Clonal dominance with retroviral vector insertions near the ANGPT1 and ANGPT2 genes in a human xenotransplant mouse model

Molecular Therapy Nucleic Acids

Volumn 3, Issue , 2014, Pages e200-

  Haemmerle, Reinhard ^a   Phaltane, Ruhi ^a   Rothe, Michael ^a   Schröder, Simon ^a   Schambach, Axel ^a   Moritz, Thomas ^a   Modlich, Ute ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b PAUL EHRLICH INSTITUT   (Germany)

Author keywords

Clonal dominance; Insertional mutagenesis; Murine xenotransplant model; Retroviral vector

Indexed keywords

CYTOKINE; MESSENGER RNA; RETROVIRUS VECTOR;

ANGPT1 GENE; ANGPT2 GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLONAL VARIATION; CLONE; CONTROLLED STUDY; GENOTOXICITY; HEMATOPOIESIS; HUMAN; IN VITRO GENE TRANSFER; IN VITRO STUDY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION SYSTEM; PRIORITY JOURNAL; TARGET CELL; TUMOR GENE; UMBILICAL CORD BLOOD; VIRUS GENE; XENOTRANSPLANTATION;

EID: 84925276626     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2014.51     Document Type: Article

References (51)

1. Candotti, F (2014). Gene transfer into hematopoietic stem cells as treatment for primary immunodeficiency diseases. Int J Hematol 99: 383-392.
2. 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.
3. Howe, SJ, Mansour, MR, Schwarzwaelder, K, Bartholomae, C, Hubank, M, Kempski, H et al. (2008). Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J Clin Invest 118: 3143-3150.
4. 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.
5. Braun, CJ, Boztug, K, Paruzynski, A, Witzel, M, Schwarzer, A, Rothe, M et al. (2014). Gene therapy for Wiskott-Aldrich syndrome - long-term efficacy and genotoxicity. Sci Transl Med 6: 227ra33.
6. Zhang, CC, Kaba, M, Iizuka, S, Huynh, H and Lodish, HF (2008). Angiopoietin-like 5 and IGFBP2 stimulate ex vivo expansion of human cord blood hematopoietic stem cells as assayed by NOD/SCID transplantation. Blood 111: 3415-3423.
7. Butler, JM, Nolan, DJ, Vertes, EL, Varnum-Finney, B, Kobayashi, H, Hooper, AT et al. (2010). Endothelial cells are essential for the self-renewal and repopulation of Notchdependent hematopoietic stem cells. Cell Stem Cell 6: 251-264.
8. de Lima, M, McNiece, I, Robinson, SN, Munsell, M, Eapen, M, Horowitz, M et al. (2012). Cordblood engraftment with ex vivo mesenchymal-cell coculture. N Engl J Med 367: 2305-2315.
9. Boitano, AE, Wang, J, Romeo, R, Bouchez, LC, Parker, AE, Sutton, SE et al. (2010). Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329: 1345-1348.
10. Sellers, S, Gomes, TJ, Larochelle, A, Lopez, R, Adler, R, Krouse, A et al. (2010). Ex vivo expansion of retrovirally transduced primate CD34+ cells results in overrepresentation of clones with MDS1/EVI1 insertion sites in the myeloid lineage after transplantation. Mol Ther 18: 1633-1639.
11. Schmidt, M, Schwarzwaelder, K, Bartholomae, C, Zaoui, K, Ball, C, Pilz, I et al. (2007). High-resolution insertion-site analysis by linear amplification-mediated PCR (LAM-PCR). Nat Methods 4: 1051-1057.
12. Wu, C, Jares, A, Winkler, T, Xie, J, Metais, JY and Dunbar, CE (2013). High efficiency restriction enzyme-free linear amplification-mediated polymerase chain reaction approach for tracking lentiviral integration sites does not abrogate retrieval bias. Hum Gene Ther 24: 38-47.
13. Paruzynski, A, Arens, A, Gabriel, R, Bartholomae, CC, Scholz, S, Wang, W et al. (2010). Genome-wide high-throughput integrome analyses by nrLAM-PCR and next-generation sequencing. Nat Protoc 5: 1379-1395.
14. Brady, T, Roth, SL, Malani, N, Wang, GP, Berry, CC, Leboulch, P et al. (2011). A method to sequence and quantify DNA integration for monitoring outcome in gene therapy. Nucleic Acids Res 39: e72.
15. 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.
16. 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.
17. 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.
18. Beard, BC, Keyser, KA, Trobridge, GD, Peterson, LJ, Miller, DG, Jacobs, M et al. (2007). Unique integration profiles in a canine model of long-term repopulating cells transduced with gammaretrovirus, lentivirus, or foamy virus. Hum Gene Ther 18: 423-434.
19. Neff, T, Beard, BC, Peterson, LJ, Anandakumar, P, Thompson, J and Kiem, HP (2005). Polyclonal chemoprotection against temozolomide in a large-animal model of drug resistance gene therapy. Blood 105: 997-1002.
20. 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.
21. 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.
22. Cornils, K, Lange, C, Schambach, A, Brugman, MH, Nowak, R, Lioznov, M et al. (2009). Stem cell marking with promotor-deprived self-inactivating retroviral vectors does not lead to induced clonal imbalance. Mol Ther 17: 131-143.
23. Maetzig, T, Brugman, MH, Bartels, S, Heinz, N, Kustikova, OS, Modlich, U et al. (2011). Polyclonal fluctuation of lentiviral vector-transduced and expanded murine hematopoietic stem cells. Blood 117: 3053-3064.
24. Rangarajan, A, Hong, SJ, Gifford, A and Weinberg, RA (2004). Species- and cell type-specific requirements for cellular transformation. Cancer Cell 6: 171-183.
25. Mestas, J and Hughes, CC (2004). Of mice and not men: differences between mouse and human immunology. J Immunol 172: 2731-2738.
26. Biffi, A, Bartolomae, CC, Cesana, D, Cartier, N, Aubourg, P, Ranzani, M et al. (2011). Lentiviral vector common integration sites in preclinical models and a clinical trial reflect a benign integration bias and not oncogenic selection. Blood 117: 5332-5339.
27. Phaltane, R, Haemmerle, R, Rothe, M, Modlich, U and Moritz, T (2014). Efficiency and safety of O6-methylguanine DNA methyltransferase (MGMT(P140K))-mediated in vivo selection in a humanized mouse model. Hum Gene Ther 25: 144-155.
28. Cai, S, Wang, H, Bailey, B, Ernstberger, A, Juliar, BE, Sinn, AL et al. (2011). Humanized bone marrow mouse model as a preclinical tool to assess therapy-mediated hematotoxicity. Clin Cancer Res 17: 2195-2206.
29. Larochelle, A and Dunbar, CE (2013). Hematopoietic stem cell gene therapy:assessing the relevance of preclinical models. Semin Hematol 50: 101-130.
30. Gabriel, R, Eckenberg, R, Paruzynski, A, Bartholomae, CC, Nowrouzi, A, Arens, A et al. (2009). Comprehensive genomic access to vector integration in clinical gene therapy. Nat Med 15: 1431-1436.
31. Akagi, K, Suzuki, T, Stephens, RM, Jenkins, NA and Copeland, NG (2004). RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res 32(Database issue): D523-D527.
32. D'Antonio, M, Pendino, V, Sinha, S and Ciccarelli, FD (2012). Network of Cancer Genes (NCG 3.0): integration and analysis of genetic and network properties of cancer genes. Nucleic Acids Res 40(Database issue): D978-D983.
33. Deichmann, A, Brugman, MH, Bartholomae, CC, Schwarzwaelder, K, Verstegen, MM, Howe, SJ et al. (2011). Insertion sites in engrafted cells cluster within a limited repertoire of genomic areas after gammaretroviral vector gene therapy. Mol Ther 19: 2031-2039.
34. Wu, X, Luke, BT and Burgess, SM (2006). Redefining the common insertion site. Virology 344: 292-295.
35. Modlich, U, Navarro, S, Zychlinski, D, Maetzig, T, Knoess, S, Brugman, MH et al. (2009). Insertional transformation of hematopoietic cells by self-inactivating lentiviral and gammaretroviral vectors. Mol Ther 17: 1919-1928.
36. Greene, MR, Lockey, T, Mehta, PK, Kim, YS, Eldridge, PW, Gray, JT et al. (2012). Transduction of human CD34+ repopulating cells with a self-inactivating lentiviral vector for SCID-X1 produced at clinical scale by a stable cell line. Hum Gene Ther Methods 23: 297-308.
37. McDermott, SP, Eppert, K, Lechman, ER, Doedens, M and Dick, JE (2010). Comparison of human cord blood engraftment between immunocompromised mouse strains. Blood 116: 193-200.
38. Cheung, AM, Nguyen, LV, Carles, A, Beer, P, Miller, PH, Knapp, DJ et al. (2013). Analysis of the clonal growth and differentiation dynamics of primitive barcoded human cord blood cells in NSG mice. Blood 122: 3129-3137.
39. Brugman, MH, Suerth, JD, Rothe, M, Suerbaum, S, Schambach, A, Modlich, U et al. (2013). Evaluating a ligation-mediated PCR and pyrosequencing method for the detection of clonal contribution in polyclonal retrovirally transduced samples. Hum Gene Ther Methods 24: 68-79.
40. Giordano, FA, Sorg, UR, Appelt, JU, Lachmann, N, Bleier, S, Roeder, I et al. (2011). Clonal inventory screens uncover monoclonality following serial transplantation of MGMT P140K-transduced stem cells and dose-intense chemotherapy. Hum Gene Ther 22: 697-710.
41. Harkey, MA, Kaul, R, Jacobs, MA, Kurre, P, Bovee, D, Levy, R et al. (2007). Multiarm high-throughput integration site detection: limitations of LAM-PCR technology and optimization for clonal analysis. Stem Cells Dev 16: 381-392.
42. Scaramuzza, S, Biasco, L, Ripamonti, A, Castiello, MC, Loperfido, M, Draghici, E et al. (2013). Preclinical safety and efficacy of human CD34(+) cells transduced with lentiviral vector for the treatment of Wiskott-Aldrich syndrome. Mol Ther 21: 175-184.
43. Baum, C, Modlich, U, Göhring, G and Schlegelberger, B (2011). Concise review: managing genotoxicity in the therapeutic modification of stem cells. Stem Cells 29: 1479-1484.
44. Stein, S, Scholz, S, Schwäble, J, Sadat, MA, Modlich, U, Schultze-Strasser, S et al. (2013). From bench to bedside: preclinical evaluation of a self-inactivating gammaretroviral vector for the gene therapy of X-linked chronic granulomatous disease. Hum Gene Ther Clin Dev 24: 86-98.
45. 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.
46. 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.
47. Sandrin, V, Boson, B, Salmon, P, Gay, W, Nègre, D, Le Grand, R et al. (2002). Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and nonhuman primates. Blood 100: 823-832.
48. Dull, T, Zufferey, R, Kelly, M, Mandel, RJ, Nguyen, M, Trono, D et al. (1998). A third-generation lentivirus vector with a conditional packaging system. J Virol 72: 8463-8471.
49. Shultz, LD, Lyons, BL, Burzenski, LM, Gott, B, Chen, X, Chaleff, S et al. (2005). Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 174: 6477-6489.
50. Rittelmeyer, I, Rothe, M, Brugman, MH, Iken, M, Schambach, A, Manns, MP et al. (2013). Hepatic lentiviral gene transfer is associated with clonal selection, but not with tumor formation in serially transplanted rodents. Hepatology 58: 397-408.
51. Huston, MW, Brugman, MH, Horsman, S, Stubbs, A, van der Spek, P and Wagemaker, G (2012). Comprehensive investigation of parameter choice in viral integration site analysis and its effects on the gene annotations produced. Hum Gene Ther 23: 1209-1219.