Reactivating Fetal Hemoglobin Expression in Human Adult Erythroblasts Through BCL11A Knockdown Using Targeted Endonucleases

Molecular Therapy Nucleic Acids

Volumn 5, Issue , 2016, Pages e351-

  Bjurström, Carmen F ^a   Mojadidi, Michelle ^a   Phillips, John ^a   Kuo, Caroline ^a   Lai, Stephen ^a   Lill, Georgia R ^a   Cooper, Aaron ^a   Kaufman, Michael ^a   Urbinati, Fabrizia ^a   Wang, Xiaoyan ^a   Hollis, Roger P ^a   Kohn, Donald B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BCL11A; CRISPR Cas9; fetal hemoglobin; nonhomologous end joining; TALENs; zinc finger nucleases

Indexed keywords

ENDONUCLEASE; HEMOGLOBIN F; MESSENGER RNA; NUCLEASE; ZINC FINGER NUCLEASE; B CELL LYMPHOMA LEUKEMIA 11A ISOFORM 1; CD34 ANTIGEN; GUIDE RNA; REPRESSOR PROTEIN; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; ELECTROPORATION; ERYTHROBLAST; ERYTHROID CELL; FEMALE; GENE; GENE EDITING; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; K-562 CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRESSOR GENE; STEM CELL; ALLELE; CRISPR CAS SYSTEM; CRISPR CAS9 SYSTEM; ENZYME SPECIFICITY; GENE ACTIVATION; GENE EXPRESSION; GENE SILENCING; PLASMID; PROTEIN CLEAVAGE;

EID: 85015241817     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2016.52     Document Type: Article

References (47)

1. 1 Holt, N, Wang, J, Kim, K, Friedman, G, Wang, X, Taupin, V, et al. Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat Biotechnol 28 (2010), 839–847.
2. 2 Tebas, P, Stein, D, Tang, WW, Frank, I, Wang, SQ, Lee, G, et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N Engl J Med 370 (2014), 901–910.
3. 3 Hendel, A, Bak, RO, Clark, JT, Kennedy, AB, Ryan, DE, Roy, S, et al. Chemically modified guide RNAs enhance CRISPR-Cas genome editing in human primary cells. Nat Biotechnol 33 (2015), 985–989.
4. 4 Mandal, PK, Ferreira, LM, Collins, R, Meissner, TB, Boutwell, CL, Friesen, M, et al. Efficient ablation of genes in human hematopoietic stem and effector cells using CRISPR/Cas9. Cell Stem Cell 15 (2014), 643–652.
5. 5 Urnov, FD, Miller, JC, Lee, YL, Beausejour, CM, Rock, JM, Augustus, S, et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435 (2005), 646–651.
6. 6 Kim, HJ, Lee, HJ, Kim, H, Cho, SW, Kim, JS, Targeted genome editing in human cells with zinc finger nucleases constructed via modular assembly. Genome Res 19 (2009), 1279–1288.
7. 7 Cermak, T, Doyle, EL, Christian, M, Wang, L, Zhang, Y, Schmidt, C, et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res, 39, 2011, e82.
8. 8 Miller, JC, Tan, S, Qiao, G, Barlow, KA, Wang, J, Xia, DF, et al. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29 (2011), 143–148.
9. 9 Mali, P, Yang, L, Esvelt, KM, Aach, J, Guell, M, DiCarlo, JE, et al. RNA-guided human genome engineering via Cas9. Science 339 (2013), 823–826.
10. 10 Cong, L, Ran, FA, Cox, D, Lin, S, Barretto, R, Habib, N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339 (2013), 819–823.
11. 11 Wang, Z, Troilo, PJ, Wang, X, Griffiths, TG, Pacchione, SJ, Barnum, AB, et al. Detection of integration of plasmid DNA into host genomic DNA following intramuscular injection and electroporation. Gene Ther 11 (2004), 711–721.
12. 12 Gurunathan, S, Klinman, DM, Seder, RA, DNA vaccines: immunology, application, and optimization*. Annu Rev Immunol 18 (2000), 927–974.
13. 13 Shimokawa, T, Okumura, K, Ra, C, DNA induces apoptosis in electroporated human promonocytic cell line U937. Biochem Biophys Res Commun 270 (2000), 94–99.
14. 14 Xu, J, Peng, C, Sankaran, VG, Shao, Z, Esrick, EB, Chong, BG, et al. Correction of sickle cell disease in adult mice by interference with fetal hemoglobin silencing. Science 334 (2011), 993–996.
15. 15 Uda, M, Galanello, R, Sanna, S, Lettre, G, Sankaran, VG, Chen, W, et al. Genome-wide association study shows BCL11A associated with persistent fetal hemoglobin and amelioration of the phenotype of beta-thalassemia. Proc Natl Acad Sci USA 105 (2008), 1620–1625.
16. 16 Sankaran, VG, Xu, J, Ragoczy, T, Ippolito, GC, Walkley, CR, Maika, SD, et al. Developmental and species-divergent globin switching are driven by BCL11A. Nature 460 (2009), 1093–1097.
17. 17 Sankaran, VG, Menne, TF, Xu, J, Akie, TE, Lettre, G, Van Handel, B, et al. Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A. Science 322 (2008), 1839–1842.
18. 18 Menzel, S, Garner, C, Gut, I, Matsuda, F, Yamaguchi, M, Heath, S, et al. A QTL influencing F cell production maps to a gene encoding a zinc-finger protein on chromosome 2p15. Nat Genet 39 (2007), 1197–1199.
19. 19 Lettre, G, Sankaran, VG, Bezerra, MA, Araújo, AS, Uda, M, Sanna, S, et al. DNA polymorphisms at the BCL11A, HBS1L-MYB, and beta-globin loci associate with fetal hemoglobin levels and pain crises in sickle cell disease. Proc Natl Acad Sci USA 105 (2008), 11869–11874.
20. 20 Xu, J, Sankaran, VG, Ni, M, Menne, TF, Puram, RV, Kim, W, et al. Transcriptional silencing of {gamma}-globin by BCL11A involves long-range interactions and cooperation with SOX6. Genes Dev 24 (2010), 783–798.
21. 21 Jawaid, K, Wahlberg, K, Thein, SL, Best, S, Binding patterns of BCL11A in the globin and GATA1 loci and characterization of the BCL11A fetal hemoglobin locus. Blood Cells Mol Dis 45 (2010), 140–146.
22. 22 Tolhuis, B, Palstra, RJ, Splinter, E, Grosveld, F, de Laat, W, Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 10 (2002), 1453–1465.
23. 23 Sedgewick, AE, Timofeev, N, Sebastiani, P, So, JC, Ma, ES, Chan, LC, et al. BCL11A is a major HbF quantitative trait locus in three different populations with beta-hemoglobinopathies. Blood Cells Mol Dis 41 (2008), 255–258.
24. 24 Fine, EJ, Cradick, TJ, Zhao, CL, Lin, Y, Bao, G, An online bioinformatics tool predicts zinc finger and TALE nuclease off-target cleavage. Nucleic Acids Res, 42, 2014, e42.
25. 25 Gabriel, R, Lombardo, A, Arens, A, Miller, JC, Genovese, P, Kaeppel, C, et al. An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat Biotechnol 29 (2011), 816–823.
26. 26 Paruzynski, A, Arens, A, Gabriel, R, Bartholomae, CC, Scholz, S, Wang, W, et al. Genome-wide high-throughput integrome analyses by nrLAM-PCR and next-generation sequencing. Nat Protoc 5 (2010), 1379–1395.
27. 27 Romero, Z, Urbinati, F, Geiger, S, Cooper, AR, Wherley, J, Kaufman, ML, et al. β-globin gene transfer to human bone marrow for sickle cell disease. J Clin Invest, 2013 epub ahead of print.
28. 28 Giarratana, MC, Kobari, L, Lapillonne, H, Chalmers, D, Kiger, L, Cynober, T, et al. Ex vivo generation of fully mature human red blood cells from hematopoietic stem cells. Nat Biotechnol 23 (2005), 69–74.
29. 29 Guda, S, Brendel, C, Renella, R, Du, P, Bauer, DE, Canver, MC, et al. miRNA-embedded shRNAs for lineage-specific BCL11A knockdown and hemoglobin F induction. Mol Ther 23 (2015), 1465–1474.
30. 30 Canver, MC, Smith, EC, Sher, F, Pinello, L, Sanjana, NE, Shalem, O, et al. BCL11A enhancer dissection by Cas9-mediated in situ saturating mutagenesis. Nature 527 (2015), 192–197.
31. 31 Hoban, MD, Cost, GJ, Mendel, MC, Romero, Z, Kaufman, ML, Joglekar, AV, et al. Correction of the sickle cell disease mutation in human hematopoietic stem/progenitor cells. Blood 125 (2015), 2597–2604.
32. 32 Genovese, P, Schiroli, G, Escobar, G, Di Tomaso, T, Firrito, C, Calabria, A, et al. Targeted genome editing in human repopulating haematopoietic stem cells. Nature 510 (2014), 235–240.
33. 33 Nissim, L, Perli, SD, Fridkin, A, Perez-Pinera, P, Lu, TK, Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells. Mol Cell 54 (2014), 698–710.
34. 34 Sakuma, T, Nishikawa, A, Kume, S, Chayama, K, Yamamoto, T, Multiplex genome engineering in human cells using all-in-one CRISPR/Cas9 vector system. Sci Rep, 4, 2014, 5400.
35. 35 Osborn, MJ, Webber, BR, Knipping, F, Lonetree, CL, Tennis, N, DeFeo, AP, et al. Evaluation of TCR gene editing achieved by TALENs, CRISPR/Cas9, and megaTAL nucleases. Mol Ther 24 (2016), 570–581.
36. 36 Kim, Y, Kweon, J, Kim, JS, TALENs and ZFNs are associated with different mutation signatures. Nat Methods, 10, 2013, 185.
37. 37 Liu, P, Keller, JR, Ortiz, M, Tessarollo, L, Rachel, RA, Nakamura, T, et al. Bcl11a is essential for normal lymphoid development. Nat Immunol 4 (2003), 525–532.
38. 38 Yu, Y, Wang, J, Khaled, W, Burke, S, Li, P, Chen, X, et al. Bcl11a is essential for lymphoid development and negatively regulates p53. J Exp Med 209 (2012), 2467–2483.
39. 39 Sumiyoshi, T, Holt, NG, Hollis, RP, Ge, S, Cannon, PM, Crooks, GM, et al. Stable transgene expression in primitive human CD34+ hematopoietic stem/progenitor cells, using the Sleeping Beauty transposon system. Hum Gene Ther 20 (2009), 1607–1626.
40. 40 Hsu, PD, Scott, DA, Weinstein, JA, Ran, FA, Konermann, S, Agarwala, V, et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31 (2013), 827–832.
41. 41 Fu, Y, Foden, JA, Khayter, C, Maeder, ML, Reyon, D, Joung, JK, et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31 (2013), 822–826.
42. 42 Tsai, SQ, Zheng, Z, Nguyen, NT, Liebers, M, Topkar, VV, Thapar, V, et al. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat Biotechnol 33 (2015), 187–197.
43. 43 Miller, JC, Zhang, L, Xia, DF, Campo, JJ, Ankoudinova, IV, Guschin, DY, et al. Improved specificity of TALE-based genome editing using an expanded RVD repertoire. Nat Methods 12 (2015), 465–471.
44. 44 Zetsche, B, Gootenberg, JS, Abudayyeh, OO, Slaymaker, IM, Makarova, KS, Essletzbichler, P, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163 (2015), 759–771.
45. 45 Kleinstiver, BP, Pattanayak, V, Prew, MS, Tsai, SQ, Nguyen, NT, Zheng, Z, et al. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529 (2016), 490–495.
46. 46 Suzuki, J, Fujita, J, Taniguchi, S, Sugimoto, K, Mori, KJ, Characterization of murine hemopoietic-supportive (MS-1 and MS-5) and non-supportive (MS-K) cell lines. Leukemia 6 (1992), 452–458.
47. 47 Candotti, F, Shaw, KL, Muul, L, Carbonaro, D, Sokolic, R, Choi, C, et al. Gene therapy for adenosine deaminase-deficient severe combined immune deficiency: clinical comparison of retroviral vectors and treatment plans. Blood 120 (2012), 3635–3646.