• ISSN 1674-8301
  • CN 32-1810/R
Volume 35 Issue 2
Mar.  2021
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Article Contents
Papizan James B., Porter Shaina N., Sharma Akshay, Pruett-Miller Shondra M.. Therapeutic gene editing strategies using CRISPR-Cas9 for the β-hemoglobinopathies[J]. The Journal of Biomedical Research, 2021, 35(2): 115-134. doi: 10.7555/JBR.34.20200096
Citation: Papizan James B., Porter Shaina N., Sharma Akshay, Pruett-Miller Shondra M.. Therapeutic gene editing strategies using CRISPR-Cas9 for the β-hemoglobinopathies[J]. The Journal of Biomedical Research, 2021, 35(2): 115-134. doi: 10.7555/JBR.34.20200096

Therapeutic gene editing strategies using CRISPR-Cas9 for the β-hemoglobinopathies

doi: 10.7555/JBR.34.20200096
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  • Corresponding author: Shondra M. Pruett-Miller, Department of Cellular and Molecular Biology, St. Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA. Tel/Fax: +1-901-595-7313/+1-901-525-8025, E-mail: shondra.miller@stjude.org
  • Received: 2020-06-18
  • Revised: 2020-09-02
  • Accepted: 2020-09-16
  • Published: 2020-11-09
  • Issue Date: 2021-03-26
  • With advancements in gene editing technologies, our ability to make precise and efficient modifications to the genome is increasing at a remarkable rate, paving the way for scientists and clinicians to uniquely treat a multitude of previously irremediable diseases. CRISPR-Cas9, short for clustered regularly interspaced short palindromic repeats and CRISPR-associated protein 9, is a gene editing platform with the ability to alter the nucleotide sequence of the genome in living cells. This technology is increasing the number and pace at which new gene editing treatments for genetic disorders are moving toward the clinic. The β-hemoglobinopathies are a group of monogenic diseases, which despite their high prevalence and chronic debilitating nature, continue to have few therapeutic options available. In this review, we will discuss our existing comprehension of the genetics and current state of treatment for β-hemoglobinopathies, consider potential genome editing therapeutic strategies, and provide an overview of the current state of clinical trials using CRISPR-Cas9 gene editing.

     

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  • [1]
    Modell B, Darlison M. Global epidemiology of haemoglobin disorders and derived service indicators[J]. Bull World Health Organ, 2008, 86(6): 480–487. doi: 10.2471/blt.06.036673
    [2]
    Nagel RL, Fabry ME, Steinberg MH. The paradox of hemoglobin SC disease[J]. Blood Rev, 2003, 17(3): 167–178. doi: 10.1016/S0268-960X(03)00003-1
    [3]
    Orkin SH, Kazazian Jr HH, Antonarakis SE, et al. Abnormal RNA processing due to the exon mutation of βE-globin gene[J]. Nature, 1982, 300(5894): 768–769. doi: 10.1038/300768a0
    [4]
    Hannemann A, Weiss E, Rees DC, et al. The properties of red blood cells from patients heterozygous for HbS and HbC (HbSC genotype)[J]. Anemia, 2011, 2011: 248527. doi: 10.1155/2011/248527.Epub2010Oct13
    [5]
    Giardine B, Borg J, Viennas E, et al. Updates of the HbVar database of human hemoglobin variants and thalassemia mutations[J]. Nucleic Acids Res, 2014, 42(D1): D1063–D1069. doi: 10.1093/nar/gkt911
    [6]
    Paulukonis ST, Eckman JR, Snyder AB, et al. Defining sickle cell disease mortality using a population-based surveillance system, 2004 through 2008[J]. Public Health Rep, 2016, 131(2): 367–375. doi: 10.1177/003335491613100221
    [7]
    Hassell KL. Population estimates of sickle cell disease in the U.S[J]. Am J Prev Med, 2010, 38(4 Suppl): S512–S521. doi: 10.1016/j.amepre.2009.12.022
    [8]
    Platt OS, Brambilla DJ, Rosse WF, et al. Mortality in sickle cell disease. Life expectancy and risk factors for early death[J]. N Engl J Med, 1994, 330(23): 1639–1644. doi: 10.1056/NEJM199406093302303
    [9]
    Powars DR, Chan LS, Hiti A, et al. Outcome of sickle cell anemia: a 4-decade observational study of 1056 patients[J]. Medicine (Baltimore), 2005, 84(6): 363–376. doi: 10.1097/01.md.0000189089.45003.52
    [10]
    Hulbert ML, McKinstry RC, Lacey JL, et al. Silent cerebral infarcts occur despite regular blood transfusion therapy after first strokes in children with sickle cell disease[J]. Blood, 2011, 117(3): 772–779. doi: 10.1182/blood-2010-01-261123
    [11]
    Piel FB, Patil AP, Howes RE, et al. Global epidemiology of sickle haemoglobin in neonates: a contemporary geostatistical model-based map and population estimates[J]. Lancet, 2013, 381(9861): 142–151. doi: 10.1016/S0140-6736(12)61229-X
    [12]
    Grosse SD, Odame I, Atrash HK, et al. Sickle cell disease in Africa: a neglected cause of early childhood mortality[J]. Am J Prev Med, 2011, 41(6 Suppl 4): S398–S405. doi: 10.1016/j.amepre.2011.09.013
    [13]
    Kauf TL, Coates TD, Liu HZ, et al. The cost of health care for children and adults with sickle cell disease[J]. Am J Hematol, 2009, 84(6): 323–327. doi: 10.1002/ajh.21408
    [14]
    Vinjamur DS, Bauer DE, Orkin SH. Recent progress in understanding and manipulating haemoglobin switching for the haemoglobinopathies[J]. Br J Haematol, 2018, 180(5): 630–643. doi: 10.1111/bjh.15038
    [15]
    Basak A, Sankaran VG. Regulation of the fetal hemoglobin silencing factor BCL11A[J]. Ann N Y Acad Sci, 2016, 1368(1): 25–30. doi: 10.1111/nyas.13024
    [16]
    Stamatoyannopoulos G. Control of globin gene expression during development and erythroid differentiation[J]. Exp Hematol, 2005, 33(3): 259–271. doi: 10.1016/j.exphem.2004.11.007
    [17]
    Serjeant GR, Serjeant BE, Mason K. Heterocellular hereditary persistence of fetal haemoglobin and homozygous sickle-cell disease[J]. Lancet, 1977, 309(8015): 795–796. doi: 10.1016/s0140-6736(77)92976-2
    [18]
    Perrine RP, Brown MJ, Clegg JB, et al. Benign sickle-cell anaemia[J]. Lancet, 1972, 300(7788): 1163–1167. doi: 10.1016/S0140-6736(72)92592-5
    [19]
    Nuinoon M, Makarasara W, Mushiroda T, et al. A genome-wide association identified the common genetic variants influence disease severity in β0-thalassemia/hemoglobin E[J]. Hum Genet, 2010, 127(3): 303–314. doi: 10.1007/s00439-009-0770-2
    [20]
    Galanello R, Sanna S, Perseu L, et al. Amelioration of Sardinianβ0 thalassemia by genetic modifiers[J]. Blood, 2009, 114(18): 3935–3937. doi: 10.1182/blood-2009-04-217901
    [21]
    Forget BG. Molecular basis of hereditary persistence of fetal hemoglobin[J]. Ann N Y Acad Sci, 1998, 850(1): 38–44. doi: 10.1111/j.1749-6632.1998.tb10460.x
    [22]
    Fessas P, Stamatoyannopoulos G. Hereditary persistence of fetal hemoglobin in Greece. A study and a Comparison[J]. Blood, 1964, 24(3): 223–240. doi: 10.1182/blood.V24.3.223.223
    [23]
    Weatherall DJ. Phenotype—genotype relationships in monogenic disease: lessons from the thalassaemias[J]. Nat Rev Genet, 2001, 2(4): 245–255. doi: 10.1038/35066048
    [24]
    Amato A, Cappabianca MP, Perri M, et al. Interpreting elevated fetal hemoglobin in pathology and health at the basic laboratory level: new and known γ- gene mutations associated with hereditary persistence of fetal hemoglobin[J]. Int J Lab Hematol, 2014, 36(1): 13–19. doi: 10.1111/ijlh.12094
    [25]
    Uda M, Galanello, R, Sanna S, et al. Genome-wide association study shows BCL11A associated with persistent fetal hemoglobin and amelioration of the phenotype of β-thalassemia[J]. Proc Natl Acad Sci U S A, 2008, 105(5): 1620–1625. doi: 10.1073/pnas.0711566105
    [26]
    Lettre G, Sankaran VG, Bezerra MAC, et al. DNA polymorphisms at the BCL11A, HBS1L-MYB, and β-globin loci associate with fetal hemoglobin levels and pain crises in sickle cell disease[J]. Proc Natl Acad Sci U S A, 2008, 105(33): 11869–11874. doi: 10.1073/pnas.0804799105
    [27]
    Menzel S, Garner C, Gut I, et al. A QTL influencing F cell production maps to a gene encoding a zinc-finger protein on chromosome 2p15[J]. Nat Genet, 2007, 39(10): 1197–1199. doi: 10.1038/ng2108
    [28]
    Thein SL, Menzel S, Peng X, et al. Intergenic variants of HBS1L-MYB are responsible for a major quantitative trait locus on chromosome 6q23 influencing fetal hemoglobin levels in adults[J]. Proc Natl Acad Sci U S A, 2007, 104(27): 11346–11351. doi: 10.1073/pnas.0611393104
    [29]
    Sankaran VG, Menne TF, Xu J, et al. Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A[J]. Science, 2008, 322(5909): 1839–1842. doi: 10.1126/science.1165409
    [30]
    Sankaran VG, Xu J, Ragoczy T, et al. Developmental and species-divergent globin switching are driven by BCL11A[J]. Nature, 2009, 460(7259): 1093–1097. doi: 10.1038/nature08243
    [31]
    Xu J, Bauer DE, Kerenyi MA, et al. Corepressor-dependent silencing of fetal hemoglobin expression by BCL11A[J]. Proc Natl Acad Sci U S A, 2013, 110(16): 6518–6523. doi: 10.1073/pnas.1303976110
    [32]
    Xu J, Sankaran VG, Ni M, et al. Transcriptional silencing of γ-globin by BCL11A involves long-range interactions and cooperation with SOX6[J]. Genes Dev, 2010, 24(8): 783–798. doi: 10.1101/gad.1897310
    [33]
    Xu J, Peng C, Sankaran VG, et al. Correction of sickle cell disease in adult mice by interference with fetal hemoglobin silencing[J]. Science, 2011, 334(6058): 993–996. doi: 10.1126/science.1211053
    [34]
    Esteghamat F, Gillemans N, Bilic I., et al. Erythropoiesis and globin switching in compound Klf1::Bcl11a mutant mice[J]. Blood, 2013, 121(13): 2553–2562. doi: 10.1182/blood-2012-06-434530
    [35]
    Luc S, Huang JL, McEldoon JL, et al. Bcl11a deficiency leads to hematopoietic stem cell defects with an aging-like phenotype[J]. Cell Rep, 2016, 16(12): 3181–3194. doi: 10.1016/j.celrep.2016.08.064
    [36]
    Ippolito GC, Dekker JD, Wang YH, et al. Dendritic cell fate is determined by BCL11A[J]. Proc Natl Acad Sci U S A, 2014, 111(11): E998–E1006. doi: 10.1073/pnas.1319228111
    [37]
    Liu PT, Keller JR, Ortiz M, et al. Bcl11a is essential for normal lymphoid development[J]. Nat Immunol, 2003, 4(6): 525–532. doi: 10.1038/ni925
    [38]
    Tsang JCH, Yu Y, Burke S, et al. Single-cell transcriptomic reconstruction reveals cell cycle and multi-lineage differentiation defects in Bcl11a-deficient hematopoietic stem cells[J]. Genome Biol, 2015, 16: 178. doi: 10.1186/s13059-015-0739-5
    [39]
    Greig LC, Woodworth MB, Greppi C, et al. Ctip1 controls acquisition of sensory area identity and establishment of sensory input fields in the developing neocortex[J]. Neuron, 2016, 90(2): 261–277. doi: 10.1016/j.neuron.2016.03.008
    [40]
    Basak A, Hancarova M, Ulirsch JC, et al. BCL11A deletions result in fetal hemoglobin persistence and neurodevelopmental alterations[J]. J Clin Invest, 2015, 125(6): 2363–2368. doi: 10.1172/JCI81163
    [41]
    Dias C, Estruch SB, Graham SA, et al. BCL11A haploinsufficiency causes an intellectual disability syndrome and dysregulates transcription[J]. Am J Hum Genet, 2016, 99(2): 253–274. doi: 10.1016/j.ajhg.2016.05.030
    [42]
    Funnell APW, Prontera P, Ottaviani V, et al. 2p15-p16.1 microdeletions encompassing and proximal to BCL11A are associated with elevated HbF in addition to neurologic impairment[J]. Blood, 2015, 126(1): 89–93. doi: 10.1182/blood-2015-04-638528
    [43]
    Bauer DE, Kamran SC, Lessard S, et al. An erythroid enhancer of BCL11A subject to genetic variation determines fetal hemoglobin level[J]. Science, 2013, 342(6155): 253–257. doi: 10.1126/science.1242088
    [44]
    Grosveld F, Van Assendelft GB, Greaves DR, et al. Position-independent, high-level expression of the human β-globin gene in transgenic mice[J]. Cell, 1987, 51(6): 975–985. doi: 10.1016/0092-8674(87)90584-8
    [45]
    Tuan D, Solomon W, Li Q, et al. The "beta-like-globin" gene domain in human erythroid cells[J]. Proc Natl Acad Sci U S A, 1985, 82(19): 6384–6388. doi: 10.1073/pnas.82.19.6384
    [46]
    Sankaran VG, Xu J, Byron R, et al. A functional element necessary for fetal hemoglobin silencing[J]. N Engl J Med, 2011, 365(9): 807–814. doi: 10.1056/NEJMoa1103070
    [47]
    Liu N, Hargreaves VV, Zhu Q, et al. Direct promoter repression by BCL11A controls the fetal to adult hemoglobin switch[J]. Cell, 2018, 173(2): 430–442. doi: 10.1016/j.cell.2018.03.016
    [48]
    Collins FS, Metherall JE, Yamakawa M, et al. A point mutation in the Aγ-globin gene promoter in Greek hereditary persistence of fetal haemoglobin[J]. Nature, 1985, 313(6000): 325–326. doi: 10.1038/313325a0
    [49]
    Gilman JG, Mishima N, Wen XJ, et al. Distal CCAAT box deletion in the Aγ globin gene of two black adolescents with elevated fetal Aγ globin[J]. Nucleic Acids Res, 1988, 16(22): 10635–10642. doi: 10.1093/nar/16.22.10635
    [50]
    Letvin NL, Linch DC, Beardsley GP, et al. Augmentation of fetal-hemoglobin production in anemic monkeys by hydroxyurea[J]. N Engl J Med, 1984, 310(14): 869–873. doi: 10.1056/NEJM198404053101401
    [51]
    Platt OS, Orkin SH, Dover G, et al. Hydroxyurea enhances fetal hemoglobin production in sickle cell anemia[J]. J Clin Invest, 1984, 74(2): 652–656. doi: 10.1172/JCI111464
    [52]
    Pule GD, Mowla S, Novitzky N, et al. A systematic review of known mechanisms of hydroxyurea-induced fetal hemoglobin for treatment of sickle cell disease[J]. Expert Rev Hematol, 2015, 8(5): 669–679. doi: 10.1586/17474086.2015.1078235
    [53]
    Yawn BP, Buchanan GR, Afenyi-Annan AN, et al. Management of sickle cell disease: summary of the 2014 evidence-based report by expert panel members[J]. JAMA, 2014, 312(10): 1033–1048. doi: 10.1001/jama.2014.10517
    [54]
    Brandow AM, Jirovec DL, Panepinto JA. Hydroxyurea in children with sickle cell disease: practice patterns and barriers to utilization[J]. Am J Hematol, 2010, 85(8): 611–613. doi: 10.1002/ajh.21749
    [55]
    Brandow AM, Panepinto JA. Hydroxyurea use in sickle cell disease: the battle with low prescription rates, poor patient compliance and fears of toxicities[J]. Expert Rev Hematol, 2010, 3(3): 255–260. doi: 10.1586/ehm.10.22
    [56]
    Niihara Y, Miller ST, Kanter J, et al. A phase 3 trial of L-glutamine in sickle cell disease[J]. N Engl J Med, 2018, 379(3): 226–235. doi: 10.1056/NEJMoa1715971
    [57]
    Li SD, Su YD, Li M, et al. Hemin-mediated hemolysis in erythrocytes: effects of ascorbic acid and glutathione[J]. Acta Biochim Biophys Sin (Shanghai), 2006, 38(1): 63–69. doi: 10.1111/j.1745-7270.2006.00127.x
    [58]
    Kato GJ, Steinberg MH, Gladwin MT. Intravascular hemolysis and the pathophysiology of sickle cell disease[J]. J Clin Invest, 2017, 127(3): 750–760. doi: 10.1172/JCI89741
    [59]
    Jones DP. Redox potential of GSH/GSSG couple: assay and biological significance[J]. Methods Enzymol, 2002, 348: 93–112. doi: 10.1016/S0076-6879(02)48630-2
    [60]
    Townsend DM, Tew KD, Tapiero H. The importance of glutathione in human disease[J]. Biomed Pharmacother, 2003, 57(3-4): 145–155. doi: 10.1016/S0753-3322(03)00043-X
    [61]
    Matsui NM, Borsig L, Rosen SD, et al. P-selectin mediates the adhesion of sickle erythrocytes to the endothelium[J]. Blood, 2001, 98(6): 1955–1962. doi: 10.1182/blood.V98.6.1955
    [62]
    Matsui NM, Varki A, Embury SH. Heparin inhibits the flow adhesion of sickle red blood cells to P-selectin[J]. Blood, 2002, 100(10): 3790–3796. doi: 10.1182/blood-2002-02-0626
    [63]
    Embury SH, Matsui NM, Ramanujam S, et al. The contribution of endothelial cell P-selectin to the microvascular flow of mouse sickle erythrocytes in vivo[J]. Blood, 2004, 104(10): 3378–3385. doi: 10.1182/blood-2004-02-0713
    [64]
    Polanowska-Grabowska R, Wallace K, Field JJ, et al. P-selectin-mediated platelet-neutrophil aggregate formation activates neutrophils in mouse and human sickle cell disease[J]. Arterioscler Thromb Vasc Biol, 2010, 30(12): 2392–2399. doi: 10.1161/ATVBAHA.110.211615
    [65]
    Ataga KI, Kutlar A, Kanter J, et al. Crizanlizumab for the Prevention of Pain Crises in Sickle Cell Disease[J]. N Engl J Med, 2017, 376(5): 429–439. doi: 10.1056/NEJMoa1611770
    [66]
    Metcalf B, Chuang C, Dufu K, et al. Discovery of GBT440, an orally bioavailable R-state stabilizer of sickle cell hemoglobin[J]. ACS Med Chem Lett, 2017, 8(3): 321–326. doi: 10.1021/acsmedchemlett.6b00491
    [67]
    Oksenberg D, Dufu K, Patel MP, et al. GBT440 increases haemoglobin oxygen affinity, reduces sickling and prolongs RBC half-life in a murine model of sickle cell disease[J]. Br J Haematol, 2016, 175(1): 141–153. doi: 10.1111/bjh.14214
    [68]
    Vichinsky E, Hoppe CC, Ataga KI, et al. A phase 3 randomized trial of voxelotor in sickle cell disease[J]. N Engl J Med, 2019, 381(6): 509–519. doi: 10.1056/NEJMoa1903212
    [69]
    Platt OS. Preventing stroke in sickle cell anemia[J]. N Engl J Med, 2005, 353(26): 2743–2745. doi: 10.1056/NEJMp058274
    [70]
    Adams RJ, McKie VC, Hsu L, et al. Prevention of a first stroke by transfusions in children with sickle cell anemia and abnormal results on transcranial Doppler ultrasonography[J]. N Engl J Med, 1998, 339(1): 5–11. doi: 10.1056/NEJM199807023390102
    [71]
    The Optimizing Primary Stroke Prevention in Sickle Cell Anemia (STOP 2) Trial Investigators. Discontinuing prophylactic transfusions used to prevent stroke in sickle cell disease[J]. N Engl J Med, 2005, 353(26): 2769–2778. doi: 10.1056/NEJMoa050460
    [72]
    Gladwin MT, Sachdev V, Jison ML, et al. Pulmonary hypertension as a risk factor for death in patients with sickle cell disease[J]. N Engl J Med, 2004, 350(9): 886–895. doi: 10.1056/NEJMoa035477
    [73]
    Chou ST. Transfusion therapy for sickle cell disease: a balancing act[J]. Hematol Am Soc Hematol Educ Program, 2013, 2013(1): 439–446. doi: 10.1182/asheducation-2013.1.439
    [74]
    Vichinsky E, Torres M, Minniti CP, et al. Efficacy and safety of deferasirox compared with deferoxamine in sickle cell disease: two-year results including pharmacokinetics and concomitant hydroxyurea[J]. Am J Hematol, 2013, 88(12): 1068–1073. doi: 10.1002/ajh.23569
    [75]
    Yazdanbakhsh K, Ware RE, Noizat-Pirenne F. Red blood cell alloimmunization in sickle cell disease: pathophysiology, risk factors, and transfusion management[J]. Blood, 2012, 120(3): 528–537. doi: 10.1182/blood-2011-11-327361
    [76]
    Chakravorty S, Williams TN. Sickle cell disease: a neglected chronic disease of increasing global health importance[J]. Arch Dis Child, 2015, 100(1): 48–53. doi: 10.1136/archdischild-2013-303773
    [77]
    Kassim AA, Sharma D. Hematopoietic stem cell transplantation for sickle cell disease: The changing landscape[J]. Hematol Oncol Stem Cell Ther, 2017, 10(4): 259–266. doi: 10.1016/j.hemonc.2017.05.008
    [78]
    ClinicalTrials.gov. Gene transfer for patients with sickle cell disease[EB/OL]. [2019-05-02]. https://clinicaltrials.gov/ct2/show/NCT02186418.
    [79]
    ClinicalTrials.gov. Stem cell gene therapy for sickle cell disease[EB/OL]. [2019-10-18].https://clinicaltrials.gov/ct2/show/NCT02247843?cond=NCT02247843&draw=2&rank=1.
    [80]
    Negre O, Bartholomae C, Beuzard Y, et al. Preclinical evaluation of efficacy and safety of an improved lentiviral vector for the treatment of β-thalassemia and sickle cell disease[J]. Curr Gene Ther, 2015, 15(1): 64–81. doi: 10.2174/1566523214666141127095336
    [81]
    Ribeil JA, Hacein-Bey-Abina S, Payen E, et al. Gene therapy in a patient with sickle cell disease[J]. N Engl J Med, 2017, 376(9): 848–855. doi: 10.1056/NEJMoa1609677
    [82]
    Negre O, Eggimann AV, Beuzard Y, et al. Gene therapy of the β-hemoglobinopathies by lentiviral transfer of the βA(T87Q)-Globin gene[J]. Hum Gene Ther, 2016, 27(2): 148–165. doi: 10.1089/hum.2016.007
    [83]
    Thompson AA, Walters MC, Kwiatkowski J, et al. Gene therapy in patients with transfusion-dependent β-thalassemia[J]. N Engl J Med, 2018, 378(16): 1479–1493. doi: 10.1056/NEJMoa1705342
    [84]
    European Medicines Agency. Zynteglo[EB/OL].[2019-05-29]. https://www.ema.europa.eu/en/medicines/human/EPAR/zynteglo.
    [85]
    Eadie GS, Brown Jr IW, Curtis WG. The potential life span and ultimate survival of fresh red blood cells in normal healthy recipients as studied by simultaneous Cr51 tagging and differential hemolysis[J]. J Clin Invest, 1955, 34(4): 629–636. doi: 10.1172/JCI103112
    [86]
    Cline MJ, Berlin NI. Red blood cell life span using DFP32 as a cohort label[J]. Blood, 1962, 19(6): 715–723. doi: 10.1182/blood.V19.6.715.715
    [87]
    Shemin D, Rittenberg D. The life span of the human red blood cell[J]. J Biol Chem, 1946, 166(2): 627–636. https://www.sciencedirect.com/science/article/pii/S0021925817352018?via%3Dihub
    [88]
    Huang XS, Wang Y, Yan W, et al. Production of gene-corrected adult beta globin protein in human erythrocytes differentiated from patient iPSCs after genome editing of the sickle point mutation[J]. Stem Cells, 2015, 33(5): 1470–1479. doi: 10.1002/stem.1969
    [89]
    Park S, Gianotti-Sommer A, Molina-Estevez FJ, et al. A comprehensive, ethnically diverse library of sickle cell disease-specific induced pluripotent stem cells[J]. Stem Cell Rep, 2017, 8(4): 1076–1085. doi: 10.1016/j.stemcr.2016.12.017
    [90]
    Li C, Ding L, Sun CW, et al. Novel HDAd/EBV reprogramming vector and highly efficient Ad/CRISPR-Cas sickle cell disease gene correction[J]. Sci Rep, 2016, 6: 30422. doi: 10.1038/srep30422
    [91]
    Martin RM, Ikeda K, Cromer MK, et al. Highly efficient and marker-free genome editing of human pluripotent stem cells by CRISPR-Cas9 RNP and AAV6 donor-mediated homologous recombination[J]. Cell Stem Cell, 2019, 24(5): 821–828. doi: 10.1016/j.stem.2019.04.001
    [92]
    DeWitt MA, Magis W, Bray NL, et al. Selection-free genome editing of the sickle mutation in human adult hematopoietic stem/progenitor cells[J]. Sci Transl Med, 2016, 8(360): 360ra134. doi: 10.1126/scitranslmed.aaf9336
    [93]
    Genovese P, Schiroli G, Escobar G, et al. Targeted genome editing in human repopulating haematopoietic stem cells[J]. Nature, 2014, 510(7504): 235–240. doi: 10.1038/nature13420
    [94]
    Walters MC, Patience M, Leisenring W, et al. Stable mixed hematopoietic chimerism after bone marrow transplantation for sickle cell anemia[J]. Biol Blood Marrow Transplant, 2001, 7(12): 665–673. doi: 10.1053/bbmt.2001.v7.pm11787529
    [95]
    Wu CJ, Gladwin M, Tisdale J, et al. Mixed haematopoietic chimerism for sickle cell disease prevents intravascular haemolysis[J]. Br J Haematol, 2007, 139(3): 504–507. doi: 10.1111/j.1365-2141.2007.06803.x
    [96]
    Iannone R, Casella JF, Fuchs EJ, et al. Results of minimally toxic nonmyeloablative transplantation in patients with sickle cell anemia and β-thalassemia[J]. Biol Blood Marrow Transplant, 2003, 9(8): 519–528. doi: 10.1016/S1083-8791(03)00192-7
    [97]
    Dever DP, Bak RO, Reinisch A, et al. CRISPR/Cas9 β-globin gene targeting in human haematopoietic stem cells[J]. Nature, 2016, 539(7629): 384–389. doi: 10.1038/nature20134
    [98]
    Eid A, Alshareef S, Mahfouz MM. CRISPR base editors: genome editing without double-stranded breaks[J]. Biochem J, 2018, 475(11): 1955–1964. doi: 10.1042/BCJ20170793
    [99]
    Anzalone AV, Randolph PB, Davis JR, et al. Search-and-replace genome editing without double-strand breaks or donor DNA[J]. Nature, 2019, 576(7785): 149–157. doi: 10.1038/s41586-019-1711-4
    [100]
    Rees HA, Liu DR. Base editing: precision chemistry on the genome and transcriptome of living cells[J]. Nat Rev Genet, 2018, 19(12): 770–788. doi: 10.1038/s41576-018-0059-1
    [101]
    Komor AC, Kim YB, Packer MS, et al. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage[J]. Nature, 2016, 533(7603): 420–424. doi: 10.1038/nature17946
    [102]
    Shimatani Z, Kashojiya S, Takayama M, et al. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion[J]. Nat Biotechnol, 2017, 35(5): 441–443. doi: 10.1038/nbt.3833
    [103]
    Gaudelli NM, Komor AC, Rees HA, et al. Programmable base editing of A·T to G·C in genomic DNA without DNA cleavage[J]. Nature, 2017, 551(7681): 464–471. doi: 10.1038/nature24644
    [104]
    Molla KA, Yang YN. CRISPR/Cas-mediated base editing: technical considerations and practical applications[J]. Trends Biotechnol, 2019, 37(10): 1121–1142. doi: 10.1016/j.tibtech.2019.03.008
    [105]
    Blackwell RQ, Oemijati S, Pribadi W, et al. Hemoglobin G makassar: β6 Glu→Ala[J]. Biochim Biophys Acta (BBA) - Protein Struct, 1970, 214(3): 396–401. doi: 10.1016/0005-2795(70)90297-7
    [106]
    Viprakasit V, Wiriyasateinkul A, Sattayasevana B, et al. Hb G-makassar[β6(A3)Glu→Ala; CODON 6 (G A G→G C G)]: molecular characterization, clinical, and hematological effects[J]. Hemoglobin, 2002, 26(3): 245–253. doi: 10.1081/HEM-120015028
    [107]
    Fucharoen S, Weatherall DJ. The hemoglobin E thalassemias[J]. Cold Spring Harb Perspect Med, 2012, 2(8): a011734. doi: 10.1101/cshperspect.a011734
    [108]
    Jacob GF, Raper AB. Hereditary persistence of foetal haemoglobin production, and its interaction with the sickle-cell trait[J]. Br J Haematol, 1958, 4(2): 138–149. doi: 10.1111/j.1365-2141.1958.tb03844.x
    [109]
    Lettre G, Bauer DE. Fetal haemoglobin in sickle-cell disease: from genetic epidemiology to new therapeutic strategies[J]. Lancet, 2016, 387(10037): 2554–2564. doi: 10.1016/S0140-6736(15)01341-0
    [110]
    Borg J, Papadopoulos P, Georgitsi M, et al. Haploinsufficiency for the erythroid transcription factor KLF1 causes hereditary persistence of fetal hemoglobin[J]. Nat Genet, 2010, 42(9): 801–805. doi: 10.1038/ng.630
    [111]
    Ye L, Wang JM, Tan YT, et al. Genome editing using CRISPR-Cas9 to create the HPFH genotype in HSPCs: an approach for treating sickle cell disease and β-thalassemia[J]. Proc Natl Acad Sci U S A, 2016, 113(38): 10661–10665. doi: 10.1073/pnas.1612075113
    [112]
    Martyn GE, Wienert B, Yang L, et al. Natural regulatory mutations elevate the fetal globin gene via disruption of BCL11A or ZBTB7A binding[J]. Nat Genet, 2018, 50(4): 498–503. doi: 10.1038/s41588-018-0085-0
    [113]
    Métais JY, Doerfler PA, Mayuranathan T, et al. Genome editing of HBG1 and HBG2 to induce fetal hemoglobin[J]. Blood Adv, 2019, 3(21): 3379–3392. doi: 10.1182/bloodadvances.2019000820
    [114]
    Traxler EA, Yao Y, Wang YD, et al. A genome-editing strategy to treat β-hemoglobinopathies that recapitulates a mutation associated with a benign genetic condition[J]. Nat Med, 2016, 22(9): 987–990. doi: 10.1038/nm.4170
    [115]
    Antoniani C, Meneghini V, Lattanzi A, et al. Induction of fetal hemoglobin synthesis by CRISPR/Cas9-mediated editing of the human β-globin locus[J]. Blood, 2018, 131(17): 1960–1973. doi: 10.1182/blood-2017-10-811505
    [116]
    Wienert B, Funnell APW, Norton LJ, et al. Editing the genome to introduce a beneficial naturally occurring mutation associated with increased fetal globin[J]. Nat Commun, 2015, 6: 7085. doi: 10.1038/ncomms8085
    [117]
    Martyn GE, Wienert B, Kurita R, et al. A natural regulatory mutation in the proximal promoter elevates fetal globin expression by creating a de novo GATA1 site[J]. Blood, 2019, 133(8): 852–856. doi: 10.1182/blood-2018-07-863951
    [118]
    Tsai SQ, Nguyen NT, Malagon-Lopez J, et al. CIRCLE-seq: a highly sensitive in vitro screen for genome-wide CRISPR-Cas9 nuclease off-targets[J]. Nat Methods, 2017, 14(6): 607–614. doi: 10.1038/nmeth.4278
    [119]
    Masuda T, Wang X, Maeda M, et al. Transcription factors LRF and BCL11A independently repress expression of fetal hemoglobin[J]. Science, 2016, 351(6270): 285–289. doi: 10.1126/science.aad3312
    [120]
    Rochette J, Craig JE, Thein SL. Fetal hemoglobin levels in adults[J]. Blood Rev, 1994, 8(4): 213–224. doi: 10.1016/0268-960X(94)90109-0
    [121]
    Hu JH, Miller SM, Geurts MH, et al. Evolved Cas9 variants with broad PAM compatibility and high DNA specificity[J]. Nature, 2018, 556(7699): 57–63. doi: 10.1038/nature26155
    [122]
    Nishimasu H, Shi X, Ishiguro S, et al. Engineered CRISPR-Cas9 nuclease with expanded targeting space[J]. Science, 2018, 361(6408): 1259–1262. doi: 10.1126/science.aas9129
    [123]
    Martin DI, Tsai SF, Orkin SH. Increased γ-globin expression in a nondeletion HPFH mediated by an erythroid-specific DNA-binding factor[J]. Nature, 1989, 338(6214): 435–438. doi: 10.1038/338435a0
    [124]
    Weatherall DJ, Cartner R, Clegg JB, et al. A form of hereditary persistence of fetal haemoglobin characterized by uneven cellular distribution of haemoglobin F and the production of haemoglobins A and A2 in homozygotes[J]. Br J Haematol, 1975, 29(2): 205–220. doi: 10.1111/j.1365-2141.1975.tb01815.x
    [125]
    Wood WG, MacRae IA, Darbre PD, et al. The British type of non-deletion HPFH: characterization of developmental changes in vivo and erythroid growth in vitro[J]. Br J Haematol, 1982, 50(3): 401–414. doi: 10.1111/j.1365-2141.1982.tb01935.x
    [126]
    Wienert B, Martyn GE, Kurita R, et al. KLF1 drives the expression of fetal hemoglobin in British HPFH[J]. Blood, 2017, 130(6): 803–807. doi: 10.1182/blood-2017-02-767400
    [127]
    Zeng J, Wu YX, Ren CY, et al. Therapeutic base editing of human hematopoietic stem cells[J]. Nat Med, 2020, 26(4): 535–541. doi: 10.1038/s41591-020-0790-y
    [128]
    Richter MF, Zhao KT, Eton E, et al. Phage-assisted evolution of an adenine base editor with improved Cas domain compatibility and activity[J]. Nat Biotechnol, 2020, 38(7): 883–891. doi: 10.1038/s41587-020-0453-z
    [129]
    Hendel A, Bak RO, Clark JT, et al. Chemically modified guide RNAs enhance CRISPR-Cas genome editing in human primary cells[J]. Nat Biotechnol, 2015, 33(9): 985–989. doi: 10.1038/nbt.3290
    [130]
    DiGiusto DL, Cannon PM, Holmes MC, et al. Preclinical development and qualification of ZFN-mediated CCR5 disruption in human hematopoietic stem/progenitor cells[J]. Mol Ther Methods Clin Dev, 2016, 3: 16067. doi: 10.1038/mtm.2016.67
    [131]
    Cromer MK, Vaidyanathan S, Ryan DE, et al. Global transcriptional response to CRISPR/Cas9-AAV6-based genome editing in CD34+ hematopoietic stem and progenitor cells[J]. Mol Ther, 2018, 26(10): 2431–2442. doi: 10.1016/j.ymthe.2018.06.002
    [132]
    Pattanayak V, Lin S, Guilinger JP, et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity[J]. Nat Biotechnol, 2013, 31(9): 839–843. doi: 10.1038/nbt.2673
    [133]
    Ihry RJ, Worringer KA, Salick MR, et al. p53 inhibits CRISPR-Cas9 engineering in human pluripotent stem cells[J]. Nat Med, 2018, 24(7): 939–946. doi: 10.1038/s41591-018-0050-6
    [134]
    Wang JB, Exline CM, DeClercq JJ, et al. Homology-driven genome editing in hematopoietic stem and progenitor cells using ZFN mRNA and AAV6 donors[J]. Nat Biotechnol, 2015, 33(12): 1256–1263. doi: 10.1038/nbt.3408
    [135]
    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[J]. Sci Transl Med, 2015, 7(307): 307ra156. doi: 10.1126/scitranslmed.aac5530
    [136]
    De Ravin SS, Reik A, Liu PQ, et al. Targeted gene addition in human CD34+ hematopoietic cells for correction of X-linked chronic granulomatous disease[J]. Nat Biotechnol, 2016, 34(4): 424–429. doi: 10.1038/nbt.3513
    [137]
    Bak RO, Dever DP, Porteus MH. CRISPR/Cas9 genome editing in human hematopoietic stem cells[J]. Nat Protoc, 2018, 13(2): 358–376. doi: 10.1038/nprot.2017.143
    [138]
    Hoban MD, Orkin SH, Bauer DE. Genetic treatment of a molecular disorder: gene therapy approaches to sickle cell disease[J]. Blood, 2016, 127(7): 839–848. doi: 10.1182/blood-2015-09-618587
    [139]
    David RM, Doherty AT. Viral vectors: the road to reducing genotoxicity[J]. Toxicol Sci, 2017, 155(2): 315–325. doi: 10.1093/toxsci/kfw220
    [140]
    Cavazzana-Calvo M, Payen E, Negre O, et al. Transfusion independence and HMGA2 activation after gene therapy of human β-thalassaemia[J]. Nature, 2010, 467(7313): 318–322. doi: 10.1038/nature09328
    [141]
    Zheng CX, Wang SM, Bai YH, et al. Lentiviral vectors and adeno-associated virus vectors: useful tools for gene transfer in pain research[J]. Anat Rec (Hoboken), 2018, 301(5): 825–836. doi: 10.1002/ar.23723
    [142]
    Moiani A, Paleari Y, Sartori D, et al. Lentiviral vector integration in the human genome induces alternative splicing and generates aberrant transcripts[J]. J Clin Invest, 2012, 122(5): 1653–1666. doi: 10.1172/JCI61852
    [143]
    Cromwell CR, Sung K, Park J, et al. Incorporation of bridged nucleic acids into CRISPR RNAs improves Cas9 endonuclease specificity[J]. Nat Commun, 2018, 9(1): 1448. doi: 10.1038/s41467-018-03927-0
    [144]
    Hoban MD, Lumaquin D, Kuo CY, et al. CRISPR/Cas9-mediated correction of the sickle mutation in human CD34+ cells[J]. Mol Ther, 2016, 24(9): 1561–1569. doi: 10.1038/mt.2016.148
    [145]
    Hoban MD, Cost GJ, Mendel MC, et al. Correction of the sickle cell disease mutation in human hematopoietic stem/progenitor cells[J]. Blood, 2015, 125(17): 2597–2604. doi: 10.1182/blood-2014-12-615948
    [146]
    Mandal PK, Ferreira LMR, Collins R, et al. Efficient ablation of genes in human hematopoietic stem and effector cells using CRISPR/Cas9[J]. Cell Stem Cell, 2014, 15(5): 643–652. doi: 10.1016/j.stem.2014.10.004
    [147]
    Canver MC, Orkin SH. Customizing the genome as therapy for the β-hemoglobinopathies[J]. Blood, 2016, 127(21): 2536–2545. doi: 10.1182/blood-2016-01-678128
    [148]
    Wu YX, Zeng J, Roscoe BP, et al. Highly efficient therapeutic gene editing of human hematopoietic stem cells[J]. Nat Med, 2019, 25(5): 776–783. doi: 10.1038/s41591-019-0401-y
    [149]
    Corbacioglu S, Cappellini MD, Chapin J, et al. Initial safety and efficacy results with a single dose of autologous CRISPR-Cas9-modified CD34+ hematopoietic stem and progenitor cells in transfusion-dependent β-thalassemia and sickle cell disease[C]//Proceedings of the 25th Congress of the European Hematology Association. Frankfurt, Germany: EHA, 2020.
    [150]
    Demirci S, Uchida N, Tisdale JF. Gene therapy for sickle cell disease: an update[J]. Cytotherapy, 2018, 20(7): 899–910. doi: 10.1016/j.jcyt.2018.04.003
    [151]
    Cavazzana M, Mavilio F. Gene therapy for hemoglobinopathies[J]. Hum Gene Ther, 2018, 29(10): 1106–1113. doi: 10.1089/hum.2018.122
    [152]
    Hirakawa MP, Krishnakumar R, Timlin JA, et al. Gene editing and CRISPR in the clinic: current and future perspectives[J]. Biosci Rep, 2020, 40(4): BSR20200127. doi: 10.1042/BSR20200127
    [153]
    Ikawa Y, Miccio A, Magrin E, et al. Gene therapy of hemoglobinopathies: progress and future challenges[J]. Hum Mol Genet, 2019, 28(R1): R24–R30. doi: 10.1093/hmg/ddz172
    [154]
    Magrin E, Miccio A, Cavazzana M. Lentiviral and genome-editing strategies for the treatment of β-hemoglobinopathies[J]. Blood, 2019, 134(15): 1203–1213. doi: 10.1182/blood.2019000949
    [155]
    Kim S, Kim D, Cho SW, et al. Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins[J]. Genome Res, 2014, 24(6): 1012–1019. doi: 10.1101/gr.171322.113
    [156]
    Dobosy JR, Rose SD, Beltz KR, et al. RNase H-dependent PCR (rhPCR): improved specificity and single nucleotide polymorphism detection using blocked cleavable primers[J]. BMC Biotechnol, 2011, 11: 80. doi: 10.1186/1472-6750-11-80
    [157]
    Porter SN, Levine RM, Pruett-Miller SM. A practical guide to genome editing using targeted nuclease technologies[J]. Compr Physiol, 2019, 9(2): 665–714. doi: 10.1002/cphy.c180022
    [158]
    Zischewski J, Fischer R, Bortesi L. Detection of on-target and off-target mutations generated by CRISPR/Cas9 and other sequence-specific nucleases[J]. Biotechnol Adv, 2017, 35(1): 95–104. doi: 10.1016/j.biotechadv.2016.12.003
    [159]
    Li JJ, Hong SY, Chen WJ, et al. Advances in detecting and reducing off-target effects generated by CRISPR-mediated genome editing[J]. J Genet Genomics, 2019, 46(11): 513–521. doi: 10.1016/j.jgg.2019.11.002
    [160]
    Cancellieri S, Canver MC, Bombieri N, et al. CRISPRitz: rapid, high-throughput and variant-aware in silico off-target site identification for CRISPR genome editing[J]. Bioinformatics, 2020, 36(7): 2001–2008. doi: 10.1093/bioinformatics/btz867
    [161]
    Bae S, Park J, Kim JS. Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases[J]. Bioinformatics, 2014, 30(10): 1473–1475. doi: 10.1093/bioinformatics/btu048
    [162]
    Haeussler M, Schönig K, Eckert H, et al. Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR[J]. Genome Biol, 2016, 17(1): 148. doi: 10.1186/s13059-016-1012-2
    [163]
    Hsu PD, Scott DA, Weinstein JA, et al. DNA targeting specificity of RNA-guided Cas9 nucleases[J]. Nat Biotechnol, 2013, 31(9): 827–832. doi: 10.1038/nbt.2647
    [164]
    Labun K, Montague TG, Gagnon JA, et al. CHOPCHOP v2: a web tool for the next generation of CRISPR genome engineering[J]. Nucleic Acids Res, 2016, 44(W1): W272–W276. doi: 10.1093/nar/gkw398
    [165]
    Listgarten J, Weinstein M, Kleinstiver BP, et al. Prediction of off-target activities for the end-to-end design of CRISPR guide RNAs[J]. Nat Biomed Eng, 2018, 2(1): 38–47. doi: 10.1038/s41551-017-0178-6
    [166]
    Moreno-Mateos MA, Vejnar CE, Beaudoin JD, et al. CRISPRscan: designing highly efficient sgRNAs for CRISPR-Cas9 targeting in vivo[J]. Nat Methods, 2015, 12(10): 982–988. doi: 10.1038/nmeth.3543
    [167]
    Lin JC, Wong KC. Off-target predictions in CRISPR-Cas9 gene editing using deep learning[J]. Bioinformatics, 2018, 34(17): I656–I663. doi: 10.1093/bioinformatics/bty554
    [168]
    Abadi S, Yan WX, Amar D, et al. A machine learning approach for predicting CRISPR-Cas9 cleavage efficiencies and patterns underlying its mechanism of action[J]. PLoS Comput Biol, 2017, 13(10): e1005807. doi: 10.1371/journal.pcbi.1005807
    [169]
    Doench JG, Fusi N, Sullender M, et al. Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9[J]. Nat Biotechnol, 2016, 34(2): 184–191. doi: 10.1038/nbt.3437
    [170]
    Doench JG, Hartenian E, Graham DB, et al. Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation[J]. Nat Biotechnol, 2014, 32(12): 1262–1267. doi: 10.1038/nbt.3026
    [171]
    Kim D, Bae S, Park J, et al. Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells[J]. Nat Methods, 2015, 12(3): 237–243. doi: 10.1038/nmeth.3284
    [172]
    Tsai SQ, Zheng ZL, Nguyen NT, et al. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases[J]. Nat Biotechnol, 2015, 33(2): 187–197. doi: 10.1038/nbt.3117
    [173]
    Crosetto N, Mitra A, Silva MJ, et al. Nucleotide-resolution DNA double-strand break mapping by next-generation sequencing[J]. Nat Methods, 2013, 10(4): 361–365. doi: 10.1038/nmeth.2408
    [174]
    Canela A, Sridharan S, Sciascia N, et al. DNA breaks and end resection measured genome-wide by end sequencing[J]. Mol Cell, 2016, 63(5): 898–911. doi: 10.1016/j.molcel.2016.06.034
    [175]
    Yan WX, Mirzazadeh R, Garnerone S, et al. BLISS is a versatile and quantitative method for genome-wide profiling of DNA double-strand breaks[J]. Nat Commun, 2017, 8: 15058. doi: 10.1038/ncomms15058
    [176]
    Giannoukos G, Ciulla DM, Marco E, et al. UDiTaSTM, a genome editing detection method for indels and genome rearrangements[J]. BMC Genomics, 2018, 19: 212. doi: 10.1186/s12864-018-4561-9
    [177]
    Wienert B, Wyman SK, Richardson CD, et al. Unbiased detection of CRISPR off-targets in vivo using DISCOVER-Seq[J]. Science, 2019, 364(6437): 286–289. doi: 10.1126/science.aav9023
    [178]
    Kim D, Kim DE, Lee G, et al. Genome-wide target specificity of CRISPR RNA-guided adenine base editors[J]. Nat Biotechnol, 2019, 37(4): 430–435. doi: 10.1038/s41587-019-0050-1
    [179]
    Zuo EW, Sun YD, Wei W, et al. Cytosine base editor generates substantial off-target single-nucleotide variants in mouse embryos[J]. Science, 2019, 364(6437): 289–292. doi: 10.1126/science.aav9973
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