Repair of Mybpc3 mRNA by 5′-trans-splicing in a mouse model of hypertrophic cardiomyopathy

Molecular Therapy Nucleic Acids

Volumn 2, Issue , 2013, Pages

  Mearini, Giulia ^a,b   Stimpel, Doreen ^a,b   Krämer, Elisabeth ^a,b   Geertz, Birgit ^a,b   Braren, Ingke ^a,b   Gedicke Hornung, Christina ^a,b   Précigout, Guillaume ^c   Müller, Oliver J ^b,d   Katus, Hugo A ^b,d   Eschenhagen, Thomas ^a,b   Voit, Thomas ^c   Garcia, Luis ^c   Lorain, Stéphanie ^c   Carrier, Lucie ^a,b,c  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c Sorbonne Université   (France)

^d UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

hypertrophic cardiomyopathy; Mybpc3; RNA based therapy; trans splicing

Indexed keywords

MESSENGER RNA;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; DNA SEQUENCE; GENE MUTATION; HEART MUSCLE CELL; HYPERTROPHIC CARDIOMYOPATHY; IMMUNOPRECIPITATION; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SARCOMERE; TRANS SPLICING; WILD TYPE;

EID: 84880084828     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2013.31     Document Type: Article

References (41)

1. Wally, V, Murauer, EM and Bauer, JW (2012). Spliceosome-mediated trans-splicing: the therapeutic cut and paste. J Invest Dermatol 132: 1959-1966.
2. Mitchell, LG and McGarrity, GJ (2005). Gene therapy progress and prospects: reprograming gene expression by trans-splicing. Gene Ther 12: 1477-1485. (Pubitemid 41508672)
3. Le Roy, F, Charton, K, Lorson, CL and Richard, I (2009). RNA-targeting approaches for neuromuscular diseases. Trends Mol Med 15: 580-591.
4. Mansfeld, SG, Chao, H and Walsh, CE (2004). RNA repair using spliceosome-mediated RNA trans-splicing. Trends Mol Med 10: 263-268. (Pubitemid 38725893)
5. Chao, H, Mansfeld, SG, Bartel, RC, Hiriyanna, S, Mitchell, LG, Garcia-Blanco, MA et al. (2003). Phenotype correction of hemophilia A mice by spliceosome-mediated RNA trans-splicing. Nat Med 9: 1015-1019. (Pubitemid 37025113)
6. Liu, X, Jiang, Q, Mansfeld, SG, Puttaraju, M, Zhang, Y, Zhou, W et al. (2002). Partial correction of endogenous DeltaF508 CFTR in human cystic fbrosis airway epithelia by spliceosome-mediated RNA trans-splicing. Nat Biotechnol 20: 47-52. (Pubitemid 34044914)
7. Coady, TH, Baughan, TD, Shababi, M, Passini, MA and Lorson, CL (2008). Development of a single vector system that enhances trans-splicing of SMN2 transcripts. PLoS ONE 3: e3468.
8. Coady, TH and Lorson, CL (2010). Trans-splicing-mediated improvement in a severe mouse model of spinal muscular atrophy. J Neurosci 30: 126-130.
9. Tahara, M, Pergolizzi, RG, Kobayashi, H, Krause, A, Luettich, K, Lesser, ML et al. (2004). Trans-splicing repair of CD40 ligand defciency results in naturally regulated correction of a mouse model of hyper-IgM X-linked immunodefciency. Nat Med 10: 835-841. (Pubitemid 39070857)
10. Rodriguez-Martin, T, Anthony, K, Garcia-Blanco, MA, Mansfeld, SG, Anderton, BH and Gallo, JM (2009). Correction of tau mis-splicing caused by FTDP-17 MAPT mutations by spliceosome-mediated RNA trans-splicing. Hum Mol Genet 18: 3266-3273.
11. Avale, ME, Rodríguez-Martín, T and Gallo, JM (2013). Trans-splicing correction of tau isoform imbalance in a mouse model of tau mis-splicing. Hum Mol Genet 22: 2603-2611.
12. Wally, V, Klausegger, A, Koller, U, Lochmüller, H, Krause, S, Wiche, G et al. (2008). 5′ trans-splicing repair of the PLEC1 gene. J Invest Dermatol 128: 568-574.
13. Rindt, H, Yen, PF, Thebeau, CN, Peterson, TS, Weisman, GA and Lorson, CL (2012). Replacement of huntingtin exon 1 by trans-splicing. Cell Mol Life Sci 69: 4191-4204.
14. Gersh, BJ, Maron, BJ, Bonow, RO, Dearani, JA, Fifer, MA, Link, MS et al.; American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. (2011). 2011 ACCF/AHA Guideline for the Diagnosis and Treatment of Hypertrophic Cardiomyopathy: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Developed in collaboration with the American Association for Thoracic Surgery, American Society of Echocardiography, American Society of Nuclear Cardiology, Heart Failure Society of America, Heart Rhythm Society, Society for Cardiovascular Angiography and Interventions, and Society of Thoracic Surgeons. J Am Coll Cardiol 58: e212-e260.
15. Elliott, P, Andersson, B, Arbustini, E, Bilinska, Z, Cecchi, F, Charron, P et al. (2008). Classifcation of the cardiomyopathies: a position statement from the European Society Of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J 29: 270-276.
16. Ehlermann, P, Weichenhan, D, Zehelein, J, Steen, H, Pribe, R, Zeller, R et al. (2008). Adverse events in families with hypertrophic or dilated cardiomyopathy and mutations in the MYBPC3 gene. BMC Med Genet 9: 95.
17. Charron, P, Carrier, L, Dubourg, O, Tesson, F, Desnos, M, Richard, P et al. (1997). Penetrance of familial hypertrophic cardiomyopathy. Genet Couns 8: 107-114. (Pubitemid 27273731)
18. Schlossarek, S, Mearini, G and Carrier, L (2011). Cardiac myosin-binding protein C in hypertrophic cardiomyopathy: mechanisms and therapeutic opportunities. J Mol Cell Cardiol 50: 613-620.
19. Richard, P, Charron, P, Carrier, L, Ledeuil, C, Cheav, T, Pichereau, C et al.; EUROGENE Heart Failure Project. (2003). Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation 107: 2227-2232. (Pubitemid 36547217)
20. Pohlmann, L, Kröger, I, Vignier, N, Schlossarek, S, Krämer, E, Coirault, C et al. (2007). Cardiac myosin-binding protein C is required for complete relaxation in intact myocytes. Circ Res 101: 928-938. (Pubitemid 350287180)
21. Cazorla, O, Szilagyi, S, Vignier, N, Salazar, G, Krämer, E, Vassort, G et al. (2006). Length and protein kinase A modulations of myocytes in cardiac myosin binding protein C-defcient mice. Cardiovasc Res 69: 370-380. (Pubitemid 43098793)
22. Vignier, N, Schlossarek, S, Fraysse, B, Mearini, G, Krämer, E, Pointu, H et al. (2009). Nonsense-mediated mRNA decay and ubiquitin-proteasome system regulate cardiac myosin-binding protein C mutant levels in cardiomyopathic mice. Circ Res 105: 239-248.
23. Olivotto, I, Girolami, F, Ackerman, MJ, Nistri, S, Bos, JM, Zachara, E et al. (2008). Myoflament protein gene mutation screening and outcome of patients with hypertrophic cardiomyopathy. Mayo Clin Proc 83: 630-638. (Pubitemid 351810562)
24. Fraysse, B, Weinberger, F, Bardswell, SC, Cuello, F, Vignier, N, Geertz, B et al. (2012). Increased myoflament Ca2+ sensitivity and diastolic dysfunction as early consequences of Mybpc3 mutation in heterozygous knock-in mice. J Mol Cell Cardiol 52: 1299-1307.
25. Brinster, RL, Allen, JM, Behringer, RR, Gelinas, RE and Palmiter, RD (1988). Introns increase transcriptional effciency in transgenic mice. Proc Natl Acad Sci USA 85: 836-840. (Pubitemid 18073924)
26. Palmiter, RD, Sandgren, EP, Avarbock, MR, Allen, DD and Brinster, RL (1991). Heterologous introns can enhance expression of transgenes in mice. Proc Natl Acad Sci USA 88: 478-482. (Pubitemid 21915488)
27. Lorain, S, Peccate, C, Le Hir, M and Garcia, L (2010). Exon exchange approach to repair Duchenne dystrophin transcripts. PLoS ONE 5: e10894.
28. Puttaraju, M, Jamison, SF, Mansfeld, SG, Garcia-Blanco, MA and Mitchell, LG (1999). Spliceosome-mediated RNA trans-splicing as a tool for gene therapy. Nat Biotechnol 17: 246-252. (Pubitemid 29122632)
29. Fuke, H and Ohno, M (2008). Role of poly (A) tail as an identity element for mRNA nuclear export. Nucleic Acids Res 36: 1037-1049. (Pubitemid 351267257)
30. Müller, OJ, Leuchs, B, Pleger, ST, Grimm, D, Franz, WM, Katus, HA et al. (2006). Improved cardiac gene transfer by transcriptional and transductional targeting of adeno-associated viral vectors. Cardiovasc Res 70: 70-78.
31. Friedrich, FW, Wilding, BR, Reischmann, S, Crocini, C, Lang, P, Charron, P et al. (2012). Evidence for FHL1 as a novel disease gene for isolated hypertrophic cardiomyopathy. Hum Mol Genet 21: 3237-3254.
32. Pacak, CA, Mah, CS, Thattaliyath, BD, Conlon, TJ, Lewis, MA, Cloutier, DE et al. (2006). Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res 99: e3-e9. (Pubitemid 44255502)
33. Chen, HY, Kathirvel, P, Yee, WC and Lai, PS (2009). Correction of dystrophia myotonica type 1 pre-mRNA transcripts by artifcial trans-splicing. Gene Ther 16: 211-217.
34. Taniguchi, Y, Choi, PJ, Li, GW, Chen, H, Babu, M, Hearn, J et al. (2010). Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329: 533-538.
35. Zhang, Y and Friedlander, RM (2011). Using non-coding small RNAs to develop therapies for Huntington's disease. Gene Ther 18: 1139-1149.
36. Friedrich, FW and Carrier, L (2012). Genetics of hypertrophic and dilated cardiomyopathy. Curr Pharm Biotechnol 13: 2467-2476.
37. Brito, D, Miltenberger-Miltenyi, G, Vale Pereira, S, Silva, D, Diogo, AN and Madeira, H (2012). Sarcomeric hypertrophic cardiomyopathy: genetic profle in a Portuguese population. Rev Port Cardiol 31: 577-587.
38. Curila, K, Benesova, L, Penicka, M, Minarik, M, Zemanek, D, Veselka, J et al. (2012). Spectrum and clinical manifestations of mutations in genes responsible for hypertrophic cardiomyopathy. Acta Cardiol 67: 23-29.
39. Grimm, D, Kay, MA and Kleinschmidt, JA (2003). Helper virus-free, optically controllable, and two-plasmid-based production of adeno-associated virus vectors of serotypes 1 to 6. Mol Ther 7: 839-850. (Pubitemid 36790261)
40. Grieger, JC, Choi, VW and Samulski, RJ (2006). Production and characterization of adeno-associated viral vectors. Nat Protoc 1: 1412-1428.
41. Sands, MS and Barker, JE (1999). Percutaneous intravenous injection in neonatal mice. Lab Anim Sci 49: 328-330. (Pubitemid 29284392)