Genomic and functional assays demonstrate reduced gammaretroviral vector genotoxicity associated with use of the cHS4 chromatin insulator

Molecular Therapy

Volumn 17, Issue 4, 2009, Pages 716-724

  Li, Chang Long ^a,b   Xiong, Ding ^b   Stamatoyannopoulos, George ^a   Emery, David W ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLOBIN; CHICKEN BETA GLOBIN; RETROVIRUS VECTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ASSAY; CELL CLONE; CELL LINE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DRUG MECHANISM; FEMALE; GENE THERAPY; GENETIC DISTANCE; GENETIC REGULATION; GENOMICS; GENOTOXICITY; HUMAN; HUMAN CELL; INSULATOR ELEMENT; MALIGNANT TRANSFORMATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; BLOTTING, SOUTHERN; CELL LINE; CHROMATIN; FEMALE; FLOW CYTOMETRY; GAMMARETROVIRUS; GENETIC VECTORS; HUMANS; INSULATOR ELEMENTS; MICE; MICE, INBRED C3H; RECOMBINATION, GENETIC;

EID: 63949083133     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2009.7     Document Type: Article

References (48)

1. Kohn, DB, Sadelain, M, Dunbar, C, Bodine, D, Kiem, HP, Candotti, F et al. (2003). American Society of Gene Therapy (ASGT) ad hoc subcommittee on retroviralmediated gene transfer to hematopoietic stem cells. Molec Ther 8: 180-187.
2. Baum, C, von Kalle, C, Staal, FJ, Li, Z, Fehse, B, Schmidt, M et al. (2004). Chance or necessity? Insertional mutagenesis in gene therapy and its consequences. Mol Ther 9: 5-13.
3. Nienhuis, AW (2006). Assays to evaluate the genotoxicity of retroviral vectors. Mol Ther 14: 459-460.
4. Hacein-Bey-Abina, S, Von Kalle, C, Schmidt, M, McCormack, MP, Wulffraat, N, Leboulch, P et al. (2003). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302: 415-419.
5. 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.
6. 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 rhesus macaque. Blood 107: 3865-3867.
7. 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.
8. Kustikova, O, Fehse, B, Modlich, U, Yang, M, Dullmann, J, Kamino, K et al. (2005). Clonal dominance of hematopoietic stem cells triggered by retroviral gene marking. Science 308: 1171-1174.
9. Shou, Y, Ma, X, 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.
10. Recchia, A, Bonini, C, Magnani, Z, Urbinati, F, Sartori, D, Muraro, S et al. (2006). Retroviral vector integration deregulates gene expression but has no consequences on the biology and function of transplanted T cells. Proc Natl Acad Sci USA 103: 1457-1462.
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. Modlich, U, Bohne, J, Schmidt, M, von Kalle, C, Knoss, S, Schambach, A et al. (2006). Cell-culture assays reveal the importance of retroviral vector design for insertional genotoxicity. Blood 108: 2545-2553.
13. Emery, DW (2006). The SINister side of retrovirus vectors. Blood 108: 2495.
14. Emery, DW, Yannaki, E, Tubb, J and Stamatoyannopoulos, G (2000). A chromatin insulator protects retrovirus vectors from position effects. Proc Natl Acad Sci USA 97: 9150-9155.
15. Nienhuis, AW, Dunbar, CE and Sorrentino, BP (2006). Genotoxicity of retroviral integration in hematopoietic cells. Mol Ther 13: 1031-1049.
16. Evans-Galea, MV, Wielgosz, MM, Hanawa, H, Srivastava, DK and Nienhuis, AW (2007). Suppression of clonal dominance in cultured human lymphoid cells by addition of the cHS4 insulator to a lentiviral vector. Mol Ther 15: 801-809.
17. West, AG, Gaszner, M and Felsenfeld, G (2002). Insulators: Many functions, many mechanisms. Genes Dev 16: 271-288.
18. Emery, DW, Aker, M and Stamatoyannopoulos, G (2003). Chromatin insulators and position effects. In: Makrides, SC (ed.) Gene Transfer and Expression in Mammalian Cells. EIC Laboratories: Norwood, MA, pp. 381-395.
19. Yannaki, E, Tubb, J, Aker, M, Stamatoyannopoulos, G and Emery, DW (2002). Topological constraints governing the use of the chicken HS4 chromatin insulator in oncoretrovirus vectors. Mol Ther 5: 589-598.
20. Emery, DW, Yannaki, E, Tubb, J, Nishino, T, Li, Q and Stamatoyannopoulos, G (2002). Development of virus vectors for gene therapy of beta chain hemoglobinopathies: Flanking with a chromatin insulator reduces gamma-globin gene silencing in vivo. Blood 100: 2012-2021.
21. Rivella, S, Callegari, JA, May, C, Tan, CW and Sadelain, M (2000). The cHS4 insulator increases the probability of retroviral expression at random chromosomal integration sites. J Virol 74: 4679-4687.
22. Ramezani, A, Hawley, TS and Hawley, RG (2003). Performance- and safety-enhanced lentiviral vectors containing the human interferon-beta scaffold attachment region and the chicken beta-globin insulator. Blood 101: 4717-4724.
23. Yao, S, Osborne, CS, Bharadwaj, RR, Pasceri, P, Sukonnik, T, Pannell, D et al. (2003). Retrovirus silencer blocking by the cHS4 insulator is CTCF independent. Nucleic Acids Res 31: 5317-5323.
24. Chung, JH, Bell, AC and Felsenfeld, G (1997). Characterization of the chicken betaglobin insulator. Proc Natl Acad Sci USA 94: 575-580.
25. Bell, AC, West, AG and Felsenfeld, G (1999). The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98: 387-396.
26. Recillas-Targa, F, Pikaart, MJ, Burgess-Beusse, B, Bell, AC, Litt, MD, West, AG et al. (2002). Position-effect protection and enhancer blocking by the chicken beta-globin insulator are separable activities. Proc Natl Acad Sci USA 99: 6883-6888.
27. 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.
28. 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 beta-thalassemic hematopoietic cells. Mol Ther 16: 525-533.
29. Li, CL and Emery, DW (2008). The cHS4 chromatin insulator reduces gammaretroviral vector silencing by epigenetic modifications of integrated provirus. Gene Ther 15: 49-53.
30. Aker, M, Tubb, J, Miller, DG, Stamatoyannopoulos, G and Emery DW (2006). Integration bias of gammaretrovirus vectors following transduction and growth of primary mouse hematopoietic progenitor cells with and without selection. Mol Ther 4: 226-235.
31. Berry, C, Hannenhalli, S, Leipzig, J and Bushman, FD (2006). Selection of target sites for mobile DNA integration in the human genome. PLoS Comput Biol 2: E157.
32. Greenberger, JS, Sakakeeny, MA, Humphries, RK, Eaves, CJ and Eckner, RJ (1983). Demonstration of permanent factor-dependent multipotential (erythroid/neutrophil/basophil) hematopoietic progenitor cell lines. Proc Natl Acad Sci USA 80: 2931-2935.
33. FitzGerald, TJ, Henault, S, Sakakeeny, M, Santucci, MA, Pierce, JH, Anklesaria, P et al. (1990). Expression of transfected recombinant oncogenes increases radiation resistance of clonal hematopoietic and fibroblast cell lines selectively at clinical low dose rate. Radiat Res 122: 44-52.
34. Guo, XY, Cuillerot, JM, Wang, T, Wang, T, Wu, Y, Arlinghaus, R et al. (1998). Peptide containing the BCR oligomerization domain (AA 1-160) reverses the transformed phenotype of p210bcr-abl positive 32D myeloid leukemia cells. Oncogene 17: 825-833.
35. Ott, MG, Schmidt, M, Stein, S, Schwarzwaelder, K, Siler, U, Koehl, U et al. (2006). Long-term clinical follow-up and safety/toxicity analysis in 3 X-CGD patients treated by gene therapy and non-myeloablative conditioning. Blood 108: 63a.
36. Akagi, K, Suzuki, T, Stephens, RM, Jenkins, NA and Copeland, NG (2004). RTCGD: Retroviral tagged cancer gene database. Nucleic Acids Res 32: D523-D527.
37. Gaozza, E, Baker, SJ, Vora, RK and Reddy, EP (1997). AATYK: A novel tyrosine kinase induced during growth arrest and apoptosis of myeloid cells. Oncogene 15: 3127-3135.
38. Yuasa, H, Oike, Y, Iwama, A, Nishikata, I, Sugiyama, D, Perkins, A et al. (2005). Oncogenic transcription factor Evi1 regulates hematopoietic stem cell proliferation through GATA-2 expression. EMBO J 24: 1976-1987.
39. Mikkers, H, Allen, J, Knipscheer, P, Knipscheer, P, Romeijn, L, Hart, A et al. (2002). High-throughput retroviral tagging to identify components of specific signaling pathways in cancer. Nat Genet 32: 153-159.
40. Ryu, BY, Persons, DA, Evans-Galea, MV, Gray, JT and Nienhuis, AW (2007). A chromatin insulator blocks interactions between globin regulatory elements and cellular promoters in erythroid cells. Blood Cells Mol Dis 39: 221-228.
41. Savitskaya, E, Melnikova, L, Kostuchenko, M, Kravchenko, E, Pomerantseva, E, Boikova, T et al. (2006). Study of long-distance functional interactions between Su(Hw) insulators that can regulate enhancer-promoter communications in Drosophila melanogaster. Mol Cell Biol 26: 754-761.
42. Du, Y, Jenkins, NA and Copeland, NG (2005). Insertional mutagenesis identifies genes that promote the immortalization of primary bone marrow progenitor cells. Blood 106: 3932-3939.
43. Zhao, Z, Tavoosidana, G, Sjolinder, M, Gondor, A, Mariano, P, Wang, S et al. (2006). Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat Genet 38: 1341-1347.
44. Gimelbrant, A, Hutchinson, JN, Thompson, BR and Chess, A (2007). Widespread monoallelic expression on human autosomes. Science 318: 1136-1140.
45. Chang, AH, Stephan, MT and Sadelain, M (2006). Stem cell-derived erythroid cells mediate long-term systemic protein delivery. Nat Biotechnol 24: 1017-1021.
46. Aker, M, Tubb, J, Groth, AC, Bukovsky, AA, Bell, AC, Felsenfeld, G et al. (2007). Extended core sequences from the cHS4 insulator are necessary for protecting retroviral vectors from silencing position effects. Hum Gene Ther 18: 333-343.
47. Ramezani, A, Hawley, TS and Hawley, RG (2006). Stable gammaretroviral vector expression during embryonic stem cell-derived in vitro hematopoietic development. Mol Ther 14: 245-254.
48. Rasheed, S, Nelson-Rees, WA, Toth, EM, Arnstein, P and Gardner, MB (1974). Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 33: 1027-1033.