Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Applications of RNA interference-based gene silencing in animal agriculture

Charles R. Long A B , Kimberly J. Tessanne A and Michael C. Golding A

A Department of Veterinary Physiology and Pharmacology, College of Veterinary Medicine and Biological Sciences, Texas A&M University, College Station, TX 77843-4466, USA.

B Corresponding author. Email: clong@cvm.tamu.edu

Reproduction, Fertility and Development 22(1) 47-58 https://doi.org/10.1071/RD09211
Published: 8 December 2009

Abstract

Classical genetic selection, recently aided by genomic selection tools, has been successful in achieving remarkable progress in livestock improvement. However, genetic selection has led to decreased genetic diversity and, in some cases, acquisition of undesirable traits. In order to meet the increased demands of our expanding population, new technologies and practices must be developed that contend with zoonotic and animal disease, environmental impacts of large farming operations and the increased food and fibre production needed to feed and clothe our society. Future increases in productivity may be dependent upon the acquisition of genetic traits not currently encoded by the genomes of animals used in standard agricultural practice, thus making classical genetic selection impossible. Genetic engineering of livestock is commonly used to produce pharmaceuticals or to impart enhanced production characteristics to animals, but has also demonstrated its usefulness in producing animals with disease resistance. However, significant challenges remain because it has been more difficult to produce animals in which specific genes have been removed. It is now possible to modify livestock genomes to block expression of endogenous and exogenous genes (such as those expressed following virus infection). In the present review, we discuss mechanisms of silencing gene expression via the biology of RNA interference (RNAi), the technology of activating the RNAi pathway and the application of this technology to enhance livestock production through increased production efficiency and prevention of disease. An increased demand for sustainable food production is at the forefront of scientific challenges and RNAi technology will undoubtedly play a key role.

Additional keywords: disease resistance, lentivirus, livestock, transgenic.


References

Akkina, R. , Banerjea, A. , Bai, J. , Anderson, J. , Li, M. J. , and Rossi, J. (2003). siRNAs, ribozymes, and RNA decoys in modeling stem cell-based gene therapy for HIV/AIDS. Anticancer Res 23, 1997–2005.
PubMed | |  CAS |

Aravin, A. A. , Hannon, G. J. , and Brennecke, J. (2007a). The Piwi–piRNA pathway provides an adaptive defense in the transposon arms race. Science 318, 761–764.
CrossRef | PubMed | CAS |

Aravin, A. A. , Sachidanandam, R. , Girard, A. , Fejes-Toth, K. , and Hannon, G. J. (2007b). Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316, 744–747.
CrossRef | PubMed | CAS |

Bagga, S. , Bracht, J. , Hunter, S. , Massirer, K. , Holtz, J. , Eachus, R. , and Pasquinelli, A. E. (2005). Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122, 553–563.
CrossRef | PubMed | CAS |

Bernstein, E. , Caudy, A. A. , Hammond, S. M. , and Hannon, G. J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363–366.
CrossRef | PubMed | CAS |

Berry, C. , Thomas, M. , Langley, B. , Sharma, M. , and Kambadur, R. (2002). Single cysteine to tyrosine transition inactivates the growth inhibitory function of Piedmontese myostatin. Am. J. Physiol. Cell Physiol. 283, C135–C141.
PubMed | |  CAS |

Bestor, T. H. (2000). Gene silencing as a threat to the success of gene therapy. J. Clin. Invest. 105, 409–411.
CrossRef | PubMed | CAS |

Blackburn, H. D. (2004). Development of national animal genetic resource programs. Reprod. Fertil. Dev. 16, 27–32.
CrossRef | PubMed | CAS |

Boden, D. , Pusch, O. , Lee, F. , Tucker, L. , and Ramratnam, B. (2003). Human immunodeficiency virus type 1 escape from RNA interference. J. Virol. 77, 11 531–11 535.
CrossRef | PubMed | CAS |

Bogdanovich, S. , Krag, T. O. , Barton, E. R. , Morris, L. D. , Whittemore, L. A. , Ahima, R. S. , and Khurana, T. S. (2002). Functional improvement of dystrophic muscle by myostatin blockade. Nature 420, 418–421.
CrossRef | PubMed | CAS |

Boman, I. A. , Klemetsdal, G. , Blichfeldt, T. , Nafstad, O. , and Vage, D. I. (2009). A frameshift mutation in the coding region of the myostatin gene (MSTN) affects carcass conformation and fatness in Norwegian White Sheep (Ovis aries). Anim. Genet. 40, 418–422.
CrossRef | PubMed | CAS |

Büeler, H. , Aguzzi, A. , Sailer, A. , Greiner, R. A. , Autenried, P. , Aguet, M. , and Weissmann, C. (1993). Mice devoid of PrP are resistant to scrapie. Cell 73, 1339–1347.
CrossRef | PubMed |

Carmell, M. A. , Xuan, Z. , Zhang, M. Q. , and Hannon, G. J. (2002). The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16, 2733–2742.
CrossRef | PubMed | CAS |

Carmell, M. A. , Zhang, L. , Conklin, D. S. , Hannon, G. J. , and Rosenquist, T. A. (2003). Germline transmission of RNAi in mice. Nat. Struct. Biol. 10, 91–92.
CrossRef | PubMed | CAS |

Carninci, P. , Kasukawa, T. , Katayama, S. , Gough, J. , and Frith, M. C. , et al. (2005). The transcriptional landscape of the mammalian genome. Science 309, 1559–1563.
CrossRef | PubMed | CAS |

Carthew, R. W. , and Sontheimer, E. J. (2009). Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642–655.
CrossRef | PubMed | CAS |

Chen, W. , Yan, W. , Du, Q. , Fei, L. , Liu, M. , Ni, Z. , Sheng, Z. , and Zheng, Z. (2004). RNA interference targeting VP1 inhibits foot-and-mouth disease virus replication in BHK-21 cells and suckling mice. J. Virol. 78, 6900–6907.
CrossRef | PubMed | CAS |

Chen, W. , Liu, M. , Jiao, Y. , Yan, W. , and Wei, X. , et al. (2006). Adenovirus-mediated RNA interference against foot-and-mouth disease virus infection both in vitro and in vivo. J. Virol. 80, 3559–3566.
CrossRef | PubMed | CAS |

Chen, M. , Granger, A. J. , Vanbrocklin, M. W. , Payne, W. S. , Hunt, H. , Zhang, H. , Dodgson, J. B. , and Holmen, S. L. (2007). Inhibition of avian leukosis virus replication by vector-based RNA interference. Virology 365, 464–472.
CrossRef | PubMed | CAS |

Chen, M. , Payne, W. S. , Hunt, H. , Zhang, H. , Holmen, S. L. , and Dodgson, J. B. (2008). Inhibition of Marek’s disease virus replication by retroviral vector-based RNA interference. Virology 377, 265–272.
CrossRef | PubMed | CAS |

Chen, M. , Payne, W. S. , Dunn, J. R. , Chang, S. , Zhang, H. M. , Hunt, H. D. , and Dodgson, J. B. (2009). Retroviral delivery of RNA interference against Marek’s disease virus in vivo. Poult. Sci. 88, 1373–1380.
CrossRef | PubMed | CAS |

Clop, A. , Marcq, F. , Takeda, H. , Pirottin, D. , and Tordoir, X. , et al. (2006). A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat. Genet. 38, 813–818.
CrossRef | PubMed | CAS |

Coburn, G. A. , and Cullen, B. R. (2002). Potent and specific inhibition of human immunodeficiency virus type-1 replication by RNA interference. J. Virol. 76, 9225–9231.
CrossRef | PubMed | CAS |

Craigo, J. K. , Sturgeon, T. J. , Cook, S. J. , Issel, C. J. , Leroux, C. , and Montelaro, R. C. (2006). Apparent elimination of EIAV ancestral species in a long-term inapparent carrier. Virology 344, 340–353.
CrossRef | CAS | PubMed |

Das, A. T. , Brummelkamp, T. R. , Westerhout, E. M. , Vink, M. , Madiredjo, M. , Bernards, R. , and Berkhout, B. (2004). Human immunodeficiency virus type 1 escapes from RNA interference-mediated inhibition. J. Virol. 78, 2601–2605.
CrossRef | PubMed | CAS |

Daude, N. , Marella, M. , and Chabry, J. (2003). Specific inhibition of pathological prion protein accumulation by small interfering RNAs. J. Cell Sci. 116, 2775–2779.
CrossRef | PubMed | CAS |

de los Santos, T. , Wu, Q. , de Avila Botton, S. , and Grubman, M. J. (2005). Short hairpin RNA targeted to the highly conserved 2B nonstructural protein coding region inhibits replication of multiple serotypes of foot-and-mouth disease virus. Virology 335, 222–231.
CrossRef | PubMed | CAS |

Denli, A. M. , Tops, B. B. , Plasterk, R. H. , Ketting, R. F. , and Hannon, G. J. (2004). Processing of primary microRNAs by the microprocessor complex. Nature 432, 231–235.
CrossRef | PubMed | CAS |

Denning, C. , Burl, S. , Ainslie, A. , Bracken, J. , and Dinnyes, A. , et al. (2001). Deletion of the α(1,3)galactosyl transferase (GGTA1) gene and the prion protein (PrP) gene in sheep. Nat. Biotechnol. 19, 559–562.
CrossRef | PubMed | CAS |

Dickins, R. A. , Hemann, M. T. , Zilfou, J. T. , Simpson, D. R. , Ibarra, I. , Hannon, G. J. , and Lowe, S. W. (2005). Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat. Genet. 37, 1289–1295.
PubMed | |  CAS |

Dickins, R. A. , McJunkin, K. , Hernando, E. , Premsrirut, P. K. , and Krizhanovsky, V. , et al. (2007). Tissue-specific and reversible RNA interference in transgenic mice. Nat. Genet. 39, 914–921.
CrossRef | PubMed | CAS |

Ding, S. F. , Lombardi, R. , Nazari, R. , and Joshi, S. (2002). A combination anti-HIV-1 gene therapy approach using a single transcription unit that expresses antisense, decoy, and sense RNAs, and transdominant negative mutant Gag and Env proteins. Front. Biosci. 7, a15–a28.
CrossRef | PubMed | CAS |

Elbashir, S. M. , Harborth, J. , Lendeckel, W. , Yalcin, A. , Weber, K. , and Tuschl, T. (2001a). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494–498.
CrossRef | PubMed | CAS |

Elbashir, S. M. , Lendeckel, W. , and Tuschl, T. (2001b). RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 15, 188–200.
CrossRef | PubMed | CAS |

Fire, A. , Xu, S. , Montgomery, M. K. , Kostas, S. A. , Driver, S. E. , and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811.
CrossRef | PubMed | CAS |

Fleury, S. , Simeoni, E. , Zuppinger, C. , Deglon, N. , von Segesser, L. K. , Kappenberger, L. , and Vassalli, G. (2003). Multiply attenuated, self-inactivating lentiviral vectors efficiently deliver and express genes for extended periods of time in adult rat cardiomyocytes in vivo. Circulation 107, 2375–2382.
CrossRef | PubMed | CAS |

Giering, J. C. , Grimm, D. , Storm, T. A. , and Kay, M. A. (2008). Expression of shRNA from a tissue-specific pol II promoter is an effective and safe RNAi therapeutic. Mol. Ther. 16, 1630–1636.
CrossRef | PubMed | CAS |

Golding, M. C. , Long, C. R. , Carmell, M. A. , Hannon, G. J. , and Westhusin, M. E. (2006). Suppression of prion protein in livestock by RNA interference. Proc. Natl Acad. Sci. USA 103, 5285–5290.
CrossRef | PubMed | CAS |

Grimm, D. , Streetz, K. L. , Jopling, C. L. , Storm, T. A. , Pandey, K. , Davis, C. R. , Marion, P. , Salazar, F. , and Kay, M. A. (2006). Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441, 537–541.
CrossRef | PubMed | CAS |

Grubman, M. J. , and Baxt, B. (2004). Foot-and-mouth disease. Clin. Microbiol. Rev. 17, 465–493.
CrossRef | PubMed | CAS |

Guttman, M. , Amit, I. , Garber, M. , French, C. , and Lin, M. F. , et al. (2009). Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223–227.
CrossRef | PubMed | CAS |

Hannon, G. J. (2002). RNA interference. Nature 418, 244–251.
CrossRef | PubMed | CAS |

He, Y. X. , Hua, R. H. , Zhou, Y. J. , Qiu, H. J. , and Tong, G. Z. (2007). Interference of porcine reproductive and respiratory syndrome virus replication on MARC-145 cells using DNA-based short interfering RNAs. Antiviral Res. 74, 83–91.
CrossRef | PubMed | CAS |

Hemann, M. T. , Fridman, J. S. , Zilfou, J. T. , Hernando, E. , Paddison, P. J. , Cordon-Cardo, C. , Hannon, G. J. , and Lowe, S. W. (2003). An epi-allelic series of p53 hypomorphs created by stable RNAi produces distinct tumor phenotypes in vivo. Nat. Genet. 33, 396–400.
CrossRef | PubMed | CAS |

Hickford, J. G. , Forrest, R. H. , and Zhou, H. (2009). Association between a g.+6723G-A SNP in the myostatin gene (MSTN) and carcass traits in New Zealand Texel sheep. J. Anim. Sci. 87, 1856–1864.
CrossRef | PubMed |

Hofmann, A. , Kessler, B. , Ewerling, S. , Weppert, M. , and Vogg, B. , et al. (2003). Efficient transgenesis in farm animals by lentiviral vectors. EMBO Rep. 4, 1054–1058.
CrossRef | PubMed | CAS |

Hofmann, A. , Zakhartchenko, V. , Weppert, M. , Sebald, H. , Wenigerkind, H. , Brem, G. , Wolf, E. , and Pfeifer, A. (2004). Generation of transgenic cattle by lentiviral gene transfer into oocytes. Biol. Reprod. 71, 405–409.
CrossRef | PubMed | CAS |

Hofmann, A. , Kessler, B. , Ewerling, S. , Kabermann, A. , Brem, G. , Wolf, E. , and Pfeifer, A. (2006). Epigenetic regulation of lentiviral transgene vectors in a large animal model. Mol. Ther. 13, 59–66.
CrossRef | CAS | PubMed |

Hu, W. Y. , Myers, C. P. , Kilzer, J. M. , Pfaff, S. L. , and Bushman, F. D. (2002). Inhibition of retroviral pathogenesis by RNA interference. Curr. Biol. 12, 1301–1311.
CrossRef | PubMed | CAS |

Humphreys, D. T. , Westman, B. J. , Martin, D. I. , and Preiss, T. (2005). MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc. Natl Acad. Sci. USA 102, 16 961–16 966.
CrossRef | PubMed | CAS |

Ivanova, N. , Dobrin, R. , Lu, R. , Kotenko, I. , Levorse, J. , DeCoste, C. , Schafer, X. , Lun, Y. , and Lemischka, I. R. (2006). Dissecting self-renewal in stem cells with RNA interference. Nature 442, 533–538.
CrossRef | PubMed | CAS |

Joulia, D. , Bernardi, H. , Garandel, V. , Rabenoelina, F. , Vernus, B. , and Cabello, G. (2003). Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Exp. Cell. Res. 286, 263–275.
CrossRef | CAS | PubMed |

Joyappa, D. H. , Sasi, S. , Ashok, K. C. , Reddy, G. R. , and Suryanarayana, V. V. (2009). The plasmid constructs producing shRNA corresponding to the conserved 3D polymerase of foot and mouth disease virus protects guinea pigs against challenge virus. Vet. Res. Commun. 33, 263–271.
CrossRef | PubMed |

Kahana, R. , Kuznetzova, L. , Rogel, A. , Shemesh, M. , Hai, D. , Yadin, H. , and Stram, Y. (2004). Inhibition of foot-and-mouth disease virus replication by small interfering RNA. J. Gen. Virol. 85, 3213–3217.
CrossRef | PubMed | CAS |

Karlas, A. , Kurth, R. , and Denner, J. (2004). Inhibition of porcine endogenous retroviruses by RNA interference: increasing the safety of xenotransplantation. Virology 325, 18–23.
CrossRef | PubMed | CAS |

Kim, S. M. , Lee, K. N. , Park, J. Y. , Ko, Y. J. , Joo, Y. S. , Kim, H. S. , and Park, J. H. (2008). Therapeutic application of RNA interference against foot-and-mouth disease virus in vitro and in vivo. Antiviral Res. 80, 178–184.
CrossRef | PubMed | CAS |

Kim, V. N. (2005). MicroRNA biogenesis: coordinated cropping and dicing. Nat. Rev. Mol. Cell Biol. 6, 376–385.
CrossRef | PubMed | CAS |

Kolber-Simonds, D. , Lai, L. , Watt, S. R. , Denaro, M. , and Arn, S. , et al. (2004). Production of alpha-1,3-galactosyltransferase null pigs by means of nuclear transfer with fibroblasts bearing loss of heterozygosity mutations. Proc. Natl Acad. Sci. USA 101, 7335–7340.
CrossRef | PubMed | CAS |

Lai, L. , Kolber-Simonds, D. , Park, K.-W. , Cheong, H.-T. , and Greenstein, J. L. , et al. (2002). Production of α-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science 295, 1089–1092.
CrossRef | PubMed | CAS |

Lambeth, L. S. , Moore, R. J. , Muralitharan, M. S. , and Doran, T. J. (2007). Suppression of bovine viral diarrhea virus replication by small interfering RNA and short hairpin RNA-mediated RNA interference. Vet. Microbiol. 119, 132–143.
CrossRef | PubMed | CAS |

Lambeth, L. S. , Zhao, Y. , Smith, L. P. , Kgosana, L. , and Nair, V. (2009). Targeting Marek’s disease virus by RNA interference delivered from a herpesvirus vaccine. Vaccine 27, 298–306.
CrossRef | PubMed | CAS |

Lander, E. S. , Linton, L. M. , Birren, B. , Nusbaum, C. , and Zody, M. C. , et al. (2001). Initial sequencing and analysis of the human genome. Nature 409, 860–921.
CrossRef | PubMed | CAS |

Langley, B. , Thomas, M. , Bishop, A. , Sharma, M. , Gilmour, S. , and Kambadur, R. (2002). Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J. Biol. Chem. 277, 49 831–49 840.
CrossRef | PubMed | CAS |

Lee, N. S. , Dohjima, T. , Bauer, G. , Li, H. , Li, M. J. , Ehsani, A. , Salvaterra, P. , and Rossi, J. (2002). Expression of small interfering RNAs targeted against HIV-1 rev transcripts in human cells. Nat. Biotechnol. 20, 500–505.
PubMed | |  CAS |

Lee, Y. , Ahn, C. , Han, J. , Choi, H. , and Kim, J. , et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419.
CrossRef | PubMed | CAS |

Leroux, C. , Cadore, J. L. , and Montelaro, R. C. (2004). Equine infectious anemia virus (EIAV): what has HIV’s country cousin got to tell us? Vet. Res. 35, 485–512.
CrossRef | PubMed | CAS |

Li, G. , Jiang, P. , Li, Y. , Wang, X. , Huang, J. , Bai, J. , Cao, J. , Wu, B. , Chen, N. , and Zeshan, B. (2009). Inhibition of porcine reproductive and respiratory syndrome virus replication by adenovirus-mediated RNA interference both in porcine alveolar macrophages and swine. Antiviral Res. 82, 157–165.
CrossRef | PubMed | CAS |

Li, M.-J. , Kim, J. , Li, S. , Zaia, J. , Yee, J.-K. , Anderson, J. , Akkina, R. , and Rossi, J. J. (2005a). 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.
CrossRef | PubMed | CAS |

Li, Y. C. , Kong, L. H. , Cheng, B. Z. , and Li, K. S. (2005b). Construction of influenza virus siRNA expression vectors and their inhibitory effects on multiplication of influenza virus. Avian Dis. 49, 562–573.
CrossRef | PubMed |

Liu, J. , Carmell, M. A. , Rivas, F. V. , Marsden, C. G. , Thomson, J. M. , Song, J. J. , Hammond, S. M. , Joshua-Tor, L. , and Hannon, G. J. (2004). Argonaute2 is the catalytic engine of mammalian RNAi. Science 305, 1437–1441.
CrossRef | PubMed | CAS |

Liu, J. , Rivas, F. V. , Wohlschlegel, J. , Yates, J. R. , Parker, R. , and Hannon, G. J. (2005a). A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7, 1261–1266.
CrossRef | PubMed |

Liu, J. , Valencia-Sanchez, M. A. , Hannon, G. J. , and Parker, R. (2005b). MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7, 719–723.
CrossRef | PubMed | CAS |

Liu, M. , Chen, W. , Ni, Z. , Yan, W. , and Fei, L. , et al. (2005c). Cross-inhibition to heterologous foot-and-mouth disease virus infection induced by RNA interference targeting the conserved regions of viral genome. Virology 336, 51–59.
CrossRef | PubMed | CAS |

Lois, C. , Hong, E. J. , Pease, S. , Brown, E. J. , and Baltimore, D. (2002). Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295, 868–872.
CrossRef | PubMed | CAS |

Long, J. A. (2008). Reproductive biotechnology and gene mapping: tools for conserving rare breeds of livestock. Reprod. Domest. Anim. 43(Suppl. 2), 83–88.
CrossRef | PubMed |

Longini, I. M. , Nizam, A. , Xu, S. , Ungchusak, K. , Hanshaoworakul, W. , Cummings, D. A. , and Halloran, M. E. (2005). Containing pandemic influenza at the source. Science 309, 1083–1087.
CrossRef | PubMed | CAS |

Ma, Y. , Creanga, A. , Lum, L. , and Beachy, P. A. (2006). Prevalence of off-target effects in Drosophila RNA interference screens. Nature 443, 359–363.
CrossRef | PubMed | CAS |

Magee, T. R. , Artaza, J. N. , Ferrini, M. G. , Vernet, D. , Zuniga, F. I. , Cantini, L. , Reisz-Porszasz, S. , Rajfer, J. , and Gonzalez-Cadavid, N. F. (2006). Myostatin short interfering hairpin RNA gene transfer increases skeletal muscle mass. J. Gene Med. 8, 1171–1181.
CrossRef | PubMed | CAS |

Malone, C. D. , and Hannon, G. J. (2009). Small RNAs as guardians of the genome. Cell 136, 656–668.
CrossRef | PubMed | CAS |

Mariante Ada, S. , and Egito, A. A. (2002). Animal genetic resources in Brazil: result of five centuries of natural selection. Theriogenology 57, 223–235.
CrossRef | PubMed |

Martinez, J. , and Tuschl, T. (2004). RISC is a 5′ phosphomonoester-producing RNA endonuclease. Genes Dev. 18, 975–980.
CrossRef | PubMed | CAS |

Mason, P. W. , Chinsangaram, J. , Moraes, M. P. , Mayr, G. A. , and Grubman, M. J. (2003a). Engineering better vaccines for foot-and-mouth disease. Dev. Biol. 114, 79–88.
PubMed | |  CAS |

Mason, P. W. , Grubman, M. J. , and Baxt, B. (2003b). Molecular basis of pathogenesis of FMDV. Virus Res. 91, 9–32.
CrossRef | PubMed | CAS |

Mason, P. W. , Pacheco, J. M. , Zhao, Q. Z. , and Knowles, N. J. (2003c). Comparisons of the complete genomes of Asian, African and European isolates of a recent foot-and-mouth disease virus type O pandemic strain (PanAsia). J. Gen. Virol. 84, 1583–1593.
CrossRef | PubMed | CAS |

Matranga, C. , Tomari, Y. , Shin, C. , Bartel, D. P. , and Zamore, P. D. (2005). Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123, 607–620.
CrossRef | PubMed | CAS |

McCaffrey, A. P. , Nakai, H. , Pandey, K. , Huang, Z. , Salazar, F. H. , Xu, H. , Wieland, S. F. , Marion, P. L. , and Kay, M. A. (2003). Inhibition of hepatitis B virus in mice by RNA interference. Nat. Biotechnol. 21, 639–644.
CrossRef | PubMed | CAS |

McPherron, A. C. , and Lee, S. J. (1997). Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl Acad. Sci. USA 94, 12 457–12 461.
CrossRef | PubMed | CAS |

McPherron, A. C. , Lawler, A. M. , and Lee, S. J. (1997). Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387, 83–90.
CrossRef | PubMed | CAS |

Mosher, D. S. , Quignon, P. , Bustamante, C. D. , Sutter, N. B. , Mellersh, C. S. , Parker, H. G. , and Ostrander, E. A. (2007). A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs. PLoS Genet. 3, e79.
CrossRef | PubMed |

Murchison, E. P. , and Hannon, G. J. (2004). miRNAs on the move: miRNA biogenesis and the RNAi machinery. Curr. Opin. Cell Biol. 16, 223–229.
CrossRef | PubMed | CAS |

Napoli, C. , Lemieux, C. , and Jorgensen, R. (1990). Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2, 279–289.
PubMed | |  CAS |

Niemann, H. , and Kues, W. A. (2003). Application of transgenesis in livestock for agriculture and biomedicine. Anim. Reprod. Sci. 79, 291–317.
CrossRef | PubMed | CAS |

Novina, C. D. , Murray, M. F. , Dykxhoorn, D. M. , Beresford, P. J. , Riess, J. , Lee, S.-K. , Collman, R. G. , Lieberman, J. , Shankar, P. , and Sharp, P. A. (2002). siRNA-directed inhibition of HIV-1 infection. Nat. Med. 8, 681–686.
PubMed | |  CAS |

Okamura, K. , Hagen, J. W. , Duan, H. , Tyler, D. M. , and Lai, E. C. (2007). The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130, 89–100.
CrossRef | PubMed | CAS |

Paddison, P. J. , and Hannon, G. J. (2003). siRNAs and shRNAs: skeleton keys to the human genome. Curr. Opin. Mol. Ther. 5, 217–224.
PubMed | |  CAS |

Paddison, P. J. , Caudy, A. A. , Bernstein, E. , Hannon, G. J. , and Conklin, D. S. (2002a). Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cells. Genes Dev. 16, 948–958.
CrossRef | PubMed | CAS |

Paddison, P. J. , Caudy, A. A. , and Hannon, G. J. (2002b). Stable suppression of gene expression by RNAi in mammalian cells. Proc. Natl Acad. Sci. USA 99, 1443–1448.
CrossRef | PubMed | CAS |

Paddison, P. J. , Silva, J. M. , Conklin, D. S. , Schlabach, M. , and Li, M. , et al. (2004). A resource for large-scale RNA-interference-based screens in mammals. Nature 428, 427–431.
CrossRef | PubMed | CAS |

Patel, K. , and Amthor, H. (2005). The function of myostatin and strategies of myostatin blockade: new hope for therapies aimed at promoting growth of skeletal muscle. Neuromuscul. Disord. 15, 117–126.
CrossRef | PubMed | CAS |

Patel, K. , Macharia, R. , and Amthor, H. (2005). Molecular mechanisms involving IGF-1 and myostatin to induce muscle hypertrophy as a therapeutic strategy for Duchenne muscular dystrophy. Acta Myol. 24, 230–241.
PubMed | |  CAS |

Pawliuk, R. , Bachelot, T. , Raftopoulos, H. , Kalberer, C. , Humphries, R. K. , Bank, A. , and Leboulch, P. (1998). Retroviral vectors aimed at the gene therapy of human beta-globin gene disorders. Ann. N. Y. Acad. Sci. 850, 151–162.
CrossRef | PubMed | CAS |

Pfeifer, A. (2006). Lentivector-mediated RNAi efficiently suppresses prion protein and prolongs survival of scrapie-infected mice. J. Clin. Invest. 116, 3204–3210.
CrossRef | PubMed | CAS |

Phelps, C. J. , Koike, C. , Vaught, T. D. , Boone, J. , and Wells, K. D. , et al. (2003). Production of α1,3-galactosyltransferase-deficient pigs. Science 299, 411–414.
CrossRef | PubMed | CAS |

Pillai, R. S. , Bhattacharyya, S. N. , Artus, C. G. , Zoller, T. , Cougot, N. , Basyuk, E. , Bertrand, E. , and Filipowicz, W. (2005). Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309, 1573–1576.
CrossRef | PubMed | CAS |

Prelle, K. , Zink, N. , and Wolf, E. (2002). Pluripotent stem cells: model of embryonic development, tool for gene targeting, and basis of cell therapy. Anat. Histol. Embryol. 31, 169–186.
CrossRef | PubMed |

Ramsoondar, J. , Vaught, T. , Ball, S. , Mendicino, M. , Monahan, J. , Jobst, P. , Vance, A. , Duncan, J. , Wells, K. , and Ayares, D. (2009). Production of transgenic pigs that express porcine endogenous retrovirus small interfering RNAs. Xenotransplantation 16, 164–180.
CrossRef | PubMed |

Richt, J. A. , Kasinathan, P. , Hamir, A. N. , Castilla, J. , and Sathiyaseelan, T. , et al. (2007). Production of cattle lacking prion protein. Nat. Biotechnol. 25, 132–138.
CrossRef | PubMed | CAS |

Rios, R. , Carneiro, I. , Arce, V. M. , and Devesa, J. (2001). Myostatin regulates cell survival during C2C12 myogenesis. Biochem. Biophys. Res. Commun. 280, 561–566.
CrossRef | CAS | PubMed |

Rossi, J. J. (2008). Expression strategies for short hairpin RNA interference triggers. Hum. Gene Ther. 19, 313–317.
CrossRef | PubMed | CAS |

Rossi, J. , Zamore, P. , and Kay, M. A. (2008). Wandering eye for RNAi. Nat. Med. 14, 611.
CrossRef | PubMed |

Ruby, J. G. , Jan, C. H. , and Bartel, D. P. (2007). Intronic microRNA precursors that bypass Drosha processing. Nature 448, 83–86.
CrossRef | PubMed | CAS |

Sailer, A. , Bueler, H. , Fischer, M. , Aguzzi, A. , and Weissmann, C. (1994). No propagation of prions in mice devoid of PrP. Cell 77, 967–968.
CrossRef | PubMed | CAS |

Schuelke, M. , Wagner, K. R. , Stolz, L. E. , Hubner, C. , Riebel, T. , Komen, W. , Braun, T. , Tobin, J. F. , and Lee, S. J. (2004). Myostatin mutation associated with gross muscle hypertrophy in a child. N. Engl. J. Med. 350, 2682–2688.
CrossRef | PubMed | CAS |

Schwarz, D. S. , Hutvagner, G. , Du, T. , Xu, Z. , Aronin, N. , and Zamore, P. D. (2003). Asymmetry in the assembly of the RNAi enzyme complex. Cell 115, 199–208.
CrossRef | PubMed | CAS |

Shen, P. C. , Lee, S. N. , Wu, J. S. , Huang, J. C. , and Chu, F. H. , et al. (2006). The effect of electrical field strength on activation and development of cloned caprine embryos. Anim. Reprod. Sci. 92, 310–320.
CrossRef | PubMed | CAS |

Shi, X. J. , Wang, B. , and Wang, M. (2007). Immune enhancing effects of recombinant bovine IL-18 on foot-and-mouth disease vaccination in mice model. Vaccine 25, 1257–1264.
CrossRef | PubMed | CAS |

Shibata, M. , Matsumoto, K. , Aikawa, K. , Muramoto, T. , Fujimura, S. , and Kadowaki, M. (2006). Gene expression of myostatin during development and regeneration of skeletal muscle in Japanese Black Cattle. J. Anim. Sci. 84, 2983–2989.
CrossRef | PubMed | CAS |

Silva, J. M. , Li, M. Z. , Chang, K. , Ge, W. , and Golding, M. C. , et al. (2005). Second-generation shRNA libraries covering the mouse and human genomes. Nat. Genet. 37, 1281–1288.
PubMed | |  CAS |

Silva, J. M. , Marran, K. , Parker, J. S. , Silva, J. , Golding, M. , Schlabach, M. R. , Elledge, S. J. , Hannon, G. J. , and Chang, K. (2008). Profiling essential genes in human mammary cells by multiplex RNAi screening. Science 319, 617–620.
CrossRef | PubMed | CAS |

Singer, O. , and Verma, I. M. (2008). Applications of lentiviral vectors for shRNA delivery and transgenesis. Curr. Gene Ther. 8, 483–488.
CrossRef | PubMed | CAS |

Song, J. J. , Smith, S. K. , Hannon, G. J. , and Joshua-Tor, L. (2004). Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305, 1434–1437.
CrossRef | PubMed | CAS |

Stegmeier, F. , Hu, G. , Rickles, R. J. , Hannon, G. J. , and Elledge, S. J. (2005). A lentiviral microRNA-based system for single-copy polymerase II-regulated RNA interference in mammalian cells. Proc. Natl Acad. Sci. USA 102, 13 212–13 217.
CrossRef | PubMed | CAS |

Tam, O. H. , Aravin, A. A. , Stein, P. , Girard, A. , and Murchison, E. P. , et al. (2008). Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453, 534–538.
CrossRef | PubMed | CAS |

The Bovine HapMap Consortium (2009). Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science 324, 528–532.
CrossRef | PubMed |

Thomas, M. , Langley, B. , Berry, C. , Sharma, M. , Kirk, S. , Bass, J. , and Kambadur, R. (2000). Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J. Biol. Chem. 275, 40 235–40 243.
CrossRef | PubMed | CAS |

Ting, A. H. , Schuebel, K. E. , Herman, J. G. , and Baylin, S. B. (2005). Short double-stranded RNA induces transcriptional gene silencing in human cancer cells in the absence of DNA methylation. Nat. Genet. 37, 906–910.
CrossRef | PubMed | CAS |

Tomari, Y. , and Zamore, P. D. (2005). Perspective: machines for RNAi. Genes Dev. 19, 517.
CrossRef | PubMed | CAS |

Tuschl, T. , Zamore, P. D. , Lehmann, R. , Bartel, D. P. , and Sharp, P. A. (1999). Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev. 13, 3191–3197.
CrossRef | PubMed | CAS |

Walsh, F. S. , and Celeste, A. J. (2005). Myostatin: a modulator of skeletal-muscle stem cells. Biochem. Soc. Trans. 33, 1513–1517.
CrossRef | PubMed | CAS |

Wang, B. , and Zhou, J. (2003). Specific genetic modifications of domestic animals by gene targeting and animal cloning. Reprod. Biol. Endocrinol. 1, 103.
CrossRef | PubMed | CAS |

Wang, Y. , Sun, H. , Shen, P. , Zhang, X. , and Xia, X. (2009). Effective inhibition of infectious bursal disease virus replication by recombinant avian adeno-associated virus-delivered microRNAs. J. Gen. Virol. 90, 1417–1422.
CrossRef | PubMed | CAS |

Watanabe, T. , Takeda, A. , Tsukiyama, T. , Mise, K. , Okuno, T. , Sasaki, H. , Minami, N. , and Imai, H. (2006). Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev. 20, 1732–1743.
CrossRef | PubMed | CAS |

Watanabe, T. , Totoki, Y. , Toyoda, A. , Kaneda, M. , and Kuramochi-Miyagawa, S. , et al. (2008). Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453, 539–543.
CrossRef | PubMed | CAS |

Weissmann, C. (1994). Molecular biology of prion diseases. Trends Cell Biol. 4, 10–14.
CrossRef | PubMed | CAS |

Welle, S. , Cardillo, A. , Zanche, M. , and Tawil, R. (2009). Skeletal muscle gene expression after myostatin knockout in mature mice. Physiol. Genomics 38, 342–350.
CrossRef | PubMed |

White, M. D. , Farmer, M. , Mirabile, I. , Brandner, S. , Collinge, J. , and Mallucci, G. R. (2008). Single treatment with RNAi against prion protein rescues early neuronal dysfunction and prolongs survival in mice with prion disease. Proc. Natl Acad. Sci. USA 105, 10 238–10 243.
CrossRef | PubMed | CAS |

Whitelaw, C. B. A. , Radcliffe, P. A. , Ritchie, W. A. , Carlisle, A. , Ellard, F. M. , Pena, R. N. , Rowe, J. , Clark, A. J. , King, T. J. , and Mitrophanous, K. A. (2004). Efficient generation of transgenic pigs using equine infectious anaemia virus (EIAV) derived vector. FEBS Lett. 571, 233–236.
CrossRef | PubMed | CAS |

Wise, T. G. , Schafer, D. S. , Lowenthal, J. W. , and Doran, T. J. (2008). The use of RNAi and transgenics to develop viral disease resistant livestock. Dev. Biol. 132, 377–382.
PubMed | |  CAS |

Zhou, K. , He, H. , Wu, Y. , and Duan, M. (2008). RNA interference of avian influenza virus H5N1 by inhibiting viral mRNA with siRNA expression plasmids. J. Biotechnol. 135, 140–144.
CrossRef | PubMed | CAS |



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