Killing the messenger: short RNAs that silence gene expression (original) (raw)
Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature391, 806–811 (1998). The first evidence that dsRNA could mediate sequence-specific gene silencing. Silencing was shown to be heritable from parentalC. elegansto their progeny. CASPubMed Google Scholar
Jorgensen, R. Altered gene expression in plants due to trans interactions between homologous genes. Trends Biotechnol.8, 340–344 (1990). CASPubMed Google Scholar
Romano, N. & Macino, G. Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol. Microbiol.6, 3343–3353 (1992). Evidence that the ectopic expression of segments of transgenes leads to silencing of the endogenous homologues. This process is known as 'quelling' inNeurosporaand is related to PTGS in plants and RNAi in animals. CASPubMed Google Scholar
Grishok, A., Tabara, H. & Mello, C. C. Genetic requirements for inheritance of RNAi in C. elegans. Science287, 2494–2497 (2000). This study begins to assemble the genes that are involved in RNAi into a pathway and explain the genetic requirements of inheritance of RNAi phenotypes from parents to offspring. CASPubMed Google Scholar
Hamilton, A. J. & Baulcombe, D. C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science286, 950–952 (1999). CASPubMed Google Scholar
Zamore, P. D., Tuschl, T., Sharp, P. A. & Bartel, D. P. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell101, 25–33 (2000). This paper shows the 'processing' of long dsRNA by Dicer into shorter fragments in 21–23-nt intervals inDrosophilaextracts and describes the biochemical requirements for the 'dicing' reactionin vitro. ArticleCASPubMed Google Scholar
Yang, D., Lu, H. & Erickson, J. W. Evidence that processed small dsRNAs may mediate sequence-specific mRNA degradation during RNAi in Drosophila embryos. Curr. Biol.10, 1191–1200 (2000). CASPubMed Google Scholar
Parrish, S., Fleenor, J., Xu, S., Mello, C. & Fire, A. Functional anatomy of a dsRNA trigger: differential requirement for the two trigger strands in RNA interference. Mol. Cell6, 1077–1087 (2000). CASPubMed Google Scholar
Hammond, S. M., Bernstein, E., Beach, D. & Hannon, G. J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature404, 293–296 (2000). CASPubMed Google Scholar
Sullenger, B. A. & Gilboa, E. Emerging clinical applications of RNA. Nature418, 252–258 (2002). CASPubMed Google Scholar
Kitabwalla, M. & Ruprecht, R. M. RNA interference — a new weapon against HIV and beyond. N. Engl. J. Med.347, 1364–1367 (2002). CASPubMed Google Scholar
Dornburg, R. & Pomerantz, R. J. HIV-1 gene therapy: promise for the future. Adv. Pharmacol.49, 229–261 (2000). CASPubMed Google Scholar
Bernstein, E., Caudy, A. A., Hammond, S. M. & Hannon, G. J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature409, 363–366 (2001). The first paper to report the cloning of Dicer. The RNase III enzyme is evolutionarily conserved and contains helicase and PAZ domains, as well as two dsRNA-binding domains. CASPubMed Google Scholar
Ketting, R. F. et al. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev.15, 2654–2659 (2001). CASPubMedPubMed Central Google Scholar
Billy, E., Brondani, V., Zhang, H., Müller, H. & Filipowicz, W. Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. Proc. Natl Acad. Sci. USA98, 14428–14433 (2001). CASPubMedPubMed Central Google Scholar
Kawasaki, H. & Taira, K. Short hairpin type of dsRNAs that are controlled by tRNAVal promoter significantly induce RNAi-mediated gene silencing in the cytoplasm of human cells. Nucleic Acids Res.31, 700–707 (2003). CASPubMedPubMed Central Google Scholar
Nykanen, A., Haley, B. & Zamore, P. D. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell107, 309–321 (2001). RNAi requires ATP for long dsRNA cleavage and for siRNA unwinding and maintaining 5′ phosphate on the siRNA. RISC is present in two alternative forms, and the inactive holo-complex can be converted to the active form by incorporation of bona fide siRNA. CASPubMed Google Scholar
Schwarz, D. S., Hutvagner, G., Haley, B. & Zamore, P. D. Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol. Cell10, 537–548 (2002). CASPubMed Google Scholar
Pasquinelli, A. E. MicroRNAs: deviants no longer. Trends Genet.18, 171–173 (2002). CASPubMed Google Scholar
Pasquinelli, A. E. & Ruvkun, G. Control of developmental timing by micrornas and their targets. Annu. Rev. Cell Dev. Biol.18, 495–513 (2002). CASPubMed Google Scholar
Grishok, A. et al. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell106, 23–34 (2001). CASPubMed Google Scholar
Mourelatos, Z. et al. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev.16, 720–728 (2002). CASPubMedPubMed Central Google Scholar
Baulcombe, D. C. Gene silencing: RNA makes RNA makes no protein. Curr. Biol.9, R599–R601 (1999). CASPubMed Google Scholar
Sánchez-Alvarado, A. & Newmark, P. A. Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc. Natl Acad. Sci. USA96, 5049–5054 (1999). PubMedPubMed Central Google Scholar
Lohmann, J. U., Endl, I. & Bosch, T. C. G. Silencing of developmental genes in Hydra. Dev. Biol.214, 211–214 (1999). CASPubMed Google Scholar
Ngô, H., Tschudi, C., Gull, K. & Ullu, E. Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc. Natl Acad. Sci. USA95, 14687–14692 (1998). PubMedPubMed Central Google Scholar
Kennerdell, J. R. & Carthew, R. W. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell95, 1017–1026 (1998). CASPubMed Google Scholar
Misquitta, L. & Paterson, B. M. Targeted disruption of gene function in Drosophila by RNA interference (RNA-i): a role for nautilus in embryonic somatic muscle formation. Proc. Natl Acad. Sci. USA96, 1451–1456 (1999). CASPubMedPubMed Central Google Scholar
Caplen, N. J., Zheng, Z., Falgout, B. & Morgan, R. A. Inhibition of viral gene expression and replication in mosquito cells by dsRNA-triggered RNA interference. Mol. Ther.6, 243–251 (2002). CASPubMed Google Scholar
Svoboda, P., Stein, P., Hayashi, H. & Schultz, R. M. Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development127, 4147–4156 (2000). CASPubMed Google Scholar
Wianny, F. & Zernicka-Goetz, M. Specific interference with gene function by double-stranded RNA in early mouse development. Nature Cell Biol.2, 70–75 (2000). CASPubMed Google Scholar
Elbashir, S. M. et al. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature411, 494–498 (2001). The first evidence that siRNAs can mediate sequence-specific gene silencing in mammals and that the dicing step can be bypassed by the introduction of siRNA into cells. CASPubMed Google Scholar
Stark, G. et al. How cells respond to interferons. Annu. Rev. Biochem.67, 227–264 (1998). CASPubMed Google Scholar
Hammond, S. M., Bernstein, E., Beach, D. & Hannon, G. J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature404, 293–296 (2000). CASPubMed Google Scholar
Caplen, N. J., Fleenor, J., Fire, A. & Morgan, R. A. dsRNA-mediated gene silencing in cultured Drosophila cells: a tissue culture model for the analysis of RNA interference. Gene252, 95–105 (2000). CASPubMed Google Scholar
Ui-Tei, K., Zenno, S., Miyata, Y. & Saigo, K. Sensitive assay of RNA interference in Drosophila and Chinese hamster cultured cells using firefly luciferase gene as target. FEBS Lett.479, 79–82 (2000). CASPubMed Google Scholar
Holen, T., Amarzguioui, M., Wiiger, M. T., Babaie, E. & Prydz, H. Positional effects of short interfering RNAs targeting the human coagulation trigger tissue factor. Nucleic Acids Res.30, 1757–1766 (2002). CASPubMedPubMed Central Google Scholar
Miyagishi, M. & Taira, K. U6 promoter-driven siRNAs with four uridine 3′ overhangs efficiently suppress targeted gene expression in mammalian cells. Nature Biotechnol.20, 497–500 (2002). CAS Google Scholar
Vickers, T. A. et al. Efficient reduction of target RNAs by siRNA and RNase H dependent antisense agents: a comparative analysis. J. Biol. Chem.278, 7108–7118 (2003). CASPubMed Google Scholar
Hemann, M. T. et al. An epi-allelic series of p53 hypomorphs created by stable RNAi produces distinct tumor phenotypes in vivo. Nature Genet.33, 396–400 (2003). CASPubMed Google Scholar
Yang, D. et al. Short RNA duplexes produced by hydrolysis with Escherichia coli RNase III mediate effective RNA interference in mammalian cells. Proc. Natl Acad. Sci. USA99, 9942–9947 (2002). CASPubMedPubMed Central Google Scholar
Calegari, F., Haubensak, W., Yang, D., Huttner, W. B. & Buchholz, F. Tissue-specific RNA interference in postimplantation mouse embryos with endoribonuclease-prepared short interfering RNA. Proc. Natl Acad. Sci. USA99, 14236–14240 (2002). CASPubMedPubMed Central Google Scholar
Kawasaki, H., Suyama, E., Iyo, M. & Taira, K. siRNAs generated by recombinant human Dicer induce specific and significant but target site-independent gene silencing in human cells. Nucleic Acids Res.31, 981–987 (2003). CASPubMedPubMed Central Google Scholar
Myers, J. W., Jones, J. T., Meyer, T. & Ferrell, J. E. Recombinant Dicer efficiently converts large dsRNAs into siRNAs suitable for gene silencing. Nature Biotechnol.21, 324–328 (2003). CAS Google Scholar
Lee, N. S. et al. Expression of small interfering RNAs targeted against HIV-1 rev transcripts in human cells. Nature Biotechnol.20, 500–505 (2002). CAS Google Scholar
Cogoni, C. & Macino, G. Homology-dependent gene silencing in plants and fungi: a number of variations on the same theme. Curr. Opin. Microbiol.2, 657–662 (1999). CASPubMed Google Scholar
Dalmay, T., Hamilton, A., Rudd, S., Angell, S. & Baulcombe, D. C. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell101, 543–553 (2000). CASPubMed Google Scholar
Sijen, T. et al. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell107, 465–476 (2001). CASPubMed Google Scholar
Paddison, P. J. & Hannon, G. J. RNA interference: the new somatic cell genetics? Cancer Cell2, 17–23 (2002). CASPubMed Google Scholar
Chiu, Y. L. & Rana, T. M. RNAi in human cells: basic structural and functional features of small interfering RNA. Mol. Cell10, 549–561 (2002). CASPubMed Google Scholar
Stein, P., Svoboda, P., Anger, M. & Schultz, R. M. RNAi: mammalian oocytes do it without RNA-dependent RNA polymerase. RNA9, 187–192 (2003). CASPubMedPubMed Central Google Scholar
Svoboda, P., Stein, P. & Schultz, R. M. RNAi in mouse oocytes and preimplantation embryos: effectiveness of hairpin dsRNA. Biochem. Biophys. Res. Commun.287, 1099–1104 (2001). CASPubMed Google Scholar
Tavernarakis, N., Wang, S. L., Dorovkov, M., Ryazanov, A. & Driscoll, M. Heritable and inducible genetic interference by double-stranded RNA encoded by transgenes. Nature Genet.24, 180–183 (2000). CASPubMed Google Scholar
Kennerdell, J. R. & Carthew, R. W. Heritable gene silencing in Drosophila using double-stranded RNA. Nature Biotechnol.18, 896–898 (2000). CAS Google Scholar
Brummelkamp, T. R., Bernards, R. & Agami, R. A system for stable expression of short interfering RNAs in mammalian cells. Science296, 550–53 (2002). CASPubMed Google Scholar
McManus, M. T., Petersen, C. P., Haines, B. B., Chen, J. & Sharp, P. A. Gene silencing using micro-RNA designed hairpins. RNA8, 842–850 (2002). CASPubMedPubMed Central Google Scholar
Paddison, P. J., Caudy, A. A., Bernstein, E., Hannon, G. J. & Conklin, D. S. Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cells. Genes Dev.16, 948–958 (2002). CASPubMedPubMed Central Google Scholar
Paddison, P. J., Caudy, A. A. & Hannon, G. J. Stable suppression of gene expression by RNAi in mammalian cells. Proc. Natl Acad. Sci. USA99, 1443–1448 (2002). CASPubMedPubMed Central Google Scholar
Paul, C. P., Good, P. D., Winer, I. & Engelke, D. R. Effective expression of small interfering RNA in human cells. Nature Biotechnol.20, 505–508 (2002). CAS Google Scholar
Sui, G. et al. A DNA vector-based RNAi technology to suppress gene expression in mammalian cells. Proc. Natl Acad. Sci. USA99, 5515–5520 (2002). CASPubMedPubMed Central Google Scholar
Yu, J. -Y., DeRuiter, S. L. & Turner, D. L. RNA interference by expression of short-interfering RNAs and hairpin RNAs in mammalian cells. Proc. Natl Acad. Sci. USA99, 6047–6052 (2002). CASPubMedPubMed Central Google Scholar
Paule, M. R. & White, R. J. Survey and summary: transcription by RNA polymerases I and III. Nucleic Acids Res.28, 1283–1298 (2000). CASPubMedPubMed Central Google Scholar
Myslinski, E., Ame, J. C., Krol, A. & Carbon, P. An unusually compact external promoter for RNA polymerase III transcription of the human H1RNA gene. Nucleic Acids Res.29, 2502–2509 (2001). CASPubMedPubMed Central Google Scholar
Reinhart, B. J. et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature403, 901–906 (2000). CASPubMed Google Scholar
Hutvagner, G. et al. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science293, 834–838 (2001). MicroRNAs are genetically related to siRNAs by Dicer processing, and the silencing of Dicer led to accumulation of the prototype microRNA precursor oflet-7. CASPubMed Google Scholar
Knight, S. W. & Bass, B. L. A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science293, 2269–2271 (2001). CASPubMedPubMed Central Google Scholar
Brummelkamp, T. R., Bernards, R. & Agami, R. Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell2, 243–247 (2002). CASPubMed Google Scholar
Rubinson, D. A. et al. A lentivirus-based system to silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nature Genet.33, 401–406 (2003). CASPubMed Google Scholar
Qin, X. F., An, D. S., Chen, I. S. & Baltimore, D. Inhibiting HIV-1 infection in human T cells by lentiviral-mediated delivery of small interfering RNA against CCR5. Proc. Natl Acad. Sci. USA100, 183–188 (2003). CASPubMed Google Scholar
Naldini, L. et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science272, 263–267 (1996). CASPubMed Google Scholar
Svoboda, J., Hejnar, J., Geryk, J., Elleder, D. & Vernerova, Z. Retroviruses in foreign species and the problem of provirus silencing. Gene261, 181–188 (2000). CASPubMed Google Scholar
Hacein-Bey-Abina, S., von Kalle, C., Schmidt, M. & Le Deist, F. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med.348, 255–256 (2003). PubMed Google Scholar
Noguchi, P. Risks and benefits of gene therapy. N. Engl. J. Med.348, 193–194 (2003). PubMed Google Scholar
Marshall, E. Gene therapy: second child in French trial is found to have leukemia. Science299, 320 (2003). CASPubMed Google Scholar
Gordon, J. W. Production of transgenic mice. Methods Enzymol.225, 747–771 (1993). CASPubMed Google Scholar
Carmell, M. A., Zhang, L., Conklin, D. S., Hannon, G. J. & Rosenquist, T. A. Germline transmission of RNAi in mice. Nature Struct. Biol.10, 91–92 (2003). CASPubMed Google Scholar
Hasuwa, H., Kaseda, K., Einarsdottir, T. & Okabe, M. Small interfering RNA and gene silencing in transgenic mice and rats. FEBS Lett.532, 227–230 (2002). CASPubMed Google Scholar
Lois, C., Hong, E. J., Pease, S., Brown, E. J. & Baltimore, D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science295, 868–872 (2002). Lentiviral vectors are efficient vehicles for gene delivery to embryos and they enable the efficient production of transgenic animals. The lentiviral vector described is the parent vector for many of the lentiviral vectors being used at present to deliver small RNAs. CASPubMed Google Scholar
Tiscornia, G., Singer, O., Ikawa, M. & Verma, I. M. A general method for gene knockdown in mice by using lentiviral vectors expressing small interfering RNA. Proc. Natl Acad. Sci. USA100, 1844–1848 (2003). CASPubMedPubMed Central Google Scholar
Liu, F., Song, Y. & Liu, D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Therapy6, 1258–1266 (1999). CASPubMed Google Scholar
Zhang, G., Budker, V. & Wolff, J. A. High levels of foreign gene expression in hepatocytes after tail vein injections of naked plasmid DNA. Hum. Gene Ther.10, 1735–1737 (1999). CASPubMed Google Scholar
Lewis, D. L., Hagstrom, J. E., Loomis, A. G., Wolff, J. A. & Herweijer, H. Efficient delivery of siRNA for inhibition of gene expression in postnatal mice. Nature Genet.32, 107–108 (2002). CASPubMed Google Scholar
McCaffrey, A. P. et al. RNA interference in adult mice. Nature418, 38–39 (2002). CASPubMed Google Scholar
Song, E. et al. RNA interference targeting Fas protects mice from fulminant hepatitis. Nature Med.9, 347–351 (2003). The first report that siRNAs could be used therapeutically in whole animals. Hydrodynamic injection of siRNAs into mice led to silencing of Fas-receptor expression, inhibition of Fas-mediated apoptosis in the liver and the prevention of fulminant hepatitis that would have led to death of the mice. CASPubMed Google Scholar
Gonczy, P. et al. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature408, 331–336 (2000). CASPubMed Google Scholar
Fraser, A. G. et al. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature408, 325–330 (2000). CASPubMed Google Scholar
Lee, S. S. et al. A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nature Genet.33, 40–48 (2003). CASPubMed Google Scholar
Ashrafi, K. et al. Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature421, 268–272 (2003). CASPubMed Google Scholar
Kamath, R. S. et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature421, 231–237 (2003). RNAi can be used in functional-genomic approaches to uncover the networks of gene that are involved in common processes. This study reports the production and screening of aC. elegansRNAi library representing ∼17,000 genes, which covers 86% of the total number of genes. CASPubMed Google Scholar
Elbashir, S. M., Harborth, J., Weber, K. & Tuschl, T. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods26, 199–213 (2002). CASPubMed Google Scholar
Martinez, J., Patkaniowska, A., Urlaub, H., Luhrmann, R. & Tuschl, T. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell110, 563–574 (2002). CASPubMed Google Scholar
McManus, M. T. et al. Small interfering RNA-mediated gene silencing in T lymphocytes. J. Immunol.169, 5754–5760 (2002). CASPubMed Google Scholar
Zeng, Y., Wagner, E. J. & Cullen, B. R. Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol. Cell9, 1327–1333 (2002). CASPubMed Google Scholar
Xia, H., Mao, Q., Paulson, H. L. & Davidson, B. L. siRNA-mediated gene silencing in vitro and in vivo. Nature Biotechnol.20, 1006–1010 (2002). CAS Google Scholar
Novina, C. D. et al. siRNA-directed inhibition of HIV-1 infection. Nature Med.8, 681–686 (2002). CASPubMed Google Scholar
Capodici, J., Kariko, K. & Weissman, D. Inhibition of HIV-1 infection by small interfering RNA-mediated RNA interference. J. Immunol.169, 5196–5201 (2002). PubMed Google Scholar
Coburn, G. A. & Cullen, B. R. Potent and specific inhibition of human immunodeficiency virus type 1 replication by RNA interference. J. Virol.76, 9225–9231 (2002). CASPubMedPubMed Central Google Scholar
Jacque, J. M., Triques, K. & Stevenson, M. Modulation of HIV-1 replication by RNA interference. Nature418, 435–438 (2002). CASPubMed Google Scholar
Gitlin, L., Karelsky, S. & Andino, R. Short interfering RNA confers intracellular antiviral immunity in human cells. Nature418, 430–434 (2002). CASPubMed Google Scholar
Jiang, M. & Milner, J. Selective silencing of viral gene expression in HPV-positive human cervical carcinoma cells treated with siRNA, a primer of RNA interference. Oncogene21, 6041–6048 (2002). CASPubMed Google Scholar
Bitko, V. & Barik, S. Phenotypic silencing of cytoplasmic genes using sequence-specific double-stranded short interfering RNA and its application in the reverse genetics of wild type negative-strand RNA viruses. BMC Microbiol.1, 34 (2001). CASPubMedPubMed Central Google Scholar
Scherr, M. et al. Specific inhibition of bcr_–_abl gene expression by small interfering RNA. Blood101, 1566–1569 (2003). CASPubMed Google Scholar
Wang, B., Matsuoka, S., Carpenter, P. B. & Elledge, S. J. 53BP1, a mediator of the DNA damage checkpoint. Science298, 1435–1438 (2002). CASPubMed Google Scholar
Kartasheva, N. N., Contente, A., Lenz-Stoppler, C., Roth, J. & Dobbelstein, M. p53 induces the expression of its antagonist p73ΔN, establishing an autoregulatory feedback loop. Oncogene21, 4715–4727 (2002). CASPubMed Google Scholar
Martinez, M. A. et al. Suppression of chemokine receptor expression by RNA interference allows for inhibition of HIV-1 replication. AIDS16, 2385–2390 (2002). CASPubMed Google Scholar