1887

Abstract

Viral infections activate the powerful interferon (IFN) response that induces the expression of several hundred IFN stimulated genes (ISGs). The principal role of this extensive response is to create an unfavourable environment for virus replication and to limit spread; however, untangling the biological consequences of this large response is complicated. In addition to a seemingly high degree of redundancy, several ISGs are usually required in combination to limit infection as individual ISGs often have low to moderate antiviral activity. Furthermore, what ISG or combination of ISGs are antiviral for a given virus is usually not known. For these reasons, and since the function(s) of many ISGs remains unexplored, genome-wide approaches are well placed to investigate what aspects of this response result in an appropriate, virus-specific phenotype. This review discusses the advances screening approaches have provided for the study of host defence mechanisms, including clustered regularly interspaced short palindromic repeats/CRISPR associated protein 9 (CRISPR/Cas9), ISG expression libraries and RNA interference (RNAi) technologies.

Funding
This study was supported by the:
  • Academy of Medical Sciences (Award SFB003/1028)
    • Principle Award Recipient: DavidJ Hughes
  • Wellcome Trust (Award ISSF)
    • Principle Award Recipient: DavidJ Hughes
  • Medical Research Council (Award MR/N001796/1)
    • Principle Award Recipient: FinnGrey
  • Biotechnology and Biological Sciences Research Council (Award BBS/E/D/20002172)
    • Principle Award Recipient: FinnGrey
  • Tenovus (Award T20/63)
    • Principle Award Recipient: DavidJ Hughes
  • Academy of Medical Sciences (Award SFB003/1028)
    • Principle Award Recipient: ChloeE. Jones
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001603
2021-05-21
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/102/5/jgv001603.html?itemId=/content/journal/jgv/10.1099/jgv.0.001603&mimeType=html&fmt=ahah

References

  1. Robinson M, Schor S, Barouch-Bentov R, Einav S. Viral journeys on the intracellular highways. Cell Mol Life Sci 2018; 75:3693–3714 [View Article][PubMed]
    [Google Scholar]
  2. Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 2011; 1:519–525 [View Article][PubMed]
    [Google Scholar]
  3. Randall RE, Goodbourn S. Interferons and viruses: An interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 2008; 89:1–47 [View Article]
    [Google Scholar]
  4. Isaacs A, Lindenmann J. Virus interference. I. The interferon. J Interferon Res 1987; 7:429–438 [View Article]
    [Google Scholar]
  5. Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: A complex web of host defenses. Annu Rev Immunol 2014; 32:513–545 [View Article][PubMed]
    [Google Scholar]
  6. Fensterl V, Chattopadhyay S, Sen GC. No love lost between viruses and interferons. Annu Rev Virol 2015; 2:549–572 [View Article][PubMed]
    [Google Scholar]
  7. Lee AJ, Ashkar AA. The dual nature of type I and type II interferons. Front Immunol 2018; 9:2061 [View Article][PubMed]
    [Google Scholar]
  8. McNab F, Mayer-Barber K, Sher A, Wack A, O’Garra A. Type I interferons in infectious disease. Nat Rev Immunol 2015; 15:87–103 [View Article]
    [Google Scholar]
  9. Levy DE, Marié IJ, Durbin JE. Induction and function of type I and III interferon in response to viral infection. Curr Opin Virol 2011; 1:476–486 [View Article][PubMed]
    [Google Scholar]
  10. Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nat Rev Immunol 2014; 14:36–49 [View Article]
    [Google Scholar]
  11. Balachandran S, Roberts PC, Brown LE, Truong H, Pattnaik AK. Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 2000; 13:129–141 [View Article][PubMed]
    [Google Scholar]
  12. Silverman RH. Viral encounters with 2’,5’-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 2007; 81:12720–12729 [View Article][PubMed]
    [Google Scholar]
  13. Shalem O, Sanjana NE, Zhang F. High-throughput functional genomics using CRISPR–Cas9. Nat Rev Genet 2015; 16:299–311 [View Article][PubMed]
    [Google Scholar]
  14. Schneeberger K. Using next-generation sequencing to isolate mutant genes from forward genetic screens. Nat Rev Genet 2014; 15:662–676 [View Article][PubMed]
    [Google Scholar]
  15. Moresco EMY, Li X, Beutler B. Going forward with genetics: Recent technological advances and forward genetics in mice. Am J Pathol 2013; 182:1462–1473 [View Article][PubMed]
    [Google Scholar]
  16. Flint M, Chatterjee P, Lin DL, McMullan LK, Shrivastava-Ranjan P. A genome-wide CRISPR screen identifies N-acetylglucosamine-1-phosphate transferase as a potential antiviral target for Ebola virus. Nat Commun 2019; 10:285 [View Article][PubMed]
    [Google Scholar]
  17. Han J, Perez JT, Chen C, Li Y, Benitez A et al. Genome-wide CRISPR/Cas9 screen identifies host factors essential for influenza virus replication. Cell Rep 2018; 23:596–607 [View Article][PubMed]
    [Google Scholar]
  18. Marceau CD, Puschnik AS, Majzoub K, Ooi YS, Brewer SM. Genetic dissection of Flaviviridae host factors through genome-scale CRISPR screens. Nature 2016; 535:159–163 [View Article][PubMed]
    [Google Scholar]
  19. Karlas A, MacHuy N, Shin Y, Pleissner KP, Artarini A. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 2010; 463:818–822 [View Article][PubMed]
    [Google Scholar]
  20. Krishnan MN, Ng A, Sukumaran B, Gilfoy FD, Uchil PD. RNA interference screen for human genes associated with West Nile virus infection. Nature 2008; 455:242–245 [View Article][PubMed]
    [Google Scholar]
  21. Zhou H, Xu M, Huang Q, Gates AT, Zhang XD et al. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 2008; 4:495–504 [View Article][PubMed]
    [Google Scholar]
  22. Zhou A, Paranjape JM, Der SD, Williams BRG, Silverman RH. Interferon action in triply deficient mice reveals the existence of alternative antiviral pathways. Virology 1999; 258:435–440 [View Article][PubMed]
    [Google Scholar]
  23. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011; 472:481–485 [View Article][PubMed]
    [Google Scholar]
  24. Bodapati S, Daley TP, Lin X, Zou J, LS Q. A benchmark of algorithms for the analysis of pooled CRISPR screens. Genome Biol 2020; 21:62 [View Article]
    [Google Scholar]
  25. Reimand J, Isserlin R, Voisin V, Kucera M, Tannus-Lopes C. Pathway enrichment analysis and visualization of omics data using g:Profiler, GSEA, Cytoscape and EnrichmentMap. Nat Protoc 2019; 14:482–517 [View Article][PubMed]
    [Google Scholar]
  26. Ramadan N, Flockhart I, Booker M, Perrimon N, Mathey-Prevot B. Design and implementation of high-throughput RNAi screens in cultured Drosophila cells. Nat Protoc 2007; 2:2245–2264 [View Article][PubMed]
    [Google Scholar]
  27. Echeverri CJ, Perrimon N. High-throughput RNAi screening in cultured cells: a user’s guide. Nat Rev Genet 2006; 7:373–384 [View Article][PubMed]
    [Google Scholar]
  28. Conrad C, Gerlich DW. Automated microscopy for high-content RNAi screening. J Cell Biol 2010; 188:453–461 [View Article][PubMed]
    [Google Scholar]
  29. Micklem DR, Blø M, Bergström P, Hodneland E, Tiron C. Flow cytometry-based functional selection of RNA interference triggers for efficient epi-allelic analysis of therapeutic targets. BMC Biotechnol 2014; 14:57 [View Article][PubMed]
    [Google Scholar]
  30. Misra A, Green MR. Fluorescence reporter-based genome-wide RNA interference screening to identify alternative splicing regulators. In Methods in Molecular Biology Vol 1507 2017 pp 1–12 [View Article][PubMed]
    [Google Scholar]
  31. Suratanee A, Rebhan I, Matula P, Kumar A, Kaderali L. Detecting host factors involved in virus infection by observing the clustering of infected cells in siRNA screening images. Bioinformatics 2010; 26:i653–8 [View Article][PubMed]
    [Google Scholar]
  32. Mali P, Yang L, Esvelt KM, Aach J, Guell M et al. RNA-guided human genome engineering via Cas9. Science 2013; 339:823–826 [View Article]
    [Google Scholar]
  33. Jinek M, East A, Cheng A, Lin S, Ma E. RNA-programmed genome editing in human cells. Elife 2013; 2:2 [View Article]
    [Google Scholar]
  34. Cong L, Ran FA, Cox D, Lin S, Barretto R. Multiplex genome engineering using CRISPR/Cas systems. Science 2013; 339:819–823 [View Article]
    [Google Scholar]
  35. Doudna JA, Charpentier E. The new frontier of genome engineering with CRISPR-Cas9. Science 2014; 346:1258096 [View Article]
    [Google Scholar]
  36. Jiang F, Doudna JA. CRISPR–Cas9 structures and mechanisms. Annu Rev Biophys 2017; 46:505–529 [View Article][PubMed]
    [Google Scholar]
  37. Khan S, Mahmood MS, Rahman SU, Zafar H, Habibullah S. CRISPR/Cas9: The Jedi against the dark empire of diseases. J Biomed Sci 2018; 25:1–18 [View Article]
    [Google Scholar]
  38. Chew SK, Rad R, Futreal PA, Bradley A, Liu P. Genetic screens using the piggyBac transposon. Methods 2011; 53:366–371 [View Article][PubMed]
    [Google Scholar]
  39. Chow RD, Guzman CD, Wang G, Schmidt F, Youngblood MW. AAV-mediated direct in vivo CRISPR screen identifies functional suppressors in glioblastoma. Nat Neurosci 2017; 20:1329–1341 [View Article][PubMed]
    [Google Scholar]
  40. Joung J, Konermann S, Gootenberg JS, Abudayyeh OO, Platt RJ. Genome-scale CRISPR–Cas9 knockout and transcriptional activation screening. Nat Protoc 2017; 12:828–863 [View Article][PubMed]
    [Google Scholar]
  41. Yau EH, Rana TM. Next-generation sequencing of genome-wide CRISPR screens. In Methods in Molecular Biology Vol 1712 NIH Public Access; 2018 pp 203–216 [View Article][PubMed]
    [Google Scholar]
  42. Miles LA, Garippa RJ, Poirier JT. Design, execution, and analysis of pooled in vitro CRISPR/Cas9 screens. FEBS J 2016; 283:3170–3180 [View Article]
    [Google Scholar]
  43. Sharma S, Petsalaki E. Application of CRISPR–Cas9 based genome-wide screening approaches to study cellular signalling mechanisms. Int J Mol Sci 2018; 19:933 [View Article]
    [Google Scholar]
  44. Wang T, Birsoy K, Hughes NW, Krupczak KM, Post Y. Identification and characterization of essential genes in the human genome. Science 2015; 350:1096–1101 [View Article]
    [Google Scholar]
  45. Sanjana NE, Shalem O, Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods 2014; 11:783–784 [View Article][PubMed]
    [Google Scholar]
  46. Hart T, Chandrashekhar M, Aregger M, Steinhart Z, Brown KR et al. High-resolution CRISPR screens reveal fitness genes and genotype-specific cancer liabilities. Cell 2015; 163:1515–1526 [View Article][PubMed]
    [Google Scholar]
  47. Doench JG, Fusi N, Sullender M, Hegde M, Vaimberg EW. Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR–Cas9. Nat Biotechnol 2016; 34:184–191 [View Article][PubMed]
    [Google Scholar]
  48. Wang H, La Russa M, LS Q. CRISPR/Cas9 in genome editing and beyond. Annu Rev Biochem 2016; 85:227–264 [View Article]
    [Google Scholar]
  49. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 2013; 154:442–451 [View Article][PubMed]
    [Google Scholar]
  50. Groner AC, Meylan S, Ciuffi A, Zangger N, Ambrosini G et al. KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading. PLoS Genet 2010; 6:e1000869 [View Article]
    [Google Scholar]
  51. Chavez A, Scheiman J, Vora S, Pruitt BW, Tuttle M. Highly efficient Cas9-mediated transcriptional programming. Nat Methods 2015; 12:326–328 [View Article][PubMed]
    [Google Scholar]
  52. Richardson RB, Ohlson MB, Eitson JL, Kumar A, McDougal MB. A CRISPR screen identifies IFI6 as an ER-resident interferon effector that blocks flavivirus replication. Nat Microbiol 2018; 3:1214–1223 [View Article][PubMed]
    [Google Scholar]
  53. Wei J, Alfajaro M, Hanna R, DeWeirdt P, Strine M. Genome-wide CRISPR screen reveals host genes that regulate SARS-CoV-2 infection. bioRxiv 2020; 2020.06.16.155101:
    [Google Scholar]
  54. Daniloski Z, Jordan TX, Wessels H-H, Hoagland DA, Kasela S et al. Identification of required host factors for SARS-CoV-2 infection in human cells. Cell 2021; 184:92–105 [View Article]
    [Google Scholar]
  55. Hoffmann H-. H, Sánchez-Rivera FJ, Schneider WM, Luna JM, Soto-Feliciano YM. Functional interrogation of a SARS-CoV-2 host protein interactome identifies unique and shared coronavirus host factors. Cell Host Microbe 2020; 0:2020
    [Google Scholar]
  56. Gordon DE, Jang GM, Bouhaddou M, Xu J, Obernier K. A SARS-CoV-2 protein interaction map reveals targets for drug repurposing. Nature 2020; 583:459–468 [View Article][PubMed]
    [Google Scholar]
  57. Dukhovny A, Lamkiewicz K, Chen Q, Fricke M, Jabrane-Ferrat N. A CRISPR activation screen identifies genes that protect against Zika virus infection. J Virol 2019; 93:16 [View Article]
    [Google Scholar]
  58. Li Y, Muffat J, Omer Javed A, Keys HR, Lungjangwa T. Genome-wide CRISPR screen for Zika virus resistance in human neural cells. Proc Natl Acad Sci U S A 2019; 116:9527–9532 [View Article][PubMed]
    [Google Scholar]
  59. Ma H, Dang Y, Wu Y, Jia G, Anaya E. A CRISPR-based screen identifies genes essential for West-Nile-virus-induced cell death. Cell Rep 2015; 12:673–683 [View Article][PubMed]
    [Google Scholar]
  60. Zhang R, Miner JJ, Gorman MJ, Rausch K, Ramage H. A CRISPR screen defines a signal peptide processing pathway required by flaviviruses. Nature 2016; 535:164–168 [View Article][PubMed]
    [Google Scholar]
  61. Park RJ, Wang T, Koundakjian D, Hultquist JF, Lamothe-Molina P. A genome-wide CRISPR screen identifies a restricted set of HIV host dependency factors. Nat Genet 2017; 49:193–203 [View Article][PubMed]
    [Google Scholar]
  62. Rathore A, Iketani S, Wang P, Jia M, Sahi V. CRISPR-based gene knockout screens reveal deubiquitinases involved in HIV-1 latency in two Jurkat cell models. Sci Rep 2020; 10:5350 [View Article][PubMed]
    [Google Scholar]
  63. Ohainle M, Helms L, Vermeire J, Roesch F, Humes D. A virus-packageable CRISPR screen identifies host factors mediating interferon inhibition of HIV. elife 2018; 7: [View Article][PubMed]
    [Google Scholar]
  64. Kane M, Zang TM, Rihn SJ, Zhang F, Kueck T et al. Identification of interferon-stimulated genes with antiretroviral activity. Cell Host Microbe 2016; 20:392–405 [View Article][PubMed]
    [Google Scholar]
  65. Lin YT, Chiweshe S, McCormick D, Raper A, Wickenhagen A. Human cytomegalovirus evades ZAP detection by suppressing CpG dinucleotides in the major immediate early 1 gene. PLOS Pathog 2020; 16:e1008844
    [Google Scholar]
  66. Schoggins JW, MacDuff DA, Imanaka N, Gainey MD, Shrestha B. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 2014; 505:691–695 [View Article][PubMed]
    [Google Scholar]
  67. Rima B, Collins P, Easton A, Fouchier R, Kurath G et al. ICTV virus taxonomy profile: Pneumoviridae. J Gen Virol 2017; 98:2912–2913 [View Article][PubMed]
    [Google Scholar]
  68. Rihn SJ, Aziz MA, Stewart DG, Hughes J, Turnbull ML. TRIM69 inhibits vesicular stomatitis Indiana virus. J Virol 2019; 93:20
    [Google Scholar]
  69. Feng J, Wickenhagen A, Turnbull ML, Rezelj VV, Kreher F et al. Interferon-stimulated gene (ISG)-expression screening reveals the specific antibunyaviral activity of ISG20. J Virol 2018; 92:e02140–17 [View Article][PubMed]
    [Google Scholar]
  70. Zheng Z, Wang L, Pan J. Interferon-stimulated gene 20-kDa protein (ISG20) in infection and disease: Review and outlook. Intractable Rare Dis Res 2017; 6:35–40 [View Article][PubMed]
    [Google Scholar]
  71. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans . Nature 1998; 391:806–811 [View Article][PubMed]
    [Google Scholar]
  72. Hao L, Sakurai A, Watanabe T, Sorensen E, Nidom CA. Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 2008; 454:890 [View Article][PubMed]
    [Google Scholar]
  73. Sharma S, Rao A. RNAi screening: Tips and techniques. Nat Immunol 2009; 10:799–804 [View Article][PubMed]
    [Google Scholar]
  74. Mohr SE, Smith JA, Shamu CE, Neumüller RA, Perrimon N. RNAi screening comes of age: Improved techniques and complementary approaches. Nat Rev Mol Cell Biol 2014; 15:591–600 [View Article][PubMed]
    [Google Scholar]
  75. Rana TM. Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol 2007; 8:23–36 [View Article][PubMed]
    [Google Scholar]
  76. Aydin I, Weber S, Snijder B, Samperio Ventayol P, Kühbacher A et al. Large scale RNAi reveals the requirement of nuclear envelope breakdown for nuclear import of human papillomaviruses. PLoS Pathog 2014; 10:e1004162e1004162 [View Article][PubMed]
    [Google Scholar]
  77. Lipovsky A, Popa A, Pimienta G, Wyler M, Bhan A. Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proc Natl Acad Sci U S A 2013; 110:7452–7457 [View Article][PubMed]
    [Google Scholar]
  78. Beard PM, Griffiths SJ, Gonzalez O, Haga IR, Jowers TP. A loss of function analysis of host factors influencing Vaccinia virus replication by RNA interference. PLoS One 2014; 9:e98431 [View Article]
    [Google Scholar]
  79. Mercer J, Snijder B, Sacher R, Burkard C, Bleck CKE et al. RNAi screening reveals proteasome- and cullin3-dependent stages in Vaccinia virus infection. Cell Rep 2012; 2:1036–1047 [View Article][PubMed]
    [Google Scholar]
  80. Sivan G, Martin SE, Myers TG, Buehler E, Szymczyk KH. Human genome-wide RNAi screen reveals a role for nuclear pore proteins in poxvirus morphogenesis. Proc Natl Acad Sci U S A 2013; 110:3519–3524 [View Article][PubMed]
    [Google Scholar]
  81. Anderson DE, Pfeffermann K, Kim SY, Sawatsky B, Pearson J et al. Comparative loss-of-function screens reveal ABCE1 as an essential cellular host factor for efficient translation of Paramyxoviridae and Pneumoviridae . mBio 2019; 10:3 [View Article]
    [Google Scholar]
  82. Tai AW, Benita Y, Peng LF, Kim S-S, Sakamoto N et al. A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host Microbe 2009; 5:298–307 [View Article][PubMed]
    [Google Scholar]
  83. Ng TI, Mo H, Pilot-Matias T, He Y, Koev G et al. Identification of host genes involved in hepatitis C virus replication by small interfering RNA technology. Hepatology 2007; 45:1413–1421 [View Article]
    [Google Scholar]
  84. Li Q, Brass AL, Ng A, Hu Z, Xavier RJ. A genome-wide genetic screen for host factors required for hepatitis C virus propagation. Proc Natl Acad Sci U S A 2009; 106:16410–16415 [View Article][PubMed]
    [Google Scholar]
  85. Fusco DN, Brisac C, John SP, Huang Y-W, Chin CR et al. A genetic screen identifies interferon-α effector genes required to suppress hepatitis C virus replication. Gastroenterology 2013; 144:1438–1449 [View Article]
    [Google Scholar]
  86. Brass AL, Huang I-C, Benita Y, John SP, Krishnan MN et al. The IFITM proteins mediate cellular resistance to influenza a H1N1 virus, West Nile virus, and dengue virus. Cell 2009; 139:1243–1254 [View Article][PubMed]
    [Google Scholar]
  87. Li J, Ding SC, Cho H, Chung BC, Gale M. A short hairpin RNA screen of interferon-stimulated genes identifies a novel negative regulator of the cellular antiviral response. mBio 2013; 4:e00385–13 [View Article][PubMed]
    [Google Scholar]
  88. Jiang F, Doudna JA. CRISPR–Cas9 structures and mechanisms. Annu Rev Biophys 2017; 46:505–529 [View Article][PubMed]
    [Google Scholar]
  89. Flockhart IT, Booker M, Hu Y, McElvany B, Gilly Q. FlyRNAi.org - The database of the Drosophila RNAi screening center: 2012 update. Nucleic Acids Res 2012; 40:D715–D719
    [Google Scholar]
  90. Jackson AL, Bartz SR, Schelter J, Kobayashi S, Burchard J. Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 2003; 21:635–637 [View Article][PubMed]
    [Google Scholar]
  91. Birmingham A, Anderson EM, Reynolds A, Ilsley-Tyree D, Leake D. 3’ UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat Methods 2006; 3:199–204 [View Article][PubMed]
    [Google Scholar]
  92. Jackson AL, Burchard J, Schelter J, Chau BN, Cleary M. Widespread siRNA ‘off-target’ transcript silencing mediated by seed region sequence complementarity. RNA 2006; 12:1179–1187 [View Article][PubMed]
    [Google Scholar]
  93. Doench JG, Petersen CP, Sharp PA. siRNAs can function as miRNAs. Genes Dev 2003; 17:438–442 [View Article][PubMed]
    [Google Scholar]
  94. Sudbery I, Enright AJ, Fraser AG, Dunham I. Systematic analysis of off-target effects in an RNAi screen reveals microRNAs affecting sensitivity to TRAIL-induced apoptosis. BMC Genomics 2010; 11:175 [View Article][PubMed]
    [Google Scholar]
  95. Marques JT, Williams BRG. Activation of the mammalian immune system by siRNAs. Nat Biotechnol 2005; 23:1399–1405 [View Article][PubMed]
    [Google Scholar]
  96. Barrows NJ, Le Sommer C, Garcia-Blanco MA, Pearson JL. Factors affecting reproducibility between genome-scale siRNA-based screens. J Biomol Screen 2010; 15:735–747 [View Article][PubMed]
    [Google Scholar]
  97. Kulkarni MM, Booker M, Silver SJ, Friedman A, Hong P. Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. Nat Methods 2006; 3:833–838 [View Article][PubMed]
    [Google Scholar]
  98. Birmingham A, Selfors LM, Forster T, Wrobel D, Kennedy CJ. Statistical methods for analysis of high-throughput RNA interference screens. Nat Methods 2009; 6:569–575 [View Article][PubMed]
    [Google Scholar]
  99. Chung N, Zhang XD, Kreamer A, Locco L, Kuan PF. Median absolute deviation to improve hit selection for genome-scale RNAi screens. J Biomol Screen 2008; 13:149–158 [View Article][PubMed]
    [Google Scholar]
  100. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136:215–233 [View Article][PubMed]
    [Google Scholar]
  101. Seok H, Lee H, Jang ES, Chi SW. Evaluation and control of miRNA-like off-target repression for RNA interference. Cell Mol Life Sci 2018; 75:797–814 [View Article][PubMed]
    [Google Scholar]
  102. Saito T, Gale M. Differential recognition of double-stranded RNA by RIG-I-like receptors in antiviral immunity. J Exp Med 2008; 205:1523–1527 [View Article]
    [Google Scholar]
  103. Sanson KR, Hanna RE, Hegde M, Donovan KF, Strand C. Optimized libraries for CRISPR–Cas9 genetic screens with multiple modalities. Nat Commun 2018; 9:5416 [View Article][PubMed]
    [Google Scholar]
  104. Chen CH, Xiao T, Xu H, Jiang P, Meyer CA. Improved design and analysis of CRISPR knockout screens. Bioinformatics 2018; 34:4095–4101 [View Article][PubMed]
    [Google Scholar]
  105. Kim DH, Rossi JJ. RNAi mechanisms and applications. BioTechniques 2008; 44:613–616 [View Article][PubMed]
    [Google Scholar]
  106. Gupta S, Schoer RA, Egan JE, Hannon GJ, Mittal V. Inducible, reversible, and stable RNA interference in mammalian cells. Proc Natl Acad Sci U S A 2004; 101:1927–1932 [View Article][PubMed]
    [Google Scholar]
  107. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA et al. Genome-scale CRISPR–CAS9 knockout screening in human cells. Science 2014; 343:84–87 [View Article]
    [Google Scholar]
  108. Liu Y, Cao Z, Wang Y, Guo Y, Xu P. Genome-wide screening for functional long noncoding RNAs in human cells by Cas9 targeting of splice sites. Nat Biotechnol 2018; 36:1203–1210 [View Article]
    [Google Scholar]
  109. Parnas O, Jovanovic M, Eisenhaure TM, Herbst RH, Dixit A et al. A genome-wide CRISPR screen in primary immune cells to dissect regulatory networks. Cell 2015; 162:675–686 [View Article][PubMed]
    [Google Scholar]
  110. Shifrut E, Carnevale J, Tobin V, Roth TL, Woo JM et al. Genome-wide CRISPR screens in primary human T cells reveal key regulators of immune function. Cell 2018; 175:1958–1971 [View Article]
    [Google Scholar]
  111. Morgens DW, Deans RM, Li A, Bassik MC. Systematic comparison of CRISPR/Cas9 and RNAi screens for essential genes. Nat Biotechnol 2016; 34:634–636 [View Article][PubMed]
    [Google Scholar]
  112. Kim HS, Lee K, Kim SJ, Cho S, Shin HJ. Arrayed CRISPR screen with image-based assay reliably uncovers host genes required for coxsackievirus infection. Genome Res 2018; 28:859–868 [View Article][PubMed]
    [Google Scholar]
  113. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712 [View Article]
    [Google Scholar]
  114. Holthaus D, Vasou A, Bamford CGG, Andrejeva J, Paulus C et al. Direct antiviral activity of IFN-stimulated genes is responsible for resistance to paramyxoviruses in ISG15-deficient cells. J Immunol 2020; 205:261–271 [View Article][PubMed]
    [Google Scholar]
  115. Young DF, Andrejeva J, Li X, Inesta-Vaquera F, Dong C. Human IFIT1 inhibits mRNA translation of Rubulaviruses but not other members of the Paramyxoviridae family. J Virol 2016; 90:9446–9456 [View Article][PubMed]
    [Google Scholar]
  116. Gupta RM, Musunuru K. Expanding the genetic editing tool kit: ZFNs, TALENs, and CRISPR–Cas9. J Clin Invest 2014; 124:4154–4161 [View Article][PubMed]
    [Google Scholar]
  117. Wang T, Wei JJ, Sabatini DM, Lander ES. Genetic screens in human cells using the CRISPR–Cas9 System. Science 343:80–84 [View Article]
    [Google Scholar]
  118. Yuen G, Khan FJ, Gao S, Stommel JM, Batchelor E. CRISPR/Cas9-mediated gene knockout is insensitive to target copy number but is dependent on guide RNA potency and Cas9/sgRNA threshold expression level. Nucleic Acids Res 2017; 45:12039–12053 [View Article][PubMed]
    [Google Scholar]
  119. Jeong HH, Kim SY, Rousseaux MWC, Zoghbi HY, Liu Z. Beta-binomial modeling of CRISPR pooled screen data identifies target genes with greater sensitivity and fewer false negatives. Genome Res 2019; 29:999–1008 [View Article][PubMed]
    [Google Scholar]
  120. RWL S, Chung SW, HHC L, Watts JJ, Gaudette E. Application of CRISPR genetic screens to investigate neurological diseases. Molecular Neurodegeneration 2019; 14:1
    [Google Scholar]
  121. Li W, Xu H, Xiao T, Cong L, Love MI. MAGeCK enables robust identification of essential genes from genome-scale CRISPR/Cas9 knockout screens. Genome Biol 2014; 15:554 [View Article][PubMed]
    [Google Scholar]
  122. Schuster A, Erasimus H, Fritah S, Nazarov PV, van Dyck E et al. RNAI/CRISPR screens: From a pool to a valid hit. Trends Biotechnol 2019; 37:38–55 [View Article][PubMed]
    [Google Scholar]
  123. Chen CH, Xiao T, Xu H, Jiang P, Meyer CA. Improved design and analysis of CRISPR knockout screens. Bioinformatics 2018; 34:4095–4101 [View Article][PubMed]
    [Google Scholar]
  124. Deans RM, Morgens DW, Ökesli A, Pillay S, Horlbeck MA. Parallel shRNA and CRISPR–Cas9 screens enable antiviral drug target identification. Nat Chem Biol 2016; 12:361–366 [View Article][PubMed]
    [Google Scholar]
  125. Kranz D, Boutros M. A synthetic lethal screen identifies FAT1 as an antagonist of caspase-8 in extrinsic apoptosis. EMBO J 2014; 33:181–197 [View Article][PubMed]
    [Google Scholar]
  126. Subramanian G, Kuzmanovic T, Zhang Y, Peter CB, Veleeparambil M et al. A new mechanism of interferon’s antiviral action: Induction of autophagy, essential for paramyxovirus replication, is inhibited by the interferon stimulated gene, TDRD7. PLOS Pathog 2018; 14:e1006877 [View Article][PubMed]
    [Google Scholar]
  127. McDonald JU, Kaforou M, Clare S, Hale C, Ivanova M et al. A simple screening approach to prioritize genes for functional analysis identifies a role for interferon regulatory factor 7 in the control of respiratory syncytial virus disease. mSystems 2016; 1:3 [View Article]
    [Google Scholar]
  128. Chattopadhyay PK, Roederer M, Bolton DL. A deadly dance: the choreography of host–pathogen interactions, as revealed by single-cell technologies. Nat Commun 2018; 9:4638 [View Article][PubMed]
    [Google Scholar]
  129. Cohn LB, da Silva IT, Valieris R, Huang AS, Lorenzi JCC. Clonal CD4+ T cells in the HIV-1 latent reservoir display a distinct gene profile upon reactivation. Nat Med 2018; 24:604–609 [View Article][PubMed]
    [Google Scholar]
  130. Dixit A, Parnas O, Li B, Chen J, Fulco CP. Perturb-seq: dissecting molecular circuits with scalable single-cell RNA profiling of pooled genetic screens. Cell 2016; 167:1853–1866 [View Article]
    [Google Scholar]
  131. Adamson B, Norman TM, Jost M, Cho MY, Nuñez JK et al. A multiplexed single-cell CRISPR screening platform enables systematic dissection of the unfolded protein response. Cell 2016; 167:1867–1882 [View Article]
    [Google Scholar]
  132. Datlinger P, Rendeiro AF, Schmidl C, Krausgruber T, Traxler P. Pooled CRISPR screening with single-cell transcriptome readout. Nat Methods 2017; 14:297–301 [View Article][PubMed]
    [Google Scholar]
  133. Jaitin DA, Weiner A, Yofe I, Lara-Astiaso D, Keren-Shaul H et al. Dissecting immune circuits by linking CRISPR-pooled screens with single-cell RNA-seq. Cell 2016; 167:1883–1896 [View Article]
    [Google Scholar]
  134. Ramage H, Cherry S. Virus–host interactions: from unbiased genetic screens to function. Annu Rev Virol 2015; 2:497–524 [View Article][PubMed]
    [Google Scholar]
  135. Friedel CC, Haas J. Virus–host interactomes and global models of virus-infected cells. Trends Microbiol 2011; 19:501–508 [View Article][PubMed]
    [Google Scholar]
  136. Nguyen DG, Yin H, Zhou Y, Wolff KC, Kuhen KL. Identification of novel therapeutic targets for HIV infection through functional genomic cDNA screening. Virology 2007; 362:16–25 [View Article][PubMed]
    [Google Scholar]
  137. Munday DC, Surtees R, Emmott E, Dove BK, Digard P. Using SILAC and quantitative proteomics to investigate the interactions between viral and host proteomes. Proteomics 2012; 12:666–672 [View Article][PubMed]
    [Google Scholar]
  138. Nightingale K, Lin KM, Ravenhill BJ, Davies C, Nobre L. High-definition analysis of host protein stability during human cytomegalovirus infection reveals antiviral factors and viral evasion mechanisms. Cell Host Microbe 2018; 24:447–460
    [Google Scholar]
  139. Andrejeva J, Norsted H, Habjan M, Thiel V, Goodbourn S et al. ISG56/IFIT1 is primarily responsible for interferon-induced changes to patterns of parainfluenza virus type 5 transcription and protein synthesis. J Gen Virol 2013; 94:59–68 [View Article][PubMed]
    [Google Scholar]
  140. Tan WS, Rong E, Dry I, Lillico SG, Law A. Genome-wide CRISPR knockout screen reveals membrane tethering complexes EARP and GARP important for Bovine Herpes Virus Type 1 replication. bioRxiv 2020; 2020.06.17.155788:
    [Google Scholar]
  141. Kuroda M, Halfmann PJ, Hill-Batorski L, Ozawa M, Lopes TJS. Identification of interferon-stimulated genes that attenuate Ebola virus infection. Nat Commun 2020; 11:2953 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001603
Loading
/content/journal/jgv/10.1099/jgv.0.001603
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error