Constitutive expression of short hairpin RNA in vivo triggers buildup of mature hairpin molecules

Human Gene Therapy

Volumn 22, Issue 12, 2011, Pages 1483-1497

  Ahn, M ^a   Witting, S R ^a   Ruiz, R ^a   Saxena, R ^a   Morral, N ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; EXPORTIN 5; INTERFERON; SHORT HAIRPIN RNA; VIRUS DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; IN VIVO STUDY; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; VIRUS PARTICLE;

ANIMALS; BIOLOGICAL MARKERS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELLS, CULTURED; FATTY ACID-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE SILENCING; GENETIC VECTORS; HEPATOCYTES; LIVER; MALE; MICE; MICE, INBRED C57BL; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSDUCTION, GENETIC;

EID: 83455169276     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2010.234     Document Type: Article

References (55)

1. Aliyari, R., and Ding, S.W. (2009). RNA-based viral immunity initiated by the Dicer family of host immune receptors. Immunol. Rev. 227, 176-188.
2. Baillat, D., and Shiekhattar, R. (2009). Functional dissection of the human TNRC6 (GW182-related) family of proteins. Mol. Cell Biol. 29, 4144-4155.
3. Banerjee, S., Neveu, P., Kosik, K.S. (2009). A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 64, 871-884.
4. Behm-Ansmant, I., Rehwinkel, J., Doerks, T., et al. (2006). mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 20, 1885-1898. (Pubitemid 44079326)
5. Boudreau, R.L., McBride, J.L., Martins, I., et al. (2009). Nonallele-specific silencing of mutant and wild-type huntingtin demonstrates therapeutic efficacy in Huntington's disease mice. Mol. Ther. 17, 1053-1063.
6. Brummelkamp, T.R., Bernards, R., and Agami, R. (2002). A system for stable expression of short interfering RNAs in mammalian cells. Science 296, 550-553. (Pubitemid 34408678)
7. Castanotto, D., Sakurai, K., Lingeman, R., et al. (2007). Combinatorial delivery of small interfering RNAs reduces RNAi efficacy by selective incorporation into RISC. Nucleic Acids Res. 35, 5154-5164. (Pubitemid 47394199)
8. Chen, C.C., Ko, T.M., Ma, H.I., et al. (2007). Long-term inhibition of hepatitis B virus in transgenic mice by double-stranded adeno-associated virus 8-delivered short hairpin RNA. Gene Ther. 14, 11-19.
9. Chendrimada, T.P., Finn, K.J., Ji, X., et al. (2007). MicroRNA silencing through RISC recruitment of eIF6. Nature 447, 823-828. (Pubitemid 46920131)
10. Colombo, R., and Moll, J. (2008). Target validation to biomarker development: Focus on RNA interference. Mol. Diagn. Ther. 12, 63-70. (Pubitemid 351570861)
11. Diederichs, S., Jung, S., Rothenberg, S.M., et al. (2008). Coex-pression of Argonaute-2 enhances RNA interference toward perfect match binding sites. Proc. Natl. Acad. Sci. U.S.A. 105, 9284-9289.
12. Ding, L., and Han, M. (2007). GW182 family proteins are crucial for microRNA-mediated gene silencing. Trends Cell Biol. 17, 411-416. (Pubitemid 47375102)
13. Gabel, H.W., and Ruvkun, G. (2008). The exonuclease ERI-1 has a conserved dual role in 5.8S rRNA processing and RNAi. Nat. Struct. Mol. Biol. 15, 531-533. (Pubitemid 351653584)
14. 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.
15. Gregory, R.I., Chendrimada, T.P., Cooch, N., and Shiekhattar, R. (2005). Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123, 631-640. (Pubitemid 41608466)
16. Grimm, D., and Kay, M.A. (2006). Therapeutic short hairpin RNA expression in the liver: Viral targets and vectors. Gene Ther. 13, 563-575.
17. Grimm, D., Streetz, K.L., Jopling, C.L., et al. (2006). Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441, 537-541. (Pubitemid 44050158)
18. Grimm, D., Wang, L., Lee, J.S., et al. (2010). Argonaute proteins are key determinants of RNAi efficacy, toxicity, and persistence in the adult mouse liver. J. Clin. Invest. 120, 3106-3119.
19. Hegenbarth, S., Gerolami, R., Protzer, U., et al. (2000). Liver sinusoidal endothelial cells are not permissive for adenovirus type 5. Hum. Gene Ther. 11, 481-486. (Pubitemid 30101957)
20. Hong, J., Qian, Z., Shen, S., et al. (2005). High doses of siRNAs induce eri-1 and adar-1 gene expression and reduce the efficiency of RNA interference in the mouse. Biochem. J. 390, 675-679. (Pubitemid 41395349)
21. Hu, P.F., Chen, H., Zhong, W., et al. (2009). Adenovirus-mediated transfer of siRNA against PAI-1 mRNA ameliorates hepatic fibrosis in rats. J. Hepatol. 51, 102-113.
22. Huang, D.W., Sherman, B.T., and Lempicki, R.A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
23. Hutvagner, G., and Zamore, P.D. (2002). A microRNA in a multiple-turnover RNAi enzyme complex. Science 297, 2056-2060.
24. Inagaki, Y., Kushida, M., Higashi, K., et al. (2005). Cell type-specific intervention of transforming growth factor b/Smad signaling suppresses collagen gene expression and hepatic fi-brosis in mice. Gastroenterology 129, 259-268. (Pubitemid 41002059)
25. Khan, A.A., Betel, D., Miller, M.L., et al. (2009). Transfection of small RNAs globally perturbs gene regulation by endogenous microRNAs. Nat. Biotechnol. 27, 549-555.
26. Lipardi, C., and Paterson, B.M. (2009). Identification of an RNA-dependent RNA polymerase in Drosophila involved in RNAi and transposon suppression. Proc. Natl. Acad. Sci. U.S.A. 106, 15645-15650.
27. Liu, J., Carmell, M.A., Rivas, F.V., et al. (2004). Argonaute2 is the catalytic engine of mammalian RNAi. Science 305, 1437-1441. (Pubitemid 39167657)
28. Lu, S., and Cullen, B.R. (2004). Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and microRNA biogenesis. J. Virol. 78, 12868-12876. (Pubitemid 39507795)
29. Matranga, C., Tomari, Y., Shin, C., et al. (2005). Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123, 607-620. (Pubitemid 41608464)
30. McBride, J.L., Boudreau, R.L., Harper, S.Q., et al. (2008). Artificial miRNAs mitigate shRNA-mediated toxicity in the brain: Implications for the therapeutic development of RNAi. Proc. Natl. Acad. Sci. U.S.A. 105, 5868-5873. (Pubitemid 351758464)
31. McCaffrey, A.P., Meuse, L., Pham, T.T., et al. (2002). RNA interference in adult mice. Nature 418, 38-39. (Pubitemid 34742563)
32. McIntyre, G.J., and Fanning, G.C. (2006). Design and cloning strategies for constructing shRNA expression vectors. BMC Biotechnol. 6, 1.
33. Meister, G., Landthaler, M., Peters, L., et al. (2005). Identification of novel Argonaute-associated proteins. Curr. Biol. 15, 2149-2155. (Pubitemid 41739749)
34. Morral, N., O'Neal, W., Zhou, H., et al. (1997). Immune responses to reporter proteins and high viral dose limit duration of expression with adenoviral vectors: Comparison of E2a wild type and E2a deleted vectors. Hum. Gene Ther. 8, 1275-1286. (Pubitemid 27394135)
35. Morral, N., Parks, R., Zhou, H., et al. (1998). High doses of a helper-dependent adenoviral vector yield supraphysiological levels of a1-antitrypsin with negligible toxicity. Hum. Gene Ther. 9, 2709-2716. (Pubitemid 29027014)
36. Morral, N., O'Neal, W., Rice, K., et al. (1999). Administration of helper-dependent adenoviral vectors and sequential delivery of different vector serotype for long-term liver-directed gene transfer in baboons. Proc. Natl. Acad. Sci. U.S.A. 96, 12816-12821. (Pubitemid 29513585)
37. Narvaiza, I., Aparicio, O., Vera, M., et al. (2006). Effect of adenovirus-mediated RNA interference on endogenous microRNAs in a mouse model of multidrug resistance protein 2 gene silencing. J. Virol. 80, 12236-12247. (Pubitemid 44904374)
38. O'Neal, W.K., Zhou, H., Morral, N., et al. (2000). Toxicity associated with repeated administration of first-generation ade-novirus vectors does not occur with a helper-dependent vector. Mol. Med. 6, 179-195.
39. Oh, S.H., Hatch, H.M., and Petersen, B.E. (2002). Hepatic oval "stem" cell in liver regeneration. Semin. Cell Dev. Biol. 13, 405-4009.
40. Parks, R.J., Chen, L., Anton, M., et al. (1996). A helper-dependent adenovirus vector system: Removal of helper virus by Cre-mediated excision of the viral packaging signal. Proc. Natl. Acad. Sci. U.S.A. 93, 13565-13570. (Pubitemid 26424159)
41. Persengiev, S.P., Zhu, X., and Green, M.R. (2004). Nonspecific, concentration-dependent stimulation and repression of mammalian gene expression by small interfering RNAs (siRNAs). RNA 10, 12-18. (Pubitemid 38018731)
42. Reynolds, A., Anderson, E.M., Vermeulen, A., et al. (2006). Induction of the interferon response by siRNA is cell type-and duplex length-dependent. RNA 12, 988-993. (Pubitemid 43788117)
43. Robbins, M., Judge, A., Ambegia, E., et al. (2008). Misinterpreting the therapeutic effects of small interfering RNA caused by immune stimulation. Hum. Gene Ther. 19, 991-999.
44. Ruiz, R., Witting, S.R., Saxena, R., and Morral, N. (2009). Robust hepatic gene silencing for functional studies using helper-dependent adenovirus vectors. Hum. Gene Ther. 20, 87-94.
45. Schiedner, G., Morral, N., Parks, R., et al. (1998). Genomic DNA transfer with a high-capacity adenovirus vector results in improved in vivo gene expression and decreased toxicity. Nat. Genet. 18, 180-183. (Pubitemid 28082470)
46. Sledz, C.A., and Williams, B.R. (2004). RNA interference and double-stranded-RNA-activated pathways. Biochem. Soc. Trans. 32, 952-956. (Pubitemid 39655513)
47. 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. (Pubitemid 39167656)
48. Stratford-Perricaudet, L.D., Levrero, M., Chase, J.F., et al. (1990). Evaluation of the transfer and expression in mice of an enzyme-encoding gene using a human adenovirus vector. Hum. Gene Ther. 1, 241-256. (Pubitemid 120034730)
49. Taniguchi, C.M., Ueki, K., and Kahn, R. (2005). Complementary roles of IRS-1 and IRS-2 in the hepatic regulation of metabolism. J. Clin. Invest. 115, 718-727. (Pubitemid 40322247)
50. Terenzi, F., Hui, D.J., Merrick, W.C., and Sen, G.C. (2006). Distinct induction patterns and functions of two closely related interferon-inducible human genes, ISG54 and ISG56. J. Biol. Chem. 281, 34064-34071. (Pubitemid 46036616)
51. Wheeler, M.D., Yamashina, S., Froh, M., et al. (2001). Adenoviral gene delivery can inactivate Kupffer cells: Role of oxidants in NF-jB activation and cytokine production. J. Leukoc. Biol. 69, 622-630. (Pubitemid 32297611)
52. Witting, S.R., Brown, M., Saxena, R., et al. (2008). Helper-dependent adenovirus-mediated short hairpin RNA expression in the liver activates the interferon response. J. Biol. Chem. 283, 2120-2128.
53. Xia, H., Mao, Q., Paulson, H.L., and Davidson, B.L. (2002). siRNA-mediated gene silencing in vitro and in vivo. Nat. Bio-technol. 20, 1006-1010.
54. Yang, Y., Li, Q., Ertl, H.C., and Wilson, J.M. (1994). Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc. Natl. Acad. Sci. U.S.A. 91, 4407-4411. (Pubitemid 24143442)
55. Zhou, Y., Santoro, R., and Grummt, I. (2002). The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J. 21, 4632-4640. (Pubitemid 34984350)