The embryonic origins of human haematopoiesis
Caroline J. Marshall,
Adrian J. Thrasher,
Caroline J. Marshall
Molecular Immunology Unit, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK
Search for more papers by this authorAdrian J. Thrasher
Molecular Immunology Unit, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK
Search for more papers by this authorCaroline J. Marshall,
Adrian J. Thrasher,
Caroline J. Marshall
Molecular Immunology Unit, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK
Search for more papers by this authorAdrian J. Thrasher
Molecular Immunology Unit, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK
Search for more papers by this author Caroline Marshall, Molecular Immunology Unit, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK. E-mail: [email protected]
References
- Asahara, T., Murohara, T., Sullivan, A., Van Der Silver, M.Z.R., Li, T., Witzenbichler, B., Schatteman, G., Isner, J.M. (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science, 275, 964–967.DOI: 10.1126/science.275.5302.964
- Bernex, F., De Sepulveda, P., Kress, C., Elbaz, C., Delouis, C., Panthier, J.J. (1996) Spatial and temporal patterns of c-kit-expressing cells in WlacZ/+ and WlacZ/WlacZ mouse embryos. Development, 122, 3023–3033.
- Bhatia, M., Bonnet, D., Wu, D., Murdoch, B., Wrana, J., Gallacher, L., Dick, J.E. (1999) Bone morphogenetic proteins regulate the developmental program of human hematopoietic stem cells. Journal of Experimental Medicine, 189, 1139–1148.
- Castilla, L.H., Wijmenga, C., Wang, Q., Stacy, T., Speck, N.A., Eckhaus, M., Marin-Padilla, M., Collins, F.S., Wynshaw-Boris, A., Liu, P.P. (1996) Failure of embryonic hematopoiesis and lethal hemorrhages in mouse embryos heterozygous for a knocked-in leukemia gene CBFB-MYH11. Cell, 87, 687–696.
- Chen, D., Ji, X., Harris, M.A., Feng, J.Q., Karsenty, G., Celeste, A.J., Rosen, V., Mundy, G.R., Harris, S.E. (1998) Differential roles for bone morphogenetic protein (BMP) receptor type IB and IA in differentiation and specification of mesenchymal precursor cells to osteoblast and adipocyte lineages. Journal of Cell Biology, 142, 295–305.
- Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J.C., Keller, G. (1998) A common precursor for hematopoietic and endothelial cells. Development, 125, 725–732.
- Cormier, F., De Paz, P., Dieterlen-Lievre, F. (1986) In vitro detection of cells with monocytic potentiality in the wall of the chick embryo aorta. Developmental Biology, 118, 167–175.
- Cortes, F., Deschaseaux, F., Uchida, N., Labastie, M.C., Friera, A.M., He, D., Charbord, P., Peault, B. (1999) HCA, an immunoglobulin-like adhesion molecule present on the earliest human hematopoietic precursor cells, is also expressed by stromal cells in blood-forming tissues. Blood, 93, 826–837.
- Crossin, K.L., Hoffman, S., Grumet, M., Thiery, J.P., Edelman, G.M. (1986) Site-restricted expression of cytotactin during development of the chicken embryo. Journal of Cell Biology, 102, 1917–1930.
- Cumano, A., Dieterlen-Lievre, F., Godin, I. (1996) Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell, 86, 907–916.
- Delassus, S., Titley, I., Enver, T. (1999) Functional and molecular analysis of hematopoietic progenitors derived from the aorta-gonad-mesonephros region of the mouse embryo. Blood, 94, 1495–1503.
- Dickson, M.C., Martin, J.S., Cousins, F.M., Kulkarni, A.B., Karlsson, S., Akhurst, R.J. (1995) Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development, 121, 1845–1854.
- Dieterlen-Lievre, F. (1975) On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. Journal of Embryological Experimental Morphology, 33, 607–619.
- Dzierzak, E. & Medvinsky, A. (1995) Mouse embryonic hematopoiesis. Trends in Genetics, 11, 359–366.
- Eichmann, A., Corbel, C., Nataf, V., Vaigot, P., Breant, C., Le Douarin, N.M. (1997) Ligand-dependent development of the endothelial and hemopoietic lineages from embryonic mesodermal cells expressing vascular endothelial growth factor receptor 2. Proceedings of the National Academy of Sciences of the United States of America, 94, 5141–5146.
- Elefanty, A.G., Robb, L., Birner, R., Begley, C.G. (1997) Hematopoietic-specific genes are not induced during in vitro differentiation of scl-null embryonic stem cells. Blood, 90, 1435–1447.
- Faloon, P., Arentson, E., Kazarov, A., Deng, C.X., Porcher, C., Orkin, S., Choi, K. (2000) Basic fibroblast growth factor positively regulates hematopoietic development [In Process Citation]. Development, 127, 1931–1941.
- Galmiche, M.C., Koteliansky, V.E., Briere, J., Herve, P., Charbord, P. (1993) Stromal cells from human long-term marrow cultures are mesenchymal cells that differentiate following a vascular smooth muscle differentiation pathway. Blood, 82, 66–76.
- Garcia-Porrero, J.A., Manaia, A., Jimeno, J., Lasky, L.L., Dieterlen-Lievre, F., Godin, I.E. (1998) Antigenic profiles of endothelial and hemopoietic lineages in murine intraembryonic hemogenic sites. Developmental Comparative Immunology, 22, 303–319.DOI: 10.1016/s0145-305x(98)00006-8
- Gering, M., Rodaway, A.R., Gottgens, B., Patient, R.K., Green, A.R. (1998) The SCL gene specifies haemangioblast development from early mesoderm. EMBO Journal, 17, 4029–4045.
- Hall, B.K. & Miyake, T. (1995) Divide, accumulate, differentiate: cell condensation in skeletal development revisited. International Journal of Developmental Biology, 39, 881–893.
- Hamaguchi, I., Huang, X.L., Takakura, N., Tada, J., Yamaguchi, Y., Kodama, H., Suda, T. (1999) In vitro hematopoietic and endothelial cell development from cells expressing TEK receptor in murine aorta-gonad-mesonephros region. Blood, 93, 1549–1556.
- Hashiyama, M., Iwama, A., Ohshiro, K., Kurozumi, K., Yasunaga, K., Shimizu, Y., Masuho, Y., Matsuda, I., Yamaguchi, N., Suda, T. (1996) Predominant expression of a receptor tyrosine kinase, TIE, in hematopoietic stem cells and B cells. Blood, 87, 93–101.
- Hogan, B.L. (1996) Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes and Development, 10, 1580–1594.
- Huber, T.L., Zhou, Y., Mead, P.E., Zon, L.I. (1998) Cooperative effects of growth factors involved in the induction of hematopoietic mesoderm. Blood, 92, 4128–4137.
- Hungerford, J.E., Owens, G.K., Argraves, W.S., Little, C.D. (1996) Development of the aortic vessel wall as defined by vascular smooth muscle and extracellular matrix markers. Developmental Biology, 178, 375–392.DOI: 10.1006/dbio.1996.0225
- Huyhn, A., Dommergues, M., Izac, B., Croisille, L., Katz, A., Vainchenker, W., Coulombel, L. (1995) Characterization of hematopoietic progenitors from human yolk sacs and embryos. Blood, 86, 4474–4485.
- Jaffredo, T., Gautier, R., Eichmann, A., Dieterlen-Lievre, F. (1998) Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development, 125, 4575–4583.
- Johansson, B.M. & Wiles, M.V. (1995) Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Molecular Cell Biology, 15, 141–151.
- Jones, C.M. & Smith, J.C. (1998) Establishment of a BMP-4 morphogen gradient by long-range inhibition. Developmental Biology, 194, 12–17.DOI: 10.1006/dbio.1997.8752
- Labastie, M.C., Cortes, F., Romeo, P.H., Dulac, C., Peault, B. (1998) Molecular identity of hematopoietic precursor cells emerging in the human embryo. Blood, 92, 3624–3635.
-
Lee, M.H.,
Javed, A.,
Kim, H.J.,
Shin, H.I.,
Gutierrez, S.,
Choi, J.Y.,
Rosen, V.,
Stein, J.L.,
Van Wijnen, A.J.,
Stein, G.S.,
Lian, J.B.,
Ryoo, H.M. (1999) Transient upregulation of CBFA1 in response to bone morphogenetic protein-2 and transforming growth factor beta1 in C2C12 myogenic cells coincides with suppression of the myogenic phenotype but is not sufficient for osteoblast differentiation.
Journal of Cell Biochemistry, 73, 114–125.
10.1002/(SICI)1097-4644(19990401)73:1<114::AID-JCB13>3.0.CO;2-M CAS PubMed Web of Science® Google Scholar
- Maeno, M., Mead, P.E., Kelley, C., Xu, R.H., Kung, H.F., Suzuki, A., Ueno, N., Zon, L.I. (1996) The role of BMP-4 and GATA-2 in the induction and differentiation of hematopoietic mesoderm in Xenopus laevis. Blood, 88, 1965–1972.
- Manaia, A., Lemarchandel, V., Klaine, M., Max-Audit, I., Romeo, P., Dieterlen-Lievre, F., Godin, I. (2000) Lmo2 and GATA-3 associated expression in intraembryonic hemogenic sites. Development, 127, 643–653.
-
Marshall, C.J.,
Moore, R.L.,
Thorogood, P.,
Brickell, P.M.,
Kinnon, C.,
Thrasher, A.J. (1999) Detailed characterization of the human aorta-gonad-mesonephros region reveals morphological polarity resembling a hematopoietic stromal layer.
Developmental Dynamics, 215, 139–147
.
10.1002/(SICI)1097-0177(199906)215:2<139::AID-DVDY6>3.0.CO;2-# CAS PubMed Web of Science® Google Scholar
- Marshall, C.J., Kinnon, C., Thrasher, A.J. (2000) Polarized expression of bone morphogenetic protein-4 in the human aorta-gonad-mesonephros region. Blood, 96, 1591–1593.
- Mead, P.E., Kelley, C.M., Hahn, P.S., Piedad, O., Zon, L.I. (1998) SCL specifies hematopoietic mesoderm in Xenopus embryos. Development, 125, 2611–2620.
- Medvinsky, A. & Dzierzak, E. (1996) Definitive hematopoiesis is autonomously initiated by the AGM region. Cell, 86, 897–906.
- Medvinsky, A.L., Samoylina, N.L., Muller, A.M., Dzierzak, E.A. (1993) An early pre-liver intraembryonic source of CFU-S in the developing mouse. Nature, 364, 64–67.
- Medvinsky, A.L., Gan, O.I., Semenova, M.L., Samoylina, N.L. (1996) Development of day-8 colony-forming unit-spleen hematopoietic progenitors during early murine embryogenesis: spatial and temporal mapping. Blood, 87, 557–566.
- Muller, A.M., Medvinsky, A., Strouboulis, J., Grosveld, F., Dzierzak, E. (1994) Development of hematopoietic stem cell activity in the mouse embryo. Immunity, 1, 291–301.
- Neubuser, A., Peters, H., Balling, R., Martin, G.R. (1997) Antagonistic interactions between FGF and BMP signaling pathways: a mechanism for positioning the sites of tooth formation. Cell, 90, 247–255.
- Nishikawa, S.I., Nishikawa, S., Hirashima, M., Matsuyoshi, N., Kodama, H. (1998) Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development, 125, 1747–1757.
- North, T., Gu, T.L., Stacy, T., Wang, Q., Howard, L., Binder, M., Marin-Padilla, M., Speck, N.A. (1999) Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development, 126, 2563–2575.
- Ohta, M., Sakai, T., Saga, Y., Aizawa, S., Saito, M. (1998) Suppression of hematopoietic activity in tenascin-C-deficient mice. Blood, 91, 4074–4083.
- Okuda, T., Van Deursen, J., Hiebert, S.W., Grosveld, G., Downing, J.R. (1996) AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell, 84, 321–330.
- Oshima, M., Oshima, H., Taketo, M.M. (1996) TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Developmental Biology, 179, 297–302.DOI: 10.1006/dbio.1996.0259
- Otto, F., Thornell, A.P., Crompton, T., Denzel, A., Gilmour, K.C., Rosewell, I.R., Stamp, G.W., Beddington, R.S., Mundlos, S., Olsen, B.R., Selby, P.B., Owen, M.J. (1997) Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development [see comments]. Cell, 89, 765–771.
- Pardanaud, L. & Dieterlen-Lievre, F. (1999) Manipulation of the angiopoietic/hemangiopoietic commitment in the avian embryo. Development, 126, 617–627.
- Pardanaud, L., Luton, D., Prigent, M., Bourcheix, L.M., Catala, M., Dieterlen-Lievre, F. (1996) Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development, 122, 1363–1371.
- Porcher, C., Swat, W., Rockwell, K., Fujiwara, Y., Alt, F.W., Orkin, S.H. (1996) The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell, 86, 47–57.
- Prieto, A.L., Jones, F.S., Cunningham, B.A., Crossin, K.L., Edelman, G.M. (1990) Localization during development of alternatively spliced forms of cytotactin mRNA by in situ hybridization. Journal of Cell Biology, 111, 685–698.
- Puri, M.C., Rossant, J., Alitalo, K., Bernstein, A., Partanen, J. (1995) The receptor tyrosine kinase TIE is required for integrity and survival of vascular endothelial cells. EMBO Journal, 14, 5884–5891.
- Ruch, J.V., Lesot, H., Begue-Kirn, C. (1995) Odontoblast differentiation. International Journal of Developmental Biology, 39, 51–68.
- Sanchez, M.J., Holmes, A., Miles, C., Dzierzak, E. (1996) Characterization of the first definitive hematopoietic stem cells in the AGM and liver of the mouse embryo. Immunity, 5, 513–525.
- Sato, T.N., Tozawa, Y., Deutsch, U., Wolburg-Buchholz, K., Fujiwara, Y., Gendron-Maguire, M., Gridley, T., Wolburg, H., Risau, W., Qin, Y. (1995) Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature, 376, 70–74.
- Seiffert, M., Beck, S.C., Schermutzki, F., Muller, C.A., Erickson, H.P., Klein, G. (1998) Mitogenic and adhesive effects of tenascin-C on human hematopoietic cells are mediated by various functional domains. Matrix Biology, 17, 47–63.
- Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.F., Breitman, M.L., Schuh, A.C. (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature, 376, 62–66.
- Shalaby, F., Ho, J., Stanford, W.L., Fischer, K.D., Schuh, A.C., Schwartz, L., Bernstein, A., Rossant, J. (1997) A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell, 89, 981–990.
- Shivdasani, R.A., Mayer, E.L., Orkin, S.H. (1995) Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature, 373, 432–434.
- Sitnicka, E., Ruscetti, F.W., Priestley, G.V., Wolf, N.S., Bartelmez, S.H. (1996) Transforming growth factor beta 1 directly and reversibly inhibits the initial cell divisions of long-term repopulating hematopoietic stem cells. Blood, 88, 82–88.
- Takakura, N., Huang, X.L., Naruse, T., Hamaguchi, I., Dumont, D.J., Yancopoulos, G.D., Suda, T. (1998) Critical role of the TIE2 endothelial cell receptor in the development of definitive hematopoiesis. Immunity, 9, 677–686.
- Tavian, M., Coulombel, L., Luton, D., Clemente, H.S., Dieterlen-Lievre, F., Peault, B. (1996) Aorta-associated CD34+ hematopoietic cells in the early human embryo. Blood, 87, 67–72.
- Tavian, M., Hallais, M.F., Peault, B. (1999) Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Development, 126, 793–803.
- Tsai, F.Y., Keller, G., Kuo, F.C., Weiss, M., Chen, J., Rosenblatt, M., Alt, F.W., Orkin, S.H. (1994) An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature, 371, 221–226.
- Tsuji, K., Ito, Y., Noda, M. (1998) Expression of the PEBP2alphaA/AML3/CBFA1 gene is regulated by BMP4/7 heterodimer and its overexpression suppresses type I collagen and osteocalcin gene expression in osteoblastic and nonosteoblastic mesenchymal cells. Bone, 22, 87–92.DOI: 10.1016/s8756-3282(97)00267-6
- Wang, Q., Stacy, T., Binder, M., Marin-Padilla, M., Sharpe, A.H., Speck, N.A. (1996) Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proceedings of the National Academy of Sciences of the United States of America, 93, 3444–3449.
- Watt, S.M., Butler, L.H., Tavian, M., Buhring, H.J., Rappold, I., Simmons, P.J., Zannettino, A.C., Buck, D., Fuchs, A., Doyonnas, R., Chan, J.Y., Levesque, J.P., Peault, B., Roxanis, I. (2000) Functionally defined CD164 epitopes are expressed on CD34 (+) cells throughout ontogeny but display distinct distribution patterns in adult hematopoietic and nonhematopoietic tissues. Blood, 95, 3113–3124.
- Weaver, M., Dunn, N.R., Hogan, B.L. (2000) Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development, 127, 2695–2704.
- Winnier, G., Blessing, M., Labosky, P.A., Hogan, B.L. (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes and Development, 9, 2105–2116.
- Wood, H.B., May, G., Healy, L., Enver, T., Morriss-Kay, G.M. (1997) CD34 expression patterns during early mouse development are related to modes of blood vessel formation and reveal additional sites of hematopoiesis. Blood, 90, 2300–2311.
- Xu, R.H., Ault, K.T., Kim, J., Park, M.J., Hwang, Y.S., Peng, Y., Sredni, D., Kung, H. (1999) Opposite effects of FGF and BMP-4 on embryonic blood formation: roles of PV.1 and GATA-2. Developmental Biology, 208, 352–361.DOI: 10.1006/dbio.1999.9205
- Yano, M., Iwama, A., Nishio, H., Suda, J., Takada, G., Suda, T. (1997) Expression and function of murine receptor tyrosine kinases, TIE and TEK, in hematopoietic stem cells. Blood, 89, 4317–4326.
- Yoder, M.C., Hiatt, K., Mukherjee, P. (1997) In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proceedings of the National Academy of Sciences of the United States of America, 94, 6776–6780.
-
Zhang, C. &
Evans, T. (1996) BMP-like signals are required after the midblastula transition for blood cell development.
Developmental Genetics, 18, 267–278.DOI: 10.1002/(sici)1520-6408(1996)18:3<267::aid-dvg7>3.3.co;2-1
10.1002/(SICI)1520-6408(1996)18:3<267::AID-DVG7>3.0.CO;2-7 CAS PubMed Web of Science® Google Scholar
- Ziegler, B.L., Valtieri, M., Porada, G.A., De Maria, R., Muller, R., Masella, B., Gabbianelli, M., Casella, I., Pelosi, E., Bock, T., Zanjani, E.D., Peschle, C. (1999) KDR receptor: a key marker defining hematopoietic stem cells. Science, 285, 1553–1558.DOI: 10.1126/science.285.5433.1553
Citing Literature
