Epigenetic regulation in antiviral innate immunity

Xiao Wang, Huawei Xia, Shengde Liu, Lili Cao, Fuping You, Xiao Wang, Huawei Xia, Shengde Liu, Lili Cao, Fuping You

Abstract

Emerging life-threatening viruses have posed great challenges to public health. It is now increasingly clear that epigenetics plays a role in shaping host-virus interactions and there is a great need for a more thorough understanding of these intricate interactions through the epigenetic lens, which may represent potential therapeutic opportunities in the clinic. In this review, we highlight the current understanding of the roles of key epigenetic regulators - chromatin remodeling and histone modification - in modulating chromatin openness during host defense against virus. We also discuss how the RNA modification m6A (N6-methyladenosine) affects fundamental aspects of host-virus interactions. We conclude with future directions for uncovering more detailed functions that epigenetic regulation exerts on both host cells and viruses during infection.

Keywords: Antiviral innate immunity; Chromatin remodeling; Epigenetics; Histone modification; m6A.

© 2021 Wiley-VCH GmbH.

References

    1. Carty, M., Guy, C. and Bowie, A. G., Detection of viral infections by innate immunity. Biochem. Pharmacol. 2021. 183: 114316.
    1. Schoggins, J. W., Interferon-stimulated genes: what do they all do? Annu. Rev. Virol. 2019. 6: 567-584.
    1. Zhang, Q. and Cao, X., Epigenetic regulation of the innate immune response to infection. Nat. Rev. Immunol. 2019. 19: 417-432.
    1. Tsai, K. and Cullen, B. R., Epigenetic and epitranscriptomic regulation of viral replication. Nat. Rev. Microbiol. 2020. 18: 559-570.
    1. Cavalli, G. and Heard, E., Advances in epigenetics link genetics to the environment and disease. Nature. 2019. 571: 489-499.
    1. Kelsey, G., Stegle, O. and Reik, W., Single-cell epigenomics: recording the past and predicting the future. Science. 2017. 358: 69-75.
    1. Wang, K. C. and Chang, H. Y., Epigenomics: technologies and applications. Circ. Res. 2018. 122: 1191-1199.
    1. Allis, C. D. and Jenuwein, T., The molecular hallmarks of epigenetic control. Nat. Rev. Genet. 2016. 17: 487-500.
    1. Gómez-Díaz, E., Jordà, M., Peinado, M. A. and Rivero, A., Epigenetics of host-pathogen interactions: the road ahead and the road behind. PLoS Pathog. 2012. 8: e1003007.
    1. Roundtree, I. A., Evans, M. E., Pan, T. and He, C., Dynamic RNA modifications in gene expression regulation. Cell. 2017. 169: 1187-1200.
    1. Kaplan, N., Moore, I. K., Fondufe-Mittendorf, Y., Gossett, A. J., Tillo, D., Field, Y., LeProust, E. M., Hughes, T. R., Lieb, J. D., Widom, J. et al., The DNA-encoded nucleosome organization of a eukaryotic genome. Nature. 2009. 458: 362-366.
    1. Richmond, T. J. and Davey, C. A., The structure of DNA in the nucleosome core. Nature. 2003. 423: 145-150.
    1. Segal, E. and Widom, J., What controls nucleosome positions? Trends Genet. 2009. 25: 335-343.
    1. Mellor, J., The dynamics of chromatin remodeling at promoters. Mol. Cell. 2005. 19: 147-157.
    1. Cairns, B. R., Chromatin remodeling: insights and intrigue from single-molecule studies. Nat. Struct. Mol. Biol. 2007. 14: 989-996.
    1. Wang, W., Côté, J., Xue, Y., Zhou, S., Khavari, P. A., Biggar, S. R., Muchardt, C., et al., Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 1996. 15: 5370-5382.
    1. Ho, L. and Crabtree, G. R., Chromatin remodelling during development. Nature. 2010. 463: 474-484.
    1. Mashtalir, N., D'Avino, A. R., Michel, B. C., Luo, J., Pan, J., Otto, J. E., Zullow, H. J., et al., Modular organization and assembly of SWI/SNF family chromatin remodeling complexes. Cell. 2018. 175: 1272-1288.
    1. Li, P. and Leonard, W. J., Chromatin accessibility and interactions in the transcriptional regulation of T cells. Front. Immunol. 2018. 9: 2738.
    1. Kim, T. K. and Maniatis, T., The mechanism of transcriptional synergy of an in vitro assembled interferon-beta enhanceosome. Mol. Cell. 1997. 1: 119-129.
    1. Agalioti, T., Lomvardas, S., Parekh, B., Yie, J., Maniatis, T. and Thanos, D., Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter. Cell. 2000. 103: 667-678.
    1. Lee, D., Sohn, H., Kalpana, G. V. and Choe, J., Interaction of E1 and hSNF5 proteins stimulates replication of human papillomavirus DNA. Nature. 1999. 399: 487-491.
    1. Cha, S. and Seo, T., hSNF5 is required for human papillomavirus E2-driven transcriptional activation and DNA replication. Intervirology. 2011. 54: 66-77.
    1. Gwack, Y., Baek, H. J., Nakamura, H., Lee, S. H., Meisterernst, M., Roeder, R. G. and Jung, J. U., Principal role of TRAP/mediator and SWI/SNF complexes in Kaposi's sarcoma-associated herpesvirus RTA-mediated lytic reactivation. Mol. Cell. Biol. 2003. 23: 2055-2067.
    1. Kalpana, G. V., Marmon, S., Wang, W., Crabtree, G. R. and Goff, S. P., Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science. 1994. 266: 2002-2006.
    1. Ariumi, Y., Serhan, F., Turelli, P., Telenti, A. and Trono, D., The integrase interactor 1 (INI1) proteins facilitate Tat-mediated human immunodeficiency virus type 1 transcription. Retrovirology. 2006. 3: 47.
    1. Agbottah, E., Deng, L., Dannenberg, L. O., Pumfery, A. and Kashanchi, F., Effect of SWI/SNF chromatin remodeling complex on HIV-1 Tat activated transcription. Retrovirology. 2006. 3: 48.
    1. Mahmoudi, T., Parra, M., Vries, R. G., Kauder, S. E., Verrijzer, C. P., Ott, M. and Verdin, E., The SWI/SNF chromatin-remodeling complex is a cofactor for Tat transactivation of the HIV promoter. J. Biol. Chem. 2006. 281: 19960-19968.
    1. Tréand, C., du Chéné, I., Brès, V., Kiernan, R., Benarous, R., Benkirane, M. and Emiliani, S., Requirement for SWI/SNF chromatin-remodeling complex in Tat-mediated activation of the HIV-1 promoter. EMBO J. 2006. 25: 1690-1699.
    1. Maroun, M., Delelis, O., Coadou, G., Bader, T., Ségéral, E., Mbemba, G., Petit, C., et al., Inhibition of early steps of HIV-1 replication by SNF5/Ini1. J. Biol. Chem. 2006. 281: 22736-22743.
    1. Ferrari, R., Gou, D., Jawdekar, G., Johnson, S. A., Nava, M., Su, T., Yousef, A. F., et al., Adenovirus small E1A employs the lysine acetylases p300/CBP and tumor suppressor Rb to repress select host genes and promote productive virus infection. Cell Host Microbe. 2014. 16: 663-676.
    1. Nevins, J. R., Ginsberg, H. S., Blanchard, J. M., Wilson, M. C. and Darnell J. E., Jr. Regulation of the primary expression of the early adenovirus transcription units. J. Virol. 1979. 32: 727-733.
    1. Berk, A. J. and Sharp, P. A., Structure of the adenovirus 2 early mRNAs. Cell. 1978. 14: 695-711.
    1. Frisch, S. M. and Mymryk, J. S., Adenovirus-5 E1A: paradox and paradigm. Nat. Rev. Mol. Cell Biol. 2002. 3: 441-452.
    1. Ray-Gallet, D., Quivy, J. P., Scamps, C., Martini, E. M., Lipinski, M. and Almouzni, G., HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell. 2002. 9: 1091-1100.
    1. Tagami, H., Ray-Gallet, D., Almouzni, G. and Nakatani, Y., Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell. 2004. 116: 51-61.
    1. Rai, T. S., Glass, M., Cole, J. J., Rather, M. I., Marsden, M., Neilson, M., Brock, C., et al., Histone chaperone HIRA deposits histone H3.3 onto foreign viral DNA and contributes to anti-viral intrinsic immunity. Nucleic. Acids. Res. 2017. 45: 11673-11683.
    1. Lallemand-Breitenbach, V. and de Thé, H., PML nuclear bodies: from architecture to function. Curr. Opin. Cell Biol. 2018. 52: 154-161.
    1. Lusic, M., Marini, B., Ali, H., Lucic, B., Luzzati, R. and Giacca, M., Proximity to PML nuclear bodies regulates HIV-1 latency in CD4+ T cells. Cell Host Microbe. 2013. 13: 665-677.
    1. Cohen, C., Corpet, A., Roubille, S., Maroui, M. A., Poccardi, N., Rousseau, A., Kleijwegt, C., et al., Promyelocytic leukemia (PML) nuclear bodies (NBs) induce latent/quiescent HSV-1 genomes chromatinization through a PML NB/Histone H3.3/H3.3 Chaperone Axis. PLoS Pathog. 2018. 14: e1007313.
    1. Nozawa, R. S., Boteva, L., Soares, D. C., Naughton, C., Dun, A. R., Buckle, A., Ramsahoye, B., et al., SAF-A regulates interphase chromosome structure through oligomerization with chromatin-associated rnas. Cell. 2017. 169: 1214-1227.
    1. Zhang, L., Song, D., Zhu, B. and Wang, X., The role of nuclear matrix protein HNRNPU in maintaining the architecture of 3D genome. Semin. Cell Dev. Biol. 2019. 90: 161-167.
    1. Fan, H., Lv, P., Huo, X., Wu, J., Wang, Q., Cheng, L., Liu, Y., et al., The nuclear matrix protein HNRNPU maintains 3D genome architecture globally in mouse hepatocytes. Genome Res. 2018. 28: 192-202.
    1. Cao, L., Liu, S., Li, Y., Yang, G., Luo, Y., Li, S., Du, H., Zhao, Y., et al., The nuclear matrix protein SAFA surveils viral RNA and facilitates immunity by activating antiviral enhancers and super-enhancers. Cell Host Microbe. 2019. 26: 369-384.
    1. Strahl, B. D. and Allis, C. D., The language of covalent histone modifications. Nature. 2000. 403: 41-45.
    1. Brownell, J. E., Zhou, J., Ranalli, T., Kobayashi, R., Edmondson, D. G., Roth, S. Y. and Allis, C. D., Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell. 1996. 84: 843-851.
    1. Bannister, A. J. and Kouzarides, T., Regulation of chromatin by histone modifications. Cell Res. 2011. 21: 381-395.
    1. Handy, D. E., Castro, R. and Loscalzo, J., Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation. 2011. 123: 2145-2156.
    1. Ptaschinski, C., Mukherjee, S., Moore, M. L., Albert, M., Helin, K., Kunkel, S. L. and Lukacs, N. W., RSV-induced H3K4 demethylase KDM5B leads to regulation of dendritic cell-derived innate cytokines and exacerbates pathogenesis in vivo. PLoS Pathog. 2015. 11: e1004978.
    1. Meng, J., Liu, X., Zhang, P., Li, D., Xu, S., Zhou, Q., Guo, M., et al., Rb selectively inhibits innate IFN-β production by enhancing deacetylation of IFN-β promoter through HDAC1 and HDAC8. J. Autoimmun. 2016. 73: 42-53.
    1. Ea, C. K., Hao, S., Yeo, K. S. and Baltimore, D., EHMT1 protein binds to nuclear factor-κB p50 and represses gene expression. J. Biol. Chem. 2012. 287: 31207-31217.
    1. Schliehe, C., Flynn, E. K., Vilagos, B., Richson, U., Swaminanthan, S., Bosnjak, B., Bauer, L., et al., The methyltransferase Setdb2 mediates virus-induced susceptibility to bacterial superinfection. Nat. Immunol. 2015. 16: 67-74.
    1. Menachery, V. D., Eisfeld, A. J., Schäfer, A., Josset, L., Sims, A. C., Proll, S., Fan, S., et al., Pathogenic influenza viruses and coronaviruses utilize similar and contrasting approaches to control interferon-stimulated gene responses. mBio. 2014. 5: e01174-01114.
    1. Fonseca, G. J., Thillainadesan, G., Yousef, A. F., Ablack, J. N., Mossman, K. L., Torchia, J. and Mymryk, J. S., Adenovirus evasion of interferon-mediated innate immunity by direct antagonism of a cellular histone posttranslational modification. Cell Host Microbe. 2012. 11: 597-606.
    1. Parekh, B. S. and Maniatis, T., Virus infection leads to localized hyperacetylation of histones H3 and H4 at the IFN-beta promoter. Mol. Cell. 1999. 3: 125-129.
    1. Sun, D., Cao, X. and Wang, C., Polycomb chromobox Cbx2 enhances antiviral innate immunity by promoting JMJD3-mediated demethylation of H3K27 at the Ifnb promoter. Protein Cell. 2019. 10: 285-294.
    1. Chen, K., Liu, J., Liu, S., Xia, M., Zhang, X., Han, D., Jiang, Y., et al.,. Methyltransferase SETD2-mediated methylation of STAT1 is critical for interferon antiviral activity. Cell. 2017. 170: 492-506.
    1. Roy, A., Ghosh, A., Kumar, B. and Chandran, B., IFI16, a nuclear innate immune DNA sensor, mediates epigenetic silencing of herpesvirus genomes by its association with H3K9 methyltransferases SUV39H1 and GLP. Elife. 2019. 8: e49500.
    1. Orzalli, M. H., Conwell, S. E., Berrios, C., DeCaprio, J. A. and Knipe, D. M., Nuclear interferon-inducible protein 16 promotes silencing of herpesviral and transfected DNA. Proc. Natl. Acad. Sci. U.S.A. 2013. 110: E4492-4501.
    1. Johnson, K. E., Bottero, V., Flaherty, S., Dutta, S., Singh, V. V. and Chandran, B., IFI16 restricts HSV-1 replication by accumulating on the hsv-1 genome, repressing HSV-1 gene expression, and directly or indirectly modulating histone modifications. PLoS Pathog. 2014. 10: e1004503.
    1. Lo Cigno, I., De Andrea, M., Borgogna, C., Albertini, S., Landini, M. M., Peretti, A., Johnson, K. E., et al.,. The nuclear DNA sensor IFI16 acts as a restriction factor for human papillomavirus replication through epigenetic modifications of the viral promoters. J. Virol. 2015. 89: 7506-7520.
    1. Hong, X., Kim, E. S. and Guo, H., Epigenetic regulation of hepatitis B virus covalently closed circular DNA: implications for epigenetic therapy against chronic hepatitis B. Hepatology. 2017. 66: 2066-2077.
    1. Yuan, Y., Zhao, K., Yao, Y., Liu, C., Chen, Y., Li, J., Wang, Y., et al., HDAC11 restricts HBV replication through epigenetic repression of cccDNA transcription. Antiviral Res. 2019. 172: 104619.
    1. Ren, J. H., Hu, J. L., Cheng, S. T., Yu, H. B., Wong, V. K. W., Law, B. Y. K., Yang, Y. F., et al., SIRT3 restricts hepatitis B virus transcription and replication through epigenetic regulation of covalently closed circular DNA involving suppressor of variegation 3-9 homolog 1 and SET domain containing 1A histone methyltransferases. Hepatology. 2018. 68: 1260-1276.
    1. Gordon, D. E., Jang, G. M., Bouhaddou, M., Xu, J., Obernier, K., White, K. M., O'Meara, M. J., et al., A SARS-CoV-2 protein interaction map reveals targets for drug repurposing. Nature. 2020. 583: 459-468.
    1. Xiao, W., Adhikari, S., Dahal, U., Chen, Y. S., Hao, Y. J., Sun, B. F., Sun, H. Y., et al., Nuclear m(6)A reader YTHDC1 regulates mRNA splicing. Mol. Cell. 2016. 61: 507-519.
    1. Wang, X., Lu, Z., Gomez, A., Hon, G. C., Yue, Y., Han, D., Fu, Y., et al., N6-methyladenosine-dependent regulation of messenger RNA stability. Nature. 2014. 505: 117-120.
    1. Wang, X., Zhao, B. S., Roundtree, I. A., Lu, Z., Han, D., Ma, H., Weng, X., et al., N(6)-methyladenosine modulates messenger RNA translation efficiency. Cell. 2015. 161: 1388-1399.
    1. Shi, H., Wang, X., Lu, Z., Zhao, B. S., Ma, H., Hsu, P. J., Liu, C. and He, C., YTHDF3 facilitates translation and decay of N(6)-methyladenosine-modified RNA. Cell Res. 2017. 27: 315-328.
    1. Liu, N., Dai, Q., Zheng, G., He, C., Parisien, M. and Pan, T., N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature. 2015. 518: 560-564.
    1. Liu, J., Yue, Y., Han, D., Wang, X., Fu, Y., Zhang, L., Jia, G., et al., A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation. Nat. Chem. Biol. 2014. 10: 93-95.
    1. Ping, X. L., Sun, B. F., Wang, L., Xiao, W., Yang, X., Wang, W. J., Adhikari, S., et al., Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase. Cell Res. 2014. 24: 177-189.
    1. Patil, D. P., Chen, C. K., Pickering, B. F., Chow, A., Jackson, C., Guttman, M. and Jaffrey, S. R., m(6)A RNA methylation promotes XIST-mediated transcriptional repression. Nature. 2016. 537: 369-373.
    1. Wen, J., Lv, R., Ma, H., Shen, H., He, C., Wang, J., Jiao, F., et al., Zc3h13 Regulates nuclear RNA m(6)A methylation and mouse embryonic stem cell self-renewal. Mol. Cell. 2018. 69: 1028-1038.
    1. Schwartz, S., Mumbach, M. R., Jovanovic, M., Wang, T., Maciag, K., Bushkin, G. G., Mertins, P., et al., Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5' sites. Cell Rep. 2014. 8: 284-296.
    1. Jia, G., Fu, Y., Zhao, X., Dai, Q., Zheng, G., Yang, Y., Yi, C., et al., N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat. Chem. Biol. 2011. 7: 885-887.
    1. Zheng, G., Dahl, J. A., Niu, Y., Fedorcsak, P., Huang, C. M., Li, C. J., Vågbø, C. B., et al., ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol. Cell. 2013. 49: 18-29.
    1. Xu, C., Liu, K., Ahmed, H., Loppnau, P., Schapira, M. and Min, J., Structural basis for the discriminative recognition of N6-methyladenosine RNA by the human YT521-B homology domain family of proteins. J. Biol. Chem. 2015. 290: 24902-24913.
    1. Li, F., Zhao, D., Wu, J. and Shi, Y., Structure of the YTH domain of human YTHDF2 in complex with an m(6)A mononucleotide reveals an aromatic cage for m(6)A recognition. Cell Res. 2014. 24: 1490-1492.
    1. Hsu, P. J., Zhu, Y., Ma, H., Guo, Y., Shi, X., Liu, Y., Qi, M., et al., YTHDC2 is an N(6)-methyladenosine binding protein that regulates mammalian spermatogenesis. Cell Res. 2017. 27: 1115-1127.
    1. Canaani, D., Kahana, C., Lavi, S. and Groner, Y., Identification and mapping of N6-methyladenosine containing sequences in simian virus 40 RNA. Nucleic. Acids. Res. 1979. 6: 2879-2899.
    1. Krug, R. M., Morgan, M. A. and Shatkin, A. J., Influenza viral mRNA contains internal N6-methyladenosine and 5'-terminal 7-methylguanosine in cap structures. J. Virol. 1976. 20: 45-53.
    1. Furuichi, Y., Shatkin, A. J., Stavnezer, E. and Bishop, J. M., Blocked, methylated 5'-terminal sequence in avian sarcoma virus RNA. Nature. 1975. 257: 618-620.
    1. Hao, H., Hao, S., Chen, H., Chen, Z., Zhang, Y., Wang, J., Wang, H., et al., N6-methyladenosine modification and METTL3 modulate enterovirus 71 replication. Nucleic. Acids. Res. 2019. 47: 362-374.
    1. Courtney, D. G., Kennedy, E. M., Dumm, R. E., Bogerd, H. P., Tsai, K., Heaton, N. S. and Cullen, B. R., Epitranscriptomic enhancement of influenza A virus gene expression and replication. Cell Host Microbe 2017. 22: 377-386.
    1. Lichinchi, G., Gao, S., Saletore, Y., Gonzalez, G. M., Bansal, V., Wang, Y., Mason, C. E. and Rana, T. M., Dynamics of the human and viral m(6)A RNA methylomes during HIV-1 infection of T cells. Nat Microbiol. 2016. 1: 16011.
    1. Kennedy, E. M., Bogerd, H. P., Kornepati, A. V., Kang, D., Ghoshal, D., Marshall, J. B., Poling, B. C., Tsai, K., et al., Posttranscriptional m(6)A editing of HIV-1 mRNAs enhances viral gene expression. Cell Host Microbe. 2016. 19: 675-685.
    1. Tsai, K., Courtney, D. G. and Cullen, B. R. Addition of m6A to SV40 late mRNAs enhances viral structural gene expression and replication. PLoS Pathog. 2018. 14: e1006919.
    1. Ye, F., Chen, E. R. and Nilsen, T. W. Kaposi's sarcoma-associated herpesvirus utilizes and manipulates RNA N(6)-adenosine methylation to promote lytic replication. J. Virol. 2017. 91.
    1. Lu, M., Zhang, Z., Xue, M., Zhao, B. S., Harder, O., Li, A., Liang, X., et al., N(6)-methyladenosine modification enables viral RNA to escape recognition by RNA sensor RIG-I. Nat Microbiol. 2020. 5: 584-598.
    1. Karikó, K., Buckstein, M., Ni, H. and Weissman, D., Suppression of RNA recognition by Toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity 2005. 23: 165-175.
    1. Durbin, A. F., Wang, C., Marcotrigiano, J. and Gehrke, L., RNAs containing modified nucleotides fail to trigger RIG-I conformational changes for innate immune signaling. mBio. 2016. 7.
    1. Rubio, R. M., Depledge, D. P., Bianco, C., Thompson, L. and Mohr, I., RNA m(6) A modification enzymes shape innate responses to DNA by regulating interferon β. Genes Dev. 2018. 32: 1472-1484.
    1. Winkler, R., Gillis, E., Lasman, L., Safra, M., Geula, S., Soyris, C., Nachshon, A., et al., m(6)A modification controls the innate immune response to infection by targeting type I interferons. Nat. Immunol. 2019. 20: 173-182.
    1. Zheng, Q., Hou, J., Zhou, Y., Li, Z. and Cao, X., The RNA helicase DDX46 inhibits innate immunity by entrapping m(6)A-demethylated antiviral transcripts in the nucleus. Nat. Immunol. 2017. 18: 1094-1103.
    1. Wang, L., Wen, M. and Cao, X., Nuclear hnRNPA2B1 initiates and amplifies the innate immune response to DNA viruses. Science. 2019. 365: eaav0758.
    1. Liu, Y., You, Y., Lu, Z., Yang, J., Li, P., Liu, L., Xu, H., et al., N (6)-methyladenosine RNA modification-mediated cellular metabolism rewiring inhibits viral replication. Science. 2019. 365: 1171-1176.
    1. Gokhale, N. S., McIntyre, A. B. R., McFadden, M. J., Roder, A. E., Kennedy, E. M., Gandara, J. A., Hopcraft, S. E., Quicke, K. M., et al., N6-methyladenosine in flaviviridae viral RNA genomes regulates infection. Cell Host Microbe. 2016. 20: 654-665.
    1. Lichinchi, G., Zhao, B. S., Wu, Y., Lu, Z., Qin, Y., He, C. and Rana, T. M., Dynamics of human and viral RNA methylation during Zika virus infection. Cell Host Microbe. 2016. 20: 666-673.
    1. Liu, J., Xu, Y. P., Li, K., Ye, Q., Zhou, H. Y., Sun, H., Li, X., et al., The m(6)A methylome of SARS-CoV-2 in host cells. Cell Res. 2021. 31: 404-414.
    1. Goldberg, A. D., Allis, C. D. and Bernstein, E., Epigenetics: a landscape takes shape. Cell. 2007. 128: 635-638.
    1. Balakrishnan, L. and Milavetz, B., Epigenetic regulation of viral biological processes. Viruses. 2017. 9: 346.
    1. Lin, W. N., Tay, M. Z., Lu, R., Liu, Y., Chen, C. H. and Cheow, L. F., The role of single-cell technology in the study and control of infectious diseases. Cells. 2020. 9: 1440.
    1. Williams, G. D., Gokhale, N. S. and Horner, S. M., Regulation of viral infection by the RNA modification N6-methyladenosine. Annu Rev Virol. 2019. 6: 235-253.

Source: PubMed

3
Subskrybuj