Gene Therapy for Severe Combined Immunodeficiency due to Adenosine Deaminase Deficiency

Current Gene Therapy

Volumn 12, Issue 1, 2012, Pages 57-65

  Montiel Equihua, Claudia A ^a   Thrasher, Adrian J ^a   Gaspar, H Bobby ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Adenosine deaminase; Clinical trial; Gene therapy; Hematopoietic stem cell; Retrovirus; Severe combined immunodeficiency

Indexed keywords

PEGADEMASE; RETROVIRUS VECTOR;

ADENOSINE DEAMINASE DEFICIENCY; ARTICLE; CLINICAL ARTICLE; ENZYME REPLACEMENT; GENE TARGETING; GENE THERAPY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; STEM CELL GENE THERAPY;

EID: 84858308338     PISSN: 15665232     EISSN: 18755631     Source Type: Journal    
DOI: 10.2174/156652312799789253     Document Type: Article

References (65)

1. Hershfield MS, Mitchell BS. Immunodeficiency diseases caused by adenosine deaminase deficiency and purine nucleoside phosphorylase deficiency. In: Scriver CR, Beaud et al, Sly WS, Valle D, editors. The Metabolic and Molecular Basis of Inherited Disease.New York: McGraw-Hill; 1995. p. 1725-68.
2. Cederbaum SD, Kaitila I, Rimoin DL, Stiehm ER. The chondroosseous dysplasia of adenosine deaminase deficiency with severe combined immunodeficiency. J Pediatr 1976; 89(5): 737-42.
3. Bollinger ME, rredondo-Vega FX, Santisteban I, Schwarz K, Hershfield MS, Lederman HM. Brief report: hepatic dysfunction as a complication of adenosine deaminase deficiency. N Engl J Med 1996; 334(21): 1367-71.
4. Nofech-Mozes Y, Blaser SI, Kobayashi J, Grunebaum E, Roifman CM. Neurologic abnormalities in patients with adenosine deaminase deficiency. Pediatr Neurol 2007; 37(3): 218-21.
5. Hurley MC, Lin B, Fox IH. Regulation of deoxyadenosine and nucleoside analog phosphorylation by human placental adenosine kinase. Adv Exp Med Biol 1986; 195 Pt B: 141-149.
6. Apasov SG, Blackburn MR, Kellems RE, Smith PT, Sitkovsky MV. Adenosine deaminase deficiency increases thymic apoptosis and causes defective T cell receptor signaling. J Clin Invest 2001; 108(1): 131-41.
7. Joachims ML, Marble PA, Laurent AB, Pastuszko P, Paliotta M, Blackburn MR, et al. Restoration of adenosine deaminase-deficient human thymocyte development in vitro by inhibition of deoxynucleoside kinases. J Immunol 2008; 181(11): 8153-61.
8. Gangi-Peterson L, Sorscher DH, Reynolds JW, Kepler TB, Mitchell BS. Nucleotide pool imbalance and adenosine deaminase deficiency induce alterations of N-region insertions during V(D)J recombination. J Clin Invest 1999; 103(6): 833-41.
9. Benveniste P, Zhu W, Cohen A. Interference with thymocyte differentiation by an inhibitor of S-adenosylhomocysteine hydrolase. J Immunol 1995; 155(2): 536-44.
10. Sauer AV, Mrak E, Hernandez RJ, Zacchi E, Cavani F, Casiraghi M, et al. ADA-deficient SCID is associated with a specific microenvironment and bone phenotype characterized by RANKL/OPG imbalance and osteoblast insufficiency. Blood 2009; 114(15): 3216-26.
11. Hasko G, Linden J, Cronstein B, Pacher P. Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat Rev Drug Discov 2008; 7(9): 759-70.
12. Cassani B, Mirolo M, Cattaneo F, Benninghoff U, Hershfield M, Carlucci F, et al. Altered intracellular and extracellular signaling leads to impaired T-cell functions in ADA-SCID patients. Blood 2008; 111(8): 4209-19.
13. Blackburn MR, Volmer JB, Thrasher JL, Zhong H, Crosby JR, Lee JJ, et al. Metabolic consequences of adenosine deaminase deficiency in mice are associated with defects in alveogenesis, pulmonary inflammation, and airway obstruction. J Exp Med 2000; 192(2): 159-70.
14. Sun CX, Zhong H, Mohsenin A, Morschl E, Chunn JL, Molina JG, et al. Role of A2B adenosine receptor signaling in adenosine-dependent pulmonary inflammation and injury. J Clin Invest 2006; 116(8): 2173-82.
15. Young HW, Molina JG, Dimina D, Zhong H, Jacobson M, Chan LN, et al. A3 adenosine receptor signaling contributes to airway inflammation and mucus production in adenosine deaminase-deficient mice. J Immunol 2004; 173(2): 1380-9.
16. Ribeiro JA, Sebastiao AM, de Mendonca A. Adenosine receptors in the nervous system: pathophysiological implications. Progress in Neurobiology 2002; 68(6): 377-92.
17. Wei CJ, Li W, Chen JF. Normal and abnormal functions of adenosine receptors in the central nervous system revealed by genetic knockout studies. Biochimica et Biophysica Acta (BBA) -BiomembranesIn Press, Corrected Proof.
18. Turner CP, Seli M, Ment L, Stewart W, Yan H, Johansson B, et al. A1 adenosine receptors mediate hypoxia-induced ventriculomegaly. Proc Natl Acad Sci U S A 2003; 100(20): 11718-22.
19. Rogers MH, Lwin R, Fairbanks L, Gerritsen B, Gaspar HB. Cognitive and behavioral abnormalities in adenosine deaminase deficient severe combined immunodeficiency. J Pediatr 2001; 139(1): 44-50.
20. Titman P, Pink E, Skucek E, O'Hanlon K, Cole TJ, Gaspar J, et al. Cognitive and behavioral abnormalities in children after hematopoietic stem cell transplantation for severe congenital immunodeficiencies. Blood 2008; 112(9): 3907-13.
21. Gaspar HB, Aiuti A, Porta F, Candotti F, Hershfield MS, Notarangelo LD. How I treat ADA deficiency. Blood 2009.
22. Booth C, Gaspar HB. Pegademase bovine (PEG-ADA) for the treatment of infants and children with severe combined immunodeficiency (SCID). Biologics: Targets & Therapy 2009; 3: 349-58.
23. Chan B, Wara D, Bastian J, Hershfield MS, Bohnsack J, Azen CG, et al. Long-term efficacy of enzyme replacement therapy for adenosine deaminase (ADA)-deficient severe combined immunodeficiency (SCID). Clin Immunol 2005; 117(2): 133-43.
24. Malacarne F, Benicchi T, Notarangelo LD, Mori L, Parolini S, Caimi L, et al. Reduced thymic output, increased spontaneous apoptosis and oligoclonal B cells in polyethylene glycol-adenosine deaminase-treated patients. Eur J Immunol 2005; 35(11): 3376-86.
25. Serana F, Sottini A, Chiarini M, Zanotti C, Ghidini C, Lanfranchi A, et al. The different extent of B and T cell immune reconstitution after hematopoietic stem cell transplantation and enzyme replacement therapies in SCID patients with adenosine deaminase deficiency. J Immunol 2010; 185(12): 7713-22.
26. Mortellaro A, Hernandez RJ, Guerrini MM, Carlucci F, Tabucchi A, Ponzoni M, et al. Ex vivo gene therapy with lentiviral vectors rescues adenosine deaminase (ADA)-deficient mice and corrects their immune and metabolic defects. Blood 2006; 108(9): 2979-88.
27. Honig M, Albert MH, Schulz A, Sparber-Sauer M, Schutz C, Belohradsky B, et al. Patients with adenosine deaminase deficiency surviving after hematopoietic stem cell transplantation are at high risk of CNS complications. Blood 2007; 109(8): 3595-602.
28. R. In vivo reversion to normal of inherited mutations in humans. J Med Genet 2003; 40(10): 721-728.
29. Liu P, Santisteban I, Burroughs LM, Ochs HD, Torgerson TR, Hershfield MS, et al. Immunologic reconstitution during PEG-ADA therapy in an unusual mosaic ADA deficient patient. Clin Immunol 2009; 130(2): 162-74.
30. Hirschhorn R. Immunodeficiency due to adenosine deaminase. In: Ochs HD, Smith CIE, Puck JM, editors. Primary Immunodeficiency Diseases: A Molecular and Genetic Approach. Oxford University Press Inc, USA; 1998.
31. Daddona PE, Mitchell BS, Meuwissen HJ, Davidson BL, Wilson JM, Koller CA. Adenosine deaminase deficiency with normal immune function. An acidic enzyme mutation. J Clin Invest 1983; 72(2): 483-92.
32. Blaese RM, Culver KW, Miller AD, Carter CS, Fleisher T, Clerici M, et al. T lymphocyte-directed gene therapy for ADA- SCID: initial trial results after 4 years. Science 1995; 270(5235): 475-80.
33. Onodera M, Ariga T, Kawamura N, Kobayashi I, Ohtsu M, Yamada M, et al. Successful peripheral T-lymphocyte-directed gene transfer for a patient with severe combined immune deficiency caused by adenosine deaminase deficiency. Blood 1998; 91(1): 30-6.
34. Bordignon C, Notarangelo LD, Nobili N, Ferrari G, Casorati G, Panina P, et al. Gene therapy in peripheral blood lymphocytes and bone marrow for ADA- immunodeficient patients. Science 1995; 270(5235): 470-5.
35. Kohn DB, Weinberg KI, Nolta JA, Heiss LN, Lenarsky C, Crooks GM, et al. Engraftment of gene-modified umbilical cord blood cells in neonates with adenosine deaminase deficiency. Nat Med 1995; 1(10): 1017-23.
36. Hoogerbrugge PM, van B, V, Fischer A, Debree M, Le DF, Perignon JL, et al. Bone marrow gene transfer in three patients with adenosine deaminase deficiency. Gene Ther 1996; 3(2): 179-83.
37. Luens KM, Travis MA, Chen BP, Hill BL, Scollay R, Murray LJ. Thrombopoietin, kit ligand, and flk2/flt3 ligand together induce increased numbers of primitive hematopoietic progenitors from human CD34+Thy-1+Lin- cells with preserved ability to engraft SCID-hu bone. Blood 1998; 91(4): 1206-15.
38. Hanenberg H, Hashino K, Konishi H, Hock RA, Kato I, Williams DA. Optimization of fibronectin-assisted retroviral gene transfer into human CD34+ hematopoietic cells. Hum Gene Ther 1997; 8(18): 2193-206.
39. Aiuti A, Slavin S, Aker M, Ficara F, Deola S, Mortellaro A, et al. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 2002; 296(5577): 2410-3.
40. Aiuti A, Vai S, Mortellaro A, Casorati G, Ficara F, Andolfi G, et al. Immune reconstitution in ADA-SCID after PBL gene therapy and discontinuation of enzyme replacement. Nat Med 2002; 8(5): 423-5.
41. Aiuti A, Cattaneo F, Galimberti S, Benninghoff U, Cassani B, Callegaro L, et al. Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N Engl J Med 2009; 360(5): 447-58.
42. Gaspar HB, Bjorkegren E, Parsley K, Gilmour KC, King D, Sinclair J, et al. Successful reconstitution of immunity in ADA-SCID by stem cell gene therapy following cessation of PEG-ADA and use of mild preconditioning. Mol Ther 2006; 14(4): 505-13.
43. Gaspar HB, Cooray S, Gilmour KC, Parsley KL, Zhang F, Adams S, 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.
44. Aiuti A, Cassani B, Andolfi G, Mirolo M, Biasco L, Recchia A, 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.
45. Hacein-Bey-Abina S, Hauer J, Lim A, Picard C, Wang GP, Berry CC, et al. Efficacy of gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2010; 363(4): 355-64.
46. Howe SJ, Mansour MR, Schwarzwaelder K, Bartholomae C, Hubank M, Kempski H, 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.
47. 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.
48. Ott MG, Schmidt M, Schwarzwaelder K, Stein S, Siler U, Koehl U, et al. Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat Med 2006; 12(4): 401-9.
49. Stein S, Ott MG, Schultze-Strasser S, Jauch A, Burwinkel B, Kinner A, 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. Cassani B, Montini E, Maruggi G, Ambrosi A, Mirolo M, Selleri S, 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.
51. Biasco L, Ambrosi A, Pellin D, Bartholomae C, Brigida I, Roncarolo MG, et al. Integration profile of retroviral vector in gene therapy treated patients is cell-specific according to gene expression and chromatin conformation of target cell. EMBO Mol Med 2011; 3(2): 89-101.
52. Montini E, Cesana D, Schmidt M, Sanvito F, Bartholomae CC, Ranzani M, et al. The genotoxic potential of retroviral vectors is strongly modulated by vector design and integration site selection in a mouse model of HSC gene therapy. J Clin Invest 2009; 119(4): 964-75.
53. Schambach A, Bohne J, Chandra S, Will E, Margison GP, Williams DA, et al. Equal potency of gammaretroviral and lentiviral SIN vectors for expression of O6-methylguanine-DNA methyltransferase in hematopoietic cells. Mol Ther 2006; 13(2): 391-400.
54. Zychlinski D, Schambach A, Modlich U, Maetzig T, Meyer J, Grassman E, et al. Physiological Promoters Reduce the Genotoxic Risk of Integrating Gene Vectors. Mol Ther 2008.
55. Montini E, Cesana D, Schmidt M, Sanvito F, Ponzoni M, Bartholomae C, et al. Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat Biotechnol 2006; 24(6): 687-96.
56. Gothot A, Pyatt R, McMahel J, Rice S, Srour EF. Functional heterogeneity of human CD34(+) cells isolated in subcompartments of the G0 /G1 phase of the cell cycle. Blood 1997; 90(11): 4384-93.
57. Cartier N, Hacein-Bey-Abina S, Bartholomae CC, Veres G, Schmidt M, Kutschera I, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 2009; 326(5954): 818-23.
58. Cavazzana-Calvo M, Payen E, Negre O, Wang G, Hehir K, Fusil F, et al. Transfusion independence and HMGA2 activation after gene therapy of human beta-thalassaemia. Nature 2010; 467(7313): 318-22.
59. Carbonaro DA, Jin X, Cotoi D, Mi T, Yu XJ, Skelton DC, et al. Neonatal bone marrow transplantation of ADA-deficient SCID mice results in immunologic reconstitution despite low levels of engraftment and an absence of selective donor T lymphoid expansion. Blood 2008; 111(12): 5745-54.
60. Silva G, Poirot L, Galetto R, Smith J, Montoya G, Duchateau P, et al. Meganucleases and other tools for targeted genome engineering: perspectives and challenges for gene therapy. Curr Gene Ther 2011; 11(1): 11-27.
61. Urnov FD, Miller JC, Lee YL, Beausejour CM, Rock JM, Augustus S, et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 2005; 435(7042): 646-51.
62. Holt N, Wang J, Kim K, Friedman G, Wang X, Taupin V, et al. Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat Biotechnol 2010; 28(8): 839-47.
63. Jayathilaka K, Sheridan SD, Bold TD, Bochenska K, Logan HL, Weichselbaum RR, et al. A chemical compound that stimulates the human homologous recombination protein RAD51. Proc Natl Acad Sci U S A 2008; 105(41): 15848-53.
64. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, et al. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 2011; 29(2): 143-8.
65. Mussolino C, Morbitzer R, Lutge F, Dannemann N, Lahaye T, Cathomen T. A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 2011.