Simultaneous analysis of large-scale RNAi screens for pathogen entry

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Rämö, Pauli ^a   Drewek, Anna ^b   Arrieumerlou, Cécile ^h   Beerenwinkel, Niko ^b,d   Ben Tekaya, Houchaima ^a   Cardel, Bettina ^c   Casanova, Alain ^a   Conde Alvarez, Raquel ^f   Cossart, Pascale ^e   Csúcs, Gábor ^b   Eicher, Simone ^a   Emmenlauer, Mario ^a   Greber, Urs ^c   Hardt, Wolf Dietrich ^b   Helenius, Ari ^b   Kasper, Christoph ^e   Kaufmann, Andreas ^a   Kreibich, Saskia ^b   Kühbacher, Andreas ^e   Kunszt, Peter ⁱ   Low, Shyan Huey ^a   Mercer, Jason ^b   Mudrak, Daria ^c   Muntwiler, Simone ^a   Pelkmans, Lucas ^c   Pizarro Cerdá, Javier ^e   Podvinec, Michael ^a   Pujadas, Eva ^a   Rinn, Bernd ^b,d   Rouilly, Vincent ^a   Schmich, Fabian ^b   Siebourg Polster, Juliane ^b   Snijder, Berend ^c   Stebler, Michael ^b   Studer, Gabriel ^a   Szczurek, Ewa ^b,d   Truttmann, Matthias ^a   von Mering, Christian ^c   Vonderheit, Andreas ^g   Yakimovich, Artur ^c   Bühlmann, Peter ^b   Dehio, Christoph ^a   more..

^a UNIVERSITY OF BASEL   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^e INSTITUT PASTEUR   (France)

^f UNIVERSITY OF NAVARRA   (Spain)

^g INSTITUTE OF MOLECULAR BIOLOGY   (Armenia)

^h INSTITUT COCHIN   (France)

ⁱ Systems Biology IT (SyBIT) SystemsXch   (Switzerland)

Author keywords

High throughput high content RNAi screening; Hit detection; Linear mixed model; Pathogen entry

Indexed keywords

SMALL INTERFERING RNA;

ANALYTIC METHOD; ARTICLE; CONTROLLED STUDY; GENE CONTROL; GENETIC DATABASE; GENETIC SCREENING; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; MICROBIAL ACTIVITY; NONHUMAN; PARALLEL MIXED MODEL APPROACH; QUALITY CONTROL; RNA INTERFERENCE; SCORING SYSTEM; STATISTICAL ANALYSIS; STATISTICAL MODEL;

EID: 84924328616     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1162.     Document Type: Article

References (59)

1. Conrad C, Gerlich DW: Automated microscopy for high-content RNAi screening. J Cell Biol 2010,188(4):453-461.10.1083/jcb.200910105.
2. Mohr S, Bakal C, Perrimon N: Genomic screening with RNAi: results and challenges. Annu Rev Biochem 2010, 79:37-64.10.1146/annurev-biochem-060408-092949.
3. Mohr SE, Perrimon N: RNAi screening: new approaches, understandings, and organisms. Wiley Interdiscip Rev RNA 2012,3(2):145-158.10.1002/wrna.110.
4. Simpson KJ, Davis GM, Boag PR: Comparative high-throughput RNAi screening methodologies in C. elegans and mammalian cells. N Biotechnol 2012,29(4):459-470.10.1016/j.nbt.2012.01.003.
5. Elbashir SM, 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(6836):494-498.10.1038/35078107.
6. Mercer J, Snijder B, Sacher R, Burkard C, Bleck CK, Stahlberg H, Pelkmans L, Helenius A: RNAi screening reveals proteasome- and cullin3-dependent stages in vaccinia virus infection. Cell Rep 2012,2(4):1036-1047.10.1016/j.celrep.2012.09.003.
7. Stertz S, Shaw ML: Uncovering the global host cell requirements for influenza virus replication via RNAi screening. Microbes Infect 2011,13(5):516-525.10.1016/j.micinf.2011.01.012.
8. Misselwitz B, Dilling S, Vonaesch P, Sacher R, Snijder B, Schlumberger M, Rout S, Stark M, von Mering C, Pelkmans L, Hardt WD: RNAi screen of Salmonella invasion shows role of COPI in membrane targeting of cholesterol and Cdc42. Mol Syst Biol 2011, 7:474.
9. Snijder B, Sacher R, Ramo P, Liberali P, Mench K, Wolfrum N, Burleigh L, Scott CC, Verheije MH, Mercer J, Moese S, Heger T, Theusner K, Jurgeit A, Lamparter D, Balistreri G, Schelhaas M, De Haan CAM, Marjomäki V, Hyypiä T, Rottier PJM, Sodeik B, Marsh M, Gruenberg J, Amara A, Greber U, Helenius A, Pelkmans L: Single-cell analysis of population context advances RNAi screening at multiple levels. Mol Syst Biol 2012, 8:579.
10. Schmidt EE, Pelz O, Buhlmann S, Kerr G, Horn T, Boutros M: GenomeRNAi: a database for cell-based and in vivo RNAi phenotypes, 2013 update. Nucleic Acids Res 2013,41(Database issue):D1021-D1026.
11. Pache L, Konig R, Chanda SK: Identifying HIV-1 host cell factors by genome-scale RNAi screening. Methods 2011,53(1):3-12.10.1016/j.ymeth.2010.07.009.
12. Sigoillot FD, King RW: Vigilance and validation: keys to success in RNAi screening. ACS Chem Biol 2011,6(1):47-60.10.1021/cb100358f.
13. Bushman FD, Malani N, Fernandes J, D'Orso I, Cagney G, Diamond TL, Zhou H, Hazuda DJ, Espeseth AS, König R, Bandyopadhyay S, Ideker T, Goff SP, Krogan NJ, Frankel AD, Young JA, Chanda SK: Host cell factors in HIV replication: meta-analysis of genome-wide studies. PLoS Pathog 2009,5(5):e1000437.10.1371/journal.ppat.1000437.
14. Heynen-Genel S, Pache L, Chanda SK, Rosen J: Functional genomic and high-content screening for target discovery and deconvolution. Expert Opin Drug Discov 2012,7(10):955-968.10.1517/17460441.2012.711311.
15. Sivan G, Martin SE, Myers TG, Buehler E, Szymczyk KH, Ormanoglu P, Moss B: Human genome-wide RNAi screen reveals a role for nuclear pore proteins in poxvirus morphogenesis. Proc Natl Acad Sci U S A 2013,110(9):3519-3524.10.1073/pnas.1300708110.
16. Buehler E, Chen YC, Martin S: C911: A bench-level control for sequence specific siRNA off-target effects. PLoS One 2012,7(12):e51942.10.1371/journal.pone.0051942.
17. Bassik MC, Kampmann M, Lebbink RJ, Wang S, Hein MY, Poser I, Weibezahn J, Horlbeck MA, Chen S, Mann M, Hyman AA, Leproust EM, McManus MT, Weissman JS: A systematic mammalian genetic interaction map reveals pathways underlying ricin susceptibility. Cell 2013,152(4):909-922.10.1016/j.cell.2013.01.030.
18. Kittler R, Surendranath V, Heninger AK, Slabicki M, Theis M, Putz G, Franke K, Caldarelli A, Grabner H, Kozak K, Wagner J, Rees E, Korn B, Frenzel C, Sachse C, Sönnichsen B, Guo J, Schelter J, Burchard J, Linsley PS, Jackson AL, Habermann B, Buchholz F: Genome-wide resources of endoribonuclease-prepared short interfering RNAs for specific loss-of-function studies. Nat Methods 2007,4(4):337-344.
19. Collinet C, Stoter M, Bradshaw CR, Samusik N, Rink JC, Kenski D, Habermann B, Buchholz F, Henschel R, Mueller MS, Nagel WE, Fava E, Kalaidzidis Y, Zerial M: Systems survey of endocytosis by multiparametric image analysis. Nature 2010,464(7286):243-249.10.1038/nature08779.
20. Marine S, Bahl A, Ferrer M, Buehler E: Common seed analysis to identify off-target effects in siRNA screens. J Biomol Screen 2012,17(3):370-378.10.1177/1087057111427348.
21. Buehler E, Khan AA, Marine S, Rajaram M, Bahl A, Burchard J, Ferrer M: siRNA off-target effects in genome-wide screens identify signaling pathway members. Sci Rep 2012, 2:428.
22. Sigoillot FD, Lyman S, Huckins JF, Adamson B, Chung E, Quattrochi B, King RW: A bioinformatics method identifies prominent off-targeted transcripts in RNAi screens. Nat Methods 2012,9(4):363-366.10.1038/nmeth.1898.
23. Dehio C, Meyer M, Berger J, Schwarz H, Lanz C: Interaction of Bartonella henselae with endothelial cells results in bacterial aggregation on the cell surface and the subsequent engulfment and internalisation of the bacterial aggregate by a unique structure, the invasome. J Cell Sci 1997,110(Pt 18):2141-2154.
24. Cossart P, Sansonetti PJ: Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 2004,304(5668):242-248.10.1126/science.1090124.
25. Meier O, Boucke K, Hammer SV, Keller S, Stidwill RP, Hemmi S, Greber UF: Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J Cell Biol 2002,158(6):1119-1131.10.1083/jcb.200112067.
26. Mercer J, Helenius A: Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008,320(5875):531-535.10.1126/science.1155164.
27. Malo N, Hanley JA, Cerquozzi S, Pelletier J, Nadon R: Statistical practice in high-throughput screening data analysis. Nat Biotechnol 2006,24(2):167-175.10.1038/nbt1186.
28. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM: Cell profiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 2006,7(10):R100.10.1186/gb-2006-7-10-r100.
29. Birmingham A, Selfors LM, Forster T, Wrobel D, Kennedy CJ, Shanks E, Santoyo-Lopez J, Dunican DJ, Long A, Kelleher D, Smith Q, Beijersbergen RL, Ghazal P, Shamu CE: Statistical methods for analysis of high-throughput RNA interference screens. Nat Methods 2009,6(8):569-575.10.1038/nmeth.1351.
30. Siebourg J, Merdes G, Misselwitz B, Hardt WD, Beerenwinkel N: Stability of gene rankings from RNAi screens. Bioinformatics 2012,28(12):1612-1618.10.1093/bioinformatics/bts192.
31. Snijder B, Pelkmans L: Origins of regulated cell-to-cell variability. Nat Rev Mol Cell Biol 2011,12(2):119-125.10.1038/nrm3044.
32. Rouilly V, Pujadas E, Hullar B, Balazs C, Kunszt P, Podvinec M: iBRAIN2: automated analysis and data handling for RNAi screens. Stud Health Technol Inform 2012, 175:205-213.
33. Pinheiro JC, Bates DM: Mixed-Effects Models in S and S-PLUS. New York: Springer. 2000.
34. Bates D, Maechler M, Bolker B: lme4: Linear Mixed-Effects Models Using S4 Classes. 2013. http://cran.r-project.org/package=lme4
35. Efron B, Turnbull BB, Narasimhan B: locfdr: Computes Local False Discovery Rates. 2011. http://cran.r-project.org/package=locfdr
36. Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
37. Pizarro-Cerda J, Kuhbacher A, Cossart P: Entry of listeria monocytogenes in Mammalian Epithelial Cells: an updated view. Cold Spring Harbor Perspect Med 2012, 2:11.
38. Tattoli I, Philpott DJ, Girardin SE: The bacterial and cellular determinants controlling the recruitment of mTOR to the Salmonella-containing vacuole. Biol Open 2012,1(12):1215-1225.10.1242/bio.20122840.
39. Konig R, Chiang CY, Tu BP, Yan SF, DeJesus PD, Romero A, Bergauer T, Orth A, Krueger U, Zhou Y, Chanda SK: A probability-based approach for the analysis of large-scale RNAi screens. Nat Methods 2007,4(10):847-849.10.1038/nmeth1089.
40. Zhang XD, Ferrer M, Espeseth AS, Marine SD, Stec EM, Crackower MA, Holder DJ, Heyse JF, Strulovici B: The use of strictly standardized mean difference for hit selection in primary RNA interference high-throughput screening experiments. J Biomol Screen 2007,12(4):497-509.10.1177/1087057107300646.
41. Meinshausen N, Bühlmann P: Stability selection. J R Stat Soc Ser B (Statistical Methodology) 2010,72(4):417-473.10.1111/j.1467-9868.2010.00740.x.
42. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP: Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005,102(43):15545-15550.10.1073/pnas.0506580102.
43. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Jensen LJ, von Mering C: The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 2011,39(Database issue):D561-D568.
44. Elfaki MG, Al-Hokail AA: Transforming growth factor beta production correlates with depressed lymphocytes function in humans with chronic brucellosis. Microbes Infect 2009,11(14-15):1089-1096.
45. Shen Y, Naujokas K, Park M, Ireton K: InlB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 2000,103(3):501-510.10.1016/S0092-8674(00)00141-0.
46. Zheng K, Chen DS, Wu YQ, Xu XJ, Zhang H, Chen CF, Chen HC, Liu ZF: MicroRNA expression profile in RAW264.7 cells in response to Brucella melitensis infection. Int J Biol Sci 2012,8(7):1013-1022.10.7150/ijbs.3836.
47. Qin QM, Pei J, Ancona V, Shaw BD, Ficht TA, de Figueiredo P: RNAi screen of endoplasmic reticulum-associated host factors reveals a role for IRE1alpha in supporting Brucella replication. PLoS Pathog 2008,4(7):e1000110.10.1371/journal.ppat.1000110.
48. Cain RJ, Vanhaesebroeck B, Ridley AJ: The PI3K p110alpha isoform regulates endothelial adherens junctions via Pyk2 and Rac1. J Cell Biol 2010,188(6):863-876.10.1083/jcb.200907135.
49. Kakumoto T, Nakata T: Optogenetic control of PIP3: PIP3 is sufficient to induce the actin-based active part of growth cones and is regulated via endocytosis. PLoS One 2013,8(8):e70861.10.1371/journal.pone.0070861.
50. Grassme H, Riehle A, Wilker B, Gulbins E: Rhinoviruses infect human epithelial cells via ceramide-enriched membrane platforms. J Biol Chem 2005,280(28):26256-26262.10.1074/jbc.M500835200.
51. Sessions OM, Barrows NJ, Souza-Neto JA, Robinson TJ, Hershey CL, Rodgers MA, Ramirez JL, Dimopoulos G, Yang PL, Pearson JL, Garcia-Blanco MA: Discovery of insect and human dengue virus host factors. Nature 2009,458(7241):1047-1050.10.1038/nature07967.
52. Suomalainen M, Luisoni S, Boucke K, Bianchi S, Engel DA, Greber UF: A direct and versatile assay measuring membrane penetration of adenovirus in single cells. J Virol 2013,87(22):12367-12379.10.1128/JVI.01833-13.
53. Yakimovich A, Gumpert H, Burckhardt CJ, Lutschg VA, Jurgeit A, Sbalzarini IF, Greber UF: Cell-free transmission of human adenovirus by passive mass transfer in cell culture simulated in a computer model. J Virol 2012,86(18):10123-10137.10.1128/JVI.01102-12.
54. Dehio M, Knorre A, Lanz C, Dehio C: Construction of versatile high-level expression vectors for Bartonella henselae and the use of green fluorescent protein as a new expression marker. Gene 1998,215(2):223-229.10.1016/S0378-1119(98)00319-9.
55. Celli J, Salcedo SP, Gorvel JP: Brucella coopts the small GTPase Sar1 for intracellular replication. Proc Natl Acad Sci U S A 2005,102(5):1673-1678.10.1073/pnas.0406873102.
56. Jurgeit A, Moese S, Roulin P, Dorsch A, Lotzerich M, Lee WM, Greber UF: An RNA replication-center assay for high content image-based quantifications of human rhinovirus and coxsackievirus infections. Virol J 2010, 7:264.10.1186/1743-422X-7-264.
57. Jurgeit A, McDowell R, Moese S, Meldrum E, Schwendener R, Greber UF: Niclosamide is a proton carrier and targets acidic endosomes with broad antiviral effects. PLoS Pathog 2012, 10:8.
58. Mosser AG, Brockman-Schneider R, Amineva S, Burchell L, Sedgwick JB, Busse WW, Gern JE: Similar frequency of rhinovirus-infectible cells in upper and lower airway epithelium. J Infect Dis 2002,185(6):734-743.10.1086/339339.
59. Efron B: Large-Scale Inference: Empirical Bayes Methods for Estimation, Testing, and Prediction. Cambridge: Cambridge University Press. 2010.