Gene therapy for inherited immunodeficiency

Expert Opinion on Biological Therapy

Volumn 14, Issue 6, 2014, Pages 789-798

  Touzot, Fabien ^a,b,c,d   Hacein Bey Abina, Salima ^a,b,c,d   Fischer, Alain ^a,b   Cavazzana, Marina ^a,b,c,d  

^a INSERM   (France)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

Adenosine deaminase; Chronic granulomatous disease; Gene therapy; Lentiviral vectors; Primary immunodeficiency; Severe combined immunodeficiency; Wiskott Aldrich syndrome

Indexed keywords

LENTIVIRUS VECTOR; RETROVIRUS VECTOR; ADENOSINE DEAMINASE;

ADENOSINE DEAMINASE DEFICIENCY; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; CHRONIC GRANULOMATOUS DISEASE; CLINICAL TRIAL (TOPIC); DRUG EFFICACY; DRUG SAFETY; GENOTOXICITY; HUMAN; IMMUNE DEFICIENCY; NONHUMAN; PROMOTER REGION; REVIEW; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; WISKOTT ALDRICH SYNDROME; X LINKED SEVERE COMBINED IMMUNODEFICIENCY; AGAMMAGLOBULINEMIA; ANIMAL; DEFICIENCY; FORECASTING; GENE THERAPY; GENETICS; GRANULOMATOUS DISEASE, CHRONIC; IMMUNOLOGY; SEVERE COMBINED IMMUNODEFICIENCY; TREATMENT OUTCOME; WISKOTT-ALDRICH SYNDROME; X-LINKED COMBINED IMMUNODEFICIENCY DISEASES;

ADENOSINE DEAMINASE; AGAMMAGLOBULINEMIA; ANIMALS; FORECASTING; GENETIC THERAPY; GRANULOMATOUS DISEASE, CHRONIC; HUMANS; SEVERE COMBINED IMMUNODEFICIENCY; TREATMENT OUTCOME; WISKOTT-ALDRICH SYNDROME; X-LINKED COMBINED IMMUNODEFICIENCY DISEASES;

EID: 84900798957     PISSN: 14712598     EISSN: 17447682     Source Type: Journal    
DOI: 10.1517/14712598.2014.895811     Document Type: Review

References (81)

1. Slatter MA, Gennery AR. Advances in hematopoietic stem cell transplantation for primary immunodeficiency. Expert Rev Clin Immunol 2013;9(10):991-9
2. Buckley RH. Molecular defects in human severe combined immunodeficiency and approaches to immune reconstitution. Annu Rev Immunol 2004;22:625-55
3. Rochman Y, Spolski R, Leonard WJ. New insights into the regulation of T cells by gamma(c) family cytokines. Nat Rev Immunol 2009;9(7):480-90
4. Bousso P, Wahn V, Douagi I, et al. Diversity, functionality, and stability of the T cell repertoire derived in vivo from a single human T cell precursor. Proc Natl Acad Sci USA 2000;97(1):274-8
5. Soudais C, Shiho T, Sharara LI, et al. Stable and functional lymphoid reconstitution of common cytokine receptor gamma chain deficient mice by retroviral-mediated gene transfer. Blood 2000;95(10):3071-7
6. Hacein-Bey S, Basile GD, Lemerle J, et al. gammac gene transfer in the presence of stem cell factor, FLT-3L, interleukin-7 (IL-7), IL-1, and IL-15 cytokines restores T-cell differentiation from gammac(-) X-linked severe combined immunodeficiency hematopoietic progenitor cells in murine fetal thymic organ cultures. Blood 1998;92(11):4090-7
7. Hacein-Bey-Abina S, Hauer J, Lim A, et al. Efficacy of gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2010;363(4):355-64
8. Gaspar HB, Cooray S, Gilmour KC, et al. Long-term persistence of a polyclonal T cell repertoire after gene therapy for X-linked severe combined immunodeficiency. Sci Transl Med 2011;3(97):97ra79
9. Thrasher AJ, Hacein-Bey-Abina S, Gaspar HB, et al. Failure of SCID-X1 gene therapy in older patients. Blood 2005;105(11):4255-7
10. Chinen J, Davis J, De Ravin SS, et al. Gene therapy improves immune function in preadolescents with X-linked severe combined immunodeficiency. Blood 2007;110(1):67-73
11. Brière F, Servet-Delprat C, Bridon JM, et al. Human interleukin 10 induces naive surface immunoglobulin D+ (sIgD +) B cells to secrete IgG1 and IgG3. J Exp Med 1994;179(2):757-62
12. Avery DT, Deenick EK, Ma CS, et al. B cell-intrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans. J Exp Med 2010;207(1):155-71
13. Kotlarz D, Ziȩtara N, Uzel G, et al. Loss-of-function mutations in the IL-21 receptor gene cause a primary immunodeficiency syndrome. J Exp Med 2013;210(3):433-43
14. Howe SJ, Mansour MR, Schwarzwaelder K, et al. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J Clin Invest 2008;118(9):3143-50
15. Hacein-Bey-Abina S, Garrigue A, Wang GP, et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest 2008;118(9):3132-42
16. Wang GP, Berry CC, Malani N, et al. Dynamics of gene-modified progenitor cells analyzed by tracking retroviral integration sites in a human SCID-X1 gene therapy trial. Blood 2010;115(22):4356-66
17. Fischer A, Abina SH-B, Thrasher A, et al. LMO2 and gene therapy for severe combined immunodeficiency. N Engl J Med 2004;350(24):2526-7; author reply 2526-2527
18. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003;302(5644):415-19
19. Gaspar HB, Cooray S, Gilmour KC, et al. Hematopoietic stem cell gene therapy for adenosine deaminase-deficient severe combined immunodeficiency leads to long-term immunological recovery and metabolic correction. Sci Transl Med 2011;3(97):97ra80
20. Aiuti A, Cattaneo F, Galimberti S, et al. Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N Engl J Med 2009;360(5):447-58
21. Aiuti A, Cassani B, Andolfi G, et al. Multilineage hematopoietic reconstitution without clonal selection in ADA-SCID patients treated with stem cell gene therapy. J Clin Invest 2007;117(8):2233-40
22. Cassani B, Montini E, Maruggi G, et al. Integration of retroviral vectors induces minor changes in the transcriptional activity of T cells from ADA-SCID patients treated with gene therapy. Blood 2009;114(17):3546-56
23. Gaspar HB, Aiuti A, Porta F, et al. How I treat ADA deficiency. Blood 2009;114(17):3524-32
24. Hassan A, Booth C, Brightwell A, et al. Outcome of hematopoietic stem cell transplantation for adenosine deaminase-deficient severe combined immunodeficiency. Blood 2012;120(17):3615-24; quiz 3626
25. Aiuti A, Slavin S, Aker M, et al. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 2002;296(5577):2410-13
26. Montiel-Equihua CA, Thrasher AJ, Gaspar HB. Gene therapy for severe combined immunodeficiency due to adenosine deaminase deficiency. Curr Gene Ther 2012;12(1):57-65
27. Candotti F, Shaw KL, Muul L, et al. Gene therapy for adenosine deaminase-deficient severe combined immune deficiency: clinical comparison of retroviral vectors and treatment plans. Blood 2012;120(18):3635-46
28. Thrasher AJ, Burns SO. WASP: a key immunological multitasker. Nat Rev Immunol 2010;10(3):182-92
29. Bosticardo M, Marangoni F, Aiuti A, et al. Recent advances in understanding the pathophysiology of Wiskott-Aldrich syndrome. Blood 2009;113(25):6288-95
30. Mahlaoui N, Pellier I, Mignot C, et al. Characteristics and outcome of early-onset, severe forms of Wiskott-Aldrich syndrome. Blood 2013;121(9):1510-16
31. Moratto D, Giliani S, Bonfim C, et al. Long-term outcome and lineage-specific chimerism in 194 patients with Wiskott-Aldrich syndrome treated by hematopoietic cell transplantation in the period 1980-2009: an international collaborative study. Blood 2011;118(6):1675-84
32. Shin CR, Kim M-O, Li D, et al. Outcomes following hematopoietic cell transplantation for Wiskott-Aldrich syndrome. Bone Marrow Transplant 2012;47(11):1428-35
33. Boztug K, Schmidt M, Schwarzer A, et al. Stem-cell gene therapy for the Wiskott-Aldrich syndrome. N Engl J Med 2010;363(20):1918-27
34. Avedillo Díez I, Zychlinski D, Coci EG, et al. Development of novel efficient SIN vectors with improved safety features for Wiskott-Aldrich syndrome stem cell based gene therapy. Mol Pharm 2011;8(5):1525-37
35. Corrigan-Curay J, Cohen-Haguenauer O, O'Reilly M, et al. Challenges in vector and trial design using retroviral vectors for long-term gene correction in hematopoietic stem cell gene therapy. Mol Ther 2012;20(6):1084-94
36. Naldini L. Ex vivo gene transfer and correction for cell-based therapies. Nat Rev Genet 2011;12(5):301-15
37. Dupré L, Trifari S, Follenzi A, et al. Lentiviral vector-mediated gene transfer in T cells from Wiskott-Aldrich syndrome patients leads to functional correction. Mol Ther 2004;10(5):903-15
38. Galy A, Roncarolo M-G, Thrasher AJ. Development of lentiviral gene therapy for Wiskott Aldrich syndrome. Expert Opin Biol Ther 2008;8(2):181-90
39. Marangoni F, Bosticardo M, Charrier S, et al. Evidence for long-term efficacy and safety of gene therapy for Wiskott-Aldrich syndrome in preclinical models. Mol Ther 2009;17(6):1073-82
40. Aiuti A, Biasco L, Scaramuzza S, et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 2013;341(6148):1233151
41. Winkelstein JA, Marino MC, Johnston RB Jr, et al. Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore) 2000;79(3):155-69
42. Martire B, Rondelli R, Soresina A, et al. Clinical features, long-term follow-up and outcome of a large cohort of patients with Chronic Granulomatous Disease: an Italian multicenter study. Clin Immunol 2008;126(2):155-64
43. Beauté J, Obenga G, Le Mignot L, et al. Epidemiology and outcome of invasive fungal diseases in patients with chronic granulomatous disease: a multicenter study in France. Pediatr Infect Dis J 2011;30(1):57-62
44. Kuhns DB, Alvord WG, Heller T, et al. Residual NADPH oxidase and survival in chronic granulomatous disease. N Engl J Med 2010;363(27):2600-10
45. Martinez CA, Shah S, Shearer WT, et al. Excellent survival after sibling or unrelated donor stem cell transplantation for chronic granulomatous disease. J Allergy Clin Immunol 2012;129(1):176-83
46. Cole T, Pearce MS, Cant AJ, et al. Clinical outcome in children with chronic granulomatous disease managed conservatively or with hematopoietic stem cell transplantation. J Allergy Clin Immunol 2013;132(5):1150-5
47. Güngör T, Teira P, Slatter M, et al. Reduced-intensity conditioning and HLA-matched haemopoietic stem-cell transplantation in patients with chronic granulomatous disease: a prospective multicentre study. Lancet 2014;383(9915):436-48
48. Grez M, Reichenbach J, Schwäble J, et al. Gene therapy of chronic granulomatous disease: the engraftment dilemma. Mol Ther 2011;19(1):28-35
49. Stein S, Ott MG, Schultze-Strasser S, et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med 2010;16(2):198-204
50. Kang EM, Choi U, Theobald N, et al. Retrovirus gene therapy for X-linked chronic granulomatous disease can achieve stable long-term correction of oxidase activity in peripheral blood neutrophils. Blood 2010;115(4):783-91
51. Kang HJ, Bartholomae CC, Paruzynski A, et al. Retroviral gene therapy for X-linked chronic granulomatous disease: results from phase I/II trial. Mol Ther 2011;19(11):2092-101
52. Bedard K, Krause K-H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007;87(1):245-313
53. Santilli G, Almarza E, Brendel C, et al. Biochemical correction of X-CGD by a novel chimeric promoter regulating high levels of transgene expression in myeloid cells. Mol Ther 2011;19(1):122-32
54. Yu SF, von Rüden T, Kantoff PW, et al. Self-inactivating retroviral vectors designed for transfer of whole genes into mammalian cells. Proc Natl Acad Sci USA 1986;83(10):3194-8
55. Naldini L, Blömer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996;272(5259):263-7
56. Dull T, Zufferey R, Kelly M, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol 1998;72(11):8463-71
57. 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):1749-51
58. Wang GP, Levine BL, Binder GK, et al. Analysis of lentiviral vector integration in HIV+ study subjects receiving autologous infusions of gene modified CD4+ T cells. Mol Ther 2009;17(5):844-50
59. Marodon G, Mouly E, Blair EJ, et al. Specific transgene expression in human and mouse CD4+ cells using lentiviral vectors with regulatory sequences from the CD4 gene. Blood 2003;101(9):3416-23
60. Moreau T, Bardin F, Imbert J, et al. Restriction of transgene expression to the B-lymphoid progeny of human lentivirally transduced CD34+ cells. Mol Ther 2004;10(1):45-56
61. Anliker B, Abel T, Kneissl S, et al. Specific gene transfer to neurons, endothelial cells and hematopoietic progenitors with lentiviral vectors. Nat Methods 2010;7(11):929-35
62. Bartelink IH, Boelens JJ, Bredius RGM, et al. Body weight-dependent pharmacokinetics of busulfan in paediatric haematopoietic stem cell transplantation patients: towards individualized dosing. Clin Pharmacokinet 2012;51(5):331-45
63. Jin P, Wang E, Ren J, et al. Differentiation of two types of mobilized peripheral blood stem cells by microRNA and cDNA expression analysis. J Transl Med 2008;6:39
64. Yannaki E, Karponi G, Zervou F, et al. Hematopoietic stem cell mobilization for gene therapy: superior mobilization by the combination of granulocyte-colony stimulating factor plus plerixafor in patients with beta-thalassemia major. Hum Gene Ther 2013;24(10):852-60
65. Devine SM, Vij R, Rettig M, et al. Rapid mobilization of functional donor hematopoietic cells without G-CSF using AMD3100, an antagonist of the CXCR4/SDF-1 interaction. Blood 2008;112(4):990-8
66. Huang J, Nguyen-McCarty M, Hexner EO, et al. Maintenance of hematopoietic stem cells through regulation of Wnt and mTOR pathways. Nat Med 2012;18(12):1778-85
67. Bibikova M, Beumer K, Trautman JK, Carroll D. Enhancing gene targeting with designed zinc finger nucleases. Science 2003;300(5620):764
68. Wood AJ, Lo T-W, Zeitler B, et al. Targeted genome editing across species using ZFNs and TALENs. Science 2011;333(6040):307
69. Pessach IM, Notarangelo LD. Gene therapy for primary immunodeficiencies: looking ahead, toward gene correction. J Allergy Clin Immunol 2011;127(6):1344-50
70. Lombardo A, Genovese P, Beausejour CM, et al. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 2007;25(11):1298-306
71. Zou J, Sweeney CL, Chou B-K, et al. Oxidase-deficient neutrophils from X-linked chronic granulomatous disease iPS cells: functional correction by zinc finger nuclease-mediated safe harbor targeting. Blood 2011;117(21):5561-72
72. Al-Herz W, Bousfiha A, Casanova J-L, et al. Primary immunodeficiency diseases: an update on the classification from the international union of immunological societies expert committee for primary immunodeficiency. Front Immunol 2011;2:54
73. Benjelloun F, Garrigue A, Demerens-de Chappedelaine C, et al. Stable and functional lymphoid reconstitution in artemis-deficient mice following lentiviral artemis gene transfer into hematopoietic stem cells. Mol Ther 2008;16(8):1490-9
74. Mostoslavsky G, Fabian AJ, Rooney S, et al. Complete correction of murine Artemis immunodeficiency by lentiviral vector-mediated gene transfer. Proc Natl Acad Sci USA 2006;103(44):16406-11
75. Pike-Overzet K, Rodijk M, Ng Y-Y, et al. Correction of murine Rag1 deficiency by self-inactivating lentiviral vector-mediated gene transfer. Leukemia 2011;25(9):1471-83
76. Van Til NP, de Boer H, Mashamba N, et al. Correction of murine Rag2 severe combined immunodeficiency by lentiviral gene therapy using a codon-optimized RAG2 therapeutic transgene. Mol Ther 2012;20(10):1968-80
77. Bauer TR Jr, Tuschong LM, Calvo KR, et al. Long-term follow-up of foamy viral vector-mediated gene therapy for canine leukocyte adhesion deficiency. Mol Ther 2013;21(5):964-72
78. Rivat C, Booth C, Alonso-Ferrero M, et al. SAP gene transfer restores cellular and humoral immune function in a murine model of X-linked lymphoproliferative disease. Blood 2013;121(7):1073-6
79. Zufferey R, Dull T, Mandel RJ, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998;72(12):9873-80
80. Miller PH, Knapp DJHF, Eaves CJ. Heterogeneity in hematopoietic stem cell populations: implications for transplantation. Curr Opin Hematol 2013;20(4):257-64
81. Knapp DJ, Eaves CJ. Control of the hematopoietic stem cell state. Cell Res 2014;24(1):3-4