High-throughput, sensitive quantification of repopulating hematopoietic stem cell clones

Journal of Virology

Volumn 84, Issue 22, 2010, Pages 11771-11780

  Kim, Sanggu ^a   Kim, Namshin ^c   Presson, Angela P ^a,b   An, Dong Sung ^a,b   Mao, Si Hua ^a,b   Bonifacino, Aylin C ^d   Donahue, Robert E ^d   Chow, Samson A ^a   Chen, Irvin S Y ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; LENTIVIRUS VECTOR;

AMPLICON; ANIMAL CELL; ARTICLE; CELL POPULATION; GENE SEQUENCE; GENE THERAPY; HEMATOPOIETIC STEM CELL; LENTIVIRINAE; MOLECULAR CLONING; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RHESUS MONKEY; VIRUS GENOME;

ANIMALS; CELLS, CULTURED; CLONE CELLS; GENE THERAPY; GENETIC VECTORS; HEMATOPOIETIC STEM CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; LENTIVIRUS; MACACA MULATTA; SEQUENCE ANALYSIS, DNA; VIRUS INTEGRATION;

PRIMATES;

EID: 78049492285     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01355-10     Document Type: Article

References (36)

1. Aiuti, A., F. Cattaneo, S. Galimberti, U. Benninghoff, B. Cassani, L. Callegaro, S. Scaramuzza, G. Andolfi, M. Mirolo, I. Brigida, A. Tabucchi, F. Carlucci, M. Eibl, M. Aker, S. Slavin, H. Al-Mousa, A. Al Ghonaium, A. Ferster, A. Duppenthaler, L. Notarangelo, U. Wintergerst, R. H. Buckley, M. Bregni, S. Marktel, M. G. Valsecchi, P. Rossi, F. Ciceri, R. Miniero, C. Bordignon, and M.-G. Roncarolo. 2009. Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N. Engl. J. Med. 360:447-458.
2. Aiuti, A., S. Slavin, M. Aker, F. Ficara, S. Deola, A. Mortellaro, S. Morecki, G. Andolfi, A. Tabucchi, F. Carlucci, E. Marinello, F. Cattaneo, S. Vai, P. Servida, R. Miniero, M. G. Roncarolo, and C. Bordignon. 2002. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 296:2410-2413.
3. An, D. S., S. K. P. Kung, A. Bonifacino, R. P. Wersto, M. E. Metzger, B. A. Agricola, S. H. Mao, I. S. Y. Chen, and R. E. Donahue. 2001. Lentivirus vector-mediated hematopoietic stem cell gene transfer of common gamma-chain cytokine receptor in rhesus macaques. J. Virol. 75:3547-3555.
4. + cells. J. Virol. 74:1286-1295.
5. Cartier, N., S. Hacein-Bey-Abina, C. C. Bartholomae, G. Veres, M. Schmidt, I. Kutschera, M. Vidaud, U. Abel, L. Dal-Cortivo, L. Caccavelli, N. Mahlaoui, V. Kiermer, D. Mittelstaedt, C. Bellesme, N. Lahlou, F. Lefrere, S. Blanche, M. Audit, E. Payen, P. Leboulch, B. l'Homme, P. Bougneres, C. Von Kalle, A. Fischer, M. Cavazzana-Calvo, and P. Aubourg. 2009. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326:818-823.
6. Cavazzana-Calvo, M., S. Hacein-Bey, G. de Saint Basile, F. Gross, E. Yvon, P. Nusbaum, F. Selz, C. Hue, S. Certain, J.-L. Casanova, P. Bousso, F. L. Deist, and A. Fischer. 2000. Gene therapy of human severe combined immunodeficiency (SCID)-X1 dis. Science 288:669-672. (Pubitemid 30241569)
7. Chun, T.-W., L. Carruth, D. Finzi, X. Shen, J. A. DiGiuseppe, H. Taylor, M. Hermankova, K. Chadwick, J. Margolick, T. C. Quinn, Y.-H. Kuo, R. Brookmeyer, M. A. Zeiger, P. Barditch-Crovo, and R. F. Siliciano. 1997. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387:183-188.
8. Deichmann, A., S. Hacein-Bey-Abina, M. Schmidt, A. Garrigue, M. H. Brugman, J. Hu, H. Glimm, G. Gyapay, B. Prum, C. C. Fraser, N. Fischer, K. Schwarzwaelder, M.-L. Siegler, D. de Ridder, K. Pike-Overzet, S. J. Howe, A. J. Thrasher, G. Wagemaker, U. Abel, F. J. T. Staal, E. Delabesse, J.-L. Villeval, B. Aronow, C. Hue, C. Prinz, M. Wissler, C. Klanke, J. Weissenbach, I. Alexander, A. Fischer, C. von Kalle, and M. Cavazzana-Calvo. 2007. Vector integration is nonrandom and clustered and influences the fate of lymphopoiesis in SCID-X1 gene therapy. J. Clin. Invest. 117:2225-2232.
9. Dick, J. E., M. C. Magli, D. Huszar, R. A. Phillips, and A. Bernstein. 1985. Introduction of a selectable gene into primitive stem cells capable of long-term reconstitution of the hemopoietic system of W/Wv mice. Cell 42:71-79.
10. Gabriel, R., R. Eckenberg, A. Paruzynski, C. C. Bartholomae, A. Nowrouzi, A. Arens, S. J. Howe, A. Recchia, C. Cattoglio, W. Wang, K. Faber, K. Schwarzwaelder, R. Kirsten, A. Deichmann, C. R. Ball, K. S. Balaggan, R. J. Yanez-Munoz, R. R. Ali, H. B. Gaspar, L. Biasco, A. Aiuti, D. Cesana, E. Montini, L. Naldini, O. Cohen-Haguenauer, F. Mavilio, A. J. Thrasher, H. Glimm, C. von Kalle, W. Saurin, and M. Schmidt. 2009. Comprehensive genomic access to vector integration in clinical gene therapy. Nat. Med. 15:1431-1436.
11. Gerrits, A., B. Dykstra, O. J. Kalmykowa, K. Klauke, E. Verovskaya, M. J. C. Broekhuis, G. de Haan, and L. V. Bystrykh. 2010. Cellular barcoding tool for clonal analysis in the hematopoietic system. Blood 115:2610-2618.
12. Hacein-Bey-Abina, S., A. Garrigue, G. P. Wang, J. Soulier, A. Lim, E. Morillon, E. Clappier, L. Caccavelli, E. Delabesse, K. Beldjord, V. Asnafi, E. MacIntyre, L. Dal Cortivo, I. Radford, N. Brousse, F. Sigaux, D. Moshous, J. Hauer, A. Borkhardt, B. H. Belohradsky, U. Wintergerst, M. C. Velez, L. Leiva, R. Sorensen, N. Wulffraat, S. Blanche, F. D. Bushman, A. Fischer, and M. Cavazzana-Calvo. 2008. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118:3132-3142.
13. Hacein-Bey-Abina, S., F. Le Deist, F. Carlier, C. Bouneaud, C. Hue, J.-P. De Villartay, A. J. Thrasher, N. Wulffraat, R. Sorensen, S. Dupuis-Girod, A. Fischer, E. G. Davies, W. Kuis, L. Leiva, and M. Cavazzana-Calvo. 2002. Sustained correction of X-linked severe combined immunodeficiency by ex vivo gene therapy. N. Engl. J. Med. 346:1185-1193.
14. Hacein-Bey-Abina, S., C. Von Kalle, M. Schmidt, M. P. McCormack, N. Wulffraat, P. Leboulch, A. Lim, C. S. Osborne, R. Pawliuk, E. Morillon, R. Sorensen, A. Forster, P. Fraser, J. I. Cohen, G. de Saint Basile, I. Alexander, U. Wintergerst, T. Frebourg, A. Aurias, D. Stoppa-Lyonnet, S. Romana, I. Radford-Weiss, F. Gross, F. Valensi, E. Delabesse, E. Macintyre, F. Sigaux, J. Soulier, L. E. Leiva, M. Wissler, C. Prinz, T. H. Rabbitts, F. Le Deist, A. Fischer, and M. Cavazzana-Calvo. 2003. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302:415-419.
15. Harkey, M. A., R. Kaul, M. A. Jacobs, P. Kurre, D. Bovee, R. Levy, and C. A. Blau. 2007. Multiarm high-throughput integration site detection: limitations of LAM-PCR technology and optimization for clonal analysis. Stem Cells Dev. 16:381-392.
16. Howe, S. J., M. R. Mansour, K. Schwarzwaelder, C. Bartholomae, M. Hubank, H. Kempski, M. H. Brugman, K. Pike-Overzet, S. J. Chatters, D. de Ridder, K. C. Gilmour, S. Adams, S. I. Thornhill, K. L. Parsley, F. J. T. Staal, R. E. Gale, D. C. Linch, J. Bayford, L. Brown, M. Quaye, C. Kinnon, P. Ancliff, D. K. Webb, M. Schmidt, C. von Kalle, H. B. Gaspar, and A. J. Thrasher. 2008. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J. Clin. Invest. 118:3143-3150.
17. Jordan, C. T., and I. R. Lemischka. 1990. Clonal and systemic analysis of long-term hematopoiesis in the mouse. Genes Dev. 4:220-232.
18. Keller, G., C. Paige, E. Gilboa, and E. F. Wagner. 1985. Expression of a foreign gene in myeloid and lymphoid cells derived from multipotent haematopoietic precursors. Nature 318:149-154.
19. Kim, S., Y. Kim, T. Liang, J. S. Sinsheimer, and S. A. Chow. 2006. A high-throughput method for cloning and sequencing human immunodeficiency virus type 1 integration sites. J. Virol. 80:11313-11321.
20. Kuramoto, K., D. A. Follmann, P. Hematti, S. Sellers, B. A. Agricola, M. E. Metzger, R. E. Donahue, C. von Kalle, and C. E. Dunbar. 2004. Effect of chronic cytokine therapy on clonal dynamics in nonhuman primates. Blood 103:4070-4077.
21. Margulies, M., M. Egholm, W. E. Altman, S. Attiya, J. S. Bader, L. A. Bemben, J. Berka, M. S. Braverman, Y.-J. Chen, Z. Chen, S. B. Dewell, L. Du, J. M. Fierro, X. V. Gomes, B. C. Godwin, W. He, S. Helgesen, C. H. Ho, G. P. Irzyk, S. C. Jando, M. L. I. Alenquer, T. P. Jarvie, K. B. Jirage, J.-B. Kim, J. R. Knight, J. R. Lanza, J. H. Leamon, S. M. Lefkowitz, M. Lei, J. Li, K. L. Lohman, H. Lu, V. B. Makhijani, K. E. McDade, M. P. McKenna, E. W. Myers, E. Nickerson, J. R. Nobile, R. Plant, B. P. Puc, M. T. Ronan, G. T. Roth, G. J. Sarkis, J. F. Simons, J. W. Simpson, M. Srinivasan, K. R. Tartaro, A. Tomasz, K. A. Vogt, G. A. Volkmer, S. H. Wang, Y. Wang, M. P. Weiner, P. Yu, R. F. Begley, and J. M. Rothberg. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376-380.
22. Mazurier, F., O. I. Gan, J. L. McKenzie, M. Doedens, and J. E. Dick. 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.
23. McKenzie, J. L., O. I. Gan, M. Doedens, J. C. Y. Wang, and J. E. Dick. 2006. Individual stem cells with highly variable proliferation and self-renewal properties comprise the human hematopoietic stem cell compartment. Nat. Immunol. 7:1225-1233.
24. Miller, A. D., and G. J. Rosman. 1989. Improved Retroviral vectors for gene transfer and expression. Biotechniques 7:980-990.
25. Montini, E., D. Cesana, M. Schmidt, F. Sanvito, C. C. Bartholomae, M. Ranzani, F. Benedicenti, L. S. Sergi, A. Ambrosi, M. Ponzoni, C. Doglioni, C. Di Serio, C. von Kalle, and L. Naldini. 2009. The genotoxic potential of retroviral vectors is strongly modulated by vector design and integration site selection in a mouse model of HSC gene therapy. J. Clin. Invest. 119:964-975.
26. Naldini, L., U. Blomer, P. Gallay, D. Ory, R. Mulligan, F. H. Gage, I. M. Verma, and D. Trono. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
27. Ott, M. G., M. Schmidt, K. Schwarzwaelder, S. Stein, U. Siler, U. Koehl, H. Glimm, K. Kuhlcke, A. Schilz, H. Kunkel, S. Naundorf, A. Brinkmann, A. Deichmann, M. Fischer, C. Ball, I. Pilz, C. Dunbar, Y. Du, N. A. Jenkins, N. G. Copeland, U. Luthi, M. Hassan, A. J. Thrasher, D. Hoelzer, C. von Kalle, R. Seger, and M. Grez. 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.
28. Roche Diagnostics. 2007. Amplicon sequencing. Roche Diagnostics GmbH, Mannheim, Germany. http://www.454.com/downloads/protocols/5-AmpliconSequencing. pdf.
29. + cells from the cord blood of ADA-deficient SCID neonates. Nat. Med. 9:463-468.
30. Schmidt, M., K. Schwarzwaelder, C. Bartholomae, K. Zaoui, C. Ball, I. Pilz, S. Braun, H. Glimm, and C. von Kalle. 2007. High-resolution insertion-site analysis by linear amplification-mediated PCR (LAM-PCR). Nat. Methods 4:1051-1057. (Pubitemid 350201778)
31. Schmidt, M., P. Zickler, G. Hoffmann, S. Haas, M. Wissler, A. Muessig, J. F. Tisdale, K. Kuramoto, R. G. Andrews, T. Wu, H.-P. Kiem, C. E. Dunbar, and C. von Kalle. 2002. Polyclonal long-term repopulating stem cell clones in a primate model. Blood 100:2737-2743.
32. Schröder, A. R., P. Shinn, H. Chen, C. Berry, J. R. Ecker, and F. Bushman. 2002. HIV-1 integration in the human genome favors active genes and local hotspots. 110:521-529.
33. Silver, J., and V. Kerrikatte. 1989. Novel use of polymerase chain reaction to amplify cellular DNA adjacent to an integrated provirus. J. Virol. 63:1924-1928. (Erratum, 64:3150, 1990.)
34. Stein, S., M. G. Ott, S. Schultze-Strasser, A. Jauch, B. Burwinkel, A. Kinner, M. Schmidt, A. Kramer, J. Schwable, H. Glimm, U. Koehl, C. Preiss, C. Ball, H. Martin, G. Gohring, K. Schwarzwaelder, W.-K. Hofmann, K. Karakaya, S. Tchatchou, R. Yang, P. Reinecke, K. Kuhlcke, B. Schlegelberger, A. J. Thrasher, D. Hoelzer, R. Seger, C. von Kalle, and M. Grez. 2010. Genomic instability and myelodysplasia with monosomy 7 consequent to EVI1 activation after gene therapy for chronic granulomatous disease. Nat. Med. 16:198-204.
35. Wang, G. P., C. C. Berry, N. Malani, P. Leboulch, A. Fischer, S. Hacein-Bey-Abina, M. Cavazzana-Calvo, and F. D. Bushman. Dynamics of gene-modified progenitor cells analyzed by tracking retroviral integration sites in a human SCID-X1 gene therapy trial. Blood 115:4356-4366.
36. Wang, G. P., A. Garrigue, A. Ciuffi, K. Ronen, J. Leipzig, C. Berry, C. Lagresle-Peyrou, F. Benjelloun, S. Hacein-Bey-Abina, A. Fischer, M. Cavazzana-Calvo, and F. D. Bushman. 2008. DNA bar coding and pyrosequencing to analyze adverse events in therapeutic gene transfer. Nucleic Acids Res. 36:e49.