β-globin gene transfer to human bone marrow for sickle cell disease

Journal of Clinical Investigation

Volumn 123, Issue 8, 2013, Pages 3317-3330

  Romero, Zulema ^a   Urbinati, Fabrizia ^a   Geiger, Sabine ^a   Cooper, Aaron R ^b   Wherley, Jennifer ^a   Kaufman, Michael L ^a   Hollis, Roger P ^a   De Assin, Rafael Ruiz ^a   Senadheera, Shantha ^a   Sahagian, Arineh ^a   Jin, Xiangyang ^a   Gellis, Alyse ^a   Wang, Xiaoyan ^c   Gjertson, David ^d   DeOliveira, Satiro ^e   Kempert, Pamela ^e   Shupien, Sally ^e   Abdel Azim, Hisham ^f   Walters, Mark C ^g   Meiselman, Herbert J ^f   Wenby, Rosalinda B ^f   Gruber, Theresa ^a   Marder, Victor ^a   Coates, Thomas D ^f   Kohn, Donald B ^a,e   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Molecular Biology Interdepartmental PhD Program   (United States)

^c Department of Medicine Statistics Core ^*  (United States)

^d School of Public Health   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^g CHILDREN S HOSPITAL OAKLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; HEMOGLOBIN; HEMOGLOBIN BETA CHAIN; LENTIVIRUS VECTOR;

ALLOTRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; DEOXYGENATION; ERYTHROCYTE; FLOW CYTOMETRY; GENETIC ENGINEERING; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IN VITRO STUDY; MORBIDITY; MOUSE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SICKLE CELL ANEMIA; STEM CELL; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

EID: 84881262533     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI67930     Document Type: Article

References (69)

1. Hoffman R, et al. Hematology: Basic Principles and Practice. 5th ed. London, United Kingdom: Churchill Livingstone; 2009.
2. Voskaridou E, et al. The effect of prolonged administration of hydroxyurea on morbidity and mortality in adult patients with sickle cell syndromes: results of a 17-year, single-center trial (LaSHS). Blood. 2010;115(12):2354-2363.
3. Eaton WA, Hofrichter J. Hemoglobin S gelation and sickle cell disease. Blood. 1987;70(5):1245-1266.
4. Stamatoyannopoulos G, Majerus PW, Perlmutter RM, Varmus H, eds. Molecular Basis of Blood Diseases. 3rd ed. Philadelphia, Pennsylvania, USA: WB Saunders; 2001.
5. Bolaños-Meade J, Brodsky RA. Blood and marrow transplantation for sickle cell disease: overcoming barriers to success. Curr Opin Oncol. 2009;21(2):158-161.
6. Rees DC, Williams TN, Gladwin MT. Sickle-cell disease. Lancet. 2010;376(9757):2018-2031.
7. Shenoy S. Hematopoietic stem cell transplantation for sickle cell disease: current practice and emerging trends. Hematology Am Soc Hematol Educ Program. 2011;2011:273-279.
8. Kamani NR, et al. Unrelated donor cord blood transplantation for children with severe sickle cell disease: results of one cohort from the phase II study from the Blood and Marrow Transplant Clinical Trials Network (BMT CTN). Biol Blood Marrow Transplant. 2012;18(8):1265-1272.
9. Locatelli F, Pagliara D. Allogeneic hematopoietic stem cell transplantation in children with sickle cell disease. Pediatr Blood Cancer. 2012;59(2):372-376.
10. Abboud M, Laver J, Blau CA. Granulocytosis causing sickle-cell crisis. Lancet. 1998;351(9107):959.
11. Adler BK, et al. Fatal sickle cell crisis after granulocyte colony-stimulating factor administration. Blood. 2001;97(10):3313-3314.
12. Fitzhugh CD, Hsieh MM, Bolan CD, Saenz C, Tisdale JF. Granulocyte colony-stimulating factor (G-CSF) administration in individuals with sickle cell disease: time for a moratorium? Cytotherapy. 2009;11(4):464-471.
13. Neumayr L, et al. Surgery in patients with hemoglobin SC disease. Preoperative Transfusion in Sickle Cell Disease Study Group. Am J Hematol. 1998;57(2):101-108.
14. Lisowski L, Sadelain M. Current status of globin gene therapy for the treatment of β-thalassaemia. Br J Haematol. 2008;141(3):335-345.
15. Gelinas RE, Bender MA, Miller AD, Novak U. Long-term expression of the human β-globin gene after retroviral transfer into pluripotent hematopoietic stem cells of the mouse. Adv Exp Med Biol. 1989;271:135-148.
16. Gelinas RE, Bender MA, Miller AD, Novak U. Regulated expression of the human β-globin gene after retroviral transfer into murine and human hematopoietic cells. Prog Clin Biol Res. 1989;316B:235-249.
17. May C, et al. Therapeutic haemoglobin synthesis in β-thalassaemic mice expressing lentivirus-encoded human β-globin. Nature. 2000;406(6791):82-86.
18. Pawliuk R, et al. Correction of sickle cell disease in transgenic mouse models by gene therapy. Science. 2001;294(5550):2368-2371.
19. Levasseur DN, Ryan TM, Pawlik KM, Townes TM. Correction of a mouse model of sickle cell disease: lentiviral/antisickling β-globin gene transduction of unmobilized, purified hematopoietic stem cells. Blood. 2003;102(13):4312- 4319.
20. Hanawa H, Hargrove PW, Kepes S, Srivastava DK, Nienhuis AW, Persons DA. Extended β-globin locus control region elements promote consistent therapeutic expression of a γ-globin lentiviral vector in murine β-thalassemia. Blood. 2004;104(8):2281-2290.
21. Puthenveetil G, et al. Successful correction of the human β-thalassemia major phenotype using a lentiviral vector. Blood. 2004;104(12):3445-3453.
22. Miccio A, et al. In vivo selection of genetically modified erythroblastic progenitors leads to long-term correction of β-thalassemia. Proc Natl Acad Sci U S A. 2008;105(30):10547-10552.
23. Pestina TI, Hargrove PW, Jay D, Gray JT, Boyd KM, Persons DA. Correction of murine sickle cell disease using γ-globin lentiviral vectors to mediate high-level expression of fetal hemoglobin. Mol Ther. 2008;17(2):245-252.
24. Platt OS, et al. Mortality in sickle cell disease. Life expectancy and risk factors for early death. N Engl J Med. 1994;330(23):1639-1644.
25. Chakalova L, et al. The Corfu deltaβ-thalassemia deletion disrupts γ-globin gene silencing and reveals post-transcriptional regulation of HbF expression. Blood. 2005;105(5):2154-2160.
26. Russell JE. A post-transcriptional process contributes to efficient γ-globin gene silencing in definitive erythroid cells. Eur J Haematol. 2007;79(6):516-525.
27. Persons DA, Hargrove PW, Allay ER, Hanawa H, Nienhuis AW. The degree of phenotypic correction of murine β-thalassemia intermedia following lentiviral- mediated transfer of a human γ-globin gene is influenced by chromosomal position effects and vector copy number. Blood. 2002;101(6):2175- 2183.
28. Perumbeti A, et al. A novel human γ-globin gene vector for genetic correction of sickle cell anemia in a humanized sickle mouse model: critical determinants for successful correction. Blood. 2009;114(6):1174-1185.
29. Breda L, et al. Therapeutic hemoglobin levels after gene transfer in β-thalassemia mice and in hematopoietic cells of β-thalassemia and sickle cells disease patients. PLoS One. 2012;7(3):e32345.
30. Nagel RL, et al. Structural bases of the inhibitory effects of hemoglobin F and hemoglobin A2 on the polymerization of hemoglobin S. Proc Natl Acad Sci USA. 1979;76(2):670-672.
31. Cavazzana-Calvo M, et al. Transfusion independence and HMGA2 activation after gene therapy of human β-thalassaemia. Nature. 2010; 467(7313):318-322.
32. McCune SL, Reilly MP, Chomo MJ, Asakura T, Townes TM. Recombinant human hemoglobins designed for gene therapy of sickle cell disease. Proc Natl Acad Sci USA. 1994;91(21):9852-9856.
33. Levasseur DN, Ryan TM, Reilly MP, McCune SL, Asakura T, Townes TM. A recombinant human hemoglobin with anti-sickling properties greater than fetal hemoglobin. J Biol Chem. 2004;279(26):27518-27524.
34. Giarratana MC, et al. Ex vivo generation of fully mature human RBCs from hematopoietic stem cells. Nat Biotechnol. 2004;23(1):69-74.
35. Dull T, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol. 1998;72(11):8463-8471.
36. Ramezani A, Hawley TS, Hawley RG. Combinatorial incorporation of enhancer-blocking components of the chicken β-globin 5'HS4 and human T-cell receptor alpha/delta BEAD-1 insulators in selfinactivating retroviral vectors reduces their genotoxic potential. Stem Cells. 2008;26(12):3257-3266.
37. Sastry L, Johnson T, Hobson MJ, Smucker B, Cornetta K. Titering lentiviral vectors: comparison of DNA, RNA and marker expression methods. Gene Ther. 2002;9(17):1155-1162.
38. Bell AC, West AG, Felsenfeld G. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell. 1999;98(3):387-396.
39. Witcher M, Emerson BM. Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. Mol Cell. 2009;34(3):271-284.
40. Bell AC, Felsenfeld G. Methylation of a CTCFdependent boundary controls imprinted expression of the Igf2 gene. Nature. 2000;405(6785):482-485.
41. Croizat H, Nagel RL. Circulating BFU-E in sickle cell anemia: relationship to percent fetal hemoglobin and BPA-like activity. Exp Hematol. 1988;16(11):946-949.
42. Douay L, Giarratana MC. Ex vivo generation of human red blood cells: a new advance in stem cell engineering. Methods Mol Biol. 2009;482:127-140.
43. Migliaccio G, et al. In vitro mass production of human erythroid cells from the blood of normal donors and of thalassemic patients. Blood Cells Mol Dis. 2002;28(2):169-180.
44. Higgins ME, Claremont M, Major JE, Sander C, Lash AE. CancerGenes: a gene selection resource for cancer genome projects. Nucleic Acids Res. 2007;35(Database issue):D721-D726.
45. Candotti F, et al. Gene therapy for adenosine deaminase-deficient severe combined immune deficiency: clinical comparison of retroviral vectors and treatment plans. Blood. 2012;1(18):3635-3646.
46. Modlich U, et al. Cell-culture assays reveal the importance of retroviral vector design for insertional genotoxicity. Blood. 2006;108(8):2545-2553.
47. Walters MC, et al. Stable mixed hematopoietic chimerism after bone marrow transplantation for sickle cell anemia. Biol Blood Marrow Transplant. 2001;7(12):665-673.
48. Andreani M, et al. Quantitatively different red cell/ nucleated cell chimerism in patients with long-term, persistent hematopoietic mixed chimerism after bone marrow transplantation for thalassemia major or sickle cell disease. Haematologica. 2010;96(1):128-133.
49. Wu CJ, et al. Mixed haematopoietic chimerism for sickle cell disease prevents intravascular haemolysis. Br J Haematol. 2007;139(3):504-507.
50. Krishnamurti L, et al. Stable long-term donor engraftment following reduced-intensity hematopoietic cell transplantation for sickle cell disease. Biol Blood Marrow Transplant. 2008;14(11):1270-1278.
51. Charache S, Dover GJ, Moyer MA, Moore JW. Hydroxyurea-induced augmentation of fetal hemoglobin production in patients with sickle cell anemia. Blood. 1987;69(1):109-116.
52. Cartier N, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science. 2009;326(5954):818-823.
53. Lisowski L, Sadelain M. Locus control region elements HS1 and HS4 enhance the therapeutic efficacy of globin gene transfer in β-thalassemic mice. Blood. 2007;110(13):4175-4178.
54. Emery DW, Yannaki E, Tubb J, Stamatoyannopoulos G. A chromatin insulator protects retrovirus vectors from chromosomal position effects. Proc Natl Acad Sci USA. 2000;97(16):9150-9155.
55. Raab JR, Kamakaka RT. Insulators and promoters: closer than we think. Nat Rev Genet. 2010;11(6):439-446.
56. Lobanenkov VV, et al. A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5'-flanking sequence of the chicken c-myc gene. Oncogene. 1990;5(12):1743-1753.
57. Filippova GN, et al. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol Cell Biol. 1996;16(6):2802-2813.
58. Vostrov AA, Quitschke WW. The zinc finger protein CTCF binds to the APBβ domain of the amyloid β-protein precursor promoter. Evidence for a role in transcriptional activation. J Biol Chem. 1997;272(52):33353-33359.
59. Brunak S, Engelbrecht J, Knudsen S. Prediction of human mRNA donor and acceptor sites from the DNA sequence. J Mol Biol. 1991;220(1):49-65.
60. Wu X, Li Y, Crise B, Burgess SM. Transcription start regions in the human genome are favored targets for MLV integration. Science. 2003;300(5626):1749- 1751.
61. Suzuki J, Fujita J, Taniguchi S, Sugimoto K, Mori KJ. Characterization of murine hemopoietic-supportive (MS-1 and MS-5) and non-supportive (MS-K) cell lines. Leukemia. 1992;6(5):452-458.
62. Cooper AR, Patel S, Senadheera S, Plath K, Kohn DB, Hollis RP. Highly efficient large-scale lentiviral vector concentration by tandem tangential flow filtration. J Virol Methods. 2011;177(1):1-9.
63. Paruzynski A, et al. Genome-wide high-throughput integrome analyses by nrLAM-PCR and next-generation sequencing. Nat Protoc. 2010;5(8):1379-1395.
64. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25.
65. Tukey JW. Variances of variance components: II. The unbalanced single classification. Ann Math Statist. 1957;28(1):43-56.
66. Snedecor GW, Cochran WG. Statistical Methods. 7th ed. Ames, Iowa, USA: Iowa State University Press; 1989.
67. Lehmann EL, D'Abrera HJM. Nonparametrics: Statistical Methods Based on Ranks. New York, New York, USA: Springer; 2006.
68. Fisher RA. On the interpretation of ?2 from contingency tables, and the calculation of P. J R Stat Soc. 1922;85(1):87-94.
69. SAS Institute. SAS/STAT 9.3 User's Guide:: The REG Procedure (Chapter). Carey, North Carolina, USA: SAS Institute, Inc.; 2011.