Antigenic Phenotype and Gene Expression Pattern of Lymphohemopoietic Progenitors during Early Mouse Ontogeny

Journal of Immunology

Volumn 158, Issue 6, 1997, Pages 2627-2637

  Marcos, Miguel A R ^a,d   Morales Alcelay, Susana ^b   Godin, Isabelle E ^c   Dieterlen Lievre, Françoise ^c   Copin, Sergio G ^a   Gaspar, Maria Luisa ^b  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c Inst of Cell and Molec Embryology   (France)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN J CHAIN; LY ANTIGEN; LY6A PROTEIN, MOUSE; MEMBRANE ANTIGEN; MEMBRANE PROTEIN;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL DIFFERENTIATION; CYTOLOGY; EMBRYO; GENE EXPRESSION REGULATION; GENE REARRANGEMENT; GENETICS; HEMATOPOIETIC STEM CELL; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE SUBPOPULATION; METABOLISM; MOUSE;

ANIMALS; ANTIGENS, LY; ANTIGENS, SURFACE; CELL DIFFERENTIATION; EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REARRANGEMENT, B-LYMPHOCYTE; HEMATOPOIETIC STEM CELLS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN J-CHAINS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOPHENOTYPING; LYMPHOCYTE SUBSETS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C;

EID: 0031569280     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (81)

1. Le Douarin, N. M., and F. V. Jotereau. 1975. Tracing of cells of the avian thymus through embryonic life in interspecific chimeras. J. Exp. Med. 142:17.
2. Le Douarin, N. M., E. Houssaint, F. V. Jotereau, and M. Belo. 1975. Origin of hemopoietic stem cells in embryonic bursa of Fabricius and bone marrow studied through interspecific chimeras. Proc. Natl. Acad. Sci. USA 72:2701.
3. Rodewall, H.-R., K. Kretzschmar, S. Takeda, and M. Dessing. 1994. Identification of pro-thymocytes in murine fetal blood: the lineage commitment can precede thymus colonization. EMBO J. 13:4229.
4. Delassus, S., and A. Cumano. 1996. Circulation of hematopoietic progenitors in the mouse embryo. Immunity 4:97.
5. Moore, M. A. S., and D. Metcalf. 1970. Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Brt. J. Haematol. 18:279.
6. Dieterlen-Lièvre, F., and N. M. Le Douarin. 1993. Developmental rules in the hemopoietic and immune systems of birds: how general are they? Semin. Dev. Biol. 4:603.
7. Turpen, J. B., C. M. Knudson, and P. B. Hoefen. 1981. The early ontogeny of hematopoietic cells studied by grafting cytogenetically labeled tissue anlagen: localization of a prospective stem cell compartment. Dev. Biol. 85:99.
8. Godin, I. E., J. A. García-Porrero, A. Coutinho, F. Dieterlen-L., and M. A. R. Marcos. 1993. Para-aortic splanchopleura from early mouse embryos contains B1a cell progenitors. Nature 364:67.
9. Marcos, M. A. R., I. Godin, A. Cumano, S. Morales, J. A. Garcia-Porrero, F. Dieterlen-L., and M. L. Gaspar. 1994. Developmental events from hemopoietic stem cells to B-cell populations and Ig repertoires. Immunol. Rev. 137:155.
10. Medvinsky, A., N. L. Samoylina, A. M. Müller, and E. A. Dzierzak. 1993. An early pre-liver intra-embryonic source of CFU-S in the developing mouse. Nature 364:64.
11. Müller, A., A. Medvinsky, J. Strouboulis, F. Grosveld, and E. Dzierzak. 1994. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1:291.
12. García-Porrero, J. A., I. E. Godin, and F. Dieterlen-Lièvre. 1995. Potential intraembryonic hemogenic sites at preliver stages in the mouse. Anal. Embryol. 192:425.
13. Tavian, M., L. Coulombel, D. Luton, H. SanClemente, F. Dieterlen-Lièvre, and B. Peault. 1996. Aorta-associated CD34(+) hematopoietic cells in the early human embryo. Blood 87:67.
14. Kubai, L., and R. Auerbach. 1983. A new source of embryonic lymphocytes in the mouse. Nature 301:154.
15. Solvason, N., A. Lehuen, and F. J. Kearney. 1991. An embryonic source of Ly1 but not conventional B cells. Int. Immunol. 3:543.
16. Godin, I., F. Dieterlen-Lièvre, and A. Cumano. 1995. Emergence of multipotential hemopoietic cells in the yolk sac and paraaortic splanchnopleura in mouse embryos beginning at 8.5 d.p.c. Proc. Natl. Acad. Sci. USA 92:773.
17. Godin, I., F. Dieterlen-Lièvre, and A. Cumano. 1995. B-lymphoid potential in pre-liver mouse embryo. Semin. Immunol. 7:131.
18. Ikuta, K., and I.-L. Weissman. 1991. The junctional modifications of a T cell receptor γ chain are determinated at the level of thymic precursors. J. Exp. Med. 174:1279.
19. Kantor, A. B., A. M. Stall, S. Adams, L. A. Herzenberg, and L. A. Herzenberg. 1992. Differential development of progenitor activity for three B-cell lineages. Proc. Natl. Acad. Sci. USA 89:3320.
20. Chabot, B., D. A. Stephenson, V. M. Chapman, P. Besmer, and A. Bernstein. 1988. The proto-oncogene c-kit encoding a transmenbrane tyrosine kinase receptor maps to the mouse W locus. Nature 335:88.
21. Jordan, C. T., J. P. McKearn, and I. R. Lemischka. 1990. Cellular and developmental properties of fetal hemopoietic stem cells. Cell 61:953.
22. Spangrude, G. J., S. Heimfeld, and I. L. Weissman. 1988. Purification and characterization of mouse hematopoietic stem cells. Science 241:58.
23. Springer, T. A., G. Galfré, D. S. Secher, and C. Milstein. 1978. Monoclonal xenogeneic antibodies to murine cell surface Ags: identification of novel leukocyte differentiation Ags. Eur. J. Immunol. 8:539.
24. Morrison, S. J., and I. L. Weissman. 1994. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1:661.
25. Baumhueter, S., M. Singer, W. Henzel, S. Hemmerich, M. Renz, S. Rosen, and L. A. Lasky. 1993. Binding of L-selectin to the vascular sialomucin CD34. Science 262:436.
26. Mombaerts, P., J. Iacomini, R. J. Johnson, K. Herrup, S. Tonegawa, and V. E. Papaionnou. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68:869.
27. Melchers, F., D. Haasner, U. Grawunder, C. Kalberer, H. Karasuyama, T. Winkler, and A. G. Rolink. 1994. Roles of IgH and L chains and of surrogate H and L chains in the development of cells of the B lymphocyte lineage. Ann. Rev. Immunol. 12:209.
28. Medvinsky, A., O. I. Gan, M. L. Semenova, and N. L. Samoylina. 1996. Development of day-8 colony-forming unit-spleen hematopoietic progenitors during early embryogenesis: spatial and temporal mapping. Blood 87:557.
29. Ogawa, M., S. I. Nishikawa, K. Yoshinaga, S. I. Hayashi, T. Kunisada, J. Nakao, T. Kina, T. Sudo, H. Kodama, and S. I. Nishikawa. 1993. Expression and function of c-kit in fetal hemopoietic progenitor cells: transition from the early c-kit-independent to the late c-kit-dependent wave of hemopoiesis in the murine embryo. Development 117:1089.
30. McKearn, J. P., J. McCubrey, and B. Fagg. 1985. Enrichment of hematopoietic precursor cells and cloning of multipotential B-lymphocyte precursors. Proc. Natl. Acad. Sci. USA 82:7414.
31. LeClair, K. P., R. G. E. Palfree, P. M. Flood, U. Hammerling, and A. Bothwell. 1986. Isolation of a murine Ly-6 cDNA reveals a new multigene family. EMBO J. 5:3227.
32. Coffman, R. L., and I. L. Weissman. 1981. A monoclonal antibody that recognizes B cells and B cell precursors in mice. J. Exp. Med. 153:269.
33. Ikuta, K., T. Kina, I. MacNeil, N. Uchida, B. Péault, Y. Chien, and I. L. Weissman. 1990. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell 62:863.
34. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chlorophorm extraction. Anal. Biochem. 162: 156.
35. Gaspar, M. L., T. Meo, and M. Tosi. 1990. Structure and size distribution of the androgen receptor mRNA in wild-type and Tfm/y mutant mice. Mol. Endocrinol. 4:1600.
36. Alonso, S., A. Minty, Y. Boulet, and M. Buckingham. 1986. Comparison of three actin-coding sequences in the mouse: evolutionary relationships between the actin genes of warm blooded vertebrates. J. Mol. Evol. 23:11.
37. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A Laboratory Manual. C. Nolan, ed. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
38. Rolink, A., M. Streb, S. I. Nishikawa, and F. Melchers. 1991. The c-kit-encoded tyrosine kinase regulates the proliferation of early pre-B cells. Eur. J. Immunol. 21:2609.
39. McClanahan, T., S. Dalrymple, M. Barkett, and F. Lee. 1993. Hematopoietic growth factor receptor genes as markers of lineage commitment during in vitro development of hematopoietic cells. Blood 81:2903.
40. Chun, J. J. M., D. G. Schatz, M. A. Oettinger, R. Jaenisch, and D. Baltimore. 1991. The recombination activating gene-1 (RAG-1) transcript is present in the murine central nervous system. Cell 64:189.
41. Marcos, M. A. R., M. L. Gaspar, E. Malenchere, and A. Coutinho. 1994. Isolation of peritoneal precursors of B-1 cells in the adult mouse. Eur. J. Immunol. 24: 1033.
42. Gu, H., D. Kitamura, and K. Rajewsky. 1991. B cell development regulated by gene rearrangement: arrest of maturation by membrane-bound Dμ protein and selection of DH element reading frames. Cell 65:47.
43. Hardy, R. R., C. E. Carmack, S. A. Shinton, J. D. Kemp, and K. Hayakawa. 1991. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173:1213.
44. Kudo, A., N. Sakaguchi, and F. Melchers. 1987. Organization of the murine Ig-related λ5 gene transcribed selectively in pre-B lymphocytes. EMBO J. 6:103.
45. Liu, C. P., P. W. Tucker, J. F. Mushinski, and F. Blattner. 1980. Structure of the genes that rearrange in development: mapping of heavy chain genes for mouse immunoglobulins M and D. Science 209:1348.
46. Qiu, F., P. Ray, K. Brown, P. Barker, S. Janwar, F. Ruddle, and P. Besmer. 1988. Primary structure of c-kit: relationship with the CSF-1/PDGF receptor kinase family. Oncogenic activation of c-kit involves deletion of extracellular domain and C terminus. EMBO J. 7:1003.
47. Feinberg, A. P., and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6.
48. Huetz, F., L. Carlsson, U. C. Tornberg, and D. Holmberg. 1993. V-region directed selection in differentiating B lymphocytes. EMBO J. 12:1819.
49. Velardi, A., and M. D. Cooper. 1984. An immunofluorescence analysis of the ontogeny of myeloid, T and B lineage cells in mouse hemopoietic tissues. J. Immunol. 133:672.
50. Wolf, N. S., I. Bertoncello, D. Z. Jiang, and G. Priestley. 1995. Developmental hematopoiesis from prenatal to young-adult life in the mouse model. Exp. Hematol. 23:142.
51. Zeigler, F. C., B. D. Bennet, C. T. Jordan, S. D. Spencer, S. Baumhueter, K. J. Karrol, J. Hooley, K. Bauer, and W. Matthews. 1994. Cellular and molecular characterization of the role of the FLK-2/FLT-3 receptor tyrosine kinase in hematopoietic stem cells. Blood 84:2422.
52. Orr-Urtreger, A., A. Avivi, Y. Zimmer, D. Givol, Y. Yarden, and P. Lonai. 1990. Developmental expression of c-kit, a proto-oncogene encoded by the W locus. Development 109:911.
53. Deleted in proof.
54. Young, P. E., S. Baumhueter, and L. A. Lasky. 1995. The sialomucin CD34 is expressed on hematopoietic cells and blood vessels during murine development. Blood 85:96.
55. Lin, G., E. Finger, and J. C. Gutierrez-Ramos. 1995. Expression of CD34 in endothelial cells, hematopoietic progenitors and nervous cells in fetal and adult mouse tissues. Eur. J. Immunol. 25:1508.
56. Murray, P. D. F. 1932. The development in vitro of blood of the early chick embryo. Proc. Roy. Soc. C. 11:497.
57. Pardanaud, L., and F. Dieterlen-Lièvre. 1993. Emergence of endothelial and hemopoietic cells in the avian embryo. Anal. Embryol. 187:107.
58. Brady, G., F. Billia, J. Knox, T. Hoang, I. R. Kirsch, E. B. Voura, R. G. Hawley, R. Cumming, M. Buchwald, K. Siminovitch, N. Miyamoto, G. Boehmelt, and N. N. Iscove. 1995. Analysis of gene expression in a complex differentiation hierarchy by global amplification of cDNA from single cells. Curr. Biol. 5:909.
59. Ehlich, A., S. Schaal, H. Gu, D. Kitamura, W. Müller, and K. Rajewsky. 1993. Immunoglobulin heavy and light chain genes rearrange independently at early stages of B cell development. Cell 72:695.
60. Chang, Y., C. J. Paige, and G. E. Wu. 1992. Enumeration and characterization of DJH structures in mouse fetal liver. EMBO J. 11:1891.
61. Shulman, M., C. D. Wilde, and G. Köhler. 1978. A better cell line for making hybridomas secreting specific antibodies. Nature 276:269.
62. Fleming, W. H., E. J. Alpern, N. Uchida, K. Ikuta, G. J. Spangrude, and I. L. Weissman. 1993. Functional heterogeneity is associated with the cell cycle status of murine hematopoietic stem cells. J. Cell Biol. 122:897.
63. Trevisan, M., and N. N. Iscove. 1995. Phenotypic analysis of murine long-term hemopoietic reconstituting cells quantitated competitively in vivo and comparison with more advanced colony-forming progeny. J. Exp. Med. 181:93.
64. Cumano, A., C. Furlonger, and C. J. Paige. 1993. Differentiation and characterization of B-cell precursors detected in the yolk sac and embryo body of embryos beginning at the 10-to 12-somite stage. Proc. Natl. Acad. Sci. USA 90:6429.
65. Huang, H., and R. Auerbach. 1993. Identification and characterization of hematopoietic stem cells from the yolk sac of the early mouse embryo. Proc. Natl. Acad. Sci. USA 90:10110.
66. Morris, L., C. F. Graham, and S. Gordon. 1991. Macrophages in haemopoietic and other tissues of the developing mouse detected by the monoclonal antibody F4/80. Development 112:517.
67. Kubagawa, H., M. D. Cooper, A. J. Carroll, and P. D. Burrows. 1989. Light-chain gene expression before heavy-chain gene rearangement in pre-B cells transformed by Epstein-Barr virus. Proc. Natl. Acad. Sci. USA 86:2356.
68. Lassoued, K., C. A. Nuñez, L. Billips, H. Kubagawa, R. C. Monteiro, T. W. LeBien, and M. D. Cooper. 1993. Expression of surrogate light chain receptors is restricted to a late stage in pre B cell differentiation. Cell 73:73.
69. Reynaud, C. A., B. A. Imhof, V. Anquez, and J. C. Weil. 1992. Emergence of committed B lymphoid progenitors in the developing chicken embryo. EMBO J. 11:4349.
70. Reynaud, C.-A., C. Garcia, W. R. Hein, and J. C. Weill. 1995. Hypermutation generating the sheep immunoglobulin repertoire is an antigen-independent process. Cell 80:115.
71. Francés, V., D. Pandrau-García, C. Guret, S. Ho, Z. Wang, V. Duvert, S. Saeland, and H. Martínez-Valdez. 1994. A surrogate λ5 kDa JCκ protein is expressed in combination with μ heavy chain by human B cell precursors. EMBO J. 13:5937.
72. Kitamura, D., A. Kudo, S. Schaal, W. Müller, F. Melchers, and K. Rajewsky. 1992. A critical role of λ5 protein in B cell development. Cell 69:823.
73. Sollbach, A. E., and G. E. Wu. 1995. Inversions produced during V(D)J rearrangement at IgH, the immunoglobulin heavy-chain locus. Mol. Cell. Biol. 15: 671.
74. Ramsden, D. A., C. J. Paige, and G. E. Wu. 1994. κ light chain rearrangement in mouse fetal liver. J. Immunol. 153:1150.
75. Fitts, M. G., and R. G. Mage. 1995. Secondary rearrangements and post-rearrangement selection contribute to restricted immunoglobulin DJH expression in young rabbit bone marrow. Eur. J. Immunol. 25:700.
76. Cumano, A., B. L. Kee, D. A. Ramsden, A. Marshall, C. J. Paige, and G. E. Wu. 1994. Development of B lymphocytes from lymphoid committed and uncommitted progenitors. Immunol. Rev. 137:5.
77. Kodama, H., M. Nose, S. Niida, S. Nishikawa, and S. I. Nishikawa. 1994. Involvement of the c-kit receptor in the adhesion of hematopoietic stem cells to stromal cells. Exp. Hematol. 22:979.
78. Lasky, L. A. 1996. Wandering progenitor cells. Curr. Biol. 6:1238.
79. Keller, G., M. Kennedy, T. Papayannopoulou, and M. V. Wiles. 1993. Hematopoietic committment during embryonic stem cell differentiation in culture. Mol. Cell. Biol. 13:473.
80. Lee, E. Y. H. P., C. Y. Chang, N. Hu, Y. C. J. Wang, C. C. Lai, K. Herrup, W. H. Lee, and A. Bradley. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359:288.
81. Mucenski, M. L., K. McLain, A. B. Kier, S. H. Swerdlow, C. M. Schreiner, T. A. Miller, D. W. Pietriga, W. J. Scott, and S. S. Potter. 1991. A functional c-myb is required for normal murine fetal liver hematopoiesis. Cell 65:677.