Efficient modification of CCR5 in primary human hematopoietic cells using a megaTAL nuclease and AAV donor template

Science Translational Medicine

Volumn 7, Issue 307, 2015, Pages

  Sather, Blythe D ^a   Ibarra, Guillermo S Romano ^a   Sommer, Karen ^a   Curinga, Gabrielle ^a   Hale, Malika ^a   Khan, Iram F ^a   Singh, Swati ^a   Song, Yumei ^a   Gwiazda, Kamila ^a   Sahni, Jaya ^a   Jarjour, Jordan ^b   Astrakhan, Alexander ^b   Wagner, Thor A ^c,d   Scharenberg, Andrew M ^a,d,e   Rawlings, David J ^a,d,e  

^a SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^b BLUEBIRD BIO   (United States)

^c SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

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

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; CHIMERIC ANTIGEN RECEPTOR; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; MEGATAL NUCLEASE; NUCLEASE; PARVOVIRUS VECTOR; UNCLASSIFIED DRUG; CD3 ANTIGEN; DEOXYRIBONUCLEASE; GREEN FLUORESCENT PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIVIRAL ACTIVITY; ARTICLE; CELL ENGINEERING; CONTROLLED STUDY; DNA MODIFICATION; ENGRAFTMENT; GENE CASSETTE; GENE DISRUPTION; GENE LOCUS; GENE TARGETING; GENETIC RECOMBINATION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; ADULT; CELL CULTURE; DEPENDOPARVOVIRUS; DNA REPAIR; GENE THERAPY; GENETICS; HEMATOPOIETIC STEM CELL; METABOLISM; RNA EDITING;

ADULT; ANTIGENS, CD3; ANTIGENS, CD34; CELLS, CULTURED; DEOXYRIBONUCLEASES; DEPENDOVIRUS; DNA REPAIR; GENETIC LOCI; GENETIC THERAPY; GREEN FLUORESCENT PROTEINS; HEMATOPOIETIC STEM CELLS; HUMANS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, CCR5; RNA EDITING; T-LYMPHOCYTES;

EID: 84942921684     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aac5530     Document Type: Article

References (62)

1. H. M. Naif, Pathogenesis of HIV Infection. Infect. Dis. Rep. 5, e6 (2013).
2. M. Dean, M. Carrington, C. Winkler, G. A. Huttley, M. W. Smith, R. Allikmets, J. J. Goedert, S. P. Buchbinder, E. Vittinghoff, E. Gomperts, S. Donfield, D. Vlahov, R. Kaslow, A. Saah, C. Rinaldo, R. Detels, S. J. O'Brien, Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Science 273, 1856-1862 (1996).
3. R. Liu, W. A. Paxton, S. Choe, D. Ceradini, S. R. Martin, R. Horuk, M. E. MacDonald, H. Stuhlmann, R. A. Koup, N. R. Landau, Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86, 367-377 (1996).
4. M. Samson, F. Libert, B. J.Doranz, J. Rucker, C. Liesnard, C.-M. Farber, S. Saragosti, C. Lapouméroulie, J. Cognaux, C. Forceille, G. Muyldermans, C. Verhofstede, G. Burtonboy, M. Georges, T. Imai, S. Rana, Y. Yi, R. J. Smyth, R. G. Collman, R. W. Doms, G. Vassart, M. Parmentier, Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382, 722-725 (1996).
5. P. Tebas, D. Stein, W.W. Tang, I. Frank, S. Q.Wang, G. Lee, S. K. Spratt, R. T. Surosky, M. A. Giedlin, G. Nichol, M. C. Holmes, P. D. Gregory, D. G. Ando, M. Kalos, R. G. Collman, G. Binder-Scholl, G. Plesa, W. T. Hwang, B. L. Levine, C. H. June, Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N. Engl. J. Med. 370, 901-910 (2014).
6. R. A. Voit, M. A. McMahon, S. L. Sawyer, M. H. Porteus, Generation of an HIV resistant T-cell line by targeted "stacking" of restriction factors. Mol. Ther. 21, 786-795 (2013).
7. S. Boissel, J. Jarjour, A. Astrakhan, A. Adey, A. Gouble, P. Duchateau, J. Shendure, B. L. Stoddard, M. T. Certo, D. Baker, A. M. Scharenberg, megaTALs: A rare-cleaving nuclease architecture for therapeutic genome engineering. Nucleic Acids Res. 42, 2591-2601 (2014).
8. T. Tsuji, Y. Niida, Development of a simple and highly sensitive mutation screening system by enzyme mismatch cleavage with optimized conditions for standard laboratories. Electrophoresis 29, 1473-1483 (2008).
9. E. K. Brinkman, T. Chen, M. Amendola, B. van Steensel, Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res. 42, e168 (2014).
10. M. T. Certo, B. Y. Ryu, J. E. Annis, M. Garibov, J. Jarjour, D. J. Rawlings, A. M. Scharenberg, Tracking genome engineering outcome at individual DNA breakpoints. Nat. Methods 8, 671-676 (2011).
11. M. D. Hoban, G. J. Cost, M. C. Mendel, Z. Romero, M. L. Kaufman, A. V. Joglekar, M. Ho, D. Lumaquin, D. Gray, G. R. Lill, A. R. Cooper, F. Urbinati, S. Senadheera, A. Zhu, P.-Q. Liu, D. E. Paschon, L. Zhang, E. J. Rebar, A. Wilber, X. Wang, P. D. Gregory, M. C. Holmes, A. Reik, R. P. Hollis, D. B. Kohn, Correction of the sickle cell disease mutation in human hematopoietic stem/progenitor cells. Blood 125, 2597-2604 (2015).
12. P. Genovese, G. Schiroli, G. Escobar, T. Di Tomaso, C. Firrito, A. Calabria, D. Moi, R. Mazzieri, C. Bonini, M. C. Holmes, P. D. Gregory, M. van der Burg, B. Gentner, E. Montini, A. Lombardo, L. Naldini, Targeted genome editing in human repopulating haematopoietic stem cells. Nature 510, 235-240 (2014).
13. Y. Wang, I. F. Khan, S. Boissel, J. Jarjour, J. Pangallo, S. Thyme, D. Baker, A. M. Scharenberg, D. J. Rawlings, Progressive engineering of a homing endonuclease genome editing reagent for the murine X-linked immunodeficiency locus. Nucleic Acids Res. 42, 6463-6475 (2014).
14. E. E. Perez, J. Wang, J. C. Miller, Y. Jouvenot, K. A. Kim, O. Liu, N. Wang, G. Lee, V. V. Bartsevich, Y.-L. Lee, D. Y. Guschin, I. Rupniewski, A. J.Waite, C. Carpenito, R.G. Carroll, J. S.Orange, F. D. Urnov, E. J. Rebar, D. Ando, P. D. Gregory, J. L. Riley, M. C. Holmes, C. H. June, Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat. Biotechnol. 26, 808-816 (2008).
15. M. Egelhofer, G. Brandenburg, H. Martinius, P. Schult-Dietrich, G. Melikyan, R. Kunert, C. Baum, I. Choi, A. Alexandrov, D. von Laer, Inhibition of human immunodeficiency virus type 1 entry in cells expressing gp41-derived peptides. J. Virol. 78, 568-575 (2004).
16. M. Hildinger, M. T. Dittmar, P. Schult-Dietrich, B. Fehse, B. S. Schnierle, S. Thaler, G. Stiegler, R. Welker, D. von Laer, Membrane-anchored peptide inhibits human immunodeficiency virus entry. J. Virol. 75, 3038-3042 (2001).
17. L.M.Walker, M. Huber, K. J. Doores, E. Falkowska, R. Pejchal, J.-P. Julien, S.-K. Wang, A. Ramos, P.-Y. Chan-Hui, M. Moyle, J. L. Mitcham, P. W. Hammond, O. A. Olsen, P. Phung, S. Fling, C.-H. Wong, S. Phogat, T. Wrin, M. D. Simek, W. C. Koff, I. A. Wilson, D. R. Burton, P. Poignard; Protocol G Principal Investigators, Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477, 466-470 (2011).
18. B. Philip, E. Kokalaki, L. Mekkaoui, S. Thomas, K. Straathof, B. Flutter, V. Marin, T. Marafioti, R. Chakraverty, D. Linch, S. A. Quezada, K. S. Peggs, M. Pule, A highly compact epitope-based marker/suicide gene for easier and safer T-cell therapy. Blood 124, 1277-1287 (2014).
19. F. D. Urnov, J. C. Miller, Y.-L. Lee, C. M. Beausejour, J. M. Rock, S. Augustus, A. C. Jamieson, M. H. Porteus, P. D. Gregory, M. C. Holmes, Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435, 646-651 (2005).
20. P. K. Mandal, L. M. R. Ferreira, R. Collins, T. B. Meissner, C. L. Boutwell, M. Friesen, V. Vrbanac, B. S. Garrison, A. Stortchevoi, D. Bryder, K. Musunuru, H. Brand, A. M. Tager, T. M. Allen, M. E. Talkowski, D. J. Rossi, C. A. Cowan, Efficient ablation of genes in human hematopoietic stem and effector cells using CRISPR/Cas9. Cell Stem Cell 15, 643-652 (2014).
21. B. Berdien, U. Mock, D. Atanackovic, B. Fehse, TALEN-mediated editing of endogenous T-cell receptors facilitates efficient reprogramming of T lymphocytes by lentiviral gene transfer. Gene Ther. 21, 539-548 (2014).
22. P. C. Hendrie, D. W. Russell, Gene targeting with viral vectors. Mol. Ther. 12, 9-17 (2005).
23. A. Vasileva, R. Jessberger, Precise hit: Adeno-associated virus in gene targeting. Nat. Rev. Microbiol. 3, 837-847 (2005).
24. A. Vasileva, R. M. Linden, R. Jessberger, Homologous recombination is required for AAVmediated gene targeting. Nucleic Acids Res. 34, 3345-3360 (2006).
25. R. K. Hirata, D. W. Russell, Design and packaging of adeno-associated virus gene targeting vectors. J. Virol. 74, 4612-4620 (2000).
26. B. L. Ellis, M. L. Hirsch, S. N. Porter, R. J. Samulski, M. H. Porteus, Zinc-finger nuclease-mediated gene correction using single AAV vector transduction and enhancement by food and drug Administration-approved drugs. Gene Ther. 20, 35-42 (2013).
27. K. Gellhaus, T. I. Cornu, R. Heilbronn, T. Cathomen, Fate of recombinant adeno-associated viral vector genomes during DNA double-strand break-induced gene targeting in human cells. Hum. Gene Ther. 21, 543-553 (2010).
28. E.M.Händel, K. Gellhaus, K. Khan, C. Bednarski, T. I. Cornu, F.Müller-Lerch, R.M. Kotin, R.Heilbronn, T. Cathomen, Versatile and efficient genome editing in human cells by combining zinc-finger nucleases with adeno-associated viral vectors. Hum. Gene Ther. 23, 321-329 (2012).
29. M. L. Hirsch, L. Green, M. H. Porteus, R. J. Samulski, Self-complementary AAV mediates gene targeting and enhances endonuclease delivery for double-strand break repair. Gene Ther. 17, 1175-1180 (2010).
30. H. Li, V. Haurigot, Y. Doyon, T. Li, S. Y.Wong, A. S. Bhagwat, N. Malani, X. M. Anguela, R. Sharma, L. Ivanciu, S. L. Murphy, J. D. Finn, F. R. Khazi, S. Zhou, D. E. Paschon, E. J. Rebar, F. D. Bushman, P. D. Gregory, M. C. Holmes, K. A. High, In vivo genome editing restores haemostasis in a mouse model of haemophilia. Nature 475, 217-221 (2011).
31. D. G. Miller, L. M. Petek, D. W. Russell, Human gene targeting by adeno-associated virus vectors is enhanced by DNA double-strand breaks. Mol. Cell Biol. 23, 3550-3557 (2003).
32. M. H. Porteus, T. Cathomen, M. D. Weitzman, D. Baltimore, Efficient gene targeting mediated by adeno-associated virus and DNA double-strand breaks. Mol. Cell Biol. 23, 3558-3565 (2003).
33. B. L. Ellis, M. L. Hirsch, J. C. Barker, J. P. Connelly, R. J. Steininger III, M. H. Porteus, A survey of ex vivo/in vitro transduction efficiency of mammalian primary cells and cell lines with nine natural adeno-associated virus (AAV1-9) and one engineered adeno-associated virus serotype. Virol. J. 10, 74 (2013).
34. L. J. Smith, T. Ul-Hasan, S. K. Carvaines, K. Van Vliet, E. Yang, K. K. Wong Jr., M. Agbandje-McKenna, S. Chatterjee, Gene transfer properties and structural modeling of human stem cell-derived AAV. Mol.Ther. 22, 1625-1634 (2014).
35. L. Song, M. A. Kauss, E. Kopin, M. Chandra, T. Ul-Hasan, E. Miller, G. R. Jayandharan, A. E. Rivers, G. V. Aslanidi, C. Ling, B. Li, W. Ma, X. Li, L. M. Andino, L. Zhong, A. F. Tarantal, M. C. Yoder, K. K. Wong Jr., M. Tan, S. Chatterjee, A. Srivastava, Optimizing the transduction efficiency of capsid-modified AAV6 serotype vectors in primary human hematopoietic stem cells in vitro and in a xenograft mouse model in vivo. Cytotherapy 15, 986-998 (2013).
36. L. Song, X. Li, G. R. Jayandharan, Y. Wang, G. V. Aslanidi, C. Ling, L. Zhong, G. Gao, M. C. Yoder, C. Ling, M. Tan, A. Srivastava, High-efficiency transduction of primary human hematopoietic stem cells and erythroid lineage-restricted expression by optimized AAV6 serotype vectors in vitro and in a murine xenograft model in vivo. PLOS One 8, e58757 (2013).
37. D. G. Miller, L. M. Petek, D. W. Russell, Adeno-associated virus vectors integrate at chromosome breakage sites. Nat. Genet. 36, 767-773 (2004).
38. C. H. June, S. R. Riddell, T. N. Schumacher, Adoptive cellular therapy: A race to the finish line. Sci. Transl. Med. 7, 280ps287 (2015).
39. P.-M. Challita, D. Skelton, A. El-Khoueiry, X.-J. Yu, K. Weinberg, D. B. Kohn, Multiple modifications in cis elements of the long terminal repeat of retroviral vectors lead to increased expression and decreased DNA methylation in embryonic carcinoma cells. J. Virol. 69, 748-755 (1995).
40. S. Halene, L. Wang, R. M. Cooper, D. C. Bockstoce, P. B. Robbins, D. B. Kohn, Improved expression in hematopoietic and lymphoid cells in mice after transplantation of bone marrow transduced with a modified retroviral vector. Blood 94, 3349-3357 (1999).
41. N. Cartier, 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. Lefrère, S. Blanche, M. Audit, E. Payen, P. Leboulch, B. l'Homme, P. Bougnères, C. Von Kalle, A. Fischer, M. Cavazzana-Calvo, P. Aubourg, Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326, 818-823 (2009).
42. R. M. Koldej, G. Carney, M. M. Wielgosz, S. Zhou, J. Zhan, B. P. Sorrentino, A. W. Nienhuis, Comparison of insulators and promoters for expression of the Wiskott-Aldrich syndrome protein using lentiviral vectors. Hum. Gene Ther. Clin. Dev. 24, 77-85 (2013).
43. S. Gill, C. H. June, Going viral: Chimeric antigen receptor T-cell therapy for hematological malignancies. Immunol. Rev. 263, 68-89 (2015).
44. J. Jarjour, H. West-Foyle, M. T. Certo, C. G. Hubert, L. Doyle, M. M. Getz, B. L. Stoddard, A. M. Scharenberg, High-resolution profiling of homing endonuclease binding and catalytic specificity using yeast surface display. Nucleic Acids Res. 37, 6871-6880 (2009).
45. T. Cermak, E. L. Doyle, M. Christian, L. Wang, Y. Zhang, C. Schmidt, J. A. Baller, N. V. Somia, A. J. Bogdanove, D. F. Voytas, Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82 (2011).
46. J. C. Miller, S. Tan, G. Qiao, K. A. Barlow, J. Wang, D. F. Xia, X. Meng, D. E. Paschon, E. Leung, S. J. Hinkley, G. P. Dulay, K. L. Hua, I. Ankoudinova, G. J. Cost, F. D. Urnov, H. S. Zhang, M. C. Holmes, L. Zhang, P. D. Gregory, E. J. Rebar, A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143-148 (2011).
47. I. F. Khan, R. K. Hirata, D. W. Russell, AAV-mediated gene targeting methods for human cells. Nat. Protoc. 6, 482-501 (2011).
48. C. Aurnhammer, M. Haase, N. Muether, M. Hausl, C. Rauschhuber, I. Huber, H. Nitschko, U. Busch, A. Sing, A. Ehrhardt, A. Baiker, Universal real-time PCR for the detection and quantification of adeno-associated virus serotype 2-derived inverted terminal repeat sequences. Hum.Gene Ther. Methods 23, 18-28 (2012).
49. X. Wang, S. C. Shin, A. F. Chiang, I. Khan, D. Pan, D. J. Rawlings, C. H. Miao, Intraosseous delivery of lentiviral vectors targeting factor VIII expression in platelets corrects murine hemophilia A. Mol. Ther. 23, 617-626 (2015).
50. Y. Akatsuka, E. G. Martin, A. Madonik, A. A. Barsoukov, J. A. Hansen, Rapid screening of T-cell receptor (TCR) variable gene usage by multiplex PCR: Application for assessment of clonal composition. Tissue Antigens 53, 122-134 (1999).
51. A. Konno, K. Okada, K. Mizuno, M.Nishida, S. Nagaoki, T. Toma, T. Uehara, K. Ohta, Y. Kasahara, H. Seki, A. Yachie, S. Koizumi, CD8aa memory effector T cells descend directly from clonally expanded CD8a+bhigh TCRab T cells in vivo. Blood 100, 4090-4097 (2002).
52. A. E. Boitano, J.Wang, R. Romeo, L. C. Bouchez, A. E. Parker, S. E. Sutton, J. R. Walker, C. A. Flaveny, G. H. Perdew, M. S. Denison, P. G. Schultz, M. P. Cooke, Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329, 1345-1348 (2010).
53. S. Terakura, T. N. Yamamoto, R. A. Gardner, C. J. Turtle, M. C. Jensen, S. R. Riddell, Generation of CD19-chimeric antigen receptor modified CD8+ T cells derived from virus-specific central memory T cells. Blood 119, 72-82 (2012).
54. J. Wang, O. W. Press, C. G. Lindgren, P. Greenberg, S. Riddell, X. Qian, C. Laugen, A. Raubitschek, S. J. Forman, M. C. Jensen, Cellular immunotherapy for follicular lymphoma using genetically modified CD20-specific CD8+ cytotoxic T lymphocytes. Mol. Ther. 9, 577-586 (2004).
55. E. A. Rutledge, C. L. Halbert, D. W. Russell, Infectious clones and vectors derived from adeno-associated virus (AAV) serotypes other than AAV type 2. J. Virol. 72, 309-319 (1998).
56. D. Grimm, J. S. Lee, L.Wang, T. Desai, B. Akache, T. A. Storm, M. A. Kay, In vitro and in vivo gene therapy vector evolution via multispecies interbreeding and retargeting of adeno-associated viruses. J. Virol. 82, 5887-5911 (2008).
57. D. E. Bowles, S. W. J. McPhee, C. Li, S. J. Gray, J. J. Samulski, A. S. Camp, J. Li, B.Wang, P. E.Monahan, J. E. Rabinowitz, J. C. Grieger, L. Govindasamy, M. Agbandje-McKenna, X. Xiao, R. J. Samulski, Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol. Ther. 20, 443-455 (2012).
58. N. Levitt, D. Briggs, A. Gil, N. J. Proudfoot, Definition of an efficient synthetic poly(A) site. Genes Dev. 3, 1019-1025 (1989).
59. M. C. Milone, J. D. Fish, C. Carpenito, R. G. Carroll, G. K. Binder, D. Teachey, M. Samanta, M. Lakhal, B. Gloss, G. Danet-Desnoyers, D. Campana, J. L. Riley, S. A. Grupp, C. H. June, Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol. Ther. 17, 1453-1464 (2009).
60. A. Buchacher, R. Predl, K. Strutzenberger, W. Steinfellner, A. Trkola, M. Purtscher, G. Gruber, C. Tauer, F. Steindl, A. Jungbauer, H. Katinger, Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res. Hum. Retroviruses 10, 359-369 (1994).
61. M. Purtscher, A. Trkola, A. Grassauer, P. M. Schulz, A. Klima, S. Döpper, G. Gruber, A. Buchacher, T. Muster, H. Katinger, Restricted antigenic variability of the epitope recognized by the neutralizing gp41 antibody 2F5. AIDS 10, 587-593 (1996).
62. M. Purtscher, A. Trkola, G. Gruber, A. Buchacher, R. Predl, F. Steindl, C. Tauer, R. Berger, N. Barrett, A. Jungbauer, H. Katinger, A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 10, 1651-1658 (1994).