Comprehensive identification of host modulators of HIV-1 replication using multiple orthologous RNAi reagents

Cell Reports

Volumn 9, Issue 2, 2014, Pages 752-766

  Zhu, Jian ^a   Davoli, Teresa ^a   Perriera, Jill M ^b   Chin, Christopher R ^b   Gaiha, Gaurav D ^c   John, Sinu P ^c   Sigiollot, Frederic D ^d   Gao, Geng ^a   Xu, Qikai ^a   Qu, Hongjing ^a   Pertel, Thomas ^c   Sims, Jennifer S ^c   Smith, Jennifer A ^e   Baker, Richard E ^b   Maranda, Louise ^b   Ng, Aylwin ^f   Elledge, Stephen J ^a,g   Brass, Abraham L ^b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c HARVARD UNIVERSITY   (United States)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CELL PROTEIN; GOLGI49 PROTEIN; NUCLEOPORIN; PROTEIN COG; PROTEIN THOC2; REGULATOR PROTEIN; SEC13 PROTEIN; SUPT16H PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; NUCLEAR PROTEIN; SEC13 PROTEIN, HUMAN; THOC1 PROTEIN, HUMAN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION; GENETIC PROCEDURES; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERMETHOD COMPARISON; NONHUMAN; NUCLEOTIDE METABOLISM; PROTEIN ANALYSIS; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; RNA INTERFERENCE GENE ENRICHMENT RANKING; VIRUS CELL INTERACTION; VIRUS REPLICATION; ALGORITHM; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HIGH THROUGHPUT SCREENING; HOST PATHOGEN INTERACTION; HUMAN; JURKAT CELL LINE; METABOLISM; PHYSIOLOGY; PROCEDURES;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ALGORITHMS; CARRIER PROTEINS; CELL CYCLE PROTEINS; HEK293 CELLS; HELA CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; JURKAT CELLS; NUCLEAR PROTEINS; RNA INTERFERENCE; VIRUS REPLICATION;

EID: 84919667982     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.09.031     Document Type: Article

References (33)

1. Adamson, B., Smogorzewska, A., Sigoillot, F.D., King, R.W., and Elledge, S.J. (2012). A genome-wide homologous recombination screen identifies the RNAbinding protein RBMX as a component of the DNA-damage response. Nat. Cell Biol. 14, 318-328.
2. Belotserkovskaya, R., Oh, S., Bondarenko, V.A., Orphanides, G., Studitsky, V.M., and Reinberg, D. (2003). FACT facilitates transcription-dependent nucleosome alteration. Science 301, 1090-1093.
3. Brass, A.L., Dykxhoorn, D.M., Benita, Y., Yan, N., Engelman, A., Xavier, R.J., Lieberman, J., and Elledge, S.J. (2008). Identification of host proteins required for HIV infection through a functional genomic screen. Science 319, 921-926.
4. Bushman, F.D., Malani, N., Fernandes, J., D'Orso, I., Cagney, G., Diamond, T.L., Zhou, H., Hazuda, D.J., Espeseth, A.S., König, R., et al. (2009). Host cell factors in HIV replication: meta-analysis of genome-wide studies. PLoS Pathog. 5, e1000437.
5. Capelson, M., Liang, Y., Schulte, R., Mair, W., Wagner, U., and Hetzer, M.W. (2010). Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140, 372-383.
6. Cheong, C.G., Wolan, D.W., Greasley, S.E., Horton, P.A., Beardsley, G.P., and Wilson, I.A. (2004). Crystal structures of human bifunctional enzyme aminoimidazole-4-carboxamide ribonucleotide transformylase/IMP cyclohydrolase in complex with potent sulfonyl-containing antifolates. J. Biol. Chem. 279, 18034-18045.
7. Ciuffi, A., Llano, M., Poeschla, E., Hoffmann, C., Leipzig, J., Shinn, P., Ecker, J.R., and Bushman, F. (2005). A role for LEDGF/p75 in targeting HIV DNA integration. Nat. Med. 11, 1287-1289.
8. Di Nunzio, F. (2013). New insights in the role of nucleoporins: a bridge leading to concerted steps from HIV-1 nuclear entry until integration. Virus Res. 178, 187-196.
9. Echeverri, C.J., Beachy, P.A., Baum, B., Boutros, M., Buchholz, F., Chanda, S.K., Downward, J., Ellenberg, J., Fraser, A.G., Hacohen, N., et al. (2006). Minimizing the risk of reporting false positives in large-scale RNAi screens. Nat. Methods 3, 777-779.
10. Gallastegui, E., Millán-Zambrano, G., Terme, J.M., Chávez, S., and Jordan, A. (2011). Chromatin reassembly factors are involved in transcriptional interference promoting HIV latency. J. Virol. 85, 3187-3202.
11. Goff, S.P. (2007). Host factors exploited by retroviruses. Nat. Rev. Microbiol. 5, 253-263.
12. Goff, S.P. (2008). Knockdown screens to knockout HIV-1. Cell 135, 417-420.
13. Hao, L., He, Q., Wang, Z., Craven, M., Newton, M.A., and Ahlquist, P. (2013). Limited agreement of independent RNAi screens for virus-required host genes owes more to false-negative than false-positive factors. PLoS Comput. Biol. 9, e1003235.
14. Hsia, K.C., Stavropoulos, P., Blobel, G., and Hoelz, A. (2007). Architecture of a coat for the nuclear pore membrane. Cell 131, 1313-1326.
15. Jäger, S., Cimermancic, P., Gulbahce, N., Johnson, J.R., McGovern, K.E., Clarke, S.C., Shales, M., Mercenne, G., Pache, L., Li, K., et al. (2012). Global landscape of HIV-human protein complexes. Nature 481, 365-370.
16. Jha, S., Shibata, E., and Dutta, A. (2008). Human Rvb1/Tip49 is required for the histone acetyltransferase activity of Tip60/NuA4 and for the downregulation of phosphorylation on H2AX after DNA damage. Mol. Cell. Biol. 28, 2690-2700.
17. Kittler, R., Surendranath, V., Heninger, A.K., Slabicki, M., Theis, M., Putz, G., Franke, K., Caldarelli, A., Grabner, H., Kozak, K., et al. (2007). Genome-wide resources of endoribonuclease-prepared short interfering RNAs for specific loss-of-function studies. Nat. Methods 4, 337-344.
18. König, R., Zhou, Y., Elleder, D., Diamond, T.L., Bonamy, G.M., Irelan, J.T., Chiang, C.Y., Tu, B.P., De Jesus, P.D., Lilley, C.E., et al. (2008). Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 135, 49-60.
19. Liptak, T. (1958). On the combination of independent tests. Magyar Tud Akad Mat Kutato Int Kozl 3, 171-197.
20. Luo, B., Cheung, H.W., Subramanian, A., Sharifnia, T., Okamoto, M., Yang, X., Hinkle, G., Boehm, J.S., Beroukhim, R., Weir, B.A., et al. (2008). Highly parallel identification of essential genes in cancer cells. Proc. Natl. Acad. Sci. USA 105, 20380-20385.
21. Meier, R., Franceschini, A., Horvath, P., Tetard, M., Mancini, R., von Mering, C., Helenius, A., and Lozach, P.Y. (2014). Genome-wide siRNA screens reveal VAMP3 as a novel host factor required for Uukuniemi virus late penetration. J. Virol. 88, 8565-8578.
22. Miller, V.J., and Ungar, D. (2012). Re'COG'nition at the Golgi. Traffic 13, 891-897.
23. Miller, M.D., Farnet, C.M., and Bushman, F.D. (1997). Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J. Virol. 71, 5382-5390.
24. Parent, M., Yung, T.M., Rancourt, A., Ho, E.L., Vispé, S., Suzuki-Matsuda, F., Uehara, A., Wada, T., Handa, H., and Satoh, M.S. (2005). Poly(ADP-ribose) polymerase-1 is a negative regulator of HIV-1 transcription through competitive binding to TAR RNA with Tat.positive transcription elongation factor b (p-TEFb) complex. J. Biol. Chem. 280, 448-457.
25. Puri, N., Wang, X., Varma, R., Burnett, C., Beauchamp, L., Batten, D.M., Young, M., Sule, V., Latham, K., Sendera, T., et al. (2008). LNA incorporated siRNAs exhibit lower off-target effects compared to 2'-OMethoxy in cell phenotypic assays and microarray analysis. Nucleic Acids Symp. Ser. (Oxf.) 52, 25-26.
26. Sigoillot, F.D., Lyman, S., Huckins, J.F., Adamson, B., Chung, E., Quattrochi, B., and King, R.W. (2012). A bioinformatics method identifies prominent offtargeted transcripts in RNAi screens. Nat. Methods 9, 363-366.
27. Strässer, K., Masuda, S., Mason, P., Pfannstiel, J., Oppizzi, M., Rodriguez-Navarro, S., Rondón, A.G., Aguilera, A., Struhl, K., Reed, R., and Hurt, E. (2002). TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417, 304-308.
28. Sundquist, W.I., and Krausslich, H.G. (2012). HIV-1 assembly, budding, and maturation. Cold Spring Harb. Perspect. Med. 2, a006924.
29. Takatalo, M., Järvinen, E., Laitinen, S., Thesleff, I., and Rönnholm, R. (2008). Expression of the novel Golgi protein GoPro49 is developmentally regulated during mesenchymal differentiation. Dev. Dyn. 237, 2243-2255.
30. Viphakone, N., Hautbergue, G.M., Walsh, M., Chang, C.T., Holland, A., Folco, E.G., Reed, R., and Wilson, S.A. (2012). TREX exposes the RNA-binding domain of Nxf1 to enable mRNA export. Nat. Commun. 3, 1006.
31. Weiss, A., Wiskocil, R.L., and Stobo, J.D. (1984). The role of T3 surface molecules in the activation of human T cells: a two-stimulus requirement for IL 2 production reflects events occurring at a pre-translational level. J. Immunol. 133, 123-128.
32. Zhou, H., Xu, M., Huang, Q., Gates, A.T., Zhang, X.D., Castle, J.C., Stec, E., Ferrer, M., Strulovici, B., Hazuda, D.J., and Espeseth, A.S. (2008). Genomescale RNAi screen for host factors required for HIV replication. Cell Host Microbe 4, 495-504.
33. Zhu, J., Gaiha, G.D., John, S.P., Pertel, T., Chin, C.R., Gao, G., Qu, H., Walker, B.D., Elledge, S.J., and Brass, A.L. (2012). Reactivation of latent HIV-1 by inhibition of BRD4. Cell Reports 2, 807-816.