Development of combinatorial RNAi transgenes targeting influenza virus

This research investigated the optimization of RNA interference against influenza A viruses. Results obtained in this study increase knowledge of the use of RNA interference in the context of creating antiviral transgenes capable of simultaneously targeting multiple viral genes and preventing the risk of viral escape.

[1]  Jennifer Taylor,et al.  Polycistronic RNA polymerase II expression vectors for RNA interference based on BIC/miR-155 , 2006, Nucleic acids research.

[2]  T. He,et al.  [Potent and specific inhibition of hepatitis B virus antigen expression by RNA interference]. , 2003, Zhonghua yi xue za zhi.

[3]  J. Rossi,et al.  Coupling of RNAi-mediated target downregulation with gene replacement. , 2003, Antisense & nucleic acid drug development.

[4]  K. Morris,et al.  The Efficacy of Generating Three Independent Anti-HIV-1 siRNAs from a Single U6 RNA Pol III-Expressed Long Hairpin RNA , 2008, PloS one.

[5]  U. Kutay,et al.  Nuclear Export of MicroRNA Precursors , 2004, Science.

[6]  Ola Snøve,et al.  A comparison of siRNA efficacy predictors. , 2004, Biochemical and biophysical research communications.

[7]  B. Ramratnam,et al.  Enhanced gene silencing of HIV-1 specific siRNA using microRNA designed hairpins. , 2004, Nucleic acids research.

[8]  Stuart A. Wilson,et al.  A direct comparison of strategies for combinatorial RNA interference , 2010, BMC Molecular Biology.

[9]  Michael T. McManus,et al.  Small Interfering RNA-Mediated Gene Silencing in T Lymphocytes1 , 2002, The Journal of Immunology.

[10]  J. Castle,et al.  Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs , 2005, Nature.

[11]  Yiping Fan,et al.  Response to Comment on "Large-Scale Sequence Analysis of Avian Influenza Isolates" , 2006, Science.

[12]  Steven A. Frank,et al.  Immunology and Evolution of Infectious Disease , 2002 .

[13]  Joshua N. Leonard,et al.  Computational Design of Antiviral RNA Interference Strategies That Resist Human Immunodeficiency Virus Escape , 2005, Journal of Virology.

[14]  L. O’Brien.  Inhibition of multiple strains of Venezuelan equine encephalitis virus by a pool of four short interfering RNAs , 2006, Antiviral Research.

[15]  Eric J Wagner,et al.  Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. , 2002, Molecular cell.

[16]  S. Hammond,et al.  An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells , 2000, Nature.

[17]  T. Tuschl,et al.  RNA interference is mediated by 21- and 22-nucleotide RNAs. , 2001, Genes & development.

[18]  B. Ramratnam,et al.  Human Immunodeficiency Virus Type 1 Escape from RNA Interference , 2003, Journal of Virology.

[19]  David P. Bartel,et al.  Passenger-Strand Cleavage Facilitates Assembly of siRNA into Ago2-Containing RNAi Enzyme Complexes , 2005, Cell.

[20]  H. Zarbl,et al.  Transcriptional and Posttranscriptional Silencing of Rodent α1(I) Collagen by a Homologous Transcriptionally Self-Silenced Transgene , 1999, Molecular and Cellular Biology.

[21]  Xiaoyu Lin,et al.  Defining the optimal parameters for hairpin-based knockdown constructs. , 2007, RNA.

[22]  K. Czaplinski,et al.  Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. , 2004, RNA.

[23]  John G Doench,et al.  Specificity of microRNA target selection in translational repression. , 2004, Genes & development.

[24]  J. Parvin,et al.  Measurement of the mutation rates of animal viruses: influenza A virus and poliovirus type 1 , 1986, Journal of virology.

[25]  Ben Berkhout,et al.  Human Immunodeficiency Virus Type 1 Escapes from RNA Interference-Mediated Inhibition , 2004, Journal of Virology.

[26]  Gyorgy Hutvagner,et al.  Small RNA asymmetry in RNAi: Function in RISC assembly and gene regulation , 2005, FEBS letters.

[27]  V. Kim,et al.  Biogenesis of small RNAs in animals , 2009, Nature Reviews Molecular Cell Biology.

[28]  L. Lim,et al.  Widespread siRNA "off-target" transcript silencing mediated by seed region sequence complementarity. , 2006, RNA.

[29]  E. Lai.  Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation , 2002, Nature Genetics.

[30]  L Misquitta,et al.  Targeted disruption of gene function in Drosophila by RNA interference (RNA-i): a role for nautilus in embryonic somatic muscle formation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Ben Berkhout,et al.  HIV-1 can escape from RNA interference by evolving an alternative structure in its RNA genome , 2005, Nucleic acids research.

[32]  Hiroyuki Miyoshi,et al.  Optimization of an siRNA‐expression system with an improved hairpin and its significant suppressive effects in mammalian cells , 2004, The journal of gene medicine.

[33]  Michael T. McManus,et al.  RNA interference of influenza virus production by directly targeting mRNA for degradation and indirectly inhibiting all viral RNA transcription , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[34]  C. Teng,et al.  Multitarget therapy of malignant cancers by the head-to-tail tandem array multiple shRNAs expression system , 2009, Cancer Gene Therapy.

[35]  M. Amarzguioui,et al.  Engineering and optimization of the mir-106b-cluster for ectopic expression of multiplexed anti-HIV RNAs , 2008, Gene Therapy.

[36]  K. Taira,et al.  Short hairpin type of dsRNAs that are controlled by tRNA(Val) promoter significantly induce RNAi-mediated gene silencing in the cytoplasm of human cells. , 2003, Nucleic acids research.

[37]  J. Dodgson,et al.  Inhibition of Marek's disease virus replication by retroviral vector-based RNA interference. , 2008, Virology.

[38]  T. Weng,et al.  A novel approach for the construction of multiple shRNA expression vectors , 2007, The journal of gene medicine.

[39]  Yaochen Li,et al.  Construction of influenza virus siRNA expression vectors and their inhibitory effects on multiplication of influenza virus. , 2005, Avian diseases.

[40]  B. Berkhout,et al.  Long-term inhibition of HIV-1 replication with RNA interference against cellular co-factors. , 2011, Antiviral research.

[41]  A. Sánchez Alvarado,et al.  Double-stranded RNA specifically disrupts gene expression during planarian regeneration. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  T. Doran,et al.  Inhibition of chicken anaemia virus replication using multiple short-hairpin RNAs. , 2008, Antiviral research.

[43]  Stanley T. Crooke,et al.  Reduced levels of Ago2 expression result in increased siRNA competition in mammalian cells , 2007, Nucleic acids research.

[44]  A. Fire,et al.  Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans , 1998, Nature.

[45]  D. Görlich,et al.  mediates nuclear export of pre-miRNAs Exportin 5 is a RanGTP-dependent dsRNA-binding protein that , 2004 .

[46]  B. Berkhout,et al.  Inhibition of HIV-1 by multiple siRNAs expressed from a single microRNA polycistron , 2008, Nucleic acids research.

[47]  T. Tuschl,et al.  Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells , 2001, Nature.

[48]  B. Scholte,et al.  Simultaneous targeting of HCV replication and viral binding with a single lentiviral vector containing multiple RNA interference expression cassettes. , 2006, Molecular therapy : the journal of the American Society of Gene Therapy.

[49]  Yong Huang,et al.  Thermodynamic stability of small hairpin RNAs highly influences the loading process of different mammalian Argonautes , 2011, Proceedings of the National Academy of Sciences.

[50]  E. Sontheimer,et al.  Origins and Mechanisms of miRNAs and siRNAs , 2009, Cell.

[51]  T. Applegate,et al.  An Infinitely Expandable Cloning Strategy plus Repeat-Proof PCR for Working with Multiple shRNA , 2008, PloS one.

[52]  Raman M. Das,et al.  A robust system for RNA interference in the chicken using a modified microRNA operon. , 2006, Developmental biology.

[53]  C. Rogler,et al.  Multi-miRNA hairpin method that improves gene knockdown efficiency and provides linked multi-gene knockdown. , 2006, BioTechniques.

[54]  A. Hatzigeorgiou,et al.  A combined computational-experimental approach predicts human microRNA targets. , 2004, Genes & development.

[55]  P. Cottee,et al.  Native microRNA loop sequences can improve short hairpin RNA processing for virus gene silencing in animal cells , 2008, Journal of RNAi and gene silencing : an international journal of RNA and gene targeting research.

[56]  C. Burge,et al.  Prediction of Mammalian MicroRNA Targets , 2003, Cell.

[57]  B. Berkhout,et al.  Combinatorial RNAi Against HIV-1 Using Extended Short Hairpin RNAs. , 2009, Molecular therapy : the journal of the American Society of Gene Therapy.

[58]  F Xiao-Feng Qin,et al.  Optimization and functional effects of stable short hairpin RNA expression in primary human lymphocytes via lentiviral vectors. , 2006, Molecular therapy : the journal of the American Society of Gene Therapy.

[59]  A. Ely,et al.  Expressed anti-HBV primary microRNA shuttles inhibit viral replication efficiently in vitro and in vivo. , 2008, Molecular therapy : the journal of the American Society of Gene Therapy.

[60]  Aimee L Jackson,et al.  Noise amidst the silence: off-target effects of siRNAs? , 2004, Trends in genetics : TIG.

[61]  B. Cullen,et al.  Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. , 2003, Genes & development.

[62]  Albert D. M. E. Osterhaus,et al.  Characterization of a Novel Influenza A Virus Hemagglutinin Subtype (H16) Obtained from Black-Headed Gulls , 2005, Journal of Virology.

[63]  B. Li,et al.  Expression profiling reveals off-target gene regulation by RNAi , 2003, Nature Biotechnology.

[64]  Samantha Barichievy,et al.  Specific inhibition of HBV replication in vitro and in vivo with expressed long hairpin RNA. , 2007, Molecular therapy : the journal of the American Society of Gene Therapy.

[65]  S. Sutou,et al.  Usage of putative chicken U6 promoters for vector-based RNA interference. , 2005, The Journal of reproduction and development.

[66]  K. Taira,et al.  Genome‐wide application of RNAi to the discovery of potential drug targets , 2005, FEBS letters.

[67]  A. Reynolds,et al.  Rational siRNA design for RNA interference , 2004, Nature Biotechnology.

[68]  B. Berkhout,et al.  Design of extended short hairpin RNAs for HIV-1 inhibition , 2007, Nucleic Acids Research.

[69]  Robert J. Moore,et al.  A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. , 2008, Genome research.

[70]  Ali Ehsani,et al.  Expression of small interfering RNAs targeted against HIV-1 rev transcripts in human cells , 2002, Nature Biotechnology.

[71]  Sanghyuk Lee,et al.  MicroRNA genes are transcribed by RNA polymerase II , 2004, The EMBO journal.

[72]  B. Cullen,et al.  Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. , 2004, Nucleic acids research.

[73]  L. Lambeth,et al.  Characterization and Comparison of Chicken U6 Promoters for the Expression of Short Hairpin RNAs , 2007, Animal biotechnology.

[74]  B. Cullen,et al.  Overexpression of exportin 5 enhances RNA interference mediated by short hairpin RNAs and microRNAs. , 2005, RNA.

[75]  R. Carthew,et al.  Use of dsRNA-Mediated Genetic Interference to Demonstrate that frizzled and frizzled 2 Act in the Wingless Pathway , 1998, Cell.

[76]  S. Elledge,et al.  A lentiviral microRNA-based system for single-copy polymerase II-regulated RNA interference in mammalian cells. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[77]  K. Taira,et al.  Screening of siRNA target sequences by using fragmentized DNA , 2006, Journal of Gene Medicine.

[78]  J. Lieberman,et al.  Lentiviral delivery of short hairpin RNAs protects CD4 T cells from multiple clades and primary isolates of HIV. , 2005, Blood.

[79]  L. Reed,et al.  A SIMPLE METHOD OF ESTIMATING FIFTY PER CENT ENDPOINTS , 1938 .

[80]  T. Tuschl,et al.  Analysis of gene function in somatic mammalian cells using small interfering RNAs. , 2002, Methods.

[81]  Anastasia Khvorova,et al.  Off-target effects by siRNA can induce toxic phenotype. , 2006, RNA.

[82]  B. Berkhout,et al.  Anticipating and blocking HIV-1 escape by second generation antiviral shRNAs , 2010, Retrovirology.

[83]  Wei Yan,et al.  Tissue-dependent paired expression of miRNAs , 2007, Nucleic acids research.

[84]  W. Fitch,et al.  Biological and genetic evolution of the nucleoprotein gene of human influenza A viruses. , 1989, The Journal of general virology.

[85]  M. Amarzguioui,et al.  Positional effects of short interfering RNAs targeting the human coagulation trigger Tissue Factor. , 2002, Nucleic acids research.

[86]  V. Nair,et al.  Targeting Marek's disease virus by RNA interference delivered from a herpesvirus vaccine. , 2009, Vaccine.

[87]  B. Berkhout,et al.  Optimization of shRNA inhibitors by variation of the terminal loop sequence. , 2010, Antiviral research.

[88]  Patrick J. Paddison,et al.  Stable suppression of gene expression by RNAi in mammalian cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[89]  Sheena M Saayman,et al.  Deriving four functional anti-HIV siRNAs from a single Pol III-generated transcript comprising two adjacent long hairpin RNA precursors , 2010, Nucleic acids research.

[90]  V. Kim,et al.  The nuclear RNase III Drosha initiates microRNA processing , 2003, Nature.

[91]  L. Steel,et al.  RNA polymerase III can drive polycistronic expression of functional interfering RNAs designed to resemble microRNAs , 2009, Nucleic acids research.

[92]  Multiple shRNA expressing vector enhances efficiency of gene silencing. , 2008, BMB reports.

[93]  T. Rana,et al.  RNAi in human cells: basic structural and functional features of small interfering RNA. , 2002, Molecular cell.

[94]  T. Hino,et al.  Escape from the interferon response associated with RNA interference using vectors that encode long modified hairpin-RNA. , 2005, Molecular bioSystems.

[95]  Stefan L Ameres,et al.  Cleavage of the siRNA passenger strand during RISC assembly in human cells , 2006, EMBO reports.

[96]  Paul A. Serbinowski,et al.  A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells , 2006, Nature Biotechnology.

[97]  N. Caplen,et al.  Inhibition of viral gene expression and replication in mosquito cells by dsRNA-triggered RNA interference. , 2002, Molecular therapy : the journal of the American Society of Gene Therapy.

[98]  M. Mathews,et al.  Interactions between double-stranded RNA regulators and the protein kinase DAI , 1992, Molecular and cellular biology.

[99]  J. Stone,et al.  Poliovirus Escape from RNA Interference: Short Interfering RNA-Target Recognition and Implications for Therapeutic Approaches , 2005, Journal of Virology.

[100]  A. Arndt,et al.  A comparison of multiple shRNA expression methods for combinatorial RNAi , 2011, Genetic vaccines and therapy.

[101]  C. Baglioni,et al.  Structural requirements of double-stranded RNA for the activation of 2',5'-oligo(A) polymerase and protein kinase of interferon-treated HeLa cells. , 1979, The Journal of biological chemistry.

[102]  M. Kohara,et al.  Intracellular-diced dsRNA has enhanced efficacy for silencing HCV RNA and overcomes variation in the viral genotype , 2006, Gene Therapy.

[103]  C. Napoli,et al.  Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans. , 1990, The Plant cell.

[104]  B. Berkhout,et al.  RNAi-mediated inhibition of HIV-1 by targeting partially complementary viral sequences , 2009, Nucleic acids research.

[105]  R. Bernards,et al.  A System for Stable Expression of Short Interfering RNAs in Mammalian Cells , 2002, Science.

[106]  M. Simon,et al.  A single lentiviral vector platform for microRNA-based conditional RNA interference and coordinated transgene expression , 2006, Proceedings of the National Academy of Sciences.

[107]  M. Carmell,et al.  Posttranscriptional Gene Silencing in Plants , 2006 .

[108]  J. Rossi,et al.  Expression of long anti-HIV-1 hairpin RNAs for the generation of multiple siRNAs: advantages and limitations. , 2008, Molecular therapy : the journal of the American Society of Gene Therapy.

[109]  J. Rossi,et al.  Amplification of RNAi--targeting HLA mRNAs. , 2005, Molecular therapy : the journal of the American Society of Gene Therapy.

[110]  B. Berkhout,et al.  Human Immunodeficiency Virus Type 1 Escape Is Restricted When Conserved Genome Sequences Are Targeted by RNA Interference , 2007, Journal of Virology.

[111]  Anne Gatignol,et al.  Combinatorial delivery of small interfering RNAs reduces RNAi efficacy by selective incorporation into RISC , 2007, Nucleic acids research.

[112]  Anastasia Khvorova,et al.  3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets , 2006, Nature Methods.

[113]  Li Yao-chen,et al.  Construction of Influenza Virus siRNA Expression Vectors and Their Inhibitory Effects on Multiplication of Influenza Virus , 2005 .

[114]  Michael Zuker,et al.  Mfold web server for nucleic acid folding and hybridization prediction , 2003, Nucleic Acids Res..

[115]  B. Berkhout,et al.  Combinatorial RNAi Against HIV-1 Using Extended Short Hairpin RNAs , 2009, Molecular therapy : the journal of the American Society of Gene Therapy.

[116]  Min Sun Kim,et al.  Inhibition of viral hemorrhagic septicemia virus replication using a short hairpin RNA targeting the G gene , 2011, Archives of Virology.

[117]  Stacy L DeRuiter,et al.  RNA interference by expression of short-interfering RNAs and hairpin RNAs in mammalian cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[118]  C. Rice,et al.  Clearance of replicating hepatitis C virus replicon RNAs in cell culture by small interfering RNAs , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[119]  Michael T. McManus,et al.  Gene silencing using micro-RNA designed hairpins. , 2002, RNA.

[120]  D. Baulcombe.  Gene silencing: RNA makes RNA makes no protein , 1999, Current Biology.

[121]  Xiaodong Wang,et al.  Argonaute2 Cleaves the Anti-Guide Strand of siRNA during RISC Activation , 2005, Cell.

[122]  Xiaoan Ruan,et al.  siRNA-mediated off-target gene silencing triggered by a 7 nt complementation , 2005, Nucleic acids research.

[123]  D. Cahill,et al.  Comparison of chicken 7SK and U6 RNA polymerase III promoters for short hairpin RNA expression , 2007, BMC biotechnology.

[124]  G. Stark,et al.  How cells respond to interferons. , 1998, Annual review of biochemistry.

[125]  R. Akkina,et al.  HIV-1 resistance conferred by siRNA cosuppression of CXCR4 and CCR5 coreceptors by a bispecific lentiviral vector , 2005, AIDS research and therapy.

[126]  T. Du,et al.  Asymmetry in the Assembly of the RNAi Enzyme Complex , 2003, Cell.

[127]  W. Forrester,et al.  A DNA vector-based RNAi technology to suppress gene expression in mammalian cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[128]  Patrick J. Paddison,et al.  Second-generation shRNA libraries covering the mouse and human genomes , 2005, Nature Genetics.

[129]  Dieter Huesken,et al.  Design of a genome-wide siRNA library using an artificial neural network , 2005, Nature Biotechnology.

[130]  V. Kim,et al.  MicroRNA maturation: stepwise processing and subcellular localization , 2002, The EMBO journal.

[131]  B. Cullen.  Induction of stable RNA interference in mammalian cells , 2006, Gene Therapy.

[132]  Christopher D. Richardson,et al.  Hepatitis C Virus Replicons Escape RNA Interference Induced by a Short Interfering RNA Directed against the NS5b Coding Region , 2005, Journal of Virology.

[133]  Cao Huang,et al.  A tightly regulated Pol III promoter for synthesis of miRNA genes in tandem. , 2008, Biochimica et biophysica acta.

[134]  H. Birnboim,et al.  A rapid alkaline extraction procedure for screening recombinant plasmid DNA. , 1979, Nucleic acids research.

[135]  Zhenbao Yu,et al.  High-throughput screening of effective siRNAs from RNAi libraries delivered via bacterial invasion , 2005, Nature Methods.

[136]  R. Andino,et al.  Short interfering RNA confers intracellular antiviral immunity in human cells , 2002, Nature.

[137]  G. Fanning,et al.  The effects of stem length and core placement on shRNA activity , 2011, BMC Molecular Biology.

[138]  Anastasia Khvorova,et al.  Functional siRNAs and miRNAs Exhibit Strand Bias , 2003, Cell.

[139]  Theresa A. Storm,et al.  Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways , 2006, Nature.

[140]  B. Cullen,et al.  Sequence requirements for micro RNA processing and function in human cells. , 2003, RNA.