MicroRNA-15b modulates Japanese encephalitis virus-mediated inflammation via targeting RNF125

Journal of Immunology

Volumn 195, Issue 5, 2015, Pages 2251-2262

  Zhu, Bibo ^a   Ye, Jing ^a   Nie, Yanru ^a   Ashraf, Usama ^a   Zohaib, Ali ^a   Duan, Xiaodong ^a   Fu, Zhen F ^a,b   Song, Yunfeng ^a   Chen, Huanchun ^a   Cao, Shengbo ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 6; MICRORNA 15B; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; REGULATOR PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; RING FINGER PROTEIN 125; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; AUTACOID; CYTOKINE; MICRORNA; MIRN15 MICRORNA, HUMAN; MIRN15 MICRORNA, MOUSE; RNF125 PROTEIN, HUMAN; RNF125 PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; GLIA CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOREGULATION; IN VITRO STUDY; INTRACELLULAR SIGNALING; JAPANESE ENCEPHALITIS; JAPANESE ENCEPHALITIS VIRUS; LETHALITY; MOUSE; NERVE CELL LESION; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; UPREGULATION; VIRUS LOAD; 3' UNTRANSLATED REGION; ANIMAL; BAGG ALBINO MOUSE; BRAIN; CELL LINE; GENETICS; HELA CELL LINE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INFLAMMATION; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; VIROLOGY; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; ANIMALS; BLOTTING, WESTERN; BRAIN; CELL LINE; CELL LINE, TUMOR; CYTOKINES; ENCEPHALITIS VIRUS, JAPANESE; ENCEPHALITIS, JAPANESE; GENE EXPRESSION REGULATION; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MICE, INBRED BALB C; MICRORNAS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; UBIQUITIN-PROTEIN LIGASES;

EID: 84940118692     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500370     Document Type: Article

References (63)

1. Cook, D. N., D. S. Pisetsky, and D. A. Schwartz. 2004. Toll-like receptors in the pathogenesis of human disease. Nat. Immunol. 5: 975-979.
2. Misra, U. K., and J. Kalita. 2010. Overview: Japanese encephalitis. Prog. Neurobiol. 91: 108-120.
3. van den Hurk, A. F., S. A. Ritchie, and J. S. Mackenzie. 2009. Ecology and geographical expansion of Japanese encephalitis virus. Annu. Rev. Entomol. 54: 17-35.
4. Mackenzie, J. S., D. J. Gubler, and L. R. Petersen. 2004. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat. Med. 10(12, Suppl.)S98-S109.
5. Erlanger, T. E., S. Weiss, J. Keiser, J. Utzinger, and K. Wiedenmayer. 2009. Past, present, and future of Japanese encephalitis. Emerg. Infect. Dis. 15: 1-7.
6. Ghoshal, A., S. Das, S. Ghosh, M. K. Mishra, V. Sharma, P. Koli, E. Sen, and A. Basu. 2007. Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia 55: 483-496.
7. Chen, C. J., J. H. Chen, S. Y. Chen, S. L. Liao, and S. L. Raung. 2004. Upregulation of RANTES gene expression in neuroglia by Japanese encephalitis virus infection. J. Virol. 78: 12107-12119.
8. Chen, C. J., S. L. Liao, M. D. Kuo, and Y. M. Wang. 2000. Astrocytic alteration induced by Japanese encephalitis virus infection. Neuroreport 11: 1933-1937.
9. Olson, J. K., and S. D. Miller. 2004. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J. Immunol. 173: 3916-3924.
10. Thongtan, T., P. Cheepsunthorn, V. Chaiworakul, C. Rattanarungsan, N. Wikan, and D. R. Smith. 2010. Highly permissive infection of microglial cells by Japanese encephalitis virus: a possible role as a viral reservoir. Microbes Infect. 12: 37-45.
11. Bhowmick, S., R. Duseja, S. Das, M. B. Appaiahgiri, S. Vrati, and A. Basu. 2007. Induction of IP-10 (CXCL10) in astrocytes following Japanese encephalitis. Neurosci. Lett. 414: 45-50.
12. Bartel, D. P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
13. Friedman, R. C., K. K. Farh, C. B. Burge, and D. P. Bartel. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19: 92-105.
14. Chen, J. F., E. M. Mandel, J. M. Thomson, Q. Wu, T. E. Callis, S. M. Hammond, F. L. Conlon, and D. Z. Wang. 2006. The role of microRNA-1 and microRNA- 133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38: 228-233.
15. Lu, J., G. Getz, E. A. Miska, E. Alvarez-Saavedra, J. Lamb, D. Peck, A. Sweet- Cordero, B. L. Ebert, R. H. Mak, A. A. Ferrando, et al. 2005. MicroRNA expression profiles classify human cancers. Nature 435: 834-838.
16. Guo, C. J., Q. Pan, D. G. Li, H. Sun, and B. W. Liu. 2009. miR-15b and miR-16 are implicated in activation of the rat hepatic stellate cell: An essential role for apoptosis. J. Hepatol. 50: 766-778.
17. Cullen, B. R. 2013. MicroRNAs as mediators of viral evasion of the immune system. Nat. Immunol. 14: 205-210.
18. Li, Y., and X. Shi. 2013. MicroRNAs in the regulation of TLR and RIG-I pathways. Cell. Mol. Immunol. 10: 65-71.
19. Hou, J., P. Wang, L. Lin, X. Liu, F. Ma, H. An, Z. Wang, and X. Cao. 2009. MicroRNA-146a feedback inhibits RIG-I-dependent type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J. Immunol. 183: 2150-2158.
20. Chen, Y., J. Chen, H.Wang, J. Shi, K. Wu, S. Liu, Y. Liu, and J. Wu. 2013. HCVinduced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1. PLoS Pathog. 9: e1003248.
21. Lu, F., A. Weidmer, C. G. Liu, S. Volinia, C. M. Croce, and P. M. Lieberman. 2008. Epstein-Barr virus-induced miR-155 attenuates NF-kappaB signaling and stabilizes latent virus persistence. J. Virol. 82: 10436-10443.
22. Taganov, K. D., M. P. Boldin, K. J. Chang, and D. Baltimore. 2006. NF-kappaBdependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. USA 103: 12481-12486.
23. Ceppi, M., P. M. Pereira, I. Dunand-Sauthier, E. Barras, W. Reith, M. A. Santos, and P. Pierre. 2009. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. USA 106: 2735-2740.
24. Chen, Y., W. Liu, T. Sun, Y. Huang, Y. Wang, D. K. Deb, D. Yoon, J. Kong, R. Thadhani, and Y. C. Li. 2013. 1,25-Dihydroxyvitamin D promotes negative feedback regulation of TLR signaling via targeting microRNA-155-SOCS1 in macrophages. J. Immunol. 190: 3687-3695.
25. Yue, J., and G. Tigyi. 2010. Conservation of miR-15a/16-1 and miR-15b/16-2 clusters. Mamm. Genome 21: 88-94.
26. Chung, G. E., J. H. Yoon, S. J. Myung, J. H. Lee, S. H. Lee, S. M. Lee, S. J. Kim, S. Y. Hwang, H. S. Lee, and C. Y. Kim. 2010. High expression of microRNA-15b predicts a low risk of tumor recurrence following curative resection of hepatocellular carcinoma. Oncol. Rep. 23: 113-119.
27. Satzger, I., A. Mattern, U. Kuettler, D. Weinspach, B. Voelker, A. Kapp, and R. Gutzmer. 2010. MicroRNA-15b represents an independent prognostic parameter and is correlated with tumor cell proliferation and apoptosis in malignant melanoma. Int. J. Cancer 126: 2553-2562.
28. Cimmino, A., G. A. Calin, M. Fabbri, M. V. Iorio, M. Ferracin, M. Shimizu, S. E. Wojcik, R. I. Aqeilan, S. Zupo, M. Dono, et al. 2005. miR-15 and miR-16 induce apoptosis by targeting BCL2. [Published erratum appears in 2006 Proc. Natl. Acad. Sci. USA 103: 2464.] Proc. Natl. Acad. Sci. USA 102: 13944-13949.
29. Xia, L., D. Zhang, R. Du, Y. Pan, L. Zhao, S. Sun, L. Hong, J. Liu, and D. Fan. 2008. miR-15b and miR-16 modulate multidrug resistance by targeting BCL2 in human gastric cancer cells. Int. J. Cancer 123: 372-379.
30. Dai, X., W. Zhang, H. Zhang, S. Sun, H. Yu, Y. Guo, Z. Kou, G. Zhao, L. Du, S. Jiang, et al. 2014. Modulation of HBV replication by microRNA-15b through targeting hepatocyte nuclear factor 1a. Nucleic Acids Res. 42: 6578-6590.
31. Lv, X., H. Jiang, Y. Liu, X. Lei, and J. Jiao. 2014. MicroRNA-15b promotes neurogenesis and inhibits neural progenitor proliferation by directly repressing TET3 during early neocortical development. EMBO Rep. 15: 1305-1314.
32. Chen, Z., L. Shao, J. Ye, Y. Li, S. Huang, H. Chen, and S. Cao. 2012. Monoclonal antibodies against NS3 and NS5 proteins of Japanese encephalitis virus. Hybridoma (Larchmt) 31: 137-141.
33. Xu, Z., S. B. Xiao, P. Xu, Q. Xie, L. Cao, D. Wang, R. Luo, Y. Zhong, H. C. Chen, and L. R. Fang. 2011. miR-365, a novel negative regulator of interleukin-6 gene expression, is cooperatively regulated by Sp1 and NF-kappaB. J. Biol. Chem. 286: 21401-21412.
34. Arimoto, K., H. Takahashi, T. Hishiki, H. Konishi, T. Fujita, and K. Shimotohno. 2007. Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc. Natl. Acad. Sci. USA 104: 7500-7505.
35. Hwang, S. Y., K. Y. Hur, J. R. Kim, K. H. Cho, S. H. Kim, and J. Y. Yoo. 2013. Biphasic RLR-IFN-b response controls the balance between antiviral immunity and cell damage. J. Immunol. 190: 1192-1200.
36. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5: 730-737.
37. Cao, S., Y. Li, J. Ye, X. Yang, L. Chen, X. Liu, and H. Chen. 2011. Japanese encephalitis virus wild strain infection suppresses dendritic cells maturation and function, and causes the expansion of regulatory T cells. Virol. J. 8: 39.
38. Ye, J., R. Jiang, M. Cui, B. Zhu, L. Sun, Y. Wang, A. Zohaib, Q. Dong, X. Ruan, Y. Song, et al. 2014. Etanercept reduces neuroinflammation and lethality in mouse model of Japanese encephalitis. J. Infect. Dis. 210: 875-889.
39. Mori, Y., T. Okabayashi, T. Yamashita, Z. Zhao, T. Wakita, K. Yasui, F. Hasebe, M. Tadano, E. Konishi, K. Moriishi, and Y. Matsuura. 2005. Nuclear localization of Japanese encephalitis virus core protein enhances viral replication. J. Virol. 79: 3448-3458.
40. Wang, H., M. Chiu, Z. Xie, M. Chiu, Z. Liu, P. Chen, S. Liu, J. C. Byrd, N. Muthusamy, R. Garzon, et al. 2012. Synthetic microRNA cassette dosing: pharmacokinetics, tissue distribution and bioactivity. Mol. Pharm. 9: 1638-1644.
41. Xu, L. J., Y. B. Ouyang, X. Xiong, C. M. Stary, and R. G. Giffard. 2015. Poststroke treatment with miR-181 antagomir reduces injury and improves long-term behavioral recovery in mice after focal cerebral ischemia. Exp. Neurol. 264: 1-7.
42. Thounaojam, M. C., K. Kundu, D. K. Kaushik, S. Swaroop, A. Mahadevan, S. K. Shankar, and A. Basu. 2014. MicroRNA 155 regulates Japanese encephalitis virus-induced inflammatory response by targeting Src homology 2-containing inositol phosphatase 1. J. Virol. 88: 4798-4810.
43. Zhu, B., J. Ye, P. Lu, R. Jiang, X. Yang, Z. F. Fu, H. Chen, and S. Cao. 2012. Induction of antigen-specific immune responses in mice by recombinant baculovirus expressing premembrane and envelope proteins of West Nile virus. Virol. J. 9: 132.
44. Dave, R. S., and K. Khalili. 2010. Morphine treatment of human monocytederived macrophages induces differential miRNA and protein expression: impact on inflammation and oxidative stress in the central nervous system. J. Cell. Biochem. 110: 834-845.
45. Das, S., M. K. Mishra, J. Ghosh, and A. Basu. 2008. Japanese Encephalitis Virus infection induces IL-18 and IL-1βeta in microglia and astrocytes: correlation with in vitro cytokine responsiveness of glial cells and subsequent neuronal death. J. Neuroimmunol. 195: 60-72.
46. Nazmi, A., K. Dutta, and A. Basu. 2011. RIG-I mediates innate immune response in mouse neurons following Japanese encephalitis virus infection. PLoS One 6: e21761.
47. Rehmsmeier, M., P. Steffen, M. Hochsmann, and R. Giegerich. 2004. Fast and effective prediction of microRNA/target duplexes. RNA 10: 1507-1517.
48. Krek, A., D. Grün, M. N. Poy, R. Wolf, L. Rosenberg, E. J. Epstein, P. MacMenamin, I. da Piedade, K. C. Gunsalus, M. Stoffel, and N. Rajewsky. 2005. Combinatorial microRNA target predictions. Nat. Genet. 37: 495-500.
49. John, B., A. J. Enright, A. Aravin, T. Tuschl, C. Sander, and D. S. Marks. 2004. Human MicroRNA targets. [Published erratum appears in 2005 PLoS Biol. 3: e264.] PLoS Biol. 2: e363.
50. Oshiumi, H., M. Matsumoto, and T. Seya. 2012. Ubiquitin-mediated modulation of the cytoplasmic viral RNA sensor RIG-I. J. Biochem. 151: 5-11.
51. Zohaib, A., X. Duan, B. Zhu, J. Ye, S. Wan, H. Chen, X. Liu, and S. Cao. 2015. The Role of Ubiquitination in Regulation of Innate Immune Signaling. Curr. Issues Mol. Biol. 18: 1-10.
52. Chen, C. J., Y. C. Ou, S. Y. Lin, S. L. Raung, S. L. Liao, C. Y. Lai, S. Y. Chen, and J. H. Chen. 2010. Glial activation involvement in neuronal death by Japanese encephalitis virus infection. J. Gen. Virol. 91: 1028-1037.
53. Pareek, S., S. Roy, B. Kumari, P. Jain, A. Banerjee, and S. Vrati. 2014. MiR-155 induction in microglial cells suppresses Japanese encephalitis virus replication and negatively modulates innate immune responses. J. Neuroinflammation 11: 97.
54. Thounaojam, M. C., D. K. Kaushik, K. Kundu, and A. Basu. 2014. MicroRNA-29b modulates Japanese encephalitis virus-induced microglia activation by targeting tumor necrosis factor alpha-induced protein 3. J. Neurochem. 129: 143-154.
55. Nazmi, A., R. Mukhopadhyay, K. Dutta, and A. Basu. 2012. STING mediates neuronal innate immune response following Japanese encephalitis virus infection. Sci. Rep. 2: 347.
56. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
57. Oshiumi, H., M. Miyashita, N. Inoue, M. Okabe, M. Matsumoto, and T. Seya. 2010. The ubiquitin ligase Riplet is essential for RIG-I-dependent innate immune responses to RNA virus infection. Cell Host Microbe 8: 496-509.
58. Kim, M. J., S. Y. Hwang, T. Imaizumi, and J. Y. Yoo. 2008. Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J. Virol. 82: 1474-1483.
59. Rosenberger, C. M., R. L. Podyminogin, G. Navarro, G. W. Zhao, P. S. Askovich, M. J. Weiss, and A. Aderem. 2012. miR-451 regulates dendritic cell cytokine responses to influenza infection. J. Immunol. 189: 5965-5975.
60. Chen, S. T., R. S. Liu, M. F. Wu, Y. L. Lin, S. Y. Chen, D. T. Tan, T. Y. Chou, I. S. Tsai, L. Li, and S. L. Hsieh. 2012. CLEC5A regulates Japanese encephalitis virus-induced neuroinflammation and lethality. PLoS Pathog. 8: e1002655.
61. Mishra, M. K., and A. Basu. 2008. Minocycline neuroprotects, reduces microglial activation, inhibits caspase 3 induction, and viral replication following Japanese encephalitis. J. Neurochem. 105: 1582-1595.
62. Swarup, V., J. Ghosh, S. Ghosh, A. Saxena, and A. Basu. 2007. Antiviral and anti-inflammatory effects of rosmarinic acid in an experimental murine model of Japanese encephalitis. Antimicrob. Agents Chemother. 51: 3367-3370.
63. Das, S., K. Dutta, K. L. Kumawat, A. Ghoshal, D. Adhya, and A. Basu. 2011. Abrogated inflammatory response promotes neurogenesis in a murine model of Japanese encephalitis. PLoS One 6: e17225.