A novel Serum-Free monolayer culture for orderly hematopoietic differentiation of human pluripotent cells via mesodermal progenitors

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Niwa, Akira ^a,b   Heike, Toshio ^b   Umeda, Katsutsugu ^b,d   Oshima, Koichi ^a   Kato, Itaru ^a,b   Sakai, Hiromi ^e   Suemori, Hirofumi ^c   Nakahata, Tatsutoshi ^a,b   Saito, Megumu K ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^e Waseda University   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; BIOLOGICAL MARKER; CD34 ANTIGEN; CD45 ANTIGEN; VASCULOTROPIN RECEPTOR 2;

ARTICLE; BLOOD CELL; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EMBRYONIC STEM CELL; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MESODERM; MONOLAYER CULTURE; PLURIPOTENT STEM CELL; PRIMITIVE STREAK; ANIMAL; CELL CLONE; CELL LINE; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECT; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; METABOLISM; METHODOLOGY; STROMA CELL;

IPS;

ANIMALS; ANTIGENS, CD34; ANTIGENS, CD45; BIOLOGICAL MARKERS; BLOOD CELLS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CLONE CELLS; CULTURE MEDIA, SERUM-FREE; EMBRYONIC STEM CELLS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MESODERM; PLURIPOTENT STEM CELLS; STROMAL CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 79960822732     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022261     Document Type: Article

References (55)

1. Evans MJ, Kaufman MH, (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154-156.
2. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
3. Keller G, (2005) Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev 19: 1129-1155.
4. Xu Y, Shi Y, Ding S, (2008) A chemical approach to stem-cell biology and regenerative medicine. Nature 453: 338-344.
5. Shi Y, Do JT, Desponts C, Hahm HS, Scholer HR, et al. (2008) A combined chemical and genetic approach for the generation of induced pluripotent stem cells. Cell Stem Cell 2: 525-528.
6. Jaenisch R, Young R, (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132: 567-582.
7. Meissner A, Wernig M, Jaenisch R, (2007) Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat Biotechnol 25: 1177-1181.
8. Garcia-Porrero JA, Manaia A, Jimeno J, Lasky LL, Dieterlen-Lievre F, et al. (1998) Antigenic profiles of endothelial and hemopoietic lineages in murine intraembryonic hemogenic sites. Dev Comp Immunol 22: 303-319.
9. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G, (1998) A common precursor for hematopoietic and endothelial cells. Development 125: 725-732.
10. Wood HB, May G, Healy L, Enver T, Morriss-Kay GM, (1997) CD34 expression patterns during early mouse development are related to modes of blood vessel formation and reveal additional sites of hematopoiesis. Blood 90: 2300-2311.
11. Shalaby F, Ho J, Stanford WL, Fischer KD, Schuh AC, et al. (1997) A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 89: 981-990.
12. Sumi T, Tsuneyoshi N, Nakatsuji N, Suemori H, (2008) Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 135: 2969-2979.
13. Flamme I, Breier G, Risau W, (1995) Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev Biol 169: 699-712.
14. Risau W, (1995) Differentiation of endothelium. FASEB J 9: 926-933.
15. Risau W, Hallmann R, Albrecht U, (1986) Differentiation-dependent expression of proteins in brain endothelium during development of the blood-brain barrier. Dev Biol 117: 537-545.
16. 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.
17. Umeda K, Heike T, Yoshimoto M, Shiota M, Suemori H, et al. (2004) Development of primitive and definitive hematopoiesis from nonhuman primate embryonic stem cells in vitro. Development 131: 1869-1879.
18. Umeda K, Heike T, Yoshimoto M, Shinoda G, Shiota M, et al. (2006) Identification and characterization of hemoangiogenic progenitors during cynomolgus monkey embryonic stem cell differentiation. Stem Cells 24: 1348-1358.
19. Ji P, Jayapal SR, Lodish HF, (2008) Enucleation of cultured mouse fetal erythroblasts requires Rac GTPases and mDia2. Nat Cell Biol 10: 314-321.
20. Vodyanik MA, Bork JA, Thomson JA, Slukvin II, (2005) Human embryonic stem cell-derived CD34+ cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 105: 617-626.
21. Kitajima K, Tanaka M, Zheng J, Yen H, Sato A, et al. (2006) Redirecting differentiation of hematopoietic progenitors by a transcription factor, GATA-2. Blood 107: 1857-1863.
22. Takayama N, Nishikii H, Usui J, Tsukui H, Sawaguchi A, et al. (2008) Generation of functional platelets from human embryonic stem cells in vitro via ES-sacs, VEGF-promoted structures that concentrate hematopoietic progenitors. Blood 111: 5298-5306.
23. Choi KD, Vodyanik MA, Slukvin II, (2009) Generation of mature human myelomonocytic cells through expansion and differentiation of pluripotent stem cell-derived lin-CD34+CD43+CD45+ progenitors. J Clin Invest 119: 2818-2829.
24. Choi KD, Yu J, Smuga-Otto K, Salvagiotto G, Rehrauer W, et al. (2009) Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 27: 559-567.
25. Niwa A, Umeda K, Chang H, Saito M, Okita K, et al. (2009) Orderly hematopoietic development of induced pluripotent stem cells via Flk-1(+) hemoangiogenic progenitors. J Cell Physiol 221: 367-377.
26. Timmermans F, Velghe I, Vanwalleghem L, De Smedt M, Van Coppernolle S, et al. (2009) Generation of T cells from human embryonic stem cell-derived hematopoietic zones. J Immunol 182: 6879-6888.
27. Morishima T, Watanabe K, Niwa A, Fujino H, Matsubara H, et al. (2011) Neutrophil differentiation from human-induced pluripotent stem cells. J Cell Physiol 226: 1283-1291.
28. Shinoda G, Umeda K, Heike T, Arai M, Niwa A, et al. (2007) alpha4-Integrin(+) endothelium derived from primate embryonic stem cells generates primitive and definitive hematopoietic cells. Blood 109: 2406-2415.
29. Ji J, Vijayaragavan K, Bosse M, Menendez P, Weisel K, et al. (2008) OP9 stroma augments survival of hematopoietic precursors and progenitors during hematopoietic differentiation from human embryonic stem cells. Stem Cells 26: 2485-2495.
30. Chadwick K, Wang L, Li L, Menendez P, Murdoch B, et al. (2003) Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102: 906-915.
31. Wang L, Li L, Shojaei F, Levac K, Cerdan C, et al. (2004) Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity 21: 31-41.
32. Wang L, Menendez P, Shojaei F, Li L, Mazurier F, et al. (2005) Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J Exp Med 201: 1603-1614.
33. Nostro MC, Cheng X, Keller GM, Gadue P, (2008) Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2: 60-71.
34. Gadue P, Huber TL, Paddison PJ, Keller GM, (2006) Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci U S A 103: 16806-16811.
35. 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.
36. Martin R, Lahlil R, Damert A, Miquerol L, Nagy A, et al. (2004) SCL interacts with VEGF to suppress apoptosis at the onset of hematopoiesis. Development 131: 693-702.
37. Grigoriadis AE, Kennedy M, Bozec A, Brunton F, Stenbeck G, et al. (2010) Directed differentiation of hematopoietic precursors and functional osteoclasts from human ES and iPS cells. Blood 115: 2769-2776.
38. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
39. Suemori H, Yasuchika K, Hasegawa K, Fujioka T, Tsuneyoshi N, et al. (2006) Efficient establishment of human embryonic stem cell lines and long-term maintenance with stable karyotype by enzymatic bulk passage. Biochem Biophys Res Commun 345: 926-932.
40. Suwabe N, Takahashi S, Nakano T, Yamamoto M, (1998) GATA-1 regulates growth and differentiation of definitive erythroid lineage cells during in vitro ES cell differentiation. Blood 92: 4108-4118.
41. Nakahata T, Ogawa M, (1982) Hemopoietic colony-forming cells in umbilical cord blood with extensive capability to generate mono- and multipotential hemopoietic progenitors. J Clin Invest 70: 1324-1328.
42. Nakahata T, Ogawa M, (1982) Identification in culture of a class of hemopoietic colony-forming units with extensive capability to self-renew and generate multipotential hemopoietic colonies. Proc Natl Acad Sci U S A 79: 3843-3847.
43. Nakahata T, Spicer SS, Ogawa M, (1982) Clonal origin of human erythro-eosinophilic colonies in culture. Blood 59: 857-864.
44. Uchida T, Kanno T, Hosaka S, (1985) Direct measurement of phagosomal reactive oxygen by luminol-binding microspheres. J Immunol Methods 77: 55-61.
45. Ma F, Ebihara Y, Umeda K, Sakai H, Hanada S, et al. (2008) Generation of functional erythrocytes from human embryonic stem cell-derived definitive hematopoiesis. Proc Natl Acad Sci U S A 105: 13087-13092.
46. Fujimi A, Matsunaga T, Kobune M, Kawano Y, Nagaya T, et al. (2008) Ex vivo large-scale generation of human red blood cells from cord blood CD34+ cells by co-culturing with macrophages. Int J Hematol 87: 339-350.
47. Yamaguchi TP, Dumont DJ, Conlon RA, Breitman ML, Rossant J, (1993) flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development 118: 489-498.
48. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, et al. (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967.
49. Kennedy M, Firpo M, Choi K, Wall C, Robertson S, et al. (1997) A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature 386: 488-493.
50. Grigoriadis AE, Kennedy M, Bozec A, Brunton F, Stenbeck G, et al. (2010) Directed differentiation of hematopoietic precursors and functional osteoclasts from human ES and iPS cells. Blood 115: 2769-2776.
51. Kim K, Doi A, Wen B, Ng K, Zhao R, et al. (2010) Epigenetic memory in induced pluripotent stem cells. Nature 467: 285-290.
52. Osafune K, Caron L, Borowiak M, Martinez RJ, Fitz-Gerald CS, et al. (2008) Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 26: 313-315.
53. Ji H, Ehrlich LI, Seita J, Murakami P, Doi A, et al. (2010) Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 467: 338-342.
54. Kyba M, Perlingeiro RC, Daley GQ, (2002) HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 109: 29-37.
55. Raaijmakers MH, Mukherjee S, Guo S, Zhang S, Kobayashi T, et al. (2010) Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature 464: 852-857.