Annotation of long non-coding RNAs expressed in Collaborative Cross founder mice in response to respiratory virus infection reveals a new class of interferon-stimulated transcripts

RNA Biology

Volumn 11, Issue 7, 2014, Pages 875-890

  Josset, Laurence ^a,b   Tchitchek, Nicolas ^a,b   Gralinski, Lisa E ^b,c   Ferris, Martin T ^b,d   Eisfeld, Amie J ^e   Green, Richard R ^a,b   Thomas, Matthew J ^a,b   Tisoncik Go, Jennifer ^a,b   Schroth, Gary P ^f   Kawaoka, Yoshihiro ^e   De Villena, Fernando Pardo Manuel ^d   Baric, Ralph S ^b,c   Heise, Mark T ^b,d   Peng, Xinxia ^a,b   Katze, Michael G ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b Pacific Northwest Regional Cntr of Excellence for Biodefense and Emerging Infectious Diseases Res   (United States)

^c The University of North Carolina at Chapel Hill   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

^f ILLUMINA INC   (United States)

Author keywords

Collaborative cross; Influenza virus; Interferon; Long non coding rna; Rna seq; Sars cov

Indexed keywords

ALPHA INTERFERON; LONG UNTRANSLATED RNA; ANTIVIRUS AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC CODE; GENETIC TRANSCRIPTION; HOMEOSTASIS; IMMUNE RESPONSE; INFLUENZA A; INFLUENZA VIRUS A; MOUSE; MOUSE STRAIN; NONHUMAN; RNA SEQUENCE; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRAL RESPIRATORY TRACT INFECTION; VIRUS PATHOGENESIS; ANIMAL; C57BL MOUSE; CELL LINE; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LUNG; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; RNA VIRUS INFECTIONS; SEQUENCE ANALYSIS; VIROLOGY;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; INFLUENZA A VIRUS; INTERFERON-ALPHA; LUNG; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE ANNOTATION; RNA VIRUS INFECTIONS; RNA, LONG NONCODING; SARS VIRUS; SEQUENCE ANALYSIS, RNA;

EID: 84906253612     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.29442     Document Type: Article

References (52)

1. Ng WF, To KF, Lam WW, Ng TK, Lee KC. The comparative pathology of severe acute respiratory syndrome and avian influenza A subtype H5N1 - a review. Hum Pathol 2006; 37:381-90; PMID:16564911; http://dx.doi.org/10.1016/j.humpath.2006.01.015
2. Josset L, Tisoncik-Go J, Katze MG. Moving H5N1 studies into the era of systems biology. Virus Res 2013; 178:151-67; PMID:23499671; http://dx.doi.org/10.1016/j.virusres.2013.02.011
3. Josset L, Belser JA, Pantin-Jackwood MJ, Chang JH, Chang ST, Belisle SE, Tumpey TM, Katze MG. Implication of inflammatory macrophages, nuclear receptors, and interferon regulatory factors in increased virulence of pandemic 2009 H1N1 influenza A virus after host adaptation. J Virol 2012; 86:7192-206; PMID:22532695; http://dx.doi.org/10.1128/JVI.00563-12
4. Tchitchek N, Eisfeld AJ, Tisoncik-Go J, Josset L, Gralinski LE, Bécavin C, Tilton SC, Webb-Robertson BJ, Ferris MT, Totura AL, et al. Specific mutations in H5N1 mainly impact the magnitude and velocity of the host response in mice. BMC Syst Biol 2013; 7:69; PMID:23895213; http://dx.doi.org/10.1186/1752-0509-7-69
5. Brandes M, Klauschen F, Kuchen S, Germain RN. A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 2013; 154:197-212; PMID:23827683; http://dx.doi.org/10.1016/j.cell.2013.06.013
6. Moran VA, Perera RJ, Khalil AM. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res 2012; 40:6391-400; PMID:22492512; http://dx.doi.org/10.1093/nar/gks296
7. Jeon Y, Lee JT. YY1 tethers Xist RNA to the inactive X nucleation center. Cell 2011; 146:119-33; PMID:21729784; http://dx.doi.org/10.1016/j.cell.2011.06.026
8. Nagano T, Mitchell JA, Sanz LA, Pauler FM, Ferguson-Smith AC, Feil R, Fraser P. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 2008; 322:1717-20; PMID:18988810; http://dx.doi.org/10.1126/science.1163802
9. Keniry A, Oxley D, Monnier P, Kyba M, Dandolo L, Smits G, Reik W. The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nat Cell Biol 2012; 14:659-65; PMID:22684254; http://dx.doi.org/10.1038/ncb2521
10. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA, et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 2010; 39:925-38; PMID:20797886; http://dx.doi.org/10.1016/j.molcel.2010.08.011
11. Yin Z, Guan D, Fan Q, Su J, Zheng W, Ma W, Ke C. lncRNA expression signatures in response to enterovirus 71 infection. Biochem Biophys Res Commun 2013; 430:629-33; PMID:23220233; http://dx.doi.org/10.1016/j.bbrc.2012.11.101
12. 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
13. 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
14. 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
15. 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
16. 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
17. Zhang Q, Chen CY, Yedavalli VS, Jeang KT. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio 2013; 4:e00596-12; PMID:23362321; http://dx.doi.org/10.1128/mBio.00596-12
18. Wan Y, Kertesz M, Spitale RC, Segal E, Chang HY. Understanding the transcriptome through RNA structure. Nat Rev Genet 2011; 12:641-55; PMID:21850044; http://dx.doi.org/10.1038/nrg3049
19. Wu LF, Hughes TR, Davierwala AP, Robinson MD, Stoughton R, Altschuler SJ. Large-scale prediction of Saccharomyces cerevisiae gene function using overlapping transcriptional clusters. Nat Genet 2002; 31:255-65; PMID:12089522; http://dx.doi.org/10.1038/ng906
20. Liao Q, Liu C, Yuan X, Kang S, Miao R, Xiao H, Zhao G, Luo H, Bu D, Zhao H, et al. Large-scale prediction of long non-coding RNA functions in a coding-non-coding gene co-expression network. Nucleic Acids Res 2011; 39:3864-78; PMID:21247874; http://dx.doi.org/10.1093/nar/gkq1348
21. Churchill GA, Airey DC, Allayee H, Angel JM, Attie AD, Beatty J, Beavis WD, Belknap JK, Bennett B, Berrettini W, et al.; Complex Trait Consortium. The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nat Genet 2004; 36:1133-7; PMID:15514660; http://dx.doi.org/10.1038/ng1104-1133
22. Ferris MT, Aylor DL, Bottomly D, Whitmore AC, Aicher LD, Bell TA, Bradel-Tretheway B, Bryan JT, Buus RJ, Gralinski LE, et al. Modeling host genetic regulation of influenza pathogenesis in the collaborative cross. PLoS Pathog 2013; 9:e1003196; PMID:23468633; http://dx.doi.org/10.1371/journal.ppat.1003196
23. Perrone LA, Plowden JK, García-Sastre A, Katz JM, Tumpey TM. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 2008; 4:e1000115; PMID:18670648; http://dx.doi.org/10.1371/journal.ppat.1000115
24. Rapicavoli NA, Qu K, Zhang J, Mikhail M, Laberge R-M, Chang HY. A mammalian pseudogene lncRNA at the interface of inflammation and antiinflammatory therapeutics. Elife 2013; 2:e00762; PMID:23898399; http://dx.doi.org/10.7554/eLife.00762
25. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009; 458:223-7; PMID:19182780; http://dx.doi.org/10.1038/nature07672
26. Gutschner T, Hämmerle M, Eissmann M, Hsu J, Kim Y, Hung G, Revenko A, Arun G, Stentrup M, Gross M, et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res 2013; 73:1180-9; PMID:23243023; http://dx.doi.org/10.1158/0008-5472.CAN-12-2850
27. Tripathi V, Shen Z, Chakraborty A, Giri S, Freier SM, Wu X, Zhang Y, Gorospe M, Prasanth SG, Lal A, et al. Long noncoding RNA MALAT1 controls cell cycle progression by regulating the expression of oncogenic transcription factor B-MYB. PLoS Genet 2013; 9:e1003368; PMID:23555285; http://dx.doi.org/10.1371/journal.pgen.1003368
28. Zhang Q, Chen C-Y, Yedavalli VSRK, Jeang K-T. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio 2013; 4:e00596-12; PMID:23362321; http://dx.doi.org/10.1128/mBio.00596-12
29. Wang Y, Davies KJA, Melendez JA, Crawford DR. Characterization of adapt33, a stress-inducible riboregulator. Gene Expr 2003; 11:85-94; PMID:12837039; http://dx.doi.org/10.3727/000000003108748982
30. Sheahan T, Whitmore A, Long K, Ferris M, Rockx B, Funkhouser W, Donaldson E, Gralinski L, Collier M, Heise M, et al. Successful vaccination strategies that protect aged mice from lethal challenge from influenza virus and heterologous severe acute respiratory syndrome coronavirus. J Virol 2011; 85:217-30; PMID:20980507; http://dx.doi.org/10.1128/JVI.01805-10
31. rd, Jeng S, Menachery VD, Proll S, Belisle SE, Matzke M, Webb-Robertson BJ, Luna ML, Shukla AK, et al. Mechanisms of severe acute respiratory syndrome coronavirus-induced acute lung injury. MBio 2013; 4:4; PMID:23919993; http://dx.doi.org/10.1128/mBio.00271-13
32. Bu D, Yu K, Sun S, Xie C, Skogerbø G, Miao R, Xiao H, Liao Q, Luo H, Zhao G, et al. NONCODE v3.0: integrative annotation of long noncoding RNAs. Nucleic Acids Res 2012; 40:D210-5; PMID:22135294; http://dx.doi.org/10.1093/nar/gkr1175
33. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, et al. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011; 477:295-300; PMID:21874018; http://dx.doi.org/10.1038/nature10398
34. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841-2; PMID:20110278; http://dx.doi.org/10.1093/bioinformatics/btq033
35. Bhagwat M, Young L, Robison RR. Using BLAT to find sequence similarity in closely related genomes. Curr Protoc Bioinformatics 2012; Chapter 10:Unit108.
36. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012; 7:562-78; PMID:22383036; http://dx.doi.org/10.1038/nprot.2012.016
37. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10:R25; PMID:19261174; http://dx.doi.org/10.1186/gb-2009-10-3-r25
38. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009; 25:1966-7; PMID:19497933; http://dx.doi.org/10.1093/bioinformatics/btp336
39. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010; 11:R106; PMID:20979621; http://dx.doi.org/10.1186/gb-2010-11-10-r106
40. Chang ST, Thomas MJ, Sova P, Green RR, Palermo RE, Katze MG. Next-generation sequencing of small RNAs from HIV-infected cells identifies phased microrna expression patterns and candidate novel microRNAs differentially expressed upon infection. MBio 2013; 4:e00549-12; PMID:23386435; http://dx.doi.org/10.1128/mBio.00549-12
41. Langfelder P, Horvath S. Fast R Functions for Robust Correlations and Hierarchical Clustering. J Stat Softw 2012; 46:46; PMID:23050260
42. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 2008; 9:559; PMID:19114008; http://dx.doi.org/10.1186/1471-2105-9-559
43. Mueller LA, Kugler KG, Graber A, Emmert-Streib F, Dehmer M. Structural measures for network biology using QuACN. BMC Bioinformatics 2011; 12:492; PMID:22195644; http://dx.doi.org/10.1186/1471-2105-12-492
44. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, et al. Ensembl 2013. Nucleic Acids Res 2013; 41:D48-55; PMID:23203987; http://dx.doi.org/10.1093/nar/gks1236
45. Croft D, Mundo AF, Haw R, Milacic M, Weiser J, Wu G, Caudy M, Garapati P, Gillespie M, Kamdar MR, et al. The Reactome pathway knowledgebase. Nucleic Acids Res 2014; 42:D472-7; PMID:24243840; http://dx.doi.org/10.1093/nar/gkt1102
46. Cilloniz C, Pantin-Jackwood MJ, Ni C, Carter VS, Korth MJ, Swayne DE, Tumpey TM, Katze MG. Molecular signatures associated with Mx1-mediated resistance to highly pathogenic influenza virus infection: mechanisms of survival. J Virol 2012; 86:2437-46; PMID:22190720; http://dx.doi.org/10.1128/JVI.06156-11
47. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, Valen E, Yusuf D, Lenhard B, Wasserman WW, Sandelin A. JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 2010; 38:D105-10; PMID:19906716; http://dx.doi.org/10.1093/nar/gkp950
48. Robasky K, Bulyk ML. UniPROBE, update 2011: expanded content and search tools in the online database of protein-binding microarray data on protein-DNA interactions. Nucleic Acids Res 2011; 39:D124-8; PMID:21037262; http://dx.doi.org/10.1093/nar/gkq992
49. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics 2011; 27:1017-8; PMID:21330290; http://dx.doi.org/10.1093/bioinformatics/btr064
50. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009; 37:W202-8; PMID:19458158; http://dx.doi.org/10.1093/nar/gkp335
51. Väremo L, Nielsen J, Nookaew I. Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods. Nucleic Acids Res 2013; 41:4378-91; PMID:23444143; http://dx.doi.org/10.1093/nar/gkt111
52. Finn RD, Stalker JW, Jackson DK, Kulesha E, Clements J, Pettett R. ProServer: a simple, extensible Perl DAS server. Bioinformatics 2007; 23:1568-70; PMID:17237073; http://dx.doi.org/10.1093/bioinformatics/btl650