Effect of Readthrough Treatment in Fibroblasts of Patients Affected by Lysosomal Diseases Caused by Premature Termination Codons

Neurotherapeutics

Volumn 12, Issue 4, 2015, Pages 874-886

  Matalonga, Leslie ^a   Arias, Ángela ^a   Tort, Frederic ^a   Ferrer Cortés, Xènia ^a   Garcia Villoria, Judit ^a   Coll, Maria Josep ^a   Gort, Laura ^a   Ribes, Antonia ^a  

^a HOSPITAL CLÍNIC   (Spain)

Author keywords

aminoglycoside; Gentamicin; lysosomal disease; premature stop codon; PTC124; readthrough treatment

Indexed keywords

ATALUREN; GENTAMICIN; MESSENGER RNA; ACETYLGLUCOSAMINIDASE; ALPHA-N-ACETYL-D-GLUCOSAMINIDASE; GLYCOPROTEIN; GLYCOSAMINOGLYCAN; IDS PROTEIN, HUMAN; OXADIAZOLE DERIVATIVE; PROTEIN SYNTHESIS INHIBITOR; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELIN PHOSPHODIESTERASE 1, HUMAN; STOP CODON;

ARTICLE; CELL VIABILITY; CLINICAL ARTICLE; COMPARATIVE STUDY; COMPUTER MODEL; CONTROLLED STUDY; DRUG EFFICACY; DRUG SCREENING; DRUG THERAPY; ENZYME ACTIVITY; FABRY DISEASE; FRAMESHIFT MUTATION; GANGLIOSIDOSIS; HUMAN; HUNTER SYNDROME; HURLER SYNDROME; IMMUNOFLUORESCENCE; LYSOSOME; LYSOSOME STORAGE DISEASE; NIEMANN PICK DISEASE; NONSENSE MEDIATED MRNA DECAY; PREDICTION; PREMATURE TERMINATION CODON; PRIORITY JOURNAL; PROTEIN LOCALIZATION; READTHROUGH TREATMENT; SANFILIPPO SYNDROME; SKIN FIBROBLAST; STOP CODON; TREATMENT RESPONSE; CELL CULTURE; CELL SURVIVAL; DRUG EFFECTS; FEMALE; FIBROBLAST; GENETICS; MALE; METABOLISM; MUTATION; PATHOLOGY;

ACETYLGLUCOSAMINIDASE; CELL SURVIVAL; CELLS, CULTURED; CODON, NONSENSE; FEMALE; FIBROBLASTS; GENTAMICINS; GLYCOPROTEINS; GLYCOSAMINOGLYCANS; HUMANS; LYSOSOMAL STORAGE DISEASES; LYSOSOMES; MALE; MUTATION; OXADIAZOLES; PROTEIN SYNTHESIS INHIBITORS; RNA, MESSENGER; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 84973909610     PISSN: 19337213     EISSN: 18787479     Source Type: Journal    
DOI: 10.1007/s13311-015-0368-4     Document Type: Article

References (56)

1. Singh G, Lykke-Andersen J. New insights into the formation of active nonsense-mediated decay complexes. Trends Biochem Sci 2003;28:464-466.
2. Kuzmiak HA, Maquat LE. Applying nonsense-mediated mRNA decay research to the clinic: progress and challenges. Trends Mol Med 2006;12:306-316.
3. Ainsworth C. Nonsense mutations: running the red light. Nature 2005;438:726-728.
4. Hers HG. The role of lysosomes in the pathogeny of storage diseases. Biochimie 1972;54:753-757.
5. Neufeld EF, Muenzer J. The mucopolysaccharidoses. In: Scriver CR, Beaudet AL, Sly WS, Valle D (eds) The metabolic and molecular bases of inherited disease. New York: McGraw Hill, 2001, pp. 3421-3452.
6. Desnick RJ, Thorpe SR, Fiddler MB. Toward enzyme therapy for lysosomal storage diseases. Physiol Rev 1976;56:57-99.
7. Seregin SS, Amalfitano A. Gene therapy for lysosomal storage diseases: progress, challenges and future prospects. Curr Pharm 2011;17:2558-2574.
8. Muntau AC, Leandro J, Staudigl M, Mayer F, Gersting SW. Innovative strategies to treat protein misfolding in inborn errors of metabolism: pharmacological chaperones and proteostasis regulators. J Inherit Metab Dis 2014;37:505-523.
9. Pérez B, Rodríguez-Pombo P, Ugarte M, Desviat LR. Readthrough strategies for therapeutic suppression of nonsense mutations in inherited metabolic disease. Mol Syndromol 2012;3:230-236.
10. Bidou L, Hatin I, Perez N, Allamand V, Panthier JJ, Rousset JP. 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.
11. Gunn G, Dai Y, Du M, et al. Long-term nonsense suppression therapy moderates MPS I-H disease progression. Mol Genet Metab 2014;111:374-381.
12. Micale L, Augello B, Maffeo C, et al. Molecular analysis, pathogenic mechanisms, and readthrough therapy on a large cohort of Kabuki syndrome patients. Hum Mutat 2014;35:841-850.
13. Sleat DE, Sohar I, Gin RM, Lobel P. Aminoglycoside-mediated suppression of nonsense mutations in late infantile neuronal ceroid lipofuscinosis. Eur J Paediatr Neurol 2001;5(Suppl. A):57-62.
14. Hein LK, Bawden M, Muller VJ, Sillence D, Hopwood JJ, Brooks DA. alpha-L-iduronidase premature stop codons and potential read-through in mucopolysaccharidosis type I patients. J Mol Biol 2004;338:453-462.
15. Miller JN, Kovács AD, Pearce DA. The novel Cln1(R151X) mouse model of infantile neuronal ceroid lipofuscinosis (INCL) for testing nonsense suppression therapy. Hum Mol Genet 2015;24:185-196.
16. Tai PC, Davis BD. Triphasic concentration effects of gentamicin on activity and misreading in protein síntesis. Biochemistry 1979;18:193-198.
17. Manuvakhova M, Keeling K, Bedwell D. Aminoglycoside antibiotics mediate context-dependent suppression of termination codons in a mammalian translation system. RNA 2000;6:1044-1055.
18. Welch EM, Barton ER, Zhuo J, et al. PTC124 targets genetic disorders caused by nonsense mutations. Nature 2007;447:87-91.
19. Wang D, Belakhov V, Kandasamy J, et al. The designer aminoglycoside NB84 significantly reduces glycosaminoglycan accumulation associated with MPS I-H in the Idua-W392X mouse. Mol Genet Metab 2012;105:116-125.
20. 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
21. Keeling KM, Brooks DA, Hopwood JJ, Li P, Thompson JN, Bedwell DM. Gentamicin-mediated suppression of Hurler syndrome stop mutations restores a low level of alpha-L-iduronidase activity and reduces lysosomal glycosaminoglycan accumulation. Hum Mol Genet 2001;10:291-299.
22. Buck NE, Wood LR, Hamilton NJ, Bennett MJ, Peters HL. Treatment of a methylmalonyl-CoA mutase stop codon mutation. Biochem Biophys Res Commun 2012;427:753-757.
23. Bartolomeo R, Polishchuk EV, Volpi N, Polishchuk RS, Auricchio A. Pharmacological read-through of nonsense ARSB mutations as a potential therapeutic approach for mucopolysaccharidosis VI. J Inherit Metab Dis 2013;36:363-371.
24. Floquet C, Hatin I, Rousset JP, Bidou L. Statistical analysis of readthrough levels for nonsense mutations in mammalian cells reveals a major determinant of response to gentamicin. PLoS Genet 2012;8:e1002608.
25. Hutchin T, Cortopassi G. Proposed molecular and cellular mechanism for aminoglycoside ototoxicity. Antimicrob Agents Chemother 1994;38:2517-2520.
26. Mingeot-Leclercq M-P, Tulkens PM. Aminoglycosides: nephrotoxicity. Antimicrob Agents Chemother 1999;43:1003-1012.
27. Tan L, Narayan SB, Chen J, Meyers GD, Bennett MJ. PTC124 improves readthrough and increases enzymatic activity of the CPT1A R160X nonsense mutation. J Inherit Metab Dis 2011;34:443-447.
28. Annunziata P, Dimatteo G. Study of influence of sex and age on human serum lysosomal enzymes by using 4-methylumbelliferyl substrates. Clin Chim Acta 1978;90:101-106.
29. Sumantran VN. Cellular chemosensitivity assays: an overview. Methods Mol Biol 2011;731:219-236.
30. Barbosa I, Garcia S, Barbier-Chassefière V, Caruelle JP, Martelly I, Papy-García D. Improved and simple micro assay for sulfated glycosaminoglycans quantification in biological extracts and its use in skin and muscle tissue studies. Glycobiology 2003;13:647-653.
31. Carter MS, Doskow J, Morris P, Li S, Nhim RP, Sandstedt S, Wilkinson MF. A regulatory mechanism that detects premature nonsense codons in T-cell receptor transcripts in vivo is reversed by protein synthesis inhibitors in vitro. J Biol Chem 1995;270:28995-29003.
32. Noensie EN, Dietz HC. A strategy for disease gene identification through nonsense-mediated mRNA decay inhibition. Nat Biotechnol 2001;19:434-439.
33. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 2000;285:194-204.
34. Adzhubei IA, Schmidt S, Peshkin L, et al. A method and server for predicting damaging missense mutations. Nat Methods 2010;7:248-249.
35. Kumar P, Henikoff S, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 2009;4:1073-1081.
36. Wilschanski M, Famini C, Blau H. 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.
37. Keeling KM, Wang D, Dai Y, et al. Attenuation of nonsense-mediated mRNA decay enhances in vivo nonsense suppression. PLoS One 2013;8:e60478.
38. Brooks DA, Muller VJ, Hopwood JJ. Stop-codon read-through for patients affected by a lysosomal storage disorder. Trends Mol Med 2006;12:367-373.
39. Barton-Davis ER, Cordier L, Shoturma DI, Le- land SE, Sweeney HL. Aminoglycoside antibiotics restore dystrophin function to skeletal muscles of mdx mice. J Clin Invest 1999;104:375-381.
40. Lai CH, Chun HH, Nahas SA, et al. Correction of ATM gene function by aminoglycoside-induced read-through of premature termination codons. Proc Natl Acad Sci U S A 2004;101:15676-15681.
41. Grayson C, Chapple JP, Willison KR, Webster AR, Hardcastle AJ Cheetham ME. In vitro analysis of aminoglycoside therapy for the Arg120stop nonsense mutation in RP2 patients. J Med Genet 2002;39:62-67
42. Du M, Liu X, Welch EM, Hirawat S, Peltz SW, Bedwell DM. PTC124 is an orally bioavailable compound that promotes suppression of the human CFTR-G542X nonsense allele in a CF mouse model. Proc Natl Acad Sci U S A 2008;105:2064-2069.
43. Kerem E, Hirawat S, Armoni S, et al. Effectiveness of PTC124 treatment of cystic fibrosis caused by nonsense mutations: a prospective phase II trial. Lancet 2008;372:719-727.
44. Sheridan C. Doubts raised over ‘read-through’ Duchenne drug mechanism. Nat Biotechnol 2013;31:771-773.
45. Cooper GM. The cell: a molecular approach. 2nd ed. Available at: http://www.ncbi.nlm.nih.gov/books/NBK9876/ (accessed 26 June 2015).
46. Boustany RM. Lysosomal storage diseases--the horizon expands. Nat Rev Neurol 2013;9:583-588.
47. Harrell L, Melcher U, Atkins JF. Predominance of six different hexanucleotide recoding signals 3' of read-through stop codons. Nucleic Acids Res 2002;30:2011-2017.
48. Howard MT, Shirts BH, Petros LM, Flanigan KM, Gesteland RF, Atkins JF. Sequence specificity of aminoglycoside-induced stop condon readthrough: potencial implications for treatment of Duchenne muscular dystrophy. Ann Neurol 2000;48:164-169.
49. Kervestin S, Jacobson A. NMD: a multifaceted response to premature translational termination. Nat Rev Mol Cell Biol 2012;13:700-712.
50. Nilsson M, Rydén-Aulin M. Glutamine is incorporated at the nonsense codons UAG and UAA in a suppressor-free Escherichia coli strain. Biochim Biophys Acta 2003;1627:1-6.
51. Sarkar C, Zhang Z, Mukherjee AB: Stop codon read-through with PTC124 induces palmitoyl-protein thioesterase-1 activity, reduces thioester load and suppresses apoptosis in cultured cells from INCL patients. Mol Genet Metab 2011;104:338-345.
52. Sánchez-Alcudia R, Pérez B, Ugarte M, Desviat LR. Feasibility of nonsense mutation readthrough as a novel therapeutical approach in propionic acidemia. Hum Mutat 2012;33:973-980.
53. Ho G, Reichardt J, Christodoulou J. In vitro read-through of phenylalanine hydroxylase (PAH) nonsense mutations using aminoglycosides: a potential therapy for phenylketonuria. J Inherit Metab Dis 2013;36:955-959.
54. Loudon JA. Ataluren: a ‘no-nonsense’ approach for pulmonary diseases. Pulm Pharmacol Ther 2013;26:398-399.
55. Wang D, Shukla C, Liu X, et al. Characterization of an MPS I-H knock-in mouse that carries a nonsense mutation analogous to the human IDUA-W402X mutation. Mol Genet Metab 2010;99:62-71.
56. Taguchi A, Hamada K, Kotake M, et al. Discovery of natural products possessing selective eukaryotic readthrough activity: 3-epi-deoxynegamycin and its leucine adduct. ChemMedChem 2014;9:2233-2237.