Hematopoietic differentiation from human ESCs as a model for developmental studies and future clinical translations. Invited review following the FEBS Anniversary Prize received on 5 July 2009 at the 34th FEBS Congress in Prague

FEBS Journal

Volumn 277, Issue 24, 2010, Pages 5014-5025

  Moreno Gimeno, Inmaculada ^a   Ledran, Maria H ^a,b   Lako, Majlinda ^a,b  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

blood cells; engraftment; hematopoiesis; hematopoietic differentiation; hematopoietic ontogeny; hematopoietic progenitors; hESC and iPSC therapeutic applications; human embryonic stem cells; induced pluripotent stem cells; SCID repopulating cells

Indexed keywords

CD45 ANTIGEN; COMPLEMENT COMPONENT C3B RECEPTOR; FIBRINOGEN RECEPTOR; STEM CELL FACTOR;

CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CLINICAL MEDICINE; COCULTURE; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENGRAFTMENT; GRAFT FAILURE; GRAFT VERSUS HOST REACTION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; INTERMETHOD COMPARISON; NONHUMAN; NUCLEAR REPROGRAMMING; ONTOGENY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; STROMA CELL;

ANIMALS; AWARDS AND PRIZES; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYONIC STEM CELLS; HUMANS; MODELS, BIOLOGICAL;

EID: 78649981800     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07926.x     Document Type: Review

References (89)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, &, Jones JM, (1998) Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147.
2. Jensen J, Hyllner J, &, Björquist P, (2009) Human embryonic stem cell technologies and drug discovery. J Cell Physiol 219, 513-519.
3. Kaufman DS, Hanson ET, Lewis RL, Auerbach R, &, Thomson JA, (2001) Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 98, 10716-10721. (Pubitemid 32878687)
4. + cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 105, 617-626.
5. Qiu C, Olivier EN, Velho M, &, Bouhassira EE, (2008) Globin switches in yolk sac-like primitive and fetal-like definitive red blood cells produced from human embryonic stem cells. Blood 111, 2400-2408.
6. Galic Z, Kitchen SG, Kacena A, Subramanian A, Burke B, Cortado R, &, Zack JA, (2006) T lineage differentiation from human embryonic stem cells. Proc Natl Acad Sci USA 103, 11742-11747.
7. Woll PS, Martin CH, Miller JS, &, Kaufman DS, (2005) Human embryonic stem cell-derived NK cells acquire functional receptors and cytolytic activity. J Immunol 175, 5095-5103.
8. (neg)PFV hemogenic precursors. Mol Ther 10, 1109-1120.
9. Wang L, Li L, Shojaei F, Levac K, Cerdan C, Menendez P, Martin T, Rouleau A, &, Bhatia M, (2004) Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity 21, 31-41.
10. Chang KH, Nelson AM, Cao H, Wang L, Nakamoto B, Ware CB, &, Papayannopoulou T, (2006) Definitive-like erythroid cells derived from human embryonic stem cells coexpress high levels of embryonic and fetal globins with little or no adult globin. Blood 108, 1515-1523.
11. Lerou PH, &, Daley GQ, (2005) Therapeutic potential of embryonic stem cells. Blood Rev 19, 321-331.
12. Menendez P, Bueno C, &, Wang L, (2006) Human embryonic stem cells: a journey beyond cell replacement therapies. Cytotherapy 8, 530-541.
13. Lensch MW, &, Daley GQ, (2006) Scientific and clinical opportunities for modeling blood disorders with embryonic stem cells. Blood 107, 2605-2612.
14. Jenq RR, &, Van Den Brink MR, (2010) Allogeneic haematopoietic stem cell transplantation: individualized stem cell and immune therapy of cancer. Nat Rev Cancer 10, 213-221.
15. Kilareski EM, Shah S, Nonnemacher MR, &, Wigdahl B, (2009) Regulation of HIV-1 transcription in cells of the monocyte-macrophage lineage. Retrovirology 6, 118.
16. Volberding PA, &, Deeks SG, (2010) Antiretroviral therapy and management of HIV infection. Lancet 376, 49-62.
17. Zhan X, Dravid G, Ye Z, Hammond H, Shamblott M, Gearhart J, &, Cheng L, (2004) Functional antigen-presenting leucocytes derived from human embryonic stem cells in vitro. Lancet 364, 163-171.
18. Anderson JS, Bandi S, Kaufman DS, &, Akkina R, (2006) Derivation of normal macrophages from human embryonic stem (hES) cells for applications in HIV gene therapy. Retrovirology 3, 24.
19. Su Z, Frye C, Bae KM, Kelley V, &, Vieweg J, (2008) Differentiation of human embryonic stem cells into immunostimulatory dendritic cells under feeder-free culture conditions. Clin Cancer Res 14, 6207-6217.
20. Senju S, Hirata S, Motomura Y, Fukuma D, Matsunaga Y, Fukushima S, &, Matsuyoshi H, (2010) Pluripotent stem cells as source of dendritic cells for immune therapy. Int J Hematol 91, 392-400.
21. Li MJ, Kim J, Li S, Zaia J, Yee JK, Anderson J, Akkina R, &, Rossi JJ, (2005) Long-term inhibition of HIV-1 infection in primary hematopoietic cells by lentiviral vector delivery of a triple combination of anti-HIV shRNA, anti-CCR5 ribozyme, and a nucleolar-localizing TAR decoy. Mol Ther 12, 900-909.
22. Liang M, Kamata M, Chen KN, Pariente N, An DS, &, Chen IS, (2010) Inhibition of HIV-1 infection by a unique short hairpin RNA to chemokine receptor 5 delivered into macrophages through hematopoietic progenitor cell transduction. J Gene Med 12, 255-265.
23. Hütter G, Nowak D, Mossner M, Ganepola S, Müssig A, Allers K, Schneider T, Hofmann J, Kücherer C, Blau O, et al. (2009) Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med 360, 692-698.
24. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, Royal RE, Kammula U, White DE, Mavroukakis SA, et al. (2005) Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 23, 2346-2357.
25. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, Royal RE, Topalian SL, Kammula US, Restifo NP, et al. (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314, 126-129.
26. Woll PS, Grzywacz B, Tian X, Marcus RK, Knorr DA, Verneris MR, &, Kaufman DS, (2009) Human embryonic stem cells differentiate into a homogeneous population of natural killer cells with potent in vivo antitumor activity. Blood 113, 6094-6101.
27. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, &, Yamanaka S, (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872.
28. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920.
29. Hanna J, Wernig M, Markoulaki S, Sun CW, Meissner A, Cassady JP, Beard C, Brambrink T, Wu LC, Townes TM, et al. (2007) Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 318, 1920-1923.
30. Xu D, Alipio Z, Fink LM, Adcock DM, Yang J, Ward DC, &, Ma Y, (2009) Phenotypic correction of murine hemophilia A using an iPS cell-based therapy. Proc Natl Acad Sci USA 106, 808-813.
31. Moore MAS, &, Metcalf D, (1970) Ontogeny of the hematopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol 18, 279-296.
32. Medvinsky A, &, Dzierzak E, (1996) Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897-906.
33. + pre-definitive HSCs. Cell Stem Cell 3, 99-108.
34. Kumaravelu P, Hook L, Morrison AM, Ure J, Zhao S, Zuyev S, Ansell J, &, Medvinsky A, (2002) Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term epopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development 129, 4891-4899. Erratum in Development (2003) 130, 425.
35. Zovein AC, Hofmann JJ, Lynch M, French WJ, Turlo KA, Yang Y, Becker MS, Zanetta L, Dejana E, Gasson JC, et al. (2008) Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3, 625-636.
36. Boisset JC, Van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, &, Robin C, (2010) In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464, 116-120.
37. Kissa K, &, Herbomel P, (2010) Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464, 112-115.
38. Sabin FR, (1920) Studies on the origin of blood vessels and of red blood corpuscles as seen in the living blastoderm of chicks during the second day of incubation. Contrib Embryol 9, 214.
39. Murray PDF, (1932) The development in vitro of blood of the early chick embryo. Proc R Soc London 111, 497-521.
40. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, &, Keller G, (1998) A common precursor for hematopoietic and endothelial cells. Development 125, 725-732.
41. Mandal L, Banerjee U, &, Hartenstein V, (2004) Evidence for a fruit fly hemangioblast and similarities between lymph-gland hematopoiesis in fruit fly and mammal aorta-gonadal-mesonephros mesoderm. Nat Genet 36, 1019-1023.
42. Vogeli KM, Jin SW, Martin GR, &, Stainier DY, (2006) A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 443, 337-339.
43. Huber TL, Kouskoff V, Fehling HJ, Palis J, &, Keller G, (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432, 625-630.
44. Gunsilius E, Duba HC, Petzer AL, Kähler CM, Grünewald K, Stockhammer G, Gabl C, Dirnhofer S, Clausen J, &, Gastl G, (2001) Evidence from a leukaemia model for maintenance of vascular endothelium by bone-marrow-derived endothelial cells. Lancet 355, 1688-1691. (Pubitemid 30248482)
45. Pelosi E, Valtieri M, Coppola S, Botta R, Gabbianelli M, Lulli V, Marziali G, Masella B, Müller R, Sgadari C, et al. (2002) Identification of the hemangioblast in postnatal life. Blood 100, 3203-3208.
46. Lancrin C, Sroczynska P, Stephenson C, Allen T, Kouskoff V, &, Lacaud G, (2009) The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 457, 892-895.
47. Eilken HM, Nishikawa SI, &, Schroeder T, (2009) Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 457, 896-901.
48. Oberlin E, El Hafny B, Petit-Cocault L, &, Souyri M, (2010) Definitive human and mouse hematopoiesis originates from the embryonic endothelium: a new class of HSCs based on VE-cadherin expression. Int J Dev Biol 54, 1165-1173.
49. Porcher C, Swat W, Rockwell K, Fujiwara Y, Alt FW, &, Orkin SH, (1996) The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86, 47-57.
50. D'Souza SL, Elefanty AG, &, Keller G, (2005) SCL/Tal-1 is essential for hematopoietic commitment of the hemangioblast but not for its development. Blood 105, 3862-3870.
51. Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, &, Speck NA, (2009) RUNX1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457, 887-891.
52. Bárcena A, Kapidzic M, Muench MO, Gormley M, Scott MA, Weier JF, Ferlatte C, &, Fisher SJ, (2009) The human placenta is a hematopoietic organ during the embryonic and fetal periods of development. Dev Biol 327, 24-33.
53. Robin C, Bollerot K, Mendes S, Haak E, Crisan M, Cerisoli F, Lauw I, Kaimakis P, Jorna R, Vermeulen M, et al. (2009) Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. Cell Stem Cell 5, 385-395.
54. Serikov V, Hounshell C, Larkin S, Green W, Ikeda H, Walters MC, &, Kuypers FA, (2009) Human term placenta as a source of hematopoietic cells. Exp Biol Med 234, 813-823.
55. Woll PS, Morris JK, Painschab MS, Marcus RK, Kohn AD, Biechele TL, Moon RT, &, Kaufman DS, (2008) Wnt signaling promotes hematoendothelial cell development from human embryonic stem cells. Blood 111, 122-131.
56. Ji J, Vijayaragavan K, Bosse M, Menendez P, Weisel K, &, Bhatia M, (2008) OP9 stroma augments survival of hematopoietic precursors and progenitors during hematopoietic differentiation from human embryonic stem cells. Stem Cells 26, 2485-2495.
57. Vodyanik MA, Thomson JA, &, Slukvin II, (2006) Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood 108, 2095-2105.
58. Ledran MH, Krassowska A, Armstrong L, Dimmick I, Renström J, Lang R, Yung S, Santibanez-Coref M, Dzierzak E, Stojkovic M, et al. (2008) Efficient hematopoietic differentiation of human embryonic stem cells on stromal cells derived from hematopoietic niches. Cell Stem Cell 3, 85-98.
59. Chadwick K, Wang L, Li L, Menendez P, Murdoch B, Rouleau A, &, Bhatia M, (2003) Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102, 906-915.
60. Wang L, Menendez P, Cerdan C, &, Bhatia M, (2005) Hematopoietic development from human embryonic stem cell lines. Exp Hematol 33, 987-996.
61. Kennedy M, D'Souza SL, Lynch-Kattman M, Schwantz S, &, Keller G, (2007) Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 109, 2679-2687.
62. Ng ES, Davis RP, Azzola L, Stanley EG, &, Elefanty AG, (2005) Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood 106, 1601-1603.
63. Ng ES, Davis RP, Hatzistavrou T, Stanley EG, &, Elefanty AG, (2008) Directed differentiation of human embryonic stem cells as spin embryoid bodies and a description of the hematopoietic blast colony forming assay. Curr Protoc Stem Cell Biol. doi:.
64. Wang L, Menendez P, Shojaei F, Li L, Mazurier F, Dick JE, Cerdan C, Levac K, &, Bhatia M, (2005) Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J Exp Med 201, 1603-1614.
65. Tian X, Woll PS, Morris JK, Linehan JL, &, Kaufman DS, (2006) Hematopoietic engraftment of human embryonic stem cell-derived cells is regulated by recipient innate immunity. Stem Cells 24, 1370-1380. (Pubitemid 44464705)
66. McDermott SP, Eppert K, Lechman E, Doedens M, &, Dick JE, (2010) Comparison of human cord blood engraftment between immunocompromised mouse strains. Blood 116, 193-200.
67. -/- mice. Exp Hematol 33, 1417-1426.
68. null mice permits multilineage engraftment without previous irradiation. Cytotherapy 12, 45-49.
69. null mutation. Clin Immunol 135, 84-98.
70. Narayan AD, Chase JL, Lewis RL, Tian X, Kaufman DS, Thomson JA, &, Zanjani ED, (2006) Human embryonic stem cell-derived hematopoietic cells are capable of engrafting primary as well as secondary fetal sheep recipients. Blood 107, 2180-2183.
71. + cells preferentially develop into endothelial cells. Stem Cells 27, 2675-2685.
72. Menendez P, Bueno C, Wang L, &, Bhatia M, (2005) Human embryonic stem cells: potential tool for achieving immunotolerance? Stem Cell Rev 1, 151-158.
73. Choi KD, Yu J, Smuga-Otto K, Salvagiotto G, Rehrauer W, Vodyanik M, Thomson J, &, Slukvin I, (2009) Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 27, 559-567.
74. Park IH, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A, Lensch MW, Cowan C, Hochedlinger K, &, Daley GQ, (2008) Disease-specific induced pluripotent stem cells. Cell 134, 877-886.
75. Lako M, Armstrong L, &, Stojkovic M, (2010) Induced pluripotent stem cells: it looks simple but can looks deceive? Stem Cells 28, 845-850.
76. Teo AK, &, Vallier L, (2010) Emerging use of stem cells in regenerative medicine. Biochem J 428, 11-23.
77. Feng Q, Lu SJ, Klimanskaya I, Gomes I, Kim D, Chung Y, Honig GR, Kim KS, &, Lanza R, (2010) Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells 28, 704-712.
78. Zhang J, Wilson GF, Soerens AG, Koonce CH, Yu J, Palecek SP, Thomson JA, &, Kamp TJ, (2009) Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 104, e30-e41.
79. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, &, Thomson JA, (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324, 797-801.
80. Hu BY, Weick JP, Yu J, Ma LX, Zhang XQ, Thomson JA, &, Zhang SC, (2010) Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc Natl Acad Sci USA 107, 4335-4340.
81. Chin MH, Mason MJ, Xie W, Volinia S, Singer M, Peterson C, Ambartsumyan G, Aimiuwu O, Richter L, Zhang J, et al. (2009) Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 5, 111-123.
82. Pick M, Stelzer Y, Bar-Nur O, Mayshar Y, Eden A, &, Benvenisty N, (2009) Clone- and gene-specific aberrations of parental imprinting in human induced pluripotent stem cells. Stem Cells 27, 2686-2690.
83. Doi A, Park IH, Wen B, Murakami P, Aryee MJ, Irizarry R, Herb B, Ladd-Acosta C, Rho J, Loewer S, et al. (2009) Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 41, 1350-1353.
84. Gutierrez-Aranda I, Ramos-Mejía V, Bueno C, Muñoz- López M, Real PJ, Macía A, Sánchez L, Ligero G, García-Pérez JL, &, Menendez P, (2010) Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless the site of injection. Stem Cells 28, 1568-1570.
85. Kim K, Doi A, Wen B, Ng K, Zhao R, Cahan P, Kim J, Aryee MJ, Ji H, Ehrlich LI, et al. (2010) Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290.
86. Polo JM, Liu S, Figueroa ME, Kulalert W, Eminli S, Tan KY, Apostolou E, Stadtfeld M, Li Y, Shioda T, et al. (2010) Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol 28, 848-855.
87. Zaehres H, Kögler G, Arauzo-Bravo MJ, Bleidissel M, Santourlidis S, Weinhold S, Greber B, Kim JB, Buchheiser A, Liedtke S, et al. (2010) Induction of pluripotency in human cord blood unrestricted somatic stem cells. Exp Hematol 38, 809-818.
88. West JA, Viswanathan SR, Yabuuchi A, Cunniff K, Takeuchi A, Park IH, Sero JE, Zhu H, Perez-Atayde A, Frazier AL, et al. (2009) A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 460, 909-913.
89. Hong H, Takahashi K, Ichisaka T, Aoi T, Kanagawa O, Nakagawa M, Okita K, &, Yamanaka S, (2009) Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460, 1132-1135.