How to cite this WIREs title:
WIREs RNA

Impact Factor: 6.846

Epitranscriptomic marks: Emerging modulators of RNA virus gene expression

Advanced Review

Rachel Netzband, Cara T. Pager

Published Online: Nov 06 2019

DOI: 10.1002/wrna.1576

Full article on Wiley Online Library: HTML PDF

Can't access this content? Tell your librarian.

Abstract Epitranscriptomics, the study of posttranscriptional chemical moieties placed on RNA, has blossomed in recent years. This is due in part to the emergence of high‐throughput detection methods as well as the burst of discoveries showing biological function of select chemical marks. RNA modifications have been shown to affect RNA structure, localization, and functions such as alternative splicing, stabilizing transcripts, nuclear export, cap‐dependent and cap‐independent translation, microRNA biogenesis and binding, RNA degradation, and immune regulation. As such, the deposition of chemical marks on RNA has the unique capability to spatially and temporally regulate gene expression. The goal of this article is to present the exciting convergence of the epitranscriptomic and virology fields, specifically the deposition and biological impact of N7‐methylguanosine, ribose 2′‐O‐methylation, pseudouridine, inosine, N6‐methyladenosine, and 5‐methylcytosine epitranscriptomic marks on gene expression of RNA viruses. This article is categorized under: RNA in Disease and Development > RNA in Disease RNA Interactions with Proteins and Other Molecules > Protein–RNA Interactions: Functional Implications

5′‐Cap on messenger RNA (mRNA). (a) Schematic of N7‐methylguanosine cap attached to nucleotides 1 and 2 of RNA that are 2′‐O‐methylated. (b) Overview of the canonical pathway for installation of Cap 0, Cap 1, and Cap 2 structures at the 5′‐end of an mRNA. The functional significance of the Cap 0, Cap 1, and Cap 2 are shown

[ Normal View | Magnified View ]

Viruses with N6‐methyladenosine (m⁶A) modifications in the viral RNA, and putative functions. Virus families shown include: Flaviviridae (purple) namely hepatitis C virus (HCV), Zika virus (ZIKV), Dengue virus (DENV), West Nile virus (WNV), and yellow fever virus (YFV); Picornaviridae (green) with enterovirus 71 (EV71) and poliovirus; Retroviridae (red) namely human immunodeficiency virus type 1 (HIV‐1), murine leukemia virus (MLV) and Rous sarcoma virus (RSV); and Influenza virus (yellow) within Orthomyxoviridae. vRNA, viral RNA

[ Normal View | Magnified View ]

N6‐methyladenosine modification on messenger RNA and functions that are modulated by writer, eraser and reader proteins

[ Normal View | Magnified View ]

Adenosine‐to‐Inosine editing. (a) ADAR deaminates the C6 position in adenosine (A) to produce inosine (I). (b) A‐to‐I editing in RNA alters RNA metabolism to impact different cellular processes. RdRp, viral RNA‐dependent RNA polymerase

[ Normal View | Magnified View ]

Editing of Uridine‐to‐Pseudouridine. (a) Pseudouridine synthase (PUS) catalyzes the isomerization of uridine (U) to form 5‐ribosyl uracil or pseudouridine (Ψ). (b) Functional outcomes of U‐to‐Ψ editing

[ Normal View | Magnified View ]

Consequences of ribose 2′‐O‐methyl modifications on RNA virus gene expression. Methylation of the 2′‐O‐position on the ribose can occur on all nucleotides and may be deposited by both viral and cellular 2′‐O‐methyltransferases (2′‐O‐MTase). The 2′‐O‐methylation of the penultimate nucleotide of the 5′‐end of the viral RNA limits innate immune sensing, first by masking the recognition of the viral RNA by the cytosolic RNA sensors RIG‐I and Mda5 to prevent transcription of innate immune response genes, and second by preventing the interaction with IFIT proteins which downregulate translation. 2′‐O‐methylated nucleotides (Nm) within viral RNA also function to mask the viral RNA from cytosolic RNA sensors. Deposition of internal 2′‐O‐methyl groups on adenosines (Am) by the viral 2′‐O‐MTase inhibit the elongation of the viral RNA‐dependent RNA polymerase during replication

[ Normal View | Magnified View ]

References

Abbas,, Y. M., Laudenbach,, B. T., Martínez‐Montero,, S., Cencic,, R., Habjan,, M., Pichlmair,, A., … Nagar,, B. (2017). Structure of human IFIT1 with capped RNA reveals adaptable mRNA binding and mechanisms for sensing N1 and N2 ribose 2′‐O methylations. Proceedings of the National Academy of Sciences of the United States of America, 114(11), E2106–E2115. https://doi.org/10.1073/pnas.1612444114
Anderson,, B. R., Muramatsu,, H., Jha,, B. K., Silverman,, R. H., Weissman,, D., & Karikó,, K. (2011). Nucleoside modifications in RNA limit activation of 2′‐5′‐oligoadenylate synthetase and increase resistance to cleavage by RNase L. Nucleic Acids Research, 39(21), 9329–9338. https://doi.org/10.1093/nar/gkr586
Anderson,, B. R., Muramatsu,, H., Nallagatla,, S. R., Bevilacqua,, P. C., Sansing,, L. H., Weissman,, D., & Karikó,, K. (2010). Incorporation of pseudouridine into mRNA enhances translation by diminishing PKR activation. Nucleic Acids Research, 38(17), 5884–5892. https://doi.org/10.1093/nar/gkq347
Arango,, D., Sturgill,, D., Alhusaini,, N., Dillman,, A. A., Sweet,, T. J., Hanson,, G., … Oberdoerffer,, S. (2018). Acetylation of cytidine in mRNA promotes translation efficiency. Cell, 175(7), 1872–1886.e24. https://doi.org/10.1016/j.cell.2018.10.030
Aspden,, J. L., & Jackson,, R. J. (2010). Differential effects of nucleotide analogs on scanning‐dependent initiation and elongation of mammalian mRNA translation in vitro. RNA, 16(6), 1130–1137. https://doi.org/10.1261/rna.1978610
Ayadi,, L., Galvanin,, A., Pichot,, F., Marchand,, V., & Motorin,, Y. (2019). RNA ribose methylation (2′‐O‐methylation): Occurrence, biosynthesis and biological functions. Biochimica et Biophysica Acta (BBA) – Gene Regulatory Mechanisms, 1862(3), 253–269. https://doi.org/10.1016/j.bbagrm.2018.11.009
Baskin,, F., & Dekker,, C. A. (1967). A rapid and specific assay for sugar methylation in ribonucleic acid. The Journal of Biological Chemistry, 242(22), 5447–5449.
Bass,, B. L., Weintraub,, H., Cattaneo,, R., & Billeter,, M. A. (1989). Biased hypermutation of viral RNA genomes could be due to unwinding/modification of double‐stranded RNA. Cell, 56(3), 331. https://doi.org/10.1016/0092-8674(89)90234-1
Baumstark,, T., & Ahlquist,, P. (2001). The brome mosaic virus RNA3 intergenic replication enhancer folds to mimic a tRNA TpsiC‐stem loop and is modified in vivo. RNA, 7(11), 1652–1670.
Becker,, H. (1998). Pseudouridine and ribothymidine formation in the tRNA‐like domain of turnip yellow mosaic virus RNA. Nucleic Acids Research, 26(17), 3991–3997. https://doi.org/10.1093/nar/26.17.3991
Beemon,, K., & Keith,, J. (1977). Localization of N6‐methyladenosine in the Rous sarcoma virus genome. Journal of Molecular Biology, 113(1), 165–179. https://doi.org/10.1016/0022-2836(77)90047-X
Bhattacharya,, T., Newton,, I. L. G., & Hardy,, R. W. (2017). Wolbachia elevates host methyltransferase expression to block an RNA virus early during infection. PLoS Pathogens, 13(6), e1006427. https://doi.org/10.1371/journal.ppat.1006427
Bilbille,, Y., Vendeix,, F. A. P., Guenther,, R., Malkiewicz,, A., Ariza,, X., Vilarrasa,, J., & Agris,, P. F. (2009). The structure of the human tRNALys3 anticodon bound to the HIV genome is stabilized by modified nucleosides and adjacent mismatch base pairs. Nucleic Acids Research, 37(10), 3342–3353. https://doi.org/10.1093/nar/gkp187
Boccaletto,, P., MacHnicka,, M. A., Purta,, E., Pitkowski,, P., Baginski,, B., Wirecki,, T. K., … Bujnicki,, J. M. (2018). MODOMICS: A database of RNA modification pathways. 2017 update. Nucleic Acids Research, 46(D1), D303–D307. https://doi.org/10.1093/nar/gkx1030
Bouvet,, M., Debarnot,, C., Imbert,, I., Selisko,, B., Snijder,, E. J., Canard,, B., & Decroly,, E. (2010). In vitro reconstitution of SARS‐coronavirus mRNA cap methylation. PLoS Pathogens, 6(4), e1000863. https://doi.org/10.1371/journal.ppat.1000863
Bouvier,, N. M., & Palese,, P. (2008). The biology of influenza viruses. Vaccine, 26(Suppl. 4), D49–D53. https://doi.org/10.1016/j.vaccine.2008.07.039
Bujnicki,, J. M., Feder,, M., Ayres,, C. L., & Redman,, K. L. (2004). Sequence–structure–function studies of tRNA:m5C methyltransferase Trm4p and its relationship to DNA:m5C and RNA:m5U methyltransferases. Nucleic Acids Research, 32(8), 2453–2463. https://doi.org/10.1093/nar/gkh564
Campbell,, E. M., & Hope,, T. J. (2015). HIV‐1 capsid: The multifaceted key player in HIV‐1 infection. Nature Reviews Microbiology, 13(8), 471–483. https://doi.org/10.1038/nrmicro3503
Canaani,, D., Kahana,, C., Lavi,, S., & Groner,, Y. (1979). Identification and mapping of N6‐methyladenosine containing sequences in simian virus 40 RNA. Nucleic Acids Research, 6(8), 2879–2899. https://doi.org/10.1093/nar/6.8.2879
Cantara,, W. A., Crain,, P. F., Rozenski,, J., McCloskey,, J. A., Harris,, K. A., Zhang,, X., … Agris,, P. F. (2011). The RNA modification database, RNAMDB: 2011 update. Nucleic Acids Research, 39(Suppl. 1), D195–D201. https://doi.org/10.1093/nar/gkq1028
Carlile,, T. M., Rojas‐Duran,, M. F., Zinshteyn,, B., Shin,, H., Bartoli,, K. M., & Gilbert,, W. V. (2014). Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature, 515(7525), 143–146. https://doi.org/10.1038/nature13802
Casey,, J. L. (2006). RNA editing in hepatitis delta virus. Current Topics in Microbiology and Immunology, 307, 67–89.
Casey,, J. L., Bergmann,, K. F., Brown,, T. L., & Gerin,, J. L. (1992). Structural requirements for RNA editing in hepatitis delta virus: Evidence for a uridine‐to‐cytidine editing mechanism. Proceedings of the National Academy of Sciences of the United States of America, 89(15), 7149–7153. https://doi.org/10.1073/pnas.89.15.7149
Casey,, J. L., & Gerin,, J. L. (1995). Hepatitis D virus RNA editing: Specific modification of adenosine in the antigenomic RNA. Journal of Virology, 69(12), 7593–7600.
Cattaneo,, R., Schmid,, A., Eschle,, D., Baczko,, K., ter Meulen,, V., & Billeter,, M. A. (1988). Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell, 55(2), 255–265. https://doi.org/10.1016/0092-8674(88)90048-7
Cattenoz,, P. B., Taft,, R. J., Westhof,, E., & Mattick,, J. S. (2013). Transcriptome‐wide identification of A%3EI RNA editing sites by inosine specific cleavage. RNA, 19(2), 257–270. https://doi.org/10.1261/rna.036202.112
Chen,, Y., Cai,, H., Pan,, J., Xiang,, N., Tien,, P., Ahola,, T., & Guo,, D. (2009). Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proceedings of the National Academy of Sciences of the United States of America, 106(9), 3484–3489. https://doi.org/10.1073/pnas.0808790106
Cohn,, W. E. (1959). 5‐Ribosyl uracil, a carbon–carbon ribofuranosyl nucleoside in ribonucleic acids. Biochimica et Biophysica Acta, 32, 569–571. https://doi.org/10.1016/0006-3002(59)90644-4
Cohn,, W. E., & Volkin,, E. (1951). Nucleoside‐5′‐phosphates from ribonucleic acid. Nature, 167(4247), 483–484. https://doi.org/10.1038/167483a0
Courtney,, D. G., Chalem,, A., Bogerd,, H. P., Law,, B. A., Kennedy,, E. M., Holley,, C. L., & Cullen,, B. R. (2019). Extensive epitranscriptomic methylation of A and C residues on murine leukemia virus transcripts enhances viral gene expression. MBio, 10(3), e01209–e01219. https://doi.org/10.1128/mBio.01209-19
Courtney,, D. G., Kennedy,, E. M., Dumm,, R. E., Bogerd,, H. P., Tsai,, K., Heaton,, N. S., & Cullen,, B. R. (2017). Epitranscriptomic enhancement of influenza A virus gene expression and replication. Cell Host and Microbe, 22(3), 377–386.e5. https://doi.org/10.1016/j.chom.2017.08.004
Cross,, S. T., Michalski,, D., Miller,, M. R., & Wilusz,, J. (2019). RNA regulatory processes in RNA virus biology. WIREs: RNA, 10, e1536. https://doi.org/10.1002/wrna.1536
Cruz‐Oliveira,, C., Freire,, J. M., Conceição,, T. M., Higa,, L. M., Castanho,, M. A. R. B., & Da Poian,, A. T. (2015). Receptors and routes of dengue virus entry into the host cells. FEMS Microbiology Reviews, 39(2), 155–170. https://doi.org/10.1093/femsre/fuu004
Daffis,, S., Szretter,, K. J., Schriewer,, J., Li,, J., Youn,, S., Errett,, J., … Diamond,, M. S. (2010). 2′‐O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature, 468(7322), 452–456. https://doi.org/10.1038/nature09489
Dai,, Q., Moshitch‐Moshkovitz,, S., Han,, D., Kol,, N., Amariglio,, N., Rechavi,, G., … He,, C. (2017). Nm‐seq maps 2′‐O‐methylation sites in human mRNA with base precision. Nature Methods, 14(7), 695–698. https://doi.org/10.1038/nmeth.4294
Dalet,, A., Gatti,, E., & Pierre,, P. (2015). Integration of PKR‐dependent translation inhibition with innate immunity is required for a coordinated anti‐viral response. FEBS Letters, 589(14), 1539–1545. https://doi.org/10.1016/j.febslet.2015.05.006
Danecek,, P., Nellåker,, C., McIntyre,, R. E., Buendia‐Buendia,, J. E., Bumpstead,, S., Ponting,, C. P., … Adams,, D. J. (2012). High levels of RNA‐editing site conservation amongst 15 laboratory mouse strains. Genome Biology, 13(4), R26. https://doi.org/10.1186/gb-2012-13-4-r26
Davis,, D. R. (1995). Stabilization of RNA stacking by pseudouridine. Nucleic Acids Research, 23(24), 5020–5026. https://doi.org/10.1093/nar/23.24.5020
Decroly,, E., & Canard,, B. (2017). Biochemical principles and inhibitors to interfere with viral capping pathways. Current Opinion in Virology, 24, 87–96. https://doi.org/10.1016/j.coviro.2017.04.003
Decroly,, E., Ferron,, F., Lescar,, J., & Canard,, B. (2012). Conventional and unconventional mechanisms for capping viral mRNA. Nature Reviews Microbiology, 10(1), 51–65. https://doi.org/10.1038/nrmicro2675
Decroly,, E., Imbert,, I., Coutard,, B., Bouvet,, M., Selisko,, B., Alvarez,, K., … Canard,, B. (2008). Coronavirus nonstructural protein 16 is a Cap‐0 binding enzyme possessing (nucleoside‐2′O)‐methyltransferase activity. Journal of Virology, 82(16), 8071–8084. https://doi.org/10.1128/jvi.00407-08
Deffrasnes,, C., Marsh,, G. A., Foo,, C. H., Rootes,, C. L., Gould,, C. M., Grusovin,, J., … Wang,, L. F. (2016). Genome‐wide siRNA screening at biosafety level 4 reveals a crucial role for fibrillarin in Henipavirus infection. PLoS Pathogens, 12(3), e1005478. https://doi.org/10.1371/journal.ppat.1005478
Devarkar,, S. C., Wang,, C., Miller,, M. T., Ramanathan,, A., Jiang,, F., Khan,, A. G., … Marcotrigiano,, J. (2016). Structural basis for m7G recognition and 2′‐O‐methyl discrimination in capped RNAs by the innate immune receptor RIG‐I. Proceedings of the National Academy of Sciences of the United States of America, 113(3), 596–601. https://doi.org/10.1073/pnas.1515152113
Dimock,, K., & Stoltzfus,, C. M. (1977). Sequence specificity of internal methylation in B77 avian sarcoma virus RNA subunits. Biochemistry, 16(3), 471–478. https://doi.org/10.1021/bi00622a021
Dimock,, K., & Stoltzfus,, C. M. (1978). Cycloleucine blocks 5′‐terminal and internal methylations of avian sarcoma virus genome RNA. Biochemistry, 17(17), 3627–3632. https://doi.org/10.1021/bi00610a032
Dominissini,, D., Moshitch‐Moshkovitz,, S., Schwartz,, S., Salmon‐Divon,, M., Ungar,, L., Osenberg,, S., … Rechavi,, G. (2012). Topology of the human and mouse m6A RNA methylomes revealed by m6A‐seq. Nature, 485(7397), 201–206. https://doi.org/10.1038/nature11112
Dong,, H., Chang,, D. C., Hua,, M. H. C., Lim,, S. P., Chionh,, Y. H., Hia,, F., … Shi,, P. Y. (2012). 2′‐O methylation of internal adenosine by flavivirus NS5 methyltransferase. PLoS Pathogens, 8(4), e1002642. https://doi.org/10.1371/journal.ppat.1002642
Dong,, H., Ren,, S., Li,, H., & Shi,, P. Y. (2008). Separate molecules of West Nile virus methyltransferase can independently catalyze the N7 and 2′‐O methylations of viral RNA cap. Virology, 377(1), 1–6. https://doi.org/10.1016/j.virol.2008.04.026
Dong,, H., Zhang,, B., & Shi,, P. Y. (2008). Flavivirus methyltransferase: A novel antiviral target. Antiviral Research, 80(1), 1–10. https://doi.org/10.1016/j.antiviral.2008.05.003
Doria,, M., Neri,, F., Gallo,, A., Farace,, M. G., & Michienzi,, A. (2009). Editing of HIV‐1 RNA by the double‐stranded RNA deaminase ADAR1 stimulates viral infection. Nucleic Acids Research, 37(17), 5848–5858. https://doi.org/10.1093/nar/gkp604
Dubin,, D. T., & Stollar,, V. (1975). Methylation of Sindbis virus “26S” messenger RNA. Biochemical and Biophysical Research Communications, 66(4), 1373–1379. https://doi.org/10.1016/0006-291X(75)90511-2
Dubin,, D. T., Stollar,, V., Hsuchen,, C. C., Timko,, K., & Guild,, G. M. (1977). Sindbis virus messenger RNA: The 5′‐termini and methylated residues of 26 and 42 S RNA. Virology, 77(2), 457–470. https://doi.org/10.1016/0042-6822(77)90471-8
Durdevic,, Z., Hanna,, K., Gold,, B., Pollex,, T., Cherry,, S., Lyko,, F., & Schaefer,, M. (2013). Efficient RNA virus control in Drosophila requires the RNA methyltransferase Dnmt2. EMBO Reports, 14(3), 269–275. https://doi.org/10.1038/embor.2013.3
Erales,, J., Marchand,, V., Panthu,, B., Gillot,, S., Belin,, S., Ghayad,, S. E., … Diaz,, J.‐J. (2017). Evidence for rRNA 2′‐O‐methylation plasticity: Control of intrinsic translational capabilities of human ribosomes. Proceedings of the National Academy of Sciences of the United States of America, 114(49), 12934–12939. https://doi.org/10.1073/pnas.1707674114
Felder,, M.‐P., Laugier,, D., Yatsula,, B., Dezélée,, P., Calothy,, G., & Marx,, M. (1994). Functional and biological properties of an avian variant long terminal repeat containing multiple A to G conversions in the U3 sequence. Journal of Virology, 68(8), 4759–4767.
Finkel,, D., & Groner,, Y. (1983). Methylations of adenosine residues (m6A) in pre‐mRNA are important for formation of late simian virus 40 mRNAs. Virology, 131(2), 409–425. https://doi.org/10.1016/0042-6822(83)90508-1
Furuichi,, Y., Morgan,, M., Muthukrishnan,, S., & Shatkin,, A. J. (1975). Reovirus messenger RNA contains a methylated, blocked 5′‐terminal structure: m‐7G(5′)ppp(5′)G‐MpCp. Proceedings of the National Academy of Sciences, 72(1), 362–366. https://doi.org/10.1073/pnas.72.1.362
Furuichi,, Y., Shatkin,, A. J., Stavnezer,, E., & Bishop,, J. M. (1975). Blocked, methylated 5′‐terminal sequence in avian sarcoma virus RNA. Nature, 257(5527), 618–620. https://doi.org/10.1038/257618a0
George,, C. X., John,, L., & Samuel,, C. E. (2014). An RNA editor, adenosine deaminase acting on double‐stranded RNA (ADAR1). Journal of Interferon %26 Cytokine Research, 34(6), 437–446. https://doi.org/10.1089/jir.2014.0001
Gokhale,, N. S., & Horner,, S. M. (2017). RNA modifications go viral. PLoS Pathogens, 13(3), e1006188. https://doi.org/10.1371/journal.ppat.1006188
Gokhale,, N. S., McIntyre,, A. B. R., McFadden,, M. J., Roder,, A. E., Kennedy,, E. M., Gandara,, J. A., … Horner,, S. M. (2016). N6‐methyladenosine in Flaviviridae viral RNA genomes regulates infection. Cell Host and Microbe, 20(5), 654–665. https://doi.org/10.1016/j.chom.2016.09.015
Gonzales‐van Horn,, S. R., & Sarnow,, P. (2017). Making the mark: The role of adenosine modifications in the life cycle of RNA viruses. Cell Host and Microbe, 21(6), 661–669. https://doi.org/10.1016/j.chom.2017.05.008
Griffin,, D. E., Lin,, W.‐H. W., & Nelson,, A. N. (2018). Understanding the causes and consequences of measles virus persistence. F1000Research, 7, 237. https://doi.org/10.12688/f1000research.12094.1
Gutsche,, I., Desfosses,, A., Effantin,, G., Ling,, W. L., Haupt,, M., Ruigrok,, R. W. H., … Schoehn,, G. (2015). Near‐atomic cryo‐EM structure of the helical measles virus nucleocapsid. Science, 348(6235), 704–707. https://doi.org/10.1126/science.aaa5137
Habjan,, M., Hubel,, P., Lacerda,, L., Benda,, C., Holze,, C., Eberl,, C. H., … Pichlmair,, A. (2013). Sequestration by IFIT1 impairs translation of 2′O‐unmethylated capped RNA. PLoS Pathogens, 9(10), e1003663. https://doi.org/10.1371/journal.ppat.1003663
Hall,, W. W., Lamb,, R. A., & Choppin,, P. W. (1979). Measles and subacute sclerosing panencephalitis virus proteins: Lack of antibodies to the M protein in patients with subacute sclerosing panencephalitis. Proceedings of the National Academy of Sciences of the United States of America, 76(4), 2047–2051. https://doi.org/10.1073/pnas.76.4.2047
Hao,, H., Hao,, S., Chen,, H., Chen,, Z., Zhang,, Y., Wang,, J., … Guan,, W. (2019). N6‐methyladenosine modification and METTL3 modulate enterovirus 71 replication. Nucleic Acids Research, 47(1), 362–374. https://doi.org/10.1093/nar/gky1007
Hashimoto,, S. I., & Green,, M. (1976). Multiple methylated cap sequences in adenovirus type 2 early mRNA. Journal of Virology, 20(2), 425–435.
Hesser,, C. R., Karijolich,, J., Dominissini,, D., He,, C., & Glaunsinger,, B. A. (2018). N6‐methyladenosine modification and the YTHDF2 reader protein play cell type specific roles in lytic viral gene expression during Kaposi`s sarcoma‐associated herpesvirus infection. PLoS Pathogens, 14(4), e1006995. https://doi.org/10.1371/journal.ppat.1006995
Hinnebusch,, A. G. (2006). eIF3: A versatile scaffold for translation initiation complexes. Trends in Biochemical Sciences, 31(10), 553–562. https://doi.org/10.1016/j.tibs.2006.08.005
Hsuchen,, C. C., & Dubin,, D. T. (1976). Di‐ and trimethylated congeners of 7‐methylguanine in Sindbis virus mRNA. Nature, 264(5582), 190–191. https://doi.org/10.1038/264190a0
Hu,, W.‐S., & Hughes,, S. H. (2012). HIV‐1 reverse transcription. Cold Spring Harbor Perspectives in Medicine, 2(10), a006882–a006882. https://doi.org/10.1101/cshperspect.a006882
Hui,, D. J., Bhasker,, C. R., Merrick,, W. C., & Sen,, G. C. (2003). Viral stress‐inducible protein p56 inhibits translation by blocking the interaction of eIF3 with the ternary complex eIF2·GTP·Met‐tRNAi. Journal of Biological Chemistry, 278(41), 39477–39482. https://doi.org/10.1074/jbc.M305038200
Hui,, D. J., Terenzi,, F., Merrick,, W. C., & Sen,, G. C. (2005). Mouse p56 blocks a distinct function of eukaryotic initiation factor 3 in translation initiation. Journal of Biological Chemistry, 280(5), 3433–3440. https://doi.org/10.1074/jbc.M406700200
Hyde,, J. L., & Diamond,, M. S. (2015). Innate immune restriction and antagonism of viral RNA lacking 2′‐O methylation. Virology, 479–480, 66–74. https://doi.org/10.1016/j.virol.2015.01.019
Iglesias,, N. G., & Gamarnik,, A. V. (2011). Dynamic RNA structures in the dengue virus genome. RNA Biology, 8(2), 249–257. https://doi.org/10.4161/hv.8.2.14992
Imam,, H., Khan,, M., Gokhale,, N. S., McIntyre,, A. B. R., Kim,, G. W., Jang,, J. Y., … Siddiqui,, A. (2018). N6‐methyladenosine modification of hepatitis B virus RNA differentially regulates the viral life cycle. Proceedings of the National Academy of Sciences of the United States of America, 115(35), 8829–8834. https://doi.org/10.1073/pnas.1808319115
Incarnato,, D., Anselmi,, F., Morandi,, E., Neri,, F., Maldotti,, M., Rapelli,, S., … Oliviero,, S. (2017). High‐throughput single‐base resolution mapping of RNA 2‐O‐methylated residues. Nucleic Acids Research, 45(3), 1433–1441. https://doi.org/10.1093/nar/gkw810
Jayan,, G. C., & Casey,, J. L. (2005). Effects of conserved RNA secondary structures on hepatitis delta virus genotype I RNA editing, replication, and virus production. Journal of Virology, 79(17), 11187–11193. https://doi.org/10.1128/JVI.79.17.11187-11193.2005
Jia,, G., Fu,, Y., Zhao,, X., Dai,, Q., Zheng,, G., Yang,, Y., … He,, C. (2011). N6‐methyladenosine in nuclear RNA is a major substrate of the obesity‐associated FTO. Nature Chemical Biology, 7(12), 885–887. https://doi.org/10.1038/nchembio.687
Kane,, S. E., & Beemon,, K. (1985). Precise localization of m6A in Rous sarcoma virus RNA reveals clustering of methylation sites: Implications for RNA processing. Molecular and Cellular Biology, 5(9), 2298–2306.
Karikó,, K., Muramatsu,, H., Welsh,, F. A., Ludwig,, J., Kato,, H., Akira,, S., & Weissman,, D. (2008). Incorporation of pseudouridine into mRNA yields superior nonimmunogenic vector with increased translational capacity and biological stability. Molecular Therapy, 16(11), 1833–1840. https://doi.org/10.1038/mt.2008.200
Kennedy,, E. M., Bogerd,, H. P., Kornepati,, A. V. R., Kang,, D., Ghoshal,, D., Marshall,, J. B., … Cullen,, B. R. (2016). Posttranscriptional m6A editing of HIV‐1 mRNAs enhances viral gene expression. Cell Host and Microbe, 19(5), 675–685. https://doi.org/10.1016/j.chom.2016.04.002
Kennedy,, E. M., Courtney,, D. G., Tsai,, K., & Cullen,, B. R. (2017). Viral Epitranscriptomics. Journal of Virology, 91(9), e02263–e02216. https://doi.org/10.1128/JVI.02263-16
Khrustalev,, V. V., Khrustaleva,, T. A., Sharma,, N., & Giri,, R. (2017). Mutational pressure in Zika virus: Local ADAR‐editing areas associated with pauses in translation and replication. Frontiers in Cellular and Infection Microbiology, 7, 44. https://doi.org/10.3389/fcimb.2017.00044
Kimura,, T., Katoh,, H., Kayama,, H., Saiga,, H., Okuyama,, M., Okamoto,, T., … Takeda,, K. (2013). Ifit1 inhibits Japanese encephalitis virus replication through binding to 5′ capped 2′‐O unmethylated RNA. Journal of Virology, 87(18), 9997–10003. https://doi.org/10.1128/JVI.00883-13
Knutson,, S. D., Ayele,, T. M., & Heemstra,, J. M. (2018). Chemical labeling and affinity capture of inosine‐containing RNAs using acrylamidofluorescein. Bioconjugate Chemistry, 29(9), 2899–2903. https://doi.org/10.1021/acs.bioconjchem.8b00541
Koh,, C., Da,, B. L., & Glenn,, J. S. (2019). HBV/HDV coinfection: A challenge for therapeutics. Clinics in Liver Disease, 23(3), 557–572. https://doi.org/10.1016/j.cld.2019.04.005
Krug,, R. M., Morgan,, M. A., & Shatkin,, A. J. (1976). Influenza viral mRNA contains internal N6‐methyladenosine and 5′‐terminal 7‐methylguanosine in cap structures. Journal of Virology, 20(1), 45–53.
Kumar,, P., Sweeney,, T. R., Skabkin,, M. A., Skabkina,, O. V., Hellen,, C. U. T., & Pestova,, T. V. (2014). Inhibition of translation by IFIT family members is determined by their ability to interact selectively with the 5′‐terminal regions of cap0‐, cap1‐ and 5′ppp‐mRNAs. Nucleic Acids Research, 42(5), 3228–3245. https://doi.org/10.1093/nar/gkt1321
Kuo,, M. Y., Chao,, M., & Taylor,, J. (1989). Initiation of replication of the human hepatitis delta virus genome from cloned DNA: Role of delta antigen. Journal of Virology, 63(5), 1945–1950.
Lane,, B. G., & Tamaoki,, T. (1967). Studies of the chain termini and alkali‐stable dinucleotide sequences in 16 s and 28 s ribosomal RNA from L cells. Journal of Molecular Biology, 27(2), 335–348. https://doi.org/10.1016/0022-2836(67)90024-1
Lang,, F., Singh,, R. K., Pei,, Y., Zhang,, S., Sun,, K., & Robertson,, E. S. (2019). EBV epitranscriptome reprogramming by METTL14 is critical for viral‐associated tumorigenesis. PLoS Pathogens, 15(6), e1007796. https://doi.org/10.1371/journal.ppat.1007796
Lazear,, H. M., & Diamond,, M. S. (2016). Zika virus: New clinical syndromes and its emergence in the Western hemisphere. Journal of Virology, 90(10), 4864–4875. https://doi.org/10.1128/jvi.00252-16
Lempp,, F. A., Ni,, Y., & Urban,, S. (2016). Hepatitis delta virus: Insights into a peculiar pathogen and novel treatment options. Nature Reviews Gastroenterology %26 Hepatology, 13(10), 580–589. https://doi.org/10.1038/nrgastro.2016.126
Li,, J. B., Levanon,, E. Y., Yoon,, J. K., Aach,, J., Xie,, B., LeProust,, E., … Church,, G. M. (2009). Genome‐wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science, 324(5931), 1210–1213. https://doi.org/10.1126/science.1170995
Li,, X., Ma,, S., & Yi,, C. (2016). Pseudouridine: The fifth RNA nucleotide with renewed interests. Current Opinion in Chemical Biology, 33, 108–116. https://doi.org/10.1016/J.CBPA.2016.06.014
Li,, X., Zhu,, P., Ma,, S., Song,, J., Bai,, J., Sun,, F., & Yi,, C. (2015). Chemical pulldown reveals dynamic pseudouridylation of the mammalian transcriptome. Nature Chemical Biology, 11(8), 592–597. https://doi.org/10.1038/nchembio.1836
Lichinchi,, G., Gao,, S., Saletore,, Y., Gonzalez,, G. M., Bansal,, V., Wang,, Y., … Rana,, T. M. (2016). Dynamics of the human and viral m(6)A RNA methylomes during HIV‐1 infection of T cells. Nature Microbiology, 1(4), 16011. https://doi.org/10.1038/nmicrobiol.2016.11
Lichinchi,, G., Zhao,, B. S., Wu,, Y., Lu,, Z., Qin,, Y., He,, C., & Rana,, T. M. (2016). Dynamics of human and viral RNA methylation during Zika virus infection. Cell Host and Microbe, 20(5), 666–673. https://doi.org/10.1016/j.chom.2016.10.002
Liddicoat,, B. J., Piskol,, R., Chalk,, A. M., Ramaswami,, G., Higuchi,, M., Hartner,, J. C., … Walkley,, C. R. (2015). RNA editing by ADAR1 prevents MDA5 sensing of endogenous dsRNA as nonself. Science, 349(6252), 1115–1120. https://doi.org/10.1126/science.aac7049
Liebert,, U. G., Baczko,, K., Budka,, H., & Ter Meulen,, V. (1986). Restricted expression of measles virus proteins in brains from cases of subacute sclerosing panencephalitis. Journal of General Virology, 67(11), 2435–2444. https://doi.org/10.1099/0022-1317-67-11-2435
Limbach,, P. A., Crain,, P. F., & Mccloskey,, J. A. (1994). Summary: The modified nucleosides of RNA. Nucleic Acids Research, 22(12), 2183–2196. https://doi.org/10.1093/nar/22.12.2183
Liu,, J., Yue,, Y., Han,, D., Wang,, X., Fu,, Y., Zhang,, L., … He,, C. (2014). A METTL3‐METTL14 complex mediates mammalian nuclear RNA N6‐adenosine methylation. Nature Chemical Biology, 10(2), 93–95. https://doi.org/10.1038/nchembio.1432
Lloyd,, R. E. (2013). Regulation of stress granules and P‐bodies during RNA virus infection. WIREs: RNA, 4(3), 317–331. https://doi.org/10.1002/wrna.1162
Lovejoy,, A. F., Riordan,, D. P., & Brown,, P. O. (2014). Transcriptome‐wide mapping of pseudouridines: Pseudouridine synthases modify specific mRNAs in S. cerevisiae. PLoS ONE, 9(10), e110799. https://doi.org/10.1371/journal.pone.0110799
Lu,, W., Tirumuru,, N., St. Gelais,, C., Koneru,, P. C., Liu,, C., Kvaratskhelia,, M., … Wu,, L. (2018). N⁶‐Methyladenosine‐binding proteins suppress HIV‐1 infectivity and viral production. Journal of Biological Chemistry, 293(34), 12992–13005. https://doi.org/10.1074/jbc.RA118.004215
Luo,, D., Kohlway,, A., Vela,, A., & Pyle,, A. M. (2012). Visualizing the determinants of viral RNA recognition by innate immune sensor RIG‐I. Structure, 20(11), 1983–1988. https://doi.org/10.1016/j.str.2012.08.029
Machnicka,, M. A., Milanowska,, K., Osman Oglou,, O., Purta,, E., Kurkowska,, M., Olchowik,, A., … Grosjean,, H. (2012). MODOMICS: A database of RNA modification pathways—2013 update. Nucleic Acids Research, 41(D1), D262–D267. https://doi.org/10.1093/nar/gks1007
Mak,, J., & Kleiman,, L. (1997). Primer tRNAs for reverse transcription. Journal of Virology, 71(11), 8087–8095.
Mannion,, N. M., Greenwood,, S. M., Young,, R., Cox,, S., Brindle,, J., Read,, D., … O`Connell,, M. A. (2014). The RNA‐editing enzyme ADAR1 controls innate immune responses to RNA. Cell Reports, 9(4), 1482–1494. https://doi.org/10.1016/j.celrep.2014.10.041
Marceau,, C. D., Puschnik,, A. S., Majzoub,, K., Ooi,, Y. S., Brewer,, S. M., Fuchs,, G., … Carette,, J. E. (2016). Genetic dissection of Flaviviridae host factors through genome‐scale CRISPR screens. Nature, 535(7610), 159–163. https://doi.org/10.1038/nature18631
Marchand,, V., Blanloeil‐Oillo,, F., Helm,, M., & Motorin,, Y. (2016). Illumina‐based RiboMethSeq approach for mapping of 2′‐O‐Me residues in RNA. Nucleic Acids Research, 44(16), e135–e135. https://doi.org/10.1093/nar/gkw547
Martin,, B., Coutard,, B., Guez,, T., Paesen,, G. C., Canard,, B., Debart,, F., … Decroly,, E. (2018). The methyltransferase domain of the Sudan ebolavirus L protein specifically targets internal adenosines of RNA substrates, in addition to the cap structure. Nucleic Acids Research, 46(15), 7902–7912. https://doi.org/10.1093/nar/gky637
Martínez,, I., Dopazo,, J., & Melero,, J. A. (1997). Antigenic structure of the human respiratory syncytial virus G glycoprotein and relevance of hypermutation events for the generation of antigenic variants. Journal of General Virology, 78(10), 2419–2429. https://doi.org/10.1099/0022-1317-78-10-2419
Martínez,, I., & Melero,, J. A. (2002). A model for the generation of multiple A to G transitions in the human respiratory syncytial virus genome: Predicted RNA secondary structures as substrates for adenosine deaminases that act on RNA. Journal of General Virology, 83(6), 1445–1455. https://doi.org/10.1099/0022-1317-83-6-1445
Mauro,, V. P., & Edelman,, G. M. (2002). The ribosome filter hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 99(19), 12031–12036. https://doi.org/10.1073/pnas.192442499
McFadden,, M. J., Gokhale,, N. S., & Horner,, S. M. (2017). Protect this house: Cytosolic sensing of viruses. Current Opinion in Virology, 22, 36–43. https://doi.org/10.1016/j.coviro.2016.11.012
McIntyre,, W., Netzband,, R., Bonenfant,, G., Biegel,, J. M., Miller,, C., Fuchs,, G., … Pager,, C. T. (2018). Positive‐sense RNA viruses reveal the complexity and dynamics of the cellular and viral epitranscriptomes during infection. Nucleic Acids Research, 46(11), 5776–5791. https://doi.org/10.1093/nar/gky029
Mentha,, N., Clément,, S., Negro,, F., & Alfaiate,, D. (2019). A review on hepatitis D: From virology to new therapies. Journal of Advanced Research, 17, 3–15. https://doi.org/10.1016/j.jare.2019.03.009
Meyer,, K. D., & Jaffrey,, S. R. (2017). Rethinking m6A readers, writers, and erasers. Annual Review of Cell and Developmental Biology, 33, 319–342. https://doi.org/10.1146/annurev-cellbio-100616
Meyer,, K. D., Saletore,, Y., Zumbo,, P., Elemento,, O., Mason,, C. E., & Jaffrey,, S. R. (2012). Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell, 149(7), 1635–1646. https://doi.org/10.1016/j.cell.2012.05.003
Moss,, B., Gershowitz,, A., Stringer,, J. R., Holland,, L. E., & Wagner,, E. K. (1977). 5′‐Terminal and internal methylated nucleosides in herpes simplex virus type 1 mRNA. Journal of Virology, 23(2), 234–239.
Moss,, B., & Koczot,, F. (1976). Sequence of methylated nucleotides at the 5′ terminus of adenovirus specific RNA. Journal of Virology, 17(2), 385–392.
Motorin,, Y., Lyko,, F., & Helm,, M. (2009). 5‐Methylcytosine in RNA: Detection, enzymatic formation and biological functions. Nucleic Acids Research, 38(5), 1415–1430. https://doi.org/10.1093/nar/gkp1117
Narayan,, P., Ayers,, D. F., Rottman,, F. M., Maroney,, P. A., & Nilsen,, T. W. (1987). Unequal distribution of N6‐methyladenosine in influenza virus mRNAs. Molecular and Cellular Biology, 7(4), 1572–1575.
Newby,, M. I., & Greenbaum,, N. L. (2002). Investigation of Overhauser effects between pseudouridine and water protons in RNA helices. Proceedings of the National Academy of Sciences of the United States of America, 99(20), 12697–12702. https://doi.org/10.1073/pnas.202477199
Nicholson,, B. L., & White,, K. A. (2015). Exploring the architecture of viral RNA genomes. Current Opinion in Virology, 12, 66–74. https://doi.org/10.1016/j.coviro.2015.03.018
Otsuka,, Y., Kedersha,, N. L., & Schoenberg,, D. R. (2009). Identification of a cytoplasmic complex that adds a Cap onto 5′‐monophosphate RNA. Molecular and Cellular Biology, 29(8), 2155–2167. https://doi.org/10.1128/MCB.01325-08
Ott,, M., Geyer,, M., & Zhou,, Q. (2011). The control of HIV transcription: Keeping RNA polymerase II on track. Cell Host and Microbe, 10(5), 426–435. https://doi.org/10.1016/j.chom.2011.11.002
Patterson,, J. B., Cornu,, T. I., Redwine,, J., Dales,, S., Lewicki,, H., Holz,, A., … Oldstone,, M. B. A. (2001). Evidence that the hypermutated M protein of a subacute sclerosing panencephalitis measles virus actively contributes to the chronic progressive CNS disease. Virology, 291(2), 215–225. https://doi.org/10.1006/viro.2001.1182
Petes,, C., Odoardi,, N., & Gee,, K. (2017). The Toll for trafficking: Toll‐like receptor 7 delivery to the endosome. Frontiers in Immunology, 8, 1075. https://doi.org/10.3389/fimmu.2017.01075
Pfaller,, C. K., Donohue,, R. C., Nersisyan,, S., Brodsky,, L., & Cattaneo,, R. (2018). Extensive editing of cellular and viral double‐stranded RNA structures accounts for innate immunity suppression and the proviral activity of ADAR1 p150. PLoS Biology, 16(11), e2006577. https://doi.org/10.1371/journal.pbio.2006577
Pfaller,, C. K., Mastorakos,, G. M., Matchett,, W. E., Ma,, X., Samuel,, C. E., & Cattaneo,, R. (2015). Measles virus defective interfering RNAs are generated frequently and early in the absence of C protein and can be destabilized by adenosine deaminase acting on RNA‐1‐like hypermutations. Journal of Virology, 89(15), 7735–7747. https://doi.org/10.1128/jvi.01017-15
Pfaller,, C. K., Radeke,, M. J., Cattaneo,, R., & Samuel,, C. E. (2014). Measles virus C protein impairs production of defective copyback double‐stranded viral RNA and activation of protein kinase R. Journal of Virology, 88(1), 456–468. https://doi.org/10.1128/jvi.02572-13
Phuphuakrat,, A., Kraiwong,, R., Boonarkart,, C., Lauhakirti,, D., Lee,, T.‐H., & Auewarakul,, P. (2008). Double‐stranded RNA adenosine deaminases enhance expression of human immunodeficiency virus type 1 proteins. Journal of Virology, 82(21), 10864–10872. https://doi.org/10.1128/JVI.00238-08
Piontkivska,, H., Frederick,, M., Miyamoto,, M. M., & Wayne,, M. L. (2017). RNA editing by the host ADAR system affects the molecular evolution of the Zika virus. Ecology and Evolution, 7(12), 4475–4485. https://doi.org/10.1002/ece3.3033
Polson,, A. G., Bass,, B. L., & Casey,, J. L. (1996). RNA editing of hepatitis delta virus antigenome by dsRNA‐adenosine deaminase. Nature, 380(6573), 454–456. https://doi.org/10.1038/380454a0
Polson,, A. G., Ley,, H. L., Bass,, B. L., & Casey,, J. L. (1998). Hepatitis delta virus RNA editing is highly specific for the amber/W site and is suppressed by hepatitis delta antigen. Molecular and Cellular Biology, 18(4), 1919–1926. https://doi.org/10.1128/mcb.18.4.1919
Prusiner,, P., Yathindra,, N., & Sundaralingam,, M. (1974). Effect of ribose O(2′)‐methylation on the conformation of nucleosides and nucleotides. BBA Section Nucleic Acids and Protein Synthesis, 366(2), 115–123. https://doi.org/10.1016/0005-2787(74)90325-6
Ramanathan,, A., Robb,, G. B., & Chan,, S. H. (2016). mRNA capping: Biological functions and applications. Nucleic Acids Research, 44(16), 7511–7526. https://doi.org/10.1093/nar/gkw551
Reichow,, S. L., Hamma,, T., Ferré‐D`Amaré,, A. R., & Varani,, G. (2007). The structure and function of small nucleolar ribonucleoproteins. Nucleic Acids Research, 35(5), 1452–1464. https://doi.org/10.1093/nar/gkl1172
Rima,, B. K., Gatherer,, D., Young,, D. F., Norsted,, H., Randall,, R. E., & Davison,, A. J. (2014). Stability of the parainfluenza virus 5 genome revealed by deep sequencing of strains isolated from different hosts and following passage in cell culture. Journal of Virology, 88(7), 3826–3836. https://doi.org/10.1128/JVI.03351-13
Ringeard,, M., Marchand,, V., Decroly,, E., Motorin,, Y., & Bennasser,, Y. (2019). FTSJ3 is an RNA 2′‐O‐methyltransferase recruited by HIV to avoid innate immune sensing. Nature, 565(7740), 500–504. https://doi.org/10.1038/s41586-018-0841-4
Rizzetto,, M., Hoyer,, B., Canese,, M. G., Shih,, J. W., Purcell,, R. H., & Gerin,, J. L. (1980). Delta agent: Association of delta antigen with hepatitis B surface antigen and RNA in serum of delta‐infected chimpanzees. Proceedings of the National Academy of Sciences of the United States of America, 77(10), 6124–6128. https://doi.org/10.1073/pnas.77.10.6124
Robbins,, M., Judge,, A., Liang,, L., McClintock,, K., Yaworski,, E., & MacLachlan,, I. (2007). 2′‐O‐methyl‐modified RNAs act as TLR7 antagonists. Molecular Therapy, 15(9), 1663–1669. https://doi.org/10.1038/sj.mt.6300240
Rose,, J. K. (1975). Heterogneeous 5′‐terminal structures occur on vesicular stomatitis virus mRNAs. The Journal of Biological Chemistry, 250(20), 8098–8104.
Roth‐Cross,, J. K., Bender,, S. J., & Weiss,, S. R. (2008). Murine coronavirus mouse hepatitis virus is recognized by MDA5 and induces type I interferon in brain macrophages/microglia. Journal of Virology, 82(20), 9829–9838. https://doi.org/10.1128/jvi.01199-08
Roundtree,, I. A., Evans,, M. E., Pan,, T., & He,, C. (2017). Dynamic RNA modifications in gene expression regulation. Cell, 169(7), 1187–1200. https://doi.org/10.1016/j.cell.2017.05.045
Rueda,, P., García‐Barreno,, B., & Melero,, J. A. (1994). Loss of conserved cysteine residues in the attachment (G) glycoprotein of two human respiratory syncytial virus escape mutants that contain multiple A‐G substitutions (hypermutations). Virology, 198(2), 653–662.
Ryu,, W. S., Bayer,, M., & Taylor,, J. (1992). Assembly of hepatitis delta virus particles. Journal of Virology, 66(4), 2310–2315.
Sakurai,, M., Yano,, T., Kawabata,, H., Ueda,, H., & Suzuki,, T. (2010). Inosine cyanoethylation identifies A‐to‐I RNA editing sites in the human transcriptome. Nature Chemical Biology, 6(10), 733–740. https://doi.org/10.1038/nchembio.434
Samuel,, C. E. (2011). Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral. Virology, 411(2), 180–193. https://doi.org/10.1016/j.virol.2010.12.004
Sato,, S., Cornillez‐Ty,, C., & Lazinski,, D. W. (2004). By inhibiting replication, the large hepatitis delta antigen can indirectly regulate amber/W editing and its own expression. Journal of Virology, 78(15), 8120–8134. https://doi.org/10.1128/JVI.78.15.8120-8134.2004
Sato,, S., Wong,, S. K., & Lazinski,, D. W. (2001). Hepatitis delta virus minimal substrates competent for editing by ADAR1 and ADAR2. Journal of Virology, 75(18), 8547–8555. https://doi.org/10.1128/jvi.75.18.8547-8555.2001
Schuberth‐Wagner,, C., Ludwig,, J., Bruder,, A. K., Herzner,, A. M., Zillinger,, T., Goldeck,, M., … Schlee,, M. (2015). A conserved histidine in the RNA sensor RIG‐I controls immune tolerance to N1‐2′O‐methylated self RNA. Immunity, 43(1), 41–51. https://doi.org/10.1016/j.immuni.2015.06.015
Schwartz,, S., Bernstein,, D. A., Mumbach,, M. R., Jovanovic,, M., Herbst,, R. H., León‐Ricardo,, B. X., … Regev,, A. (2014). Transcriptome‐wide mapping reveals widespread dynamic‐regulated pseudouridylation of ncRNA and mRNA. Cell, 159(1), 148–162. https://doi.org/10.1016/J.CELL.2014.08.028
Schwartz,, S., & Motorin,, Y. (2017). Next‐generation sequencing technologies for detection of modified nucleotides in RNAs. RNA Biology, 14(9), 1124–1137. https://doi.org/10.1080/15476286.2016.1251543
Sharmeen,, L., Bass,, B., Sonenberg,, N., Weintraub,, H., & Groudine,, M. (1991). Tat‐dependent adenosine‐to‐inosine modification of wild‐type transactivation response RNA. Proceedings of the National Academy of Sciences of the United States of America, 88(18), 8096–8100. https://doi.org/10.1073/pnas.88.18.8096
Shi,, H., Wei,, J., & He,, C. (2019). Where, when, and how: Context‐dependent functions of RNA methylation writers, readers, and erasers. Molecular Cell, 74(4), 640–650. https://doi.org/10.1016/j.molcel.2019.04.025
Shi,, Z., Fujii,, K., Kovary,, K. M., Genuth,, N. R., Röst,, H. L., Teruel,, M. N., & Barna,, M. (2017). Heterogeneous ribosomes preferentially translate distinct subpools of mRNAs genome‐wide. Molecular Cell, 67(1), 71–83.e7. https://doi.org/10.1016/j.molcel.2017.05.021
Slotkin,, W., & Nishikura,, K. (2013). Adenosine‐to‐inosine RNA editing and human disease. Genome Medicine, 5(11), 105. https://doi.org/10.1186/gm508
Sommer,, S., Salditt‐Georgieff,, M., Bachenheimer,, S., Darnell,, J. E., Furuichi,, Y., Morgan,, M., & Shatkin,, A. J. (1976). The methylation of adenovirus‐specific nuclear and cytoplasmic RNA. Nucleic Acids Research, 3(3), 749–766. https://doi.org/10.1093/nar/3.3.749
Spenkuch,, F., Motorin,, Y., & Helm,, M. (2014). Pseudouridine: Still mysterious, but never a fake (uridine)! RNA Biology, 11(12), 1540–1554. https://doi.org/10.4161/15476286.2014.992278
Squires,, J. E., Patel,, H. R., Nousch,, M., Sibbritt,, T., Humphreys,, D. T., Parker,, B. J., … Preiss,, T. (2012). Widespread occurrence of 5‐methylcytosine in human coding and non‐coding RNA. Nucleic Acids Research, 40(11), 5023–5033. https://doi.org/10.1093/nar/gks144
Stoltzfus,, C. M., & Dane,, R. W. (1982). Accumulation of spliced avian retrovirus mRNA is inhibited in S‐adenosylmethionine‐depleted chicken embryo fibroblasts. Journal of Virology, 42(3), 918–931.
Stoltzfus,, C. M., & Dimock,, K. (1976). Evidence of methylation of B77 avian sarcoma virus genome RNA subunits. Journal of Virology, 18(2), 586–595.
Tan,, B., Liu,, H., Zhang,, S., Da Silva,, S. R., Zhang,, L., Meng,, J., … Gao,, S. J. (2017). Viral and cellular N6‐methyladenosine and N6,2′‐O‐dimethyladenosine epitranscriptomes in the KSHV life cycle. Nature Microbiology, 3(1), 108–120. https://doi.org/10.1038/s41564-017-0056-8
Taylor,, D. R., Puig,, M., Darnell,, M. E. R., Mihalik,, K., & Feinstone,, S. M. (2005). New antiviral pathway that mediates hepatitis C virus replicon interferon sensitivity through ADAR1. Journal of Virology, 79(10), 6291–6298. https://doi.org/10.1128/JVI.79.10.6291-6298.2005
Terenzi,, F., Hui,, D. J., Merrick,, W. C., & Sen,, G. C. (2006). Distinct induction patterns and functions of two closely related interferon‐inducible human genes, ISG54 and ISG56. Journal of Biological Chemistry, 281(45), 34064–34071. https://doi.org/10.1074/jbc.M605771200
Tirumuru,, N., & Wu,, L. (2019). HIV‐1 envelope proteins up‐regulate N6‐methyladenosine levels of cellular RNA independently of viral replication. Journal of Biological Chemistry, 294(9), 3249–3260. https://doi.org/10.1074/jbc.RA118.005608
Tirumuru,, N., Zhao,, B. S., Lu,, W., Lu,, Z., He,, C., & Wu,, L. (2016). N6‐methyladenosine of HIV‐1 RNA regulates viral infection and HIV‐1 Gag protein expression. eLife, 5. https://doi.org/10.7554/eLife.15528
Tollervey,, D., Lehtonen,, H., Carmo‐Fonseca,, M., & Hurt,, E. C. (1991). The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre‐rRNA processing in yeast. The EMBO Journal, 10(3), 573–583. Retrieved from. http://www.ncbi.nlm.nih.gov/pubmed/1825809
Topisirovic,, I., Svitkin,, Y. V., Sonenberg,, N., & Shatkin,, A. J. (2011). Cap and cap‐binding proteins in the control of gene expression. WIREs: RNA, 2(2), 277–298. https://doi.org/10.1002/wrna.52
Trim,, A. R., & Parker,, J. E. (1970). Preparation, purification and analyses of thirteen alkali‐stable dinucleotides from ribonucleic acid. Biochemical Journal, 116(4), 589–598. https://doi.org/10.1042/bj1160589
Trixl,, L., & Lusser,, A. (2019). The dynamic RNA modification 5‐methylcytosine and its emerging role as an epitranscriptomic mark. WIREs: RNA, 10(1), e1510. https://doi.org/10.1002/wrna.1510
Trotman,, J. B., Giltmier,, A. J., Mukherjee,, C., & Schoenberg,, D. R. (2017). RNA guanine‐7 methyltransferase catalyzes the methylation of cytoplasmically recapped RNAs. Nucleic Acids Research, 45(18), 10726–10739. https://doi.org/10.1093/nar/gkx801
Tsai,, K., Courtney,, D. G., & Cullen,, B. R. (2018). Addition of m6A to SV40 late mRNAs enhances viral structural gene expression and replication. PLoS Pathogens, 14(2), e1006919. https://doi.org/10.1371/journal.ppat.1006919
van den Hoogen,, B. G., van Boheemen,, S., de Rijck,, J., van Nieuwkoop,, S., Smith,, D. J., Laksono,, B., … Fouchier,, R. A. M. (2014). Excessive production and extreme editing of human metapneumovirus defective interfering RNA is associated with type I IFN induction. Journal of General Virology, 95(PART 8), 1625–1633. https://doi.org/10.1099/vir.0.066100-0
van Duijn,, L. P., Kasperaitis,, M., Ameling,, C., & Voorma,, H. O. (1986). Additional methylation at the N(2)‐position of the cap of 26S Semliki Forest virus late mRNA and initiation of translation. Virus Research, 5(1), 61–66.
Vieyres,, G., & Pietschmann,, T. (2019). HCV pit stop at the lipid droplet: Refuel lipids and put on a lipoprotein coat before exit. Cell, 8(3), 233. https://doi.org/10.3390/cells8030233
Wei,, C.‐M., Gershowitz,, A., & Moss,, B. (1975). Methylated nucleotides block 5′ terminus of HeLa cell messenger RNA. Cell, 4(4), 379–386. https://doi.org/10.1016/0092-8674(75)90158-0
Wei,, C. M., & Moss,, B. (1975). Methylated nucleotides block 5′‐terminus of vaccinia virus messenger RNA. Proceedings of the National Academy of Sciences of the United States of America, 72(1), 318–322. https://doi.org/10.1073/pnas.72.1.318
Wong,, S. K., & Lazinski,, D. W. (2002). Replicating hepatitis delta virus RNA is edited in the nucleus by the small form of ADAR1. Proceedings of the National Academy of Sciences of the United States of America, 99(23), 15118–15123. https://doi.org/10.1073/pnas.232416799
Yang,, X., Yang,, Y., Sun,, B.‐F., Chen,, Y.‐S., Xu,, J.‐W., Lai,, W.‐Y., … Yang,, Y.‐G. (2017). 5‐Methylcytosine promotes mRNA export – NSUN2 as the methyltransferase and ALYREF as an m5C reader. Cell Research, 27(5), 606–625. https://doi.org/10.1038/cr.2017.55
Ye,, F., Chen,, E. R., & Nilsen,, T. W. (2017). Kaposi`s sarcoma‐associated herpesvirus utilizes and manipulates RNA N⁶‐adenosine methylation to promote lytic replication. Journal of Virology, 91(16), e00466–e00417. https://doi.org/10.1128/JVI.00466-17
Yedavalli,, V. S. R. K., & Jeang,, K.‐T. (2010). Trimethylguanosine capping selectively promotes expression of Rev‐dependent HIV‐1 RNAs. Proceedings of the National Academy of Sciences of the United States of America, 107(33), 14787–14792. https://doi.org/10.1073/pnas.1009490107
Zalinger,, Z. B., Elliott,, R., Rose,, K. M., & Weiss,, S. R. (2015). MDA5 is critical to host defense during infection with murine coronavirus. Journal of Virology, 89(24), 12330–12340. https://doi.org/10.1128/jvi.01470-15
Zerfass,, K., & Beier,, H. (1992). Pseudouridine in the anticodon GψA of plant cytoplasmic tRNA Tyr is required for UAG and UAA suppression in the TMV‐specific context. Nucleic Acids Research, 20(22), 5911–5918. https://doi.org/10.1093/nar/20.22.5911
Zhang,, L.‐S., Liu,, C., Ma,, H., Dai,, Q., Sun,, H.‐L., Luo,, G., … He,, C. (2019). Transcriptome‐wide mapping of internal N7‐methylguanosine methylome in mammalian mRNA. Molecular Cell, 74(6), 1304–1316.e8. https://doi.org/10.1016/j.molcel.2019.03.036
Zheng,, G., Dahl,, J. A., Niu,, Y., Fedorcsak,, P., Huang,, C. M., Li,, C. J., … He,, C. (2013). ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Molecular Cell, 49(1), 18–29. https://doi.org/10.1016/j.molcel.2012.10.015
Zhou,, J., Wan,, J., Gao,, X., Zhang,, X., Jaffrey,, S. R., & Qian,, S. B. (2015). Dynamic m6A mRNA methylation directs translational control of heat shock response. Nature, 526(7574), 591–594. https://doi.org/10.1038/nature15377
Zhou,, Y., Ray,, D., Zhao,, Y., Dong,, H., Ren,, S., Li,, Z., … Li,, H. (2007). Structure and function of flavivirus NS5 methyltransferase. Journal of Virology, 81(8), 3891–3903. https://doi.org/10.1128/JVI.02704-06
Zhu,, Y., Pirnie,, S. P., & Carmichael,, G. G. (2017). High‐throughput and site‐specific identification of 2′‐O‐methylation sites using ribose oxidation sequencing (RibOxi‐seq). RNA, 23(8), 1303–1314. https://doi.org/10.1261/rna.061549.117
Züst,, R., Cervantes‐Barragan,, L., Habjan,, M., Maier,, R., Neuman,, B. W., Ziebuhr,, J., … Thiel,, V. (2011). Ribose 2′‐O‐methylation provides a molecular signature for the distinction of self and non‐self mRNA dependent on the RNA sensor Mda5. Nature Immunology, 12(2), 137–143. https://doi.org/10.1038/ni.1979

Access to this WIREs title is by subscription only.

Recommend to Your
Librarian Now!

The latest WIREs articles in your inbox

Sign Up for Article Alerts