The long noncoding RNA NEAT1 exerts antihantaviral effects by acting as positive feedback for RIG-I signaling

Journal of Virology

Volumn 91, Issue 9, 2017, Pages

  Ma, Hongwei ^a   Han, Peijun ^a   Ye, Wei ^a   Chen, Hesong ^a   Zheng, Xuyang ^b   Cheng, Linfeng ^a   Zhang, Liang ^a   Yu, Lan ^a   Wu, Xing'an ^a   Xu, Zhikai ^a   Lei, Yingfeng ^a   Zhang, Fanglin ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Beta interferon; DDX60; Hantaan virus; Innate immunity; Interferons; Long noncoding RNA; NEAT1; RIG I; SFPQ

Indexed keywords

BETA INTERFERON; INTERFERON REGULATORY FACTOR 7; LONG UNTRANSLATED RNA; NEAT1 PROTEIN; PROLINE RICH PROTEIN; REGULATOR PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; TRANSCRIPTOME; UNCLASSIFIED DRUG; DDX58 PROTEIN, HUMAN; DDX60 PROTEIN, HUMAN; DEAD BOX PROTEIN; NEAT1 LONG NON-CODING RNA, HUMAN; PTB ASSOCIATED SPLICING FACTOR; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; HANTAVIRUS INFECTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; VIRUS REPLICATION; VIRUS STRAIN; A-549 CELL LINE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CHLOROCEBUS AETHIOPS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HANTAAN VIRUS; HEK293 CELL LINE; HELA CELL LINE; IMMUNOLOGY; METABOLISM; RNA INTERFERENCE; TUMOR CELL LINE; VERO CELL LINE; VIROLOGY;

A549 CELLS; ANIMALS; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; DEAD BOX PROTEIN 58; DEAD-BOX RNA HELICASES; HANTAAN VIRUS; HANTAVIRUS INFECTIONS; HEK293 CELLS; HELA CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNITY, INNATE; INTERFERON-BETA; MALE; MICE; MICE, INBRED C57BL; PTB-ASSOCIATED SPLICING FACTOR; RNA INTERFERENCE; RNA, LONG NONCODING; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VERO CELLS; VIRUS REPLICATION;

EID: 85017571776     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02250-16     Document Type: Article

References (47)

1. Holmes EC, Zhang YZ. 2015. The evolution and emergence of hantaviruses. Curr Opin Virol 10:27-33. https://doi.org/10.1016/j.coviro.2014.12 .007
2. Vaheri A, Strandin T, Hepojoki J, Sironen T, Henttonen H, Makela S, Mustonen J. 2013. Uncovering the mysteries of hantavirus infections. Nat Rev Microbiol 11:539-550. https://doi.org/10.1038/nrmicro3066
3. Ma Y, Yuan B, Zhuang R, Zhang Y, Liu B, Zhang C, Zhang Y, Yu H, Yi J, Yang A, Jin B. 2015. Hantaan virus infection induces both Th1 and ThGranzyme B+ cell immune responses that associated with viral control and clinical outcome in humans. PLoS Pathog 11:e1004788. https://doi.org/10.1371/journal.ppat.1004788
4. Zhang WY, Wang LY, Liu YX, Yin WW, Hu WB, Magalhaes RJ, Ding F, Sun HL, Zhou H, Li SL, Haque U, Tong SL, Glass GE, Bi P, Clements AC, Liu QY, Li CY. 2014. Spatiotemporal transmission dynamics of hemorrhagic fever with renal syndrome in China, 2005-2012. PLoS Negl Trop Dis 8:e3344. https://doi.org/10.1371/journal.pntd.0003344
5. Lee MH, Lalwani P, Raftery MJ, Matthaei M, Lutteke N, Kirsanovs S, Binder M, Ulrich RG, Giese T, Wolff T, Kruger DH, Schonrich G. 2011. RNA helicase retinoic acid-inducible gene I as a sensor of Hantaan virus replication. J Gen Virol 92:2191-2200. https://doi.org/10.1099/vir.0.032367-0
6. Naganuma T, Hirose T. 2013. Paraspeckle formation during the biogenesis of long non-coding RNAs. RNA Biol 10:456-461. https://doi.org/10 .4161/rna.23547
7. XianGuo C, ZongYao H, Jun Z, Song F, GuangYue L, LiGang Z, KaiPing Z, YangYang Z, ChaoZhao L. 15 June 2016. Promoting progression and clinicopathological significance of NEAT1 over-expression in bladder cancer. Oncotarget https://doi.org/10.18632/oncotarget.10084
8. Sun C, Li S, Zhang F, Xi Y, Wang L, Bi Y, Li D. 2016. Long non-coding RNA NEAT1 promotes non-small cell lung cancer progression through regulation of miR-377-3p-E2F3 pathway. Oncotarget 7:51784-51814. https://doi.org/10.18632/oncotarget.10108
9. Ke H, Zhao L, Feng X, Xu H, Zou L, Yang Q, Su X, Peng L, Jiao B. 2016. NEAT1 is required for survival of breast cancer cells through FUS and miR-548. Gene Regul Syst Biol 10(Suppl 1):11-17. https://doi.org/10 .4137/GRSB.S29414
10. Adriaens C, Standaert L, Barra J, Latil M, Verfaillie A, Kalev P, Boeckx B, Wijnhoven PW, Radaelli E, Vermi W, Leucci E, Lapouge G, Beck B, van den Oord J, Nakagawa S, Hirose T, Sablina AA, Lambrechts D, Aerts S, Blanpain C, Marine JC. 2016. p53 induces formation of NEAT1 lncRNAcontaining paraspeckles that modulate replication stress response and chemosensitivity. Nat Med 22:861- 868. https://doi.org/10.1038/nm .4135
11. Imamura K, Imamachi N, Akizuki G, Kumakura M, Kawaguchi A, Nagata K, Kato A, Kawaguchi Y, Sato H, Yoneda M, Kai C, Yada T, Suzuki Y, Yamada T, Ozawa T, Kaneki K, Inoue T, Kobayashi M, Kodama T, Wada Y, Sekimizu K, Akimitsu N. 2014. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol Cell 53:393- 406. https://doi.org/10.1016/j.molcel.2014.01.009
12. Kraus AA, Raftery MJ, Giese T, Ulrich R, Zawatzky R, Hippenstiel S, Suttorp N, Kruger DH, Schonrich G. 2004. Differential antiviral response of endothelial cells after infection with pathogenic and nonpathogenic hantaviruses. J Virol 78:6143- 6150. https://doi.org/10.1128/JVI.78.12.6143-6150.2004
13. Jonsson CB, Figueiredo LT, Vapalahti O. 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23: 412-441. https://doi.org/10.1128/CMR.00062-09
14. Matthys VS, Cimica V, Dalrymple NA, Glennon NB, Bianco C, Mackow ER. 2014. Hantavirus GnT elements mediate TRAF3 binding and inhibit RIG-I/TBK1-directed beta interferon transcription by blocking IRF3 phosphorylation. J Virol 88:2246-2259. https://doi.org/10.1128/JVI.02647-13
15. Yu HT, Jiang H, Zhang Y, Nan XP, Li Y, Wang W, Jiang W, Yang DQ, Su WJ, Wang JP, Wang PZ, Bai XF. 2012. Hantaan virus triggers TLR4-dependent innate immune responses. Viral Immunol 25:387-393. https://doi.org/10 .1089/vim.2012.0005
16. Handke W, Oelschlegel R, Franke R, Kruger DH, Rang A. 2009. Hantaan virus triggers TLR3-dependent innate immune responses. J Immunol 182:2849-2858. https://doi.org/10.4049/jimmunol.0802893
17. Goubau D, van der Veen AG, Chakravarty P, Lin R, Rogers N, Rehwinkel J, Deddouche S, Rosewell I, Hiscott J, Reis ESC. 2015. Mouse superkiller- 2-like helicase DDX60 is dispensable for type I IFN induction and immunity to multiple viruses. Eur J Immunol 45:3386-3403. https://doi.org/10.1002/eji.201545794
18. Oshiumi H, Miyashita M, Okamoto M, Morioka Y, Okabe M, Matsumoto M, Seya T. 2015. DDX60 is involved in RIG-I-dependent and independent antiviral responses, and its function is attenuated by virus-induced EGFR activation. Cell Rep 11:1193-1207. https://doi.org/10.1016/j.celrep.2015 .04.047
19. Zhang Y, Cao X. 2016. Long noncoding RNAs in innate immunity. Cell Mol Immunol 13:138-147. https://doi.org/10.1038/cmi.2015.68
20. Carpenter S, Aiello D, Atianand MK, Ricci EP, Gandhi P, Hall LL, Byron M, Monks B, Henry-Bezy M, Lawrence JB, O'Neill LA, Moore MJ, Caffrey DR, Fitzgerald KA. 2013. A long noncoding RNA mediates both activation and repression of immune response genes. Science 341:789-792. https://doi.org/10.1126/science.1240925
21. Li Z, Chao TC, Chang KY, Lin N, Patil VS, Shimizu C, Head SR, Burns JC, Rana TM. 2014. The long noncoding RNA THRIL regulates TNFalpha expression through its interaction with hnRNPL. Proc Natl Acad Sci U S A 111:1002-1007. https://doi.org/10.1073/pnas.1313768111
22. IIott NE, Heward JA, Roux B, Tsitsiou E, Fenwick PS, Lenzi L, Goodhead I, Hertz-Fowler C, Heger A, Hall N, Donnelly LE, Sims D, Lindsay MA. 2014. Long non-coding RNAs and enhancer RNAs regulate the lipopolysaccharide- induced inflammatory response in human monocytes. Nat Commun 5:3979. https://doi.org/10.1038/ncomms4979
23. Rapicavoli NA, Qu K, Zhang J, Mikhail M, Laberge RM, Chang HY. 2013. A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. eLife 2:e00762. https://doi.org/10.7554/eLife.00762
24. Zhang Q, Chen CY, Yedavalli VS, Jeang KT. 2013. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. mBio 4:e00596-12. https://doi.org/10.1128/mBio.00596-12
25. Ouyang J, Zhu X, Chen Y, Wei H, Chen Q, Chi X, Qi B, Zhang L, Zhao Y, Gao GF, Wang G, Chen JL. 2014. NRAV, a long noncoding RNA, modulates antiviral responses through suppression of interferon-stimulated gene transcription. Cell Host Microbe 16:616-626. https://doi.org/10 .1016/j.chom.2014.10.001
26. Kambara H, Niazi F, Kostadinova L, Moonka DK, Siegel CT, Post AB, Carnero E, Barriocanal M, Fortes P, Anthony DD, Valadkhan S. 2014. Negative regulation of the interferon response by an interferon-induced long non-coding RNA. Nucleic Acids Res 42:10668-10680. https://doi .org/10.1093/nar/gku713
27. Gomez JA, Wapinski OL, Yang YW, Bureau JF, Gopinath S, Monack DM, Chang HY, Brahic M, Kirkegaard K. 2013. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell 152:743-754. https://doi.org/10.1016/j.cell.2013.01.015
28. Barriocanal M, Carnero E, Segura V, Fortes P. 2014. Long non-coding RNA BST2/BISPR is induced by IFN and regulates the expression of the antiviral factor tetherin. Front Immunol 5:655. https://doi.org/10.3389/fimmu.2014.00655
29. Sunwoo JS, Lee ST, Im W, Lee M, Byun JI, Jung KH, Park KI, Jung KY, Lee SK, Chu K, Kim M. 25 May 2016. Altered expression of the long noncoding RNA NEAT1 in Huntington's disease. Mol Neurobiol. Epub ahead of print
30. Zhang F, Wu L, Qian J, Qu B, Xia S, La T, Wu Y, Ma J, Zeng J, Guo Q, Cui Y, Yang W, Huang J, Zhu W, Yao Y, Shen N, Tang Y. 2016. Identification of the long noncoding RNA NEAT1 as a novel inflammatory regulator acting through MAPK pathway in human lupus. J Autoimmun 75: 96-104. https://doi.org/10.1016/j.jaut.2016.07.012
31. Miyashita M, Oshiumi H, Matsumoto M, Seya T. 2011. DDX60, a DEXD/H box helicase, is a novel antiviral factor promoting RIG-I-like receptormediated signaling. Mol Cell Biol 31:3802-3819. https://doi.org/10.1128/MCB.01368-10
32. Jiang H, Du H, Wang LM, Wang PZ, Bai XF. 2016. Hemorrhagic fever with renal syndrome: pathogenesis and clinical picture. Front Cell Infect Microbiol 6:1
33. Jiang H, Wang PZ, Zhang Y, Xu Z, Sun L, Wang LM, Huang CX, Lian JQ, Jia ZS, Li ZD, Bai XF. 2008. Hantaan virus induces toll-like receptor 4 expression, leading to enhanced production of beta interferon, interleukin-6 and tumor necrosis factor-alpha. Virology 380:52-59. https://doi.org/10.1016/j.virol.2008.07.002
34. Lee HW, Cho HJ. 1981. Electron microscope appearance of Hantaan virus, the causative agent of Korean haemorrhagic fever. Lancet i: 1070-1072
35. Hamada C, Sato NL, Niimura S, Kato A, Fujisawa N, Maeda Y, Kumanishi T, Lee HW. 1986. Growth experiment of Hantaan virus in A549 cells: an attempt to improve the immunofluorescent antibody technique for hemorrhagic fever with renal syndrome. Jikken Dobutsu 35:1-9
36. Nam JH, Hwang KA, Yu CH, Kang TH, Shin JY, Choi WY, Kim IB, Joo YR, Cho HW, Park KY. 2003. Expression of interferon inducible genes following Hantaan virus infection as a mechanism of resistance in A549 cells. Virus Genes 26:31-38. https://doi.org/10.1023/A:1022373904357
37. Park SW, Han MG, Park C, Ju YR, Ahn BY, Ryou J. 2013. Hantaan virus nucleocapsid protein stimulates MDM2-dependent p53 degradation. J Gen Virol 94:2424-2428. https://doi.org/10.1099/vir.0.054312-0
38. Levine JR, Prescott J, Brown KS, Best SM, Ebihara H, Feldmann H. 2010. Antagonism of type I interferon responses by new world hantaviruses. J Virol 84:11790-11801. https://doi.org/10.1128/JVI.00916-10
39. Prescott J, Hall P, Acuna-Retamar M, Ye C, Wathelet MG, Ebihara H, Feldmann H, Hjelle B. 2010. New World hantaviruses activate IFNlambda production in type I IFN-deficient Vero E6 cells. PLoS One 5:e11159. https://doi.org/10.1371/journal.pone.0011159
40. Markotic A, Hensley L, Geisbert T, Spik K, Schmaljohn C. 2003. Hantaviruses induce cytopathic effects and apoptosis in continuous human embryonic kidney cells. J Gen Virol 84:2197-2202. https://doi.org/10 .1099/vir.0.19090-0
41. Jin M, Park J, Lee S, Park B, Shin J, Song KJ, Ahn TI, Hwang SY, Ahn BY, Ahn K. 2002. Hantaan virus enters cells by clathrin-dependent receptormediated endocytosis. Virology 294:60-69. https://doi.org/10.1006/viro .2001.1303
42. Kandasamy M, Suryawanshi A, Tundup S, Perez JT, Schmolke M, Manicassamy S, Manicassamy B. 2016. RIG-I signaling is critical for efficient polyfunctional T cell responses during influenza virus infection. PLoS Pathog 12:e1005754. https://doi.org/10.1371/journal.ppat.1005754
43. Xu Z, Wei L, Wang L, Wang H, Jiang S. 2002. The in vitro and in vivo protective activity of monoclonal antibodies directed against Hantaan virus: potential application for immunotherapy and passive immuniza- tion. Biochem Biophys Res Commun 298:552-558. https://doi.org/10 .1016/S0006-291X(02)02491-9
44. Bosco A, Wiehler S, Proud D. 2016. Interferon regulatory factor 7 regulates airway epithelial cell responses to human rhinovirus infection. BMC Genomics 17:76. https://doi.org/10.1186/s12864-016-2405-z
45. Ye W, Xu Y, Wang Y, Dong Y, Xi Q, Cao M, Yu L, Zhang L, Cheng L, Wu X, Xu Z, Lei Y, Zhang F. 2015. Hantaan virus can infect human keratinocytes and activate an interferon response through the nuclear translocation of IRF-3. Infect Genet Evol 29:146-155. https://doi.org/10.1016/j .meegid.2014.11.009
46. Yi J, Xu Z, Zhuang R, Wang J, Zhang Y, Ma Y, Liu B, Zhang Y, Zhang C, Yan G, Zhang F, Xu Z, Yang A, Jin B. 2013. Hantaan virus RNA load in patients having hemorrhagic fever with renal syndrome: correlation with disease severity. J Infect Dis 207:1457-1461. https://doi.org/10.1093/infdis/jis475
47. Cheng L, Yu L, Wu X, Li K, Wang F, Zhang L, Ye W, Li P, Zhang F, Xu Z. 2014. Induction of specific humoral and cellular immune responses in a mouse model following gene fusion of HSP70C and Hantaan virus Gn and S0.7 in an adenoviral vector. PLoS One 9:e88183. https://doi.org/10 .1371/journal.pone.0088183