Deep sequencing of virus-infected cells reveals HIV-encoded small RNAs

Nucleic Acids Research

Volumn 40, Issue 1, 2012, Pages 414-427

  Schopman, Nick C T ^a   Willemsen, Marcel ^a   Liu, Ying Poi ^a   Bradley, Ted ^a   Van Kampen, Antoine ^a,b   Baas, Frank ^a   Berkhout, Ben ^a   Haasnoot, Joost ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; SMALL INTERFERING RNA; SMALL VIRUS INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS RNA;

3' UNTRANSLATED REGION; ARTICLE; CELL POLARITY; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA GENE; RNA INTERFERENCE; RNA SEQUENCE; T LYMPHOCYTE; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INHIBITION;

BASE SEQUENCE; CELLS, CULTURED; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HIV-1; HUMANS; MICRORNAS; MOLECULAR SEQUENCE DATA; RNA INTERFERENCE; RNA, ANTISENSE; RNA, SMALL INTERFERING; RNA, TRANSFER, LYS; RNA, VIRAL; SEQUENCE ANALYSIS, RNA;

HEXAPODA; HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA; NEMATODA;

EID: 84855295489     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr719     Document Type: Article

References (54)

1. Waterhouse, P.M., Wang, M.B. and Lough, T. (2001) Gene silencing as an adaptive defence against viruses. Nature, 411, 834-842. (Pubitemid 32588111)
2. Voinnet, O. (2001) RNA silencing as a plant immune system against viruses. Trends Genet., 17, 449-459. (Pubitemid 32727237)
3. Wilkins, C., Dishongh, R., Moore, S.C., Whitt, M.A., Chow, M. and Machaca, K. (2005) RNA interference is an antiviral defence mechanism in Caenorhabditis elegans. Nature, 436, 1044-1047. (Pubitemid 41191690)
4. Wang, X.H., Aliyari, R., Li, W.X., Li, H.W., Kim, K., Carthew, R., Atkinson, P. and Ding, W. (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science, 312, 452-454.
5. Segers, G.C., Zhang, X., Deng, F., Sun, Q. and Nuss, D.L. (2007) Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proc. Natl Acad. Sci. USA, 104, 12902-12906. (Pubitemid 47255252)
6. de Vries, W. and Berkhout, B. (2008) RNAi suppressors encoded by pathogenic human viruses. Int. J. Biochem. Cell Biol., 40, 2007-2012.
7. Meister, G. and Tuschl, T. (2004) Mechanisms of gene silencing by double-stranded RNA. Nature, 431, 343-349. (Pubitemid 39265674)
8. Boss, I.W., Plaisance, K.B. and Renne, R. (2009) Role of virus-encoded microRNAs in herpesvirus biology. Trends Microbiol., 17, 544-553.
9. Pfeffer, S., Zavolan, M., Grasser, F.A., Chien, M., Russo, J.J., Ju, J., John, B., Enright, A.J., Marks, D., Sander, C. et al. (2004) Identification of virus-encoded microRNAs. Science, 304, 734-736. (Pubitemid 38560879)
10. Umbach, J.L., Kramer, M.F., Jurak, I., Karnowski, H.W., Coen, D.M. and Cullen, B.R. (2008) MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature, 454, 780-783.
11. Wu, Q., Luo, Y., Lu, R., Lau, N., Lai, E.C., Li, W.X. and Ding, S.W. (2010) Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc. Natl Acad. Sci. USA, 107, 1606-1611.
12. Fischer, W., Ganusov, V.V., Giorgi, E.E., Hraber, P.T., Keele, B.F., Leitner, T., Han, C.S., Gleasner, C.D., Green, L., Lo, C.C. et al. (2010) Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS ONE, 5.
13. Reese, T.A., Xia, J., Johnson, L.S., Zhou, X., Zhang, W. and Virgin, H.W. (2010) Identification of novel microRNA-like molecules generated from herpesvirus and host tRNA transcripts. J. Virol., 84, 10344-10353.
14. Metzker, M.L. (2010) Sequencing technologies -the next generation. Nat. Rev. Genet., 11, 31-46.
15. Parameswaran, P., Sklan, E., Wilkins, C., Burgon, T., Samuel, M.A., Lu, R., Ansel, K.M., Heissmeyer, V., Einav, S., Jackson, W. et al. (2010) Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS. Pathog., 6, e1000764.
16. Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., Chiba, H., Kohara, Y., Kono, T., Nakano, T. et al. (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature, 453, 539-543. (Pubitemid 351733315)
17. Yeung, M.L., Bennasser, Y., Watashi, K., Le, S.Y., Houzet, L. and Jeang, K.T. (2009) Pyrosequencing of small non-coding RNAs in HIV-1 infected cells: evidence for the processing of a viral-cellular double-stranded RNA hybrid. Nucleic Acids Res., 37, 6575-6586.
18. Lefebvre, G., Desfarges, S., Uyttebroeck, F., Munoz, M., Beerenwinkel, N., Rougemont, J., Telenti, A. and Ciuffi, A. (2011) Analysis of HIV-1 expression level and sense of transcription by high-throughput sequencing of the infected cell. J. Virol., 85, 6205-6211.
19. Peden, K., Emerman, M. and Montagnier, L. (1991) Changes in growth properties on passage in tissue culture of viruses derived from infectious molecular clones of HIV-1LAI, HIV-1MAL, and HIV-1ELI. Virology, 185, 661-672.
20. Zhou, X., Vink, M., Klaver, B., Berkhout, B. and Das, A.T. (2006) Optimization of the Tet-On system for regulated gene expression through viral evolution. Gene Ther., 13, 1382-1390. (Pubitemid 44420633)
21. Schopman, N.C., Ter Brake, O. and Berkhout, B. (2010) Anticipating and blocking HIV-1 escape by second generation antiviral shRNAs. Retrovirology, 7, 52.
22. Ruijter, J.M., Thygesen, H.H., Schoneveld, O.J., Das, A.T., Berkhout, B. and Lamers, W.H. (2006) Factor correction as a tool to eliminate between-session variation in replicate experiments: application to molecular biology and retrovirology. Retrovirology, 3, 1-8.
23. Schopman, N.C., Liu, Y.P., Konstantinova, P., Ter Brake, O. and Berkhout, B. (2010) Optimization of shRNA inhibitors by variation of the terminal loop sequence. Antiviral Res., 86, 204-211.
24. Berkhout, B., Silverman, R.H. and Jeang, K.T. (1989) Tat trans-activates the human immunodeficiency virus through a nascent RNA target. Cell, 59, 273-282. (Pubitemid 19264373)
25. Verhoef, K., Marzio, G., Hillen, W., Bujard, H. and Berkhout, B. (2001) Strict control of human immunodeficiency virus type 1 replication by a genetic switch: Tet for Tat. J. Virol., 75, 979-987. (Pubitemid 32037300)
26. Cole, C., Sobala, A., Lu, C., Thatcher, S.R., Bowman, A., Brown, J.W., Green, P.J., Barton, G.J. and Hutvagner, G. (2009) Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA, 15, 2147-2160.
27. Haussecker, D., Huang, Y., Lau, A., Parameswaran, P., Fire, A.Z. and Kay, M.A. (2010) Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA, 16, 673-695.
28. Schopman, N.C., Heynen, S., Haasnoot, J. and Berkhout, B. (2010) A miRNA-tRNA mix-up: tRNA origin of proposed miRNA. RNA. Biol., 7, 573-576.
29. Abbink, T.E. and Berkhout, B. (2008) HIV-1 reverse transcription initiation: a potential target for novel antivirals? Virus Res., 134, 4-18.
30. Jiang, P., Wu, H., Wang, W., Ma, W., Sun, X. and Lu, Z. (2007) MiPred: classification of real and pseudo microRNA precursors using random forest prediction model with combined features. Nucleic Acids Res., 35, W339-W344.
31. Bennasser, Y., Le, S.Y., Yeung, M.L. and Jeang, K.T. (2004) HIV-1 encoded candidate micro-RNAs and their cellular targets. Retrovirology, 1, 43.
32. Klase, Z., Winograd, R., Davis, J., Carpio, L., Hildreth, R., Heydarian, M., Fu, S., McCaffrey, T., Meiri, E., yash-Rashkovsky, M. et al. (2009) HIV-1 TAR miRNA protects against apoptosis by altering cellular gene expression. Retrovirology, 6, 18.
33. Klase, Z., Kale, P., Winograd, R., Gupta, M.V., Heydarian, M., Berro, R., McCaffrey, T. and Kashanchi, F. (2007) HIV-1 TAR element is processed by Dicer to yield a viral micro-RNA involved in chromatin remodeling of the viral LTR. BMC. Mol. Biol., 8, 63.
34. Ouellet, D.L., Plante, I., Landry, P., Barat, C., Janelle, M.E., Flamand, L., Tremblay, M.J. and Provost, P. (2008) Identification of functional microRNAs released through asymmetrical processing of HIV-1 TAR element. Nucleic Acids Res., 36, 2353-2365. (Pubitemid 351567008)
35. Berkhout, B., Vastenhouw, N.L., Klasens, B.I. and Huthoff, H. (2001) Structural features in the HIV-1 repeat region facilitate strand transfer during reverse transcription. RNA, 7, 1097-1114. (Pubitemid 32726909)
36. Klasens, B.I.F., Huthoff, H.T., Das, A.T., Jeeninga, R.E. and Berkhout, B. (1999) The effect of template RNA structure on elongation by HIV-1 reverse transcriptase. Biochim. Biophys. Acta, 1444, 355-370. (Pubitemid 29147308)
37. Larocca, D., Chao, L.A., Seto, M.H. and Brunck, T.K. (1989) Human T-cell leukemia virus minus strand transcription in infected T-cells. Biochem. Biophys. Res. Commun., 163, 1006-1013. (Pubitemid 19236950)
38. Gaudray, G., Gachon, F., Basbous, J., Biard-Piechaczyk, M., Devaux, C. and Mesnard, J.M. (2002) The complementary strand of the human T-cell leukemia virus type 1 RNA genome encodes a bZIP transcription factor that down-regulates viral transcription. J. Virol., 76, 12813-12822. (Pubitemid 35386965)
39. Cavanagh, M.H., Landry, S., Audet, B., Arpin-Andre, C., Hivin, P., Pare, M.E., Thete, J., Wattel, E., Marriott, S.J., Mesnard, J.M. et al. (2006) HTLV-I antisense transcripts initiating in the 30LTR are alternatively spliced and polyadenylated. Retrovirology, 3, 15.
40. Briquet, S., Richardson, J., Vanhee-Brossollet, C. and Vaquero, C. (2001) Natural antisense transcripts are detected in different cell lines and tissues of cats infected with feline immunodeficiency virus. Gene, 267, 157-164. (Pubitemid 32324132)
41. Rasmussen, M.H., Ballarin-Gonzalez, B., Liu, J., Lassen, L.B., Fuchtbauer, A., Fuchtbauer, E.M., Nielsen, A.L. and Pedersen, F.S. (2010) Antisense transcription in gammaretroviruses as a mechanism of insertional activation of host genes. J. Virol., 84, 3780-3788.
42. Landry, S., Halin, M., Lefort, S., Audet, B., Vaquero, C., Mesnard, J.M. and Barbeau, B. (2007) Detection, characterization and regulation of antisense transcripts in HIV-1. Retrovirology, 4, 71.
43. Morris, K.V., Santoso, S., Turner, A.M., Pastori, C. and Hawkins, P.G. (2008) Bidirectional transcription directs both transcriptional gene activation and suppression in human cells. PLoS Genet., 4, e1000258.
44. Ghildiyal, M. and Zamore, P.D. (2009) Small silencing RNAs: an expanding universe. Nat. Rev. Genet., 10, 94-108.
45. Yang, N. and Kazazian, H.H. Jr (2006) L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat. Struct. Mol. Biol., 13, 763-771. (Pubitemid 44338769)
46. Kasschau, K.D. and Carrington, J.C. (1998) A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell, 95, 461-470. (Pubitemid 28533303)
47. Haasnoot, J., Westerhout, E.M. and Berkhout, B. (2007) RNA interference against viruses: strike and counterstrike. Nat. Biotechnol., 25, 1435-1443. (Pubitemid 350233142)
48. Qi, X., Bao, F.S. and Xie, Z. (2009) Small RNA deep sequencing reveals role for Arabidopsis thaliana RNA-dependent RNA polymerases in viral siRNA biogenesis. PLoS ONE, 4, e4971.
49. Haasnoot, J., de Vries, W., Geutjes, E.J., Prins, M., de Haan, P. and Berkhout, B. (2007) The Ebola virus VP35 protein is a suppressor of RNA silencing. PLoS Pathog., 3, e86.
50. Bennasser, Y., Le, S.Y., Benkirane, M. and Jeang, K.T. (2005) Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity, 22, 607-619. (Pubitemid 40719196)
51. Huang, J., Wang, F., Argyris, E., Chen, K., Liang, Z., Tian, H., Huang, W., Squires, K., Verlinghieri, G. and Zhang, H. (2007) Cellular microRNAs contribute to HIV-1 latency in resting primary CD4(+) T lymphocytes. Nat. Med., 13, 1241-1247. (Pubitemid 47530631)
52. Das, A.T., Klaver, B. and Berkhout, B. (1995) Reduced replication of human immunodeficiency virus type 1 mutants that use reverse transcription primers other than the natural tRNA(3Lys). J. Virol., 69, 3090-3097.
53. Qian, S., Zhong, X., Yu, L., Ding, B., de Haan, P. and Boris-Lawrie, K. (2009) HIV-1 Tat RNA silencing suppressor activity is conserved across kingdoms and counteracts translational repression of HIV-1. Proc. Natl Acad. Sci. USA, 106, 605-610.
54. Michael, N.L., Vahey, M.T., D'Arcy, L., Ehrenberg, P.K., Mosca, J.D., Rappaport, J. and Redfield, R.R. (1994) Negative-strand RNA transcripts are produced in human immunodeficiency virus type 1-infected cells and patients by a novel promoter downregulated by Tat. J. Virol., 68, 979-987. (Pubitemid 24022202)