Deep sequencing of the mouse lung transcriptome reveals distinct long non-coding RNAs expression associated with the high virulence of H5N1 avian influenza virus in mice

References

• Szretter KJ, Gangappa S, Lu X, et al. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J Virol. 2007;81:2736–2744.
   PubMed Web of Science ®Google Scholar
• Perrone LA, Plowden JK, Garcia-Sastre A, et al. 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.
   PubMed Web of Science ®Google Scholar
• Cameron CM, Cameron MJ, Bermejo-Martin JF, et al. Gene expression analysis of host innate immune responses during Lethal H5N1 infection in ferrets. J Virol. 2008;82:11308–11317.
   PubMed Web of Science ®Google Scholar
• Baskin CR, Bielefeldt-Ohmann H, Tumpey TM, et al. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc Natl Acad Sci U S A. 2009;106:3455–3460.
   PubMed Web of Science ®Google Scholar
• Costa FF. Non-coding RNAs: meet thy masters. Bioessays. 2010;32:599–608.
   PubMed Web of Science ®Google Scholar
• Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012;81:145–166.
   PubMed Web of Science ®Google Scholar
• Yoon JH, Abdelmohsen K, Gorospe M. Posttranscriptional gene regulation by long noncoding RNA. J Mol Biol. 2013;425:3723–3730.
   PubMed Web of Science ®Google Scholar
• Magistri M, Faghihi MA, St Laurent G 3rd, et al. Regulation of chromatin structure by long noncoding RNAs: focus on natural antisense transcripts. Trends Genet. 2012;28:389–396.
   PubMed Web of Science ®Google Scholar
• Tsai MC, Manor O, Wan Y, et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science. 2010;329:689–693.
   PubMed Web of Science ®Google Scholar
• Cesana M, Cacchiarelli D, Legnini I, et al. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell. 2011;147:358–369.
   PubMed Web of Science ®Google Scholar
• Ouyang J, Zhu X, Chen Y, et al. NRAV, a long noncoding RNA, modulates antiviral responses through suppression of interferon-stimulated gene transcription. Cell Host Microbe. 2014;16:616–626.
   PubMed Web of Science ®Google Scholar
• Huarte M, Guttman M, Feldser D, et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell. 2010;142:409–419.
   PubMed Web of Science ®Google Scholar
• Carpenter S, Aiello D, Atianand MK, et al. A long noncoding RNA mediates both activation and repression of immune response genes. Science. 2013;341:789–792.
   PubMed Web of Science ®Google Scholar
• Tripathi V, Ellis JD, Shen Z, et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell. 2010;39:925–938.
   PubMed Web of Science ®Google Scholar
• Yin QF, Yang L, Zhang Y, et al. Long noncoding RNAs with snoRNA ends. Mol Cell. 2012;48:219–230.
   PubMed Web of Science ®Google Scholar
• Jalali S, Jayaraj GG, Scaria V. Integrative transcriptome analysis suggest processing of a subset of long non-coding RNAs to small RNAs. Biol Direct. 2012;7:25.
   PubMed Web of Science ®Google Scholar
• Willingham AT, Orth AP, Batalov S, et al. A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science. 2005;309:1570–1573.
   PubMed Web of Science ®Google Scholar
• Rapicavoli NA, Qu K, Zhang J, et al. A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. Elife 2013; 2:e00762.
   PubMed Web of Science ®Google Scholar
• Wright PW, Huehn A, Cichocki F, et al. Identification of a KIR antisense lncRNA expressed by progenitor cells. Genes Immun. 2013;14:427–433.
   PubMed Web of Science ®Google Scholar
• Carpenter S. Long noncoding RNA: novel links between gene expression and innate immunity. Virus Res. 2015.
   PubMed Web of Science ®Google Scholar
• Aune TM, Spurlock CF 3rd. Long non-coding RNAs in innate and adaptive immunity. Virus Res. 2015.
   PubMed Web of Science ®Google Scholar
• Heward JA, Lindsay MA. Long non-coding RNAs in the regulation of the immune response. Trends Immunol. 2014;35:408–419.
   PubMed Web of Science ®Google Scholar
• Fitzgerald KA, Caffrey DR. Long noncoding RNAs in innate and adaptive immunity. Curr Opin Immunol. 2014;26:140–146.
   PubMed Web of Science ®Google Scholar
• Collier SP, Collins PL, Williams CL, et al. Cutting edge: influence of Tmevpg1, a long intergenic noncoding RNA, on the expression of Ifng by Th1 cells. J Immunol. 2012;189:2084–2088.
   PubMed Web of Science ®Google Scholar
• Broadbent KM, Park D, Wolf AR, et al. A global transcriptional analysis of Plasmodium falciparum malaria reveals a novel family of telomere-associated lncRNAs. Genome Biol. 2011;12:R56.
   PubMed Web of Science ®Google Scholar
• Scaria V, Pasha A. Long Non-Coding RNAs in Infection Biology. Front Genet. 2012;3:308.
   PubMedGoogle Scholar
• Fortes P, Morris KV. Long noncoding RNAs in viral infections. Virus Res. 2015.
   Web of Science ®Google Scholar
• Rossetto CC, Pari GS. Kaposi’s sarcoma-associated herpesvirus noncoding polyadenylated nuclear RNA interacts with virus- and host cell-encoded proteins and suppresses expression of genes involved in immune modulation. J Virol. 2011;85:13290–13297.
   PubMed Web of Science ®Google Scholar
• Cazalla D, Yario T, Steitz JA. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science. 2010;328:1563–1566.
   PubMed Web of Science ®Google Scholar
• Imamura K, Imamachi N, Akizuki G, et al. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol Cell. 2014;53:393–406.
   PubMed Web of Science ®Google Scholar
• Barriocanal M, Carnero E, Segura V, et al. Long non-coding RNA BST2/BISPR is induced by IFN and regulates the expression of the antiviral factor tetherin. Front Immunol. 2014;5:655.
   PubMed Web of Science ®Google Scholar
• Kambara H, Gunawardane L, Zebrowski E, et al. Regulation of interferon-stimulated gene BST2 by a lncRNA transcribed from a shared bidirectional promoter. Front Immunol. 2014;5:676.
   PubMed Web of Science ®Google Scholar
• Winterling C, Koch M, Koeppel M, et al. Evidence for a crucial role of a host non-coding RNA in influenza A virus replication. RNA Biol. 2014;11:66–75.
   PubMed Web of Science ®Google Scholar
• Hu J, Zhao K, Liu X, et al. Two highly pathogenic avian influenza H5N1 viruses of clade 2.3.2.1 with similar genetic background but with different pathogenicity in mice and ducks. Transbound Emerg Dis. 2012.
   Web of Science ®Google Scholar
• Hu J, Hu Z, Song Q, et al. The PA-gene-mediated lethal dissemination and excessive innate immune response contribute to the high virulence of H5N1 avian influenza virus in mice. J Virol. 2013;87:2660–2672.
   PubMed Web of Science ®Google Scholar
• Hu J, Gao Z, Wang X, et al. iTRAQ-based quantitative proteomics reveals important host factors involved in the high pathogenicity of the H5N1 avian influenza virus in mice. Med Microbiol Immunol. 2017;206:125–147.
   PubMed Web of Science ®Google Scholar
• Hu J, Zhao K, Liu X, et al. Two highly pathogenic avian influenza H5N1 viruses of clade 2.3.2.1 with similar genetic background but with different pathogenicity in mice and ducks. Transbound Emerg Dis. 2013;60:127–139.
   PubMed Web of Science ®Google Scholar
• Li J, Gu M, Liu D, et al. Phylogenetic and biological characterization of three K1203 (H5N8)-like avian influenza A virus reassortants in China in 2014. Arch Virol. 2016;161:289–302.
   PubMed Web of Science ®Google Scholar
• Cui Z, Hu J, He L, et al. Differential immune response of mallard duck peripheral blood mononuclear cells to two highly pathogenic avian influenza H5N1 viruses with distinct pathogenicity in mallard ducks. Arch Virol. 2014;159:339–343.
   PubMed Web of Science ®Google Scholar
• Kriegel AJ, Liu Y, Liu PY, et al. Characteristics of microRNAs enriched in specific cell types and primary tissue types in solid organs. Physiol Genomics. 2013;45:1144–1156.
   PubMed Web of Science ®Google Scholar
• Li R, Yu C, Li Y, et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics. 2009;25:1966–1967.
   PubMed Web of Science ®Google Scholar
• Trapnell C, Williams BA, Pertea G, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511–U174.
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat. 2001;29:1165–1188.
   Web of Science ®Google Scholar
• Sun L, Zhang ZH, Bailey TL, et al. Prediction of novel long non-coding RNAs based on RNA-Seq data of mouse Klf1 knockout study. In: Bmc Bioinformatics. 2012. p. 13.
   Google Scholar
• Tafer H, Hofacker IL. RNAplex: a fast tool for RNA-RNA interaction search. Bioinformatics. 2008;24:2657–2663.
   PubMed Web of Science ®Google Scholar
• Liao Q, Liu CN, Yuan XY, et al. Large-scale prediction of long non-coding RNA functions in a coding-non-coding gene co-expression network. Nucleic Acids Res. 2011;39:3864–3878.
   PubMed Web of Science ®Google Scholar
• Wingender E, Chen X, Hehl R, et al. TRANSFAC: an integrated system for gene expression regulation. Nucleic Acids Res. 2000;28:316–319.
   PubMed Web of Science ®Google Scholar
• Washietl S, Hofacker IL, Lukasser M, et al. Mapping of conserved RNA secondary structures predicts thousands of functional noncoding RNAs in the human genome. Nat Biotechnol. 2005;23:1383–1390.
   PubMed Web of Science ®Google Scholar
• Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature. 2012;489:101–108.
   PubMed Web of Science ®Google Scholar
• Oldstone MB. Lessons learned and concepts formed from study of the pathogenesis of the two negative-strand viruses lymphocytic choriomeningitis and influenza. Proc Natl Acad Sci U S A. 2013;110:4180–4183.
   PubMed Web of Science ®Google Scholar
• Opal SM, Fedson DS. The dysfunctional host response to influenza A H7N9: a potential treatment option? Crit Care. 2014;18:135.
   PubMed Web of Science ®Google Scholar
• Thomas M, Mani RS, Philip M, et al. Proinflammatory chemokines are major mediators of exuberant immune response associated with Influenza A (H1N1) pdm09 virus infection. J Med Virol. 2017.
   PubMed Web of Science ®Google Scholar
• Wu H, Zhao M, Yoshimura A, et al. Critical link between epigenetics and transcription factors in the induction of autoimmunity: a comprehensive review. Clin Rev Allergy Immunol. 2016;50:333–344.
   PubMed Web of Science ®Google Scholar
• Chen R, Yang Z, Zhou Q. Phosphorylated positive transcription elongation factor b (P-TEFb) is tagged for inhibition through association with 7SK snRNA. J Biol Chem. 2004;279:4153–4160.
   PubMed Web of Science ®Google Scholar
• Sharma S, Findlay GM, Bandukwala HS, et al. Dephosphorylation of the nuclear factor of activated T cells (NFAT) transcription factor is regulated by an RNA-protein scaffold complex. Proc Natl Acad Sci U S A. 2011;108:11381–11386.
   PubMed Web of Science ®Google Scholar
• Tamura T, Yanai H, Savitsky D, et al. The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol. 2008;26:535–584.
   PubMed Web of Science ®Google Scholar
• Ikushima H, Negishi H, Taniguchi T. The IRF family transcription factors at the interface of innate and adaptive immune responses. Cold Spring Harb Symp Quant Biol. 2013;78:105–116.
   PubMedGoogle Scholar
• Savitsky D, Tamura T, Yanai H, et al. Regulation of immunity and oncogenesis by the IRF transcription factor family. Cancer Immunol Immunother. 2010;59:489–510.
   PubMed Web of Science ®Google Scholar
• Chung MC, Kawamoto S. IRF-2 is involved in up-regulation of nonmuscle myosin heavy chain II-A gene expression during phorbol ester-induced promyelocytic HL-60 differentiation. J Biol Chem. 2004;279:56042–56052.
   PubMed Web of Science ®Google Scholar
• Manzella L, Giuffrida MA, Pilastro MR, et al. Possible role of the transcription factor interferon regulatory factor 1 (IRF-1) in the regulation of ornithine decarboxylase (ODC) gene expression during IFN gamma macrophage activation. FEBS Lett. 1994;348:177–180.
   PubMed Web of Science ®Google Scholar
• Liang J, Yan R, Chen G, et al. Downregulation of ZBTB24 hampers the G0/1- to S-phase cell-cycle transition via upregulating the expression of IRF-4 in human B cells. Genes Immun. 2016;17:276–282.
   PubMed Web of Science ®Google Scholar
• Armstrong MJ, Stang MT, Liu Y, et al. Interferon Regulatory Factor 1 (IRF-1) induces p21(WAF1/CIP1) dependent cell cycle arrest and p21(WAF1/CIP1) independent modulation of survivin in cancer cells. Cancer Lett. 2012;319:56–65.
   PubMed Web of Science ®Google Scholar
• Kano A, Haruyama T, Akaike T, et al. IRF-1 is an essential mediator in IFN-gamma-induced cell cycle arrest and apoptosis of primary cultured hepatocytes. Biochem Biophys Res Commun. 1999;257:672–677.
   PubMed Web of Science ®Google Scholar
• Zhao J, Chen C, Xiao JR, et al. An up-regulation of IRF-1 after a spinal cord injury: implications for neuronal apoptosis. J Mol Neurosci. 2015;57:595–604.
   PubMed Web of Science ®Google Scholar
• Zhang C, Guo ZM. Multiple functions of Maf in the regulation of cellular development and differentiation. Diabetes Metab Res Rev. 2015;31:773–778.
   PubMed Web of Science ®Google Scholar
• Ranzani V, Rossetti G, Panzeri I, et al. The long intergenic noncoding RNA landscape of human lymphocytes highlights the regulation of T cell differentiation by linc-MAF-4. Nat Immunol. 2015;16:318–325.
   PubMed Web of Science ®Google Scholar
• Lopez-Pajares V, Qu K, Zhang J, et al. A LncRNA-MAF:MAFB transcription factor network regulates epidermal differentiation. Dev Cell. 2015;32:693–706.
   PubMed Web of Science ®Google Scholar
• Brundage ME, Tandon P, Eaves DW, et al. MAF mediates crosstalk between Ras-MAPK and mTOR signaling in NF1. Oncogene. 2014;33:5626–5636.
   PubMed Web of Science ®Google Scholar
• James SJ, Jiao H, Teh HY, et al. MAPK phosphatase 5 expression induced by influenza and other RNA virus infection negatively regulates IRF3 activation and type I interferon response. Cell Rep. 2015.
   Web of Science ®Google Scholar
• Hui KP, Lee SM, Cheung CY, et al. Induction of proinflammatory cytokines in primary human macrophages by influenza A virus (H5N1) is selectively regulated by IFN regulatory factor 3 and p38 MAPK. J Immunol. 2009;182:1088–1098.
   PubMed Web of Science ®Google Scholar
• Lee DC, Cheung CY, Law AH, et al. p38 mitogen-activated protein kinase-dependent hyperinduction of tumor necrosis factor alpha expression in response to avian influenza virus H5N1. J Virol. 2005;79:10147–10154.
   PubMed Web of Science ®Google Scholar
• Kujime K, Hashimoto S, Gon Y, et al. p38 mitogen-activated protein kinase and c-jun-NH2-terminal kinase regulate RANTES production by influenza virus-infected human bronchial epithelial cells. J Immunol. 2000;164:3222–3228.
   PubMed Web of Science ®Google Scholar
• Ludwig S, Ehrhardt C, Neumeier ER, et al. Influenza virus-induced AP-1-dependent gene expression requires activation of the JNK signaling pathway. J Biol Chem 2001; 276:10990–10998.
   Web of Science ®Google Scholar
• Pleschka S, Wolff T, Ehrhardt C, et al. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat Cell Biol. 2001;3:301–305.
   PubMed Web of Science ®Google Scholar
• Ehrhardt C, Marjuki H, Wolff T, et al. Bivalent role of the phosphatidylinositol-3-kinase (PI3K) during influenza virus infection and host cell defence. Cell Microbiol. 2006;8:1336–1348.
   PubMed Web of Science ®Google Scholar
• Ehrhardt C, Wolff T, Pleschka S, et al. Influenza A virus NS1 protein activates the PI3K/Akt pathway to mediate antiapoptotic signaling responses. J Virol. 2007;81:3058–3067.
   PubMed Web of Science ®Google Scholar
• Hale BG, Jackson D, Chen YH, et al. Influenza A virus NS1 protein binds p85 beta and activates phosphatidylinositol-3-kinase signaling. P Natl Acad Sci USA 2006; 103:14194–14199.
   PubMed Web of Science ®Google Scholar
• Shin YK, Li Y, Liu Q, et al. SH3 binding motif 1 in influenza a virus NS1 protein is essential for PI3K/Akt signaling pathway activation. J Virol. 2007;81:12730–12739.
   PubMed Web of Science ®Google Scholar
• Shin YK, Liu Q, Tikoo SK, et al. Effect of the phosphatidylinositol 3-kinase/Akt pathway on influenza A virus propagation. J Gen Virol. 2007;88:942–950.
   PubMed Web of Science ®Google Scholar
• Shin YK, Liu Q, Tikoo SK, et al. Influenza A virus NS1 protein activates the phosphatidylinositol 3-kinase (PI3K)/Akt pathway by direct interaction with the p85 subunit of PI3K. J Gen Virol. 2007;88:13–18.
   PubMed Web of Science ®Google Scholar
• Tong Z, Jiang B, Zhang L, et al. HSF-1 is involved in attenuating the release of inflammatory cytokines induced by LPS through regulating autophagy. Shock. 2014;41:449–453.
   PubMed Web of Science ®Google Scholar
• Duarte FM, Fuda NJ, Mahat DB, Core LJ, Guertin MJ, Lis JT. Transcription factors GAF and HSF act at distinct regulatory steps to modulate stress-induced gene activation. Genes Dev. 2016;30:1731–1746.
   PubMed Web of Science ®Google Scholar
• Kinet MJ, Malin JA, Abraham MC, et al. HSF-1 activates the ubiquitin proteasome system to promote non-apoptotic developmental cell death in C elegans. In: Elife. 2016. p. 5.
   Google Scholar
• Lentjes MH, Niessen HE, Akiyama Y, et al. The emerging role of GATA transcription factors in development and disease. Expert Rev Mol Med 2016; 18:e3.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Li F, Xiao X, et al. Regulator of G protein signaling 4 is a novel target of GATA-6 transcription factor. Biochem Biophys Res Commun. 2017;483:923–929.
   PubMed Web of Science ®Google Scholar
• Chen Q, Zhang F, Wang Y, et al. The transcription factor c-Myc suppresses MiR-23b and MiR-27b transcription during fetal distress and increases the sensitivity of neurons to hypoxia-induced apoptosis. PLoS One 2015; 10:e0120217.
   PubMed Web of Science ®Google Scholar
• Zhu ZH, Yu YP, Shi YK, et al. CSR1 induces cell death through inactivation of CPSF3. Oncogene. 2009;28:41–51.
   PubMed Web of Science ®Google Scholar
• Palencia A, Bougdour A, Brenier-Pinchart MP, et al. Targeting Toxoplasma gondii CPSF3 as a new approach to control toxoplasmosis. EMBO Mol Med. 2017;9:385–394.
   PubMed Web of Science ®Google Scholar
• Raheja R, Gandhi R. FXR1: linking cellular quiescence, immune genes and cancer. Cell Cycle. 2016;15:2695–2696.
   PubMed Web of Science ®Google Scholar
• Qian J, Hassanein M, Hoeksema MD, et al. The RNA binding protein FXR1 is a new driver in the 3q26-29 amplicon and predicts poor prognosis in human cancers. P Natl Acad Sci USA 2015; 112:3469–3474.
   PubMed Web of Science ®Google Scholar
• Durfee T, Mancini MA, Jones D, et al. The amino-terminal region of the retinoblastoma gene product binds a novel nuclear matrix protein that co-localizes to centers for RNA processing. J Cell Biol. 1994;127:609–622.
   PubMed Web of Science ®Google Scholar
• Wan J, Zou S, Hu M, et al. Thoc1 inhibits cell growth via induction of cell cycle arrest and apoptosis in lung cancer cells. Mol Med Rep. 2014;9:2321–2327.
   PubMed Web of Science ®Google Scholar
• Chinnam M, Wang X, Zhang X, et al. Evaluating effects of hypomorphic Thoc1 alleles on embryonic development in Rb1 null mice. Mol Cell Biol. 2016;36:1621–1627.
   PubMed Web of Science ®Google Scholar
• Li Y, Wang X, Zhang X, et al. Human hHpr1/p84/Thoc1 regulates transcriptional elongation and physically links RNA polymerase II and RNA processing factors. Mol Cell Biol. 2005;25:4023–4033.
   PubMed Web of Science ®Google Scholar
• Katoh T, Hojo H, Suzuki T. Destabilization of microRNAs in human cells by 3ʹ deadenylation mediated by PARN and CUGBP1. Nucleic Acids Res. 2015;43:7521–7534.
   PubMed Web of Science ®Google Scholar
• Moon DH, Segal M, Boyraz B, et al. Poly(A)-specific ribonuclease (PARN) mediates 3ʹ-end maturation of the telomerase RNA component. Nat Genet. 2015;47:1482–1488.
   PubMed Web of Science ®Google Scholar
• Zhang LN, Yan YB. Depletion of poly(A)-specific ribonuclease (PARN) inhibits proliferation of human gastric cancer cells by blocking cell cycle progression. Biochim Biophys Acta. 2015;1853:522–534.
   PubMed Web of Science ®Google Scholar