Long noncoding RNA AANCR modulates innate antiviral responses by blocking miR-210-dependent MITA downregulation in teleost fish, Miichthys miiuy.


Journal

Science China. Life sciences
ISSN: 1869-1889
Titre abrégé: Sci China Life Sci
Pays: China
ID NLM: 101529880

Informations de publication

Date de publication:
Jul 2021
Historique:
received: 22 05 2020
accepted: 03 08 2020
pubmed: 1 10 2020
medline: 6 1 2022
entrez: 30 9 2020
Statut: ppublish

Résumé

Viral infection induces the initiation of antiviral effectors and cytokines which are critical mediators of innate antiviral responses. The critical molecular determinants are responsible for triggering an appropriate immune response. Long noncoding RNAs (lncRNAs) have emerged as new gene modulators involved in various biological processes, while how lncRNAs operate in lower vertebrates are still unknown. Here, we discover a long noncoding RNA, termed antiviral-associated long noncoding RNA (AANCR), as a novel regulator for innate antiviral responses in teleost fish. The results indicate that fish MITA plays an essential role in host antiviral responses and inhibition of Siniperca chuatsi rhabdovirus (SCRV) production. miR-210 reduces MITA expression and suppress MITA-mediated antiviral responses, which may help viruses evade host antiviral responses. Further, AANCR functions as a competing endogenous RNA (ceRNA) for miR-210 to control protein abundance of MITA, thereby inhibiting SCRV replication and promoting antiviral responses. Our data not only shed new light on understanding the function role of lncRNA in biological processes in teleost fish, but confirmed the hypothesis that ceRNA networks exist widely in vertebrates.

Identifiants

pubmed: 32997329
doi: 10.1007/s11427-020-1789-5
pii: 10.1007/s11427-020-1789-5
doi:

Substances chimiques

Antiviral Restriction Factors 0
MIRN210 microRNA, human 0
MicroRNAs 0
RNA, Long Noncoding 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1131-1148

Références

Aggad, D., Mazel, M., Boudinot, P., Mogensen, K.E., Hamming, O.J., Hartmann, R., Kotenko, S., Herbomel, P., Lutfalla, G., and Levraud, J.P. (2009). The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. J Immunol 183, 3924–3931.
pubmed: 19717522
Aguirre, S., Maestre, A.M., Pagni, S., Patel, J.R., Savage, T., Gutman, D., Maringer, K., Bernal-Rubio, D., Shabman, R.S., Simon, V., et al. (2012). DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog 8, e1002934.
pubmed: 23055924 pmcid: 3464218
Akira, S., Uematsu, S., and Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell 124, 783–801.
Biacchesi, S., LeBerre, M., Lamoureux, A., Louise, Y., Lauret, E., Boudinot, P., and Bremont, M. (2009). Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses. J Virol 83, 7815–7827.
pubmed: 19474100 pmcid: 2715792
Burdette, D.L., and Vance, R.E. (2013). STING and the innate immune response to nucleic acids in the cytosol. Nat Immunol 14, 19–26.
pubmed: 23238760
Burdette, D.L., Monroe, K.M., Sotelo-Troha, K., Iwig, J.S., Eckert, B., Hyodo, M., Hayakawa, Y., and Vance, R.E. (2011). STING is a direct innate immune sensor of cyclic di-GMP. Nature 478, 515–518.
pubmed: 21947006 pmcid: 3203314
Cesana, M., Cacchiarelli, D., Legnini, I., Santini, T., Sthandier, O., Chinappi, M., Tramontano, A., and Bozzoni, I. (2011). A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147, 358–369.
pubmed: 3234495 pmcid: 3234495
Chu, Q., Sun, Y., Bi, D., Cui, J., and Xu, T. (2017a). Up-regulated of miR-8159–5p and miR-217–5p by LPS stimulation negatively co-regulate TLR1 in miiuy croaker. Dev Comp Immunol 67, 117–125.
pubmed: 27832948
Chu, Q., Sun, Y., Cui, J., and Xu, T. (2017b). MicroRNA-3570 modulates the NF-κB pathway in teleost fish by targeting MyD88. J Immunol 198, 3274–3282.
pubmed: 28250156
Cullen, B.R. (2013). MicroRNAs as mediators of viral evasion of the immune system. Nat Immunol 14, 205–210.
pubmed: 23416678 pmcid: 3642974
Fitzgerald, K.A., McWhirter, S.M., Faia, K.L., Rowe, D.C., Latz, E., Golenbock, D.T., Coyle, A.J., Liao, S.M., and Maniatis, T. (2003). IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4, 491–496.
pubmed: 12692549
Fu, X., Lin, Q., Liang, H., Liu, L., Huang, Z., Li, N., and Su, J. (2017). The biological features and genetic diversity of novel fish rhabdovirus isolates in China. Arch Virol 162, 2829–2834.
pubmed: 28550433
Hansen, T.B., Jensen, T.I., Clausen, B.H., Bramsen, J.B., Finsen, B., Damgaard, C.K., and Kjems, J. (2013). Natural RNA circles function as efficient microRNA sponges. Nature 495, 384–388.
pubmed: 23446346 pmcid: 23446346
Harrow, J., Frankish, A., Gonzalez, J.M., Tapanari, E., Diekhans, M. Kokocinski, F., Aken, B.L., Barrell, D., Zadissa, A., Searle, S., et al. (2012). GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res 22, 1760–1774.
pubmed: 22955987 pmcid: 3431492
Ishikawa, H., Ma, Z., and Barber, G.N. (2009). STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788–792.
pubmed: 19776740 pmcid: 19776740
Jin, L., Hill, K.K., Filak, H., Mogan, J., Knowles, H., Zhang, B., Perraud, A.L., Cambier, J.C., and Lenz, L.L. (2011). MPYS is required for IFN response factor 3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. J Immunol 187, 2595–2601.
pubmed: 21813776
Komuro, A., and Horvath, C.M. (2006). RNA- and virus-independent inhibition of antiviral signaling by RNA helicase LGP2. J Virol 80, 12332–12342.
pubmed: 17020950 pmcid: 1676302
Kong, L., Zhang, Y., Ye, Z.Q., Liu, X.Q., Zhao, S.Q., Wei, L., and Gao, G. (2007). CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35, W345–W349.
pubmed: 17631615 pmcid: 1933232
Li, H., Gu, Z., Yang, L., Tian, Y., Kang, X., and Liu, X. (2018). Transcriptome profile analysis reveals an estrogen induced lncRNA associated with lipid metabolism and carcass traits in chickens (Gallus Gallus). Cell Physiol Biochem 50, 1638–1658.
pubmed: 30384372
Lin, Q., Zhao, Y., Fu, X., Liu, L., Liang, H., Niu, Y., Chen, X., Huang, Z., Lin, L., and Li, N. (2019). Development of strand-specific real-time RT-PCR for the analysis of SCRV transcription and replication dynamics. Microb Pathog 129, 146–151.
pubmed: 30731189
Liu, T.T., Yang, Q., Li, M., Zhong, B., Ran, Y., Liu, L.L., Yang, Y., Wang, Y.Y., and Shu, H.B. (2016). LSm14A plays a critical role in antiviral immune responses by regulating MITA level in a cell-specific manner. J Immunol 196, 5101–5111.
pubmed: 27183626
Liu, Y., Li, M., Fan, S., Lin, Y., Lin, B., Luo, F., Zhang, C., Chen, S., Li, Y., and Xu, A. (2010). A unique feature of Toll/IL-1 receptor domain-containing adaptor protein is partially responsible for lipopolysaccharide insensitivity in zebrafish with a highly conserved function of MyD88. J Immunol 185, 3391–3400.
pubmed: 20702732
Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2
pubmed: 11846609 pmcid: 11846609
Lu, S., Wang, T., Zhang, G., and He, Q.Y. (2020). Understanding the proteome encoded by “non-coding RNAs”: new insights into human genome. Sci China Life Sci 63, 986–995.
pubmed: 32318910
Ma, M., Cai, B., Jiang, L., Abdalla, B.A., Li, Z., Nie, Q., and Zhang, X. (2018). lncRNA-six1 is a target of miR-1611 that functions as a ceRNA to regulate six1 protein expression and fiber type switching in chicken myogenesis. Cells 7, 243.
pmcid: 6315877
Ma, M.Z., Chu, B.F., Zhang, Y., Weng, M.Z., Qin, Y.Y., Gong, W., and Quan, Z.W. (2015). Long non-coding RNA CCAT1 promotes gallbladder cancer development via negative modulation of miRNA-218–5p. Cell Death Dis 6, e1583.
pubmed: 25569100 pmcid: 4669740
Magnadóttir, B. (2006). Innate immunity of fish (overview). Fish Shellfish Immunol 20, 137–151.
pubmed: 15950491
Marques, A.C., and Ponting, C.P. (2014). Intergenic lncRNAs and the evolution of gene expression. Curr Opin Genets Dev 27, 48–53.
Mercer, T.R., Dinger, M.E., and Mattick, J.S. (2009). Long non-coding RNAs: insights into functions. Nat Rev Genet 10, 155–159.
pubmed: 19188922
Nesterova, T.B., Ya. Slobodyanyuk, S., Elisaphenko, E.A., Shevchenko, A. I., Johnston, C., Pavlova, M.E., Rogozin, I.B., Kolesnikov, N.N., Brockdorff, N., and Zakian, S.M. (2001). Characterization of the genomic Xist locus in rodents reveals conservation of overall gene structure and tandem repeats but rapid evolution of unique sequence. Genome Res 11, 833–849.
pubmed: 11337478 pmcid: 311126
Nitta, S., Sakamoto, N., Nakagawa, M., Kakinuma, S., Mishima, K., Kusano-Kitazume, A., Kiyohashi, K., Murakawa, M., Nishimura-Sakurai, Y., Azuma, S., et al. (2013). Hepatitis C virus NS4B protein targets STING and abrogates RIG-I-mediated type I interferon-dependent innate immunity. Hepatology 57, 46–58.
pubmed: 22911572
O’Neill, L.A.J., and Bowie, A.G. (2010). Sensing and signaling in antiviral innate immunity. Curr Biol 20, R328–R333.
pubmed: 20392426
Pang, K.C., Frith, M.C., and Mattick, J.S. (2006). Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genets 22, 1–5.
Pasquinelli, A.E., Reinhart, B.J., Slack, F., Martindale, M.Q., Kuroda, M.I., Maller, B., Hayward, D.C., Ball, E.E., Degnan, B., Müller, P., et al. (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86–89.
pubmed: 11081512
Ran, Y., Shu, H.B., and Wang, Y.Y. (2014). MITA/STING: a central and multifaceted mediator in innate immune response. Cytokine Growth Factor Rev 25, 631–639.
pubmed: 24929887 pmcid: 7108248
Sai, L., Qu, B., Zhang, J., Liu, J., Jia, Q., Bo, C Zhang, Y., Yu G., Han, R., and Peng, C. (2019). Analysis of long non-coding RNA involved in atrazine-induced testicular degeneration of Xenopus laevis. Environ Toxicol 34, 505–512.
pubmed: 30675760
Stefani, G., and Slack, F.J. (2008). Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 9, 219–230.
pubmed: 18270516
Sun, F., Zhang, Y.B., Liu, T.K., Shi, J., Wang, B., and Gui, J.F. (2011). Fish MITA serves as a mediator for distinct fish IFN gene activation dependent on IRF3 or IRF7. J Immunol 187, 2531–2539.
pubmed: 21795596
Sun, W., Li, Y., Chen, L., Chen, H., You, F., Zhou, X., Zhou, Y., Zhai, Z., Chen, D., and Jiang, Z. (2009). ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc Natl Acad Sci USA 106, 8653–8658.
pubmed: 19433799 pmcid: 2689030
Tao, J.J., Gui, J.F., and Zhang, Q.Y. (2007). Isolation and characterization of a rhabdovirus from co-infection of two viruses in mandarin fish. Aquaculture 262, 1–9.
Tsuchida, T., Zou, J., Saitoh, T., Kumar, H., Abe, T., Matsuura, Y., Kawai, T., and Akira, S. (2010). The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 33, 765–776.
pubmed: 21074459
van der Vaart, M., Spaink, H.P., and Meijer, A.H. (2012). Pathogen recognition and activation of the innate immune response in zebrafish. Adv Hematol 2012, 1–19.
Wang, J., Liu, X., Wu, H., Ni, P., Gu, Z., Qiao, Y., Chen, N., Sun, F., and Fan, Q. (2010). CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acids Res 38, 5366–5383.
pubmed: 20423907 pmcid: 2938198
Wang, K., Liu, F., Zhou, L.Y., Long, B., Yuan, S.M., Wang, Y., Liu, C.Y., Sun, T., Zhang, X.J., and Li, P.F. (2014). The long noncoding RNA CHRF regulates cardiac hypertrophy by targeting miR-489. Circ Res 114, 1377–1388.
pubmed: 24557880
Wang, Z.D., Shen, L.P., Chang, C., Zhang, X.Q., Chen, Z.M., Li, L., Chen, H., and Zhou, P.K. (2016). Long noncoding RNA lnc-RI is a new regulator of mitosis via targeting miRNA-210–3p to release PLK1 mRNA activity. Sci Rep 6, 25385.
pubmed: 27160062 pmcid: 4861912
Xu, L.G., Wang, Y.Y., Han, K.J., Li, L.Y., Zhai, Z., and Shu, H.B. (2005). VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol Cell 19, 727–740.
pubmed: 16153868
Xu, T., Chu, Q., and Cui, J. (2018a). Rhabdovirus-inducible microRNA-210 modulates antiviral innate immune response via targeting STING/MITA in fish. J Immunol 201, 982–994.
pubmed: 29967101
Xu, T., Chu, Q., Cui, J., and Bi, D. (2018b). Inducible microRNA-3570 feedback inhibits the RIG-I-dependent innate immune response to rhabdovirus in teleost fish by targeting MAVS/IPS-1. J Virol 92, e01594–17.
pubmed: 29093090 pmcid: 5752954
Yang, L., Froberg, J.E., and Lee, J.T. (2014). Long noncoding RNAs: fresh perspectives into the RNA world. Trends Biochem Sci 39, 35–43.
pubmed: 24290031
Yarbrough, M.L., Zhang, K., Sakthivel, R., Forst, C.V., Posner, B.A., Barber, G.N., White, M.A., and Fontoura, B.M.A. (2014). Primatespecific miR-576–3p sets host defense signalling threshold. Nat Commun 5, 4963.
pubmed: 25232931
Yoneyama, M., and Fujita, T. (2009). RNA recognition and signal transduction by RIG-I-like receptors. Immunol Rev 227, 54–65.
pubmed: 19120475
Zhang, J., Hu, M.M., Wang, Y.Y., and Shu, H.B. (2012). TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination. J Biol Chem 287, 28646–28655.
pubmed: 22745133 pmcid: 3436586
Zhang, J., Yu, P., Zhou, Q., Li, X., Ding, S., Su, S., Zhang, X., Yang, X., Zhou, W., Wan, Q., et al. (2018). Screening and characterisation of sex differentiation-related long non-coding RNAs in Chinese soft-shell turtle (Pelodiscus sinensis). Sci Rep 8, 8630.
pubmed: 29872091 pmcid: 5988831
Zhao, Y., Lin, Q., Li, N., Babu, V.S., Fu, X., Liu, L., Liang, H., Liu, X., and Lin, L. (2018). MicroRNAs profiles of Chinese Perch Brain (CPB) cells infected with Siniperca chuatsi rhabdovirus (SCRV). Fish Shellfish Immunol 84, 1075–1082.
pubmed: 30423456
Zhong, B., Yang, Y., Li, S., Wang, Y.Y., Li, Y., Diao, F., Lei, C., He, X., Zhang, L., Tien, P., et al. (2008). The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29, 538–550.
pubmed: 18818105
Zhou, Q., Lin, H., Wang, S., Wang, S., Ran, Y., Liu, Y., Ye, W., Xiong, X., Zhong, B., Shu, H.B., et al. (2014). The ER-associated protein ZDHHC1 is a positive regulator of DNA virus-triggered, MITA/STING-dependent innate immune signaling. Cell Host Microbe 16, 450–461.
pubmed: 25299331
Zhu, L., Nie, L., Zhu, G., Xiang, L., and Shao, J. (2013). Advances in research of fish immune-relevant genes: a comparative overview of innate and adaptive immunity in teleosts. Dev Comp Immunol 39, 39–62.
pubmed: 22504163

Auteurs

Qing Chu (Q)

Laboratory of Fish Molecular Immunology, College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, China.
Laboratory of Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China.

Tianjun Xu (T)

Laboratory of Fish Molecular Immunology, College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, China. tianjunxu@163.com.
Laboratory of Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China. tianjunxu@163.com.
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, 201306, China. tianjunxu@163.com.
National Pathogen Collection Center for Aquatic Animals, Shanghai Ocean University, Shanghai, 201306, China. tianjunxu@163.com.

Weiwei Zheng (W)

Laboratory of Fish Molecular Immunology, College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, China.
Laboratory of Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China.

Renjie Chang (R)

Laboratory of Fish Molecular Immunology, College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, China.

Lei Zhang (L)

Laboratory of Fish Molecular Immunology, College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, China.

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