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Development, Vol 125, Issue 4 725-732, Copyright © 1998 by Company of Biologists

JOURNAL ARTICLES

A common precursor for hematopoietic and endothelial cells

K Choi, M Kennedy, A Kazarov, JC Papadimitriou and G Keller
Department of Pathology, University of Maryland at Baltimore, Baltimore, MD 21201, USA. kchoi@umabnet.ab.umd.edu

Embryonic stem cell-derived embryoid bodies contain a unique precursor population which, in response to vascular endothelial growth factor, gives rise to blast colonies in semi-solid medium. Upon transfer to liquid culture with appropriate cytokines, these blast colonies generate both hematopoietic and adherent, stromal-type cells. Cells within the adherent population display characteristics of endothelial lineage including the expression of CD31, flk-1, flt-1, tie-2, the capacity to take up acetylated LDL and the presence of cytoplasmic Weibel-Palade bodies. Mixing studies demonstrated that the hematopoietic and endothelial precursors within the blast colonies develop from the same cell, the blast colony-forming cell. Kinetic analysis showed that the blast colony-forming cell represents a transient cell population that develops early and is lost quickly during embryoid body development. These findings provide strong evidence that the blast colony-forming cell represents the long-hypothesized hemangioblast, the common precursor of the hematopoietic and endothelial lineages.
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K. Umeda, T. Heike, M. Yoshimoto, G. Shinoda, M. Shiota, H. Suemori, H. Y. Luo, D. H. K. Chui, R. Torii, M. Shibuya, et al.
Identification and Characterization of Hemoangiogenic Progenitors During Cynomolgus Monkey Embryonic Stem Cell Differentiation
Stem Cells, May 1, 2006; 24(5): 1348 - 1358.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Glasker, J. Li, J. B. Xia, H. Okamoto, W. Zeng, R. R. Lonser, Z. Zhuang, E. H. Oldfield, and A. O. Vortmeyer
Hemangioblastomas share protein expression with embryonal hemangioblast progenitor cell.
Cancer Res., April 15, 2006; 66(8): 4167 - 4172.
[Abstract] [Full Text] [PDF]

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 BloodHome page
S. Willey, A. Ayuso-Sacido, H. Zhang, S. T. Fraser, K. E. Sahr, M. J. Adlam, M. Kyba, G. Q. Daley, G. Keller, and M. H. Baron
Acceleration of mesoderm development and expansion of hematopoietic progenitors in differentiating ES cells by the mouse Mix-like homeodomain transcription factor
Blood, April 15, 2006; 107(8): 3122 - 3130.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
J. E. Pimanda, L. Silberstein, M. Dominici, B. Dekel, M. Bowen, S. Oldham, A. Kallianpur, S. J. Brandt, D. Tannahill, B. Gottgens, et al.
Transcriptional Link between Blood and Bone: the Stem Cell Leukemia Gene and Its +19 Stem Cell Enhancer Are Active in Bone Cells.
Mol. Cell. Biol., April 1, 2006; 26(7): 2615 - 2625.
[Abstract] [Full Text] [PDF]

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 Stem CellsHome page
H. Priddle, D. R. E. Jones, P. W. Burridge, and R. Patient
Hematopoiesis from Human Embryonic Stem Cells: Overcoming the Immune Barrier in Stem Cell Therapies
Stem Cells, April 1, 2006; 24(4): 815 - 824.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
U. Fiedler, S. Christian, S. Koidl, D. Kerjaschki, M. S. Emmett, D. O. Bates, G. Christofori, and H. G. Augustin
The Sialomucin CD34 Is a Marker of Lymphatic Endothelial Cells in Human Tumors
Am. J. Pathol., March 1, 2006; 168(3): 1045 - 1053.
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 Stem CellsHome page
G.-M. Zou, R. J. Chan, W. C. Shelley, and M. C. Yoder
Reduction of Shp-2 Expression by Small Interfering RNA Reduces Murine Embryonic Stem Cell-Derived In Vitro Hematopoietic Differentiation
Stem Cells, March 1, 2006; 24(3): 587 - 594.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
E. Poon, F. Clermont, M. T. Firpo, and R. J. Akhurst
TGF{beta} inhibition of yolk-sac-like differentiation of human embryonic stem-cell-derived embryoid bodies illustrates differences between early mouse and human development
J. Cell Sci., February 15, 2006; 119(4): 759 - 768.
[Abstract] [Full Text] [PDF]

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 BloodHome page
N. Matsumoto, A. Kubo, H. Liu, K. Akita, F. Laub, F. Ramirez, G. Keller, and S. L. Friedman
Developmental regulation of yolk sac hematopoiesis by Kruppel-like factor 6
Blood, February 15, 2006; 107(4): 1357 - 1365.
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 BloodHome page
A. L. Olsen, D. L. Stachura, and M. J. Weiss
Designer blood: creating hematopoietic lineages from embryonic stem cells
Blood, February 15, 2006; 107(4): 1265 - 1275.
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 Am. J. Pathol.Home page
M. Anghelina, P. Krishnan, L. Moldovan, and N. I. Moldovan
Monocytes/Macrophages Cooperate with Progenitor Cells during Neovascularization and Tissue Repair: Conversion of Cell Columns into Fibrovascular Bundles
Am. J. Pathol., February 1, 2006; 168(2): 529 - 541.
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 Biol. Reprod.Home page
H. Zhang, K. Saeki, A. Kimura, K. Saeki, M. Nakahara, M. Doshi, Y. Kondo, T. Nakano, and A. Yuo
Efficient and Repetitive Production of Hematopoietic and Endothelial Cells from Feeder-Free Monolayer Culture System of Primate Embryonic Stem Cells
Biol Reprod, February 1, 2006; 74(2): 295 - 306.
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 BloodHome page
I. Hamaguchi, T. Morisada, M. Azuma, K. Murakami, M. Kuramitsu, T. Mizukami, K. Ohbo, K. Yamaguchi, Y. Oike, D. J. Dumont, et al.
Loss of Tie2 receptor compromises embryonic stem cell-derived endothelial but not hematopoietic cell survival
Blood, February 1, 2006; 107(3): 1207 - 1213.
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 Am. J. Physiol. Heart Circ. Physiol.Home page
J. Muller-Ehmsen, A. Schmidt, B. Krausgrill, R. H. G. Schwinger, and W. Bloch
Role of erythropoetin for angiogenesis and vasculogenesis: from embryonic development through adulthood
Am J Physiol Heart Circ Physiol, January 1, 2006; 290(1): H331 - H340.
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 BloodHome page
M. Ema, S. Takahashi, and J. Rossant
Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors
Blood, January 1, 2006; 107(1): 111 - 117.
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 Proc. Natl. Acad. Sci. USAHome page
Y. Wang, F. Yates, O. Naveiras, P. Ernst, and G. Q. Daley
Embryonic stem cell-derived hematopoietic stem cells
PNAS, December 27, 2005; 102(52): 19081 - 19086.
[Abstract] [Full Text] [PDF]

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 Eur. J. Cardiothorac. Surg.Home page
I. Dimarakis, N. A. Habib, and M. Y.A. Gordon
Adult bone marrow-derived stem cells and the injured heart: just the beginning?
Eur. J. Cardiothorac. Surg., November 1, 2005; 28(5): 665 - 676.
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 Arterioscler. Thromb. Vasc. Bio.Home page
J.E. Ferguson III, R. W. Kelley, and C. Patterson
Mechanisms of Endothelial Differentiation in Embryonic Vasculogenesis
Arterioscler. Thromb. Vasc. Biol., November 1, 2005; 25(11): 2246 - 2254.
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 PhysiologyHome page
H.-G. Kopp, S. T. Avecilla, A. T. Hooper, and S. Rafii
The Bone Marrow Vascular Niche: Home of HSC Differentiation and Mobilization
Physiology, October 1, 2005; 20(5): 349 - 356.
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 BloodHome page
E. Elsheikh, M. Uzunel, Z. He, J. Holgersson, G. Nowak, and S. Sumitran-Holgersson
Only a specific subset of human peripheral-blood monocytes has endothelial-like functional capacity
Blood, October 1, 2005; 106(7): 2347 - 2355.
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 Proc. Natl. Acad. Sci. USAHome page
V. Kouskoff, G. Lacaud, S. Schwantz, H. J. Fehling, and G. Keller
Sequential development of hematopoietic and cardiac mesoderm during embryonic stem cell differentiation
PNAS, September 13, 2005; 102(37): 13170 - 13175.
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 Arterioscler. Thromb. Vasc. Bio.Home page
M. B. Rookmaaker, M. C. Verhaar, C. J.M. Loomans, R. Verloop, E. Peters, P. E. Westerweel, T. Murohara, F. J.T. Staal, A. J. van Zonneveld, P. Koolwijk, et al.
CD34+ Cells Home, Proliferate, and Participate in Capillary Formation, and in Combination With CD34- Cells Enhance Tube Formation in a 3-Dimensional Matrix
Arterioscler. Thromb. Vasc. Biol., September 1, 2005; 25(9): 1843 - 1850.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
M. Kobayashi-Osaki, O. Ohneda, N. Suzuki, N. Minegishi, T. Yokomizo, S. Takahashi, K.-C. Lim, J. D. Engel, and M. Yamamoto
GATA Motifs Regulate Early Hematopoietic Lineage-Specific Expression of the Gata2 Gene
Mol. Cell. Biol., August 15, 2005; 25(16): 7005 - 7020.
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 BloodHome page
E. T. Zambidis, B. Peault, T. S. Park, F. Bunz, and C. I. Civin
Hematopoietic differentiation of human embryonic stem cells progresses through sequential hematoendothelial, primitive, and definitive stages resembling human yolk sac development
Blood, August 1, 2005; 106(3): 860 - 870.
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 BloodHome page
I. Kim, O. H. Yilmaz, and S. J. Morrison
CD144 (VE-cadherin) is transiently expressed by fetal liver hematopoietic stem cells
Blood, August 1, 2005; 106(3): 903 - 905.
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 BloodHome page
S. Sumanas, T. Jorniak, and S. Lin
Identification of novel vascular endothelial-specific genes by the microarray analysis of the zebrafish cloche mutants
Blood, July 15, 2005; 106(2): 534 - 541.
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