Production of β-globin and adult hemoglobin following G418 treatment of erythroid precursor cells from homozygous β039 thalassemia patients

American Journal of Hematology

Volumn 84, Issue 11, 2009, Pages 720-728

  Salvatori, Francesca ^a   Breveglieri, Giulia ^a   Zuccato, Cristina ^a   Finotti, Alessia ^a   Bianchi, Nicoletta ^a   Borgatti, Monica ^a   Feriotto, Giordana ^a   Destro, Federica ^a   Canella, Alessandro ^a   Brognara, Eleonora ^a   Lampronti, Ilaria ^a   Breda, Laura ^b   Rivella, Stefano ^b   Gambari, Roberto ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC G 418; BETA GLOBIN; HEMOGLOBIN; LENTIVIRUS VECTOR;

ADULT; ARTICLE; BETA 0 39 THALASSEMIA; BETA THALASSEMIA; CELL CLONE; CELL STRAIN K 562; CONTROLLED STUDY; ERYTHROID PRECURSOR CELL; FLUORESCENCE ACTIVATED CELL SORTING; GENE CASSETTE; GENE CONSTRUCT; GENE CONTROL; GENE EXPRESSION; GLOBIN GENE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION;

BETA-GLOBINS; BETA-THALASSEMIA; CELLS, CULTURED; CODON, NONSENSE; ERYTHROID PRECURSOR CELLS; GENTAMICINS; HEMOGLOBINS; HOMOZYGOTE; HUMANS; K562 CELLS;

EID: 70449567429     PISSN: 03618609     EISSN: 10968652     Source Type: Journal    
DOI: 10.1002/ajh.21539     Document Type: Article

References (71)

1. Kondrashov AS. Direct estimates of human per nucleotide mutation rates at 20 loci causing Mendelian diseases. Hum Mutat 2003;21:12-27.
2. Atkinson J, Martin R. Mutations to nonsense codons in human genetic disease: Implications for gene therapy by nonsense suppressor tRNAs. Nucleic Acids Res 1994;22:1327-1334. (Pubitemid 24166827)
3. Urlaub G, Mitchell PJ, Ciudad CJ, Chasin LA. Nonsense mutations in the dihydrofolate reductase gene affect RNA processing. Mol Cell Biol 1989;9:2868-2880. (Pubitemid 19163049)
4. Inácio A, Silva AL, Pinto J, et al. Nonsense mutations in close proximity to the initiation codon fail to trigger full nonsense-mediated mRNA decay. J Biol Chem 2004;279:32170-32180. (Pubitemid 39014664)
5. Mashima Y, Murakami A, Weleber RG, et al. Nonsense-codon mutations of the ornithine aminotransferase gene with decreased levels of mutant mRNA in gyrate atrophy. Am J Hum Genet 1992;51:81-91.
6. Mort M, Ivanov D, Cooper DN, Chuzhanova NA. A meta-analysis of nonsense mutations causing human genetic disease. Hum Mutat 2008;29:1037-1047.
7. Feldmann D, Laroze F, Troadec C, et al. A novel nonsense mutation (Q1291X) in exon 20 of CFTR (ABCC7) gene. Hum Mutat 2001;17:356.
8. Pagani F, Buratti E, Stuani C, Baralle FE. Missense, nonsense, and neutral mutations define juxtaposed regulatory elements of splicing in cystic fibrosis transmembrane regulator exon 9. J Biol Chem 2003;278:26580-26588. (Pubitemid 36876802)
9. 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.
10. Tran VK, Takeshima Y, Zhang Z, et al. A nonsense mutation-created intraexonic splice site is active in the lymphocytes, but not in the skeletal muscle of a DMD patient. Hum Genet 2007;120:737-742. (Pubitemid 44942858)
11. Ito T, Takeshima Y, Yagi M, et al. Analysis of dystrophin mRNA from skeletal muscle but not from lymphocytes led to identification of a novel nonsense mutation in a carrier of Duchenne muscular dystrophy. J Neurol 2003;250:581-587. (Pubitemid 36613302)
12. Trecartin R, Liebhaber SA, Chang JC, et al. b0 thalassemia in Sardinia is caused by a nonsense mutation. J Clin Invest 1981;68:1012-1017. (Pubitemid 11023529)
13. Piras I, Vona G, Falchi A, et al. Beta-globin cluster haplotypes in normal individuals and beta(0)39-thalassemia carriers from Sardinia, Italy. Am J Hum Biol 2005;17:765-772.
14. 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.
15. Khajavi M, Inoue K, Lupski JR. Nonsense-mediated mRNA decay modulates clinical outcome of genetic disease. Eur J Hum Genet 2006;14:1074-1081. (Pubitemid 44463965)
16. Stalder L, Mühlemann O. The meaning of nonsense. Trends Cell Biol 2008;18:315-321.
17. Isken O, Maquat LE. Quality control of eukaryotic mRNA: Safeguarding cells from abnormal mRNA function. Genes Dev 2007;21:1833-1856. (Pubitemid 47204924)
18. Behm-Ansmant I, Kashima I, Rehwinkel J, Saulière J. mRNA quality control: An ancient machinery recognizes and degrades mRNAs with nonsense codons. FEBS Lett 2007;581:2845-2853. (Pubitemid 46874393)
19. Takeshita K, Forget BG, Scarpa A, Benz EJ Jr. Intracellular defect in beta-globin mRNA accumulation due to a premature translation termination codon. Blood 1984;64:13-22. (Pubitemid 14085721)
20. Lim SK, Sigmund CD, Gross KW, Maquat LE. Nonsense codons in human beta-globin mRNA result in the production of mRNA degradation products. Mol Cell Biol 1992;12:1149-1161.
21. Huisman THJ, Carver MFH, Baysal E. A Syllabus of Thalassemia Mutations. Augusta, GA: The Sickle Cell Anemia Foundation; 1997.
22. Ahmed M, Stuhrmann M, Bashawri L, et al. The beta-globin genotype E121Q/W15X (cd121GAA - >CAA/cd15TGG - >TGA) underlines Hb d/beta-(0) thalassaemia marked by domination of haemoglobin D. Ann Hematol 2001;80:629-633.
23. Kornblit B, Taaning P, Birgens H. Beta-thalassemia due to a novel nonsense mutation at codon 37 (TGG - >TAG) found in an Afghanistani family. Hemoglobin 2005;29:209-213. (Pubitemid 41099688)
24. Li D, Liao C, Li J, Tang X. The codon 37 (TGG - >TAG) beta(0)-thalassemia mutation found in a Chinese family. Hemoglobin 2006;30:171-173.
25. Préhu C, Pissard S, Al-Sheikh M, et al. Two French Caucasian families with dominant thalassemia-like phenotypes due to hyper unstable hemoglobin variants: Hb Sainte Seve [codon 118 (-T)] and codon 127 [CAG - >TAG (Gln - >stop]). Hemoglobin 2005;29:229-233. (Pubitemid 41099692)
26. Patterson M, Walker L, Chui DH, et al. Identification of a new beta-thalassemia nonsense mutation [codon 59 (AAG - >TAG)]. Hemoglobin 2003;27:201-203. (Pubitemid 36962055)
27. Amato A, Pia Cappabianca M, Ponzini D, et al. Detection of a rare beta-globin nonsense mutation [codon 59 (AAG - >TAG)] in an Italian family. Hemoglobin 2006;30:405-407. (Pubitemid 44091805)
28. Welch EM, Barton ER, Zhuo J, et al. PTC124 targets genetic disorders caused by nonsense mutations. Nature 2007;447:87-91. (Pubitemid 46685839)
29. Du M, Liu X, Welch EM, et al. 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 USA 2008;105:2064-2069.
30. Hirawat S, Welch EM, Elfring GL, et al. Safety, tolerability, and pharmacokinetics of PTC124, a nonaminoglycoside nonsense mutation suppressor, following single- and multiple-dose administration to healthy male and female adult volunteers. J Clin Pharmacol 2007;47:430-444. (Pubitemid 46465953)
31. Kellermayer R. Translational readthrough induction of pathogenic nonsense mutations. Eur J Med Genet 2006;49:445-450. (Pubitemid 46037580)
32. Zingman LV, Park S, Olson TM, et al. Aminoglycoside-induced translational read-through in disease: Overcoming nonsense mutations by pharmacogenetic therapy. Clin Pharmacol Ther 2007;81:99-103. (Pubitemid 46050873)
33. Hainrichson M, Nudelman I, Baasov T. Designer aminoglycosides: The race to develop improved antibiotics and compounds for the treatment of human genetic diseases. Org Biomol Chem 2008;6:227-239.
34. Howard M, Frizzell RA, Bedwell DM. Aminoglycoside antibiotics restore CFTR function by overcoming premature stop mutations. Nat Med 1996;2:467-469. (Pubitemid 26191920)
35. 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. (Pubitemid 27508832)
36. Du M, Jones JR, Lanier J, et al. Aminoglycoside suppression of a premature stop mutation in a Cftr-/- mouse carrying a human CFTR-G542X transgene. J Mol Med 2002;80:595-604.
37. Du M, Keeling KM, Fan L, et al. Clinical doses of amikacin provide more effective suppression of the human CFTR-G542X stop mutation than gentamicin in a transgenic CF mouse model. J Mol Med 2006;84:573-582. (Pubitemid 43992849)
38. Wilchanski 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. (Pubitemid 37211058)
39. Kerem E. Pharmacologic therapy for stop mutations: How much CFTR activity is enough? Curr Opin Pulm Med 2004;10:547-552.
40. Bidou L, Hatin I, Perez N, et al. 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. (Pubitemid 38455980)
41. Howard MT, Anderson CB, Fass U, et al. Readthrough of dystrophin stop codon mutations induced by aminoglycosides. Ann Neurol 2004;55:422-426. (Pubitemid 38269595)
42. Howard MT, Shirts BH, Petros LM, et al. Sequence specificity of aminoglycoside-induced stop condon readthrough: Potential implications for treatment of Duchenne muscular dystrophy. Ann Neurol 2000;48:164-169.
43. 039 thalassaemia mutation for the screening of correctors of stop codon mutations. Biotechnol Appl Biochem 2009;54:41-52.
44. Fibach E, Manor D, Oppenheim A, Rachmilewitz EA. Proliferation and maturation of human erythroid progenitors in liquid culture. Blood 1989;73:100-103. (Pubitemid 19040960)
45. Pope SH, Fibach E, Sun J, et al. Two-phase liquid culture system models normal human adult erythropoiesis at the molecular level. Eur J Haematol 2000;64:292-303. (Pubitemid 30307701)
46. Weatherall DJ. Pathophysiology of thalassaemia. Baillieres Clin Haematol 1998;11:127-146.
47. Schrier SL. Pathophysiology of thalassemia. Curr Opin Hematol 2002;9:123-126.
48. Fibach E, Burke LP, Schechter AN, et al. Hydroxyurea increases fetal haemoglobin in cultured erythroid cells derived from normal individual and patients with sickle cell anemia or beta-thalassemia. Blood 1993;81:1630-1635. (Pubitemid 23083845)
49. Koren A, Levin C, Dgany O, et al. Response to hydroxyurea therapy in beta-thalassemia. Am J Hematol 2008;83:366-370.
50. Singh G, Rebbapragada I, Lykke-Andersen J. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol 2008 Apr;29:e111.
51. Usuki F, Yamashita A, Kashima I, et al. Specific inhibition of nonsense-mediated mRNA decay components, SMG-1 or Upf1, rescues the phenotype of Ullrich disease fibroblasts. Mol Ther 2006;14:351-360. (Pubitemid 44184971)
52. Gardner LB. Hypoxic inhibition of nonsense-mediated RNA decay regulates gene expression and the integrated stress response. Mol Cell Biol 2008;28:3729-3741.
53. Bonetti B, Fu L, Moon J, Bedwell DM. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J Mol Biol 1995;251:334-345.
54. 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. (Pubitemid 30471140)
55. James PD, Raut S, Rivard GE, et al. Aminoglycoside suppression of nonsense mutations in severe hemophilia. Blood 2005;106:3043-3048. (Pubitemid 41565897)
56. Pinotti M, Rizzotto L, Pinton P, et al. Intracellular readthrough of nonsense mutations by aminoglycosides in coagulation factor VII. J Thromb Haemost 2006;4:1-7. (Pubitemid 43756710)
57. 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 USA 2004;101:15676-15681.
58. Keeling KM, Brooks DA, Hopwood JJ, et al. Gentamicin-mediated suppression of Hurler syndrome stop mutations restores a low level of α-L-iduronidase activity and reduces lysosomal-glycosaminoglycan accumulation. Hum Mol Genet 2001;10:291-299.
59. Gambari R, Fibach E. Medicinal chemistry of fetal hemoglobin inducers for treatment of beta-thalassemia. Curr Med Chem 2007;14:199-212. (Pubitemid 46043915)
60. Bianchi N, Zuccato C, Lampronti I, et al. Fetal hemoglobin inducers from the natural world: A novel approach for identification of drugs for the treatment of beta-thalassemia and sickle-cell anemia. Evid Based Complement Altern Med 2009;6:141-151.
61. Sadelain M. Globin gene transfer as a potential treatment for the β-thalassemias and sickle cells disease. Vox Sang 2004;87 (Suppl 2): S235-S242. (Pubitemid 39165316)
62. Puthenveetil G, Scholes J, Carbonell D, et al. Successful correction of the human β -thalassemia major phenotype using a lentiviral vector. Blood 2004;104:3445-3453.
63. Lucarelli G, Clift RA, Galimberti M, et al. Bone marrow transplantation in adult thalassemic patients. Blood 1999;93:1164-1167. (Pubitemid 29076130)
64. Lawson SE, Roberts IAG, Amrolia P, et al. Bone marrow transplantation for β-thalassemia major: The UK experience in two pediatric centres. Br J Haematol 2003;120:289-295. (Pubitemid 36194180)
65. Lozzio CB, Lozzio BB. Human chronic myelogenous leukaemia cell-line with positive Philadelphia chromosome. Blood 1975;45:321-334.
66. Lampronti I, Bianchi N, Borgatti M, et al. Accumulation of gamma-globin mRNA in human erythroid cells treated with angelicin. Eur J Haematol 2003;71:189-195. (Pubitemid 37082842)
67. Fibach E, Bianchi N, Borgatti M, et al. Effects of rapamycin on accumulation of α-, β- and γ-globin mRNAs in erythroid precursor cells from β-thalassaemia patients. Eur J Haematol 2006;77:437-441. (Pubitemid 44483948)
68. Zuccato C, Bianchi N, Borgatti M, et al. Everolimus is a potent inducer of erythroid differentiation and gamma-globin gene expression in human erythroid cells. Acta Haematol 2006;117:168-176.
69. Huisman THJ. Separation of Hemoglobins and hemoglobin chains by HPLC. J Chromatogr 1987;418:277-304.
70. Andrews NC, Faller DV. A rapid micropreparetion technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 1991;19:2499.
71. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.