CoChat
Sign Up
Cited by 50

The DOI matches its Crossref record; 31 of the 31 references it cites were found in a registry or an index.

CRISPR/Cas9 for Sickle Cell Disease: Applications, Future Possibilities, and Challenges

Demirci, Selami, Leonard, Alexis, Haro-Mora, Juan J., Uchida, Naoya, Tisdale, John F.·2019·Advances in Experimental Medicine and Biology
DOI 10.1007/5584_2018_331
Open this paper in CoChat — free account

Abstract

Sickle cell disease (SCD) is an inherited monogenic disorder resulting in serious mortality and morbidity worldwide. Although the disease was characterized more than a century ago, there are only two FDA approved medications to lessen disease severity, and a definitive cure available to all patients with SCD is lacking. Rapid and substantial progress in genome editing approaches have proven valuable as a curative option given plausibility to either correct the underlying mutation in patient-derived hematopoietic stem/progenitor cells (HSPCs), induce fetal hemoglobin expression to circumvent sickling of red blood cells (RBCs), or create corrected induced pluripotent stem cells (iPSCs) among other approaches. Recent discovery of CRISPR/Cas9 has not only revolutionized genome engineering but has also brought the possibility of translating these concepts into a clinically meaningful reality. Here we summarize genome engineering applications using CRISPR/Cas9, addressing challenges and future perspectives of CRISPR/Cas9 as a curative option for SCD.

Overview

Integrity signals

Registry

Crossref · 10.1007/5584_2018_331

Cites

31 of 31 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Research works printed but not linked: 73

  1. Anders C, Bargsten K, Jinek M (2016) Structural plasticity of PAM recognition by engineered variants of the RNA-guided endonuclease Cas9. Mol Cell 61(6):895–902 · DOI · Paper page
  2. Arnold SD, Brazauskas R, He N, Li Y, Aplenc R, Jin Z, Hall M, Atsuta Y, Dalal J, Hahn T (2017) Clinical risks and healthcare utilization of haematopoietic cell transplantation for sickle cell disease in the US using merged databases. Haematologica 102(11):1823–1832. https://doi.org/10.3324/haematol.2017.169581 · DOI
  3. Bak RO, Gomez-Ospina N, Porteus MH (2018) Gene editing on center stage. Trends Genet 34(8):600–611 · DOI
  4. Ballas SK (2009) The cost of health care for patients with sickle cell disease. Am J Hematol 84(6):320–322 · DOI
  5. Bhatia M, Kolva E, Cimini L, Jin Z, Satwani P, Savone M, George D, Garvin J, Paz ML, Briamonte C (2015) Health-related quality of life after allogeneic hematopoietic stem cell transplantation for sickle cell disease. Biol Blood Marrow Transplant 21(4):666–672 · DOI
  6. Chakrabarti S, Bareford D (2007) A survey on patient perception of reduced-intensity transplantation in adults with sickle cell disease. Bone Marrow Transplant 39(8):447–451 · DOI
  7. Chatterjee P, Jakimo N, Jacobson JM (2018) Minimal PAM specificity of a highly similarSpCas9 ortholog. Sci Adv 4:eaau0766 · DOI
  8. Chung JE, Magis W, Vu J, Heo S-J, Wartiovaara K, Walters MC, Kurita R, Nakamura Y, Boffelli D, Martin DI (2018) CRISPR-Cas9 interrogation of a putative fetal globin repressor in human erythroid cells. BioRxiv:335729. https://doi.org/10.1101/335729 · DOI
  9. Demirci S, Uchida N, Tisdale JF (2018) Gene therapy for sickle cell disease: an update. Cytotherapy 20(7):899–910 · DOI
  10. DeWitt MA, Magis W, Bray NL, Wang T, Berman JR, Urbinati F, Heo S-J, Mitros T, Muñoz DP, Boffelli D (2016) Selection-free genome editing of the sickle mutation in human adult hematopoietic stem/progenitor cells. Science Transl Med 8(360):360ra134–360ra134 · DOI · Paper page
  11. Esrick EB, Bauer DE (2018) Genetic therapies for sickle cell disease. Semin Hematol 55(8):76–86 · DOI
  12. Esrick EB, Brendel C, Manis JP, Armant MA, Negre H, Dansereau C, Ciuculescu MF, Patriarca S, Mackinnon B, Daley H (2018) Flipping the switch: initial results of genetic targeting of the fetal to adult globin switch in sickle cell patients. Blood 132:1023 · DOI
  13. Ferreira AF, Calin GA, Picanço-Castro V, Kashima S, Covas DT, de Castro FA (2018) Hematopoietic stem cells from induced pluripotent stem cells–considering the role of microRNA as a cell differentiation regulator. J Cell Sci 131(4):jcs203018 · DOI
  14. Fonfara I, Le Rhun A, Chylinski K, Makarova KS, Lecrivain A-L, Bzdrenga J, Koonin EV, Charpentier E (2013) Phylogeny of Cas9 determines functional exchangeability of dual-RNA and Cas9 among orthologous type II CRISPR-Cas systems. Nucleic Acids Res 42(4):2577–2590 · DOI · Paper page
  15. Forget BG (1998) Molecular basis of hereditary persistence of fetal hemoglobin. Ann N Y Acad Sci 850(1):38–44 · DOI
  16. Fujita A, Uchida N, Haro-Mora JJ, Winkler T, Tisdale J (2016) β-globin-expressing definitive erythroid progenitor cells generated from embryonic and induced pluripotent stem cell-derived sacs. Stem Cells 34(6):1541–1552 · DOI
  17. Gluckman E, Cappelli B, Bernaudin F, Labopin M, Volt F, Carreras J, Simões BP, Ferster A, Dupont S, De La Fuente J (2017) Sickle cell disease: an international survey of results of HLA-identical sibling hematopoietic stem cell transplantation. Blood 129(11):1548–1556 · DOI
  18. Grevet JD, Lan X, Hamagami N, Edwards CR, Sankaranarayanan L, Ji X, Bhardwaj SK, Face CJ, Posocco DF, Abdulmalik O (2018) Domain-focused CRISPR screen identifies HRI as a fetal hemoglobin regulator in human erythroid cells. Science 361(6399):285–290 · DOI
  19. Hendel A, Bak RO, Clark JT, Kennedy AB, Ryan DE, Roy S, Steinfeld I, Lunstad BD, Kaiser RJ, Wilkens AB (2015) Chemically modified guide RNAs enhance CRISPR-Cas genome editing in human primary cells. Nat Biotechnol 33(9):985–989. https://doi.org/10.1038/nbt.3290 · DOI · Paper page
  20. Hirano S, Nishimasu H, Ishitani R, Nureki O (2016) Structural basis for the altered PAM specificities of engineered CRISPR-Cas9. Mol Cell 61(6):886–894 · DOI · Paper page
  21. Hoban MD, Orkin SH, Bauer DE (2016b) Genetic treatment of a molecular disorder: gene therapy approaches to sickle cell disease. Blood 127(7):839–848 · DOI · Paper page
  22. Hsieh MM, Fitzhugh CD, Weitzel RP, Link ME, Coles WA, Zhao X, Rodgers GP, Powell JD, Tisdale JF (2014) Nonmyeloablative HLA-matched sibling allogeneic hematopoietic stem cell transplantation for severe sickle cell phenotype. JAMA 312(1):48–56 · DOI
  23. Huang X, Wang Y, Yan W, Smith C, Ye Z, Wang J, Gao Y, Mendelsohn L, Cheng L (2015) Production of gene-corrected adult beta globin protein in human erythrocytes differentiated from patient iPSCs after genome editing of the sickle point mutation. Stem Cells 33(5):1470–1479 · DOI
  24. Humbert O, Peterson CW, Norgaard ZK, Radtke S, Kiem H-P (2018) A nonhuman primate transplantation model to evaluate hematopoietic stem cell gene editing strategies for β-hemoglobinopathies. Mol Ther Methods Clin Dev 8:75–86 · DOI
  25. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science 337(6096):816–821. https://doi.org/10.1126/science.1225829 · DOI · Paper page
  26. Kim YB, Komor AC, Levy JM, Packer MS, Zhao KT, Liu DR (2017) Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nat Biotechnol 35(4):371–376 · DOI · Paper page
  27. Kim S, Koo T, Jee H-G, Cho H-Y, Lee G, Lim D-G, Shin HS, Kim J-S (2018) CRISPR RNAs trigger innate immune responses in human cells. Genome Res 28:367–373. https://doi.org/10.1101/gr.231936.117 · DOI · Paper page
  28. Kleinstiver BP, Prew MS, Tsai SQ, Nguyen NT, Topkar VV, Zheng Z, Joung JK (2015b) Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nat Biotechnol 33(12):1293–1298 · DOI · Paper page
  29. Kosicki M, Tomberg K, Bradley A (2018) Repair of double-strand breaks induced by CRISPR–Cas9 leads to large deletions and complex rearrangements. Nat Biotechnol 36(8):765–771 · DOI · Paper page
  30. Lan X, Khandros E, Grevet JD, Peslak SA, Bhardwaj S, Keller CA, Giardine B, Garcia BA, Hardison RC, Shi J (2018) Domain-focused CRISPR-Cas9 screen identifies the E3 ubiquitin ligase substrate adaptor protein SPOP as a novel repressor of fetal hemoglobin. Blood 132:414 · DOI
  31. Lanzkron S, Carroll CP, Haywood C Jr (2013) Mortality rates and age at death from sickle cell disease: US, 1979–2005. Public Health Rep 128(2):110–116 · DOI · Paper page
  32. Lee JK, Jeong E, Lee J, Jung M, Shin E, Kim Y-h, Lee K, Jung I, Kim D, Kim S (2018) Directed evolution of CRISPR-Cas9 to increase its specificity. Nat Commun 9(1):3048 · DOI · Paper page
  33. Leenay RT, Beisel CL (2017) Deciphering, communicating, and engineering the CRISPR PAM. J Mol Biol 429(2):177–191 · DOI
  34. Li Q, Peterson KR, Fang X, Stamatoyannopoulos G (2002) Locus control regions. Blood 100(9):3077–3086 · DOI · Paper page
  35. Li C, Ding L, Sun C-W, Wu L-C, Zhou D, Pawlik KM, Khodadadi-Jamayran A, Westin E, Goldman FD, Townes TM (2016) Novel HDAd/EBV reprogramming vector and highly efficient Ad/CRISPR-Cas sickle cell disease gene correction. Sci Rep 6:30422 · DOI · Paper page
  36. Li C, Psatha N, Sova P, Gil S, Wang H, Kim J, Kulkarni C, Valensisi C, Hawkins RD, Stamatoyannopoulos G (2018) Reactivation of γ-globin in adult β-YAC mice after ex vivo and in vivo hematopoietic stem cell genome editing. Blood 131:2915–2928. https://doi.org/10.1182/blood-2018-03-838540 · DOI
  37. Lobner K, Lanzkron S, Haywood C (2013) NIH and National Foundation Expenditures for sickle cell disease and cystic fibrosis are associated with Pubmed publications and FDA approvals. Blood 122:1739
  38. Lomova A, Clark DN, Campo-Fernandez B, Flores-Bjurström C, Kaufman ML, Fitz-Gibbon S, Wang X, Miyahira EY, Brown D, DeWitt MA (2018) Improving gene editing outcomes in human hematopoietic stem and progenitor cells by temporal control of DNA repair. Stem Cells:1–11. https://doi.org/10.1002/stem.2935 · DOI
  39. M Scharenberg A, Duchateau P, Smith J (2013) Genome engineering with TAL-effector nucleases and alternative modular nuclease technologies. Curr Gene Ther 13(4):291–303 · DOI
  40. Magis W, DeWitt MA, Wyman SK, Vu JT, Heo S-J, Shao SJ, Hennig F, Romero ZG, Campo-Fernandez B, McNeill M (2018) In vivo selection for corrected β-globin alleles after CRISPR/Cas9 editing in human sickle hematopoietic stem cells enhances therapeutic potential. BioRxiv:432716. https://doi.org/10.1101/432716 · DOI
  41. Martin R, Ikeda K, Uchida N, Cromer MK, Nishimura T, Dever DP, Camarena J, Bak R, Lausten A, Jakobsen MR (2018) Selection-free, high frequency genome editing by homologous recombination of human pluripotent stem cells using Cas9 RNP and AAV6. BioRxiv:252163. https://doi.org/10.1101/252163 · DOI
  42. Nihongaki Y, Kawano F, Nakajima T, Sato M (2015) Photoactivatable CRISPR-Cas9 for optogenetic genome editing. Nat Biotechnol 33(7):755–760 · DOI
  43. Paikari A, Sheehan VA (2018) Fetal haemoglobin induction in sickle cell disease. Br J Haematol 180(2):189–200 · DOI
  44. Park S, Gianotti-Sommer A, Molina-Estevez FJ, Vanuytsel K, Skvir N, Leung A, Rozelle SS, Shaikho EM, Weir I, Jiang Z (2017) A comprehensive, ethnically diverse library of sickle cell disease-specific induced Pluripotent stem cells. Stem Cell Rep 8(4):1076–1085 · DOI · Paper page
  45. Paulukonis ST, Eckman JR, Snyder AB, Hagar W, Feuchtbaum LB, Zhou M, Grant AM, Hulihan MM (2016) Defining sickle cell disease mortality using a population-based surveillance system, 2004 through 2008. Public Health Rep 131(2):367–375 · DOI
  46. Piel FB, Hay SI, Gupta S, Weatherall DJ, Williams TN (2013) Global burden of sickle cell anaemia in children under five, 2010–2050: modelling based on demographics, excess mortality, and interventions. PLoS Med 10(7):e1001484 · DOI
  47. Psatha N, Reik A, Phelps S, Zhou Y, Dalas D, Yannaki E, Levasseur DN, Urnov FD, Holmes MC, Papayannopoulou T (2018) Disruption of the BCL11A erythroid enhancer reactivates fetal hemoglobin in erythroid cells of patients with β-thalassemia major. Mol Ther Methods Clin Dev 10:313–326 · DOI
  48. Rahdar M, McMahon MA, Prakash TP, Swayze EE, Bennett CF, Cleveland DW (2015) Synthetic CRISPR RNA-Cas9–guided genome editing in human cells. Proc Natl Acad Sci 112(51):E7110–E7117 · DOI
  49. Ran FA, Hsu PD, Lin C-Y, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154(6):1380–1389 · DOI · Paper page
  50. Roy B, Zhao J, Yang C, Luo W, Xiong T, Li Y, Fang X, Gao G, Singh CO, Madsen L (2018) CRISPR/cascade 9-mediated genome editing-challenges and opportunities. Front Genet 9:240–252 · DOI
  51. Saenz C, Tisdale JF (2015) Assessing costs, benefits, and risks in chronic disease: taking the long view. Biol Blood Marrow Transplant 21(7):1149–1150 · DOI
  52. Shim G, Kim D, Park GT, Jin H, Suh S-K, Oh Y-K (2017) Therapeutic gene editing: delivery and regulatory perspectives. Acta Pharmacol Sin 38(6):738–753 · DOI
  53. Shin HY, Wang C, Lee HK, Yoo KH, Zeng X, Kuhns T, Yang CM, Mohr T, Liu C, Hennighausen L (2017) CRISPR/Cas9 targeting events cause complex deletions and insertions at 17 sites in the mouse genome. Nat Commun 8:15464 · DOI
  54. Simhadri VL, McGill J, McMahon S, Wang J, Jiang H, Sauna ZE (2018) Prevalence of pre-existing antibodies to CRISPR-associated nuclease Cas9 in the US population. Mol Ther Methods Clin Dev 10:105–112 · DOI · Paper page
  55. Smith LA, Oyeku SO, Homer C, Zuckerman B (2006) Sickle cell disease: a question of equity and quality. Pediatrics 117(5):1763–1770 · DOI
  56. Smith EC, Luc S, Croney DM, Woodworth MB, Greig LC, Fujiwara Y, Nguyen M, Sher F, Macklis JD, Bauer DE (2016) Strict in vivo specificity of the Bcl11a erythroid enhancer. Blood 128(19):2338–2342. https://doi.org/10.1182/blood-2016-08-736249 · DOI
  57. Stamatoyannopoulos G, Wood W, Papayannopoulou T, Nute P (1975) A new form of hereditary persistence of fetal hemoglobin in blacks and its association with sickle cell trait. Blood 46(5):683–692 · DOI
  58. Steinberg MH, Barton F, Castro O, Pegelow CH, Ballas SK, Kutlar A, Orringer E, Bellevue R, Olivieri N, Eckman J (2003) Effect of hydroxyurea on mortality and morbidity in adult sickle cell anemia: risks and benefits up to 9 years of treatment. JAMA 289(13):1645–1651 · DOI
  59. Stoddard BL (2011) Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification. Structure 19(1):7–15 · DOI
  60. Sugimura R, Jha DK, Han A, Soria-Valles C, da Rocha EL, Lu Y-F, Goettel JA, Serrao E, Rowe RG, Malleshaiah M (2017) Haematopoietic stem and progenitor cells from human pluripotent stem cells. Nature 545(7655):432–438 · DOI
  61. Tasan I, Jain S, Zhao H (2016) Use of genome-editing tools to treat sickle cell disease. Hum Genet 135(9):1011–1028 · DOI
  62. Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, Goodwin MJ, Aryee MJ, Joung JK (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol 32(6):569–576 · DOI · Paper page
  63. Tsang JC, Yu Y, Burke S, Buettner F, Wang C, Kolodziejczyk AA, Teichmann SA, Lu L, Liu P (2015) Single-cell transcriptomic reconstruction reveals cell cycle and multi-lineage differentiation defects in Bcl11a-deficient hematopoietic stem cells. Genome Biol 16(1):178 · DOI
  64. Uda M, Galanello R, Sanna S, Lettre G, Sankaran VG, Chen W, Usala G, Busonero F, Maschio A, Albai G (2008) Genome-wide association study shows BCL11A associated with persistent fetal hemoglobin and amelioration of the phenotype of β-thalassemia. Proc Natl Acad Sci 105(5):1620–1625 · DOI · Paper page
  65. Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD (2010) Genome editing with engineered zinc finger nucleases. Nat Rev Genet 11(9):636–646 · DOI · Paper page
  66. Walters MC, Patience M, Leisenring W, Eckman JR, Scott JP, Mentzer WC, Davies SC, Ohene-Frempong K, Bernaudin F, Matthews DC (1996) Bone marrow transplantation for sickle cell disease. N Engl J Med 335(6):369–376 · DOI
  67. Walters M, Patience M, Leisenring W, Rogers Z, Aquino V, Buchanan G, Roberts I, Yeager A, Hsu L, Adamkiewicz T (2001) Stable mixed hematopoietic chimerism after bone marrow transplantation for sickle cell anemia. Biol Blood Marrow Transplant 7(12):665–673 · DOI
  68. Wang X, Thein SL (2018) Switching from fetal to adult hemoglobin. Nat Genet 50(4):478–480 · DOI
  69. Ware RE (2010) How I use hydroxyurea to treat young patients with sickle cell anemia. Blood 115(26):5300–5311. https://doi.org/10.1182/blood-2009-Blood · DOI
  70. Watson J, Stahman AW, Bilello FP (1948) The significance of the paucity of sickle cells in newborn Negro infants. Obstet Gynecol Surv 3(6):819–820 · DOI
  71. Wen J, Tao W, Hao S, Zu Y (2017) Cellular function reinstitution of offspring red blood cells cloned from the sickle cell disease patient blood post CRISPR genome editing. J Hematol Oncol 10(1):119 · DOI
  72. Zetsche B, Volz SE, Zhang F (2015) A split-Cas9 architecture for inducible genome editing and transcription modulation. Nat Biotechnol 33(2):139–142 · DOI
  73. Zimmerman SA, Schultz WH, Burgett S, Mortier NA, Ware RE (2007) Hydroxyurea therapy lowers transcranial Doppler flow velocities in children with sickle cell anemia. Blood 110(3):1043–1047 · DOI

Cited by

Sorted by citations

See all 50

Metadata

Authors
Demirci, S., Leonard, A., Haro-Mora, J. J., Uchida, N., & Tisdale, J. F.
Venue
Advances in Experimental Medicine and Biology
Publisher
Springer International Publishing
Published
2019
Pages
37-52
ISSN
  • 0065-2598
  • 2214-8019
DOI
10.1007/5584_2018_331
Cited by
50
References
31
Language
en
Licence
www.springer.com/tdm (tdm)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review