The alternative cap-binding complex is required for antiviral defense in vivo


Autoři: Anna Gebhardt aff001;  Valter Bergant aff001;  Daniel Schnepf aff003;  Markus Moser aff005;  Arno Meiler aff002;  Dieudonnée Togbe aff007;  Claire Mackowiak aff007;  Line Reinert aff008;  Søren R. Paludan aff008;  Bernhard Ryffel aff007;  Alexey Stukalov aff001;  Peter Staeheli aff003;  Andreas Pichlmair aff001
Působiště autorů: Institute of Virology, Technical University of Munich, School of Medicine, Munich, Germany aff001;  Innate Immunity Laboratory, Max-Planck Institute of Biochemistry, Martinsried, Germany aff002;  Institute of Virology, University of Freiburg, Freiburg, Germany aff003;  Spemann Graduate School of Biology and Medicine, Albert Ludwigs University Freiburg, Freiburg, Germany aff004;  Department of Molecular Medicine, Max-Planck Institute of Biochemistry, Martinsried, Germany aff005;  Center for Translational Cancer Research (TranslaTUM), TUM School of Medicine, Technical University of Munich, Munich, Germany aff006;  INEM, Experimental Molecular Immunology, UMR7355 CNRS and University, Orleans, France aff007;  Department of Biomedicine, University of Aarhus, Aarhus, Denmark aff008;  Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Cape Town, South Africa aff009;  Faculty of Medicine, University of Freiburg, Freiburg, Germany aff010;  German Center for Infection Research (DZIF), Munich partner site, Munich, Germany aff011
Vyšlo v časopise: The alternative cap-binding complex is required for antiviral defense in vivo. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008155
Kategorie: Research Article
doi: 10.1371/journal.ppat.1008155

Souhrn

Cellular response to environmental challenges requires immediate and precise regulation of transcriptional programs. During viral infections, this includes the expression of antiviral genes that are essential to combat the pathogen. Transcribed mRNAs are bound and escorted to the cytoplasm by the cap-binding complex (CBC). We recently identified a protein complex consisting of NCBP1 and NCBP3 that, under physiological conditions, has redundant function to the canonical CBC, consisting of NCBP1 and NCBP2. Here, we provide evidence that NCBP3 is essential to mount a precise and appropriate antiviral response. Ncbp3-deficient cells allow higher virus growth and elicit a reduced antiviral response, a defect happening on post-transcriptional level. Ncbp3-deficient mice suffered from severe lung pathology and increased morbidity after influenza A virus challenge. While NCBP3 appeared to be particularly important during viral infections, it may be more broadly involved to ensure proper protein expression.

Klíčová slova:

Antiviral immune response – Cytokines – Immune response – Influenza A virus – Messenger RNA – Small interfering RNAs – Viral replication – Vesicular stomatitis virus


Zdroje

1. Gebhardt A, Laudenbach BT, Pichlmair A. Discrimination of Self and Non-Self Ribonucleic Acids. J Interferon Cytokine Res. 2017;37(5):184–97. doi: 10.1089/jir.2016.0092 28475460; PubMed Central PMCID: PMC5439445.

2. Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol. 2015;16(4):343–53. Epub 2015/03/20. doi: 10.1038/ni.3123 25789684; PubMed Central PMCID: PMC4507498.

3. Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol. 2014;32:513–45. Epub 2014/02/22. doi: 10.1146/annurev-immunol-032713-120231 24555472; PubMed Central PMCID: PMC4313732.

4. Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Current opinion in virology. 2011;1(6):519–25. Epub 2012/02/14. doi: 10.1016/j.coviro.2011.10.008 22328912; PubMed Central PMCID: PMC3274382.

5. Hubel P, Urban C, Bergant V, Schneider WM, Knauer B, Stukalov A, et al. A protein-interaction network of interferon-stimulated genes extends the innate immune system landscape. Nat Immunol. 2019;20(4):493–502. Epub 2019/03/06. doi: 10.1038/s41590-019-0323-3 30833792.

6. Gonatopoulos-Pournatzis T, Cowling VH. Cap-binding complex (CBC). The Biochemical journal. 2014;457(2):231–42. Epub 2013/12/21. doi: 10.1042/BJ20131214 24354960; PubMed Central PMCID: PMC3901397.

7. Mazza C, Ohno M, Segref A, Mattaj IW, Cusack S. Crystal structure of the human nuclear cap binding complex. Molecular cell. 2001;8(2):383–96. doi: 10.1016/s1097-2765(01)00299-4 11545740.

8. Topisirovic I, Svitkin YV, Sonenberg N, Shatkin AJ. Cap and cap-binding proteins in the control of gene expression. Wiley interdisciplinary reviews RNA. 2011;2(2):277–98. Epub 2011/10/01. doi: 10.1002/wrna.52 21957010.

9. Kohler A, Hurt E. Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol. 2007;8(10):761–73. Epub 2007/09/06. doi: 10.1038/nrm2255 17786152.

10. Gebhardt A, Habjan M, Benda C, Meiler A, Haas DA, Hein MY, et al. mRNA export through an additional cap-binding complex consisting of NCBP1 and NCBP3. Nature communications. 2015;6:8192. doi: 10.1038/ncomms9192 26382858; PubMed Central PMCID: PMC4595607.

11. Hale BG, Randall RE, Ortin J, Jackson D. The multifunctional NS1 protein of influenza A viruses. The Journal of general virology. 2008;89(Pt 10):2359–76. doi: 10.1099/vir.0.2008/004606-0 18796704.

12. Kuss SK, Mata MA, Zhang L, Fontoura BM. Nuclear imprisonment: viral strategies to arrest host mRNA nuclear export. Viruses. 2013;5(7):1824–49. Epub 2013/07/23. doi: 10.3390/v5071824 23872491; PubMed Central PMCID: PMC3738964.

13. Bartlett DL, Liu Z, Sathaiah M, Ravindranathan R, Guo Z, He Y, et al. Oncolytic viruses as therapeutic cancer vaccines. Mol Cancer. 2013;12(1):103. Epub 2013/09/12. doi: 10.1186/1476-4598-12-103 24020520; PubMed Central PMCID: PMC3847443.

14. Chiocca EA, Rabkin SD. Oncolytic viruses and their application to cancer immunotherapy. Cancer Immunol Res. 2014;2(4):295–300. Epub 2014/04/26. doi: 10.1158/2326-6066.CIR-14-0015 24764576; PubMed Central PMCID: PMC4303349.

15. Zeitlinger J, Stark A. Developmental gene regulation in the era of genomics. Dev Biol. 2010;339(2):230–9. Epub 2010/01/05. doi: 10.1016/j.ydbio.2009.12.039 20045679.

16. Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nature reviews. 2014;14(1):36–49. Epub 2013/12/24. doi: 10.1038/nri3581 24362405; PubMed Central PMCID: PMC4084561.

17. Carpenter S, Ricci EP, Mercier BC, Moore MJ, Fitzgerald KA. Post-transcriptional regulation of gene expression in innate immunity. Nature reviews. 2014;14(6):361–76. Epub 2014/05/24. doi: 10.1038/nri3682 24854588.

18. Mears HV, Sweeney TR. Better together: the role of IFIT protein-protein interactions in the antiviral response. The Journal of general virology. 2018;99(11):1463–77. Epub 2018/09/21. doi: 10.1099/jgv.0.001149 30234477.

19. Bego MG, Cote E, Aschman N, Mercier J, Weissenhorn W, Cohen EA. Vpu Exploits the Cross-Talk between BST2 and the ILT7 Receptor to Suppress Anti-HIV-1 Responses by Plasmacytoid Dendritic Cells. PLoS Pathog. 2015;11(7):e1005024. Epub 2015/07/15. doi: 10.1371/journal.ppat.1005024 26172439; PubMed Central PMCID: PMC4501562.

20. Zhao C, Hsiang TY, Kuo RL, Krug RM. ISG15 conjugation system targets the viral NS1 protein in influenza A virus-infected cells. Proc Natl Acad Sci U S A. 2010;107(5):2253–8. Epub 2010/02/06. doi: 10.1073/pnas.0909144107 20133869; PubMed Central PMCID: PMC2836655.

21. Perng YC, Lenschow DJ. ISG15 in antiviral immunity and beyond. Nature reviews Microbiology. 2018;16(7):423–39. Epub 2018/05/18. doi: 10.1038/s41579-018-0020-5 29769653.

22. Schulze WM, Stein F, Rettel M, Nanao M, Cusack S. Structural analysis of human ARS2 as a platform for co-transcriptional RNA sorting. Nature communications. 2018;9(1):1701. Epub 2018/04/29. doi: 10.1038/s41467-018-04142-7 29703953; PubMed Central PMCID: PMC5923425.

23. Sandler NG, Bosinger SE, Estes JD, Zhu RT, Tharp GK, Boritz E, et al. Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression. Nature. 2014;511(7511):601–5. Epub 2014/07/22. doi: 10.1038/nature13554 25043006; PubMed Central PMCID: PMC4418221.

24. Newton AH, Cardani A, Braciale TJ. The host immune response in respiratory virus infection: balancing virus clearance and immunopathology. Semin Immunopathol. 2016;38(4):471–82. Epub 2016/03/12. doi: 10.1007/s00281-016-0558-0 26965109; PubMed Central PMCID: PMC4896975.

25. Peiris JS, Cheung CY, Leung CY, Nicholls JM. Innate immune responses to influenza A H5N1: friend or foe? Trends in immunology. 2009;30(12):574–84. Epub 2009/10/30. doi: 10.1016/j.it.2009.09.004 19864182; PubMed Central PMCID: PMC5068224.

26. Quicke KM, Diamond MS, Suthar MS. Negative regulators of the RIG-I-like receptor signaling pathway. Eur J Immunol. 2017;47(4):615–28. Epub 2017/03/16. doi: 10.1002/eji.201646484 28295214; PubMed Central PMCID: PMC5554756.

27. Cao X. Self-regulation and cross-regulation of pattern-recognition receptor signalling in health and disease. Nature reviews. 2016;16(1):35–50. Epub 2015/12/30. doi: 10.1038/nri.2015.8 26711677.

28. McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A. Type I interferons in infectious disease. Nature reviews. 2015;15(2):87–103. Epub 2015/01/24. doi: 10.1038/nri3787 25614319.

29. Klinkhammer J, Schnepf D, Ye L, Schwaderlapp M, Gad HH, Hartmann R, et al. IFN-lambda prevents influenza virus spread from the upper airways to the lungs and limits virus transmission. eLife. 2018;7. Epub 2018/04/14. doi: 10.7554/eLife.33354 29651984; PubMed Central PMCID: PMC5953542.

30. Kochs G, Koerner I, Thiel L, Kothlow S, Kaspers B, Ruggli N, et al. Properties of H7N7 influenza A virus strain SC35M lacking interferon antagonist NS1 in mice and chickens. The Journal of general virology. 2007;88(Pt 5):1403–9. Epub 2007/04/07. doi: 10.1099/vir.0.82764-0 17412966.

31. Pichlmair A, Lassnig C, Eberle CA, Gorna MW, Baumann CL, Burkard TR, et al. IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat Immunol. 2011;12(7):624–30. doi: 10.1038/ni.2048 21642987.

32. Reuther P, Gopfert K, Dudek AH, Heiner M, Herold S, Schwemmle M. Generation of a variety of stable Influenza A reporter viruses by genetic engineering of the NS gene segment. Sci Rep. 2015;5:11346. Epub 2015/06/13. doi: 10.1038/srep11346 26068081; PubMed Central PMCID: PMC4464305.

33. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, et al. A conditional knockout resource for the genome-wide study of mouse gene function. Nature. 2011;474(7351):337–42. Epub 2011/06/17. doi: 10.1038/nature10163 21677750; PubMed Central PMCID: PMC3572410.

34. Pettitt SJ, Liang Q, Rairdan XY, Moran JL, Prosser HM, Beier DR, et al. Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nature methods. 2009;6(7):493–5. Epub 2009/06/16. doi: 10.1038/nmeth.1342 19525957; PubMed Central PMCID: PMC3555078.

35. Scaturro P, Stukalov A, Haas DA, Cortese M, Draganova K, Plaszczyca A, et al. An orthogonal proteomic survey uncovers novel Zika virus host factors. Nature. 2018;561(7722):253–7. Epub 2018/09/05. doi: 10.1038/s41586-018-0484-5 30177828.

36. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26(12):1367–72. Epub 2008/11/26. doi: 10.1038/nbt.1511 19029910.

37. Cox J, Hein MY, Luber CA, Paron I, Nagaraj N, Mann M. MaxLFQ allows accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction. Mol Cell Proteomics. 2014. Epub 2014/06/20. doi: 10.1074/mcp.M113.031591 PubMed PMID: 24942700.

38. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic acids research. 2015;43(7):e47. Epub 2015/01/22. doi: 10.1093/nar/gkv007 25605792; PubMed Central PMCID: PMC4402510.

39. Rusinova I, Forster S, Yu S, Kannan A, Masse M, Cumming H, et al. Interferome v2.0: an updated database of annotated interferon-regulated genes. Nucleic acids research. 2013;41(Database issue):D1040–6. Epub 2012/12/04. doi: 10.1093/nar/gks1215 23203888; PubMed Central PMCID: PMC3531205.

40. Michaudel C, Mackowiak C, Maillet I, Fauconnier L, Akdis CA, Sokolowska M, et al. Ozone exposure induces respiratory barrier biphasic injury and inflammation controlled by IL-33. J Allergy Clin Immunol. 2018;142(3):942–58. Epub 2018/01/15. doi: 10.1016/j.jaci.2017.11.044 29331644.

Štítky
Hygiena a epidemiologie Infekční lékařství Laboratoř

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