Evidence for a crucial role of a host non-coding RNA in influenza a virus replication

RNA Biology

Volumn 11, Issue 1, 2014, Pages 66-75

  Winterling, Carla ^a   Koch, Manuel ^a   Koeppel, Max ^a   Garcia Alcalde, Fernando ^a   Karlas, Alexander ^a   Meyer, Thomas F ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

Host factor; IAV; LincRNA; Non protein coding genome; VIN

Indexed keywords

BETA INTERFERON; LONG UNTRANSLATED RNA; UNTRANSLATED RNA; VIRUS PROTEIN;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; FRACTIONATION; GENE EXPRESSION; HOST CELL; HUMAN; HUMAN CELL; HUMAN GENOME; INFLUENZA A; INFLUENZA A (H1N1); INFLUENZA VIRUS A; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H7N7; INFLUENZA VIRUS B; LUNG ALVEOLUS EPITHELIUM; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; VESICULAR STOMATITIS VIRUS; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS STRAIN;

HOST FACTOR; IAV; LINCRNA; NON-PROTEIN CODING GENOME; VIN;

ANIMALS; CELL LINE; CELL NUCLEUS; DOGS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INFLUENZA A VIRUS; KIDNEY; LUNG; MADIN DARBY CANINE KIDNEY CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, LONG NONCODING; RNA, SMALL INTERFERING; VESICULAR STOMATITIS INDIANA VIRUS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84894501374     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.27504     Document Type: Article

References (45)

1. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. Landscape of transcription in human cells. Nature 2012; 489:101-8; PMID:22955620; http://dx.doi.org/10.1038/ nature11233
2. Amaral PP, Dinger ME, Mercer TR, Mattick JS. The eukaryotic genome as an RNA machine. Science 2008; 319:1787-9; PMID:18369136; http://dx.doi.org/10.1126/ science.1155472
3. Mattick JS. RNA regulation: a new genetics? Nat Rev Genet 2004; 5:316-23; PMID:15131654; http://dx.doi.org/10.1038/nrg1321
4. Carthew RW, Sontheimer EJ. Origins and Mechanisms of miRNAs and siRNAs. Cell 2009; 136:642-55; PMID:19239886; http://dx.doi.org/10.1016/j.cell.2009.01. 035
5. Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS. Non-coding RNAs: regulators of disease. J Pathol 2010; 220:126-39; PMID:19882673; http://dx.doi.org/10.1002/path.2638
6. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 2012; 22:1775-89; PMID:22955988; http://dx.doi.org/10.1101/gr.132159. 111
7. Ørom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 2010; 143:46-58; PMID:20887892; http://dx.doi.org/10.1016/j.cell.2010.09.001
8. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007; 129:1311-23; PMID:17604720; http://dx.doi.org/10.1016/j.cell.2007.05.022
9. Lee JT. Lessons from X-chromosome inactivation: long ncRNA as guides and tethers to the epigenome. Genes Dev 2009; 23:1831-42; PMID:19684108; http://dx.doi.org/10.1101/gad.1811209
10. Peng X, Gralinski L, Armour CD, Ferris MT, Thomas MJ, Proll S, Bradel-Tretheway BG, Korth MJ, Castle JC, Biery MC, et al. Unique signatures of long noncoding RNA expression in response to virus infection and altered innate immune signaling. MBio 2010; 1:e00206-10; PMID:20978541; http://dx.doi.org/10. 1128/mBio.00206-10
11. Medina RA, García-Sastre A. Influenza A viruses: new research developments. Nat Rev Microbiol 2011; 9:590-603; PMID:21747392; http://dx.doi.org/10.1038/nrmicro2613
12. Karlas A, Machuy N, Shin Y, Pleissner KP, Artarini A, Heuer D, Becker D, Khalil H, Ogilvie LA, Hess S, et al. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 2010; 463:818-22; PMID:20081832; http://dx.doi.org/10.1038/nature08760
13. Watanabe T, Watanabe S, Kawaoka Y. Cellular networks involved in the influenza virus life cycle. Cell Host Microbe 2010; 7:427-39; PMID:20542247; http://dx.doi.org/10.1016/j.chom.2010.05.008
14. Li Y, Chan EY, Li J, Ni C, Peng X, Rosenzweig E, Tumpey TM, Katze MG. MicroRNA expression and virulence in pandemic influenza virus-infected mice. J Virol 2010; 84:3023-32; PMID:20071585; http://dx.doi.org/10.1128/JVI.02203-09
15. Meliopoulos VA, Andersen LE, Brooks P, Yan X, Bakre A, Coleman JK, Tompkins SM, Tripp RA. MicroRNA regulation of human protease genes essential for influenza virus replication. PLoS One 2012; 7:e37169; PMID:22606348; http://dx.doi.org/10.1371/journal.pone.0037169
16. Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet 2009; 10:155-9; PMID:19188922; http://dx.doi.org/10. 1038/nrg2521
17. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell 2011; 43:904-14; PMID:21925379; http://dx.doi.org/10.1016/j.molcel.2011.08.018
18. Dinger ME, Pang KC, Mercer TR, Mattick JS. Differentiating protein-coding and noncoding RNA: challenges and ambiguities. PLoS Comput Biol 2008; 4:e1000176; PMID:19043537; http://dx.doi.org/10.1371/journal.pcbi.1000176
19. Washietl S, Will S, Hendrix DA, Goff LA, Rinn JL, Berger B, Kellis M. Computational analysis of noncoding RNAs. Wiley Interdiscip Rev RNA 2012; 3:759-78; PMID:22991327; http://dx.doi.org/10.1002/wrna.1134
20. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. The human genome browser at UCSC. Genome Res 2002; 12:996-1006; PMID:12045153
21. Volders PJ, Helsens K, Wang X, Menten B, Martens L, Gevaert K, Vandesompele J, Mestdagh P. LNCipedia: a database for annotated human lncRNA transcript sequences and structures. Nucleic Acids Res 2013; 41:D246-51; PMID:23042674; http://dx.doi.org/10.1093/nar/gks915
22. Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G. CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 2007; 35:W345-9; PMID:17631615; http://dx.doi.org/10.1093/nar/gkm391
23. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 2011; 25:1915-27; PMID:21890647; http://dx.doi.org/10.1101/gad.17446611
24. Bovolenta M, Erriquez D, Valli E, Brioschi S, Scotton C, Neri M, Falzarano MS, Gherardi S, Fabris M, Rimessi P, et al. The DMD locus harbours multiple long non-coding RNAs which orchestrate and control transcription of muscle dystrophin mRNA isoforms. PLoS One 2012; 7:e45328; PMID:23028937; http://dx.doi.org/10.1371/journal.pone.0045328
25. Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet 2006; 15:R17-29; PMID:16651366; http://dx.doi.org/10.1093/hmg/ddl046
26. Washietl S, Hofacker IL, Lukasser M, Hüttenhofer A, Stadler PF. Mapping of conserved RNA secondary structures predicts thousands of functional non-coding RNAs in the human genome. Nat Biotechnol 2005; 23:1383-90; PMID:16273071; http://dx.doi.org/10.1038/nbt1144
27. Hofacker IL. Vienna RNA secondary structure server. Nucleic Acids Res 2003; 31:3429-31; PMID:12824340; http://dx.doi.org/10.1093/nar/gkg599
28. Mattick JS. The genetic signatures of noncoding RNAs. PLoS Genet 2009; 5:e1000459; PMID:19390609; http://dx.doi.org/10.1371/journal.pgen.1000459
29. Hao L, Sakurai A, Watanabe T, Sorensen E, Nidom CA, Newton MA, Ahlquist P, Kawaoka Y. Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 2008; 454:890-3; PMID:18615016; http://dx.doi.org/10.1038/nature07151
30. Ma YJ, Yang J, Fan XL, Zhao HB, Hu W, Li ZP, Yu GC, Ding XR, Wang JZ, Bo XC, et al. Cellular microRNA let-7c inhibits M1 protein expression of the H1N1 influenza A virus in infected human lung epithelial cells. J Cell Mol Med 2012; 16:2539-46; PMID:22452878; http://dx.doi.org/10.1111/j.1582-4934.2012.01572.x
31. Song L, Liu H, Gao S, Jiang W, Huang W. Cellular microRNAs inhibit replication of the H1N1 influenza A virus in infected cells. J Virol 2010; 84:8849-60; PMID:20554777; http://dx.doi.org/10.1128/JVI.00456-10
32. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, Ryan BJ, Weyer JL, van der Weyden L, Fikrig E, et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009; 139:1243-54; PMID:20064371; http://dx.doi.org/10.1016/j.cell.2009.12.017
33. König R, Stertz S, Zhou Y, Inoue A, Hoffmann HH, Bhattacharyya S, Alamares JG, Tscherne DM, Ortigoza MB, Liang Y, et al. Human host factors required for influenza virus replication. Nature 2010; 463:813-7; PMID:20027183; http://dx.doi.org/10.1038/nature08699
34. Ravasi T, Suzuki H, Pang KC, Katayama S, Furuno M, Okunishi R, Fukuda S, Ru K, Frith MC, Gongora MM, et al. Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. Genome Res 2006; 16:11-9; PMID:16344565; http://dx.doi.org/10.1101/gr.4200206
35. Saha S, Murthy S, Rangarajan PN. Identification and characterization of a virus-inducible non-coding RNA in mouse brain. J Gen Virol 2006; 87:1991-5; PMID:16760401; http://dx.doi.org/10.1099/vir.0.81768-0
36. Ehrhardt C, Wolff T, Ludwig S. Activation of phosphatidylinositol 3-kinase signaling by the nonstructural NS1 protein is not conserved among type A and B influenza viruses. J Virol 2007; 81:12097-100; PMID:17715214; http://dx.doi.org/10.1128/JVI.01216-07
37. Jagger BW, Wise HM, Kash JC, Walters KA, Wills NM, Xiao YL, Dunfee RL, Schwartzman LM, Ozinsky A, Bell GL, et al. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 2012; 337:199-204; PMID:22745253; http://dx.doi.org/10.1126/science.1222213
38. Chen LL, Carmichael GG. Decoding the function of nuclear long non-coding RNAs. Curr Opin Cell Biol 2010; 22:357-64; PMID:20356723; http://dx.doi.org/10. 1016/j.ceb.2010.03.003
39. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 2009; 106:11667-72; PMID:19571010; http://dx.doi.org/10.1073/pnas.0904715106
40. Clemson CM, Hutchinson JN, Sara SA, Ensminger AW, Fox AH, Chess A, Lawrence JB. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell 2009; 33:717-26; PMID:19217333; http://dx.doi.org/10.1016/j.molcel.2009.01.026
41. 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; 454:126-30; PMID:18509338; http://dx.doi.org/10.1038/nature06992
42. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011; 147:358-69; PMID:22000014; http://dx.doi.org/10.1016/j.cell.2011.09.028
43. Pang KC, Dinger ME, Mercer TR, Malquori L, Grimmond SM, Chen W, Mattick JS. Genomewide identification of long noncoding RNAs in CD8+ T cells. J Immunol 2009; 182:7738-48; PMID:19494298; http://dx.doi.org/10.4049/jimmunol.0900603
44. Collier SP, Collins PL, Williams CL, Boothby MR, Aune TM. Cutting edge: influence of Tmevpg1, a long intergenic noncoding RNA, on the expression of Ifng by Th1 cells. J Immunol 2012; 189:2084-8; PMID:22851706; http://dx.doi.org/10. 4049/jimmunol.1200774
45. Gomez JA, Wapinski OL, Yang YW, Bureau JF, Gopinath S, Monack DM, Chang HY, Brahic M, Kirkegaard K. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon- γ locus. Cell 2013; 152:743-54; PMID:23415224; http://dx.doi.org/10.1016/j.cell.2013.01.015