Lentivirus mediated correction of artemis-deficient severe combined immunodeficiency

Human Gene Therapy

Volumn 28, Issue 1, 2017, Pages 112-124

  Punwani, Divya ^a   Kawahara, Misako ^a   Yu, Jason ^a   Sanford, Ukina ^a   Roy, Sushmita ^a   Patel, Kiran ^a   Carbonaro, Denise A ^b   Karlen, Andrea D ^c   Khan, Sara ^a   Cornetta, Kenneth ^d   Rothe, Michael ^e   Schambach, Axel ^e   Kohn, Donald B ^b   Malech, Harry L ^f   McIvor, R Scott ^c   Puck, Jennifer M ^a   Cowan, Morton J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d INDIANA UNIVERSITY   (United States)

^e HANNOVER MEDICAL SCHOOL   (Germany)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Artemis; Gene therapy; Lentivirus; Radiation sensitivity; Severe combined immunodeficiency

Indexed keywords

ARTEMIS; CD34 ANTIGEN; COMPLEMENTARY DNA; EXONUCLEASE; LENTIVIRUS VECTOR; UNCLASSIFIED DRUG; DCLRE1C PROTEIN, HUMAN; DCLRE1C PROTEIN, MOUSE; ENDONUCLEASE; NUCLEAR PROTEIN;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANIMAL CELL; APLASIA; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; ENDOCRINE DISEASE; GRAFT REJECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LENTIVIRINAE; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PROMOTER REGION; RADIOSENSITIVITY; SEVERE COMBINED IMMUNODEFICIENCY; SHORT STATURE; SKIN FIBROBLAST; T LYMPHOCYTE; TRANSCRIPTION REGULATION; ADMINISTRATION AND DOSAGE; ANIMAL; CELL CULTURE; CYTOLOGY; DEFICIENCY; DISEASE MODEL; DNA REPAIR; FIBROBLAST; GAMMA RADIATION; GENE THERAPY; GENE VECTOR; GENETICS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; KNOCKOUT MOUSE; METABOLISM; MULTIMODALITY CANCER THERAPY; RADIATION RESPONSE; RADIATION TOLERANCE; SCID MOUSE;

ANIMALS; B-LYMPHOCYTES; CELLS, CULTURED; COMBINED MODALITY THERAPY; DISEASE MODELS, ANIMAL; DNA REPAIR; ENDONUCLEASES; FIBROBLASTS; GAMMA RAYS; GENETIC THERAPY; GENETIC VECTORS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; LENTIVIRUS; MICE; MICE, KNOCKOUT; MICE, SCID; NUCLEAR PROTEINS; RADIATION TOLERANCE; SEVERE COMBINED IMMUNODEFICIENCY; T-LYMPHOCYTES;

EID: 85009964387     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2016.064     Document Type: Article

References (45)

1. Al-Herz W, Bousfiha A, Casanova JL, et al. Primary immunodeficiency diseases: An update on the classification from the international union of immunological societies expert committee for primary immunodeficiency. Front Immunol 2014; 5: 162.
2. Kwan A, Abraham RS, Currier R, et al. Newborn screening for severe combined immunodeficiency in 11 screening programs in the United States. JAMA 2014;312: 729-738.
3. Brown L, Xu-Bayford J, Allwood Z, et al. Neonatal diagnosis of severe combined immunodeficiency leads to significantly improved survival outcome: The case for newborn screening. Blood 2011; 117: 3243-3246.
4. Puck JM. Laboratory technology for populationbased screening for severe combined immunodeficiency in neonates: The winner is T-cell receptor excision circles. J Allergy Clin Immunol 2012;129: 607-616.
5. Dvorak CC, Cowan MJ, Logan BR, et al. The natural history of children with severe combined immunodeficiency: Baseline features of the first fifty patients of the primary immune deficiency treatment consortium prospective study 6901. J Clin Immunol 2013;33: 1156-1164.
6. Pai SY, Logan BR, Griffith LM, et al. Transplantation outcomes for severe combined immunodeficiency, 2000-2009. N Engl J Med 2014;371: 434-446.
7. Dvorak CC, Hassan A, Slatter MA, et al. Comparison of outcomes of hematopoietic stem cell transplantation without chemotherapy conditioning by using matched sibling and unrelated donors for treatment of severe combined immunodeficiency. J Allergy Clin Immunol 2014;134: 935- 943.e15.
8. Bertrand Y, Landais P, Friedrich W, et al. Influence of severe combined immunodeficiency phenotype on the outcome of HLA non-identical, T-celldepleted bone marrow transplantation: A retrospective European survey from the European group for bone marrow transplantation and the european society for immunodeficiency. J Pediatr 1999;134: 740-748.
9. Moshous D, Li L, Chasseval R, et al. A new gene involved in DNA double-strand break repair and V(D)J recombination is located on human chromosome 10p. Hum Mol Gen 2000;9: 583-588.
10. Moshous D, Callebaut I, de Chasseval R, et al. Artemis, a novel DNA double-strand break repair/ V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 2001; 105: 177-186.
11. Murphy S, Hayward A, Troup G, Devor EJ, Coons T. Gene enrichment in an American Indian population: An excess of severe combined immunodeficiency disease. Lancet 1980;2: 502-505.
12. Li L, Drayna D, Hu D, et al. The gene for severe combined immunodeficiency disease in Athabascan-speaking Native Americans is located on chromosome 10p. Am J Hum Genet 1998;62: 136-144.
13. Li L, Moshous D, Zhou Y, et al. A founder mutation in Artemis, an SNM1-like protein, causes SCID in Athabascan-speaking Native Americans. J Immunol 2002;168: 6323-6239.
14. Kwan A, Hu D, Song M, et al. Successful newborn screening for SCID in the Navajo Nation. Clin Immunol 2015;158: 29-34.
15. O'Marcaigh AS, DeSantes K, Hu D, et al. Bone marrow transplantation for T-B- severe combined immunodeficiency disease in Athabascan-speaking native Americans. Bone Marrow Transplant 2001; 27: 703-709.
16. Dvorak CC, Cowan MJ. Radiosensitive severe combined immunodeficiency disease. Immunology and allergy clinics of North America 2010;30: 125-142.
17. Mostoslavsky G, Fabian AJ, Rooney S, Alt FW, Mulligan RC. Complete correction of murine Artemis immunodeficiency by lentiviral vectormediated gene transfer. Proc Natl Acad Sci U S A 2006;103: 16406-16411.
18. 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: 1490-1499.
19. Riviere J, Hauer J, Poirot L, et al. Variable correction of Artemis deficiency by I-Sce1- meganuclease-assisted homologous recombination in murine hematopoietic stem cells. Gene Ther 2014;21: 529-532.
20. Xiao Z, Dunn E, Singh K, Khan IS, Yannone SM, Cowan MJ. A non-leaky Artemis-deficient mouse that accurately models the human severe combined immune deficiency phenotype, including resistance to hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2009;15: 1-11.
21. Li L, Salido E, Zhou Y, et al. Targeted disruption of the Artemis murine counterpart results in SCID and defective V(D)J recombination that is partially corrected with bone marrow transplantation. J Immunol 2005;174: 2420-2428.
22. Multhaup MM, Podetz-Pedersen KM, Karlen AD, et al. Role of transgene regulation in ex vivo lentiviral correction of artemis deficiency. Hum Gene Ther 2015;26: 232-243.
23. Multhaup M, Karlen AD, Swanson DL, et al. Cytotoxicity associated with artemis overexpression after lentiviral vector-mediated gene transfer. Hum Gene Ther 2010;21: 865-875.
24. Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM. Development of a self-inactivating lentivirus vector. J Virol 1998;72: 8150-8157.
25. Carbonaro DA, Zhang L, Jin X, et al. Preclinical demonstration of lentiviral vector-mediated correction of immunological and metabolic abnormalities in models of adenosine deaminase deficiency. MolTher 2014;22: 607-622.
26. Charrier S, Ferrand M, Zerbato M, et al. Quantification of lentiviral vector copy numbers in individual hematopoietic colony-forming cells shows vector dose-dependent effects on the frequency and level of transduction. Gene Ther 2011;18: 479-487.
27. Zhang W, Muck-Hausl M, Wang J, et al. Integration profile and safety of an adenovirus hybrid-vector utilizing hyperactive sleeping beauty transposase for somatic integration. PLoS One 2013;8: E75344.
28. Modlich U, Bohne J, Schmidt M, et al. Cell-culture assays reveal the importance of retroviral vector design for insertional genotoxicity. Blood 2006; 108: 2545-53.
29. Multhaup M, Karlen AD, Swanson DL, et al. Cytotoxicity associated with artemis overexpression after lentiviral vector-mediated gene transfer. Hum Gene Ther 2010;21: 865-875.
30. Multhaup MM, Gurram S, Podetz-Pedersen KM, et al. Characterization of the human artemis promoter by heterologous gene expression in vitro and in vivo. DNA Cell Biol 2011;30: 751-761.
31. O'Driscoll M, Cerosaletti KM, Girard PM, et al. DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency. Mol Cell 2001;8: 1175-1185.
32. Cowan MJ, Gennery AR. Radiation-sensitive severe combined immunodeficiency: The arguments for and against conditioning before hematopoietic cell transplantation-what to do? J Allergy Clin Immunol 2015;136: 1178-1185.
33. Czechowicz A, Kraft D, Weissman IL, Bhattacharya D. Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science 2007;318: 1296-1299.
34. Schuetz C, Neven B, Dvorak CC, et al. SCID patients with ARTEMIS vs RAG deficiencies following HCT: Increased risk of late toxicity in ARTEMIS-deficient SCID. Blood 2014;123: 281-289.
35. Sottini A, Ghidini C, Zanotti C, et al. Simultaneous quantification of recent thymic T-cell and bone marrow B-cell emigrants in patients with primary immunodeficiency undergone to stem cell transplantation. Clin Immunol 2010;136: 217-227.
36. Sarzotti M, Patel DD, Li X, et al. T cell repertoire development in humans with SCID after nonablative allogeneic marrow transplantation. J Immunol 2003;170: 2711-8.
37. Rosenbloom KR, Armstrong J, Barber GP, et al. The UCSC Genome Browser database: 2015 update. Nucleic Acids Res 2015;43: D670-81.
38. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4: 44-57.
39. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009;37: 1-13.
40. Zychlinski D, Schambach A, Modlich U, et al. Physiological promoters reduce the genotoxic risk of integrating gene vectors. Mol Ther 2008;16: 718-725.
41. Aiuti A, Cattaneo F, Galimberti S, et al. Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N Engl J Med 2009;360: 447-58.
42. De Ravin SS, Wu X, Moir S, et al. Lentiviral hematopoietic stem cell gene therapy for X-linked severe combined immunodeficiency. Sci Transl Med 2016;8: 335ra57.
43. Neven B, Leroy S, Decaluwe H, et al. Long-term outcome after hematopoietic stem cell transplantation of a single-center cohort of 90 patients with severe combined immunodeficiency. Blood 2009;113: 4114-24.
44. Qasim W, Gaspar HB, Thrasher AJ. Progress and prospects: Gene therapy for inherited immunodeficiencies. Gene Ther 2009;16: 1285-1291.
45. 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: 3143-50.