Drug-induced readthrough of premature stop codons leads to the stabilization of laminin α2 chain mRNA in CMD myotubes

Journal of Gene Medicine

Volumn 10, Issue 2, 2008, Pages 217-224

  Allamand, Valérie ^a,b   Bidou, Laure ^c,d   Arakawa, Masayuki ^e   Floquet, Célia ^c,d   Shiozuka, Masataka ^e   Paturneau Jouas, Marion ^a,b   Gartioux, Corine ^a,b   Butler Browne, Gillian S ^f   Mouly, Vincent ^f   Rousset, Jean Pierre ^c,d   Matsuda, Ryoichi ^e   Ikeda, Daishiro ^g   Guicheney, Pascale ^a,b  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d CNRS   (France)

^e UNIVERSITY OF TOKYO   (Japan)

^f PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^g INSTITUTE OF MICROBIAL CHEMISTRY   (Japan)

Author keywords

Antibiotic mediated readthrough; Congenital muscular dystrophy; Laminin 2 chain; Nonsense mediated mRNA decay; Premature termination codon

Indexed keywords

AMIKACIN; GENTAMICIN; LAMININ ALPHA2; MESSENGER RNA; MYOSIN; NEGAMYCIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EX VIVO STUDY; FETUS; GENE EXPRESSION; GENE TARGETING; GENETIC STABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUSCULAR DYSTROPHY; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; STOP CODON; TRANSLATION REGULATION;

EID: 39449127401     PISSN: 1099498X     EISSN: 15212254     Source Type: Journal    
DOI: 10.1002/jgm.1140     Document Type: Article

References (51)

1. Fardeau M. Congenital myopathies. In Skeletal Muscle Pathology, Mastaglia FL, Detchant. LWo (eds). Churchill Livingstone: Edinburgh, 1992; 237-281.
2. Banker BQ. The congenital muscular dystrophies. In Myology, Engel AG, Franzini-Amstrong C (eds). McGraw-Hill: New York, 1994; 1275-1289.
3. Tomé FMS, Guicheney P, Fardeau M. Congenital muscular dystrophies. In Neuromuscular Disorders, Clinical and Molecular Genetics, Emery AEH (ed). John Wiley: Chichester, 1998; 21-57.
4. Tomé FM. The Peter Emil Becker Award lecture 1998. The saga of congenital muscular dystrophy. Neuroped 1999; 30: 55-65.
5. Helbling-Leclerc A, Zhang X, Topaloglu H, et al. Mutations in the laminin α2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nat Genet 1995; 11: 216-218.
6. Nissinen M, Helbling-Leclerc A, Zhang X, et al. Substitution of a conserved cysteine-996 in a cysteine-rich motif of the laminin α2-chain in congenital muscular dystrophy with partial deficiency of the protein. Am J Hum Genet 1996; 58: 1177-1184.
7. Allamand V, Guicheney P. Merosin-deficient congenital muscular dystrophy, autosomal recessive (MDC1A, MIM#156225, LAMA2 gene coding for α2 chain of laminin). Eur J Hum Genet 2002; 10: 91-94.
8. Allamand V, Sunada Y, Salih MAM, et al. Mild congenital muscular dystrophy in two patients with an internally deleted laminin α2-chain. Hum Mol Genet 1997; 6: 747-752.
9. Guicheney P, Vignier N, Helbling-Leclerc A, et al. Genetics of laminin alpha 2 chain (or merosin) deficient congenital muscular dystrophy: from identification of mutations to prenatal diagnosis. Neuromuscul Disord 1997; 7: 180-186.
10. Palmer E, Wilhelm JM, Sherman F. Phenotypic suppression of nonsense mutants in yeast by aminoglycoside antibiotics. Nature 1979; 277: 148-150.
11. Singh A, Ursic D, Davies J. Phenotypic suppression and misreading in Saccharomyces cerevisiae. Nature 1979; 277: 146-148.
12. Burke JF, Mogg AE. Suppression of a nonsense mutation in mammalian cells in vivo by the aminoglycoside antibiotics G-418 and paromomycin. Nucleic Acids Res 1985; 13: 6265-6272.
13. Martin R, Mogg AE, Heywood LA, Nitschke L, Burke JF. Aminoglycoside suppression at UAG, UAA and UGA codons in Escherichia coli and human tissue culture cells. Mol Gen Genet 1989; 217: 411-418.
14. Kaufman RJ. Correction of genetic disease by making sense from nonsense. J Clin Invest 1999; 104: 367-368.
15. Howard MT, Anderson CB, Fass U, et al. Readthrough of dystrophin stop codon mutations induced by aminoglycosides. Ann Neurol 2004; 55: 422-426.
16. Bedwell DM, Kaenjak A, Benos DJ, et al. Suppression of a CFTR premature stop mutation in a bronchial epithelial cell line. Nat Med 1997; 3: 1280-1284.
17. Barton-Davis ER, Cordier L, Shoturma DI, Leland SE, Sweeney HL. Aminoglycoside antibiotics restore dystrophin function to skeletal muscles of mdx mice. J Clin Invest 1999; 104: 375-381.
18. Wilschanski M, Famini C, Blau H, et al. A pilot study of the effect of gentamicin on nasal potential difference measurements in cystic fibrosis patients carrying stop mutations. Am J Respir Crit Care Med 2000; 161: 860-865.
19. Clancy JP, Bebök Z, Ruiz F, et al. Evidence that systemic gentamicin suppresses premature stop mutations in patients with cystic fibrosis. Am J Respir Crit Care Med 2001; 163: 1683-1692.
20. Keeling KM, Bedwell DM. Clinically relevant aminoglycosides can suppress disease-associated premature stop mutations in the IDUA and P53 cDNAs in a mammalian translation system. J Mol Med 2002; 80: 367-376.
21. Bidou L, Hatin I, Perez N, Allamand V, Panthier J-J, Rousset J-P. Premature stop codons involved in muscular dystrophies show a broad spectrum of readthrough efficiencies in response to gentamicin treatment. Gene Ther 2004; 11: 619-627.
22. Kellermayer R, Szigeti R, Keeling KM, Bedekovics T, Bedwell DM. Aminoglycosides as potential pharmacogenetic agents in the treatment of Hailey-Hailey disease. J Invest Dermatol 2006; 126: 229-231.
23. Wagner KR, Hatted S, Hadley DW, et al. Gentamicin treatment of Duchenne and Becker muscular dystrophy due to nonsense mutations. Ann Neurol 2001; 49: 706-711.
24. Politano L, Nigro G, Nigro V, et al. Gentamicin administration in Duchenne patients with premature stop codon. Preliminary results. Acta Myologica 2003; 22: 15-21.
25. Wilschanski M, Yahav Y, Yaacov Y, et al. Gentamicin-induced correction of CFTR function in patients with cystic fibrosis and CFTR stop mutations. N Engl J Med 2003; 349: 1433-1441.
26. James PD, Raut S, Rivard GE, et al. Aminoglycoside suppression of nonsense mutations in severe hemophilia. Blood 2005; 106: 3043-3048.
27. Phillips-Jones M, Hill L, Atkinson J, Martin R. Context effects on misreading and suppression at UAG codons in human cells. Mol Cell Biol 1995; 15: 6593-6600.
28. Howard MT, Shirts BH, Petros LM, Flanigan KM, Gesteland RF, Atkins JF. Sequence specificity of aminoglycoside-induced stop codon readthrough: potential implications for treatment of Duchenne muscular dystrophy. Ann Neurol 2000; 48: 164-169.
29. Aurino S, Nigro V. Readthrough strategies for stop codons in Duchenne muscular dystrophy. Acta Myologica 2006; 25: 5-12.
30. Sermet-Gaudelus I, Renouil M, Fajac A, et al. In vitro prediction of stop-codon suppression by intravenous gentamicin in patients with cystic fibrosis: a pilot study. BMC Med 2007; 5: 5.
31. Swann SK. Aminoglycoside nephrotoxicity. Semin Nephrol 1997; 17: 27-33.
32. Forge A, Schacht J. Aminoglycoside antibiotics. Audiol Neurootol 2000; 5: 3-22.
33. Dunant P, Walter MC, Karpati G, Lochmuller H. Gentamicin fails to increase dystrophin expression in dystrophin- deficient muscle. Muscle Nerve 2003; 27: 624-627.
34. Wolstencroft EC, Mattis V, Bajer AA, Young PJ, Lorson CL. A non-sequence-specific requirement for SION protein activity: the role of aminoglycosides in inducing elevated SMN protein levels. Hum Mol Genet 2005; 14: 1199-1210.
35. Hamada M, Tadeuchi T, Kondo S, et al. A new antibiotic, negamycin. J Antibiot 1970; 23: 170-171.
36. Uehara Y, Hori M, Umezawa H. Negamycin inhibits termination of protein synthesis directed by phage f2 RNA in vitro. Biochim Biophys Acta 1974; 374: 82-95.
37. Arakawa M, Nakayama Y, Hara T, et al. Negamycin can restore dystrophin in mdx skeletal muscle. Acta Myologica 2001; 20: 154-158.
38. Arakawa M, Shiozuka M, Nakayama Y, et al. Negamycin restores dystrophin expression in skeletal and cardiac muscles of mdx mice. J Biochem (Tokyo) 2003; 134: 751-758.
39. Guicheney P, Vignier N, Zhang X, et al. PCR based mutation screening of the laminin alpha2 chain gene (LAMA2): application to prenatal diagnosis and search for founder effects in congenital muscular dystrophy. J Med Genet 1998; 35: 211-217.
40. Bidou L, Stahl G, Hatin I, Namy O, Rousset J-P, Farabaugh PJ. Nonsense-mediated decay mutants do not affect programmed -1 frameshifting. RNA 2000; 6: 952-961.
41. Martin R, Philips-Jones MK, Watson FJ, Hills LS. Codon context effects on nonsense suppression in human cells. Biochem Soc Trans 1993; 21: 846-851.
42. Manuvakhova M, Keeling K, Bedwell DM. Aminoglycoside antibiotics mediate context-dependent suppression of termination codons in a mammalian translation system. RNA 2000; 6: 1044-1055.
43. Cassan M, Rousset JP. UAG readthrough in mammalian cells: Effect of upstream and downstream stop codon contexts reveal different signals. BMC Mol Biol 2001; 2: 3.
44. Maquat LE. Nonsense-mediated mRNA decay in mammals. J Cell Sci 2005; 118: 1773-1776.
45. Moriarty PM, Reddy CC, Maquat LE. Selenium deficiency reduces the abundance of mRNA for Se-dependent glutathione peroxidase 1 by a UGA-dependent mechanism likely to be nonsense codon-mediated decay of cytoplasmic mRNA. Mol Cell Biol 1998; 18: 2932-2939.
46. Keeling W, Lanier J, Du M, et al. Leaky termination at premature stop codons antagonize nonsense-mediated mRNA decay in S. cerevisiae. RNA 2004; 10: 691-703.
47. Linde L, Boelz S, Nissim-Rafinia M, et al. Nonsense-mediated mRNA decay affects nonsense transcript levels and governs response of cystic fibrosis patients to gentamicin. J Clin Invest 2007; 117: 683-692.
48. Welch EM, Barton ER, Zhuo J, et al. PTC124 targets genetic disorders caused by nonsense mutations. Nature 2007; 447: 87-91.
49. Nilsson M, Ryden-Aulin M. Glutamine is incorporated at the nonsense codons UAG and UAA in a suppressor-free Escherichia coli strain. Biochim Biophys Acta - Gene Structure and Expression 2003; 1627: 1-6.
50. Available: www.bork.embl-heidelberg.de/PolyPhen.
51. Sunyaev S, Ramensky V, Koch I, Lathe Wr, Kondrashov A, Bork P. Prediction of deleterious human alleles. Hum Mol Genet 2001; 10: 591-597.