CRISPR/Cas9 β-globin gene targeting in human haematopoietic stem cells

Nature

Volumn 539, Issue 7629, 2016, Pages 384-389

  Dever, Daniel P ^a   Bak, Rasmus O ^a   Reinisch, Andreas ^b   Camarena, Joab ^a   Washington, Gabriel ^a   Nicolas, Carmencita E ^a   Pavel Dinu, Mara ^a   Saxena, Nivi ^a   Wilkens, Alec B ^a   Mantri, Sruthi ^a   Uchida, Nobuko ^c,d   Hendel, Ayal ^a   Narla, Anupama ^a   Majeti, Ravindra ^b   Weinberg, Kenneth I ^a   Porteus, Matthew H ^a  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c StemCells Inc   (United States)

^d Stanford Medicine Children s Health   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CASPASE 9; HEMOGLOBIN BETA CHAIN; MESSENGER RNA; RIBONUCLEOPROTEIN; CD34 ANTIGEN; CRISPR ASSOCIATED PROTEIN; MICROSPHERE;

BLOOD; CELLS AND CELL COMPONENTS; GENE EXPRESSION; MUTATION; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; CRISPR CAS SYSTEM; ENGRAFTMENT; ERYTHROCYTE; FLUORESCENCE ACTIVATED CELL SORTING; GENE; GENE EXPRESSION; GENE FREQUENCY; GENE MUTATION; GENE TARGETING; HEMATOPOIETIC STEM CELL; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA EDITING; SICKLE CELL ANEMIA; TRANSCRIPTION REGULATION; ALLELE; ANEMIA, SICKLE CELL; ANIMAL; BETA-THALASSEMIA; BIOSYNTHESIS; CELL LINEAGE; CELL SEPARATION; DEPENDOPARVOVIRUS; FEMALE; FLOW CYTOMETRY; GENE EDITING; GENE THERAPY; GENETICS; MAGNET; METABOLISM; MUTATION; NONOBESE DIABETIC MOUSE; PATHOLOGY; PROCEDURES; REPORTER GENE; SCID MOUSE;

ALLELES; ANEMIA, SICKLE CELL; ANIMALS; ANTIGENS, CD34; BETA-GLOBINS; BETA-THALASSEMIA; CELL DIFFERENTIATION; CELL LINEAGE; CELL SEPARATION; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; DEPENDOVIRUS; ERYTHROCYTES; FEMALE; FLOW CYTOMETRY; GENE EDITING; GENE TARGETING; GENES, REPORTER; GENETIC THERAPY; HEMATOPOIETIC STEM CELLS; HOMOLOGOUS RECOMBINATION; HUMANS; MAGNETS; MICE, INBRED NOD; MICE, SCID; MICROSPHERES; MUTATION; RNA, MESSENGER;

EID: 84996587545     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature20134     Document Type: Article

References (48)

1. Naldini, L. Ex vivo gene transfer and correction for cell-based therapies. Nat. Rev. Genet. 12, 301-315 (2011).
2. Porteus, M. Genome editing: a new approach to human therapeutics. Annu. Rev. Pharmacol. Toxicol. 56, 163-190 (2016).
3. Smithies, O., Gregg, R. G., Boggs, S. S., Koralewski, M. A., Kucherlapati, R. S. Insertion of DNA sequences into the human chromosomal-globin locus by homologous recombination. Nature 317, 230-234 (1985).
4. Porteus, M. H., Baltimore, D. Chimeric nucleases stimulate gene targeting in human cells. Science 300, 763 (2003).
5. Rouet, P., Smih, F., Jasin, M. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc. Natl Acad. Sci. USA 91, 6064-6068 (1994).
6. Hsu, P. D., Lander, E. S., Zhang, F. Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262-1278 (2014).
7. Doudna, J. A., Charpentier, E. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346, 1258096 (2014).
8. Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 (2012).
9. Kass, E. M., Jasin, M. Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett. 584, 3703-3708 (2010).
10. Porteus, M. H. Towards a new era in medicine: therapeutic genome editing. Genome Biol. 16, 286 (2015).
11. Woods, N. B., Bottero, V., Schmidt, M., von Kalle, C., Verma, I. M. Gene therapy: therapeutic gene causing lymphoma. Nature 440, 1123 (2006).
12. Hubbard, N. et al. Targeted gene editing restores regulated CD40L expression and function in X-HIGM T cells. Blood 127, 2513-2522 (2016).
13. Voit, R. A., Hendel, A., Pruett-Miller, S. M., Porteus, M. H. Nuclease-mediated gene editing by homologous recombination of the human globin locus. Nucleic Acids Res. 42, 1365-1378 (2014).
14. Hendel, A. et al. Chemically modified guide RNAs enhance CRISPR-Cas genome editing in human primary cells. Nat. Biotechnol. 33, 985-989 (2015).
15. Baum, C. M., Weissman, I. L., Tsukamoto, A. S., Buckle, A. M., Peault, B. Isolation of a candidate human hematopoietic stem-cell population. Proc. Natl Acad. Sci. USA 89, 2804-2808 (1992).
16. Mukherjee, S., Thrasher, A. J. Gene therapy for PIDs: progress, pitfalls and prospects. Gene 525, 174-181 (2013).
17. Cavazzana-Calvo, M. et al. Transfusion independence and HMGA2 activation after gene therapy of human-thalassaemia. Nature 467, 318-322 (2010).
18. Naldini, L. Gene therapy returns to centre stage. Nature 526, 351-360 (2015).
19. Jenq, R. R., van den Brink, M. R. Allogeneic haematopoietic stem cell transplantation: individualized stem cell and immune therapy of cancer. Nat. Rev. Cancer 10, 213-221 (2010).
20. Hoban, M. D. et al. Correction of the sickle cell disease mutation in human hematopoietic stem/progenitor cells. Blood 125, 2597-2604 (2015).
21. Genovese, P. et al. Targeted genome editing in human repopulating haematopoietic stem cells. Nature 510, 235-240 (2014).
22. Wang, J. et al. Homology-driven genome editing in hematopoietic stem and progenitor cells using ZFN mRNA and AAV6 donors. Nat. Biotechnol. 33, 1256-1263 (2015).
23. De Ravin, S. S. et al. Targeted gene addition in human CD34+ hematopoietic cells for correction of X-linked chronic granulomatous disease. Nat. Biotechnol. 34, 424-429 (2016).
24. Sather, B. D. et al. Efficient modification of CCR5 in primary human hematopoietic cells using a megaTAL nuclease and AAV donor template. Sci. Transl. Med. 7, 307-156 (2015).
25. Wang, J. 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. 44, e30 (2016).
26. Miller, D. G., Petek, L. M., Russell, D. W. Adeno-associated virus vectors integrate at chromosome breakage sites. Nat. Genet. 36, 767-773 (2004).
27. Russell, D. W., Hirata, R. K. Human gene targeting by viral vectors. Nat. Genet. 18, 325-330 (1998).
28. Barzel, A. et al. Promoterless gene targeting without nucleases ameliorates haemophilia B in mice. Nature 517, 360-364 (2015).
29. Hoban, M. D., Orkin, S. H., Bauer, D. E. Genetic treatment of a molecular disorder: gene therapy approaches to sickle cell disease. Blood 127, 839-848 (2016).
30. Bonini, C. et al. HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versus-leukemia. Science 276, 1719-1724 (1997).
31. Ciceri, F. et al. Infusion of suicide-gene-engineered donor lymphocytes after family haploidentical haemopoietic stem-cell transplantation for leukaemia (the TK007 trial): a non-randomised phase I-II study. Lancet Oncol. 10, 489-500 (2009).
32. Oliveira, G. et al. Tracking genetically engineered lymphocytes long-term reveals the dynamics of T cell immunological memory. Sci. Transl. Med. 7, 317ra198 (2015).
33. Bonini, C. et al. Safety of retroviral gene marking with a truncated NGF receptor. Nat. Med. 9, 367-369 (2003).
34. Seita, J., Weissman, I. L. Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip. Rev. Syst. Biol. Med. 2, 640-653 (2010).
35. Majeti, R., Park, C. Y., Weissman, I. L. Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell 1, 635-645 (2007).
36. Doulatov, S., Notta, F., Laurenti, E., Dick, J. E. Hematopoiesis: a human perspective. Cell Stem Cell 10, 120-136 (2012).
37. Gu, A. et al. Engraftment and lineage potential of adult hematopoietic stem and progenitor cells is compromised following short-term culture in the presence of an aryl hydrocarbon receptor antagonist. Hum. Gene Ther. Methods 25, 221-231 (2014).
38. Levasseur, D. N. et al. A recombinant human hemoglobin with anti-sickling properties greater than fetal hemoglobin. J. Biol. Chem. 279, 27518-27524 (2004).
39. Dulmovits, B. M. et al. Pomalidomide reverses-globin silencing through the transcriptional reprogramming of adult hematopoietic progenitors. Blood 127, 1481-1492 (2016).
40. Hu, J. et al. Isolation and functional characterization of human erythroblasts at distinct stages: implications for understanding of normal and disordered erythropoiesis in vivo. Blood 121, 3246-3253 (2013).
41. Romero, Z. et al.-globin gene transfer to human bone marrow for sickle cell disease. J. Clin. Invest. 123, 3317-3330 (2013).
42. Fares, I. et al. Cord blood expansion. Pyrimidoindole derivatives are agonists of human hematopoietic stem cell self-renewal. Science 345, 1509-1512 (2014).
43. Khan, I. F., Hirata, R. K., Russell, D. W. AAV-mediated gene targeting methods for human cells. Nat. Protocols 6, 482-501 (2011).
44. Aurnhammer, C. et al. 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).
45. Hendel, A. et al. Quantifying genome-editing outcomes at endogenous loci with SMRT sequencing. Cell Reports 7, 293-305 (2014).
46. Cradick, T. J., Fine, E. J., Antico, C. J., Bao, G. CRISPR/Cas9 systems targeting-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res. 41, 9584-9592 (2013).
47. Brinkman, E. K., Chen, T., Amendola, M., van Steensel, B. Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res. 42, e168 (2014).
48. Boggs, D. R. The total marrow mass of the mouse: a simplified method of measurement. Am. J. Hematol. 16, 277-286 (1984).