Lymphocyte development from stem cells

Annual Review of Immunology

Volumn 10, Issue , 1992, Pages 759-783

  Ikuta, Koichi ^a   Uchida, Nobuko ^a   Friedman, Jeff ^a   Weissman, Irving L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

c kit receptor; gamma delta T cell; N nucleotide insertion; steel factor; thymus

Indexed keywords

PROTEIN KINASE; T LYMPHOCYTE RECEPTOR;

ANIMAL TISSUE; B LYMPHOCYTE; CELL DIFFERENTIATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; REVIEW; THYMUS;

EID: 0026716473     PISSN: 03013782     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.iy.10.040192.003551     Document Type: Review

References (136)

1. Spangrude, G. J. 1989. Enrichment of murine haemopoietic stem cells: diverging roads. Immunol. Today 10: 344-50
2. Visser, J. W. M., Van Bekkum, D. W. 1990. Purification of pluripotent hemopoietic stem cells: past and present. Exp. Hematol. 18: 248-56
3. Visser, J. W. M., Bol, S. J. L., van den Engh, G. 1981. Characterization and enrichment of murine hemopoietic stem cells by fluorescence activated cell sorting. Exp. Hematol. 9: 644-55
4. Lord, B. I., Spooncer, E. 1986. Isolation of haemopoietic spleen colony forming cells. Lymphokine Res. 5: 59-72
5. Spangrude, G. J., Heimfeld, S., Weissman, I. L. 1988. Purification and characterization of mouse hematopoietic stem cells. Science 241: 58-62
6. Nicola, N. A., Metcalf, D., von Melchner, H., Burgess, A. W. 1981. Isolation of murine fetal hemopoietic progenitor cells and selective fractionation of various erythroid precursors. Blood 58: 376-86
7. McKearn, J. P., McCubrey, J., Fagg, B. 1985. Enrichment of hematopoietic precursor cells and cloning of multi-potential B-lymphocyte precursors. Proc. Natl. Acad. Sci. USA 82: 7414-18
8. Jordan, C. T., McKearn, J. P., Lemischka, I. R. 1990. Cellular and developmental properties of fetal hematopoietic stem cells. Cell 61: 953-63
9. Ikuta, K., Kina, T., MacNeil, I., Uchida, N., Peault, B., Chien, Y., Weissman, I. L. 1990. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell 62: 863-74
10. Till, J. E., McCulloch, E. A. 1961. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiation Res. 14: 213-22
11. Hodgson, G. S., Bradley, T. R. 1979. Properties of haematopoietic stem cells surviving 5-fluorouracil treatment: evidence for a pre-CFU-S cell? Nature 281: 381-82
12. Visser, J. W. M., de Vries, P. 1988. Isolation of spleen-colony forming cells (CFU-s) using wheat germ agglutinin and rhodamine 123 labeling. Blood Cells 14: 369-84
13. van de Rijn, M., Heimfeld, S., Spangrude, G. J., Weissman, I. L. 1989. Mouse hematopoietic stem-cell antjgen Sca-1 is a member of the Ly-6 antigen family. Proc. Natl. Acad. Sci. USA 86: 4634-38
14. Smith, L. G., Weissman, I. L., Heimfeld, S. 1991. Clonal analysis of hematopoietic stem-cell differentiation in vivo. Proc. Natl. Acad. Sci. USA 88: 2788-92
15. Spangrude, G. J., Johnson, G. R. 1990. Resting and activated subsets of mouse multipotent hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 87: 7433-37
16. Weilbaecher, K., Weissman, I., Blume, K., Heimfeld, S. 1991. An in vitro assay for hematopoietic stem cells: long-term colony formation in micro-Dexter cultures. Blood 78: 945-52
17. Moore, M. A. S., Metcalf, D. 1970. Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br. J. Haematol. 18: 279-96
18. Metcalf, D., Moore, M. A. S. 1971. Embryonic aspects of haemopoiesis. In Frontiers of Biology, ed. A. Neuberger, E. L. Tatum, 24 (Haemopoietic cells): 172-271. Amsterdam/London: North-Holland. 550 pp.
19. Johnson, G. R., Moore, M. A. S. 1975. Role of stem cell migration in initiation of mouse foetal liver haemopoiesis. Nature 258: 726-28
20. Weissman, I. L., Baird, S., Gardner, R. L., Papaioannou, V. E., Raschke, W. 1977. Normal and neoplastic maturation of T-lineage lymphocytes. Cold Spring Harbor Symp. Quant. Biol. XLI: 9-21
21. Weissman, I., Papaioannou, V., Gardner, R. 1978. Fetal hematopoietic origins of the adult hematolymphoid system. In Differentiation of Normal and Neoplastic Hematopoietic Cells, ed. B. Clarkson, P. A. Marks, J. E. Till, pp. 33-47. New York: Cold Spring Harbor Lab.
22. Doetschman, T. C., Eistetter, H., Katz, M., Schmidt, W., Kemler, R. 1985. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol. 87: 27-45
23. Wiles, M. V., Keller, G. 1991. Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development 111: 259-67
24. Schmitt, R. M., Bruyns, E., Snodgrass, H. R. 1991. Hematopoietic development of embryonic stem cells in vitro: cytokine and receptor gene expression. Genes Dev. 5: 728-40
25. Matthews, W., Jordan, C. T., Wiegand, G. W., Pardoll, D., Lemischka, I. R. 1991. A receptor tyrosine kinase specific to hematopoietic stem and progenitor cell-enriched populations. Cell 65: 1143-52
26. Russell, E. S. 1979. Hereditary anemias of the mouse: a review for geneticists. Adv. Genet. 20: 357-459
27. v. Science 144: 844-46
28. l. Blood 26: 399-410
29. Altus, M. S., Bernstein, S. E., Russell, E. S., Carsten, A. L., Upton, A. C. 1971. Defect extrinsic to stem cells in spleens of steel anemic mice. Proc. Soc. Exp. Biol. Med. 138: 985-88
30. Seller, M. J. 1966. Donor haemoglobin in anaemic mice of the W-series transplanted with haematopoietic tissue from an unrelated donor. Nature 212: 81-82
31. v) deficient in response to erythropoietin. Ann. NY Acad. Sci. 149: 475-85
32. Seller, M. J. 1968. Transplantation of anaemic mice of the W-series with haemopoietic tissue bearing marker chromosomes. Nature 220: 300-1
33. Qiu, F., Ray, P., Brown, K., Barker, P. E., Jhanwar, S., Ruddle, F. H., Besmer, P. 1988. Primary structure of c-kit: relationship with the CSF-1/PDGF receptor kinase family-oncogenic activation of v-kit involves deletion of extracellular domain and C terminus. EMBO J. 7: 1003-11
34. Yarden, Y., Kuang, W. J., Yang-Feng, T., Coussens, L., Munemitsu, S., Dull, T. J., Chen, E., Schlessinger, J., Francke, U., Ullrich, A. 1987. Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J. 6: 3341-51
35. Chabot, B., Stephenson, D. A., Chapman, V. M., Besmer, P., Bernstein, A. 1988. The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335: 88-89
36. Geissler, E. N., Ryan, M. A., Housman, D. E. 1988. The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55: 185-92
37. Williams, D. E., Eisenman, J., Baird, A., Rauch, C., Van Ness, K., March, C. J., Park, L. S., Martin, U., Mochizuki, D. Y., Boswell, H. S., Burgess, G. S., Cosman, D., Lyman, S. D. 1990. Identification of a ligand for the c-kit proto-oncogene. Cell 63: 167-74
38. Copeland, N. G., Gilbert, D. J., Cho, B. C., Donovan, P. J., Jenkins, N. A., Cosman, D., Anderson, D., Lyman, S. D., Williams, D. E. 1990. Mast cell growth factor maps near the steel locus on mouse chromosome 10 and is deleted in a number of steel alleles. Cell 63: 175-83
39. Flanagan, J. G., Leder, P. 1990. The kit ligand: a cell surface molecule altered in steel mutant fibroblasts. Cell 63: 185-94
40. Zsebo, K. M., Wypych, J., McNiece, I. K., Lu, H. S., Smith, K. A., Karkare, S. B., Sachdev, R. K., Yuschenkoff, V. N., Birkett, N. C., Williams, L. R., Satyagal, V. N., Tung, W., Bosselman, R. A., Mendiaz, E. A., Langley, K. E. 1990. Identification, purification, and biological characterization of hematopoietic stem cell factor from Buffalo rat liver-conditioned medium. Cell 63: 195-201
41. Martin, F. H., Suggs, S. V., Langley, K. E., Lu, H. S., Ting, J., Okino, K. H., Morris, C. F., McNiece, I. K., Jacobsen, F. W., Mendiaz, E. A., Birkett, N. C., Smith, K. A., Johnson, M. J., Parker, V. P., Flores, J. C., Patel, A. C., Fisher, E. F., Erjavec, H. O., Herrera, C. J., Wypych, J., Sachdev, R. K., Pope, J. A., Leslie, I., Wen, D., Lin, C. H., Cupples, R. L., Zsebo, K. M. 1990. Primary structure and functional expression of rat and human stem cell factor DNAs. Cell 63: 203-11
42. Zsebo, K. M., Williams, D. A., Geissler, E. N., Broudy, V. C., Martin, F. H., Atkins, H. L., Hsu, R. Y., Birkett, N. C, Okino, K. H., Murdock, D. C., Jacobsen, F. W., Langley, K. E., Smith, K. A., Takeishi, T., Cattanach, B. M., Galli, S. J., Suggs, S. V. 1990. Stem cell factor is encoded at the SI locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 63: 213-24
43. Huang, E., Nocka, K., Beier, D. R., Chu, T. Y., Buck, J., Lahm, H. W., Wellner, D., Leder, P., Besmer, P. 1990. The hematopoietic growth factor KL is encoded by the Sl locus and is the ligand of the c-kit receptor, the gene product of the W locus. Cell 63: 225-33
44. Anderson, D. M., Lyman, S. D., Baird, A., Wignall, J. M., Eisenman, J., Rauch, C., March, C. J., Boswell, H. S., Gimpel, S. D., Cosman, D., Williams, D. E. 1990. Molecular cloning of mast cell growth factor, a hematopoietin that is active in both membrane bound and soluble forms. Cell 63: 235-43
45. d mutant. Cell 64: 1025-35
46. Ogawa, M., Matsuzaki, Y., Nishikawa, S., Hayashi, S. I., Kunisada, T., Sudo, T., Kina, T., Nakauchi, H., Nishikawa, S. I. 1991. Expression and function of c-kit in hemopoietic progenitor cells. J. Exp. Med. 174: 63-71
47. Metcalf, D., Nicola, N. A. 1991. Direct proliferative actions of stem cell factor on murine bone marrow cells in vitro: Effects of combination with colony-stimulating factors. Proc. Natl. Acad. Sci. USA 88: 6239-43
48. - cells cultured with interleukin-3, granulocyte colony-stimulating factor, or granulocyte-macrophage colony-stimulating factor. Blood 77: 2316-21
49. de Vries, P., Brasel, K. A., Eisenman, J. R., Alpert, A. R., Williams, D. E. 1991. The effect of recombinant mast cell growth factor on purified murine hematopoietic stem cells. J. Exp. Med. 173: 1205-11
50. Sarvella, P. A., Russell, L. B. 1956. Steel, a new dominant gene in the house mouse. J. Hered. 47: 123-28
51. Lepault, F., Weissman, I. L. 1981. An in vivo assay for thymus-homing bone marrow cells. Nature 293: 151-54
52. Lepault, F., Coffman, R. L., Weissman, I. L. 1983. Characteristics of thymus-homing bone marrow cells. J. Immunol. 131:64-69
53. Ezine, S., Weissman, I. L., Rouse, R. V. 1984. Bone marrow cells give rise to distinct cell clones within the thymus. Nature 309: 629-31
54. Ezine, S., Jerabek, L., Weissman, I. 1987. The phenotype of thymocytes derived from a single clonogenic precursor. J. Immunol. 139: 2195-99
55. Spangrude, G. J., Weissman, I. L. 1988. Mature T cells generated from single thymic clones are phenotypically and functionally heterogeneous. J. Immunol. 141: 1877-90
56. Kina, T., Amagai, T., Nishikawa, S. I., Araya, S. I., Katsura, Y. 1988. Functional differentiation and repertoire diversification of T cells derived from single progenitor cells. Eur. J. Immunol. 18: 897-903
57. Abramson, S., Miller, R. G., Phillips, R. A. 1977. The identification in adult bone marrow of pluripotent and restricted stem cells of the myeloid and lymphoid systems. J. Exp. Med. 145: 1567-79
58. v mice. Cell 42: 71-79
59. Keller, G., Paige, C., Gilboa, E., Wagner, E. F. 1985. Expression of a foreign gene in myeloid and lymphoid cells derived from multipotent haematopoietic precursors. Nature 318: 149-54
60. Lemischka, I. R., Raulet, D. H., Mulligan, R. C. 1986. Developmental potential and dynamic behavior of hematopoietic stem cells. Cell 45: 917-27
61. v mice. Proc. Natl. Acad. Sci. USA 86: 4564-68
62. Jordan, C. T., Lemischka, I. R. 1990. Clonal and systemic analysis of long-term hematopoiesis in the mouse. Genes Dev. 4: 220-32
63. lo bone marrow cells repopulate the thymus. J. Exp. Med. 167: 1671-83
64. Spangrude, G. J., Klein, J., Heimfeld, S., Aihara, Y., Weissman, I. L. 1989. Two monoclonal antibodies identify thymic-repopulating cells in mouse bone marrow. J. Immunol. 142: 425-30
65. Le Douarin, N. M., Jotereau, F. V. 1975. Tracing of cells of the avian thymus through embryonic life in interspecific chimeras. J. Exp. Med. 142: 17-40
66. Owen, J. J. T., Jenkinson, E. J. 1981. Embryology of the lymphoid system. Prog. Allergy 29: 1-34
67. Owen, J. J. T., Jenkinson, E. J. 1984. Early events in T lymphocyte genesis in the fetal thymus. Am. J. Anat. 170: 301-10
68. Jotereau, F. V., Houssaint, E., Le Douarin, N. M. 1980. Lymphoid stem cell homing to the early thymic primordium of the avian embryo. Eur. J. Immunol. 10: 620-27
69. Barg, M., Mandel, T. E., Johnson, G. R. 1978. Haemopoietic stem cells in the foetal mouse thymus. Aust. J. Exp. Biol. Med. Sci. 56: 195-200
70. Fontaine-Perus, J. C., Caiman, F. M., Kaplan, C., Le Douarin, N. M. 1981. Seeding of the 10-day mouse embryo thymic rudiment by lymphocyte precursors in vitro. J. Immunol. 126: 2310-16
71. Pyke, K. W., Bach, J. F. 1979. The in vitro migration of murine fetal liver cells to thymic rudiments. Eur. J. Immunol. 9: 317-23
72. Champion, S., Imhof, B. A., Savagner, P., Thiery, J. P. 1986. The embryonic thymus produces chemotactic peptides involved in the homing of hemopoietic precursors. Cell 44: 781-90
73. Imhof, B. A., Deugnier, M. A., Girault, J. M., Champion, S., Damais, C., Itoh, T., Thiery, J. P. 1988. Thymotaxin: a thymic epithelial peptide chemotactic for T-cell precursors. Proc. Natl. Acad. Sci. USA 85: 7699-7703
74. Bauvois, B., Ezine, S., Imhof, B., Denoyelle, M., Thiery, J. P. 1989. A role for the thymic epithelium in the selection of pre-T cells from murine bone marrow. J. Immunol. 143: 1077-86
75. Deugnier, M. A., Imhof, B. A., Bauvois, B., Dunon, D., Denoyelle, M., Thiery, J. P. 1989. Characterization of rat T cell precursors sorted by chemotactic migration toward thymotaxin. Cell 56: 1073-83
76. Dunon, D., Kaufman, J., Salomonsen, J., Skjoedt, K., Vainio, O., Thiery, J. P., Imhof, B. A. 1990. T cell precursor migration towards β2-microglobulin is involved in thymus colonization of chicken embryos. EMBO J. 9: 3315-22
77. Springer, T. A. 1990. Adhesion receptors of the immune system. Nature 346: 425-34
78. Lesley, J., Schulte, R., Hyman, R. 1990. Binding of hyaluronic acid to lymphoid cell lines is inhibited by monoclonal antibodies against Pgp-1. Exp. Cell Res. 187: 224-33
79. O'Neill, H. C., De Cello, G., O'Neill, T. J. Characterisation of lymphoid cell lines from murine spleen which can localise in thymus. Int. Immunol. In press
80. Scollay, R., Bartlett, P., Shortman, K. 1984. T cell development in the adult murine thymus: changes in the expression of the surface antigens Ly2, L3T4 and B2A2 during development from early precursor cells to emigrants. Immunol. Rev. 82: 79-103
81. Mathieson, B. J., Fowlkes, B. J. 1984. Cell surface antigen expression on thymocytes: development and phenotypic differentiation of intrathymic subsets. Immunol. Rev. 82: 141-73
82. Scollay, R., Smith, J., Stauffer, V. 1986. Dynamics of early T cells: prothymocyte migration and proliferation in the adult mouse thymus. Immunol. Rev. 91: 129-57
83. + precursors. Proc. Natl. Acad. Sci. USA 86: 7542-46
84. - T cells bearing αβ T cell receptor. J. Immunol.142: 3773-80
85. Guidos, C. J., Danska, J. S., Fathman, C. G., Weissman, I. L. 1990. TCR-mediated negative selection of autoreactive T lymphocyte precursors occurs after commitment to the CD4 or CD8 lineages. J. Exp. Med. 172: 835-45
86. Wu, L., Scollay, R., Egerton, M., Pearse, M., Spangrude, G. J., Shortman, K. 1991. CD4 expressed on earliest T-lineage precursor cells in the adult murine thymus. Nature 349: 71-74
87. Kingston, R., Jenkinson, E. J., Owen, J. J. T. 1985. A single stem cell can recolonize an embryonic thymus, producing phenotypically distinct T-cell populations. Nature 317: 811-13
88. Williams, G. T., Kingston, R., Owen, M. J., Jenkinson, E. J., Owen, J. J. T. 1986. A single micromanipulated stem cell gives rise to multiple T-cell receptor gene rearrangements in the thymus in vitro. Nature 324: 63-64
89. Snodgrass, H. R., Dembic, Z., Steinmetz, M., von Boehmer, H. 1985. Expression of T-cell antigen receptor genes during fetal development in the thymus. Nature 315: 232-33
90. Raulet, D. H., Garman, R. D., Saito, H., Tonegawa, S. 1985. Developmental regulation of T-cell receptor gene expression. Nature 314: 103-7
91. Haars, R., Kronenberg, M., Gallatin, M., Weissman, I. L., Owen, F. L., Hood, L. 1986. Rearrangement and expression of T cell antigen receptor and y genes during thymic development. J. Exp. Med. 164: 1-24
92. Raulet, D. H., Spencer, D. M., Hsiang, Y. H., Goldman, J. P., Bix, M., Liao, N. S., Zijlstra, M., Jaenisch, R., Correa, I. 1991. Control of γδ T-cell development. Immunol. Rev. 120: 185-204
93. Garman, R. D., Doherty, P. J., Raulet, D. H. 1986. Diversity, rearrangement, and expression of murine T cell gamma genes. Cell 45: 733-12
94. Elliott, J. F., Rock, E. P., Patten, P. A., Davis, M. M., Chien, Y. 1988. The adult T-cell receptor δ-chain is diverse and distinct from that of fetal thymocytes. Nature 331: 627-31
95. Lafaille, J. J., DeCloux, A., Bonneville, M., Takagaki, Y., Tonegawa, S. 1989. Junctional sequences of T cell receptor γδ genes: implications for γδ T cell line-ages and for a novel intermediate of V-(D)-J joining. Cell 59: 859-70
96. Havran, W. L., Allison, J. P. 1988. Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature 335: 443-45
97. + dendritic epidermal cells. Cell 55: 837-47
98. + dendritic epidermal cells revealed by Vγ3-specific monoclonal antibody. Proc. Natl. Acad. Sci. USA 86: 4185-89
99. Asarnow, D. M., Goodman, T., LeFrancois, L., Allison, J. P. 1989. Distinct antigen receptor repertoires of two classes of murine epithelium-associated T cells. Nature 341: 60-62
100. + dendritic epidermal cells of adult mice from fetal thymic precursors. Nature 344: 68-70
101. Ito, K., Bonneville, M., Takagaki, Y., Nakanishi, N., Kanagawa, O., Krecko, E. G., Tonegawa, S. 1989. Different γδ T-cell receptors are expressed on thymocytes at different stages of development. Proc. Natl. Acad. Sci. USA 86: 631-35
102. Itohara, S., Farr, A. G., Lafaille, J. J., Bonneville, M., Takagaki, Y., Haas, W., Tonegawa, S. 1990. Homing of a γδ thymocyte subset with homogeneous T-cell receptors to mucosal epithelia. Nature 343: 754-57
103. Takagaki, Y., DeCloux, A., Bonneville, M., Tonegawa, S. 1989. Diversity of γδ T-cell receptors on murine intestinal intraepithelial lymphocytes. Nature 339: 712-14
104. Ikuta, K., Weissman, I. L. 1991. The junctional modifications of a T cell receptor y chain are determined at the level of thymic precursors. J. Exp. Med. 174: 1279-82
105. H fusions. Proc. Natl. Acad. Sci. USA 79: 4118-22
106. Desiderio, S. V., Yancopoulos, G. D., Paskind, M., Thomas, E., Boss, M. A., Landau, N., Alt, F. W., Baltimore, D. 1984. Insertion of N regions into heavy-chain genes is correlated with expression of terminal deoxytransferase in B cells. Nature 311: 752-55
107. Fantoni, A., Bank, A., Marks, P. A. 1967. Globin composition and synthesis of hemoglobins in developing fetal mice erythroid cells. Science 157: 1327-29
108. Jotereau, F., Heuze, F., Salomon-Vie, V., Gascan, H. 1987. Cell kinetics in the fetal mouse thymus: precursor cell input, proliferation, and emigration. J. Immunol. 138: 1026-30
109. Feeney, A. J. 1991. Junctional sequences of fetal T cell receptor β chains have few N regions. J. Exp. Med. 174: 115-24
110. Meek, K. 1990. Analysis of Junctional diversity during B lymphocyte development. Science 250: 820-23
111. H joining: implications for the joining mechanism and the ontogenetic timing of Ly1 B cell and B-CLL progenitor generation. EMBO J. 9: 2133-40
112. Ogimoto, M., Yoshikai, Y., Matsuzaki, G., Matsumoto, K., Kishihara, K., Nomoto, K. 1990. Expression of T cell receptor Vγ5 in the adult thymus of irradiated mice after transplantation with fetal liver cells. Eur. J. Immunol. 20: 1965-70
113. Whitlock, C. A., Robertson, D., Witte, O. N. 1984. Murine B cell lymphopoiesis in long term culture. J. Immunol. Meth. 1967: 353-69
114. Whitlock, C., Denis, K., Robertson, D., Witte, O. 1985. In vitro analysis of murine B-cell development. Annu. Rev. Immunol. Meth. 1967: 353-69
115. Kincade, P. W., Lee, G., Pietrangeli, C. E., Hayashi, S. I., Gimble, J. M. 1989. Cells and molecules that regulate B lymphopoesis in bone marrow. Annu. Rev. Immunol. 7: 111-43
116. Dexter, T. M., Allen, T. D., Lajtha, L. G. 1977. Conditions controlling the proliferation of haematopoietic stem cells in vitro. J. Cell. Physiol. 91: 335-44
117. Dexter, T. M., Moore, M. A. S. 1977. In vitro duplication and "cure" of haemopoietic defects in genetically anaemic mice. Nature 269: 412-14
118. Whitlock, C. A., Witte, O. N. 1982. Long-term culture of B lymphocytes and their precursors from murine bone marrow. Proc. Natl. Acad. Sci. USA 79: 3608-12
119. Schrader, J. W., Schrader, S. 1978. In vitro studies on lymphocyte differentiation. I. Long term in vitro culture of cells giving rise to functional lymphocytes in irradiated mice. J. Exp. Med. 148: 823-28
120. Jones-Villeneuve, E. V., Rusthoven, J. J., Miller, R. G., Phillips, R. A. 1980. Differentiation of Thy 1-bearing cells from progenitors in long-term bone marrow cultures. J. Immunol. 124: 597-601
121. Dorshkind, K., Phillips, R. A. 1983. Characterization of early B lymphocyte precursors present in long-term bone marrow cultures. J. Immunol. 131: 2240-45
122. Denis, K. A., Witte, O. N. 1986. In vitro development of B lymphocytes from long-term cultured precursor cells. Proc. Natl. Acad. Sci. USA 83: 441-45
123. Hunt, P., Robertson, D., Weiss, D., Rennick, D., Lee, F., Witte, O. N. 1987. A single bone marrow-derived stromal cell type supports the in vitro growth of early lymphoid and myeloid cells. Cell 48: 997-1007
124. Whitlock, C. A., Tidmarsh, G. F., Muller-Sieburg, C., Weissman, I. L. 1987. Bone marrow stromal cell lines with lymphopoietic activity express high levels of a pre-B neoplasia-associated molecule. Cell 48: 1009-21
125. Namen, A. E., Schmierer, A. E., March, C. J., Overell, R. W., Park, L. S., Urdal, D. L., Mochizuki, D. Y. 1988. B cell precursor growth-promoting activity. Purification and characterization of a growth factor active on lymphocyte precursors. J. Exp. Med. 167: 988-1002
126. Namen, A. E., Lupton, S., Hjerrild, K., Wienall, J., Mochizuki, D. Y., Schmierer, A., Mosley, B., March, C. J., Urdal, D., Gillis, S., Cosman, D., Goodwin, R. G. 1988. Stimulation of B-cell progenitors by cloned murine interleukin-7. Nature 333: 571-73
127. Hayashi, S.-I., Kunisada, T., Ogawa, M., Sudo, T., Kodama, H., Suda, T., Nishikawa, S., Nishikawa, S. I. 1990. Stepwise progression of B lineage differentiation supported by interleukin 7 and other stromal cell molecules. J. Exp. Med. 171: 1683-95
128. lo hematopoietic stem cell. Cell 44: 653-62
129. Tidmarsh, G., Heimfeld, S., Whitlock, C., Weissman, I. L., Muller-Sieburg, C. E. 1989. Identification of a novel bone marrow-derived B-cell progenitor population that coexpresses B220 and Thy-1 and is highly enriched for Abelson leukemia virus targets. Mol. Cell. Biol. 96: 2665-71
130. Heimfeld, S., Guidos, C. J., Holzmann, B., Siegelman, M. H., Weissman, I. L. 1989. Developmental analysis of the mouse hematolymphoid system. Cold Spring Harbor Symp. Quant. Biol. LIV: 75-85
131. Hardy, R. R., Hayakawa, K. 1986. Development and physiology of Ly-1 B and its human homolog, Leu-1 B. Immunol. Rev. 93: 53-79
132. Herzenberg, L. A., Stall, A. M., Lalor, P. A., Sidman, C., Moore, W. A., Parks, D. R., Herzenberg, L. A. 1986. The Ly-1 B cell lineage. Immunol. Rev. 93: 81-102
133. Hayakawa, K., Hardy, R. R., Herzenberg, L. A., Herzenberg, L. A. 1985. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 161: 1554-68
134. Hayakawa, K., Hardy, R. R., Stall, A. M., Herzenberg, L. A., Herzenberg, L. A. 1986. Immunoglobulin-bearing B cells reconstitute and maintain the murine Ly-1 B cell lineage. Eur. J. Immunol. 16: 1313-16
135. Kubai, L., Auerbach, R. 1983. A new source of embryonic lymphocytes in the mouse. Nature 301: 154-56
136. Solvason, N., Lehuen, A., Kearney, J. F. 1991. An embryonic source of Ly1 but not conventional B cells. Int. Immunol. 3: 543-50