Deciphering the hierarchy of angiohematopoietic progenitors from human pluripotent stem cells

Cell Cycle

Volumn 12, Issue 5, 2013, Pages 720-727

  Slukvin, Igor I ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

Author keywords

Endothelial cells; Endothelial hematopoietic transition; Hemangioblast; Hematopoietic stem cells; Hemogenic endothelium; Human embryonic stem cells; Human induced pluripotent stem cells; Mesoderm

Indexed keywords

5' NUCLEOTIDASE; CD34 ANTIGEN; CD38 ANTIGEN; FIBRINOGEN RECEPTOR; LEUKOSIALIN; STEM CELL FACTOR RECEPTOR; VASCULAR ENDOTHELIAL CADHERIN;

ARTICLE; CELL ASSAY; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL RENEWAL; COCULTURE; ERYTHROID PRECURSOR CELL; HEMANGIOBLAST; HEMATOPOIETIC STEM CELL; HUMAN; IN VITRO STUDY; MESODERM; PLURIPOTENT STEM CELL;

EID: 84874625804     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.23823     Document Type: Article

References (74)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282:1145-7; PMID:9804556; http://dx.doi. org/10.1126/science.282. 5391.1145
2. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-72; PMID:18035408; http://dx.doi.org/10.1016/j.cell. 2007.11.019
3. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318:1917-20; PMID:18029452; http://dx.doi.org/10.1126/science. 1151526
4. Timmermans F, Velghe I, Vanwalleghem L, De Smedt M, Van Coppernolle S, Taghon T, et al. Generation of T cells from human embryonic stem cell-derived hematopoietic zones. J Immunol 2009; 182:6879-88; PMID:19454684; http://dx.doi. org/10.4049/jimmunol.0803670
5. Woll PS, Martin CH, Miller JS, Kaufman DS. Human embryonic stem cell-derived NK cells acquire functional receptors and cytolytic activity. J Immunol 2005; 175:5095-103; PMID:16210613
6. Lu SJ, Feng Q, Park JS, Vida L, Lee BS, Strausbauch M, et al. Biologic properties and enucleation of red blood cells from human embryonic stem cells. Blood 2008; 112:4475-84; PMID:18713948; http://dx.doi.org/10.1182/blood-2008-05- 157198
7. Olivier EN, Qiu C, Velho M, Hirsch RE, Bouhassira EE. Large-scale production of embryonic red blood cells from human embryonic stem cells. Exp Hematol 2006; 34:1635-42; PMID:17157159; http://dx.doi. org/10.1016/j.exphem. 2006.07.003
8. Choi KD, Vodyanik MA, Slukvin II. Generation of mature human myelomonocytic cells through expansion and differentiation of pluripotent stem cell-derived lin-CD34+CD43+CD45+ progenitors. J Clin Invest 2009; 119:2818-29; PMID:19726877; http://dx.doi.org/10.1172/JCI38591
9. Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 2008; 132:661-80; PMID:18295582; http://dx.doi.org/10.1016/j. cell.2008.02.008
10. Maximow AA. Relation of blood cells to connective tissues and endothelium. Physiol Rev 1924; 4:533-63
11. Sabin F. Origin and development of the primitive vessels of the chick and of the pig. Carnegie Inst Wash Publ Contribs Embryol 1917; 6:61-124
12. Murray PDF. The development in vitro of the blood of the early chick embryo. Proc R Soc Lond, B 1932; 111:497-521; http://dx.doi.org/10.1098/rspb. 1932.0070
13. Palis J, Robertson S, Kennedy M, Wall C, Keller G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 1999; 126:5073-84; PMID:10529424
14. Xu M J, Matsuoka S, Yang FC, Ebihara Y, Manabe A, Tanaka R, et al. Evidence for the presence of murine primitive megakaryocytopoiesis in the early yolk sac. Blood 2001; 97:2016-22; PMID:11264166; http://dx.doi.org/10.1182/ blood.V97.7.2016
15. Müller AM, Medvinsky A, Strouboulis J, Grosveld F, Dzierzak E. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1994; 1:291-301; PMID:7889417; http://dx.doi. org/10.1016/1074-7613(94)90081-7
16. Medvinsky A, Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 1996; 86:897-906; PMID:8808625; http://dx.doi. org/10.1016/S0092-8674(00)80165-8
17. de Bruijn MF, Ma X, Robin C, Ottersbach K, Sanchez MJ, Dzierzak E. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 2002; 16:673-83; PMID:12049719; http://dx.doi.org/10.1016/S1074-7613(02)00313-8
18. Cumano A, Dieterlen-Lievre F, Godin I. Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 1996; 86:907-16; PMID:8808626; http://dx.doi.org/10.1016/S0092-8674(00) 80166-X
19. Zovein AC, Hofmann JJ, Lynch M, French WJ, Turlo KA, Yang Y, et al. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 2008; 3:625-36; PMID:19041779; http://dx.doi. org/10.1016/j.stem.2008.09. 018
20. Jaffredo T, Gautier R, Brajeul V, Dieterlen-Lièvre F. Tracing the progeny of the aortic hemangioblast in the avian embryo. Dev Biol 2000; 224:204-14; PMID:10926760; http://dx.doi.org/10.1006/dbio.2000.9799
21. Dantschakoff V. Uber das erate auftreten der blutelemente in huhnerembryo. Folla Haematologica 1907; 4:159-66
22. Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 2010; 464:116-20; PMID:20154729; http://dx.doi.org/10.1038/ nature08764
23. Kissa K, Herbomel P. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 2010; 464:112-5; PMID:20154732; http://dx.doi.org/10.1038/nature08761
24. Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, Traver D. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 2010; 464:108-11; PMID:20154733; http://dx.doi.org/10.1038/ nature08738
25. Yokomizo T, Dzierzak E. Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos. Development 2010; 137:3651-61; PMID:20876651; http://dx.doi. org/10.1242/dev.051094
26. Gekas C, Dieterlen-Lièvre F, Orkin SH, Mikkola HK. The placenta is a niche for hematopoietic stem cells. Dev Cell 2005; 8:365-75; PMID:15737932; http://dx.doi.org/10.1016/j.devcel.2004.12.016
27. Li Z, Lan Y, He W, Chen D, Wang J, Zhou F, et al. Mouse embryonic head as a site for hematopoietic stem cell development. Cell Stem Cell 2012; 11:663-75; PMID:23122290; http://dx.doi.org/10.1016/j. stem.2012.07.004
28. Li W, Ferkowicz MJ, Johnson SA, Shelley WC, Yoder MC. Endothelial cells in the early murine yolk sac give rise to CD41-expressing hematopoietic cells. Stem Cells Dev 2005; 14:44-54; PMID:15725743; http://dx.doi.org/10.1089/scd. 2005.14.44
29. Vodyanik MA, Bork JA, Thomson JA, Slukvin II. Human embryonic stem cell-derived CD34+ cells: efficient production in the co-culture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 2005; 105:617-26; PMID:15374881; http://dx.doi.org/10.1182/blood-2004-04-1649
30. Choi KD, Yu J, Smuga-Otto K, Salvagiotto G, Rehrauer W, Vodyanik M, et al. Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 2009; 27:559-67; PMID:19259936
31. Vodyanik MA, Yu J, Zhang X, Tian S, Stewart R, Thomson JA, et al. A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell 2010; 7:718-29; PMID:21112566; http://dx.doi.org/10.1016/j.stem.2010.11. 011
32. D'Aniello C, Lonardo E, Iaconis S, Guardiola O, Liguoro AM, Liguori GL, et al. G protein-coupled receptor APJ and its ligand apelin act downstream of Cripto to specify embryonic stem cells toward the cardiac lineage through extracellular signal-regulated kinase/p70S6 kinase signaling pathway. Circ Res 2009; 105:231-8; PMID:19574549; http://dx.doi. org/10.1161/CIRCRESAHA.109.201186
33. Yu QC, Hirst CE, Costa M, Ng ES, Schiesser JV, Gertow K, et al. APELIN promotes hematopoiesis from human embryonic stem cells. Blood 2012; 119:6243-54; PMID:22611158; http://dx.doi. org/10.1182/blood-2011-12-396093
34. Shalaby F, Ho J, Stanford WL, Fischer KD, Schuh AC, Schwartz L, et al. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 1997; 89:981-90; PMID:9200616; http://dx.doi.org/10.1016/ S0092-8674(00)80283-4
35. Kataoka H, Takakura N, Nishikawa S, Tsuchida K, Kodama H, Kunisada T, et al. Expressions of PDGF receptor alpha, c-Kit and Flk1 genes clustering in mouse chromosome 5 define distinct subsets of nascent mesodermal cells. Dev Growth Differ 1997; 39:729-40; PMID:9493833; http://dx.doi. org/10.1046/j.1440-169X. 1997.t01-5-00009.x
36. Vodyanik MA, Thomson JA, Slukvin II. Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood 2006; 108:2095-105; PMID:16757688; http://dx.doi.org/10.1182/blood-2006- 02-003327
37. Choi KD, Vodyanik MA, Togarrati PP, Suknuntha K, Kumar A, Samarjeet F, et al. Identification of the hemogenic endothelial progenitor and its direct precursor in human pluripotent stem cell differentiation cultures. Cell Rep 2012; 2:553-67; PMID:22981233; http://dx.doi.org/10.1016/j.celrep.2012.08.002
38. Kennedy M, D'Souza SL, Lynch-Kattman M, Schwantz S, Keller G. Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 2007; 109:2679-87; PMID:17148580
39. Slukvin II, Vodyanik M. Endothelial origin of mesenchymal stem cells. Cell Cycle 2011; 10:1370-3; PMID:21444996; http://dx.doi.org/10.4161/cc.10.9. 15345
40. Breier G, Breviario F, Caveda L, Berthier R, Schnürch H, Gotsch U, et al. Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system. Blood 1996; 87:630-41; PMID:8555485
41. Lampugnani MG, Resnati M, Raiteri M, Pigott R, Pisacane A, Houen G, et al. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J Cell Biol 1992; 118:1511-22; PMID:1522121; http://dx.doi.org/10. 1083/jcb.118.6.1511
42. Shibuya A, Campbell D, Hannum C, Yssel H, Franz-Bacon K, McClanahan T, et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 1996; 4:573-81; PMID:8673704; http://dx.doi.org/10.1016/ S1074-7613(00)70060-4
43. Kojima H, Kanada H, Shimizu S, Kasama E, Shibuya K, Nakauchi H, et al. CD226 mediates platelet and megakaryocytic cell adhesion to vascular endothelial cells. J Biol Chem 2003; 278:36748-53; PMID:12847109; http://dx.doi.org/10. 1074/jbc. M300702200
44. Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 2009; 457:887-91; PMID:19129762; http://dx.doi.org/10.1038/nature07619
45. Otani T, Inoue T, Tsuji-Takayama K, Ijiri Y, Nakamura S, Motoda R, et al. Progenitor analysis of primitive erythropoiesis generated from in vitro culture of embryonic stem cells. Exp Hematol 2005; 33:632-40; PMID:15911087; http://dx.doi. org/10.1016/j.exphem.2005.03.006
46. Mikkola HK, Fujiwara Y, Schlaeger TM, Traver D, Orkin SH. Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood 2003; 101:508-16; PMID:12393529; http://dx.doi.org/10.1182/blood-2002-06-1699
47. Kennedy M, Firpo M, Choi K, Wall C, Robertson S, Kabrun N, et al. A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature 1997; 386:488-93; PMID:9087406; http://dx.doi. org/10.1038/386488a0
48. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G. A common precursor for hematopoietic and endothelial cells. Development 1998; 125:725-32; PMID:9435292
49. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 2004; 432:625-30; PMID:15577911; http://dx.doi. org/10.1038/nature03122
50. Fehling HJ, Lacaud G, Kubo A, Kennedy M, Robertson S, Keller G, et al. Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 2003; 130:4217-27; PMID:12874139; http://dx.doi.org/10.1242/dev.00589
51. Flamme I, Risau W. Induction of vasculogenesis and hematopoiesis in vitro. Development 1992; 116:435-9; PMID:1286617
52. Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 1995; 11:73-91; PMID:8689573; http://dx.doi.org/10.1146/annurev.cb.11.110195.000445
53. Cox CM, Poole TJ. Angioblast differentiation is inf luenced by the local environment: FGF-2 induces angioblasts and patterns vessel formation in the quail embryo. Dev Dyn 2000; 218:371-82; PMID:10842363; http://dx.doi.org/10. 1002/(SICI)1097-0177(200006)218:2<371: :AIDDVDY10> 3.0.CO;2-Z
54. Flamme I, Breier G, Risau W. Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev Biol 1995; 169:699-712; PMID:7781909; http://dx.doi. org/10.1006/dbio.1995.1180
55. Vittet D, Buchou T, Schweitzer A, Dejana E, Huber P. Targeted null-mutation in the vascular endothelialcadherin gene impairs the organization of vascularlike structures in embryoid bodies. Proc Natl Acad Sci USA 1997; 94:6273-8; PMID:9177207; http://dx.doi.org/10.1073/pnas.94.12.6273
56. Ema M, Yokomizo T, Wakamatsu A, Terunuma T, Yamamoto M, Takahashi S. Primitive erythropoiesis from mesodermal precursors expressing VE-cadherin, PECAM-1, Tie2, endoglin, and CD34 in the mouse embryo. Blood 2006; 108:4018-24; PMID:16926294; http://dx.doi.org/10.1182/blood-2006-03-012872
57. Yokomizo T, Takahashi S, Mochizuki N, Kuroha T, Ema M, Wakamatsu A, et al. Characterization of GATA-1(+) hemangioblastic cells in the mouse embryo. EMBO J 2007; 26:184-96; PMID:17159898; http://dx.doi.org/10.1038/sj.emboj. 7601480
58. Drake CJ, Fleming PA. Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 2000; 95:1671-9; PMID:10688823
59. McGrath KE, Frame JM, Fromm GJ, Koniski AD, Kingsley PD, Little J, et al. A transient definitive erythroid lineage with unique regulation of the β-globin locus in the mammalian embryo. Blood 2011; 117:4600-8; PMID:21378272; http://dx.doi. org/10.1182/blood-2010-12-325357
60. Rafii S, Kloss CC, Butler JM, Ginsberg M, Gars E, Lis R, et al. Human ESC-derived hemogenic endothelial cells undergo distinct waves of endothelial to hematopoietic transition. Blood 2013; 121:770-80; PMID:23169780
61. Kennedy M, Awong G, Sturgeon CM, Ditadi A, Lamotte-Mohs R, Zúñiga-Pflücker JC, et al. T lymphocyte potential marks the emergence of definitive hematopoietic progenitors in human pluripotent stem cell differentiation cultures. Cell Rep 2012; 2:1722-35; PMID:23219550; http://dx.doi.org/10.1016/j. celrep.2012.11.003
62. Wang L, Menendez P, Shojaei F, Li L, Mazurier F, Dick JE, et al. Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J Exp Med 2005; 201:1603-14; PMID:15883170; http://dx.doi. org/10.1084/jem.20041888
63. Kaufman DS, Woll PHC, Martin JL, Xinghui TL. CD34+ Cells Derived from Human Embryonic Stem Cells Demonstrate Hematopoietic Stem Cell Potential In Vitro and In Vivo. Blood 2004; 104:163a
64. Narayan AD, Chase JL, Lewis RL, Tian X, Kaufman DS, Thomson JA, et al. Human embryonic stem cellderived hematopoietic cells are capable of engrafting primary as well as secondary fetal sheep recipients. Blood 2006; 107:2180-3; PMID:16278307; http://dx.doi.org/10.1182/blood-2005-05-1922
65. Ledran MH, Krassowska A, Armstrong L, Dimmick I, Renström J, Lang R, et al. Efficient hematopoietic differentiation of human embryonic stem cells on stromal cells derived from hematopoietic niches. Cell Stem Cell 2008; 3:85-98; PMID:18593561; http://dx.doi.org/10.1016/j.stem.2008.06.001
66. Lu M, Kardel MD, O'Connor MD, Eaves CJ. Enhanced generation of hematopoietic cells from human hepatocarcinoma cell-stimulated human embryonic and induced pluripotent stem cells. Exp Hematol 2009; 37:924-36; PMID:19481135; http://dx.doi.org/10.1016/j.exphem.2009.05.007
67. Risueño RM, Sachlos E, Lee JH, Lee JB, Hong SH, Szabo E, et al. Inability of human induced pluripotent stem cell-hematopoietic derivatives to downregulate microRNAs in vivo reveals a block in xenograft hematopoietic regeneration. Stem Cells 2012; 30:131-9; PMID:22131151; http://dx.doi. org/10.1002/stem.1684
68. Kyba M, Perlingeiro RC, Daley GQ. HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 2002; 109:29-37; PMID:11955444; http://dx.doi.org/10.1016/S0092-8674(02)00680-3
69. Wang Y, Yates F, Naveiras O, Ernst P, Daley GQ. Embryonic stem cell-derived hematopoietic stem cells. Proc Natl Acad Sci USA 2005; 102:19081-6; PMID:16357205; http://dx.doi.org/10.1073/pnas.0506127102
70. Lee GS, Kim BS, Sheih JH, Moore M. Forced expression of HoxB4 enhances hematopoietic differentiation by human embryonic stem cells. Mol Cells 2008; 25:487-93; PMID:18511880
71. Unger C, Kärner E, Treschow A, Stellan B, Felldin U, Concha H, et al. Lentiviral-mediated HoxB4 expression in human embryonic stem cells initiates early hematopoiesis in a dose-dependent manner but does not promote myeloid differentiation. Stem Cells 2008; 26:2455-66; PMID:18617691; http://dx.doi. org/10.1634/stemcells.2007-0876
72. Matsumoto K, Isagawa T, Nishimura T, Ogaeri T, Eto K, Miyazaki S, et al. Stepwise development of hematopoietic stem cells from embryonic stem cells. PLoS ONE 2009; 4:e4820; PMID:19287487; http://dx.doi.org/10.1371/journal.pone. 0004820
73. Salvagiotto G, Zhao Y, Vodyanik M, Ruotti V, Stewart R, Marra M, et al. Molecular profiling reveals similarities and differences between primitive subsets of hematopoietic cells generated in vitro from human embryonic stem cells and in vivo during embryogenesis. Exp Hematol 2008; 36:1377-89; PMID:18922365; http://dx.doi.org/10.1016/j. exphem.2008.06.015
74. McKinney-Freeman S, Cahan P, Li H, Lacadie SA, Huang HT, Curran M, et al. The transcriptional landscape of hematopoietic stem cell ontogeny. Cell Stem Cell 2012; 11:701-14; PMID:23122293; http://dx.doi.org/10.1016/j.stem.2012.07. 018