Epstein-Barr Virus miR-BART6-3p Inhibits the RIG-I Pathway

Journal of Innate Immunity

Volumn 9, Issue 6, 2017, Pages 574-586

  Lu, Yuanjun ^a,b   Qin, Zailong ^b   Wang, Jia ^b   Zheng, Xiang ^b   Lu, Jianhong ^b   Zhang, Xuemei ^b   Wei, Lingyu ^b   Peng, Qiu ^a,b   Zheng, Ying ^b   Ou, Chunlin ^a,b   Ye, Qiurong ^b   Xiong, Wei ^a,b   Li, Guiyuan ^a,b   Fu, Yuxin ^a   Yan, Qun ^a   Ma, Jian ^a,b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Epstein Barr virus; Innate immunity; Interferon; miR BART6 3p; RIG I

Indexed keywords

BETA INTERFERON; INTERFERON; MICRORNA; MICRORNA BART6-3P; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATTERN RECOGNITION RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; TRANSCRIPTOME; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRUS RNA; RARRES3 PROTEIN, HUMAN; RETINOIC ACID RECEPTOR;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNE EVASION; IMMUNE RESPONSE; INNATE IMMUNITY; LATENT VIRUS INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SEQUENCE; SIGNAL TRANSDUCTION; CELL LINE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KIDNEY PROXIMAL TUBULE; METABOLISM; VIROLOGY;

CELL LINE; EPSTEIN-BARR VIRUS INFECTIONS; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; KIDNEY TUBULES, PROXIMAL; MICRORNAS; PATHOGEN-ASSOCIATED MOLECULAR PATTERN MOLECULES; RECEPTORS, PATTERN RECOGNITION; RECEPTORS, RETINOIC ACID; RNA, VIRAL; SIGNAL TRANSDUCTION;

EID: 85028962012     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000479749     Document Type: Article

References (52)

1. Epstein MA, Achong BG, Barr YM: Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet 1964; 1: 702-703.
2. Luzuriaga K, Sullivan JL: Infectious mononucleosis. New Engl J Med 2010; 362: 1993-2000.
3. Geser A, de The G, Lenoir G, Day NE, Williams EH: Final case reporting from the Ugandan prospective study of the relationship between EBV and Burkitt's lymphoma. Int J Cancer 1982; 29: 397-400.
4. Henle W, Henle G: The relation of the Epstein-Barr virus to Burkitt's lymphoma. Zentralbl Bakteriol Orig A 1972; 220: 40-46.
5. Henle W, Henle G: Epstein-Barr virus-related serology in Hodgkin's disease. Natl Cancer Inst Monogr 1973; 36: 79-84.
6. Henle W, Henle G: Evidence for an oncogenic potential of the Epstein-Barr virus. Cancer Res 1973; 33: 1419-1423.
7. Henle W, Henle G: The Epstein-Barr Virus (EBV) in Burkitt's lymphoma and nasopharyngeal carcinoma. Ann Clin Lab Sci 1974; 4: 109-114.
8. Henle W, Henle G: Epstein-Barr virus and human malignancies. Cancer 1974; 34(suppl): 1368-1374.
9. Henle W, Henle G: The sero-epidemiology of Epstein-Barr virus. Adv Pathobiol 1976; 5: 5-17.
10. Henle W, Henle G: Evidence for an etiologic relation of the Epstein-Barr virus to human malignancies. Laryngoscope 1977; 87: 467-473.
11. Zeng Y, Zhang LG, Wu YC, Huang YS, Huang NQ, Li JY, Wang YB, Jiang MK, Fang Z, Meng NN: Prospective studies on nasopharyngeal carcinoma in Epstein-Barr virus IgA/VCA antibody-positive persons in Wuzhou City, China. Int J Cancer 1985; 36: 545-547.
12. Young LS, Rickinson AB: Epstein-Barr virus 13 years on. Nat Rev Cancer 2004; 4: 757-768.
13. Tu C, Zeng Z, Qi P, Li X, Yu Z, Guo C, Xiong F, Xiang B, Zhou M, Gong Z, Liao Q, Yu J, He Y, Zhang W, Li X, Li Y, Li G, Xiong W: Genome-wide analysis of eighteen Epstein-Barr viruses isolated from primary nasopharyngeal carcinoma biopsies. J Virol 2017; 91: e00301-17.
14. Barth S, Meister G, Grasser FA: EBV-encoded miRNAs. Biochim Biophys Acta 2011; 1809: 631-640.
15. Wong AM, Kong KL, Tsang JW, Kwong DL, Guan XY: Profiling of Epstein-Barr virus-encoded microRNAs in nasopharyngeal carcinoma reveals potential biomarkers and oncomirs. Cancer 2012; 118: 698-710.
16. Zuo L, Yue W, Du S, Xin S, Zhang J, Liu L, Li G, Lu J: An update: Epstein-Barr virus and immune evasion via microRNA regulation. Virol Sin 2017; 32: 175-187.
17. Baum A, Sachidanandam R, Garcia-Sastre A: Preference of RIG-I for short viral RNA molecules in infected cells revealed by next-generation sequencing. Proc Natl Acad Sci USA 2010; 107: 16303-16308.
18. Komarova AV, Combredet C, Sismeiro O, Dillies MA, Jagla B, Sanchez David RY, Vabret N, Coppee JY, Vidalain PO, Tangy F: Identification of RNA partners of viral proteins in infected cells. RNA Biol 2013; 10: 944-956.
19. Lin TC, Liu TY, Hsu SM, Lin CW: Epstein-Barr virus-encoded miR-BART20-5p inhibits T-bet translation with secondary suppression of p53 in invasive nasal NK/T-cell lymphoma. Am J Pathol 2013; 182: 1865-1875.
20. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reis e Sousa C: RIG-Imediated antiviral responses to single-stranded RNA bearing 5 phosphates. Science 2006; 314: 997-1001.
21. Samanta M, Iwakiri D, Kanda T, Imaizumi T, Takada K: EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 2006; 25: 4207-4214.
22. Der SD, Zhou A, Williams BR, Silverman RH: Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 1998; 95: 15623-15628.
23. de Veer MJ, Holko M, Frevel M, Walker E, Der S, Paranjape JM, Silverman RH, Williams BRG: Functional classification of interferonstimulated genes identified using microarrays. J Leukoc Biol 2001; 69: 912-920.
24. Gaudreault E, Fiola S, Olivier M, Gosselin J: Epstein-Barr virus induces MCP-1 secretion by human monocytes via TLR2. J Virol 2007; 81: 8016-8024.
25. Junying J, Herrmann K, Davies G, Lissauer D, Bell A, Timms J, Reynolds GM, Hubscher SG, Young LS, Niedobitek G, Murray PG: Absence of Epstein-Barr virus DNA in the tumor cells of European hepatocellular carcinoma. Virology 2003; 306: 236-243.
26. Zuo L, Yu H, Liu L, Tang Y, Wu H, Yang J, Zhu M, Du S, Zhao L, Cao L, Li G, Lu J: The copy number of Epstein-Barr virus latent genome correlates with the oncogenicity by the activation level of LMP1 and NF-B. Oncotarget 2015; 6: 41033-41044.
27. Zheng Y, Zhang W, Ye Q, Zhou Y, Xiong W, He W, Deng M, Zhou M, Guo X, Chen P, Fan S, Liu X, Wang Z, Li X, Ma J, Li G: Inhibition of Epstein-Barr virus infection by lactoferrin. J Innate Immun 2012; 4: 387-398.
28. Tang A, Li N, Li X, Yang H, Wang W, Zhang L, Li G, Xiong W, Ma J, Shen S: Dynamic activation of the key pathways: linking colitis to colorectal cancer in a mouse model. Carcinogenesis 2012; 33: 1375-1383.
29. Warde-Farley D, Donaldson SL, Comes O, Zuberi K, Badrawi R, Chao P, Franz M, Grouios C, Kazi F, Lopes CT, Maitland A, Mostafavi S, Montojo J, Shao Q, Wright G, Bader GD, Morris Q: The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res 2010; 38: W214-W220.
30. Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
31. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP: Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-15550.
32. Cancer Genome Atlas Research Network: Comprehensive molecular characterization of gastric adenocarcinoma. Nature 2014; 513: 202-209.
33. Duan Y, Li Z, Cheng S, Chen Y, Zhang L, He J, Liao Q, Yang L, Gong Z, Sun LQ: Nasopharyngeal carcinoma progression is mediated by EBER-triggered inflammation via the RIG-I pathway. Cancer Lett 2015; 361: 67-74.
34. Samanta M, Iwakiri D, Takada K: Epstein-Barr virus-encoded small RNA induces IL-10 through RIG-I-mediated IRF-3 signaling. Oncogene 2008; 27: 4150-4160.
35. Satoh T, Wada R, Yajima N, Imaizumi T, Yagihashi S: Tumor microenvironment and RIG-I signaling molecules in Epstein Barr virus-positive and-negative classical Hodgkin lymphoma of the elderly. J Clin Exp Hematopathol 2014; 54: 75-84.
36. Weil R, Laplantine E, Genin P: Regulation of TBK1 activity by Optineurin contributes to cell cycle-dependent expression of the interferon pathway. Cytokine Growth Factor Rev 2016; 29: 23-33.
37. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa C, Matsuura Y, Fujita T, Akira S: Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441: 101-105.
38. Ramos HJ, Gale M Jr: RIG-I like receptors and their signaling crosstalk in the regulation of antiviral immunity. Curr Opin Virol 2011; 1: 167-176.
39. Sanchez David RY, Combredet C, Sismeiro O, Dillies MA, Jagla B, Coppee JY, Mura M, Guerbois Galla M, Despres P, Tangy F, Komarova AV: Comparative analysis of viral RNA signatures on different RIG-I-like receptors. eLife 2016; 5: e11275.
40. Taylor KE, Mossman KL: Recent advances in understanding viral evasion of type I interferon. Immunology 2013; 138: 190-197.
41. Marquitz AR, Raab-Traub N: The role of miRNAs and EBV BARTs in NPC. Semin Cancer Biol 2012; 22: 166-172.
42. Haneklaus M, Gerlic M, Kurowska-Stolarska M, Rainey AA, Pich D, McInnes IB, Hammerschmidt W, O'Neill LA, Masters SL: Cutting edge: miR-223 and EBV miR-BART15 regulate the NLRP3 inflammasome and IL-1 production. J Immunol 2012; 189: 3795-3799.
43. Ambrosio MR, Navari M, Di Lisio L, Leon EA, Onnis A, Gazaneo S, Mundo L, Ulivieri C, Gomez G, Lazzi S, Piris MA, Leoncini L, De Falco G: The Epstein Barr-encoded BART-6-3p microRNA affects regulation of cell growth and immuno response in Burkitt lymphoma. Infect Agent Cancer 2014; 9: 12.
44. Deng L, Wang X, Jiang L, Yang J, Zhou X, Lu Z, Hu H: Modulation of miR-185-5p expression by EBV-miR-BART6 contributes to developmental differences in ABCG4 gene expression in human megakaryocytes. Int J Biochem Cell Biol 2016; 81: 105-111.
45. He B, Li W, Wu Y, Wei F, Gong Z, Bo H, Wang Y, Li X, Xiang B, Guo C, Liao Q, Chen P, Zu X, Zhou M, Ma J, Li X, Li Y, Li G, Xiong W, Zeng Z: Epstein-Barr virus-encoded miRBART6-3p inhibits cancer cell metastasis and invasion by targeting long non-coding RNA LOC553103. Cell Death Dis 2016; 7: e2353.
46. Iizasa H, Wulff BE, Alla NR, Maragkakis M, Megraw M, Hatzigeorgiou A, Iwakiri D, Takada K, Wiedmer A, Showe L, Lieberman P, Nishikura K: Editing of Epstein-Barr virusencoded BART6 microRNAs controls their dicer targeting and consequently affects viral latency. J Biol Chem 2010; 285: 33358-33370.
47. Chijioke O, Azzi T, Nadal D, Munz C: Innate immune responses against Epstein Barr virus infection. J Leukocyte Biol 2013; 94: 1185-1190.
48. Croft NP, Shannon-Lowe C, Bell AI, Horst D, Kremmer E, Ressing ME, Wiertz EJ, Middeldorp JM, Rowe M, Rickinson AB, Hislop AD: Stage-specific inhibition of MHC class I presentation by the Epstein-Barr virus BNLF2a protein during virus lytic cycle. PLoS Pathogens 2009; 5: e1000490.
49. Zuo J, Quinn LL, Tamblyn J, Thomas WA, Feederle R, Delecluse HJ, Hislop AD, Rowe M: The Epstein-Barr virus-encoded BILF1 protein modulates immune recognition of endogenously processed antigen by targeting major histocompatibility complex class I molecules trafficking on both the exocytic and endocytic pathways. J Virol 2011; 85: 1604-1614.
50. Zuo J, Thomas W, van Leeuwen D, Middeldorp JM, Wiertz EJ, Ressing ME, Rowe M: The DNase of gammaherpesviruses impairs recognition by virus-specific CD8 + T cells through an additional host shutoff function. J Virol 2008; 82: 2385-2393.
51. Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O: Diverse herpesvirus micro-RNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 2009; 5: 376-385.
52. Gourzones C, Gelin A, Bombik I, Klibi J, Verillaud B, Guigay J, Lang P, Temam S, Schneider V, Amiel C, Baconnais S, Jimenez AS, Busson P: Extra-cellular release and blood diffusion of BART viral micro-RNAs produced by EBV-infected nasopharyngeal carcinoma cells. Virol J 2010; 7: 271.