoma. Clin Cancer Res. 19:4780–4791. 2013. View Article : Google Scholar : PubMed/NCBI | |
Cheng H, Zhang L, Cogdell DE, Zheng H, Schetter AJ, Nykter M, Harris CC, Chen K, Hamilton SR and Zhang W: Circulating plasma MiR-141 is a novel biomarker for metastatic colon cancer and predicts poor prognosis. PLoS One. 6:e177452011. View Article : Google Scholar : PubMed/NCBI | |
Subramanian S, Lui WO, Lee CH, Espinosa I, Nielsen TO, Heinrich MC, Corless CL, Fire AZ and van de Rijn M: MicroRNA expression signature of human sarcomas. Oncogene. 27:2015–2026. 2008. View Article : Google Scholar : PubMed/NCBI | |
Osaki M, Takeshita F and Ochiya T: MicroRNAs as biomarkers and therapeutic drugs in human cancer. Biomarkers. 13:658–670. 2008. View Article : Google Scholar : PubMed/NCBI | |
Nair VS, Maeda LS and Ioannidis JP: Clinical outcome prediction by microRNAs in human cancer: A systematic review. J Natl Cancer Inst. 104:528–540. 2012. View Article : Google Scholar : PubMed/NCBI | |
Hu Z, Chen X, Zhao Y, Tian T, Jin G, Shu Y, Chen Y, Xu L, Zen K, Zhang C and Shen H: Serum microRNA signatures identified in a genome-wide serum microRNA expression profiling predict survival of non-small-cell lung cancer. J Clin Oncol. 28:1721–1726. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zuo Z, Calin GA, de Paula HM, Medeiros LJ, Fernandez MH, Shimizu M, Garcia-Manero G and Bueso-Ramos CE: Circulating microRNAs let-7a and miR-16 predict progression-free survival and overall survival in patients with myelodysplastic syndrome. Blood. 118:413–415. 2011. View Article : Google Scholar : PubMed/NCBI | |
Esquela-Kerscher A and Slack FJ: Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer. 6:259–269. 2006. View Article : Google Scholar : PubMed/NCBI | |
Zhang MX, Li J, Shen GP, Zou X, Xu JJ, Jiang R, You R, Hua YJ, Sun Y, Ma J, et al: Intensity-modulated radiotherapy prolongs the survival of patients with nasopharyngeal carcinoma compared with conventional two-dimensional radiotherapy: A 10-year experience with a large cohort and long follow-up. Eur J Cancer. 51:2587–2595. 2015. View Article : Google Scholar : PubMed/NCBI | |
Chung IC, Chen LC, Chung AK, Chao M, Huang HY, Hsueh C, Tsang NM, Chang KP, Liang Y, Li HP and Chang YS: Matrix metalloproteinase 12 is induced by heterogeneous nuclear ribonucleoprotein K and promotes migration and invasion in nasopharyngeal carcinoma. BMC Cancer. 14:3482014. View Article : Google Scholar : PubMed/NCBI | |
Yi W, Li X, Liu Z, Jiang C, Niu D and Xia Y: A risk score model for the metastasis of level Ib lymph node based on the clinicopathological features of nasopharyngeal carcinoma in a large sample. Mol Clin Oncol. 2:789–797. 2014. View Article : Google Scholar : PubMed/NCBI | |
Shi Q, Shen C, Kong L, Wang X, Ding J, Gao Y, Xu T and Hu C: Involvement of both cervical lymph nodes and retropharyngeal lymph nodes has prognostic value for N1 patients with nasopharyngeal carcinoma. Radiat Oncol. 9:72014. View Article : Google Scholar : PubMed/NCBI | |
Wang HZ, Cao CN, Luo JW, Yi JL, Huang XD, Zhang SP, Wang K, Qu Y, Xiao JP, Li SY, et al: High-risk factors of parotid lymph node metastasis in nasopharyngeal carcinoma: A case-control study. Radiat Oncol. 11:1132016. View Article : Google Scholar : PubMed/NCBI | |
Tang LL, Tang XR, Li WF, Chen L, Tian L, Lin AH, Sun Y and Ma J: The feasibility of contralateral lower neck sparing intensity modulation radiated therapy for nasopharyngeal carcinoma patients with unilateral cervical lymph node involvement. Oral Oncol. 69:68–73. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Li WF, Chen L, Mao YP, Guo R, Zhang F, Peng H, Liu LZ, Li L, Liu Q and Ma J: Prognostic value of parotid lymph node metastasis in patients with nasopharyngeal carcinoma receiving intensity-modulated radiotherapy. Sci Rep. 5:139192015. View Article : Google Scholar : PubMed/NCBI | |
Tagawa T, Albanese M, Bouvet M, Moosman A, Mautner J, Heissmeyer V Zielinski C, Hoser J, Hastreiter M, Hayes M, et al: Epstein-Barr viral miRNAs inhibit antiviral CD4+ T cell responses targeting IL-12 and peptide processing. J Exp Med. 213:2065–2080. 2016. View Article : Google Scholar : PubMed/NCBI | |
Feederle R, Haar J, Bernhardt K, Linnstaedt SD, Bannert H, Lips H, Cullen BR and Delecluse HJ: The members of an Epstein-Barr virus microRNA cluster cooperate to transform B lymphocytes. J Virol. 85:9801–9810. 2011. View Article : Google Scholar : PubMed/NCBI |