Expressing short hairpin RNAs in vivo

Nature Methods

Volumn 3, Issue 9, 2006, Pages 689-695

  Snøve Jr , Ola ^a,b,c   Rossi, John J ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b Interagon AS   (Norway)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; DNA DIRECTED RNA POLYMERASE III; DOXYCYCLINE; ECDYSONE; EXPORTIN 5; MICRORNA; PARVOVIRUS VECTOR; PLASMID DNA; RETROVIRUS VECTOR; RNA POLYMERASE II; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ALGORITHM; ARTICLE; CONGESTIVE CARDIOMYOPATHY; DOSE RESPONSE; DRUG DESIGN; DRUG EFFICACY; DRUG FATALITY; DRUG MEGADOSE; DRUG POTENCY; DRUG SAFETY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENE SILENCING; GENE TARGETING; GENE THERAPY; HEPATITIS; HUMAN; IMMUNE RESPONSE; IN VIVO STUDY; INNATE IMMUNITY; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PRIORITY JOURNAL; RESPIRATORY TRACT INFECTION; RETINA MACULA DEGENERATION; RNA INTERFERENCE; RNA STRUCTURE; VIRAL GENE DELIVERY SYSTEM; VIRUS INFECTION;

ANIMALS; GENE EXPRESSION; GENETIC VECTORS; HUMANS; PROMOTER REGIONS (GENETICS); RNA; RNA INTERFERENCE;

EID: 33747779678     PISSN: 15487091     EISSN: 15491676     Source Type: Journal    
DOI: 10.1038/nmeth927     Document Type: Article

References (108)

1. Pei, Y. & Tuschl, T. On the art of identifying effective and specific siRNAs. Nat. Methods 3, 670-676 (2006).
2. Cullen, B.R. Enhancing and confirming the specificity of RNAi experiments. Nat. Methods 3, 677-681 (2006).
3. Behlke, M.A. Progress towards in vivo use of siRNAs. Mol. Ther. 13, 644-670 (2006).
4. Song, E. et al. RNA interference targeting Fas protects mice from fulminant hepatitis. Nat. Med. 9, 347-351 (2003).
5. Reich, S.J. et al. Small interfering RNA (siRNA) targeting VEGF effectively inhibits ocular neovascularization in a mouse model. Mol. Vis. 9, 210-216 (2003).
6. Li, B.J. et al. Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in Rhesus macaque. Nat. Med. 11, 944-951 (2005).
7. Morrissey, D.V. et al. Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat. Biotechnol. 23, 1002-1007 (2005).
8. Song, E. et al. Antibody mediated in vivo delivery of small interfering RNAs via cell-surface receptors. Nat. Biotechnol. 23, 709-717 (2005).
9. Soutschek, J. et al. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 432, 173-178 (2004).
10. Zimmermann, T.S. et al. RNAi-mediated gene silencing in non-human primates. Nature 441, 111-114 (2006).
11. Wang, Q., Contag, C.H., Ilves, H., Johnston, B.H. & Kaspar, R.L. Small hairpin RNAs efficiently inhibit hepatitis C IRES-mediated gene expression in human tissue culture cells and a mouse model. Mol. Ther. 12, 562-568 (2005).
12. Lewis, D.L. & Wolff, J.A. Delivery of siRNA and siRNA expression constructs to adult mammals by hydrodynamic intravascular injection. Methods Enzymol. 392, 336-350 (2005).
13. Zhang, G. et al. Hydroporation as the mechanism of hydrodynamic delivery. Gene Ther. 11, 675-682 (2004).
14. Kay, M.A., Glorioso, J.C. & Naldini, L. Viral vectors for gene therapy: the art of turning infectious agents into vehicles of therapeutics. Nat. Med. 7, 33-40 (2001).
15. Huang, A. et al. Functional silencing of hepatic microsomal glucose-6-phosphatase gene expression in vivo by adenovirus-mediated delivery of short hairpin RNA. FEBS Lett. 558, 69-73 (2004).
16. Huang, B. & Kochanek, S. Adenovirus-mediated silencing of huntingtin expression by shRNA. Hum. Gene Ther. 16, 618-626 (2005).
17. Kuninger, D. et al. Gene disruption by regulated short interfering RNA expression, using a two-adenovirus system. Hum. Gene Ther. 15, 1287-1292 (2004).
18. Xia, H. et al. RNAi suppresses polyglutamine-induced neurodegeneration in a model of spinocerebellar ataxia. Nat. Med. 10, 816-820 (2004).
19. Hong, C.S., Goins, W.F., Goss, J.R., Burton, E.A. & Glorioso, J.C. Herpes simplex virus RNAi and neprilysin gene transfer vectors reduce accumulation of Alzheimer's disease-related amyloid-beta peptide in vivo. Gene Ther. 13, 1068-1079 (2006).
20. Thomas, C.E., Ehrhardt, A. & Kay, M.A. Progress and problems with the use of viral vectors for gene therapy. Nat. Rev. Genet. 4, 346-358 (2003).
21. Lin, G. et al. Improving erectile function by silencing phosphodiesterase-5. J. Urol. 174, 1142-1148 (2005).
22. Rubinson, D.A. et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33, 401-406 (2003).
23. Stegmeier, F., Hu, G., Rickles, R.J., Hannon, G.J. & Elledge, S.J. A lentiviral microRNA-based system for single-copy polymerase II-regulated RNA interference in mammalian cells. Proc. Natl. Acad. Sci. USA 102, 13212-13217 (2005).
24. Romano, G. Current development of lentiviral-mediated gene transfer. Drug News Perspect. 18, 128-134 (2005).
25. Burger, C. et al. Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol. Ther. 10, 302-317 (2004).
26. Cronin, J., Zhang, X.Y. & Reiser, J. Altering the tropism of lentiviral vectors through pseudotyping. Curr. Gene Ther. 5, 387-398 (2005).
27. Lagos-Quintana, M., Rauhut, R., Lendeckel, W. & Tuschl, T. Identification of novel genes coding for small expressed RNAs. Science 294, 853-858 (2001).
28. Lau, N.C., Lim, L.P., Weinstein, E.G. & Bartel, D.P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858-862 (2001).
29. Lee, R.C. & Ambros, V. An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862-864 (2001).
30. Bernstein, E., Caudy, A.A., Hammond, S.M. & Hannon, G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366 (2001).
31. Hutvagner, G. et al. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834-838 (2001).
32. Doench, J.G., Petersen, C.P. & Sharp, P.A. siRNAs can function as miRNAs. Genes Dev. 17, 438-442 (2003).
33. Mourelatos, Z. et al. miRNPs: A novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev. 16, 720-728 (2002).
34. Hutvagner, G. & Zamore, P.D. A microRNA in a multiple-turnover RNAi enzyme complex. Science 297, 2056-2060 (2002).
35. Yekta, S., Shih, I.H. & Bartel, D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 304, 594-596 (2004).
36. Meister, G. et al. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15, 185-197 (2004).
37. 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. Cell 101, 25-33 (2000).
38. Bagga, S. et al. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122, 553-563 (2005).
39. Giraldez, A.J. et al. MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833-838 (2005).
40. Wu, L., Fan, J. & Belasco, J.G. MicroRNAs direct rapid deadenylation of mRNA. Proc. Natl. Acad. Sci. USA 103, 4034-4039 (2006).
41. Olsen, P.H. & Ambros, V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671-680 (1999).
42. Reinhart, B.J. et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906 (2000).
43. Wightman, B., Ha, I. & Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855-862 (1993).
44. Glover, D.J., Lipps, H.J. & Jans, D.A. Towards safe, non-viral therapeutic gene expression in humans. Nat. Rev. Genet. 6, 299-310 (2005).
45. Patil, S.D., Rhodes, D.G. & Burgess, D.J. DNA-based therapeutics and DNA delivery systems: A comprehensive review. AAPS J. 7, E61-E77 (2005).
46. Sledz, C.A., Holko, M., de Veer, M.J., Silverman, R.H. & Williams, B.R. Activation of the interferon system by short-interfering RNAs. Nat. Cell Biol. 5, 834-839 (2003).
47. Bridge, A.J., Pebernard, S., Ducraux, A., Nicoulaz, A.L. & Iggo, R. Induction of an interferon response by RNAi vectors in mammalian cells. Nat. Genet. 34, 263-264 (2003).
48. Manche, L., Green, S.R., Schmedt, C. & Mathews, M.B. Interactions between double-stranded RNA regulators and the protein kinase DAI. Mol. Cell. Biol. 12, 5238-5248 (1992).
49. Robbins, M.A. et al. Stable expression of shRNAs in human CD34(+) progenitor cells can avoid induction of interferon responses to siRNAs in vitro. Nat. Biotechnol. 24, 566-571 (2006).
50. Marques, J.T. & Williams, B.R. Activation of the mammalian immune system by siRNAs. Nat. Biotechnol. 23, 1399-1405 (2005).
51. Yi, R., Doehle, B.P., Qin, Y., Macara, I.G. & Cullen, B.R. Overexpression of exportin 5 enhances RNA interference mediated by short hairpin RNAs and microRNAs. RNA 11, 220-226 (2005).
52. Bohnsack, M.T., Czaplinski, K. & Gorlich, D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10, 185-191 (2004).
53. Lund, E., Guttinger, S., Calado, A., Dahlberg, J.E. & Kutay, U. Nuclear export of microRNA precursors. Science 303, 95-98 (2004).
54. Yi, R., Qin, Y., Macara, I.G. & Cullen, B.R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17, 3011-3016 (2003).
55. Grimm, D. et al. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441, 537-541 (2006).
56. Gregory, R.I. et al. The Microprocessor complex mediates the genesis of microRNAs. Nature 432, 235-240 (2004).
57. Han, J. et al. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 18, 3016-3027 (2004).
58. Lee, Y. et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419 (2003).
59. Chendrimada, T.P. et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740-744 (2005).
60. 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).
61. Schwarz, D.S. et al. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115, 199-208 (2003).
62. Khvorova, A., Reynolds, A. & Jayasena, S.D. Functional siRNAs and miRNAs exhibit strand bias. Cell 115, 209-216 (2003).
63. Reynolds, A. et al. Rational siRNA design for RNA interference. Nat. Biotechnol. 22, 326-330 (2004).
64. Lewis, B.P., Burge, C.B. & Bartel, D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20 (2005).
65. Lim, L.P. et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769-773 (2005).
66. Boutla, A., Delidakis, C., Livadaras, I., Tsagris, M. & Tabler, M. Short 5′-phosphorylated double-stranded RNAs induce RNA interference in Drosophila. Curr. Biol. 11, 1776-1780 (2001).
67. Elbashir, S.M. et al. Duplexes of 21-nucleotide RNAs mediate. RNA interference in cultured mammalian cells. Nature 411, 494-498 (2001).
68. Birmingham, A. et al. 3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat. Methods 3, 199-204 (2006).
69. Harborth, J. et al. Sequence, chemical, and structural variation of small interfering RNAs and short hairpin RNAs and the effect on mammalian gene silencing. Antisense Nucleic Acid Drug Dev. 13, 83-105 (2003).
70. Jackson, A.L. et al. Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21, 635-637 (2003).
71. Jackson, A.L. et al. Widespread siRNA "off-target' transcript silencing mediated by seed region sequence complementarity. RNA 12, 1179-1187 (2006).
72. Persengiev, S.P., Zhu, X. & Green, M.R. Nonspecific, concentration-dependent stimulation and repression of mammalian gene expression by small interfering RNAs (siRNAs). RNA 10, 12-18 (2004).
73. Saxena, S., Jonsson, Z.O. & Dutta, A. Small RNAs with imperfect match to endogenous mRNA repress translation. Implications for off-target activity of small inhibitory RNA in mammalian cells. J. Biol. Chem. 278, 44312-44319 (2003).
74. Martinez, J. & Tuschl, T. RISC is a 5′ phosphomonoester-producing RNA endonuclease. Genes Dev. 18, 975-980 (2004).
75. Haley, B. & Zamore, P.D. Kinetic analysis of the RNAi enzyme complex. Nat. Struct. Mol. Biol. 31, 599-606 (2004).
76. Roush, S. & Slack, F. Micromanagement: MicroRNAs stabilize mRNAs. ACS Chem. Biol. 1, 132-134 (2006).
77. Brennecke, J., Stark, A., Russell, R.B. & Cohen, S.M. Principles of microRNA-target recognition. PLoS Biol. 3, e85 (2005).
78. Grun, D., Wang, Y.L., Langenberger, D., Gunsalus, K.C. & Rajewsky, N. microRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput. Biol. 1, e13 (2005).
79. John, B. et al. Human MicroRNA targets. PLoS Biol. 2, e363 (2004).
80. Lewis, B.P., Shih, I.H., Jones-Rhoades, M.W., Bartel, D.P. & Burge, C.B. Prediction of mammalian microRNA targets. Cell 115, 787-798 (2003).
81. Bartel, D.P. & Chen, C.Z. Micromanagers of gene expression: The potentially widespread influence of metazoan microRNAs. Nat. Rev. Genet. 5, 396-400 (2004).
82. Krek, A. et al. Combinatorial microRNA target predictions. Nat. Genet. 37, 495-500 (2005).
83. Fedorov, Y. et al. Off-target effects by siRNA can induce toxic phenotype. RNA 12, 1188-1196 (2006).
84. Hannon, G.J. & Rossi, J.J. Unlocking the potential of the human genome with RNA interference. Nature 431, 371-378 (2004).
85. Brummelkamp, T.R., Bernards, R. & Agami, R. A system for stable expression of short interfering RNAs in mammalian cells. Science 296, 550-553 (2002).
86. 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).
87. McManus, M.T., Petersen, C.P., Haines, B.B., Chen, J. & Sharp, P.A. Gene silencing using micro-RNA designed hairpins. RNA 8, 842-850 (2002).
88. 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. Cell 9, 1327-1333 (2002).
89. Saetrom, P. et al. Conserved microRNA characteristics in mammals. Oligonucleotides 16, 115-144 (2006).
90. Denti, M.A., Rosa, A., Sthandier, O., De Angelis, F.G. & Bozzoni, I. A new vector, based on the PolII promoter of the U1 snRNA gene, for the expression of siRNAs in mammalian cells. Mol. Ther. 10, 191-199 (2004).
91. Szulc, J., Wiznerowicz, M., Sauvain, M.O., Trono, D. & Aebischer, P. A versatile tool for conditional gene expression and knockdown. Nat. Methods 3, 109-116 (2006).
92. Unwalla, H.J. et al. Negative feedback inhibition of HIV-1 by TAT-inducible expression of siRNA. Nat. Biotechnol. 22, 1573-1578 (2004).
93. Kim, D.H. et al. Interferon induction by siRNAs and ssRNAs synthesized by phage polymerase. Nat. Biotechnol. 22, 321-325 (2004).
94. Lee, Y. et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051-4060 (2004).
95. Amarzguioui, M., Rossi, J.J. & Kim, D. Approaches for chemically synthesized siRNA and vector-mediated RNAi. FEBS Lett. 579, 5974-5981 (2005).
96. Gupta, S., Schoer, R.A., Egan, J.E., Hannon, G.J. & Mittal, V. Inducible, reversible, and stable RNA interference in mammalian cells. Proc. Natl. Acad. Sci. USA 101, 1927-1932 (2004).
97. Gossen, M. et al. Transcriptional activation by tetracyclines in mammalian cells. Science 268, 1766-1769 (1995).
98. No, D., Yao, T.P. & Evans, R.M. Ecdysone-inducible gene expression in mammalian cells and transgenic mice. Proc. Natl. Acad. Sd. USA 93, 3346-3351 (1996).
99. Wang, S. & El-Deiry, W.S. Inducible silencing of KILLER/DR5 in vivo promotes bioluminescent colon tumor xenograft growth and confers resistance to chemotherapeutic agent 5-fluorouracil. Cancer Res. 64, 6666-6672 (2004).
100. Stolarov, J. et al. Design of a retroviral-mediated ecdysone-inducible system and its application to the expression profiling of the PTEN tumor suppressor. Proc. Natl. Acad. Sci. USA 98, 13043-13048 (2001).
101. Czauderna, F. et al. Inducible shRNA expression for application in a prostate cancer mouse model. Nucleic Acids Res. 31, e127 (2003).
102. Heinonen, J.E., Mohamed, A.J., Nore, B.F. & Smith, C.I. Inducible H1 promoter-driven lentiviral siRNA expression by Stuffer reporter deletion. Oligonucleotides 15, 139-144 (2005).
103. Lin, X. et al. Development of a tightly regulated U6 promoter for shRNA expression. FEBS Lett. 577, 376-380 (2004).
104. Matthess, Y. et al. Conditional inhibition of cancer cell proliferation by tetracycline-responsive, H1 promoter-driven silencing of PLK1. Oncogene 24, 2973-2980 (2005).
105. Wiznerowicz, M., Szulc, J. & Trono, D. Tuning silence: Conditional systems for RNA interference. Nat. Methods 3, 682-688 (2006).
106. Janas, J., Skowronski, J. & Van Aelst, L. Lentiviral delivery of RNAi in hippocampal neurons. Methods Enzymol. 406, 593-605 (2006).
107. Li, M.J. et al. Long-term inhibition of HIV-1 infection in primary hematopoietic cells by lentiviral vector delivery of a triple combination of anti-HIV shRNA, anti-CCR5 ribozyme, and a nucleolar-localizing TAR decoy. Mol. Ther. 12, 900-909 (2005).
108. Li, M.J. & Rossi, J.J. Lentiviral vector delivery of recombinant small interfering RNA expression cassettes. Methods Enzymol. 392, 218-226 (2005).