Pol-miR-731, a teleost miRNA upregulated by megalocytivirus, negatively regulates virus-induced type I interferon response, apoptosis, and cell cycle arrest

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Zhang, Bao Cun ^a,b   Zhou, Ze Jun ^a,b,c   Sun, Li ^a,b  

^a INSTITUTE OF OCEANOLOGY   (China)

^b QINGDAO NATIONAL LABORATORY FOR MARINE SCIENCE AND TECHNOLOGY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FISH PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 7; MICRORNA; PROTEIN P53; VIRUS RNA;

ANIMAL; APOPTOSIS; CELL CYCLE CHECKPOINT; FLOUNDER; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; IRIDOVIRIDAE; PHYSIOLOGY; VIROLOGY; VIRUS REPLICATION;

ANIMALS; APOPTOSIS; CELL CYCLE CHECKPOINTS; FISH PROTEINS; FLOUNDER; HOST-PATHOGEN INTERACTIONS; INTERFERON REGULATORY FACTOR-7; INTERFERON TYPE I; IRIDOVIRIDAE; MICRORNAS; RNA, VIRAL; TUMOR SUPPRESSOR PROTEIN P53; VIRUS REPLICATION;

EID: 84975484950     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep28354     Document Type: Article

References (55)

1. Chinchar, V. G., Hyatt, A., Miyazaki, T. & Williams, T. Family Iridoviridae: poor viral relations no longer. Curr Top Microbiol 328, 123-170 (2009).
2. Zhang, B. C., Zhang, J. & Sun, L. Streptococcus iniae SF1: complete genome sequence, proteomic profile, and immunoprotective antigens. Plos One 9, doi: ARTN e91324 10.1371/journal.pone.0091324 (2014).
3. Kurita, J. & Nakajima, K. Megalocytiviruses. Viruses-Basel 4, 521-538, doi: 10.3390/v4040521 (2012).
4. Wang, R. et al. ORF005L from infectious spleen and kidney necrosis virus is located in the inner mitochondrial membrane and induces apoptosis. Virus Genes 49, 269-277, doi: 10.1007/s11262-014-1088-2 (2014).
5. He, B. L. et al. The viral TRAF protein (ORF111L) from infectious spleen and kidney necrosis virus interacts with TRADD and induces caspase 8-mediated apoptosis. Plos One 7, doi: ARTN e37001 10.1371/journal.pone.0037001 (2012).
6. Yuan, J. M. et al. Interaction of infectious spleen and kidney necrosis virus ORF119L with PINCH leads to dominant-negative inhibition of integrin-linked kinase and cardiovascular defects in zebrafish. J Virol 89, 763-775, doi: 10.1128/Jvi.01955-14 (2015).
7. Xie, J. F. et al. RING finger proteins of infectious spleen and kidney necrosis virus (ISKNV) function as ubiquitin ligase enzymes. Virus Res 123, 170-177, doi: 10.1016/j.virusres.2006.09.003 (2007).
8. Guo, C. J. et al. The viral ankyrin repeat protein (ORF1 24L) from infectious spleen and kidney necrosis virus attenuates nuclear factor-kappa B activation and interacts with I kappa B kinase beta. J Gen Virol 92, 1561-1570, doi: 10.1099/vir.0.031120-0 (2011).
9. Guo, C. J. et al. A novel viral SOCS from infectious spleen and kidney necrosis virus: interacts with Jak1 and inhibits IFN-alpha induced stat1/3 activation. Plos One 7, doi: ARTN e41092 10.1371/journal.pone.0041092 (2012).
10. Cullen, B. R. MicroRNAs as mediators of viral evasion of the immune system. Nat Immunol 14, 205-210, doi: 10.1038/ni.2537 (2013).
11. Asgari, S. MicroRNA functions in insects. Insect biochemistry and molecular biology 43, 388-397, doi: 10.1016/j.ibmb.2012.10.005 (2013).
12. Choy, E. Y. W. et al. An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J Exp Med 205, 2551-2560, doi: 10.1084/jem.20072581 (2008).
13. 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 5, 376-385, doi: 10.1016/j.chom.2009.03.003 (2009).
14. Diebel, K. W. et al. Gammaherpesvirus small noncoding rnas are bifunctional elements that regulate infection and contribute to virulence in vivo. Mbio 6, doi: ARTN e01670-14 10.1128/mBio.01670-14 (2015).
15. Feldman, E. R. et al. Virus-encoded micrornas facilitate gammaherpesvirus latency and pathogenesis in vivo. Mbio 5, doi: ARTN e00981-14 10.1128/mBio.00981-14 (2014).
16. Hussain, M. et al. West Nile virus encodes a microRNA-like small RNA in the 3′ untranslated region which up-regulates GATA4 mRNA and facilitates virus replication in mosquito cells. Nucleic Acids Res 40, 2210-2223, doi: 10.1093/nar/gkr848 (2012).
17. Ren, Q., Huang, Y., He, Y., Wang, W. & Zhang, X. A white spot syndrome virus microRNA promotes the virus infection by targeting the host STAT. Scientific reports 5, 18384, doi: 10.1038/srep18384 (2015).
18. Guo, Y. E. & Steitz, J. A. Virus meets host microRNA: the destroyer, the booster, the hijacker. Mol Cell Biol 34, 3780-3787, doi: 10.1128/Mcb.00871-14 (2014).
19. Li, J. F. et al. Upregulation of microRNA-146a by hepatitis B virus X protein contributes to hepatitis development by downregulating complement factor H. Mbio 6, doi: ARTN e02459-14 10.1128/mBio.02459-14 (2015).
20. Thornburg, N. J., Hayward, S. L. & Crowe, J. E. Respiratory syncytial virus regulates human microRNAs by using mechanisms involving beta interferon and NF-kappa B. Mbio 3, doi: ARTN e00220-12 10.1128/mBio.00220-12 (2012).
21. Zhang, B. C., Zhang, J. & Sun, L. In-depth profiling and analysis of host and viral microRNAs in Japanese flounder (Paralichthys olivaceus) infected with megalocytivirus reveal involvement of microRNAs in host-virus interaction in teleost fish. Bmc Genomics 15, doi: Artn 878 10.1186/1471-2164-15-878 (2014).
22. Zhang, B. C., Zhang, J., Xiao, Z. Z. & Sun, L. Rock bream (Oplegnathus fasciatus) viperin is a virus-responsive protein that modulates innate immunity and promotes resistance against megalocytivirus infection. Dev Comp Immunol 45, 35-42, doi: 10.1016/j. dci.2014.02.001 (2014).
23. Zhu, L. Y., Nie, L., Zhu, G., Xiang, L. X. & Shao, J. Z. Advances in research of fish immune-relevant genes: A comparative overview of innate and adaptive immunity in teleosts. Dev Comp Immunol 39, 39-62, doi: 10.1016/j.dci.2012.04.001 (2013).
24. Zhang, Y. B. & Gui, J. F. Molecular regulation of interferon antiviral response in fish. Dev Comp Immunol 38, 193-202, doi: 10.1016/j. dci.2012.06.003 (2012).
25. Song, Y. et al. Early stress responses in Atlantic salmon (Salmo salar) exposed to environmentally relevant concentrations of uranium. Aquat Toxicol 112, 62-71, doi: 10.1016/j.aquatox.2012.01.019 (2012).
26. Ohtsuka, T. et al. ASC is a Bax adaptor and regulates the p53-Bax mitochondrial apoptosis pathway. Nat Cell Biol 6, 121- +, doi: 10.1038/ncb1087 (2004).
27. Cayrol, C., Knibiehler, M. & Ducommun, B. p21 binding to PCNA causes G1 and G2 cell cycle arrest in p53-deficient cells. Oncogene 16, 311-320, doi: DOI 10.1038/sj.onc.1201543 (1998).
28. Skalsky, R. L. & Cullen, B. R. Viruses, microRNAs, and host interactions. Annu Rev Microbiol 64, 123-141, doi: 10.1146/annurev. micro.112408.134243 (2010).
29. Chen, H., Zhang, L. R., Yu, K. F. & Wang, A. M. Pathogenesis of soybean mosaic virus in soybean carrying Rsv1 gene is associated with miRNA and siRNA pathways, and breakdown of AGO1 homeostasis. Virology 476, 395-404, doi: 10.1016/j.virol.2014.12.034 (2015).
30. Cazalla, D., Yario, T. & Steitz, J. Down-regulation of a host microRNA by a herpesvirus saimiri noncoding RNA. Science 328, 1563-1566, doi: 10.1126/science.1187197 (2010).
31. Lanford, R. E. et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327, 198-201, doi: 10.1126/science.1178178 (2010).
32. Hussain, M. & Asgari, S. Functional analysis of a cellular microRNA in insect host-ascovirus interaction. J Virol 84, 612-620, doi: 10.1128/JVI.01794-09 (2010).
33. O'Connor, C. M., Vanicek, J. & Murphy, E. A. Host microRNA regulation of human cytomegalovirus immediate early protein translation promotes viral latency. J Virol 88, 5524-5532, doi: 10.1128/Jvi.00481-14 (2014).
34. Murphy, E., Vanicek, J., Robins, H., Shenk, T. & Levine, A. J. Suppression of immediate-early viral gene expression by herpesviruscoded microRNAs: implications for latency. P Natl Acad Sci USA 105, 5453-5458, doi: 10.1073/pnas.0711910105 (2008).
35. Broekema, N. M. & Imperiale, M. J. miRNA regulation of BK polyomavirus replication during early infection. P Natl Acad Sci USA 110, 8200-8205, doi: 10.1073/pnas.1301907110 (2013).
36. Schyth, B. D. et al. Two virus-induced microRNAs known only from teleost fishes are orthologues of micrornas involved in cell cycle control in humans. Plos One 10, doi: ARTN e0132434 10.1371/journal.pone.0132434 (2015).
37. Paludan, S. R., Bowie, A. G., Horan, K. A. & Fitzgerald, K. A. Recognition of herpesviruses by the innate immune system. Nat Rev Immunol 11, 143-154, doi: 10.1038/nri2937 (2011).
38. Garcia-Sastre, A. & Biron, C. A. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312, 879-882, doi: 10.1126/science.1125676 (2006).
39. Rasmussen, S. B. et al. Type I interferon production during herpes simplex virus infection is controlled by cell-type-specific viral recognition through toll-like receptor 9, the mitochondrial antiviral signaling protein pathway, and novel recognition systems. J Virol 81, 13315-13324, doi: 10.1128/Jvi.01167-07 (2007).
40. Forster, S. C., Tate, M. D. & Hertzog, P. J. MicroRNA as type I interferon-regulated transcripts and modulators of the innate immune response. Front Immunol 6, 1-9, doi: Artn 334 10.3389/Fimmu.2015.00334 (2015).
41. Zhou, Z. J. & Sun, L. CsCTL1, a teleost C-type lectin that promotes antibacterial and antiviral immune defense in a manner that depends on the conserved EPN motif. Dev Comp Immunol 50, 69-77, doi: 10.1016/j.dci.2015.01.007 (2015).
42. Xu, C. Z. et al. Downregulation of microRNA miR-526a by enterovirus inhibits RIG-I-dependent innate immune response. J Virol 88, 11356-11368, doi: 10.1128/Jvi.01400-14 (2014).
43. Liang, D. G. et al. A human herpesvirus miRNA attenuates interferon signaling and contributes to maintenance of viral latency by targeting IKK epsilon. Cell Res 21, 793-806, doi: 10.1038/cr.2011.5 (2011).
44. Hou, J. et al. MicroRNA-146a feedback inhibits RIG-I-dependent type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J Immunol 183, 2150-2158, doi: 10.4049/jimmunol.0900707 (2009).
45. Zhou, H. B. et al. miR-155 and its star-form partner miR-155∗ cooperatively regulate type I interferon production by human plasmacytoid dendritic cells. Blood 116, 5885-5894, doi: 10.1182/blood-2010-04-280156 (2010).
46. Peng, W. Z., Ma, R., Wang, F., Yu, J. & Liu, Z. B. Role of miR-191/425 cluster in tumorigenesis and diagnosis of gastric cancer. Int J Mol Sci 15, 4031-4048, doi: 10.3390/ijms15034031 (2014).
47. Wang, S. F. et al. Loss of microRNA 122 expression in patients with hepatitis B enhances hepatitis B virus replication through cyclin G1-modulated P53 activity. Hepatology 55, 730-741, doi: 10.1002/hep.24809 (2012).
48. Gottwein, E. & Cullen, B. R. A Human Herpesvirus microRNA inhibits p21 expression and attenuates p21-mediated cell cycle arrest. J Virol 84, 5229-5237, doi: 10.1128/Jvi.00202-10 (2010).
49. Zhang, M., Xiao, Z. Z., Hu, Y. H. & Sun, L. Characterization of a megalocytivirus from cultured rock bream, Oplegnathus fasciatus (Temminck & Schlege), in China. Aquac Res 43, 556-564, doi: 10.1111/j.1365-2109.2011.02861.x (2012).
50. Zhang, J., Hu, Y. H., Sun, B. G., Xiao, Z. Z. & Sun, L. Selection of normalization factors for quantitative real time RT-PCR studies in Japanese flounder (Paralichthys olivaceus) and turbot (Scophthalmus maximus) under conditions of viral infection. Vet Immunol Immunop 152, 303-316, doi: 10.1016/j.vetimm.2012.12.018 (2013).
51. Zhang, B. C. & Sun, L. Tongue sole (Cynoglossus semilaevis) prothymosin alpha: cytokine-like activities associated with the intact protein and the C-terminal region that lead to antiviral immunity via Myd88-dependent and -independent pathways respectively. Dev Comp Immunol 53, 96-104, doi: 10.1016/j.dci.2015.07.004 (2015).
52. Tong, S. L., Li, H. & Miao, H. Z. The establishment and partial characterization of a continuous fish cell line FG-9307 from the gill of flounder Paralichthys olivaceus. Aquaculture 156, 327-333, doi: 10.1016/S0044-8486(97)00070-7 (1997).
53. Zhou, Z. X., Zhang, B. C. & Sun, L. Poly(I:C) induces antiviral immune responses in Japanese flounder (Paralichthys olivaceus) that require TLR3 and MDA5 and is negatively regulated by Myd88. Plos One 9, doi: ARTN e112918 10.1371/journal.pone.0112918 (2014).
54. Ohtani, M. et al. Transcriptional regulation of type I interferon gene expression by interferon regulatory factor-3 in Japanese flounder. Paralichthys olivaceus. Dev Comp Immunol 36, 697-706, doi: 10.1016/j.dci.2011.10.008 (2012).
55. Zhou, B. S. et al. MicroRNA-503 targets FGF2 and VEGFA and inhibits tumor angiogenesis and growth. Cancer Lett 333, 159-169, doi: 10.1016/j.canlet.2013.01.028 (2013).