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Research Article

NSUN2-mediated m5C methylation of IRF3 mRNA negatively regulates type I interferon responses during various viral infections

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Article: 2178238 | Received 28 Dec 2022, Accepted 04 Feb 2023, Published online: 20 Feb 2023

References

  • Roundtree IA, Evans ME, Pan T, et al. Dynamic RNA modifications in gene expression regulation. Cell. 2017 Jun 15;169(7):1187–1200.
  • Dezi V, Ivanov C, Haussmann IU, et al. Nucleotide modifications in messenger RNA and their role in development and disease. Biochem Soc Trans. 2016 Oct 15;44(5):1385–1393.
  • Trixl L, Lusser A. The dynamic RNA modification 5-methylcytosine and its emerging role as an epitranscriptomic mark. Wiley Interdiscip Rev RNA. 2019 Jan;10(1):e1510.
  • Chellamuthu A, Gray SG. The RNA methyltransferase NSUN2 and Its potential roles in cancer. Cells. 2020 Jul 22;9(8):1758.
  • Yang Y, Hsu PJ, Chen YS, et al. Dynamic transcriptomic m(6)A decoration: writers, erasers, readers and functions in RNA metabolism. Cell Res. 2018 Jun;28(6):616–624.
  • Cao G, Li HB, Yin Z, et al. Recent advances in dynamic m6A RNA modification. Open Biol. 2016 Apr;6(4):160003.
  • Yang J, Wang H, Zhang W. Regulation of virus replication and T cell homeostasis by N(6)-methyladenosine. Virol Sin. 2019 Feb;34(1):22–29.
  • Han D, Liu J, Chen C, et al. Anti-tumour immunity controlled through mRNA m(6)A methylation and YTHDF1 in dendritic cells. Nature. 2019 Feb;566(7743):270–274.
  • Frye M, Harada BT, Behm M, et al. RNA modifications modulate gene expression during development. Science. 2018 Sep 28;361(6409):1346–1349.
  • Winkler R, Gillis E, Lasman L, et al. M6a modification controls the innate immune response to infection by targeting type I interferons (vol 20, pg 173, 2018). Nat Immunol. 2019 Feb;20(2):243–243.
  • Rubio RM, Depledge DP, Bianco C, et al. RNA m(6) A modification enzymes shape innate responses to DNA by regulating interferon beta. Genes Dev. 2018 Dec 1;32(23-24):1472–1484.
  • Liu Y, You Y, Lu Z, et al. N6-methyladenosine RNA modification–mediated cellular metabolism rewiring inhibits viral replication. Science. 2019;365(6458):1171–1176.
  • Zheng Q, Hou J, Zhou Y, et al. The RNA helicase DDX46 inhibits innate immunity by entrapping m(6)A-demethylated antiviral transcripts in the nucleus. Nat Immunol. 2017 Oct;18(10):1094–1103.
  • Qin F, Cai B, Zhao J, et al. Methyltransferase-Like protein 14 attenuates mitochondrial antiviral signaling protein expression to negatively regulate antiviral immunity via N(6) -methyladenosine modification. Adv Sci (Weinh. 2021 Aug;8(15):e2100606.
  • Wang L, Wen M, Cao X. Nuclear hnRNPA2B1 initiates and amplifies the innate immune response to DNA viruses. Science. 2019;365(6454):eaav0758.
  • Squires JE, Patel HR, Nousch M, et al. Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res. 2012 Jun;40(11):5023–5033.
  • Tuorto F, Liebers R, Musch T, et al. RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nat Struct Mol Biol. 2012 Sep;19(9):900–905.
  • Zhang X, Liu Z, Yi J, et al. The tRNA methyltransferase NSun2 stabilizes p16INK(4) mRNA by methylating the 3'-untranslated region of p16. Nat Commun. 2012 Mar 6;3:712.
  • Mei L, Shen C, Miao R, et al. RNA methyltransferase NSUN2 promotes gastric cancer cell proliferation by repressing p57(Kip2) by an m(5)C-dependent manner. Cell Death Dis. 2020 Apr 24;11(4):270.
  • Tang H, Fan X, Xing J, et al. NSun2 delays replicative senescence by repressing p27 (KIP1) translation and elevating CDK1 translation. Aging (Albany NY). 2015 Dec;7(12):1143–1158.
  • Li Q, Li X, Tang H, et al. NSUN2-Mediated m5c methylation and METTL3/METTL14-mediated m6A methylation cooperatively enhance p21 translation. J Cell Biochem. 2017 Sep;118(9):2587–2598.
  • Schumann U, Zhang HN, Sibbritt T, et al. Multiple links between 5-methylcytosine content of mRNA and translation. BMC Biol. 2020 Apr 15;18(1):40.
  • Yang X, Yang Y, Sun BF, et al. 5-methylcytosine promotes mRNA export-NSUN2 as the methyltransferase and ALYREF as an m(5)C reader. Cell Res. 2017 May;27(5):606–625.
  • Chen X, Li A, Sun BF, et al. 5-methylcytosine promotes pathogenesis of bladder cancer through stabilizing mRNAs. Nat Cell Biol. 2019 Aug;21(8):978–990.
  • Yang Y, Wang L, Han X, et al. RNA 5-Methylcytosine facilitates the maternal-to-zygotic transition by preventing maternal mRNA decay. Mol Cell. 2019 Sep 19;75(6):1188–1202. e11.
  • Zou F, Tu R, Duan B, et al. Drosophila YBX1 homolog YPS promotes ovarian germ line stem cell development by preferentially recognizing 5-methylcytosine RNAs. Proc Natl Acad Sci U S A. 2020 Feb 18;117(7):3603–3609.
  • Eckwahl M, Xu R, Michalkiewicz J, et al. 5-Methylcytosine RNA modifications promote retrovirus replication in an ALYREF reader protein-dependent manner. J Virol. 2020 Jun 16;94(13):e00544-20.
  • Honda K, Takaoka A, Taniguchi T. Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity. 2006 Sep;25(3):349–360.
  • Ablasser A, Hur S. Regulation of cGAS- and RLR-mediated immunity to nucleic acids. Nat Immunol. 2019;21(1):17–29.
  • Fitzgerald KA, Kagan JC. Toll-like receptors and the control of immunity. Cell. 2020 Mar 19;180(6):1044–1066.
  • Rehwinkel J, Gack MU. RIG-I-like receptors: their regulation and roles in RNA sensing. Nat Rev Immunol. 2020 Sep;20(9):537–551.
  • Honda K, Taniguchi T. IRFs: master regulators of signalling by toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol. 2006 Sep;6(9):644–658.
  • Wu J, Chen ZJ. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol. 2014;32:461–488.
  • Tamura T, Yanai H, Savitsky D, et al. The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol. 2008;26:535–584.
  • Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol. 2014;32:513–545.
  • Li S, Zhu M, Pan R, et al. The tumor suppressor PTEN has a critical role in antiviral innate immunity. Nat Immunol. 2016 Mar;17(3):241–249.
  • Mancino A, Natoli G. Specificity and function of IRF family transcription factors: insights from genomics. J Interferon Cytokine Res. 2016 Jul;36(7):462–469.
  • Cao Y, Wang H, Yang L, et al. PTEN-L promotes type I interferon responses and antiviral immunity. Cell Mol Immunol. 2018 Jan;15(1):48–57.
  • Zhou Y, Li M, Xue Y, et al. Interferon-inducible cytoplasmic lncLrrc55-AS promotes antiviral innate responses by strengthening IRF3 phosphorylation. Cell Res. 2019 Aug;29(8):641–654.
  • Xia Z, Xu G, Yang X, et al. Inducible TAP1 negatively regulates the antiviral innate immune response by targeting the TAK1 complex. J Immunol. 2017 May 1;198(9):3690–3704.
  • Xiong Y, Liu Y, Cao L, et al. Transcriptomic characteristics of bronchoalveolar lavage fluid and peripheral blood mononuclear cells in COVID-19 patients. Emerg Microbes Infect. 2020 Dec;9(1):761–770.
  • Courtney DG, Tsai K, Bogerd HP, et al. Epitranscriptomic addition of m(5)C to HIV-1 transcripts regulates viral gene expression. Cell Host Microbe. 2019 Aug 14;26(2):217–227. e6.
  • Subtelny AO, Eichhorn SW, Chen GR, et al. Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature. 2014 Apr 3;508(7494):66–71.
  • Li X, Xiong X, Wang K, et al. Transcriptome-wide mapping reveals reversible and dynamic N(1)-methyladenosine methylome. Nat Chem Biol. 2016 May;12(5):311–316.
  • Pollex T, Hanna K, Schaefer M. Detection of cytosine methylation in RNA using bisulfite sequencing. Cold Spring Harb Protoc. 2010 Oct 1;2010(10). pdb prot5505.
  • Schaefer M, Pollex T, Hanna K, et al. RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res. 2009 Feb;37(2):e12.
  • Su R, Fan LH, Cao C, et al. Global profiling of RNA-binding protein target sites by LACE-seq. Nat Cell Biol. 2021 Jun;23(6):664–675.
  • Yuan S, Tang H, Xing J, et al. Methylation by NSun2 represses the levels and function of microRNA 125b. Mol Cell Biol. 2014 Oct 1;34(19):3630–3641.
  • Huai W, Liu X, Wang C, et al. KAT8 selectively inhibits antiviral immunity by acetylating IRF3. J Exp Med. 2019 Apr 1;216(4):772–785.
  • Wang P, Zhao W, Zhao K, et al. TRIM26 negatively regulates interferon-beta production and antiviral response through polyubiquitination and degradation of nuclear IRF3. PLoS Pathog. 2015 Mar;11(3):e1004726.
  • Wang H, Zhang L, Zeng C, et al. NSUN2-mediated m5c methylation of IRF3 mRNA negatively regulates type I interferon responses. bioRxiv. 2021:2021.07.09.451748.
  • Zhang Y, Zhang LS, Dai Q, et al. 5-methylcytosine (m(5)C) RNA modification controls the innate immune response to virus infection by regulating type I interferons. Proc Natl Acad Sci U S A. 2022 Oct 18;119(42):e2123338119.
  • Moon HJ, Redman KL. Trm4 and Nsun2 RNA:m5C methyltransferases form metabolite-dependent, covalent adducts with previously methylated RNA. Biochemistry. 2014 Nov 18;53(45):7132–7144.
  • Wang X, Lu Z, Gomez A, et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature. 2014 Jan 2;505(7481):117–120.
  • Shi H, Wang X, Lu Z, et al. YTHDF3 facilitates translation and decay of N(6)-methyladenosine-modified RNA. Cell Res. 2017 Mar;27(3):315–328.
  • Wang X, Zhao BS, Roundtree IA, et al. N(6)-methyladenosine modulates messenger RNA translation efficiency. Cell. 2015 Jun 4;161(6):1388–1399.
  • Xiao W, Adhikari S, Dahal U, et al. Nuclear m(6)A reader YTHDC1 regulates mRNA splicing. Mol Cell. 2016 Feb 18;61(4):507–519.
  • Huang T, Chen W, Liu J, et al. Genome-wide identification of mRNA 5-methylcytosine in mammals. Nat Struct Mol Biol. 2019 May;26(5):380–388.