A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis

Blood

Volumn 114, Issue 8, 2009, Pages 1506-1517

  Klimchenko, Olena ^a   Mori, Marcella ^a   DiStefano, Antonio ^a   Langlois, Thierry ^a   Larbret, Frédéric ^a   Lecluse, Yann ^a   Feraud, Olivier ^a,b   Vainchenker, William ^a   Norol, Françoise ^a,c   Debili, Najet ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b HÔPITAL PAUL BROUSSE   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIBODY; ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; FIBRINOGEN RECEPTOR; GLYCOPHORIN A; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 1; KRUPPEL LIKE FACTOR 4; LEUKOSIALIN; STEM CELL FACTOR; THROMBOPOIETIN RECEPTOR; TRANSCRIPTION FACTOR FLI 1; UNCLASSIFIED DRUG; CD34 ANTIGEN; GLYCOPHORIN; GLYCOPROTEIN IIB; THROMBIN RECEPTOR;

ARTICLE; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL MATURATION; CELL POPULATION; CONTROLLED STUDY; CORRELATION ANALYSIS; EMBRYONIC STEM CELL; ERYTHROCYTE; ERYTHROID CELL; GENE EXPRESSION; HEMATOPOIESIS; HUMAN; HUMAN CELL; MEGAKARYOCYTE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; CELL CULTURE; CELL LINEAGE; COCULTURE; CYTOLOGY; ERYTHROID MEGAKARYOCYTE PROGENITOR CELL; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD34; ANTIGENS, CD43; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYONIC STEM CELLS; ERYTHROID CELLS; GLYCOPHORIN; HEMATOPOIESIS; HUMANS; MEGAKARYOCYTE-ERYTHROID PROGENITOR CELLS; MEGAKARYOCYTES; MICE; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PLATELET MEMBRANE GLYCOPROTEIN IIB;

EID: 70349568677     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-09-178863     Document Type: Article

References (45)

1. Kaushansky K. Historical review: megakaryopoiesis and thrombopoiesis. Blood. 2008;111:981-986.
2. Ihle JN, Witthuhn B, Tang B, Yi T, Quelle FW. Cytokine receptors and signal transduction. Baillieres Clin Haematol. 1994;7:17-48.
3. Witthuhn BA, Quelle FW, Silvennoinen O, et al. JAK2 associates with the erythropoietin receptor and is tyrosine phosphorylated and activated following stimulation with erythropoietin. Cell. 1993;74:227-236. (Pubitemid 23221699)
4. Tortolani PJ, Johnston JA, Bacon CM, et al. Thrombopoietin induces tyrosine phosphorylation and activation of the Janus kinase, JAK2. Blood. 1995;85:3444-3451.
5. Cantor AB, Orkin SH. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene. 2002;21:3368-3376.
6. Goldfarb AN. Transcriptional control of megakaryocyte development. Oncogene. 2007; 26:6795-6802.
7. Chang Y, Bluteau D, Debili N, Vainchenker W. From hematopoietic stem cells to platelets. J Thromb Haemost. 2007;5[suppl 1]:318-327.
8. Frontelo P, Manwani D, Galdass M, et al. Novel role for EKLF in megakaryocyte lineage commitment. Blood. 2007;110:3871-3880. (Pubitemid 350248442)
9. Bouilloux F, Juban G, Cohet N, et al. EKLF restricts megakaryocytic differentiation at the benefit of erythrocytic differentiation. Blood. 2008; 112:576-584.
10. -/- mice: c-Myb mutation causes supraphysiological production of platelets in the absence of thrombopoietin signaling. Proc Natl Acad Sci U S A. 2004;101:6553-6558.
11. Hart A, Melet F, Grossfeld P, et al. Fli-1 is required for murine vascular and megakaryocytic development and is hemizygously deleted in patients with thrombocytopenia. Immunity. 2000;13:167-177. (Pubitemid 30951883)
12. Pang L, Xue HH, Szalai G, et al. Maturation stage-specific regulation of megakaryopoiesis by pointed-domain Ets proteins. Blood. 2006;108: 2198-2206. (Pubitemid 44497500)
13. Song WJ, Sullivan MG, Legare RD, et al. Haplo-insufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat Genet. 1999;23:166-175.
14. Debili N, Coulombel L, Croisille L, et al. Characterization of a bipotent erythro-megakaryocytic progenitor in human bone marrow. Blood. 1996; 88:1284-1296. (Pubitemid 26276803)
15. Forsberg EC, Serwold T, Kogan S, Weissman IL, Passegue E. New evidence supporting megakaryocyte-erythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors. Cell. 2006;126:415-426. (Pubitemid 44092964)
16. Vannucchi AM, Paoletti F, Linari S, et al. Identification and characterization of a bipotent (erythroid and megakaryocytic) cell precursor from the spleen of phenylhydrazine-treated mice. Blood. 2000;95:2559-2568. (Pubitemid 30210534)
17. Pronk CJ, Rossi DJ, Mansson R, et al. Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell. 2007;1:428-442. (Pubitemid 47506534)
18. Adolfsson J, Mansson R, Buza-Vidas N, et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell. 2005;121:295-306. (Pubitemid 40546396)
19. Tober J, Koniski A, McGrath KE, et al. The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis. Blood. 2007;109:1433-1441. (Pubitemid 46239574)
20. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145-1147.
21. Chang KH, Nelson AM, Cao H, et al. 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. 2006;108:1515-1523. (Pubitemid 44316116)
22. 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;34:1635-1642. (Pubitemid 44838996)
23. Qiu C, Olivier EN, Velho M, Bouhassira EE. Globin switches in yolk sac-like primitive and fetal-like definitive red blood cells produced from human embryonic stem cells. Blood. 2008;111: 2400-2408.
24. Gaur M, Kamata T, Wang S, Moran B, Shattil SJ, Leavitt AD. Megakaryocytes derived from human embryonic stem cells: a genetically tractable system to study megakaryocytopoiesis and integrin function. J Thromb Haemost. 2006;4:436-442.
25. Eto K, Murphy R, Kerrigan SW, et al. Megakaryocytes derived from embryonic stem cells implicate CalDAG-GEFI in integrin signaling. Proc Natl Acad Sci U S A. 2002;99:12819-12824.
26. Gilles L, Guieze R, Bluteau D, et al. P19INK4D links endomitotic arrest and megakaryocyte maturation and is regulated by AML-1. Blood. 2008;111:4081-4091.
27. Vandesompele J, De Preter K, Pattyn F, et al. Accurate normalization of real-time quantitative RTPCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3: RESEARCH0034.
28. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45.
29. Otani T, Inoue T, Tsuji-Takayama K, et al. Progenitor analysis of primitive erythropoiesis generated from in vitro culture of embryonic stem cells. Exp Hematol. 2005;33:632-640. (Pubitemid 40725829)
30. Vodyanik MA, Slukvin II. Hematoendothelial differentiation of human embryonic stem cells. Curr Protoc Cell Biol. 2007;Chapter 23:Unit 23.6.
31. Keller G, Kennedy M, Papayannopoulou T, Wiles MV. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol Cell Biol. 1993;13:473-486. (Pubitemid 23006925)
32. Vodyanik MA, Thomson JA, Slukvin II. Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood. 2006;108:2095-2105.
33. 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;101:508-516. (Pubitemid 36082842)
34. Mitjavila-Garcia MT, Cailleret M, Godin I, et al. Expression of CD41 on hematopoietic progenitors derived from embryonic hematopoietic cells. Development. 2002;129:2003-2013. (Pubitemid 34874215)
35. Xu MJ, Matsuoka S, Yang FC, et al. Evidence for the presence of murine primitive megakaryocytopoiesis in the early yolk sac. Blood. 2001;97: 2016-2022. (Pubitemid 32239081)
36. Wu H, Liu X, Jaenisch R, Lodish HF. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell. 1995;83:59-67.
37. Lee R, Kertesz N, Joseph SB, Jegalian A, Wu H. Erythropoietin (Epo) and EpoR expression and 2 waves of erythropoiesis. Blood. 2001;98:1408-1415.
38. Lin CS, Lim SK, D'Agati V, Costantini F. Differential effects of an erythropoietin receptor gene disruption on primitive and definitive erythropoiesis. Genes Dev. 1996;10:154-164. (Pubitemid 26044603)
39. Sanchez M, Weissman IL, Pallavicini M, et al. Differential amplification of murine bipotent megakaryocytic/erythroid progenitor and precursor cells during recovery from acute and chronic erythroid stress. Stem Cells. 2006;24:337-348. (Pubitemid 44464803)
40. Starck J, Cohet N, Gonnet C, et al. Functional cross-antagonism between transcription factors FLI-1 and EKLF. Mol Cell Biol. 2003;23:1390-1402. (Pubitemid 36177047)
41. Emambokus N, Vegiopoulos A, Harman B, Jenkinson E, Anderson G, Frampton J. Progression through key stages of haemopoiesis is dependent on distinct threshold levels of c-Myb. EMBO J. 2003;22:4478-4488. (Pubitemid 37087201)
42. Lu J, Guo S, Ebert BL, et al. MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev Cell. 2008;14:843-853. (Pubitemid 351757199)
43. Tober J, McGrath KE, Palis J. Primitive erythropoiesis and megakaryopoiesis in the yolk sac are independent of c-myb. Blood. 2008;111:2636-2639.
44. Lecuyer E, Lariviere S, Sincennes MC, et al. Protein stability and transcription factor complex assembly determined by the SCL-LMO2 interaction. J Biol Chem. 2007;282:33649-33658. (Pubitemid 350159506)
45. Schlaeger TM, Schuh A, Flitter S, et al. Decoding hematopoietic specificity in the helix-loop-helix domain of the transcription factor SCL/Tal-1. Mol Cell Biol. 2004;24:7491-7502. (Pubitemid 39121477)