Generation of Megakaryocytic Progenitors from Human Embryonic Stem Cells in a Feeder- and Serum-Free Medium

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Pick, Marjorie ^a,c   Azzola, Lisa ^a   Osborne, Elissa ^b   Stanley, Edouard G ^a,d   Elefanty, Andrew G ^a,d  

^a MONASH UNIVERSITY   (Australia)

^b MONASH IVF   (Australia)

^c HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^d ROYAL CHILDREN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; BETA3 INTEGRIN; CD34 ANTIGEN; CD4 ANTIGEN; CD41A ANTIGEN; CD45 ANTIGEN; FIBRINOGEN RECEPTOR; GLYCOPROTEIN IB ALPHA; THROMBOPOIETIN RECEPTOR; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CD34 SELECTION; CELL DIFFERENTIATION; CELL LINEAGE; CELL SUBPOPULATION; COLONY FORMATION; COLONY FORMING UNIT; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EMBRYONIC STEM CELL; FEEDER CELL; GENE; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; MEGAKARYOBLAST; MOUSE; MPL GENE; NONHUMAN; PF4 GENE; PLOIDY; PROCEDURES CONCERNING CELLS; REAL TIME POLYMERASE CHAIN REACTION; SPIN EMBRYOID BODY METHOD; THROMBOCYTE ACTIVATION; THROMBOCYTOPOIESIS;

ADENOSINE DIPHOSPHATE; ANTIGENS, CD; BLOOD PLATELETS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CULTURE MEDIA, SERUM-FREE; EMBRYONIC STEM CELLS; FEEDER CELLS; GENE EXPRESSION REGULATION; HUMANS; MEGAKARYOCYTES; PLATELET FACTOR 4; POLYPLOIDY; RECEPTORS, THROMBOPOIETIN; TIME FACTORS;

EID: 84873738263     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055530     Document Type: Article

References (35)

1. Berthier R, Prandini M, Sxhweitzer A, Thevenon D, (1997) The MS-5 murine stromal cell line and hematopoietic growth factors synergize to support the megakaryocytic differentiation of embryonic stem cells. Experimental Hematology 23: 481-490.
2. Eto K, Murphy R, Kerrigan SW, Bertoni A, Stuhlmann H, et al. (2002) Megakaryocytes derived from embryonic stem cells implicate CalDAG-GEFI in integrin signaling. Proc Natl Acad Sci U S A 99: 12819-12824.
3. Uzan G, Prandini MH, Rosa JP, Berthier R, (1996) Hematopoietic differentiation of embryonic stem cells: an in vitro model to study gene regulation during megakaryocytopoiesis. Stem Cells 14Suppl 1: 194-199.
4. 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.
5. Fujimoto TT, Kohata S, Suzuki H, Miyazaki H, Fujimura K, (2003) Production of functional platelets by differentiated embryonic stem (ES) cells in vitro. Blood 102: 4044-4051.
6. 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.
7. Klimchenko O, Mori M, Distefano A, Langlois T, Larbret F, et al. (2009) A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis. Blood 114: 1506-1517.
8. Lu SJ, Li F, Yin H, Feng Q, Kimbrel EA, et al. (2011) Platelets generated from human embryonic stem cells are functional in vitro and in the microcirculation of living mice. Cell Res 21: 530-545.
9. 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.
10. Pick M, Azzola L, Mossman A, Stanley EG, Elefanty AG, (2007) Differentiation of human embryonic stem cells in serum free medium reveals distinct roles for BMP4, VEGF, SCF and FGF2 in hematopoiesis. Stem Cells 25: 2206-2214.
11. Richards M, Fong CY, Chan WK, Wong PC, Bongso A, (2002) Human feeders support prolonged undifferentiated growth of human inner cell masses and embryonic stem cells. Nat Biotechnol 20: 933-936.
12. Costa M, Dottori M, Ng E, Hawes SM, Sourris K, et al. (2005) The hESC line Envy expresses high levels of GFP in all differentiated progeny. Nat Methods 2: 259-260.
13. Costa M, Sourris K, Hatzistavrou T, Elefanty AG, Stanley EG, (2008) Expansion of human embryonic stem cells in vitro. Curr Protoc Stem Cell Biol Chapter 1: 1C.1.1-1C.1.7.
14. Ng ES, Davis R, Stanley EG, Elefanty AG, (2008) A protocol describing the use of a recombinant protein-based, animal product-free medium (APEL) for human embryonic stem cell differentiation as spin embryoid bodies. Nat Protoc 3: 768-776.
15. Ruf A, Pick M, Deutsch V, Patscheke H, Goldfarb A, et al. (1997) In-vivo platelet activation correlates with red cell anionic phospholipid exposure in patients with beta-thalassaemia major. Br J Haematol 98: 51-56.
16. Mitjavila-Garcia MT, Cailleret M, Godin I, Nogueira MM, Cohen-Solal K, et al. (2002) Expression of CD41 on hematopoietic progenitors derived from embryonic hematopoietic cells. Development 129: 2003-2013.
17. Mikkola HK, Fujiwara Y, Schlaeger TM, Traver D, Orkin SH, (2003) Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood 101: 508-516.
18. Ferkowicz MJ, Starr M, Xie X, Li W, Johnson SA, et al. (2003) CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development 130: 4393-4403.
19. Basch RS, Zhang XM, Dolzhanskiy A, Karpatkin S, (1999) Expression of CD41 and c-mpl does not indicate commitment to the megakaryocyte lineage during haemopoietic development. British Journal of Haematology 105: 1044-1054.
20. Vodyanik MA, Thomson JA, Slukvin II, (2006) Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood 108: 2095-2105.
21. Ryo R, Proffitt RT, Poger ME, O'Bear R, Deuel TF, (1980) Platelet factor 4 antigen in megakaryocytes. Thromb Res 17: 645-652.
22. Elefanty AG, Begley CG, Hartley L, Papaevangeliou B, Robb L, (1999) SCL expression in the mouse embryo detected with a targeted lacZ reporter gene demonstrates its localization to hematopoietic, vascular, and neural tissues. Blood 94: 3754-3763.
23. Yu QC, Hirst CE, Costa M, Ng ES, Schiesser JV, et al. (2012) APELIN promotes hematopoiesis from human embryonic stem cells. Blood 119: 6243-6254.
24. Nerlov C, Querfurth E, Kulessa H, Graf T, (2000) GATA-1 interacts with the myeloid PU.1 transcription factor and represses PU.1-dependent transcription. Blood 95: 2543-2551.
25. Zhang P, Behre G, Pan J, Iwama A, Wara-Aswapati N, et al. (1999) Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1. Proc Natl Acad Sci U S A 96: 8705-8710.
26. 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.
27. Zambidis ET, Park TS, Yu W, Tam A, Levine M, et al. (2008) Expression of angiotensin-converting enzyme (CD143) identifies and regulates primitive hemangioblasts derived from human pluripotent stem cells. Blood 112: 3601-3614.
28. Zambidis ET, Peault B, Park TS, Bunz F, Civin CI, (2005) Hematopoietic differentiation of human embryonic stem cells progresses through sequential hemato-endothelial, primitive, and definitive stages resembling human yolk sac development. Blood 106: 860-870.
29. Debili N, Wendling F, Katz A, Guichard J, Breton-Gorius J, et al. (1995) The Mpl-ligand or thrombopoietin or megakaryocyte growth and differentiative factor has both direct proliferative and differentiative activities on human megakaryocyte progenitors. Blood 86: 2516-2525.
30. Feng R, Shimazaki C, Inaba T, Takahashi R, Hirai H, et al. (1998) CD34+/CD41a+ cells best predict platelet recovery after autologous peripheral blood stem cell transplantation. Bone Marrow Transplant 21: 1217-1222.
31. Dumon S, Heath VL, Tomlinson MG, Gottgens B, Frampton J, (2006) Differentiation of murine committed megakaryocytic progenitors isolated by a novel strategy reveals the complexity of GATA and Ets factor involvement in megakaryocytopoiesis and an unexpected potential role for GATA-6. Exp Hematol 34: 654-663.
32. Schipper LF, Brand A, Reniers N, Melief CJ, Willemze R, et al. (2003) Differential maturation of megakaryocyte progenitor cells from cord blood and mobilized peripheral blood. Exp Hematol 31: 324-330.
33. Schipper LF, Brand A, Fibbe WE, Van Hensbergen Y, (2012) Functional characterization of TPO-expanded CD34+ cord blood cells identifies CD34- CD61- cells as platelet-producing cells early after transplantation in NOD/SCID mice and rCD34+ cells as CAFC colony-forming cells. Stem Cells 30: 988-996.
34. Gaur M, Kamata T, Wang S, Moran B, Shattil SJ, et al. (2006) Megakaryocytes derived from human embryonic stem cells: a genetically tractable system to study megakaryocytopoiesis and integrin function. J Thromb Haemost 4: 436-442.
35. Takayama N, Nishimura S, Nakamura S, Shimizu T, Ohnishi R, et al. (2010) Transient activation of c-MYC expression is critical for efficient platelet generation from human induced pluripotent stem cells. J Exp Med 207: 2817-2830.