Lineage Relationships Between B Lymphocytes and Macrophages

  • Barbara L. Kee
  • Christopher J. Paige
Part of the Contemporary Immunology book series (CONTIM)


B lymphocytes, like all members of the hematopoietic system, develop from a common hematopoietic stem cell (HSC) in the bone marrow and fetal liver (1). Restricted stem cells, apparently able to give rise to myeloid lineage cells but not to B and T lymphocytes, have also been identified (2,3). However, lymphoid restricted stem cells have proven more difficult to identify conclusively, despite widespread belief that they exist (see refs. 4 and 5). The development of hematopoietic cells committed to a single lineage is thought to occur through the progressive restriction of the differentiation options of multipotent progenitors. For example, multipotent myeloid stem cells develop into nonself-renewing progenitors that give rise to granulocytes, erythrocytes, macrophages, and megakaryocytes (GEMM progenitors) and subsequently into granulocytes and macrophages (GM progenitors) under conditions that support the development of all myeloid cell types (6). Recently, bipotent progenitors, which develop into both B lymphocytes and macrophages, have been identified in the fetal liver of mice by the twelfth day of gestation (Fig. 1) (7).


Hematopoietic Stem Cell Fetal Liver Stem Cell Factor Murine Bone Marrow Lineage Determination 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Wu, A. M., Till, J. E., Siminovitch, L., and McCulloch, E. A. (1967) Cytological evidence for a relationship between normal hemopoietic colony-forming cells and cells of the lymphoid system. J. Exp. Med. 127, 455–463.CrossRefGoogle Scholar
  2. 2.
    Abramson, S., Miller, R. G., and Phillips, R. A. (1977) The identification in adult bone marrow of pluripotent and restricted stem cells ofthe myeloid and lymphoid systems. J. Exp. Med. 145, 1567–1579.PubMedCrossRefGoogle Scholar
  3. 3.
    Paige, C. J., Kincade, P. W., Moore, M. A. S., and Lee, G. (1979) The fate of fetal and adult B-cell progenitors grafted into immunodeficient CBA/N mice. J. Exp. Med. 150, 548–563.PubMedCrossRefGoogle Scholar
  4. 4.
    Lemischka, I. R., Raulet, D. H., and Mulligan, R. C. (1986) Developmental potential and dynamic behavior of hemopoietic stem cells. Cell 45, 917–927.PubMedCrossRefGoogle Scholar
  5. 5.
    Phillips, R. A. (1991) Hematopoietic stem cells: concepts, assays, and controversies. Sem. Immunol. 3, 337–347.Google Scholar
  6. 6.
    Metcalfe, D. (1989) The molecular control of cell division, differentiation, commitment and maturation in haematopoietic cells. Nature 339, 27–30.CrossRefGoogle Scholar
  7. 7.
    Cumano, A., Paige, C. J., Iscove, N. N., and Brady, G. (1992) Bipotential precursors of B cells and macrophages in murine fetal liver. Nature 356, 612–615.PubMedCrossRefGoogle Scholar
  8. 8.
    Greaves, M. F., Chan, L. C., Furley, A. J., Watt, S. M., and Molgaard, H. V. (1986) Lineage promiscuity in hemopoietic differentiation and leukemia. Blood 67, 1–11.PubMedGoogle Scholar
  9. 9.
    Hu, M., Krause, D., Greaves, M., Sharkis, S., Dexter, M., Heyworth, C., and Enver, T. (1997) Multi-lineage gene expression precedes commitment in the hemopoietic system. Genes Dev. 11, 774–785.PubMedCrossRefGoogle Scholar
  10. 10.
    Kee, B. L. and Paige, C. J. (1995) In vitro models of B lineage commitment. Semin. Immunol. 7, 143–154.PubMedCrossRefGoogle Scholar
  11. 11.
    Alt, F. W., Blackwell, T. K., DePinho, R. A., Reth, M. G., and Yancopoulos, G. D. (1986) Regulation of genome rearrangement events during lymphocyte differentiation. Immunol. Rev. 89, 5–30.PubMedCrossRefGoogle Scholar
  12. 12.
    Loffert, D., Schaal, S., Ehlich, A., Hardy, R. R., Zou, Y.-R., Muller, W., and Rajewsky, K. (1994) Early B-cell development in the mouse: insights from mutations introduced by gene targeting. lmmunol. Rev. 137, 135–153.CrossRefGoogle Scholar
  13. 13.
    Ramsden, D. A., van Gent, D. C., and Gellert, M. (1997) Specificity in V(D)J recombination: new lessons from biochemistry and genetics. Curr. Opin. Immunol. 9, 114–120.PubMedCrossRefGoogle Scholar
  14. 14.
    Rolink, A., Haasner, D., Melchers, F., and Andersson, J. (1996) The surrogate light chain in mouse B-cell development. Int. Rev. Immunol. 13, 341–356.PubMedCrossRefGoogle Scholar
  15. 15.
    Kee, B. L. and Paige, C. J. (1996) In vitro tracking of IL-7 responsiveness and gene expression during commitment of bipotent B-cell/macrophage progenitors. Curr. Biol. 6, 1159–1169.PubMedCrossRefGoogle Scholar
  16. 16.
    Kee, B. L. and Paige, C. J. (1995) Murine B cell development: commitment and progression from multipotential progenitors to mature B lymphocytes. Int. Rev. Cytol. 157, 129–179.PubMedCrossRefGoogle Scholar
  17. 17.
    Rolink, A., ten Boekel, E., Melchers, F., Fearon, D. T., Krop, I., and Andersson, J. (1996) A subpopulation of B220+ cells in murine bone marrow does not express CD19 and contains natural killer cell progenitors. J. Exp. Med. 183, 187–194.PubMedCrossRefGoogle Scholar
  18. 18.
    Hardy, R. R., Carmack, C. E., Shinton, S. A., Kemp, J. D., and Hayakawa, K. (1991) Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173, 1213–1225.PubMedCrossRefGoogle Scholar
  19. 19.
    Pallant, A., Eskenazi, A., Mattei, M. G., Fournier, R. E. K., Carlsson, R., Fukuda, M., and Frelinger, J. G. (1992) Characterization ofcDNAs encoding human leukosialin and localization of the leukosialin gene to chromosome 16. Proc. Natl. Acad. Sci. USA 86, 1328–1331.CrossRefGoogle Scholar
  20. 20.
    Cumano, A. and Paige, C. J. (1992) Enrichment and characterization of uncommitted B-cell precursors from fetal liver a day 12 of gestation. EMBO J. 11, 593–601.PubMedGoogle Scholar
  21. 21.
    Cumano, A., Dieterlen, F., and Godin, I. (1996) Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 86, 907–916.PubMedCrossRefGoogle Scholar
  22. 22.
    Godin, I., Dieterlen-Lievre, F., and Cumano, A. (1995) Emergence of multipotent hematopoietic cells in the yolk sac and para-aortic splanchnopleura of 8.5 dpc mouse embryos. Proc. Natl. Acad. Sci. USA 92, 773–777.PubMedCrossRefGoogle Scholar
  23. 23.
    Cumano, A., Furlonger, C., and Paige, C. J. (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, 6429–6433.PubMedCrossRefGoogle Scholar
  24. 24.
    Huang, H. and Auerbach, R. (1993) Identification and characterization of hematopoietic stem cells from the yolk sac and early mouse embryo. Proc. Natl. Acad. Sci. USA 90,10, 110–10, 114.Google Scholar
  25. 25.
    Jordan, C. T., McKearn, J. T., and Lemischka, I. R. (1990) Cellular and developmental properties of fetal hematopoietic stem cells. Cell 61, 953–963.PubMedCrossRefGoogle Scholar
  26. 26.
    McKearn, J. P., McCubrey, J., and Fagg, B. (1985) Enrichment of hematopoietic precursor cells and cloning of multipotential B-lymphocyte precursors. Proc. Natl. Acad. Sci. USA 82, 7414–7418.PubMedCrossRefGoogle Scholar
  27. 27.
    Li, Y.-S., Wasserman, R., Hayakawa, K., and Hardy, R. R. (1997) Identification of the earliest B lineage stage in mouse bone marrow. Immunity 5, 527–535.CrossRefGoogle Scholar
  28. 28.
    Szilvassy, S. J. and Cory, S. (1993) Phenotypic and functional characterization of competitive long-term repopulating hematopoietic stem cells enriched from 5-fluorouracil-treated murine marrow. Blood 81, 2310–2320.PubMedGoogle Scholar
  29. 29.
    Trevisan, M. and Iscove, N. N. (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, 93–103.PubMedCrossRefGoogle Scholar
  30. 30.
    Spangrude, G. J. and Brooks, D. M. (1993) Mouse strain variability in the expression of the hematopoietic stem cell antigen Ly-6A/E by bone marrow cells. Blood 82, 3327–3332.PubMedGoogle Scholar
  31. 31.
    Hayashi, S.-I., Kunisada, T., Ogawa, M., Sudo, T., Kodama, H., Suda, T., Nishikawa, S., and Nishikawa, S.-I. (1990) Stepwise progression of B lineage differentiation supported by interleukin 7 and other stromal cell molecules. J. Exp. Med. 171, 1683–1695.PubMedCrossRefGoogle Scholar
  32. 32.
    Henderson, A. J., Johnson, A., and Dorshkind, K. (1990) Functional characterization of two stromal cell lines that support B lymphopoiesis. J. Immunol. 145, 423–428.PubMedGoogle Scholar
  33. 33.
    Paige, C. J. ( 1983. Surface immunoglobulin-negative B-cell precursors detected by formation of antibody-secreting colonies in agar. Nature 302, 711–713.PubMedCrossRefGoogle Scholar
  34. 34.
    Rolink, A., Kudo, A., Karasuyama, H., Kikuchi, Y., and Melchers, F. (1991) Long-term proliferating early pre-B cell lines and clones with the potential to develop to surface Ig-positive, mitogen reactive B cells in vitro and in vivo. EMBO J. 10, 327–336.Google Scholar
  35. 35.
    Whitlock, C. A. and Witte, O. N. (1982) Long-term culture B lymphocytes and their precursors from murine bone marrow. Proc. Natl. Acad. Sci. USA 79, 3608–3612.PubMedCrossRefGoogle Scholar
  36. 36.
    Kincade, P. W. (1991) Molecular interactions between stromal cells and B lymphocyte precursors. Sem. Immunol. 3, 379–390.Google Scholar
  37. 37.
    Namen, A. E., Lupton, S., Hjerrild, K., Wignall, J., Mochizuki, D. Y., Schmierer, A., Mosley, B., March, C. J., Urdal, K., Gillis, S., Cosman, D., and Goodwin, R. G. (1988) Stimulation of B cell progenitors by cloned murine interleukin 7. Nature 333, 571–573.PubMedCrossRefGoogle Scholar
  38. 38.
    Cumano, A., Kee, B. L., Ramsden, D. A., Marshall, A., Paige, C. J., and Wu, G. E. (1994) Development of B lymphocytes from lymphoid committed and uncommitted progenitors. Immunol. Rev. 137, 5–33.PubMedCrossRefGoogle Scholar
  39. 39.
    Kee, B. L., Cumano, A., Iscove, N. N., and Paige, C. J. (1994) Stromal cell independent growth of bipotent B cell-macrophage precursors from murine fetal liver. Int. Immunol. 6, 401–407.PubMedCrossRefGoogle Scholar
  40. 40.
    Hilton, D. J., Hilton, A. A., Raicevic, A., Rakar, S., Harrison-Smith, M., Gough, N. M., Begley, C. G., Metcalf, D., Nicola, N. A., and Willson, T. A. (1994) Cloning of a murine IL-11 receptor alpha-chain; requirement for gp130 for high affinity binding and signal transduction. EMBO J. 13, 4765–4775.PubMedGoogle Scholar
  41. 41.
    Yin, T., Yaga, T., Tsang, M. L.-S., Yasukawa, D., Kishimoto, T., and Yang, Y.-C. (1993) Involvement of IL-6 signal transducer gp 130 in IL-11 mediated signal transduction. J. Immunol. 151, 2555–2561.PubMedGoogle Scholar
  42. 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., and Sugges, S. V. (1990) Stem cell factor is encoded at the Sl locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 63, 213–224.Google Scholar
  43. 43.
    Chabot, B., Stephenson, D. A., Chapman, V. M., Besmer, P., and Bernstein, A. (1988) The protooncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335, 88, 89.Google Scholar
  44. 44.
    Geissler, E. N., Ryan, M. A., and Houseman, D. E. (1988) The dominant white spotting locus of the mouse encodes the c-kit protooncogene. Cell 55, 185–192.PubMedCrossRefGoogle Scholar
  45. 45.
    Ray, R. J., Paige, C. J., Furlonger, C., Lyman, S. D., and Rottapel, R. (1996) Flt 3 ligand supports the differentiation of early B cell progenitors in the presence of interleukin-11 and interleukin7. Eur. J. Immunol. 26, 1504–1510.PubMedCrossRefGoogle Scholar
  46. 46.
    Veibry, O. P., Jacobsen, F. W., Cui, L., Lyman, S. D., and Jacobsen, S. E. W. (1996) The flt3 ligand promotes the survival of primitive hemopoietic progenitor cells with myeloid as well as B lymphoid potential. J. Immunol. 157, 2953–2960.Google Scholar
  47. 47.
    Veiby, O. P., Lyman, S. D., and Jacobsen, S. E. W. (1996) Combined signaling through interleukin-7 receptors and flt3 but not c-kit potently and selectively promotes B-cell commitment and differentiation from uncommitted murine bone marrow progenitor cells. Blood 88, 1256–1265.PubMedGoogle Scholar
  48. 48.
    Matthews, W., Jordan, C. T., Gavin, M., Jenkins, N. A., Copeland, N. G., and Lemischka, I. R. (1991) A receptor tyrosine kinase cDNA isolated from a population of enriched primitive hematopoietic cells and exhibiting close genetic linkage to c-kit. Proc. Natl. Acad. Sci. USA 88, 9026–9030.CrossRefGoogle Scholar
  49. 49.
    Goodwin, R. G., Friend, D., Ziegler, S. F., Jerzy, R., Falk, B. A., Gimpel, S., Cosman, D., Dower, S. L., March, C. J., Namen, A. E., and Park, L. S. (1990) Cloning of the human and murine interleukin-7 receptors: demonstration of a soluble form and homology to a new receptor superfamily. Cell 60, 941–951.PubMedCrossRefGoogle Scholar
  50. 50.
    Kondo, M., Takeshita, T., Ishii, N., Nakamura, M., Watanabe, S., Arai, K.-I., and Sugamura, K. (1993) Sharing of the interleukin-2 (IL-2) receptor y chain between receptors for IL-2 and IL-4. Science 262, 1874–1876.PubMedCrossRefGoogle Scholar
  51. 51.
    Noguchi, M., Nakamura, Y., Russell, S. M., Ziegler, S. F., Tsang, M., Cao, X., and Leonard, W. J. (1993) Interleukin-2 receptor y chain: a functional component of the interleukin-7 receptor. Science 262, 1877–1880.PubMedCrossRefGoogle Scholar
  52. 52.
    Russell, S. M., Keegan, A. D., Harada, N., Nakamura, Y., Noguchi, M., Leland, P., Friedmann, M. C., Miyajima, A., Puri, R. K., Paul, W. E., and Leonard, W. J. (1993) Interleukin-2 receptor y chain: a functional component of the interleukin-4 receptor. Science 262, 1880–1883.PubMedCrossRefGoogle Scholar
  53. 53.
    Cumano, A., Dorshkind, K., Gillis, S., and Paige, C. J. (1990) The influence of S17 stromal cells and interleukin 7 on B cell development. Eur. J. Immunol. 20, 2183–2189.PubMedCrossRefGoogle Scholar
  54. 54.
    Lee, G., Namen, A. E., Gillis, S., Ellingsworth, L. R., and Kincade, P. W. (1989) Normal B cell precursors responsive to recombinant murine IL-7 and inhibition of IL-7 activity by transforming growth factor-ß. J. Immunol. 142, 3875–3883.PubMedGoogle Scholar
  55. 55.
    McNiece, I. K., Langley, K. E., and Zsebo, K. M. (1991) The role of recombinant stem cell factor in early B cell development-synergistic interaction with IL-7. J. Immunol. 146, 3785.PubMedGoogle Scholar
  56. 56.
    Fisher, A. G., Burdet, C., LeMeur, M., Haasner, D., Gerber, P., and Ceredig, R. (1992) Lymphoproliferative disorders in an IL-7 transgenic mouse line. Leukemia 2, 566–568.Google Scholar
  57. 57.
    Peschon, J. J., Morrissey, P. J., Grabstein, K. H, Ramsdell, F. J., Maraskovsky, E., Gliniak, B. C., Park, L. S., Ziegler, S. F., Williams, D. E., Ware, C. B., Mayer, J. D., and Davison, B. L. (1994) Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J. Exp. Med. 180, 1955–1959.PubMedCrossRefGoogle Scholar
  58. 58.
    von Freeden-Jeffrey, U., Vieira, P., Lucian, L. A., McNeil, T., Burdach, S. E. G., and Murray, R. (1995) Lymphopenia in IL-7 gene deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181, 1519–1526.CrossRefGoogle Scholar
  59. 59.
    Corcoran, A. E., Smart, F. M., Cowling, R. J., Crompton, T., Owen, M. J., and Venkitaraman, A. R. (1996) The interleukin-7 receptor a chain transmits distinct signals for proliferation and differentiation during B lymphopoiesis. EMBO J. 15, 1924–1932.PubMedGoogle Scholar
  60. 60.
    Nagasawa, T., Hirota, S., Tachibana, K., Takakura, M., Nishikawa, S.-I., Kitamura, Y., Yoshida, N., Kikutani, H., and Kishimoto, T. (1996) Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382, 635–638.PubMedCrossRefGoogle Scholar
  61. 61.
    Rossant, J., Vijh, K. M., Grossi, C. E., and Cooper, M. D. (1986) Clonal origin ofhaematopoietic colonies in the postnatal mouse liver. Nature 319, 507–511.PubMedCrossRefGoogle Scholar
  62. 62.
    Singh, H. (1996) Gene targeting reveals a hierarchy of transcription factors regulating specification of lymphoid cell fates. Curr. Opin. Immunol. 8, 160–165.PubMedCrossRefGoogle Scholar
  63. 63.
    Porcher, C., Swat, W., Rockwell, K., Fujiwara, Y., Alt, F. W., and Orkin, S. H. (1996) The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86, 47–57.PubMedCrossRefGoogle Scholar
  64. 64.
    Robb, L., Elwood, N. J., Elefanty, A. G., Kontgen, F., Li, R., Farnett, L. D., and Begley, C. G. (1996) The SCL gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J. 15, 4123–4129.Google Scholar
  65. 65.
    Mucenski, M. L., McLain, K., Kier, A. B., Swerdlow, S. H., Schreiner, C. M., Miller, T. A., Pietryga, D. W., Scott, W. J., Jr., and Potter, S. S. (1991) A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell 65, 677–689.PubMedCrossRefGoogle Scholar
  66. 66.
    McKercher, S. R., Torbett, B. E., Anderson, K. L., Henkel, G. W., Vestal, D. J., Baribault, H., Klemsz, M., Feeney, A. J., Wu, G. E., Paige, C. J., and Maki, R. A. (1996) Targeted disruption of the PU. 1 gene results in multiple hematopoietic abnormalities. EMBO J. 15, 5647–5658.PubMedGoogle Scholar
  67. 67.
    Scott, E., Simon, M., Anastasi, J., and Singh, H. (1994) Requirement of transcription factor PU. 1 in the development of multiple hematopoietic lineages. Science 265, 1573–1577.PubMedCrossRefGoogle Scholar
  68. 68.
    Nutt, S. L., Urbanek, P., Rolink, A., and Busslinger, M. (1997) Essential functions of PaxS (B SAP) in pro-B cell development: difference between fetal and adult B Tymphopoiesis and reduced V-to-DJ recombination at the IgH locus. Genes Dev. 11, 476–491.PubMedCrossRefGoogle Scholar
  69. 69.
    Urbanek, P., Wang, Z. Q., Fetka, I., Wagner, E. F., and Buslinger, M. (1994) Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax-5/BSAP. Cell 79, 901–913.PubMedCrossRefGoogle Scholar
  70. 70.
    Lin, H. and Grosschedl, R. (1995) Failure ofB-cell differentiation in mice lacking the transcription factor EBF. Nature 376, 263–267.PubMedCrossRefGoogle Scholar
  71. 71.
    Bain, G., Robanus Maandag, E. C., Izon, D. J., Amsen, D., Kruisbeek, A. M., Weintraub, B. C., Krop, I., Schussel, M. S., Feeney, A. J., van Roon, M., van der Valk, M., to Riele, H. P. J., Berns, A., and Murre, C. (1994) E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79, 885–892.PubMedCrossRefGoogle Scholar
  72. 72.
    Zhuang, Y., Soriano, P., and Weintraub, H. (1994) The helix-loop-helix gene E2A is required for B cell formation. Cell 79, 875–884.PubMedCrossRefGoogle Scholar
  73. 73.
    Murre, C. and Baltimore, D. (1992) The helix-loop-helix motif: Structure and Function, in Transcriptional Regulation ( McKnight, S. L. and Yamamoto, K. R., eds.), Cold Spring Harbor Laboratory, NY, pp. 861–879.Google Scholar
  74. 74.
    Murre, C., Bain, G., van Kijk, M. A., Engel, I., Fumari, B. A., Massari, M. E., Matthews, J. R., Quong, M. W., Rivera, R. R., and Stuiver, M. H. (1994) Structure and function of helix-loophelix proteins. BBA 1218, 129–135.Google Scholar
  75. 75.
    Lassar, A. B. and Weintraub, H. (1992) The myogenic helix-loop-helix family: regulators of skeletal muscle determination and differentiation, in Transcriptional Regulation ( McKnight, S. L. and Yamamoto, K. R., eds.), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 1037–1061.Google Scholar
  76. 76.
    Lee, J. E., Hollenberg, S. M., Snider, L., Turner, D. L., Lipnick, N., and Weintraub, H. (1995) Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268, 836–844.PubMedCrossRefGoogle Scholar
  77. 77.
    Tapscott, S. J., Davis, R. L., Thayer, M. J., Cheng, P.-F., Weintraub, H., and Lassar, A. B. (1988) MyoD 1: a nuclear phosphoprotein requiring a myc homology region to convert fibroblasts to myoblasts. Science 242, 405–411.PubMedCrossRefGoogle Scholar
  78. 78.
    Shen, C.-P. and Kadesch, T. (1995) B-cell-specific DNA binding by an E47 homodimer. Mol. Cell. Bio1.15, 4518–4524.Google Scholar
  79. 79.
    Sloan, S. R., Shen, C.-P., McCarrick-Walmsley, R., and Kadesch, T. (1996) Phosphorylation of E47 as a potential determinant of B-cell-specific activity. Mol. Cell. Biol. 16, 6900–6908.PubMedGoogle Scholar
  80. 80.
    Bain, G., Robanus Maandag, E. C., to Riele, H. P. J., Feeney, A. J., Sheehy, A., Schlíssel, M., Shinton, S. A., Hardy, R. R., and Murre, C. (1997) Both E12 and E47 allow commitment to the B cell lineage. Immunity 6, 145–154.PubMedCrossRefGoogle Scholar
  81. 81.
    Jacobs, Y., Xin, X.-Z., Dorshkind, K., and Nelson, C. (1994) Pan/E2A expression precedes immunoglobulin heavy-chain expression during B lymphopoiesis in nontransformed cells, and Pan/E2A proteins are not detected in myeloid cells. Mol. Cell. Biol. 14, 4087–4096.PubMedGoogle Scholar
  82. 82.
    Xin, X. Q., Nelson, C., Collins, C., and Dorshkind, K. (1994) Kinetics of E2A HLH protein expression during myelopoiesis and primary B cell differentiation. J. Immunol. 16, 351–356.Google Scholar
  83. 83.
    Kreider, B. L., Benezra, R., Rovera, G., and Kadesch, T. (1992) Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science 255, 1700–1702.PubMedCrossRefGoogle Scholar
  84. 84.
    Voronova, A. F. and Lee, F. (1994) The E2A and tal-1 helix-loop-helix proteins associate in vivo and are modulated by Id proteins during interleukin 6-induced myeloid differentiation. Proc. Natl. Acad. Sci. USA 91, 5952–5956.PubMedCrossRefGoogle Scholar
  85. 85.
    Hara, H., Sam, M., Maki, R. A., Wu, G. E., and Paige, C. J. (1990) Characterization of a 70Z/3 pre-B cell derived macrophage clone. Differential expression ofhox family genes. Int. Immunol. 2, 691–696.PubMedCrossRefGoogle Scholar
  86. 86.
    Tanaka, T., Wu, G. E., and Paige, C. J. (1994) Characterization of the B cell-macrophage lineage transition in 70Z/3 cells. Eur. J. Immunol. 24, 1544–1548.PubMedCrossRefGoogle Scholar
  87. 87.
    Kee, B. L. and Murre, C. (1997) The basic helix-loop-helix protein E12 acts upstream of EBF and Pax-5 in a cascade of transcription factors that coordinately regulate B lineage development. Submitted.Google Scholar
  88. 88.
    Ghysen, A., Dambly-Chaudiere, C., Jan, L. Y., and Jan, Y.-N. (1993) Cell interaction and gene interactions in peripheral neurogenesis. Genes Dey. 7, 723–733.CrossRefGoogle Scholar
  89. 89.
    Nye, J. S. and Kopan, R. (1995) Vertebrate ligands for Notch. Current Biol. 5, 966–969.CrossRefGoogle Scholar
  90. 90.
    Robey, E., Chang, D., Itano, A., Cado, D., Alexander, H., Lans, D., Weinmaster, G., and Salmon, P. (1996) An activated form of Notch influences the choice between CD4 and CD8 T cell lineages. Cell 87, 483–492.PubMedCrossRefGoogle Scholar
  91. 91.
    Washburn, T., Schweighoffer, E., Gridley, T., Chang, D., Fowlkes, B. J., Cado, D., and Robey, E. (1997) Notch activity influences the aß versus yS T cell lineage decision. Cell 88, 833–843.PubMedCrossRefGoogle Scholar
  92. 92.
    Zhuang, Y., Cheng, P., and Weintraub, H. (1996) B-Lymphocyte development is regulated by the combined dosage of three basic helix-loop-helix genes, E2A, E2–2, and HEB. Mol. Cell. Biol. 16, 2898–2905.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1998

Authors and Affiliations

  • Barbara L. Kee
  • Christopher J. Paige

There are no affiliations available

Personalised recommendations