Cell-intrinsic and vector-related properties cooperate to determine the incidence and consequences of insertional mutagenesis

Molecular Therapy

Volumn 17, Issue 9, 2009, Pages 1537-1547

  Kustikova, Olga S ^a   Schiedlmeier, Bernhard ^a   Brugman, Martijn H ^a   Stahlhut, Maike ^a   Bartels, Stefan ^a   Li, Zhixiong ^a   Baum, Christopher ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LENTIVIRUS VECTOR;

ANIMAL CELL; ARTICLE; BONE MARROW TRANSPLANTATION; CELL CLONE; CELL SELECTION; CELL SUBPOPULATION; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE INSERTION; GENETIC TRANSDUCTION; HEMATOPOIETIC STEM CELL; MOUSE; MUTAGENESIS; NONHUMAN; POLYMERASE CHAIN REACTION; PROGENY; PROTO ONCOGENE; UPREGULATION;

ANIMALS; FEMALE; GENETIC VECTORS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; LENTIVIRUS; MICE; MICE, INBRED C57BL; MUTAGENESIS, INSERTIONAL; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSDUCTION, GENETIC;

ANIMALIA; MUS;

EID: 69949164575     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2009.134     Document Type: Article

References (50)

1. Niwa, H (2007). Open conformation chromatin and pluripotency. Genes Dev 21: 2671-2676.
2. Lansdorp, PM (2005). Role of telomerase in hematopoietic stem cells. Ann N Y Acad Sci 1044: 220-227.
3. Martinez-Agosto, JA, Mikkola, HK, Hartenstein, V and Banerjee, U (2007). The hematopoietic stem cell and its niche: A comparative view. Genes Dev 21: 3044-3060.
4. Hacein-Bey-Abina, S, Garrigue, A, Wang, GP, Soulier, J, Lim, A, Morillon, E et al. (2008). Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest 118: 3132-3142.
5. Aiuti, A, Cattaneo, F, Galimberti, S, Benninghoff, U, Cassani, B, Callegaro, L et al. (2009). Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N Engl J Med 360: 447-458.
6. Li, Z, Dullmann, J, Schiedlmeier, B, Schmidt, M, von Kalle, C, Meyer, J et al. (2002). Murine leukemia induced by retroviral gene marking. Science 296: 497.
7. Kustikova, O, Fehse, B, Modlich, U, Yang, M, Düllmann, J, Kamino, K et al. (2005). Clonal dominance of hematopoietic stem cells triggered by retroviral gene marking. Science 308: 1171-1174.
8. 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.
9. Seggewiss, R, Pittaluga, S, Adler, RL, Guenaga, FJ, Ferguson, C, Pilz, IH et al. (2006). Acute myeloid leukemia is associated with retroviral gene transfer to hematopoietic progenitor cells in a rhesus macaque. Blood 107: 3865-3867.
10. Modlich, U, Kustikova, OS, Schmidt, M, Rudolph, C, Meyer, J, Li, Z et al. (2005). Leukemias following retroviral transfer of multidrug resistance 1 (MDR1) are driven by combinatorial insertional mutagenesis. Blood 105: 4235-4246.
11. Montini, E, Cesana, D, Schmidt, M, Sanvito, F, Ponzoni, M, Bartholomae, C et al. (2006). Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat Biotechnol 24: 687-696.
12. 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.
13. 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.
14. Deichmann, A, Hacein-Bey-Abina, S, Schmidt, M, Garrigue, A, Brugman, MH, Hu, J et al. (2007). Vector integration is nonrandom and clustered and influences the fate of lymphopoiesis in SCID-X1 gene therapy. J Clin Invest 117: 2225-2232.
15. Schwarzwaelder, K, Howe, SJ, Schmidt, M, Brugman, MH, Deichmann, A, Glimm, H et al. (2007). Gammaretrovirus-mediated correction of SCID-X1 is associated with skewed vector integration site distribution in vivo. J Clin Invest 117: 2241-2249.
16. Aiuti, A, Cassani, B, Andolfi, G, Mirolo, M, Biasco, L, Recchia, A et al. (2007). Multilineage hematopoietic reconstitution without clonal selection in ADA-SCID patients treated with stem cell gene therapy. J Clin Invest 117: 2233-2240.
17. Mostoslavsky, G, Kotton, DN, Fabian, AJ, Gray, JT, Lee, JS and Mulligan, RC (2005). Efficiency of transduction of highly purified murine hematopoietic stem cells by lentiviral and oncoretroviral vectors under conditions of minimal in vitro manipulation. Mol Ther 11: 932-940.
18. Cozzio, A, Passegué, E, Ayton, PM, Karsunky, H, Cleary, ML and Weissman, IL (2003). Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 17: 3029-3035.
19. Huntly, BJ, Shigematsu, H, Deguchi, K, Lee, BH, Mizuno, S, Duclos, N et al. (2004). MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell 6: 587-596.
20. Krivtsov, AV, Twomey, D, Feng, Z, Stubbs, MC, Wang, Y, Faber, J et al. (2006). Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442: 818-822.
21. Okada, S, Nakauchi, H, Nagayoshi, K, Nishikawa, S, Miura, Y and Suda, T (1992). In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells. Blood 80: 3044-3050.
22. + Lin(low/-) hemopoietic stem cells. J Immunol 156: 3207-3214.
23. +Flt3- short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients. Blood 105: 2717-2723.
24. Kustikova, OS, Geiger, H, Li, Z, Brugman, MH, Chambers, SM, Shaw, CA et al. (2007). Retroviral vector insertion sites associated with dominant hematopoietic clones mark "stemness" pathways. Blood 109: 1897-1907.
25. Akagi, K, Suzuki, T, Stephens, RM, Jenkins, NA and Copeland, NG (2004). RTCGD: Retroviral tagged cancer gene database. Nucleic Acids Res 32: D523-D527.
26. Bowie, MB, McKnight, KD, Kent, DG, McCaffrey, L, Hoodless, PA and Eaves, CJ (2006). Hematopoietic stem cells proliferate until after birth and show a reversible phase-specific engraftment defect. J Clin Invest 116: 2808-2816.
27. Modlich, U, Schambach, A, Brugman, MH, Wicke, DC, Knoess, S, Li, Z et al. (2008). Leukemia induction after a single retroviral vector insertion in Evi1 or Prdm16. Leukemia 22: 1519-1528.
28. Wang, GP, Garrigue, A, Ciuffi, A, Ronen, K, Leipzig, J, Berry, C et al. (2008). DNA bar coding and pyrosequencing to analyze adverse events in therapeutic gene transfer. Nucleic Acids Res 36: e49.
29. Hamady, M, Walker, JJ, Harris, JK, Gold, NJ and Knight, R (2008). Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5: 235-237.
30. Takash, W, Cañizares, J, Bonneaud, N, Poulat, F, Mattéi, MG, Jay, P et al. (2001). SOX7 transcription factor: Sequence, chromosomal localisation, expression, transactivation and interference with Wnt signalling. Nucleic Acids Res 29: 4274-4283.
31. Goyama, S, Yamamoto, G, Shimabe, M, Sato, T, Ichikawa, M, Ogawa, S et al. (2008). Evi-1 is a critical regulator for hematopoietic stem cells and transformed leukemic cells. Cell Stem Cell 3: 207-220.
32. Kent, DG, Dykstra, BJ, Cheyne, J, Ma, E and Eaves, CJ (2008). Steel factor coordinately regulates the molecular signature and biologic function of hematopoietic stem cells. Blood 112: 560-567.
33. Shou, Y, Ma, Z, Lu, T and Sorrentino, BP (2006). Unique risk factors for insertional mutagenesis in a mouse model of XSCID gene therapy. Proc Natl Acad Sci USA 103: 11730-11735.
34. Lewinski, MK and Bushman, FD (2005). Retroviral DNA integration-mechanism and consequences. Adv Genet 55: 147-181.
35. Lapidot, T, Dar, A and Kollet, O (2005). How do stem cells find their way home? Blood 106: 1901-1910.
36. Samper, E, Fernández, P, Eguía, R, Martín-Rivera, L, Bernad, A, Blasco, MA et al. (2002). Long-term repopulating ability of telomerase-deficient murine hematopoietic stem cells. Blood 99: 2767-2775.
37. Faubert, A, Chagraoui, J, Mayotte, N, Frechette, M, Iscove, NN, Humphries, RK et al. (2008). Complementary and independent function for hoxb4 and bmi2 in HSC activity. Cold Spring Harbor Symposia Quant Biol 73: 555-564.
38. Modlich, U, Bohne, J, Schmidt, M, von Kalle, C, Knöss, S, Schambach, A et al. (2006). Cell-culture assays reveal the importance of retroviral vector design for insertional genotoxicity. Blood 108: 2545-2553.
39. Ball, CR, Pilz, IH, Schmidt, M, Fessler, S, Williams, DA, von Kalle, C et al. (2007). Stable differentiation and clonality of murine long-term hematopoiesis after extended reduced-intensity selection for MGMT P140K transgene expression. Blood 110: 1779-1787.
40. + hematopoietic cells. Blood 110: 1770-1778.
41. Beard, BC, Dickerson, D, Beebe, K, Gooch, C, Fletcher, J, Okbinoglu, T et al. (2007). Comparison of HIV-derived lentiviral and MLV-based gammaretroviral vector integration sites in primate repopulating cells. Mol Ther 15: 1356-1365.
42. Ryu, BY, Evans-Galea, MV, Gray, JT, Bodine, DM, Persons, DA and Nienhuis, AW (2008). An experimental system for the evaluation of retroviral vector design to diminish the risk for proto-oncogene activation. Blood 111: 1866-1875.
43. Hargrove, PW, Kepes, S, Hanawa, H, Obenauer, JC, Pei, D, Cheng, C et al. (2008). Globin lentiviral vector insertions can perturb the expression of endogenous genes in β-thalassemic hematopoietic cells. Mol Ther 16: 525-533.
44. Mazurier, F, Gan, OI, McKenzie, JL, Doedens, M and Dick, JE (2004). Lentivector-mediated clonal tracking reveals intrinsic heterogeneity in the human hematopoietic stem cell compartment and culture-induced stem cell impairment. Blood 103: 545-552.
45. Ema, H, Sudo, K, Seita, J, Matsubara, A, Morita, Y, Osawa, M et al (2005). Quantification of self-renewal capacity in single hematopoietic stem cells from normal and Lnk-deficient mice. Dev Cell 8: 907-914.
46. Gonzalez-Murillo, A, Lozano, ML, Montini, E, Bueren, JA and Guenechea, G (2008). Unaltered repopulation properties of mouse hematopoietic stem cells transduced with lentiviral vectors. Blood 112: 3138-3147.
47. Schambach, A, Mueller, D, Galla, M, Verstegen, MM, Wagemaker, G, Loew, R et al. (2006). Overcoming promoter competition in packaging cells improves production of self-inactivating retroviral vectors. Gene Ther 13: 1524-1533.
48. Zufferey, R, Dull, T, Mandel, RJ, Bukovsky, A, Quiroz, D, Naldini, L et al. (1998). Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 72: 9873-9880.
49. Kustikova, OS, Modlich, U and Fehse, B (2009). Retroviral insertion site analysis in dominant haematopoietic clones. Methods Mol Biol 506: 373-390.
50. Li, W and Godzik, A (2006). Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.