Alpharetroviral vector-mediated gene therapy for X-CGD: Functional correction and lack of aberrant splicing

Molecular Therapy

Volumn 21, Issue 3, 2013, Pages 648-661

  Kaufmann, Kerstin B ^a   Brendel, Christian ^a   Suerth, Julia D ^b   Mueller Kuller, Uta ^a   Chen Wichmann, Linping ^a   Schwäble, Joachim ^a   Pahujani, Shweta ^a   Kunkel, Hana ^a   Schambach, Axel ^b   Baum, Christopher ^b   Grez, Manuel ^a  

^a INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR 1ALPHA; GLYCOPROTEIN GP 91; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; VIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CD34 SELECTION; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; EXON; GENE DOSAGE; GENE SEQUENCE; GENETIC TRANSCRIPTION; GRANULOMATOSIS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHENOTYPE; PROMOTER REGION; RETROVIRUS; TRANSCRIPTION INITIATION SITE; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRUS EXPRESSION; VIRUS REPLICATION;

MURINAE;

EID: 84875218155     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.249     Document Type: Article

References (48)

1. Segal, BH, Veys, P, Malech, H and Cowan, MJ (2011). Chronic granulomatous disease: lessons from a rare disorder. Biol Blood Marrow Transplant 17(1 Suppl): S123-S131.
2. Seger, RA (2008). Modern management of chronic granulomatous disease. Br J Haematol 140: 255-266.
3. Johnston, RB Jr (2001). Clinical aspects of chronic granulomatous disease. Curr Opin Hematol 8: 17-22.
4. Ott, MG, Schmidt, M, Schwarzwaelder, K, Stein, S, Siler, U, Koehl, U et al. (2006). Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat Med 12: 401-409.
5. Stein, S, Ott, MG, Schultze-Strasser, S, Jauch, A, Burwinkel, B, Kinner, A et al. (2010). Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med 16: 198-204.
6. Rivat, C, Santilli, G, Gaspar, HB and Thrasher, AJ (2012). Gene therapy for primary immunodeficiencies. Hum Gene Ther 23: 668-675.
7. Suerth, JD, Maetzig, T, Galla, M, Baum, C and Schambach, A (2010). Self-inactivating alpharetroviral vectors with a split-packaging design. J Virol 84: 6626-6635.
8. Suerth, JD, Maetzig, T, Brugman, MH, Heinz, N, Appelt, JU, Kaufmann, KB et al. (2012). Alpharetroviral self-inactivating vectors: long-term transgene expression in murine hematopoietic cells and low genotoxicity. Mol Ther 20: 1022-1032.
9. Mitchell, RS, Beitzel, BF, Schroder, AR, Shinn, P, Chen, H, Berry, CC et al. (2004). Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2: E234.
10. Narezkina, A, Taganov, KD, Litwin, S, Stoyanova, R, Hayashi, J, Seeger, C et al. (2004). Genome-wide analyses of avian sarcoma virus integration sites. J Virol 78: 11656-11663.
11. Derse, D, Crise, B, Li, Y, Princler, G, Lum, N, Stewart, C et al. (2007). Human T-cell leukemia virus type 1 integration target sites in the human genome: comparison with those of other retroviruses. J Virol 81: 6731-6741.
12. Barsov, EV and Hughes, SH (1996). Gene transfer into mammalian cells by a Rous sarcoma virus-based retroviral vector with the host range of the amphotropic murine leukemia virus. J Virol 70: 3922-3929.
13. Greger, JG, Katz, RA, Taganov, K, Rall, GF and Skalka, AM (2004). Transduction of terminally differentiated neurons by avian sarcoma virus. J Virol 78: 4902-4906.
14. Moiani, A, Paleari, Y, Sartori, D, Mezzadra, R, Miccio, A, Cattoglio, C et al. (2012). Lentiviral vector integration in the human genome induces alternative splicing and generates aberrant transcripts. J Clin Invest 122: 1653-1666.
15. Cesana, D, Sgualdino, J, Rudilosso, L, Merella, S, Naldini, L and Montini, E (2012). Whole transcriptome characterization of aberrant splicing events induced by lentiviral vector integrations. J Clin Invest 122: 1667-1676.
16. Cavazzana-Calvo, M, Payen, E, Negre, O, Wang, G, Hehir, K, Fusil, F et al. (2010). Transfusion independence and HMGA2 activation after gene therapy of human ß-thalassaemia. Nature 467: 318-322.
17. Moreno-Carranza, B, Gentsch, M, Stein, S, Schambach, A, Santilli, G, Rudolf, E et al. (2009). Transgene optimization significantly improves SIN vector titers, gp91phox expression and reconstitution of superoxide production in X-CGD cells. Gene Ther 16: 111-118.
18. Schambach, A, Bohne, J, Baum, C, Hermann, FG, Egerer, L, von Laer, D et al. (2006). Woodchuck hepatitis virus post-transcriptional regulatory element deleted from X protein and promoter sequences enhances retroviral vector titer and expression. Gene Ther 13: 641-645.
19. Schambach, A, Bohne, J, Chandra, S, Will, E, Margison, GP, Williams, DA et al. (2006). Equal potency of gammaretroviral and lentiviral SIN vectors for expression of O6-methylguanine-DNA methyltransferase in hematopoietic cells. Mol Ther 13: 391-400.
20. Zychlinski, D, Schambach, A, Modlich, U, Maetzig, T, Meyer, J, Grassman, E et al. (2008). Physiological promoters reduce the genotoxic risk of integrating gene vectors. Mol Ther 16: 718-725.
21. Zhou, S, Mody, D, DeRavin, SS, Hauer, J, Lu, T, Ma, Z et al. (2010). A self-inactivating lentiviral vector for SCID-X1 gene therapy that does not activate LMO2 expression in human T cells. Blood 116: 900-908.
22. Lombardo, A, Cesana, D, Genovese, P, Di Stefano, B, Provasi, E, Colombo, DF et al. (2011). Site-specific integration and tailoring of cassette design for sustainable gene transfer. Nat Methods 8: 861-869.
23. Zhang, F, Frost, AR, Blundell, MP, Bales, O, Antoniou, MN and Thrasher, AJ (2010). A ubiquitous chromatin opening element (UCOE) confers resistance to DNA methylation-mediated silencing of lentiviral vectors. Mol Ther 18: 1640-1649.
24. Zhen, L, King, AA, Xiao, Y, Chanock, SJ, Orkin, SH and Dinauer, MC (1993). Gene targeting of X chromosome-linked chronic granulomatous disease locus in a human myeloid leukemia cell line and rescue by expression of recombinant gp91phox. Proc Natl Acad Sci USA 90: 9832-9836.
25. Zentilin, L, Qin, G, Tafuro, S, Dinauer, MC, Baum, C and Giacca, M (2000). Variegation of retroviral vector gene expression in myeloid cells. Gene Ther 7: 153-166.
26. Heckl, D, Schwarzer, A, Haemmerle, R, Steinemann, D, Rudolph, C, Skawran, B et al. (2012). Lentiviral vector induced insertional haploinsufficiency of Ebf1 causes murine leukemia. Mol Ther 20: 1187-1195.
27. Montiel-Equihua, CA, Zhang, L, Knight, S, Saadeh, H, Scholz, S, Carmo, M et al. (2012). The ß-globin locus control region in combination with the EF1a short promoter allows enhanced lentiviral vector-mediated erythroid gene expression with conserved multilineage activity. Mol Ther 20: 1400-1409.
28. Santilli, G, Almarza, E, Brendel, C, Choi, U, Beilin, C, Blundell, MP et al. (2011). Biochemical correction of X-CGD by a novel chimeric promoter regulating high levels of transgene expression in myeloid cells. Mol Ther 19: 122-132.
29. Chatziandreou, I, Siapati, EK and Vassilopoulos, G (2011). Genetic correction of X-linked chronic granulomatous disease with novel foamy virus vectors. Exp Hematol 39: 643-652.
30. Barde, I, Laurenti, E, Verp, S, Wiznerowicz, M, Offner, S, Viornery, A et al. (2011). Lineage- and stage-restricted lentiviral vectors for the gene therapy of chronic granulomatous disease. Gene Ther 18: 1087-1097.
31. Thornhill, SI, Schambach, A, Howe, SJ, Ulaganathan, M, Grassman, E, Williams, D et al. (2008). Self-inactivating gammaretroviral vectors for gene therapy of X-linked severe combined immunodeficiency. Mol Ther 16: 590-598.
32. Avedillo Díez, I, Zychlinski, D, Coci, EG, Galla, M, Modlich, U, Dewey, RA et al. (2011). Development of novel efficient SIN vectors with improved safety features for Wiskott- Aldrich syndrome stem cell based gene therapy. Mol Pharm 8: 1525-1537.
33. Newrzela, S, Cornils, K, Li, Z, Baum, C, Brugman, MH, Hartmann, M et al. (2008). Resistance of mature T cells to oncogene transformation. Blood 112: 2278-2286.
34. Kustikova, OS, Schiedlmeier, B, Brugman, MH, Stahlhut, M, Bartels, S, Li, Z et al. (2009). Cell-intrinsic and vector-related properties cooperate to determine the incidence and consequences of insertional mutagenesis. Mol Ther 17: 1537-1547.
35. Grez, M, Reichenbach, J, Schwäble, J, Seger, R, Dinauer, MC and Thrasher, AJ (2011). Gene therapy of chronic granulomatous disease: the engraftment dilemma. Mol Ther 19: 28-35.
36. Brown, BD and Naldini, L (2009). Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications. Nat Rev Genet 10: 578-585.
37. Gentner, B, Visigalli, I, Hiramatsu, H, Lechman, E, Ungari, S, Giustacchini, A et al. (2010). Identification of hematopoietic stem cell-specific miRNAs enables gene therapy of globoid cell leukodystrophy. Sci Transl Med 2: 58ra84.
38. Ellis, J (2005). Silencing and variegation of gammaretrovirus and lentivirus vectors. Hum Gene Ther 16: 1241-1246.
39. Kobayashi, S, Imajoh-Ohmi, S, Nakamura, M and Kanegasaki, S (1990). Occurrence of cytochrome b558 in B-cell lineage of human lymphocytes. Blood 75: 458-461.
40. Sumiyoshi, T, Holt, NG, Hollis, RP, Ge, S, Cannon, PM, Crooks, GM et al. (2009). Stable transgene expression in primitive human CD34+ hematopoietic stem/progenitor cells, using the Sleeping Beauty transposon system. Hum Gene Ther 20: 1607-1626.
41. Malech, HL (1999). Progress in gene therapy for chronic granulomatous disease. J Infect Dis 179 Suppl 2: S318-S325.
42. Kuhns, DB, Alvord, WG, Heller, T, Feld, JJ, Pike, KM, Marciano, BE et al. (2010). Residual NADPH oxidase and survival in chronic granulomatous disease. N Engl J Med 363: 2600-2610.
43. Nakamura, M, Murakami, M, Koga, T, Tanaka, Y and Minakami, S (1987). Monoclonal antibody 7D5 raised to cytochrome b558 of human neutrophils: immunocytochemical detection of the antigen in peripheral phagocytes of normal subjects, patients with chronic granulomatous disease, and their carrier mothers. Blood 69: 1404-1408.
44. Mayo, LA and Curnutte, JT (1990). Kinetic microplate assay for superoxide production by neutrophils and other phagocytic cells. Meth Enzymol 186: 567-575.
45. Brendel, C, Müller-Kuller, U, Schultze-Strasser, S, Stein, S, Chen-Wichmann, L, Krattenmacher, A et al. (2012). Physiological regulation of transgene expression by a lentiviral vector containing the A2UCOE linked to a myeloid promoter. Gene Ther 19: 1018-1029.
46. Wu, X, Li, Y, Crise, B and Burgess, SM (2003). Transcription start regions in the human genome are favored targets for MLV integration. Science 300: 1749-1751.
47. Zhang, CC and Lodish, HF (2005). Murine hematopoietic stem cells change their surface phenotype during ex vivo expansion. Blood 105: 4314-4320.
48. Pollock, JD, Williams, DA, Gifford, MA, Li, LL, Du, X, Fisherman, J et al. (1995). Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 9: 202-209.