Polyclonal fluctuation of lentiviral vector-transduced and expanded murine hematopoietic stem cells

Blood

Volumn 117, Issue 11, 2011, Pages 3053-3064

  Maetzig, Tobias ^a   Brugman, Martijn H ^a   Bartels, Stefan ^a   Heinz, Niels ^a   Kustikova, Olga S ^a   Modlich, Ute ^a   Li, Zhixiong ^a   Galla, Melanie ^a   Schiedlmeier, Bernhard ^a   Schambach, Axel ^a   Baum, Christopher ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; SOMATOMEDIN B; STEM CELL FACTOR; THROMBOPOIETIN;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL EXPANSION; CLONAL VARIATION; CONTROLLED STUDY; GENE INSERTION; GENE TRANSFER; GENE VECTOR; HEMATOPOIETIC STEM CELL; LENTIVIRINAE; LEUKEMOGENESIS; MOUSE; MUTANT; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTO ONCOGENE; SIGNAL TRANSDUCTION;

EID: 79953072037     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-08-303222     Document Type: Article

References (50)

1. Wilson A, Laurenti E, Oser G, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell. 2008;135(6):1118-1129.
2. Drize NJ, Olshanskaya YV, Gerasimova LP, et al. Lifelong hematopoiesis in both reconstituted and sublethally irradiated mice is provided by multiple sequentially recruited stem cells. Exp Hematol. 2001;29(6):786-794. (Pubitemid 32500381)
3. Jordan CT, Lemischka IR. Clonal and systemic analysis of long-term hematopoiesis in the mouse. Genes Dev. 1990;4(2):220-232.
4. Laukkanen MO, Kuramoto K, Calmels B, et al. Low-dose total body irradiation causes clonal fluctuation of primate hematopoietic stem and progenitor cells. Blood. 2005;105(3):1010-1015. (Pubitemid 40170869)
5. McKenzie JL, Gan OI, Doedens M, Wang JC, Dick JE. Individual stem cells with highly variable proliferation and self-renewal properties comprise the human hematopoietic stem cell compartment. Nat Immunol. 2006;7(11):1225-1233. (Pubitemid 44594319)
6. Aiuti A, Cassani B, Andolfi G, et al. Multilineage hematopoietic reconstitution without clonal selection in ADA-SCID patients treated with stem cell gene therapy. J Clin Invest. 2007;117(8):2233-2240. (Pubitemid 47219568)
7. Hacein-Bey-Abina S, Garrigue A, Wang GP, et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest. 2008;118(9):3132-3142.
8. Stein S, Ott MG, Schultze-Strasser S, et al. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat Med. 2010;16(2):198-204.
9. Cartier N, Hacein-Bey-Abina S, Bartholomae CC, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science. 2009;326(5954):818-823.
10. Li Z, Dullmann J, Schiedlmeier B, et al. Murine leukemia induced by retroviral gene marking. Science. 2002;296(5567):497. (Pubitemid 34408663)
11. Kustikova OS, Fehse B, Modlich U, et al. Clonal dominance of hematopoietic stem cells triggered by retroviral gene marking. Science. 2005;308:1171-1174. (Pubitemid 40696434)
12. Akagi K, Suzuki T, Stephens RM, Jenkins NA, Copeland NG. RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res. 2004;32:D523-527.
13. Naldini L, Blomer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 1996;272(5259):263-267.
14. Levine BL, Humeau LM, Boyer J, et al. Gene transfer in humans using a conditionally replicating lentiviral vector. Proc Natl Acad Sci U S A. 2006;103(46):17372-17377. (Pubitemid 44788976)
15. Wu X, Li Y, Crise B, Burgess SM. Transcription start regions in the human genome are favored targets for MLV integration. Science. 2003;300(5626):1749- 1751. (Pubitemid 36712571)
16. Lewinski MK, Yamashita M, Emerman M, et al. Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog. 2006;2(6):e60.
17. Montini E, Cesana D, Schmidt M, et al. The genotoxic potential of retroviral vectors is strongly modulated by vector design and integration site selection in a mouse model of HSCs gene therapy. J Clin Invest. 2009;119(4):964-975.
18. Modlich U, Navarro S, Zychlinski D, et al. Insertional transformation of hematopoietic cells by self-inactivating lentiviral and gammaretroviral vectors. Mol Ther. 2009;17(11):1919-1928.
19. Kurre P, Anandakumar P, Kiem HP. Rapid 1-hour transduction of whole bone marrow leads to longterm repopulation of murine recipients with lentivirus-modified hematopoietic stem cells. Gene Ther. 2006;13(4):369-373. (Pubitemid 43223106)
20. Zhang CC, Lodish HF. Murine hematopoietic stem cells change their surface phenotype during ex vivo expansion. Blood. 2005;105(11):4314-4320. (Pubitemid 40723656)
21. Brady T, Agosto LM, Malani N, Berry CC, O'Doherty U, Bushman F. HIV integration site distributions in resting and activated CD4+ T cells infected in culture. Aids. 2009;23(12):1461-1471.
22. Ciuffi A, Mitchell RS, Hoffmann C, et al. Integration site selection by HIV-based vectors in dividing and growth-arrested IMR-90 lung fibroblasts. Mol Ther. 2006;13(2):366-373. (Pubitemid 43056902)
23. Gonzalez-Murillo A, Lozano ML, Montini E, Bueren JA, Guenechea G. Unaltered repopulation properties of mouse hematopoietic stem cells transduced with lentiviral vectors. Blood. 2008; 112(8):3138-3147.
24. Cornils K, Lange C, Schambach A, et al. Stem cell marking with promotor-deprived self-inactivating retroviral vectors does not lead to induced clonal imbalance. Mol Ther. 2009;17(1):131-143.
25. Modlich U, Kustikova O, Schmidt M, et al. Leukemias following retroviral transfer of multidrug resistance 1 are driven by combinatorial insertional mutagenesis. Blood. 2005;105:4235-4246. (Pubitemid 40720768)
26. Sellers S, Gomes TJ, Larochelle A, et al. 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. 2010; 18(9):1633-1639.
27. Schambach A, Mueller D, Galla M, et al. Overcoming promoter competition in packaging cells improves production of self-inactivating retroviral vectors. Gene Ther. 2006;13(21):1524-1533. (Pubitemid 44567149)
28. Modlich U, Schambach A, Brugman MH, et al. Leukemia induction after a single retroviral vector insertion in Evi1 or Prdm16. Leukemia. 2008;22(8):1519-1528.
29. Kustikova OS, Baum C, Fehse B. Retroviral integration site analysis in hematopoietic stem cells. Methods Mol Biol. 2008;430:255-267.
30. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R. Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods. 2008;5(3):235-237. (Pubitemid 351325646)
31. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22(13):1658-1659. (Pubitemid 43985301)
32. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403-410.
33. de Ridder J, Uren A, Kool J, Reinders M, Wessels L. Detecting Statistically Significant Common Insertion Sites in Retroviral Insertional Mutagenesis Screens. PLoS Comput Biol. 2006;2(12):e166.
34. Thomas PD, Kejariwal A, Campbell MJ, et al. PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res. 2003;31(1):334-341. (Pubitemid 36150398)
35. Kustikova OS, Geiger H, Li Z, et al. Retroviral vector insertion sites associated with dominant hematopoietic clones mark "stemness" pathways. Blood. 2007;109(5):1897-1907.
36. Kustikova OS, Schiedlmeier B, Brugman MH, et al. Cell-intrinsic and vector-related properties cooperate to determine the incidence and consequences of insertional mutagenesis. Mol Ther. 2009;17(9):1537-1547.
37. Noda S, Horiguchi K, Ichikawa H, Miyoshi H. Repopulating activity of ex vivo-expanded murine hematopoietic stem cells resides in the CD48-c-Kit+Sca-1+lineage marker- cell population. Stem Cells. 2008;26(3):646-655.
38. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109-1121. (Pubitemid 40884400)
39. Zychlinski D, Schambach A, Modlich U, et al. Physiological promoters reduce the genotoxic risk of integrating gene vectors. Mol Ther. 2008;16(4):718-725. (Pubitemid 351426173)
40. Modlich U, Bohne J, Schmidt M, et al. Cell-culture assays reveal the importance of retroviral vector design for insertional genotoxicity. Blood. 2006;108(8):2545-2553.
41. Bryder D, Jacobsen SE. Interleukin-3 supports expansion of long-term multilineage repopulating activity after multiple stem cell divisions in vitro. Blood. 2000;96(5):1748-1755. (Pubitemid 30661058)
42. Gabriel R, Eckenberg R, Paruzynski A, et al. Comprehensive genomic access to vector integration in clinical gene therapy. Nat Med. 2009;15(12):1431-1436.
43. Whelan JT, Ludwig DL, Bertrand FE. HoxA9 induces insulin-like growth factor-1 receptor expression in B-lineage acute lymphoblastic leukemia. Leukemia. 2008;22(6):1161-1169. (Pubitemid 351833783)
44. Huynh H, Iizuka S, Kaba M, et al. Insulin-like growth factor-binding protein 2 secreted by a tumorigenic cell line supports ex vivo expansion of mouse hematopoietic stem cells. Stem Cells. 2008;26(6):1628-1635.
45. Zhang CC, Lodish HF. Insulin-like growth factor 2 expressed in a novel fetal liver cell population is a growth factor for hematopoietic stem cells. Blood. 2004;103(7):2513-2521. (Pubitemid 38393001)
46. Gerrits A, Dykstra B, Kalmykowa OJ, et al. Cellular barcoding tool for clonal analysis in the hematopoietic system. Blood. 2010;115(13):2610-2618.
47. Drize NJ, Keller JR, Chertkov JL. Local clonal analysis of the hematopoietic system shows that multiple small short-living clones maintain lifelong hematopoiesis in reconstituted mice. Blood. 1996;88(8):2927-2938. (Pubitemid 26357373)
48. Cattoglio C, Facchini G, Sartori D, et al. Hot spots of retroviral integration in human CD34+ hematopoietic cells. Blood. 2007;110(6):1770-1778. (Pubitemid 47443887)
49. Roeder I, Kamminga LM, Braesel K, Dontje B, de Haan G, Loeffler M. Competitive clonal hematopoiesis in mouse chimeras explained by a stochastic model of stem cell organization. Blood. 2005;105(2):609-616. (Pubitemid 40070743)
50. Marusyk A, DeGregori J. Declining cellular fitness with age promotes cancer initiation by selecting for adaptive oncogenic mutations. Biochim Biophys Acta. 2008;1785(1):1-11. (Pubitemid 350192081)