Functional Genomic Strategies for Elucidating Human-Virus Interactions: Will CRISPR Knockout RNAi and Haploid Cells?

Advances in Virus Research

Volumn 94, Issue , 2016, Pages 1-51

  Perreira, Jill M ^a   Meraner, Paul ^a   Brass, Abraham L ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

CRISPR Cas9; Genetic screening; Haploid cells; Human virus interactions; RNA interference; ShRNA; SiRNA

Indexed keywords

BACTERIAL PROTEIN; CAS9 ENDONUCLEASE STREPTOCOCCUS PYOGENES; ENDONUCLEASE; SMALL INTERFERING RNA;

CRISPR CAS SYSTEM; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETIC SCREENING; GENETICS; GENOMICS; HAPLOIDY; HOST PATHOGEN INTERACTION; HUMAN; PATHOGENICITY; PROCEDURES; RNA INTERFERENCE; VIROLOGY; VIRUS;

BACTERIAL PROTEINS; CRISPR-CAS SYSTEMS; ENDONUCLEASES; GENE KNOCKOUT TECHNIQUES; GENETIC TESTING; GENOMICS; HAPLOIDY; HOST-PATHOGEN INTERACTIONS; HUMANS; MUTAGENESIS, INSERTIONAL; RNA INTERFERENCE; RNA, SMALL INTERFERING; VIRUSES;

EID: 84959440683     PISSN: 00653527     EISSN: 15578399     Source Type: Book Series    
DOI: 10.1016/bs.aivir.2015.11.001     Document Type: Chapter

References (106)

1. Andersson B.S., Beran M., Pathak S., Goodacre A., Barlogie B., McCredie K.B. Ph-positive chronic myeloid leukemia with near-haploid conversion in vivo and establishment of a continuously growing cell line with similar cytogenetic pattern. Cancer Genetics and Cytogenetics 1987, 24:335-343.
2. Arita M., Wakita T., Shimizu H. Valosin-containing protein (VCP/p97) is required for poliovirus replication and is involved in cellular protein secretion pathway in poliovirus infection. Journal of Virology 2012, 86:5541-5553.
3. Arkov K., Rosenbaum B., Christiansen L., Jonsson H., Munchow M. Treatment of suicidal patients: The Collaborative Assessment and Management of Suicidality. Ugeskrift for Laeger 2008, 170:149-153.
4. Aydin I., Weber S., Snijder B., Samperio Ventayol P., Kuhbacher A., Becker M., et al. Large scale RNAi reveals the requirement of nuclear envelope breakdown for nuclear import of human papillomaviruses. PLoS Pathogens 2014, 10:e1004162.
5. Balistreri G., Horvath P., Schweingruber C., Zund D., McInerney G., Merits A., et al. The host nonsense-mediated mRNA decay pathway restricts mammalian RNA virus replication. Cell Host & Microbe 2014, 16:403-411.
6. Barrows N.J., Jamison S.F., Bradrick S.S., Le Sommer C., Kim S.Y., Pearson J., et al. Functional genomics approach for the identification of human host factors supporting dengue viral propagation. Methods in Molecular Biology 2014, 1138:285-299.
7. Beard P.M., Griffiths S.J., Gonzalez O., Haga I.R., Pechenick Jowers T., Reynolds D.K., et al. A loss of function analysis of host factors influencing Vaccinia virus replication by RNA interference. PLoS One 2014, 9:e98431.
8. Berns K., Hijmans E.M., Mullenders J., Brummelkamp T.R., Velds A., Heimerikx M., et al. A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature 2004, 428:431-437.
9. Boettcher M., Hoheisel J.D. Pooled RNAi screens-Technical and biological aspects. Current Genomics 2010, 11:162-167.
10. Booker M., Samsonova A.A., Kwon Y., Flockhart I., Mohr S.E., Perrimon N. False negative rates in Drosophila cell-based RNAi screens: A case study. BMC Genomics 2011, 12:50.
11. Brass A.L., Dykxhoorn D.M., Benita Y., Yan N., Engelman A., Xavier R.J., et al. Identification of host proteins required for HIV infection through a functional genomic screen. Science 2008, 319:921-926.
12. Brass A.L., Huang I.C., Benita Y., John S.P., Krishnan M.N., Feeley E.M., et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009, 139:1243-1254.
13. Bushman F.D., Malani N., Fernandes J., D'Orso I., Cagney G., Diamond T.L., et al. Host cell factors in HIV replication: Meta-analysis of genome-wide studies. PLoS Pathogens 2009, 5:e1000437.
14. Carette J.E., Guimaraes C.P., Varadarajan M., Park A.S., Wuethrich I., Godarova A., et al. Haploid genetic screens in human cells identify host factors used by pathogens. Science 2009, 326:1231-1235.
15. Carette J.E., Pruszak J., Varadarajan M., Blomen V.A., Gokhale S., Camargo F.D., et al. Generation of iPSCs from cultured human malignant cells. Blood 2010, 115:4039-4042.
16. Carette J.E., Raaben M., Wong A.C., Herbert A.S., Obernosterer G., Mulherkar N., et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 2011, 477:340-343.
17. Cherry S. RNAi screening for host factors involved in viral infection using Drosophila cells. Methods in Molecular Biology 2011, 721:375-382.
18. Cherry S., Doukas T., Armknecht S., Whelan S., Wang H., Sarnow P., et al. Genome-wide RNAi screen reveals a specific sensitivity of IRES-containing RNA viruses to host translation inhibition. Genes & Development 2005, 19:445-452.
19. Chin C.R., Brass A.L. A genome wide RNA interference screening method to identify host factors that modulate influenza A virus replication. Methods 2013, 59:217-224.
20. Cho S.W., Kim S., Kim Y., Kweon J., Kim H.S., Bae S., et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Research 2014, 24:132-141.
21. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
22. Coyne C.B., Bozym R., Morosky S.A., Hanna S.L., Mukherjee A., Tudor M., et al. Comparative RNAi screening reveals host factors involved in enterovirus infection of polarized endothelial monolayers. Cell Host & Microbe 2011, 9:70-82.
23. de Wilde A.H., Wannee K.F., Scholte F.E., Goeman J.J., Ten Dijke P., Snijder E.J., et al. A kinome-wide small interfering RNA screen identifies proviral and antiviral host factors in severe acute respiratory syndrome coronavirus replication, including double-stranded RNA-activated protein kinase and early secretory pathway proteins. Journal of Virology 2015, 89:8318-8333.
24. Doudna J.A., Charpentier E. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 2014, 346:1258096.
25. Dziuba N., Ferguson M.R., O'Brien W.A., Sanchez A., Prussia A.J., McDonald N.J., et al. Identification of cellular proteins required for replication of human immunodeficiency virus type 1. AIDS Research and Human Retroviruses 2012, 28:1329-1339.
26. Echeverri C.J., Beachy P.A., Baum B., Boutros M., Buchholz F., Chanda S.K., et al. Minimizing the risk of reporting false positives in large-scale RNAi screens. Nature Methods 2006, 3:777-779.
27. Echeverri C.J., Perrimon N. High-throughput RNAi screening in cultured cells: A user's guide. Nature Reviews. Genetics 2006, 7:373-384.
28. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411:494-498.
29. Espeseth A.S., Fishel R., Hazuda D., Huang Q., Xu M., Yoder K., et al. siRNA screening of a targeted library of DNA repair factors in HIV infection reveals a role for base excision repair in HIV integration. PLoS One 2011, 6:e17612.
30. Evans M.J., Carlton M.B., Russ A.P. Gene trapping and functional genomics. Trends in Genetics 1997, 13:370-374.
31. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
32. Fusco D.N., Brisac C., John S.P., Huang Y.W., Chin C.R., Xie T., et al. A genetic screen identifies interferon-α effector genes required to suppress hepatitis C virus replication. Gastroenterology 2013, 144:1438-1449.
33. Gilbert L.A., Horlbeck M.A., Adamson B., Villalta J.E., Chen Y., Whitehead E.H., et al. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 2014, 159:647-661.
34. Grishok A., Mello C.C. RNAi (Nematodes: Caenorhabditis elegans). Advances in Genetics 2002, 46:339-360.
35. Hao L., He Q., Wang Z., Craven M., Newton M.A., Ahlquist P. Limited agreement of independent RNAi screens for virus-required host genes owes more to false-negative than false-positive factors. PLoS Computational Biology 2013, 9:e1003235.
36. Hao L., Sakurai A., Watanabe T., Sorensen E., Nidom C.A., Newton M.A., et al. Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 2008, 454:890-893.
37. He B., Guo W. The exocyst complex in polarized exocytosis. Current Opinion in Cell Biology 2009, 21:537-542.
38. Hopkins K.C., McLane L.M., Maqbool T., Panda D., Gordesky-Gold B., Cherry S. A genome-wide RNAi screen reveals that mRNA decapping restricts bunyaviral replication by limiting the pools of Dcp2-accessible targets for cap-snatching. Genes & Development 2013, 27:1511-1525.
39. Hussain K.M., Leong K.L., Ng M.M., Chu J.J. The essential role of clathrin-mediated endocytosis in the infectious entry of human enterovirus 71. The Journal of Biological Chemistry 2011, 286:309-321.
40. Jae L.T., Raaben M., Riemersma M., van Beusekom E., Blomen V.A., Velds A., et al. Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry. Science 2013, 340:479-483.
41. Karlas A., Machuy N., Shin Y., Pleissner K.P., Artarini A., Heuer D., et al. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 2010, 463:818-822.
42. Kittler R., Surendranath V., Heninger A.K., Slabicki M., Theis M., Putz G., et al. Genome-wide resources of endoribonuclease-prepared short interfering RNAs for specific loss-of-function studies. Nature Methods 2007, 4:337-344.
43. Kleinfelter L.M., Jangra R.K., Jae L.T., Herbert A.S., Mittler E., Stiles K.M., et al. Haploid genetic screen reveals a profound and direct dependence on cholesterol for hantavirus membrane fusion. MBio 2015, 6:e00801.
44. Knott S.R., Maceli A.R., Erard N., Chang K., Marran K., Zhou X., et al. A computational algorithm to predict shRNA potency. Molecular Cell 2014, 56:796-807.
45. Kolokoltsov A.A., Saeed M.F., Freiberg A.N., Holbrook M.R., Davey R.A. Identification of novel cellular targets for therapeutic intervention against Ebola virus infection by siRNA screening. Drug Development Research 2009, 70:255-265.
46. Konig R., Stertz S., Zhou Y., Inoue A., Hoffmann H.H., Bhattacharyya S., et al. Human host factors required for influenza virus replication. Nature 2010, 463:813-817.
47. Kotecki M., Reddy P.S., Cochran B.H. Isolation and characterization of a near-haploid human cell line. Experimental Cell Research 1999, 252:273-280.
48. Krishnan M.N., Ng A., Sukumaran B., Gilfoy F.D., Uchil P.D., Sultana H., et al. RNA interference screen for human genes associated with West Nile virus infection. Nature 2008, 455:242-245.
49. Kwon Y.J., Heo J., Wong H.E., Cruz D.J., Velumani S., da Silva C.T., et al. Kinome siRNA screen identifies novel cell-type specific dengue host target genes. Antiviral Research 2014, 110:20-30.
50. Lavanya M., Cuevas C.D., Thomas M., Cherry S., Ross S.R. siRNA screen for genes that affect Junin virus entry uncovers voltage-gated calcium channels as a therapeutic target. Science Translational Medicine 2013, 5:204ra131.
51. Le Sommer C., Barrows N.J., Bradrick S.S., Pearson J.L., Garcia-Blanco M.A. G protein-coupled receptor kinase 2 promotes flaviviridae entry and replication. PLoS Neglected Tropical Diseases 2012, 6:e1820.
52. Lee A.S., Burdeinick-Kerr R., Whelan S.P. A genome-wide small interfering RNA screen identifies host factors required for vesicular stomatitis virus infection. Journal of Virology 2014, 88:8355-8360.
53. Li Q., Brass A.L., Ng A., Hu Z., Xavier R.J., Liang T.J., et al. A genome-wide genetic screen for host factors required for hepatitis C virus propagation. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:16410-16415.
54. Liu L., Oliveira N.M., Cheney K.M., Pade C., Dreja H., Bergin A.M., et al. A whole genome screen for HIV restriction factors. Retrovirology 2011, 8:94.
55. Luo B., Cheung H.W., Subramanian A., Sharifnia T., Okamoto M., Yang X., et al. Highly parallel identification of essential genes in cancer cells. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:20380-20385.
56. Ma H., Dang Y., Wu Y., Jia G., Anaya E., Zhang J., et al. A CRISPR-based screen identifies genes essential for West-Nile-virus-induced cell death. Cell Reports 2015, 12:673-683.
57. Meier R., Franceschini A., Horvath P., Tetard M., Mancini R., von Mering C., et al. Genome-wide small interfering RNA screens reveal VAMP3 as a novel host factor required for Uukuniemi virus late penetration. Journal of Virology 2014, 88:8565-8578.
58. Mercer J., Snijder B., Sacher R., Burkard C., Bleck C.K., Stahlberg H., et al. RNAi screening reveals proteasome- and Cullin3-dependent stages in vaccinia virus infection. Cell Reports 2012, 2:1036-1047.
59. Mohr S.E., Perrimon N. RNAi screening: New approaches, understandings, and organisms. Wiley Interdisciplinary Reviews. RNA 2012, 3:145-158.
60. Moser T.S., Jones R.G., Thompson C.B., Coyne C.B., Cherry S. A kinome RNAi screen identified AMPK as promoting poxvirus entry through the control of actin dynamics. PLoS Pathogens 2010, 6:e1000954.
61. Ooi Y.S., Stiles K.M., Liu C.Y., Taylor G.M., Kielian M. Genome-wide RNAi screen identifies novel host proteins required for alphavirus entry. PLoS Pathogens 2013, 9:e1003835.
62. Organ E.L., Sheng J., Ruley H.E., Rubin D.H. Discovery of mammalian genes that participate in virus infection. BMC Cell Biology 2004, 5:41.
63. Ortblad K.F., Lozano R., Murray C.J. The burden of HIV: Insights from the Global Burden of Disease Study 2010. AIDS 2013, 27:2003-2017.
64. Paddison P.J., Silva J.M., Conklin D.S., Schlabach M., Li M., Aruleba S., et al. A resource for large-scale RNA-interference-based screens in mammals. Nature 2004, 428:427-431.
65. Panda D., Cherry S. A genome-wide RNAi screening method to discover novel genes involved in virus infection. Methods 2015, 91:75-81.
66. Panda D., Das A., Dinh P.X., Subramaniam S., Nayak D., Barrows N.J., et al. RNAi screening reveals requirement for host cell secretory pathway in infection by diverse families of negative-strand RNA viruses. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:19036-19041.
67. Panda D., Rose P.P., Hanna S.L., Gold B., Hopkins K.C., Lyde R.B., et al. Genome-wide RNAi screen identifies SEC61A and VCP as conserved regulators of Sindbis virus entry. Cell Reports 2013, 5:1737-1748.
68. Parnas O., Jovanovic M., Eisenhaure T.M., Herbst R.H., Dixit A., Ye C.J., et al. A genome-wide CRISPR screen in primary immune cells to dissect regulatory networks. Cell 2015, 162:675-686.
69. Perreira J., Aker A., Savidis G., Chin C., McDougall W., Portmann J., et al. RNASEK is a V-ATPase-associated factor required for endocytosis and the replication of rhinovirus, influenza A virus, and dengue virus. Cell Reports 2015, 12:850-863.
70. Petersen J., Drake M.J., Bruce E.A., Riblett A.M., Didigu C.A., Wilen C.B., et al. The major cellular sterol regulatory pathway is required for Andes virus infection. PLoS Pathogens 2014, 10:e1003911.
71. Petri S., Meister G. siRNA design principles and off-target effects. Methods in Molecular Biology 2013, 986:59-71.
72. Poenisch M., Metz P., Blankenburg H., Ruggieri A., Lee J.Y., Rupp D., et al. Identification of HNRNPK as regulator of hepatitis C virus particle production. PLoS Pathogens 2015, 11:e1004573.
73. Pohl M.O., Edinger T.O., Stertz S. Prolidase is required for early trafficking events during influenza A virus entry. Journal of Virology 2014, 88:11271-11283.
74. Puri N., Wang X., Varma R., Burnett C., Beauchamp L., Batten D.M., et al. LNA incorporated siRNAs exhibit lower off-target effects compared to 2'-OMethoxy in cell phenotypic assays and microarray analysis. Nucleic Acids Symposium Series 2008, 25-26.
75. Qi L.S., Larson M.H., Gilbert L.A., Doudna J.A., Weissman J.S., Arkin A.P., et al. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 2013, 152:1173-1183.
76. Ran F.A., Hsu P.D., Wright J., Agarwala V., Scott D.A., Zhang F. Genome engineering using the CRISPR-Cas9 system. Nature Protocols 2013, 8:2281-2308.
77. Randall G., Panis M., Cooper J.D., Tellinghuisen T.L., Sukhodolets K.E., Pfeffer S., et al. Cellular cofactors affecting hepatitis C virus infection and replication. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:12884-12889.
78. Root D.E., Hacohen N., Hahn W.C., Lander E.S., Sabatini D.M. Genome-scale loss-of-function screening with a lentiviral RNAi library. Nature Methods 2006, 3:715-719.
79. Sanjana N.E., Shalem O., Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nature Methods 2014, 11:783-784.
80. Schreiber C.A., Sakuma T., Izumiya Y., Holditch S.J., Hickey R.D., Bressin R.K., et al. An siRNA screen identifies the U2 snRNP spliceosome as a host restriction factor for recombinant adeno-associated viruses. PLoS Pathogens 2015, 11:e1005082.
81. Schweitzer A., Horn J., Mikolajczyk R.T., Krause G., Ott J.J. Estimations of worldwide prevalence of chronic hepatitis B virus infection: A systematic review of data published between 1965 and 2013. Lancet 2015, 386:1546-1555.
82. Sessions O.M., Barrows N.J., Souza-Neto J.A., Robinson T.J., Hershey C.L., Rodgers M.A., et al. Discovery of insect and human dengue virus host factors. Nature 2009, 458:1047-1050.
83. Shalem O., Sanjana N.E., Hartenian E., Shi X., Scott D.A., Mikkelsen T.S., et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 2014, 343:84-87.
84. Shalem O., Sanjana N.E., Zhang F. High-throughput functional genomics using CRISPR-Cas9. Nature Reviews. Genetics 2015, 16:299-311.
85. Shapira S.D., Gat-Viks I., Shum B.O., Dricot A., de Grace M.M., Wu L., et al. A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 2009, 139:1255-1267.
86. Sigoillot F.D., Lyman S., Huckins J.F., Adamson B., Chung E., Quattrochi B., et al. A bioinformatics method identifies prominent off-targeted transcripts in RNAi screens. Nature Methods 2012, 9:363-366.
87. Silva J.M., Li M.Z., Chang K., Ge W., Golding M.C., Rickles R.J., et al. Second-generation shRNA libraries covering the mouse and human genomes. Nature Genetics 2005, 37:1281-1288.
88. Sivan G., Martin S.E., Myers T.G., Buehler E., Szymczyk K.H., Ormanoglu P., et al. Human genome-wide RNAi screen reveals a role for nuclear pore proteins in poxvirus morphogenesis. Proceedings of the National Academy of Sciences of the United States of America 2013, 110:3519-3524.
89. Sivan G., Ormanoglu P., Buehler E.C., Martin S.E., Moss B. Identification of restriction factors by human genome-wide RNA interference screening of viral host range mutants exemplified by discovery of SAMD9 and WDR6 as inhibitors of the Vaccinia virus K1L-C7L- mutant. MBio 2015, 6:e01122.
90. Slaymaker I.M., Gao L., Zetsche B., Scott D.A., Yan W.X., Zhang F. Rationally engineered Cas9 nucleases with improved specificity. Science 2016, 351:84-88.
91. Smith J.A., White E.A., Sowa M.E., Powell M.L., Ottinger M., Harper J.W., et al. Genome-wide siRNA screen identifies SMCX, EP400, and Brd4 as E2-dependent regulators of human papillomavirus oncogene expression. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:3752-3757.
92. Stertz S., Shaw M.L. Uncovering the global host cell requirements for influenza virus replication via RNAi screening. Microbes and Infection/Institut Pasteur 2011, 13:516-525.
93. Su W.C., Chen Y.C., Tseng C.H., Hsu P.W., Tung K.F., Jeng K.S., et al. Pooled RNAi screen identifies ubiquitin ligase Itch as crucial for influenza A virus release from the endosome during virus entry. Proceedings of the National Academy of Sciences of the United States of America 2013, 110:17516-17521.
94. Tai A.W., Benita Y., Peng L.F., Kim S.S., Sakamoto N., Xavier R.J., et al. A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host & Microbe 2009, 5:298-307.
95. Tran A.T., Rahim M.N., Ranadheera C., Kroeker A., Cortens J.P., Opanubi K.J., et al. Knockdown of specific host factors protects against influenza virus-induced cell death. Cell Death & Disease 2013, 4:e769.
96. von Melchner H., Ruley H.E. Identification of cellular promoters by using a retrovirus promoter trap. Journal of Virology 1989, 63:3227-3233.
97. Wang X., Wang Y., Wu X., Wang J., Wang Y., Qiu Z., et al. Unbiased detection of off-target cleavage by CRISPR-Cas9 and TALENs using integrase-defective lentiviral vectors. Nature Biotechnology 2015, 33:175-178.
98. Wang T., Wei J.J., Sabatini D.M., Lander E.S. Genetic screens in human cells using the CRISPR-Cas9 system. Science 2014, 343:80-84.
99. Ward S.E., Kim H.S., Komurov K., Mendiratta S., Tsai P.L., Schmolke M., et al. Host modulators of H1N1 cytopathogenicity. PLoS One 2012, 7:e39284.
100. Wen X., Ding L., Hunter E., Spearman P. An siRNA screen of membrane trafficking genes highlights pathways common to HIV-1 and M-PMV virus assembly and release. PLoS One 2014, 9:e106151.
101. Wideman J.G. The ubiquitous and ancient ER membrane protein complex (EMC): Tether or not?. F1000Research 2015, 4:624.
102. Williams C.A., Abbink T.E., Jeang K.T., Lever A.M. Identification of RNA helicases in human immunodeficiency virus 1 (HIV-1) replication-A targeted small interfering RNA library screen using pseudotyped and WT HIV-1. The Journal of General Virology 2015, 96:1484-1489.
103. Wu X., Scott D.A., Kriz A.J., Chiu A.C., Hsu P.D., Dadon D.B., et al. Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nature Biotechnology 2014, 32:670-676.
104. Yasunaga A., Hanna S.L., Li J., Cho H., Rose P.P., Spiridigliozzi A., et al. Genome-wide RNAi screen identifies broadly-acting host factors that inhibit arbovirus infection. PLoS Pathogens 2014, 10:e1003914.
105. Yeung M.L., Houzet L., Yedavalli V.S., Jeang K.T. A genome-wide short hairpin RNA screening of jurkat T-cells for human proteins contributing to productive HIV-1 replication. The Journal of Biological Chemistry 2009, 284:19463-19473.
106. Zhu J., Davoli T., Perriera J.M., Chin C.R., Gaiha G.D., John S.P., et al. Comprehensive identification of host modulators of HIV-1 replication using multiple orthologous RNAi reagents. Cell Reports 2014, 9:752-766.