Targeted Application of Human Genetic Variation Can Improve Red Blood Cell Production from Stem Cells

Cell Stem Cell

Volumn 18, Issue 1, 2016, Pages 73-78

  Giani, Felix C ^a,b,f   Fiorini, Claudia ^a,b   Wakabayashi, Aoi ^a,b   Ludwig, Leif S ^a,b,f,g   Salem, Rany M ^a,b   Jobaliya, Chintan D ^c   Regan, Stephanie N ^b,d   Ulirsch, Jacob C ^a,b   Liang, Ge ^c   Steinberg Shemer, Orna ^c   Guo, Michael H ^a,b   Esko, Tõnu ^a,b   Tong, Wei ^c   Brugnara, Carlo ^a   Hirschhorn, Joel N ^a,b   Weiss, Mitchell J ^e   Zon, Leonard I ^a,b,d   Chou, Stella T ^c   French, Deborah L ^c   Musunuru, Kiran ^b,d   Sankaran, Vijay G ^a,b   more..

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d Harvard University   (United States)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^g FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDES AND PROTEINS; SH2B3 PROTEIN; UNCLASSIFIED DRUG; CYTOKINE; HEMOGLOBIN;

ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; ERYTHROCYTE COUNT; ERYTHROID CELL; GENE INACTIVATION; GENETIC VARIABILITY; HEMATOPOIETIC STEM CELL; HUMAN; LOSS OF FUNCTION MUTATION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL EXPANSION; STEM CELL TRANSPLANTATION; CRISPR CAS SYSTEM; CYTOLOGY; EMBRYONIC STEM CELL; ERYTHROCYTE; FETUS BLOOD; GENETIC PROCEDURES; GENETIC VARIATION; HUMAN GENOME; METABOLISM; MUTATION; PROCEDURES; REGENERATIVE MEDICINE; STEM CELL;

CELL DIFFERENTIATION; CRISPR-CAS SYSTEMS; CYTOKINES; EMBRYONIC STEM CELLS; ERYTHROCYTES; FETAL BLOOD; GENETIC TECHNIQUES; GENETIC VARIATION; GENOME, HUMAN; HEMATOPOIETIC STEM CELLS; HEMOGLOBINS; HUMANS; MUTATION; PLURIPOTENT STEM CELLS; REGENERATIVE MEDICINE; STEM CELLS;

EID: 84954385240     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.09.015     Document Type: Article

References (35)

1. J.L. Abkowitz, K.M. Sabo, B. Nakamoto, C.A. Blau, F.H. Martin, K.M. Zsebo, and T. Papayannopoulou Diamond-blackfan anemia: in vitro response of erythroid progenitors to the ligand for c-kit Blood 78 1991 2198 2202
2. A. Bersenev, C. Wu, J. Balcerek, and W. Tong Lnk controls mouse hematopoietic stem cell self-renewal and quiescence through direct interactions with JAK2 J. Clin. Invest. 118 2008 2832 2844
3. G. d'Onofrio, R. Chirillo, G. Zini, G. Caenaro, M. Tommasi, and G. Micciulli Simultaneous measurement of reticulocyte and red blood cell indices in healthy subjects and patients with microcytic and macrocytic anemia Blood 85 1995 818 823
4. Q. Ding, Y.K. Lee, E.A. Schaefer, D.T. Peters, A. Veres, K. Kim, N. Kuperwasser, D.L. Motola, T.B. Meissner, W.T. Hendriks, and et al. A TALEN genome-editing system for generating human stem cell-based disease models Cell Stem Cell 12 2013 238 251
5. Q. Ding, S.N. Regan, Y. Xia, L.A. Oostrom, C.A. Cowan, and K. Musunuru Enhanced efficiency of human pluripotent stem cell genome editing through replacing TALENs with CRISPRs Cell Stem Cell 12 2013 393 394
6. I.J. Fox, G.Q. Daley, S.A. Goldman, J. Huard, T.J. Kamp, and M. Trucco Stem cell therapy. Use of differentiated pluripotent stem cells as replacement therapy for treating disease Science 345 2014 1247391
7. S. Gery, and H.P. Koeffler Role of the adaptor protein LNK in normal and malignant hematopoiesis Oncogene 32 2013 3111 3118
8. M.C. Giarratana, H. Rouard, A. Dumont, L. Kiger, I. Safeukui, P.Y. Le Pennec, S. François, G. Trugnan, T. Peyrard, T. Marie, and et al. Proof of principle for transfusion of in vitro-generated red blood cells Blood 118 2011 5071 5079
9. R.M. Gupta, and K. Musunuru Expanding the genetic editing tool kit: ZFNs, TALENs, and CRISPR-Cas9 J. Clin. Invest. 124 2014 4154 4161
10. S. Hirose, N. Takayama, S. Nakamura, K. Nagasawa, K. Ochi, S. Hirata, S. Yamazaki, T. Yamaguchi, M. Otsu, S. Sano, and et al. Immortalization of erythroblasts by c-MYC and BCL-XL enables large-scale erythrocyte production from human pluripotent stem cells Stem Cell Reports 1 2013 499 508
11. X. Huang, S. Shah, J. Wang, Z. Ye, S.N. Dowey, K.M. Tsang, L.G. Mendelsohn, G.J. Kato, T.S. Kickler, and L. Cheng Extensive ex vivo expansion of functional human erythroid precursors established from umbilical cord blood cells by defined factors Mol. Ther. 22 2014 451 463
12. X. Huang, Y. Wang, W. Yan, C. Smith, Z. Ye, J. Wang, Y. Gao, L. Mendelsohn, and L. Cheng 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 2015 1470 1479
13. M. Kennedy, G. Awong, C.M. Sturgeon, A. Ditadi, R. LaMotte-Mohs, J.C. Zúñiga-Pflücker, and G. Keller T lymphocyte potential marks the emergence of definitive hematopoietic progenitors in human pluripotent stem cell differentiation cultures Cell Rep. 2 2012 1722 1735
14. L. Kobari, F. Yates, N. Oudrhiri, A. Francina, L. Kiger, C. Mazurier, S. Rouzbeh, W. El-Nemer, N. Hebert, M.C. Giarratana, and et al. Human induced pluripotent stem cells can reach complete terminal maturation: in vivo and in vitro evidence in the erythropoietic differentiation model Haematologica 97 2012 1795 1803
15. R. Kurita, N. Suda, K. Sudo, K. Miharada, T. Hiroyama, H. Miyoshi, K. Tani, and Y. Nakamura Establishment of immortalized human erythroid progenitor cell lines able to produce enucleated red blood cells PLoS ONE 8 2013 e59890
16. T.L. Lasho, A. Pardanani, and A. Tefferi LNK mutations in JAK2 mutation-negative erythrocytosis N. Engl. J. Med. 363 2010 1189 1190
17. H.Y. Lee, X. Gao, M.I. Barrasa, H. Li, R.R. Elmes, L.L. Peters, and H.F. Lodish PPAR-α and glucocorticoid receptor synergize to promote erythroid progenitor self-renewal Nature 522 2015 474 477
18. L.S. Ludwig, H.T. Gazda, J.C. Eng, S.W. Eichhorn, P. Thiru, R. Ghazvinian, T.I. George, J.R. Gotlib, A.H. Beggs, C.A. Sieff, and et al. Altered translation of GATA1 in Diamond-Blackfan anemia Nat. Med. 20 2014 748 753
19. M.F. McMullin, C. Wu, M.J. Percy, and W. Tong A nonsynonymous LNK polymorphism associated with idiopathic erythrocytosis Am. J. Hematol. 86 2011 962 964
20. A.R. Migliaccio, C. Whitsett, T. Papayannopoulou, and M. Sadelain The potential of stem cells as an in vitro source of red blood cells for transfusion Cell Stem Cell 10 2012 115 119
21. J.A. Mills, P. Paluru, M.J. Weiss, P. Gadue, and D.L. French Hematopoietic differentiation of pluripotent stem cells in culture Methods Mol. Biol. 1185 2014 181 194
22. I. Moraga, G. Wernig, S. Wilmes, V. Gryshkova, C.P. Richter, W.J. Hong, R. Sinha, F. Guo, H. Fabionar, T.S. Wehrman, and et al. Tuning cytokine receptor signaling by re-orienting dimer geometry with surrogate ligands Cell 160 2015 1196 1208
23. S. Perrotta, P.G. Gallagher, and N. Mohandas Hereditary spherocytosis Lancet 372 2008 1411 1426
24. G.F. Rousseau, M.C. Giarratana, and L. Douay Large-scale production of red blood cells from stem cells: what are the technical challenges ahead? Biotechnol. J. 9 2014 28 38
25. V.G. Sankaran, and S.H. Orkin The switch from fetal to adult hemoglobin Cold Spring Harb. Perspect. Med. 3 2013 a011643
26. V.G. Sankaran, T.F. Menne, D. Šćepanović, J.A. Vergilio, P. Ji, J. Kim, P. Thiru, S.H. Orkin, E.S. Lander, and H.F. Lodish MicroRNA-15a and -16-1 act via MYB to elevate fetal hemoglobin expression in human trisomy 13 Proc. Natl. Acad. Sci. USA 108 2011 1519 1524
27. V.G. Sankaran, L.S. Ludwig, E. Sicinska, J. Xu, D.E. Bauer, J.C. Eng, H.C. Patterson, R.A. Metcalf, Y. Natkunam, S.H. Orkin, and et al. Cyclin D3 coordinates the cell cycle during differentiation to regulate erythrocyte size and number Genes Dev. 26 2012 2075 2087
28. I.I. Slukvin Hematopoietic specification from human pluripotent stem cells: current advances and challenges toward de novo generation of hematopoietic stem cells Blood 122 2013 4035 4046
29. A. Spolverini, L. Pieri, P. Guglielmelli, A. Pancrazzi, T. Fanelli, C. Paoli, A. Bosi, I. Nichele, M. Ruggeri, and A.M. Vannucchi Infrequent occurrence of mutations in the PH domain of LNK in patients with JAK2 mutation-negative 'idiopathic' erythrocytosis Haematologica 98 2013 e101 e102
30. C.M. Sturgeon, A. Ditadi, R.L. Clarke, and G. Keller Defining the path to hematopoietic stem cells Nat. Biotechnol. 31 2013 416 418
31. C.M. Sturgeon, A. Ditadi, G. Awong, M. Kennedy, and G. Keller Wnt signaling controls the specification of definitive and primitive hematopoiesis from human pluripotent stem cells Nat. Biotechnol. 32 2014 554 561
32. P. van der Harst, W. Zhang, I. Mateo Leach, A. Rendon, N. Verweij, J. Sehmi, D.S. Paul, U. Elling, H. Allayee, X. Li, and et al. Seventy-five genetic loci influencing the human red blood cell Nature 492 2012 369 375
33. L. Velazquez, A.M. Cheng, H.E. Fleming, C. Furlonger, S. Vesely, A. Bernstein, C.J. Paige, and T. Pawson Cytokine signaling and hematopoietic homeostasis are disrupted in Lnk-deficient mice J. Exp. Med. 195 2002 1599 1611
34. A. Veres, B.S. Gosis, Q. Ding, R. Collins, A. Ragavendran, H. Brand, S. Erdin, C.A. Cowan, M.E. Talkowski, and K. Musunuru Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing Cell Stem Cell 15 2014 27 30
35. L.M. Williamson, and D.V. Devine Challenges in the management of the blood supply Lancet 381 2013 1866 1875