Vector integration and tumorigenesis

Human Gene Therapy

Volumn 25, Issue 6, 2014, Pages 475-481

  Von Kalle, Christof ^a   Deichmann, Annette ^a   Schmidt, Manfred ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LENS EPITHELIUM DERIVED GROWTH FACTOR; RETROVIRUS VECTOR; ZINC FINGER NUCLEASE;

B LYMPHOCYTE; CLINICAL PROTOCOL; DNA FLANKING REGION; DNA SEQUENCE; DNA STRAND; DRUG MIXTURE; GENE INSERTION SEQUENCE; GENE VECTOR; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HISTONE MODIFICATION; HUMAN; HUMAN GENOME; HUMAN GENOME PROJECT; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOLOGIST; INTENSIVE CARE UNIT; INVERSE POLYMERASE CHAIN REACTION; INVERTED TERMINAL REPEAT; LONG TERMINAL REPEAT; METACHROMATIC LEUKODYSTROPHY; MITOCHONDRIAL GENOME; PHYSICIAN; POLYMERASE CHAIN REACTION; PROTO ONCOGENE; RESTRICTION SITE; REVIEW; T CELL LEUKEMIA; VIRUS CARCINOGENESIS; VIRUS DNA CELL DNA INTERACTION; ANIMAL; CARCINOGENESIS; GENE REARRANGEMENT; GENE THERAPY; GENETICS; HEMATOPOIESIS; RETROVIRUS;

ANIMALS; CARCINOGENESIS; GENE REARRANGEMENT, B-LYMPHOCYTE; GENETIC THERAPY; GENETIC VECTORS; GENOME, HUMAN; HEMATOPOIESIS; HUMANS; RETROVIRIDAE; VIRUS INTEGRATION;

EID: 84902952172     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2014.2525     Document Type: Review

References (70)

1. Abel, U., Deichmann, A., Bartholomae, C., et al. (2007). Realtime definition of non-randomness in the distribution of genomic events. PLoS One 2, e570.
2. Abel, U., Deichmann, A., Nowrouzi, A., et al. (2011). Analyzing the number of common integration sites of viral vectors - new methods and computer programs. PLoS One 6, e24247.
3. Aiuti, A., Cassani, B., Andolfi, G., 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. (Pubitemid 47219568)
4. Aiuti, A., Biasco, L., Scaramuzza, S., et al. (2013). Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science 341, 1233151.
5. Appelt, J.U., Giordano, F.A., Ecker, M., et al. (2009). Quick- Map: a public tool for large-scale gene therapy vector insertion site mapping and analysis. Gene Ther. 16, 885-893.
6. Arens, A., Appelt, J.U., Bartholomae, C., et al. (2012). Bioinformatic clonality analysis of next-generation sequencingderived viral vector integration sites. Hum. Gene Ther. Methods 23, 111-118.
7. Avedillo Di'ez, I., Zychlinski, D., Coci, E.G., 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.
8. Berry, C.C., Gillet, N.A., Melamed, A., et al. (2012). Estimating abundances of retroviral insertion sites from DNA fragment length data. Bioinformatics 28, 755-762.
9. Bester, A.C., Schwartz, M., Schmidt, M., et al. (2006). Fragile sites are preferential targets for integrations of MLV vectors in gene therapy. Gene Ther. 13, 1057-1059. (Pubitemid 43905859)
10. Biffi, A., Montini, E., Lorioli, L., et al. (2013). Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 341, 1233158.
11. Boztug, K., Schmidt, M., Schwarzer, A., et al. (2010). Stem-cell gene therapy for the Wiskott-Aldrich syndrome. N. Engl. J. Med. 363, 1918-1927.
12. Braun, C.J., Boztug, K., Paruzynski, A., et al. (2014). Gene therapy for Wiskott-Aldrich syndrome - long-term efficacy and genotoxicity. Sci. Transl. Med. 6, 227ra33.
13. Bushman, F.D. (2003). Targeting survival: integration site selection by retroviruses and LTR-retrotransposons. Cell 115, 135-138. (Pubitemid 37329577)
14. Calmels, B., Ferguson, C., Laukkanen, M.O., et al. (2005). Recurrent retroviral vector integration at the Mds1/Evi1 locus in nonhuman primate hematopoietic cells. Blood 106, 2530- 2533. (Pubitemid 41510830)
15. Cartier, N., Hacein-Bey-Abina, S., Bartholomae, C.C., et al. (2009). Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326, 818-823.
16. Cattoglio, C., Facchini, G., Sartori, D., et al. (2007). Hot spots of retroviral integration in human CD34 + hematopoietic cells. Blood 110, 1770-1778. (Pubitemid 47443887)
17. Cavazzana-Calvo, M., Hacein-Bey, S., De Saint Basile, G., et al. (2000). Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288, 669-672. (Pubitemid 30241569)
18. Ciuffi, A., Llano, M., Poeschla, E., et al. (2005). A role for LEDGF/p75 in targeting HIV DNA integration. Nat. Med. 11, 1287-1289.
19. Collas, P., Husebye, H., and Alestrom, P. (1996). The nuclear localization sequence of the SV40 T antigen promotes transgene uptake and expression in zebrafish embryo nuclei. Transgenic Res. 5, 451-458. (Pubitemid 26367902)
20. Deichmann, A., Hacein-Bey-Abina, S., Schmidt, M., 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. (Pubitemid 47219567)
21. De Ridder, J., Uren, A., Kool, J., et al. (2006). Detecting statistically significant common insertion sites in retroviral insertional mutagenesis screens. PLoS Comput. Biol. 2, e166.
22. De Rijck, J., De Kogel, C., Demeulemeester, J., et al. (2013). The BET family of proteins targets moloney murine leukemia virus integration near transcription start sites. Cell Rep. 5, 886-894.
23. Dilloo, D., Rill, D.R., Grossmann, M.E., et al. (1996). Gene marking and gene therapy for transplantation medicine. J. Hematother. 5, 553-555.
24. Gabriel, R., Eckenberg, R., Paruzynski, A., et al. (2009). Comprehensive genomic access to vector integration in clinical gene therapy. Nat. Med. 15, 1431-1436.
25. Gabriel, R., Lombardo, A., Arens, A., et al. (2011). An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat. Biotechnol. 29, 816-823.
26. Gaspar, H.B., Parsley, K.L., Howe, S., et al. (2004). Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet 364, 2181-2187. (Pubitemid 40018447)
27. Glimm, H., Schmidt, M., Fischer, M., et al. (2005). Efficient marking of human cells with rapid but transient repopulating activity in autografted recipients. Blood 106, 893-898. (Pubitemid 41076429)
28. Guenechea, G., Gan, O.I., Dorrell, C., and Dick, J.E. (2001). Distinct classes of human stem cells that differ in proliferative and self-renewal potential. Nat. Immunol. 2, 75-82. (Pubitemid 33704957)
29. Hacein-Bey-Abina, S., Von Kalle, C., Schmidt, M., et al. (2003a). A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med. 348, 255-256.
30. Hacein-Bey-Abina, S., Von Kalle, C., Schmidt, M., et al. (2003b). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415-419. (Pubitemid 37296260)
31. Hacein-Bey-Abina, S., Garrigue, A., Wang, G.P., et al. (2008). Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118, 3132-3142.
32. Hematti, P., Hong, B.K., Ferguson, C., et al. (2004). Distinct genomic integration of MLV and SIV vectors in primate hematopoietic stem and progenitor cells. PLoS Biol. 2, e423.
33. Howe, S.J., Mansour, M.R., Schwarzwaelder, K., et al. (2008a). Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J. Clin. Invest. 118, 3143-3150.
34. Inagaki, K., Lewis, S.M., Wu, X., et al. (2007). DNA palindromes with a modest arm length of greater, similar 20 base pairs are a significant target for recombinant adeno-associated virus vector integration in the liver, muscles, and heart in mice. J. Virol. 81, 11290-11303. (Pubitemid 47536101)
35. Kaeppel, C., Beattie, S.G., Fronza, R., et al. (2013). A largely random AAV integration profile after LPLD gene therapy. Nat. Med. 19, 889-891.
36. Kohn, D.B. (1997). Gene therapy for haematopoietic and lymphoid disorders. Clin. Exp. Immunol. 107 Suppl 1, 54-57.
37. Kohn, D.B., Hershfield, M.S., Carbonaro, D., et al. (1998). T lymphocytes with a normal ADA gene accumulate after transplantation of transduced autologous umbilical cord blood CD34 + cells in ADA-deficient SCID neonates. Nat. Med. 4, 775-780.
38. Laufs, S., Gentner, B., Nagy, K.Z., et al. (2003). Retroviral vector integration occurs in preferred genomic targets of human bone marrow-repopulating cells. Blood 101, 2191-2198. (Pubitemid 36302057)
39. Lemischka, I.R., and Jordan, C.T. (2001). The return of clonal marking sheds new light on human hematopoietic stem cells. Nat. Immunol. 2, 11-12. (Pubitemid 33704945)
40. Li, Z., Duellmann, F., Schiedlmeier, B., et al. (2002). Murine leukemia induced by retroviral gene marking. Science 296, 497. (Pubitemid 34408663)
41. Li, H., Malani, N., Hamilton, S.R., et al. (2011). Assessing the potential for AAV vector genotoxicity in a murine model. Blood 117, 3311-3319.
42. Mitchell, R.S., Beitzel, B.F., Schroder, A.R., et al. (2004). Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol. 2, E234.
43. Mueller, P.R., and Wold, B. (1989). In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science 246, 780-786. (Pubitemid 19279168)
44. Mullis, K., Faloona, F., Scharf, S., et al. (1986). Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harb. Symp. Quant. Biol. 51 Pt 1, 263-273. (Pubitemid 17076711)
45. Nakai, H., Montini, E., Fuess, S., et al. (2003). AAV serotype 2 vectors preferentially integrate into active genes in mice. Nat. Genet. 34, 297-302. (Pubitemid 36792862)
46. Nolta, J.A., Dao, M.A., Wells, S., et al. (1996). Transduction of pluripotent human hematopoietic stem cells demonstrated by clonal analysis after engraftment in immune-deficient mice. Proc. Natl. Acad. Sci. USA 93, 2414-2419. (Pubitemid 26104364)
47. Nowrouzi, A., Penaud-Budloo, M., Kaeppel, C., et al. (2012). Integration frequency and intermolecular recombination of rAAV vectors in non-human primate skeletal muscle and liver. Mol. Ther. 20, 1177-1186.
48. Okou, D.T., Steinberg, K.M., Middle, C., et al. (2007). Microarray-based genomic selection for high-throughput resequencing. Nat. Methods 4, 907-909. (Pubitemid 350042376)
49. Ott, M.G., Schmidt, M., Schwarzwaelder, K., 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.
50. Paruzynski, A., Arens, A., Gabriel, R., et al. (2010). Genomewide high-throughput integrome analyses by nrLAM-PCR and next-generation sequencing. Nat. Protoc. 5, 1379-1395.
51. Peters, B., Dirscherl, S., Dantzer, J., et al. (2008). Automated analysis of viral integration sites in gene therapy research using the SeqMap web resource. Gene Ther. 15, 1294-1298.
52. Pfeifer, G.P., Steigerwald, S.D., Mueller, P.R., et al. (1989). Genomic sequencing and methylation analysis by ligation mediated PCR. Science 246, 810-813. (Pubitemid 19279172)
53. Popescu, N.C. (2003). Genetic alterations in cancer as a result of breakage at fragile sites. Cancer Lett. 192, 1-17. (Pubitemid 36292164)
54. Porreca, G.J., Zhang, K., Li, J.B., et al. (2007). Multiplex amplification of large sets of human exons. Nat. Methods 4, 931-936. (Pubitemid 350042382)
55. Recchia, A., Bonini, C., Magnani, Z., et al. (2006). Retroviral vector integration deregulates gene expression but has no consequence on the biology and function of transplanted T cells. Proc. Natl. Acad. Sci. USA 103, 1457-1462. (Pubitemid 43191187)
56. Rosenberg, S.A., Blaese, R.M., Brenner, M.K., et al. (1997). Human gene marker/therapy clinical protocols. Hum. Gene Ther. 8, 2301-2338.
57. Saiki, R.K., Gelfand, D.H., Stoffel, S., et al. (1988). Primerdirected enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239, 487-491. (Pubitemid 18084310)
58. Scherdin, U., Rhodes, K., and Breindl, M. (1990). Transcriptionally active genome regions are preferred targets for retrovirus integration. J. Virol. 64, 907-912. (Pubitemid 20032710)
59. Schmidt, M., Zickler, P., Hoffmann, G., et al. (2002). Polyclonal long-term repopulating stem cell clones in a primate model. Blood 100, 2737-2743.
60. Schmidt, M., Carbonaro, D.A., Speckmann, C., et al. (2003). Clonality analysis after retroviral-mediated gene transfer to CD34 + cells from the cord blood of ADA-deficient SCID neonates. Nat. Med. 9, 463-468. (Pubitemid 36460082)
61. Schmidt, M., Hacein-Bey-Abina, S., Wissler, M., et al. (2005). Clonal evidence for the transduction of CD34 + cells with lymphomyeloid differentiation potential and self-renewal capacity in the SCID-X1 gene therapy trial. Blood 105, 2699- 2706. (Pubitemid 40446259)
62. Schmidt, M., Schwarzwaelder, K., Bartholomae, C., et al. (2007). High-resolution insertion-site analysis by linear amplificationmediated PCR (LAM-PCR). Nat. Methods 4, 1051-1057. (Pubitemid 350201778)
63. Schroder, A.R., Shinn, P., Chen, H., et al. (2002). HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110, 521-529. (Pubitemid 35232295)
64. Schwarzwaelder, K., Howe, S.J., Schmidt, M., 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. (Pubitemid 47219569)
65. Silver, J., and Keerikatte, V. (1989). Novel use of polymerase chain reaction to amplify cellular DNA adjacent to an integrated provirus. J. Virol. 63, 1924-1928. (Pubitemid 19107786)
66. Stein, S., Ott, M.G., Schultze-Strasser, S., 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.
67. Wang, G.P., Berry, C.C., Malani, N., et al. (2010). Dynamics of gene-modified progenitor cells analyzed by tracking retroviral integration sites in a human SCID-X1 gene therapy trial. Blood 115, 4356-4366.
68. Waterston, R.H., Lander, E.S., and Sulston, J.E. (2002). On the sequencing of the human genome. Proc. Natl. Acad. Sci. USA 99, 3712-3716. (Pubitemid 34252171)
69. Wu, X., Li, Y., Crise, B., and Burgess, S.M. (2003). Transcription start regions in the human genome are favored targets for MLV integration. Science 300, 1749-1751. (Pubitemid 36712571)
70. Yu, H., Koilkonda, R.D., Chou, T.H., et al. (2012). Gene delivery to mitochondria by targeting modified adenoassociated virus suppresses Leber's hereditary optic neuropathy in a mouse model. Proc. Natl. Acad. Sci. USA 109, E1238-E1247.