Gene editing and its application for hematological diseases

International Journal of Hematology

Volumn 104, Issue 1, 2016, Pages 18-28

  Osborn, Mark J ^a   Belanto, Joseph J ^a   Tolar, Jakub ^a   Voytas, Daniel F ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Blood disorders; CRISPR Cas9; Hematopoiesis; Hematopoietic stem cells; TALEN; ZFN

Indexed keywords

ENDONUCLEASE;

GENE EDITING; GENE TARGETING; GENE THERAPY; GENETICS; HEMATOLOGIC DISEASES; HUMAN; PROCEDURES;

ENDONUCLEASES; GENE EDITING; GENE TARGETING; GENETIC THERAPY; HEMATOLOGIC DISEASES; HUMANS;

EID: 84970971336     PISSN: 09255710     EISSN: 18653774     Source Type: Journal    
DOI: 10.1007/s12185-016-2017-z     Document Type: Review

References (116)

1. 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;118:3132–42.
2. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science. 2003;302:415–9.
3. Cumming RC, Liu JM, Youssoufian H, Buchwald M. Suppression of apoptosis in hematopoietic factor-dependent progenitor cell lines by expression of the FAC gene. Blood. 1996;88:4558–67.
4. Beerli RR, Barbas CF 3rd. Engineering polydactyl zinc-finger transcription factors. Nat Biotechnol. 2002;20:135–41.
5. Kim YG, Cha J, Chandrasegaran S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA. 1996;93:1156–60.
6. Doyon Y, Vo TD, Mendel MC, et al. Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat Methods. 2011; 8:74–79
7. Ramirez CL, Foley JE, Wright DA, et al. Unexpected failure rates for modular assembly of engineered zinc fingers. Nat Methods. 2008;5:374–5.
8. 2 zinc-finger arrays. Nucleic Acids Res. 2011;39:4680–90.
9. Maeder ML, Thibodeau-Beganny S, Osiak A, et al. Rapid “open-source” engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell. 2008;31:294–301.
10. Maeder ML, Thibodeau-Beganny S, Sander JD, Voytas DF, Joung JK. Oligomerized pool engineering (OPEN): an ‘open-source’ protocol for making customized zinc-finger arrays. Nat Protoc. 2009;4:1471–501.
11. Reyon D, Kirkpatrick JR, Sander JD, et al. ZFNGenome: a comprehensive resource for locating zinc finger nuclease target sites in model organisms. BMC Genom. 2011;12:83.
12. Hermann M, Maeder ML, Rector K, et al. Evaluation of OPEN zinc finger nucleases for direct gene targeting of the ROSA26 locus in mouse embryos. PLoS One. 2012;7:e41796.
13. Sander JD, Dahlborg EJ, Goodwin MJ, et al. Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nat Methods. 2011;8:67–9.
14. Osborn MJ, DeFeo AP, Blazar BR, Tolar J. Synthetic zinc finger nuclease design and rapid assembly. Hum Gene Ther. 2011;22:1155–65.
15. Voytas DF, Joung JK. Plant science. DNA binding made easy. Science. 2009;326:1491–2.
16. Kay S, Hahn S, Marois E, Hause G, Bonas U. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science. 2007;318:648–51.
17. Romer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science. 2007;318:645–8.
18. Boch J, Scholze H, Schornack S, et al. Breaking the code of DNA binding specificity of TAL-type III effectors. Science. 2009;326:1509–12.
19. Bogdanove AJ, Voytas DF. TAL effectors: customizable proteins for DNA targeting. Science. 2011;333:1843–6.
20. Streubel J, Blucher C, Landgraf A, Boch J. TAL effector RVD specificities and efficiencies. Nat Biotechnol. 2012;30:593–5.
21. Engler C, Gruetzner R, Kandzia R, Marillonnet S. Golden gate shuffling: a one-pot DNA shuffling method based on type IIs restriction enzymes. PLoS One. 2009;4:e5553.
22. Cermak T, Doyle EL, Christian M, et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 2011;39:e82.
23. Li L, Piatek MJ, Atef A, et al. Rapid and highly efficient construction of TALE-based transcriptional regulators and nucleases for genome modification. Plant Mol Biol. 2012;78:407–16.
24. Sanjana NE, Cong L, Zhou Y, Cunniff MM, Feng G, Zhang F. A transcription activator-like effector toolbox for genome engineering. Nat Protoc. 2012;7:171–92.
25. Maeder ML, Linder SJ, Reyon D, et al. Robust, synergistic regulation of human gene expression using TALE activators. Nat Methods. 2013;10:243–5.
26. Holkers M, Maggio I, Liu J, et al. Differential integrity of TALE nuclease genes following adenoviral and lentiviral vector gene transfer into human cells. Nucleic Acids Res. 2013;41:e63.
27. Silva G, Poirot L, Galetto R, et al. Meganucleases and other tools for targeted genome engineering: perspectives and challenges for gene therapy. Curr Gene Ther. 2011;11:11–27.
28. Baxter S, Lambert AR, Kuhar R, et al. Engineering domain fusion chimeras from I-OnuI family LAGLIDADG homing endonucleases. Nucleic Acids Res. 2012;40:7985–8000.
29. Stoddard BL. Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification. Structure. 2011;19:7–15.
30. Baxter S, Lambert AR, Kuhar R, et al. Engineering domain fusion chimeras from I-OnuI family LAGLIDADG homing endonucleases. Nucleic Acids Res. 2012;40:7985–8000.
31. Boissel S, Jarjour J, Astrakhan A, et al. megaTALs: a rare-cleaving nuclease architecture for therapeutic genome engineering. Nucleic Acids Res. 2014;42:2591–601.
32. Poirot L, Philip B, Schiffer-Mannioui C et al. Multiplex genome edited T-cell manufacturing platform for “off-the-shelf” adoptive T-cell immunotherapies. Cancer Res. 2015;75:3853–64.
33. Baxter SK, Lambert AR, Scharenberg AM, Jarjour J. Flow cytometric assays for interrogating LAGLIDADG homing endonuclease DNA-binding and cleavage properties. Methods Mol Biol. 2013;978:45–61.
34. Osborn MJ, Webber BR, Knipping F, et al. Evaluation of TCR Gene Editing achieved by TALENs, CRISPR/Cas9 and megaTAL nucleases. Mol Ther. 2016;24:570–81.
35. Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol. 1987;169:5429–33.
36. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology. 2005;151:2551–61.
37. Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, Soria E. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol. 2005;60:174–82.
38. Pourcel C, Salvignol G, Vergnaud G. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology. 2005;151:653–63.
39. Marraffini LA, Sontheimer EJ. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature. 2010;463:568–71.
40. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337:816–21.
41. Qi LS, Larson MH, Gilbert LA, et al. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell. 2013;152:1173–83.
42. L. Cong, F. A. Ran, D. Cox et al. Multiplex Genome Engineering Using CRISPR/Cas Systems. Science.
43. Mali P, Yang L, Esvelt KM, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339:823–6.
44. Cho SW, Kim S, Kim JM, Kim JS. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol. 2013;31:230–2.
45. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J. RNA-programmed genome editing in human cells. Elife. 2013;2:e00471.
46. Hendel A, Bak RO, Clark JT, et al. Chemically modified guide RNAs enhance CRISPR-Cas genome editing in human primary cells. Nat Biotechnol. 2015;33:985–9.
47. Cheng AW, Wang H, Yang H, et al. Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Res. 2013;23:1163–71.
48. Cong L, Ran FA, Cox D, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339:819–23.
49. Konermann S, Brigham MD, Trevino AE, et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature. 2015;517:583–8.
50. Esvelt KM, Mali P, Braff JL, Moosburner M, Yaung SJ, Church GM. Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat Methods. 2013;10:1116–21.
51. Hou Z, Zhang Y, Propson NE, et al. Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc Natl Acad Sci USA. 2013;110:15644–9.
52. Ran FA, Cong L, Yan WX, et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature. 2015;520:186–91.
53. Zetsche B, Gootenberg JS, Abudayyeh OO, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 2015;163:759–71.
54. Kleinstiver BP, Prew MS, Tsai SQ, et al. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature. 2015;523:481–5.
55. Kleinstiver BP, Prew MS, Tsai SQ, et al. Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nat Biotechnol. 2015;33:1293–8.
56. Fu Y, Foden JA, Khayter C, et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol. 2013;31:822–6.
57. Kleinstiver BP, Pattanayak V, Prew MS, et al. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature. 2016;529:490–5.
58. Kleinstiver BP, Prew MS, Tsai SQ, et al. Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nat Biotechnol. 2015;33:1293–8.
59. Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol. 2014;32:279–84.
60. Dahlman JE, Abudayyeh OO, Joung J, Gootenberg JS, Zhang F, Konermann S. Orthogonal gene knockout and activation with a catalytically active Cas9 nuclease. Nat Biotechnol. 2015;33:1159–61.
61. Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F. Rationally engineered Cas9 nucleases with improved specificity. Science. 2016;351:84–8.
62. Shen B, Zhang W, Zhang J, et al. Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat Methods. 2014;11:399–402.
63. Fujii W, Onuma A, Sugiura K, Naito K. Efficient generation of genome-modified mice via offset-nicking by CRISPR/Cas system. Biochem Biophys Res Commun. 2014;445:791–4.
64. Ran FA, Hsu PD, Lin CY, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell. 2013;154:1380–9.
65. Guilinger JP, Thompson DB, Liu DR. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol. 2014;32:577–82.
66. Farzadfard F, Perli SD, Lu TK. Tunable and multifunctional eukaryotic transcription factors based on CRISPR/Cas. ACS Synth Biol. 2013;2:604–13.
67. Perez-Pinera P, Kocak DD, Vockley CM, et al. RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat Methods. 2013;10:973–6.
68. Gilbert LA, Larson MH, Morsut L, et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell. 2013;154:442–51.
69. Lombardo A, Genovese P, Beausejour CM, et al. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol. 2007;25:1298–306.
70. Genovese P, Schiroli G, Escobar G, et al. Targeted genome editing in human repopulating haematopoietic stem cells. Nature. 2014;510:235–40.
71. Goessling W, Allen RS, Guan X, et al. Prostaglandin E2 enhances human cord blood stem cell xenotransplants and shows long-term safety in preclinical nonhuman primate transplant models. Cell Stem Cell. 2011;8:445–58.
72. North TE, Goessling W, Walkley CR, et al. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature. 2007;447:1007–11.
73. Boitano AE, Wang J, Romeo R, et al. Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science. 2010;329:1345–8.
74. Hoggatt J, Singh P, Sampath J, Pelus LM. Prostaglandin E2 enhances hematopoietic stem cell homing, survival, and proliferation. Blood. 2009;113:5444–55.
75. Wang J, Exline CM, DeClercq JJ, et al. Homology-driven genome editing in hematopoietic stem and progenitor cells using ZFN mRNA and AAV6 donors. Nat Biotechnol. 2015;33:1256–63.
76. Sather BD, Romano Ibarra GS, Sommer K, et al. Efficient modification of CCR5 in primary human hematopoietic cells using a megaTAL nuclease and AAV donor template. Sci Transl Med. 2015;7:307ra156.
77. Wang J, DeClercq JJ, Hayward SB, et al. Highly efficient homology-driven genome editing in human T cells by combining zinc-finger nuclease mRNA and AAV6 donor delivery. Nucleic Acids Res. 2016;44:e30.
78. Tebas P, Stein D, Tang WW, et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N Engl J Med. 2014;370:901–10.
79. 4+ T cells from HIV-1 infection. Blood. 2014;123:61–9.
80. Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371:1507–17.
81. Provasi E, Genovese P, Lombardo A, et al. Editing T cell specificity towards leukemia by zinc finger nucleases and lentiviral gene transfer. Nat Med. 2012;18:807–15.
82. Torikai H, Reik A, Liu PQ, et al. A foundation for universal T-cell based immunotherapy: T cells engineered to express a CD19-specific chimeric-antigen-receptor and eliminate expression of endogenous TCR. Blood. 2012;119:5697–705.
83. Berdien B, Mock U, Atanackovic D, Fehse B. TALEN-mediated editing of endogenous T-cell receptors facilitates efficient reprogramming of T lymphocytes by lentiviral gene transfer. Gene Ther. 2014;21:539–48.
84. Alinari L, Lapalombella R, Andritsos L, Baiocchi RA, Lin TS, Byrd JC. Alemtuzumab (Campath-1H) in the treatment of chronic lymphocytic leukemia. Oncogene. 2007;26:3644–53.
85. Frock RL, Hu J, Meyers RM, Ho YJ, Kii E, Alt FW. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat Biotechnol. 2015;33:179–86.
86. Tsai SQ, Zheng Z, Nguyen NT, et al. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat Biotechnol. 2015;33:187–97.
87. Mussolino C, Alzubi J, Fine EJ, et al. TALENs facilitate targeted genome editing in human cells with high specificity and low cytotoxicity. Nucleic Acids Res. 2014;42:6762–73.
88. Cho SW, Kim S, Kim Y, et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res. 2014;24:132–41.
89. Gabriel R, Lombardo A, Arens A, et al. An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat Biotechnol. 2011;29:816–23.
90. Qasim W, Amrolia PJ, Samarasinghe S, Ghorashian S, Zhan H, Stafford S, Butler K, Ahsan G, Gilmour K, Adams S, Pinner D, Chiesa R, Chatters S, Swift S, Goulden N, Peggs K, Thrasher AJ, Veys P, Pule M. First clinical application of Talen engineered universal CAR19 T cells in B-ALL. Blood. 2015;126:2046.
91. Hofmeister CC, Zhang J, Knight KL, Le P, Stiff PJ. Ex vivo expansion of umbilical cord blood stem cells for transplantation: growing knowledge from the hematopoietic niche. Bone Marrow Transpl. 2007;39:11–23.
92. Medvinsky A, Rybtsov S, Taoudi S. Embryonic origin of the adult hematopoietic system: advances and questions. Development. 2011;138:1017–31.
93. Tavian M, Biasch K, Sinka L, Vallet J, Peault B. Embryonic origin of human hematopoiesis. Int J Dev Biol. 2010;54:1061–5.
94. Arora N, Wenzel PL, McKinney-Freeman SL, et al. Effect of developmental stage of HSC and recipient on transplant outcomes. Dev Cell. 2014;29:621–8.
95. Vo LT, Daley GQ. De novo generation of HSCs from somatic and pluripotent stem cell sources. Blood. 2015;125:2641–8.
96. Li H, Haurigot V, Doyon Y, et al. In vivo genome editing restores haemostasis in a mouse model of haemophilia. Nature. 2011;475:217–21.
97. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–72.
98. Moreau T, Colzani M, Arumugam M, et al. In vitro production of megakaryocytes and platelets from human induced pluripotent cells by GMP compatible methods. Blood. 2013;122:2401.
99. Themeli M, Kloss CC, Ciriello G, et al. Generation of tumor-targeted human T lymphocytes from induced pluripotent stem cells for cancer therapy. Nat Biotechnol. 2013;31:928–33.
100. Lee DW, Barrett DM, Mackall C, Orentas R, Grupp SA. The future is now: chimeric antigen receptors as new targeted therapies for childhood cancer. Clin Cancer Res. 18:2780–2790.
101. Maude SL, Shpall EJ, Grupp SA. Chimeric antigen receptor T-cell therapy for ALL. Hematol Am Soc Hematol Educ Progr. 2014;2014:559–64.
102. Gattinoni L, Klebanoff CA, Restifo NP. Paths to stemness: building the ultimate antitumour T cell. Nat Rev Cancer. 2012;12:671–84.
103. Lugli E, Dominguez MH, Gattinoni L, et al. Superior T memory stem cell persistence supports long-lived T cell memory. J Clin Invest. 2013;123:594–9.
104. Giani FC, Fiorini C, Wakabayashi A, et al. Targeted application of human genetic variation can improve red blood cell production from stem cells. Cell Stem Cell. 2016;18:73–8.
105. Osborn MJ, Gabriel R, Webber BR, et al. Fanconi anemia gene editing by the CRISPR/Cas9 system. Hum Gene Ther. 2015;26:114–26.
106. Rio P, Banos R, Lombardo A, et al. Targeted gene therapy and cell reprogramming in Fanconi anemia. EMBO Mol Med. 2014;6:835–48.
107. Muller LU, Milsom MD, Harris CE, et al. Overcoming reprogramming resistance of Fanconi anemia cells. Blood. 2012;119:5449–57.
108. Keller G, Kennedy M, Papayannopoulou T, Wiles MV. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol Cell Biol. 1993;13:473–86.
109. Amabile G, Welner RS, Nombela-Arrieta C, et al. In vivo generation of transplantable human hematopoietic cells from induced pluripotent stem cells. Blood. 2013;121:1255–64.
110. Suzuki N, Yamazaki S, Yamaguchi T, et al. Generation of engraftable hematopoietic stem cells from induced pluripotent stem cells by way of teratoma formation. Mol Ther. 2013;21:1424–31.
111. Sandler VM, Lis R, Liu Y, et al. Reprogramming human endothelial cells to haematopoietic cells requires vascular induction. Nature. 2014;511:312–8.
112. Mali P, Yang L, Esvelt KM, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339:823–6.
113. Shalem O, Sanjana NE, Hartenian E, et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science. 2014;343:84–7.
114. Bauer DE, Kamran SC, Lessard S, et al. An erythroid enhancer of BCL11A subject to genetic variation determines fetal hemoglobin level. Science. 2013;342:253–7.
115. Canver MC, Smith EC, Sher F, et al. BCL11A enhancer dissection by Cas9-mediated in situ saturating mutagenesis. Nature. 2015;527:192–7.
116. Hilton IB, D’Ippolito AM, Vockley CM, et al. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol. 2015;33:510–7.