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Development, Vol 125, Issue 9 1747-1757, Copyright © 1998 by Company of Biologists

JOURNAL ARTICLES

Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages

SI Nishikawa, S Nishikawa, M Hirashima, N Matsuyoshi and H Kodama
Department of Molecular Genetics, Faculty of Medicine, Kyoto University, Kyoto, Japan. snishika@virus1.kyoto-u.ac.jp

Totipotent murine ES cells have an enormous potential for the study of cell specification. Here we demonstrate that ES cells can differentiate to hemopoietic cells through the proximal lateral mesoderm, merely upon culturing in type IV collagen-coated dishes. Separation of the Flk1+ mesoderm from other cell lineages was critical for hemopoietic cell differentiation, whereas formation of the embryoid body was not. Since the two-dimensionally spreading cells can be monitored easily in real time, this culture system will greatly facilitate the study of the mechanisms involved in the cell specification to mesoderm, endothelial, and hemopoietic cells. In the culture of ES cells, however, lineages and stages of differentiating cells can only be defined by their own characteristics. We showed that a combination of monoclonal antibodies against E-cadherin, Flk1/KDR, PDGF receptor(alpha), VE-cadherin, CD45 and Ter119 was sufficient to define most intermediate stages during differentiation of ES cells to blood cells. Using this culture system and surface markers, we determined the following order for blood cell differentiation: ES cell (E-cadherin+Flk1-PDGFRalpha-), proximal lateral mesoderm (E-cadherin-Flk1+VE-cadherin-), progenitor with hemoangiogenic potential (Flk1+VE-cadherin+CD45-), hemopoietic progenitor (CD45+c-Kit+) and mature blood cells (c-Kit-CD45+ or Ter119+), though direct differentiation of blood cells from the Flk1+VE-cadherin- stage cannot be ruled out. Not only the VE-cadherin+CD45- population generated from ES cells but also those directly sorted from the yolk sac of 9.5 dpc embryos have a potential to give rise to hemopoietic cells. Progenitors with hemoangiogenic potential were identified in both the Flk1+VE-cadherin- and Flk1+VE-cadherin+ populations by the single cell deposition experiment. This line of evidence implicates Flk1+VE-cadherin+ cells as a diverging point of hemopoietic and endothelial cell lineages.
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Y. J. Liu, S. H. Lu, B. Xu, R. C. Yang, Q. Ren, B. Liu, B. Li, M. Lu, F. Y. Yan, Z. B. Han, et al.
Hemangiopoietin, a novel human growth factor for the primitive cells of both hematopoietic and endothelial cell lineages
Blood, June 15, 2004; 103(12): 4449 - 4456.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
K. Umeda, T. Heike, M. Yoshimoto, M. Shiota, H. Suemori, H. Y. Luo, D. H. K. Chui, R. Torii, M. Shibuya, N. Nakatsuji, et al.
Development of primitive and definitive hematopoiesis from nonhuman primate embryonic stem cells in vitro
Development, April 15, 2004; 131(8): 1869 - 1879.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
A. Kubo, K. Shinozaki, J. M. Shannon, V. Kouskoff, M. Kennedy, S. Woo, H. J. Fehling, and G. Keller
Development of definitive endoderm from embryonic stem cells in culture
Development, April 1, 2004; 131(7): 1651 - 1662.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
P. Magnusson, C. Rolny, L. Jakobsson, C. Wikner, Y. Wu, D. J. Hicklin, and L. Claesson-Welsh
Deregulation of Flk-1/vascular endothelial growth factor receptor-2 in fibroblast growth factor receptor-1-deficient vascular stem cell development
J. Cell Sci., March 15, 2004; 117(8): 1513 - 1523.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
B. Gottgens, C. Broccardo, M.-J. Sanchez, S. Deveaux, G. Murphy, J. R. Gothert, E. Kotsopoulou, S. Kinston, L. Delaney, S. Piltz, et al.
The scl +18/19 Stem Cell Enhancer Is Not Required for Hematopoiesis: Identification of a 5' Bifunctional Hematopoietic-Endothelial Enhancer Bound by Fli-1 and Elf-1
Mol. Cell. Biol., March 1, 2004; 24(5): 1870 - 1883.
[Abstract] [Full Text] [PDF]

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 BloodHome page
D. S. Kaufman, R. L. Lewis, E. T. Hanson, R. Auerbach, J. Plendl, and J. A. Thomson
Functional endothelial cells derived from rhesus monkey embryonic stem cells
Blood, February 15, 2004; 103(4): 1325 - 1332.
[Abstract] [Full Text] [PDF]

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 BloodHome page
Z. Wang, K. Cohen, Y. Shao, P. Mole, D. Dombkowski, and D. T. Scadden
Ephrin receptor, EphB4, regulates ES cell differentiation of primitive mammalian hemangioblasts, blood, cardiomyocytes, and blood vessels
Blood, January 1, 2004; 103(1): 100 - 109.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
M. Gering, Y. Yamada, T. H. Rabbitts, and R. K. Patient
Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1
Development, December 22, 2003; 130(25): 6187 - 6199.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
I. Nobuhisa, M. Takizawa, S. Takaki, H. Inoue, K. Okita, M. Ueno, K. Takatsu, and T. Taga
Regulation of Hematopoietic Development in the Aorta-Gonad-Mesonephros Region Mediated by Lnk Adaptor Protein
Mol. Cell. Biol., December 1, 2003; 23(23): 8486 - 8494.
[Abstract] [Full Text] [PDF]

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 BloodHome page
Y. Guo, R. Chan, H. Ramsey, W. Li, X. Xie, W. C. Shelley, J. P. Martinez-Barbera, B. Bort, K. Zaret, M. Yoder, et al.
The homeoprotein Hex is required for hemangioblast differentiation
Blood, October 1, 2003; 102(7): 2428 - 2435.
[Abstract] [Full Text] [PDF]

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B. M. Nadin, M. A. Goodell, and K. K. Hirschi
Phenotype and hematopoietic potential of side population cells throughout embryonic development
Blood, October 1, 2003; 102(7): 2436 - 2443.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
Y. Toyooka, N. Tsunekawa, R. Akasu, and T. Noce
Embryonic stem cells can form germ cells in vitro
PNAS, September 30, 2003; 100(20): 11457 - 11462.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
M. J. Ferkowicz, M. Starr, X. Xie, W. Li, S. A. Johnson, W. C. Shelley, P. R. Morrison, and M. C. Yoder
CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo
Development, September 15, 2003; 130(18): 4393 - 4403.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
H. J. Fehling, G. Lacaud, A. Kubo, M. Kennedy, S. Robertson, G. Keller, and V. Kouskoff
Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation
Development, September 1, 2003; 130(17): 4217 - 4227.
[Abstract] [Full Text] [PDF]

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 BloodHome page
R. F. de Pooter, S. K. Cho, J. R. Carlyle, and J. C. Zuniga-Pflucker
In vitro generation of T lymphocytes from embryonic stem cell-derived prehematopoietic progenitors
Blood, September 1, 2003; 102(5): 1649 - 1653.
[Abstract] [Full Text] [PDF]

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N. Minegishi, N. Suzuki, T. Yokomizo, X. Pan, T. Fujimoto, S. Takahashi, T. Hara, A. Miyajima, S.-i. Nishikawa, and M. Yamamoto
Expression and domain-specific function of GATA-2 during differentiation of the hematopoietic precursor cells in midgestation mouse embryos
Blood, August 1, 2003; 102(3): 896 - 905.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
N. Rosenthal
Prometheus's Vulture and the Stem-Cell Promise
N. Engl. J. Med., July 17, 2003; 349(3): 267 - 274.
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J. E. Ohm, D. I. Gabrilovich, G. D. Sempowski, E. Kisseleva, K. S. Parman, S. Nadaf, and D. P. Carbone
VEGF inhibits T-cell development and may contribute to tumor-induced immune suppression
Blood, June 15, 2003; 101(12): 4878 - 4886.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
N. Nakayama, D. Duryea, R. Manoukian, G. Chow, and C.-y. E. Han
Macroscopic cartilage formation with embryonic stem-cell-derived mesodermal progenitor cells
J. Cell Sci., May 15, 2003; 116(10): 2015 - 2028.
[Abstract] [Full Text] [PDF]

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 BloodHome page
S. Wong, J. McLaughlin, D. Cheng, and O. N. Witte
Cell context-specific effects of the BCR-ABL oncogene monitored in hematopoietic progenitors
Blood, May 15, 2003; 101(10): 4088 - 4097.
[Abstract] [Full Text] [PDF]

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 Cardiovasc ResHome page
S. G. Nir, R. David, M. Zaruba, W.-M. Franz, and J. Itskovitz-Eldor
Human embryonic stem cells for cardiovascular repair
Cardiovasc Res, May 1, 2003; 58(2): 313 - 323.
[Abstract] [Full Text] [PDF]

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 Cardiovasc ResHome page
R. Passier and C. Mummery
Origin and use of embryonic and adult stem cells in differentiation and tissue repair
Cardiovasc Res, May 1, 2003; 58(2): 324 - 335.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
M. Sone, H. Itoh, J. Yamashita, T. Yurugi-Kobayashi, Y. Suzuki, Y. Kondo, A. Nonoguchi, N. Sawada, K. Yamahara, K. Miyashita, et al.
Different Differentiation Kinetics of Vascular Progenitor Cells in Primate and Mouse Embryonic Stem Cells
Circulation, April 29, 2003; 107(16): 2085 - 2088.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
M. L. S. Sequeira Lopez, D. R. Chernavvsky, T. Nomasa, L. Wall, M. Yanagisawa, and R. A. Gomez
The embryo makes red blood cell progenitors in every tissue simultaneously with blood vessel morphogenesis
Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2003; 284(4): R1126 - R1137.
[Abstract] [Full Text] [PDF]

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T. Yurugi-Kobayashi, H. Itoh, J. Yamashita, K. Yamahara, H. Hirai, T. Kobayashi, M. Ogawa, S. Nishikawa, S.-I. Nishikawa, and K. Nakao
Effective contribution of transplanted vascular progenitor cells derived from embryonic stem cells to adult neovascularization in proper differentiation stage
Blood, April 1, 2003; 101(7): 2675 - 2678.
[Abstract] [Full Text] [PDF]

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M. Hirashima, M. Ogawa, S. Nishikawa, K. Matsumura, K. Kawasaki, M. Shibuya, and S.-I. Nishikawa
A chemically defined culture of VEGFR2+ cells derived from embryonic stem cells reveals the role of VEGFR1 in tuning the threshold for VEGF in developing endothelial cells
Blood, March 15, 2003; 101(6): 2261 - 2267.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
M. Walmsley, A. Ciau-Uitz, and R. Patient
Adult and embryonic blood and endothelium derive from distinct precursor populations which are differentially programmed by BMP in Xenopus
Development, March 14, 2003; 129(24): 5683 - 5695.
[Abstract] [Full Text] [PDF]

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A. Damert, L. Miquerol, M. Gertsenstein, W. Risau, and A. Nagy
Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation
Development, March 6, 2003; 129(8): 1881 - 1892.
[Abstract] [Full Text] [PDF]

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 Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
Q. He, J. Li, E. Bettiol, and M. E. Jaconi
Embryonic Stem Cells: New Possible Therapy for Degenerative Diseases That Affect Elderly People
J. Gerontol. A Biol. Sci. Med. Sci., March 1, 2003; 58(3): M279 - 287.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
J.-L. Hillebrands, F. A. Klatter, and J. Rozing
Origin of Vascular Smooth Muscle Cells and the Role of Circulating Stem Cells in Transplant Arteriosclerosis
Arterioscler Thromb Vasc Biol, March 1, 2003; 23(3): 380 - 387.
[Abstract] [Full Text] [PDF]


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