The cellular processing capacity limits the amounts of chimeric U7 snRNA available for antisense delivery

Molecular Therapy Nucleic Acids

Volumn 1, Issue 6, 2012, Pages e31-

  Eckenfelder, Agathe ^a   Tordo, Julie ^a,b   Babbs, Arran ^c   Davies, Kay E ^c   Goyenvalle, Aurélie ^a,c   Danos, Olivier ^a,b  

^a INSERM   (France)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Antisense; Dystrophin; Exon skipping; U7snRNA

Indexed keywords

EID: 84868377903     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2012.24     Document Type: Article

References (37)

1. Tuck, AC and Tollervey, D (2011). RNA in pieces. Trends Genet 27: 422-432.
2. Buratti, E, Baralle, M and Baralle, FE (2006). Defective splicing, disease and therapy: searching for master checkpoints in exon definition. Nucleic Acids Res 34: 3494-3510.
3. Wang, ET, Sandberg, R, Luo, S, Khrebtukova, I, Zhang, L, Mayr, C et al. (2008). Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476. (Pubitemid 352759009)
4. Tazi, J, Durand, S and Jeanteur, P (2005). The spliceosome: a novel multi-faceted target for therapy. Trends Biochem Sci 30: 469-478. (Pubitemid 41033243)
5. Hammond, SM and Wood, MJ (2011). Genetic therapies for RNA mis-splicing diseases. Trends Genet 27: 196-205.
6. Kinali, M, Arechavala-Gomeza, V, Feng, L, Cirak, S, Hunt, D, Adkin, C et al. (2009). Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol 8: 918-928.
7. van Deutekom, JC, Janson, AA, Ginjaar, IB, Frankhuizen, WS, Aartsma-Rus, A, Bremmer- Bout, M et al. (2007). Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 357: 2677-2686.
8. Goemans, NM, Tulinius, M, van den Akker, JT, Burm, BE, Ekhart, PF, Heuvelmans, N et al. (2011). Systemic administration of PRO051 in Duchenne's muscular dystrophy. N Engl J Med 364: 1513-1522.
9. Cirak, S, Arechavala-Gomeza, V, Guglieri, M, Feng, L, Torelli, S, Anthony, K et al. (2011). Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study. Lancet 378: 595-605.
10. Gorman, L, Suter, D, Emerick, V, Schümperli, D and Kole, R (1998). Stable alteration of pre-mRNA splicing patterns by modified U7 small nuclear RNAs. Proc Natl Acad Sci USA 95: 4929-4934. (Pubitemid 28208527)
11. Gorman, L, Mercatante, DR and Kole, R (2000). Restoration of correct splicing of thalassemic beta-globin pre-mRNA by modified U1 snRNAs. J Biol Chem 275: 35914-35919.
12. De Angelis, FG, Sthandier, O, Berarducci, B, Toso, S, Galluzzi, G, Ricci, E et al. (2002). Chimeric snRNA molecules carrying antisense sequences against the splice junctions of exon 51 of the dystrophin pre-mRNA induce exon skipping and restoration of a dystrophin synthesis in Delta 48-50 DMD cells. Proc Natl Acad Sci USA 99: 9456-9461. (Pubitemid 34764635)
13. Goyenvalle, A, Vulin, A, Fougerousse, F, Leturcq, F, Kaplan, JC, Garcia, L et al. (2004). Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 306: 1796-1799. (Pubitemid 39601401)
14. Goyenvalle, A, Babbs, A, Wright, J, Wilkins, V, Powell, D, Garcia, L et al. (2012). Rescue of severely affected dystrophin/utrophin-deficient mice through scAAV-U7snRNA-mediated exon skipping. Hum Mol Genet 21: 2559-2571.
15. Bish, LT, Sleeper, MM, Forbes, SC, Wang, B, Reynolds, C, Singletary, GE et al. (2012). Long-term restoration of cardiac dystrophin expression in golden retriever muscular dystrophy following rAAV6-mediated exon skipping. Mol Ther 20: 580-589.
16. Vaillend, C, Perronnet, C, Ros, C, Gruszczynski, C, Goyenvalle, A, Laroche, S et al. (2010). Rescue of a dystrophin-like protein by exon skipping in vivo restores GABAAreceptor clustering in the hippocampus of the mdx mouse. Mol Ther 18: 1683-1688.
17. Baillat, D, Hakimi, MA, Näär, AM, Shilatifard, A, Cooch, N and Shiekhattar, R (2005). Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell 123: 265-276. (Pubitemid 41457216)
18. Patel, SB and Bellini, M (2008). The assembly of a spliceosomal small nuclear ribonucleoprotein particle. Nucleic Acids Res 36: 6482-6493.
19. Grimm, C, Stefanovic, B and Schümperli, D (1993). The low abundance of U7 snRNA is partly determined by its Sm binding site. EMBO J 12: 1229-1238. (Pubitemid 23095872)
20. Brun, C, Suter, D, Pauli, C, Dunant, P, Lochmüller, H, Burgunder, JM et al. (2003). U7 snRNAs induce correction of mutated dystrophin pre-mRNA by exon skipping. Cell Mol Life Sci 60: 557-566. (Pubitemid 36459534)
21. Salva, MZ, Himeda, CL, Tai, PW, Nishiuchi, E, Gregorevic, P, Allen, JM et al. (2007). Design of tissue-specific regulatory cassettes for high-level rAAV-mediated expression in skeletal and cardiac muscle. Mol Ther 15: 320-329. (Pubitemid 46111882)
22. Aartsma-Rus, A, Bremmer-Bout, M, Janson, AA, den Dunnen, JT, van Ommen, GJ and van Deutekom, JC (2002). Targeted exon skipping as a potential gene correction therapy for Duchenne muscular dystrophy. Neuromuscul Disord 12 Suppl 1: S71-S77. (Pubitemid 36158776)
23. Vincent-Lacaze, N, Snyder, RO, Gluzman, R, Bohl, D, Lagarde, C and Danos, O (1999). Structure of adeno-associated virus vector DNA following transduction of the skeletal muscle. J Virol 73: 1949-1955. (Pubitemid 29098096)
24. Bartlett, JS, Sethna, M, Ramamurthy, L, Gowen, SA, Samulski, RJ and Marzluff, WF (1996). Efficient expression of protein coding genes from the murine U1 small nuclear RNA promoters. Proc Natl Acad Sci USA 93: 8852-8857. (Pubitemid 26281980)
25. Phillips, SC and Turner, PC (1992). A transcriptional analysis of the gene encoding mouse U7 small nuclear RNA. Gene 116: 181-186.
26. Bojak, A, Hammer, D, Wolf, H and Wagner, R (2002). Muscle specific versus ubiquitous expression of Gag based HIV-1 DNA vaccines: a comparative analysis. Vaccine 20: 1975-1979. (Pubitemid 34450796)
27. Nakai, H, Thomas, CE, Storm, TA, Fuess, S, Powell, S, Wright, JF et al. (2002). A limited number of transducible hepatocytes restricts a wide-range linear vector dose response in recombinant adeno-associated virus-mediated liver transduction. J Virol 76: 11343-11349. (Pubitemid 35231289)
28. Azzouz, TN and Schumperli, D (2003). Evolutionary conservation of the U7 small nuclear ribonucleoprotein in Drosophila melanogaster. RNA 9: 1532-1541. (Pubitemid 37463478)
29. Suter, D, Tomasini, R, Reber, U, Gorman, L, Kole, R and Schümperli, D (1999). Doubletarget antisense U7 snRNAs promote efficient skipping of an aberrant exon in three human beta-thalassemic mutations. Hum Mol Genet 8: 2415-2423.
30. Seipelt, RL, Zheng, B, Asuru, A and Rymond, BC (1999). U1 snRNA is cleaved by RNase III and processed through an Sm site-dependent pathway. Nucleic Acids Res 27: 587-595. (Pubitemid 29210027)
31. Ezzeddine, N, Chen, J, Waltenspiel, B, Burch, B, Albrecht, T, Zhuo, M et al. (2011). A subset of Drosophila integrator proteins is essential for efficient U7 snRNA and spliceosomal snRNA 3'-end formation. Mol Cell Biol 31: 328-341.
32. VandenDriessche, T, Naldini, L, Collen, D and Chuah, MK (2002). Oncoretroviral and lentiviral vector-mediated gene therapy. Meth Enzymol 346: 573-589. (Pubitemid 41103160)
33. Nathwani, AC, Gray, JT, McIntosh, J, Ng, CY, Zhou, J, Spence, Y et al. (2007). Safe and efficient transduction of the liver after peripheral vein infusion of self-complementary AAV vector results in stable therapeutic expression of human FIX in nonhuman primates. Blood 109: 1414-1421. (Pubitemid 46239572)
34. Naldini, L, Blömer, U, Gallay, P, Ory, D, Mulligan, R, Gage, FH et al. (1996). In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267. (Pubitemid 26119138)
35. Allay, JA, Sleep, S, Long, S, Tillman, DM, Clark, R, Carney, G et al. (2011). Good manufacturing practice production of self-complementary serotype 8 adeno-associated viral vector for a hemophilia B clinical trial. Hum Gene Ther 22: 595-604.
36. Allocca, M, Doria, M, Petrillo, M, Colella, P, Garcia-Hoyos, M, Gibbs, D et al. (2008). Serotype-dependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J Clin Invest 118: 1955-1964. (Pubitemid 351632397)
37. Herson, S, Hentati, F, Rigolet, A, Behin, A, Romero, NB, Leturcq, F et al. (2012). A phase I trial of adeno-associated virus serotype 1-γ-Sarcoglycan gene therapy for limb girdle muscular dystrophy type 2C. Brain 135(Pt 2): 483-492.