Tailored enrichment strategy detects low abundant small noncoding RNAs in HIV-1 infected cells

Retrovirology

Volumn 9, Issue , 2012, Pages

  Althaus, Claudia F ^a   Vongrad, Valentina ^a   Niederöst, Barbara ^a   Joos, Beda ^a   Di Giallonardo, Francesca ^a   Rieder, Philip ^a   Pavlovic, Jovan ^b   Trkola, Alexandra ^b   Günthard, Huldrych F ^a   Metzner, Karin J ^a   Fischer, Marek ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Antisense RNA; HIV 1; Hybridization capture; Small noncoding RNA

Indexed keywords

MICRORNA; SMALL INTERFERING RNA; SMALL UNTRANSLATED RNA; VIRUS RNA;

ARTICLE; CD4+ T LYMPHOCYTE; CLONE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HYBRIDIZATION; HYBRIDIZATION CAPTURE; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; RNA ANALYSIS; RNA SEQUENCE; RNA STRUCTURE; VIRUS GENOME; VIRUS REPLICATION; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOGENICITY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; GENE EXPRESSION REGULATION, VIRAL; HIV-1; HUMANS; MACROPHAGES; RNA, SMALL UNTRANSLATED; RNA, VIRAL;

EID: 84858980105     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-9-27     Document Type: Article

References (47)

1. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811. 10.1038/35888, 9486653.
2. Farazi TA, Juranek SA, Tuschl T. The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 2008, 135:1201-1214. 10.1242/dev.005629, 18287206.
3. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat Rev Genet 2008, 9:102-114.
4. Huttenhofer A, Vogel J. Experimental approaches to identify non-coding RNAs. Nucleic Acids Res 2006, 34:635-646. 10.1093/nar/gkj469, 1351373, 16436800.
5. Kong W, Zhao JJ, He L, Cheng JQ. Strategies for profiling microRNA expression. J Cell Physiol 2009, 218:22-25. 10.1002/jcp.21577, 18767038.
6. Lu C, Tej SS, Luo S, Haudenschild CD, Meyers BC, Green PJ. Elucidation of the small RNA component of the transcriptome. Science 2005, 309:1567-1569. 10.1126/science.1114112, 16141074.
7. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
8. Schopman NC, Willemsen M, Liu YP, Bradley T, van Kampen A, Baas F, Berkhout B, Haasnoot J. Deep sequencing of virus-infected cells reveals HIV-encoded small RNAs. Nucleic Acids Res 2012, 40:414-427. 10.1093/nar/gkr719, 3245934, 21911362.
9. Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T. Identification of virus-encoded microRNAs. Science 2004, 304:734-736. 10.1126/science.1096781, 15118162.
10. Mrazek J, Kreutmayer SB, Grasser FA, Polacek N, Huttenhofer A. Subtractive hybridization identifies novel differentially expressed ncRNA species in EBV-infected human B cells. Nucleic Acids Res 2007, 35:e73. 10.1093/nar/gkm244, 1904266, 17478510.
11. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, Grasser FA, van Dyk LF, Ho CK, Shuman S, Chien M, et al. Identification of microRNAs of the herpesvirus family. Nat Methods 2005, 2:269-276. 10.1038/nmeth746, 15782219.
12. Parameswaran P, Sklan E, Wilkins C, Burgon T, Samuel MA, Lu R, Ansel KM, Heissmeyer V, Einav S, Jackson W, et al. Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS Pathog 2010, 6:e1000764. 10.1371/journal.ppat.1000764, 2820531, 20169186.
13. Yeung ML, Bennasser Y, Watashi K, Le SY, Houzet L, Jeang KT. 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 2009, 37:6575-6586. 10.1093/nar/gkp707, 2770672, 19729508.
14. Lin J, Cullen BR. Analysis of the interaction of primate retroviruses with the human RNA interference machinery. J Virol 2007, 81:12218-12226. 10.1128/JVI.01390-07, 2169020, 17855543.
15. Klase Z, Kale P, Winograd R, Gupta MV, Heydarian M, Berro R, McCaffrey T, Kashanchi F. 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 2007, 8:63. 10.1186/1471-2199-8-63, 1955452, 17663774.
16. Ouellet DL, Plante I, Landry P, Barat C, Janelle ME, Flamand L, Tremblay MJ, Provost P. Identification of functional microRNAs released through asymmetrical processing of HIV-1 TAR element. Nucleic Acids Res 2008, 36:2353-2365. 10.1093/nar/gkn076, 2367715, 18299284.
17. Bennasser Y, Le SY, Benkirane M, Jeang KT. Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity 2005, 22:607-619. 10.1016/j.immuni.2005.03.010, 15894278.
18. Omoto S, Ito M, Tsutsumi Y, Ichikawa Y, Okuyama H, Brisibe EA, Saksena NK, Fujii YR. HIV-1 nef suppression by virally encoded microRNA. Retrovirology 2004, 1:44. 10.1186/1742-4690-1-44, 544868, 15601474.
19. Kaul D, Khanna A, Suman. Evidence and nature of a novel miRNA encoded by HIV-1. Proc Indian Natl Sci Acad 2006, 72:91-95.
20. Cloonan N, Wani S, Xu Q, Gu J, Lea K, Heater S, Barbacioru C, Steptoe AL, Martin HC, Nourbakhsh E, et al. MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol 2011, 12:R126. 10.1186/gb-2011-12-12-r126, 22208850.
21. Mamanova L, Coffey AJ, Scott CE, Kozarewa I, Turner EH, Kumar A, Howard E, Shendure J, Turner DJ. Target-enrichment strategies for next-generation sequencing. Nat Methods 2010, 7:111-118. 10.1038/nmeth.1419, 20111037.
22. Huang J, Wang F, Argyris E, Chen K, Liang Z, Tian H, Huang W, Squires K, Verlinghieri G, Zhang H. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat Med 2007, 13:1241-1247. 10.1038/nm1639, 17906637.
23. Rieder P, Joos B, von Wyl V, Kuster H, Grube C, Leemann C, Boni J, Yerly S, Klimkait T, Burgisser P, et al. HIV-1 transmission after cessation of early antiretroviral therapy among men having sex with men. AIDS 2010, 24:1177-1183. 10.1097/QAD.0b013e328338e4de, 20386427.
24. Huelsmann PM, Rauch P, Allers K, John MJ, Metzner KJ. Inhibition of drug-resistant HIV-1 by RNA interference. Antiviral Res 2006, 69:1-8. 10.1016/j.antiviral.2005.10.001, 16290277.
25. Cella M, Salio M, Sakakibara Y, Langen H, Julkunen I, Lanzavecchia A. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J Exp Med 1999, 189:821-829. 10.1084/jem.189.5.821, 2192946, 10049946.
26. Vaz C, Ahmad HM, Sharma P, Gupta R, Kumar L, Kulshreshtha R, Bhattacharya A. Analysis of microRNA transcriptome by deep sequencing of small RNA libraries of peripheral blood. BMC Genomics 2010, 11:288. 10.1186/1471-2164-11-288, 2885365, 20459673.
27. Michael NL, Vahey MT, D'Arcy L, Ehrenberg PK, Mosca JD, Rappaport J, Redfield RR. 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 1994, 68:979-987. 236536, 8289399.
28. Landry S, Halin M, Lefort S, Audet B, Vaquero C, Mesnard JM, Barbeau B. Detection, characterization and regulation of antisense transcripts in HIV-1. Retrovirology 2007, 4:71. 10.1186/1742-4690-4-71, 2099442, 17910760.
29. Ludwig LB, Ambrus JL, Krawczyk KA, Sharma S, Brooks S, Hsiao CB, Schwartz SA. Human Immunodeficiency Virus-Type 1 LTR DNA contains an intrinsic gene producing antisense RNA and protein products. Retrovirology 2006, 3:80. 10.1186/1742-4690-3-80, 1654176, 17090330.
30. Lefebvre G, Desfarges S, Uyttebroeck F, Munoz M, Beerenwinkel N, Rougemont J, Telenti A, Ciuffi A. Analysis of HIV-1 expression level and sense of transcription by high-throughput sequencing of the infected cell. J Virol 2011, 85:6205-6211. 10.1128/JVI.00252-11, 3126515, 21507965.
31. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermuller J, Hofacker IL, et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 2007, 316:1484-1488. 10.1126/science.1138341, 17510325.
32. Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK, Kurokawa R. Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 2008, 454:126-130. 10.1038/nature06992, 2823488, 18509338.
33. Rother S, Meister G. Small RNAs derived from longer non-coding RNAs. Biochimie 2011, 93:1905-1915. 10.1016/j.biochi.2011.07.032, 21843590.
34. Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS. Non-coding RNAs: regulators of disease. J Pathol 2010, 220:126-139. 10.1002/path.2638, 19882673.
35. Lenasi T, Contreras X, Peterlin BM. Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe 2008, 4:123-133. 10.1016/j.chom.2008.05.016, 18692772.
36. Hafner M, Landgraf P, Ludwig J, Rice A, Ojo T, Lin C, Holoch D, Lim C, Tuschl T. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods 2008, 44:3-12. 10.1016/j.ymeth.2007.09.009, 2847350, 18158127.
37. Wang X, Ye L, Hou W, Zhou Y, Wang YJ, Metzger DS, Ho WZ. Cellular microRNA expression correlates with susceptibility of monocytes/macrophages to HIV-1 infection. Blood 2009, 113:671-674. 10.1182/blood-2008-09-175000, 2628373, 19015395.
38. Trkola A, Kuster H, Rusert P, Joos B, Fischer M, Leemann C, Manrique A, Huber M, Rehr M, Oxenius A, et al. Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat Med 2005, 11:615-622. 10.1038/nm1244, 15880120.
39. Moore JP, McKeating JA, Weiss RA, Sattentau QJ. Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science 1990, 250:1139-1142. 10.1126/science.2251501, 2251501.
40. Rusert P, Kuster H, Joos B, Misselwitz B, Gujer C, Leemann C, Fischer M, Stiegler G, Katinger H, Olson WC, et al. Virus isolates during acute and chronic human immunodeficiency virus type 1 infection show distinct patterns of sensitivity to entry inhibitors. J Virol 2005, 79:8454-8469. 10.1128/JVI.79.13.8454-8469.2005, 1143729, 15956589.
41. Koyanagi Y, Miles S, Mitsuyasu RT, Merrill JE, Vinters HV, Chen IS. Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science 1987, 236:819-822. 10.1126/science.3646751, 3646751.
42. Hall TA. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95 = 98 NT. Nucleic Acids Symp Ser 1999, 41:95-98.
43. Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 1988, 85:2444-2448. 10.1073/pnas.85.8.2444, 280013, 3162770.
44. Reuter JS, Mathews DH. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinforma 2010, 11:129.
45. Landis H, Simon-Jodicke A, Kloti A, Di Paolo C, Schnorr JJ, Schneider-Schaulies S, Hefti HP, Pavlovic J. Human MxA protein confers resistance to Semliki Forest virus and inhibits the amplification of a Semliki Forest virus-based replicon in the absence of viral structural proteins. J Virol 1998, 72:1516-1522. 124633, 9445055.
46. Kinkaid RP, Burke JM, Sullivan CS. RNA virus microRNA that mimics a B-cell oncomiR. Proc Natl Acad Sci USA 2012, 109:3077-3082. 10.1073/pnas.1116107109, 22308400.
47. Klase Z, Houzet L, Jeang KT. Replication competent HIV-1 viruses that express intragenomic microRNA reveal discrete RNA-interference mechanisms that affect viral replication. Cell Biosci 2011, 1:38. 10.1186/2045-3701-1-38, 3256098, 22112720.