Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Science 3 May 1996:
Vol. 272. no. 5262, pp. 722 - 724
DOI: 10.1126/science.272.5262.722
Prev | Table of Contents | Next

Reports

In Vitro Development of Primitive and Definitive Erythrocytes from Different Precursors

Toru Nakano, * Hiroaki Kodama, Tasuku Honjo

During mouse embryogenesis the production of ``primitive'' erythrocytes (EryP) precedes the production of ``definitive'' erythrocytes (EryD) in parallel with the transition of the hematopoietic site from the yolk sac to the fetal liver. On a macrophage colony-stimulating factor-deficient stromal cell line OP9, mouse embryonic stem cells were shown to give rise to EryP and EryD sequentially with a time course similar to that seen in murine ontogeny. Studies of the different growth factor requirements and limiting dilution analysis of precursor frequencies indicate that most EryP and EryD probably developed from different precursors by way of distinct differentiation pathways.

T. Nakano and T. Honjo, Department of Medical Chemistry, Faculty of Medicine, Kyoto University, Yoshida, Sakyo-ku, Kyoto 606, Japan.
H. Kodama, Department of Anatomy, Ohu University School of Dentistry, Tomitamachi, Koriyama, Fukushima 963, Japan.
* Present address: Department of Molecular Cell Biology, Research Institute for Microbial Diseases, Osaka University, Yamada-Oka, Suita, Osaka 565, Japan.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Expression of angiotensin-converting enzyme (CD143) identifies and regulates primitive hemangioblasts derived from human pluripotent stem cells.
E. T. Zambidis, T. Soon Park, W. Yu, A. Tam, M. Levine, X. Yuan, M. Pryzhkova, and B. Peault (2008)
Blood 112, 3601-3614
   Abstract »    Full Text »    PDF »
Bloodlines of haematopoietic stem cell research in Japan.
H. Ema and H. Nakauchi (2008)
Phil Trans R Soc B 363, 2089-2097
   Abstract »    Full Text »    PDF »
Neural stem cells: involvement in adult neurogenesis and CNS repair.
H. Okano and K. Sawamoto (2008)
Phil Trans R Soc B 363, 2111-2122
   Abstract »    Full Text »    PDF »
{alpha}4-Integrin+ endothelium derived from primate embryonic stem cells generates primitive and definitive hematopoietic cells.
G. Shinoda, K. Umeda, T. Heike, M. Arai, A. Niwa, F. Ma, H. Suemori, H. Y. Luo, D. H. K. Chui, R. Torii, et al. (2007)
Blood 109, 2406-2415
   Abstract »    Full Text »    PDF »
Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures.
M. A. Vodyanik, J. A. Thomson, and I. I. Slukvin (2006)
Blood 108, 2095-2105
   Abstract »    Full Text »    PDF »
Notch Signaling Requires GATA-2 to Inhibit Myelopoiesis from Embryonic Stem Cells and Primary Hemopoietic Progenitors.
R. F. de Pooter, T. M. Schmitt, J. L. de la Pompa, Y. Fujiwara, S. H. Orkin, and J. C. Zuniga-Pflucker (2006)
J. Immunol. 176, 5267-5275
   Abstract »    Full Text »    PDF »
Multipotential differentiation ability of GATA-1-null erythroid-committed cells..
K. Kitajima, J. Zheng, H. Yen, D. Sugiyama, and T. Nakano (2006)
Genes & Dev. 20, 654-659
   Abstract »    Full Text »    PDF »
Redirecting differentiation of hematopoietic progenitors by a transcription factor, GATA-2.
K. Kitajima, M. Tanaka, J. Zheng, H. Yen, A. Sato, D. Sugiyama, H. Umehara, E. Sakai, and T. Nakano (2006)
Blood 107, 1857-1863
   Abstract »    Full Text »    PDF »
Designer blood: creating hematopoietic lineages from embryonic stem cells.
A. L. Olsen, D. L. Stachura, and M. J. Weiss (2006)
Blood 107, 1265-1275
   Abstract »    Full Text »    PDF »
Efficient and Repetitive Production of Hematopoietic and Endothelial Cells from Feeder-Free Monolayer Culture System of Primate Embryonic Stem Cells.
H. Zhang, K. Saeki, A. Kimura, K. Saeki, M. Nakahara, M. Doshi, Y. Kondo, T. Nakano, and A. Yuo (2006)
Biol Reprod 74, 295-306
   Abstract »    Full Text »    PDF »
Differential effects of GATA-1 on proliferation and differentiation of erythroid lineage cells.
J. Zheng, K. Kitajima, E. Sakai, T. Kimura, N. Minegishi, M. Yamamoto, and T. Nakano (2006)
Blood 107, 520-527
   Abstract »    Full Text »    PDF »
Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture.
S. Tada, T. Era, C. Furusawa, H. Sakurai, S. Nishikawa, M. Kinoshita, K. Nakao, T. Chiba, and S.-I. Nishikawa (2005)
Development 132, 4363-4374
   Abstract »    Full Text »    PDF »
GATA Motifs Regulate Early Hematopoietic Lineage-Specific Expression of the Gata2 Gene.
M. Kobayashi-Osaki, O. Ohneda, N. Suzuki, N. Minegishi, T. Yokomizo, S. Takahashi, K.-C. Lim, J. D. Engel, and M. Yamamoto (2005)
Mol. Cell. Biol. 25, 7005-7020
   Abstract »    Full Text »    PDF »
Hematopoietic differentiation of human embryonic stem cells progresses through sequential hematoendothelial, primitive, and definitive stages resembling human yolk sac development.
E. T. Zambidis, B. Peault, T. S. Park, F. Bunz, and C. I. Civin (2005)
Blood 106, 860-870
   Abstract »    Full Text »    PDF »
Graded Levels of GATA-1 Expression Modulate Survival, Proliferation, and Differentiation of Erythroid Progenitors.
X. Pan, O. Ohneda, K. Ohneda, F. Lindeboom, F. Iwata, R. Shimizu, M. Nagano, N. Suwabe, S. Philipsen, K.-C. Lim, et al. (2005)
J. Biol. Chem. 280, 22385-22394
   Abstract »    Full Text »    PDF »
Embryonic Stem Cells: Prospects for Developmental Biology and Cell Therapy.
A. M. Wobus and K. R. Boheler (2005)
Physiol Rev 85, 635-678
   Abstract »    Full Text »    PDF »
Human embryonic stem cell-derived CD34+ cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential.
M. A. Vodyanik, J. A. Bork, J. A. Thomson, and I. I. Slukvin (2005)
Blood 105, 617-626
   Abstract »    Full Text »    PDF »
Induction of Epithelial Progenitors In Vitro from Mouse Embryonic Stem Cells and Application for Reconstruction of Damaged Cornea in Mice.
R. Homma, H. Yoshikawa, M. Takeno, M. S. Kurokawa, C. Masuda, E. Takada, K. Tsubota, S. Ueno, and N. Suzuki (2004)
Invest. Ophthalmol. Vis. Sci. 45, 4320-4326
   Abstract »    Full Text »    PDF »
Differentiation status dependent function of FOG-1.
M. Tanaka, J. Zheng, K. Kitajima, K. Kita, H. Yoshikawa, and T. Nakano (2004)
Genes Cells 9, 1213-1226
   Abstract »    Full Text »    PDF »
Directed differentiation and mass cultivation of pure erythroid progenitors from mouse embryonic stem cells.
S. Carotta, S. Pilat, A. Mairhofer, U. Schmidt, H. Dolznig, P. Steinlein, and H. Beug (2004)
Blood 104, 1873-1880
   Abstract »    Full Text »    PDF »
Cross Talk between Retinoic Acid Signaling and Transcription Factor GATA-2.
S. Tsuzuki, K. Kitajima, T. Nakano, A. Glasow, A. Zelent, and T. Enver (2004)
Mol. Cell. Biol. 24, 6824-6836
   Abstract »    Full Text »    PDF »
Development of primitive and definitive hematopoiesis from nonhuman primate embryonic stem cells in vitro.
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. (2004)
Development 131, 1869-1879
   Abstract »    Full Text »    PDF »
VEGF-A165 augments erythropoietic development from human embryonic stem cells.
C. Cerdan, A. Rouleau, and M. Bhatia (2004)
Blood 103, 2504-2512
   Abstract »    Full Text »    PDF »
Production of functional platelets by differentiated embryonic stem (ES) cells in vitro.
T.-T. Fujimoto, S. Kohata, H. Suzuki, H. Miyazaki, and K. Fujimura (2003)
Blood 102, 4044-4051
   Abstract »    Full Text »    PDF »
Generation and genetic modification of dendritic cells derived from mouse embryonic stem cells.
S. Senju, S. Hirata, H. Matsuyoshi, M. Masuda, Y. Uemura, K. Araki, K.-i. Yamamura, and Y. Nishimura (2003)
Blood 101, 3501-3508
   Abstract »    Full Text »    PDF »
Recombination signal sequence-binding protein Jkappa alters mesodermal cell fate decisions by suppressing cardiomyogenesis.
T. Schroeder, S. T. Fraser, M. Ogawa, S. Nishikawa, C. Oka, G. W. Bornkamm, S.-I. Nishikawa, T. Honjo, and U. Just (2003)
PNAS 100, 4018-4023
   Abstract »    Full Text »    PDF »
Embryonic Stem Cells: New Possible Therapy for Degenerative Diseases That Affect Elderly People.
Q. He, J. Li, E. Bettiol, and M. E. Jaconi (2003)
J. Gerontol. A Biol. Sci. Med. Sci. 58, M279-287
   Abstract »    Full Text »    PDF »
The role of nuclear factor-kappa B essential modulator (NEMO) in B cell development and survival.
S. Kim, R. N. A. La Motte-Mohs, D. Rudolph, J. C. Zuniga-Pflucker, and T. W. Mak (2003)
PNAS 100, 1203-1208
   Abstract »    Full Text »    PDF »
Aberrant iron accumulation and oxidized status of erythroid-specific delta -aminolevulinate synthase (ALAS2)-deficient definitive erythroblasts.
H. Harigae, O. Nakajima, N. Suwabe, H. Yokoyama, K. Furuyama, T. Sasaki, M. Kaku, M. Yamamoto, and S. Sassa (2003)
Blood 101, 1188-1193
   Abstract »    Full Text »    PDF »
Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo.
H. K. A. Mikkola, Y. Fujiwara, T. M. Schlaeger, D. Traver, and S. H. Orkin (2003)
Blood 101, 508-516
   Abstract »    Full Text »    PDF »
Expression and function of CD105 during the onset of hematopoiesis from Flk1+ precursors.
S. K. Cho, A. Bourdeau, M. Letarte, and J. C. Zuniga-Pflucker (2001)
Blood 98, 3635-3642
   Abstract »    Full Text »    PDF »
Erythropoietin (Epo) and EpoR expression and 2 waves of erythropoiesis.
R. Lee, N. Kertesz, S. B. Joseph, A. Jegalian, and H. Wu (2001)
Blood 98, 1408-1415
   Abstract »    Full Text »    PDF »
Stem Cells: A Journey into a New Frontier.
B. E. PETERSEN and N. TERADA (2001)
J. Am. Soc. Nephrol. 12, 1773-1780
   Full Text »    PDF »
Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis.
J. Palis, R. J. Chan, A. Koniski, R. Patel, M. Starr, and M. C. Yoder (2001)
PNAS 98, 4528-4533
   Abstract »    Full Text »    PDF »
Evidence for the presence of murine primitive megakarycytopoiesis in the early yolk sac.
M.-j. Xu, S. Matsuoka, F.-C. Yang, Y. Ebihara, A. Manabe, R. Tanaka, M. Eguchi, S. Asano, T. Nakahata, and K. Tsuji (2001)
Blood 97, 2016-2022
   Abstract »    Full Text »    PDF »
Vascular endothelial growth factor synergistically enhances bone morphogenetic protein-4-dependent lymphohematopoietic cell generation from embryonic stem cells in vitro.
N. Nakayama, J. Lee, and L. Chiu (2000)
Blood 95, 2275-2283
   Abstract »    Full Text »    PDF »
Regulated expression of P210 Bcr-Abl during embryonic stem cell differentiation stimulates multipotential progenitor expansion and myeloid cell fate.
T. Era and O. N. Witte (2000)
PNAS 97, 1737-1742
   Abstract »    Full Text »    PDF »
Characterization of hematopoietic lineage-specific gene expression by ES cell in vitro differentiation induction system.
T. Era, T. Takagi, T. Takahashi, J.-C. Bories, and T. Nakano (2000)
Blood 95, 870-878
   Abstract »    Full Text »    PDF »
Functional characterization of B lymphocytes generated in vitro from embryonic stem cells.
S. K. Cho, T. D. Webber, J. R. Carlyle, T. Nakano, S. M. Lewis, and J. C. Zuniga-Pflucker (1999)
PNAS 96, 9797-9802
   Abstract »    Full Text »    PDF »
bcl-x Prevents Apoptotic Cell Death of Both Primitive and Definitive Erythrocytes at the End of Maturation.
N. Motoyama, T. Kimura, T. Takahashi, T. Watanabe, and T. Nakano (1999)
J. Exp. Med. 189, 1691-1698
   Abstract »    Full Text »    PDF »
Expression Trapping: Identification of Novel Genes Expressed in Hematopoietic and Endothelial Lineages by Gene Trapping in ES Cells.
W. L. Stanford, G. Caruana, K. A. Vallis, M. Inamdar, M. Hidaka, V. L. Bautch, and A. Bernstein (1998)
Blood 92, 4622-4631
   Abstract »    Full Text »    PDF »
GATA-1 Regulates Growth and Differentiation of Definitive Erythroid Lineage Cells During In Vitro ES Cell Differentiation.
N. Suwabe, S. Takahashi, T. Nakano, and M. Yamamoto (1998)
Blood 92, 4108-4118
   Abstract »    Full Text »    PDF »
Overexpression of HOX11 Leads to the Immortalization of Embryonic Precursors With Both Primitive and Definitive Hematopoietic Potential.
G. Keller, C. Wall, A. Z.C. Fong, T. S. Hawley, and R. G. Hawley (1998)
Blood 92, 877-887
   Abstract »    Full Text »    PDF »
Growth-Supporting Activities of Fibronectin on Hematopoietic Stem/Progenitor Cells In Vitro and In Vivo: Structural Requirement for Fibronectin Activities of CS1 and Cell-Binding Domains.
T. Yokota, K. Oritani, H. Mitsui, K. Aoyama, J. Ishikawa, H. Sugahara, I. Matsumura, S. Tsai, Y. Tomiyama, Y. Kanakura, et al. (1998)
Blood 91, 3263-3272
   Abstract »    Full Text »    PDF »
Natural Killer and B-Lymphoid Potential in CD34+ Cells Derived From Embryonic Stem Cells Differentiated in the Presence of Vascular Endothelial Growth Factor.
N. Nakayama, I. Fang, and G. Elliott (1998)
Blood 91, 2283-2295
   Abstract »    Full Text »    PDF »
Expansion in vitro of adult murine hematopoietic stem cells with transplantable lympho-myeloid reconstituting ability.
C. L. Miller and C. J. Eaves (1997)
PNAS 94, 13648-13653
   Abstract »    Full Text »    PDF »
Developmental regulation of erythropoietin and erythropoiesis.
K. M. Moritz, G. B. Lim, and E. M. Wintour (1997)
Am J Physiol Regulatory Integrative Comp Physiol 273, R1829-R1844
   Abstract »    Full Text »    PDF »
Development of Osteoclasts From Embryonic Stem Cells Through a Pathway That Is c-fms but not c-kit Dependent.
T. Yamane, T. Kunisada, H. Yamazaki, T. Era, T. Nakano, and S.-I. Hayashi (1997)
Blood 90, 3516-3523
   Abstract »    Full Text »    PDF »
Hemato-lymphoid in vivo reconstitution potential of subpopulations derived from in vitro differentiated embryonic stem cells.
A. J. Potocnik, H. Kohler, and K. Eichmann (1997)
PNAS 94, 10295-10300
   Abstract »    Full Text »    PDF »
Engraftment of Embryonic Hematopoietic Cells in Conditioned Newborn Recipients.
M. C. Yoder and K. Hiatt (1997)
Blood 89, 2176-2183
   Abstract »    Full Text »    PDF »
Thrombopoietin Enhances Proliferation and Differentiation of Murine Yolk Sac Erythroid Progenitors.
T. Era, T. Takahashi, K. Sakai, K. Kawamura, and T. Nakano (1997)
Blood 89, 1207-1213
   Abstract »    Full Text »    PDF »
GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene.
Q Long, A Meng, H Wang, J. Jessen, M. Farrell, and S Lin (1997)
Development 124, 4105-4111
   Abstract »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)