Terminal uridylyltransferases target RNA viruses as part of the innate immune system

Nature Structural and Molecular Biology

Volumn 25, Issue 9, 2018, Pages 778-786

  Le Pen, Jérémie ^a,b,i   Jiang, Hongbing ^c   Di Domenico, Tomás ^a,b,d,j   Kneuss, Emma ^a,e   Kosałka, Joanna ^a,b   Leung, Christian ^c   Morgan, Marcos ^f,g   Much, Christian ^f,g   Rudolph, Konrad L M ^a,b,d   Enright, Anton J ^h   O’Carroll, Dónal ^f,g   Wang, David ^c   Miska, Eric A ^a,b,d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

^g EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

^h EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

ⁱ ROCKEFELLER UNIVERSITY   (United States)

^j Structural Biology and Biocomputing Programme   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HEXOSE 1 PHOSPHATE URIDYLYLTRANSFERASE; PROTEIN CDE1; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG; RNA POLYMERASE; TRANSCRIPTOME; UTP-RNA URIDYLYLTRANSFERASE; VIRUS RNA;

ANTIVIRAL ACTIVITY; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE DELETION; INFLUENZA A VIRUS; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA INTERFERENCE; RNA VIRUS; VIRUS GENOME; A-549 CELL LINE; ANIMAL; ENZYMOLOGY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS REPLICATION;

A549 CELLS; ANIMALS; CAENORHABDITIS ELEGANS; HUMANS; IMMUNITY, INNATE; RNA INTERFERENCE; RNA NUCLEOTIDYLTRANSFERASES; RNA VIRUSES; RNA, VIRAL; TRANSCRIPTOME; VIRUS REPLICATION;

EID: 85052333834     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/s41594-018-0106-9     Document Type: Article

References (49)

1. Ding, S.-W. & Voinnet, O. Antiviral immunity directed by small RNAs. Cell 130, 413–426 (2007).
2. Goubau, D., Deddouche, S. & Reis e Sousa, C. Cytosolic sensing of viruses. Immunity 38, 855–869 (2013).
3. Schoggins, J. W. et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472, 481–485 (2011).
4. Félix, M.-A. et al. Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLoS Biol. 9, e1000586 (2011).
5. Ashe, A. et al. A deletion polymorphism in the Caenorhabditis elegans RIG-I homolog disables viral RNA dicing and antiviral immunity. eLife 2, e00994 (2013).
6. Ashe, A., Sarkies, P., Le Pen, J., Tanguy, M. & Miska, E. A. Antiviral RNAi against Orsay virus is neither systemic nor transgenerational in Caenorhabditis elegans. J. Virol. 89, 12035–12046 (2015).
7. Guo, Y. R. et al. Crystal structure of a nematode-infecting virus. Proc. Natl. Acad. Sci. USA 111, 12781–12786 (2014).
8. Jiang, H. et al. Orsay virus utilizes ribosomal frameshifting to express a novel protein that is incorporated into virions. Virology 450-451, 213–221 (2014).
9. Franz, C. J. et al. Orsay, Santeuil and Le Blanc viruses primarily infect intestinal cells in Caenorhabditis nematodes. Virology 448, 255–264 (2014).
10. Sarkies, P., Ashe, A., Le Pen, J., McKie, M. A. & Miska, E. A. Competition between virus-derived and endogenous small RNAs regulates gene expression in Caenorhabditis elegans. Genome Res. 23, 1258–1270 (2013).
11. Guo, X., Zhang, R., Wang, J., Ding, S.-W. & Lu, R. Homologous RIG-I-like helicase proteins direct RNAi-mediated antiviral immunity in C. elegans by distinct mechanisms. Proc. Natl. Acad. Sci. USA 110, 16085–16090 (2013).
12. Fan, Y. et al. Structure of a pentameric virion-associated fiber with a potential role in Orsay virus entry to host cells. PLoS Pathog. 13, e1006231 (2017).
13. Duchaine, T. F. et al. Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways. Cell 124, 343–354 (2006).
14. Tabara, H., Yigit, E., Siomi, H. & Mello, C. C. The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans. Cell 109, 861–871 (2002).
15. Jiang, H., Chen, K., Sandoval, L. E., Leung, C. & Wang, D. An evolutionarily conserved pathway essential for Orsay virus infection of Caenorhabditis elegans. MBio 8, e00940–17 (2017).
16. Tanguy, M. et al. An alternative STAT signaling pathway acts in viral immunity in Caenorhabditis elegans. MBio 8, e00924–17 (2017).
17. van Wolfswinkel, J. C. et al. CDE-1 affects chromosome segregation through uridylation of CSR-1-bound siRNAs. Cell 139, 135–148 (2009).
18. Olsen, A., Vantipalli, M. C. & Lithgow, G. J. Checkpoint proteins control survival of the postmitotic cells in Caenorhabditis elegans. Science 312, 1381–1385 (2006).
19. Kwak, J. E. & Wickens, M. A family of poly(U) polymerases. RNA 13, 860–867 (2007).
20. Heo, I. et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 138, 696–708 (2009).
21. Norbury, C. J. Cytoplasmic RNA: a case of the tail wagging the dog. Nat. Rev. Mol. Cell Biol. 14, 643–653 (2013).
22. Wickens, M. & Kwak, J. E. Molecular biology. A tail tale for U. Science 319, 1344–1345 (2008).
23. 6 A and U-tail. Cell 158, 980–987 (2014).
24. Rissland, O. S. & Norbury, C. J. Decapping is preceded by 3′ uridylation in a novel pathway of bulk mRNA turnover. Nat. Struct. Mol. Biol. 16, 616–623 (2009).
25. Morgan, M. et al. mRNA 3′ uridylation and poly(A) tail length sculpt the mammalian maternal transcriptome. Nature 548, 347–351 (2017).
26. Lim, J. et al. Uridylation by TUT4 and TUT7 marks mRNA for degradation. Cell 159, 1365–1376 (2014).
27. Chang, H., Lim, J., Ha, M. & Kim, V. N. TAIL-seq: genome-wide determination of poly(A) tail length and 3′ end modifications. Mol. Cell 53, 1044–1052 (2014).
28. Miki, T. S., Rüegger, S., Gaidatzis, D., Stadler, M. B. & Großhans, H. Engineering of a conditional allele reveals multiple roles of XRN2 in Caenorhabditis elegans development and substrate specificity in microRNA turnover. Nucleic Acids Res. 42, 4056–4067 (2014).
29. Kamath, R. S. et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231–237 (2003).
30. Molleston, J. M. et al. A conserved virus-induced cytoplasmic TRAMP-like complex recruits the exosome to target viral RNA for degradation. Genes Dev. 30, 1658–1670 (2016).
31. Huo, Y. et al. Widespread 3′-end uridylation in eukaryotic RNA viruses. Sci. Rep. 6, 25454 (2016).
32. Samji, T. Influenza A: understanding the viral life cycle. Yale J. Biol. Med. 82, 153–159 (2009).
33. Rehwinkel, J. Is anti-viral defence the evolutionary origin of mRNA turnover? BioEssays 38, 817 (2016).
34. Hamid, F. M. & Makeyev, E. V. Exaptive origins of regulated mRNA decay in eukaryotes. BioEssays 38, 830–838 (2016).
35. Manokaran, G. et al. Dengue subgenomic RNA binds TRIM25 to inhibit interferon expression for epidemiological fitness. Science 350, 217–221 (2015).
36. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).
37. Fire, A. Integrative transformation of Caenorhabditis elegans. EMBO J. 5, 2673–2680 (1986).
38. Jorgensen, E. M. & Mango, S. E. The art and design of genetic screens: Caenorhabditis elegans. Nat. Rev. Genet. 3, 356–369 (2002).
39. Sarov, M. et al. A genome-scale resource for in vivo tag-based protein function exploration in C. elegans. Cell 150, 855–866 (2012).
40. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
41. Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
42. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
43. Paix, A., Folkmann, A., Rasoloson, D. & Seydoux, G. High efficiency, homology-directed genome editing in Caenorhabditis elegans using CRISPR-Cas9 ribonucleoprotein complexes. Genetics 201, 47–54 (2015).
44. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17, 10 (2011).
45. Harris, T. W. et al. WormBase 2014: new views of curated biology. Nucleic Acids Res. 42, D789–D793 (2014).
46. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
47. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
48. Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614–620 (2014).
49. Kawakami, E. et al. Strand-specific real-time RT-PCR for distinguishing influenza vRNA, cRNA, and mRNA. J. Virol. Methods 173, 1–6 (2011).