Long-Term Murine Hemopoietic Cultures as Model Systems for Analysis of B Lymphocyte Differentiation

  • K. Dorshkind
  • O. N. Witte
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 135)

Abstract

The development of B lymphocytes in the bone marrow proceeds in parallel with that of other hemopoietic lineages (Rosse 1976). Phenotypic analysis using antibodies that detect immunoglobulin (Ig; Osmond and Nossal 1974; Abney et al. 1978; Landreth et al. 1981; Rahal and Osmond 1984) and other nonIg cellular determinants (reviewed by Scheid et al. 1982) has identified cells in the B-lymphocyte lineage and contributed greatly to the delineation of stages of that process. However, these studies have not always identified the earliest stages of B lymphopoiesis, or permitted regulatory events that occur during B-cell differentiation to be dissected. In order to facilitate such investigations, considerable efforts have been made to develop in vitro systems that permit all phases of primary B-cell development to be studied under controlled conditions.

Keywords

Agar Leukemia Corticosteroid Sedimentation Nylon 

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References

  1. Abney ER, Cooper MD, Kearney JF, Lawton AR, Parkhouse RME (1978) Sequential expression of immunoglobulin in developing mouse B lymphocytes: a systematic survey that suggests a model for the generation of immunoglobulin isotype diversity. J Immunol 120: 2041–2049PubMedGoogle Scholar
  2. Allen TD, Dexter TM (1976) Cellular interrelationships during in vitro granulopoiesis. Differentiation 6: 191–194PubMedCrossRefGoogle Scholar
  3. Aspinall R, Owen JJT (1983) An investigation into the B lymphopoietic capacity of long-term bone marrow cultures. Immunilogy 48: 9–15Google Scholar
  4. Boettiger D, Anderson S, Dexter TM (1985) Effect of SRC on hemopoietic pronator cells: increased self-renewal without leukemia. Cell 36: 763–773CrossRefGoogle Scholar
  5. Bosma GC, Custer RP, Bosma MJ (1983) A severe combined immunodeficiency mutation in the mouse. Nature 301: 527–530PubMedCrossRefGoogle Scholar
  6. Cass CE, Lowe JK, Machak JM, Henderson JF (1977) Biological effects of inhibition of guanine nucleotide synthesis by mycophenolic acid in cultured neurblastoma cells. Cancer Res 37: 3314–3320PubMedGoogle Scholar
  7. Denis KA, Witte ON (1986) In vitro development of B lymphocyte from long-term cultured precursor cells. Proc Natl Acad Sci USA (to be published)Google Scholar
  8. Denis KA, Treiman LJ, St Claire JI, Witte ON (1984) Long-term cultures of murine fetal liver retain very early B lymphoid phenotype. J Exp Med 160: 1087–1101PubMedCrossRefGoogle Scholar
  9. Dexter TM, Spooncer E (1978) Loss of immunoreactivity in long-term bone marrow culture. Nature 275: 135–136PubMedCrossRefGoogle Scholar
  10. Dexter TM, Allen TD, Lajtha LG (1977a) Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol 91: 335–344PubMedCrossRefGoogle Scholar
  11. Dexter TM, Moore MAS, Sheridan APC (1977b) Maintenance of hemopoietic stem cells and production of differentiated progeny in allogeneic and semiallogeneic bone marrow chimeras in vitro. J Exp Med 145: 1612–1616PubMedCrossRefGoogle Scholar
  12. Dick JE, Magli MC, Huszar D, Phillips RA, Bernstein A (1985) Introduction of a selectable gene into primitive stem cells capable of long–term reconstitution of the hemopoietic system of W/W mice. Cell 42: 71–79PubMedCrossRefGoogle Scholar
  13. Dorshkind K (1986) In vitro differentiation of B lymphocytes from primitive hemopoietic precursors present in long-term bone marrow cultures. J Immunol 136: 422–429PubMedGoogle Scholar
  14. Dorshkind K, Phillips RA (1982) Maturational state of lymphoid cells in long-term bone marrow cultures. J Immunol 129: 2444–2450PubMedGoogle Scholar
  15. Dorshkind K, Phillips RA (1983) Characterization of early B lymphocyte precursors present in long-term bone marrow cultures. J Immunol 131: 2240–2245PubMedGoogle Scholar
  16. Dorshkind K, Keller GM, Phillips RA, Miller RG, Bosma GC, O’Toole M, Bosma MJ (1984) Functional status of cells from lymphomyeloid tissues in mice with severe combined immunodeficiency disease. J Immunol 132: 1804–1808PubMedGoogle Scholar
  17. Dorshkind K, Schouest L, Fletcher WH (1985) Morphologic analysis of long-term bone marrow cultures that support B lymphopoiesis or myelopoiesis. Cell Tissue Res 239: 375–382PubMedCrossRefGoogle Scholar
  18. Dorshkind K, Johnson A, Collins L, Keller GM, Philips RA (1986) Generation of purified stromal cell cultures that support lymphoid and myeloid precursors. J Immunol Methods 89: 37–47PubMedCrossRefGoogle Scholar
  19. Fulop GM, Osmond DG (1983) Regulation of bone marrow lymphocyte production. III. Increased production of B and non-B lymphocytes after administering systemic antigens. Cell Immunol 75: 80–90PubMedCrossRefGoogle Scholar
  20. Johnson A, Dorshkind K (1986) Stromal cells in myeloid and lymphoid long-term bone marrow cultures can support multiple hemopoietic lineages and modulate their production of hemopoietic growth factors. Blood 68: 1348–1354PubMedGoogle Scholar
  21. Jones-Villeneuve E, Phillips RA (1980) Potentials for lymphoid differentiation by cells from long-term cultures of bone marrow. Exp Hematol 8: 65–76PubMedGoogle Scholar
  22. Joyner A, Keller G, Phillips RA, Bernstein A (1983) Retrovirus mediated transfer of a bacterial gene into mouse hematopoietic progenitor cells. Nature 305: 206–208CrossRefGoogle Scholar
  23. Jyonouchi H, Kincade PW (1984) Precocious and enhanced functional maturation of B lineage cells in New Zealand black mice during embryonic development. J Exp Med 159: 1277–1282PubMedCrossRefGoogle Scholar
  24. Keller G, Paige C, Gilboa E, Wagner EF (1985) Expression of a foreign gene in myeloid and lymphoid cells derived from multipotent haematopoietic precursors. Nature 318: 149–154PubMedCrossRefGoogle Scholar
  25. Keller GM, Johnson GR, Phillips RA (1983) Hemopoiesis in spleen and bone marrow cultures. J Cell Physiol 116: 7–15PubMedCrossRefGoogle Scholar
  26. Kincade PW (1977) Defective colony formation by B lymphocytes from CBA/N and C3H/HeJ mice. J Exp Med 145: 249–263PubMedCrossRefGoogle Scholar
  27. Kincade PW, Lee G, Paige CJ, Scheid MP (1981) Cellular interactions affecting the maturation of murine B lymphocyte precursors in vitro. J Immunol 127: 255–260PubMedGoogle Scholar
  28. Kurland JI, Ziegler SF, Witte ON (1984) Long-term cultured B lymphocytes and their precursors reconstitute the B-lymphocyte lineage in vivo. Proc Natl Acad Sci USA 81: 7754–7558CrossRefGoogle Scholar
  29. Landreth KS, Rosse C, Clagett J (1981) Myelogenous production and maturation of B lymphocytes in the mouse. J Immunol 127: 2027–2034PubMedGoogle Scholar
  30. Landreth KS, Kincade PW, Lee G, Medlock ES (1983) Phenotypic and functional characterization of murine B lymphocyte precursors isolated from fetal and adult tissues. J Immunol 131: 572–580PubMedGoogle Scholar
  31. Landreth KS, Engelhard D, Bear MH, Kincade PW, Kapoor W, Good RA (1985) Regulation of human B lymphopoiesis: Effect of urinary activity associated with cyclic neutropenia. J Immunol 134: 2305–2309PubMedGoogle Scholar
  32. Lanotte M, Scott D, Dexter TM, Allen TD (1982) Clonal preadipocyte cell lines with different phenotypes derived from murine marrow stroma. Factors influencing growth and adipogenesis in vitro. J Cell Physiol 111: 177–186PubMedCrossRefGoogle Scholar
  33. Lau CY, Melchers F, Miller RG, Phillips RA (1979) In vitro differentiation of B lymphocytes from pre-B cells. J Immunol 122: 1273–1277PubMedGoogle Scholar
  34. Lichtman MA (1981) The ultrastrueture of the hemopoietic environment of the marrow: a review. Exp Hematol 9: 391–420PubMedGoogle Scholar
  35. Mauch P, Greenberger JS, Botnick LE, Hannon EC, Hellman S (1980) Evidence for structured variation in self–renewal capacity within long-term bone marrow cultures. Proc Natl Acad Sci USA 77: 2927–2930PubMedCrossRefGoogle Scholar
  36. Melchers F (1977) B lymphocyte development in fetal liver. I. Development of reactivities to B cell mitogens in vivo and in vitro. Eur J Immunol 7: 476–481PubMedCrossRefGoogle Scholar
  37. Mongini PKA, Paul WE, Metcalf ES (1983) IgG subclass, IgE, and IgA anti-trinitrophenyl antibody production within trinitrophenyl-Ficoll-responsive B cell clones. Evidence in support of three distinct switching pathways. J Exp Med 157: 69–85PubMedCrossRefGoogle Scholar
  38. Nagasawa R, Kanagawa O, Tittle TV, Chiller JM (1985) In vivo maturation of in vitro derived pre-B cells. J Immunol 135: 965–972PubMedGoogle Scholar
  39. Nishikawa S, Kina T, Amagai T, Katsura Y (1985) Early B cell precursors in long-term bone marrow culture: selective development in the bone marrow of irradiated recipients. Eur J Immunol 15: 696–701PubMedCrossRefGoogle Scholar
  40. Osmond DG, Nossal GJV (1974) Differentiation of lymphocytes in mouse bone marrow. II. Kinetics of maturation and renewal of antiglobulin-binding cells studied by double labelling. Cell Immunol 13: 132–145PubMedCrossRefGoogle Scholar
  41. Owen JJT, Cooper MD, Raff MC (1974) In vitro generation of B lymphocytes in mouse fetal liver; a mammalian bursal equivalent. Nature 249: 361–363PubMedCrossRefGoogle Scholar
  42. Paige CJ (1983) Surface immunoglobulin-negative B-cell precursors detected by formation of antibody-secreting colonies in agar. Nature 302: 711–713PubMedCrossRefGoogle Scholar
  43. Paige CJ, Gisler RH, McKearn JP, Iscove NN (1984) Differentiation of murine B cell precursors in agar culture. Frequency, surface marker analysis and requirements for growth of clonable pre-B cells. Eur J Immunol 17: 979–987CrossRefGoogle Scholar
  44. Palacios R, Steinmetz M (1985) IL-3 dependent mouse clones that express B-220 surface antigen, contain Ig genes in germ-line configuration, and generate B lymphocytes. Cell 41: 727–734PubMedCrossRefGoogle Scholar
  45. Palacios R, Henson G, Steinmetz M, McKearn J (1984) Interleukin 3 supports growth of mouse Pre-B cells clones in vitro. Nature 309: 126–134PubMedCrossRefGoogle Scholar
  46. Phillips RA (1980) Enhanced lymphoid and decreased myeloid reconstituting ability of stem cells from long-term cultures of mouse bone marrow. J Supramol Struct 14: 77–83PubMedCrossRefGoogle Scholar
  47. Phillips RA (1985) Comparison of different assays for multipotent haemopoietic stem cells. In: Ford RJ, Maizel AL (eds) Mediators in cell growth and differentiation. Raven, New York, p 135Google Scholar
  48. Phillips RA, Bosma M, Dorshkind K (1984) Reconstitution of immune-deficient mice with cells from long-term bone marrow cultures. In: Wright DG, Greenberger JS (eds), Long-term bone marrow culture. Liss, New York, p 309Google Scholar
  49. Rahal MD, Osmond DG (1984) Heterogeneity of bone marrow lymphocytes: Radioautographic detection of pre-B cells bearing cytoplasmic μ chains and of B and T lymphocytes and characterization of null lymphoid cells. Cell Immunol 87: 379–388PubMedCrossRefGoogle Scholar
  50. Rosenberg N, Baltimore D (1980) Abelson virus. In: Klein G (ed) Viral oncology, Raven, New York, p 187Google Scholar
  51. Rosse C (1976) Small lymphocyte and transitional cell populations of the bone marrow; their role in the mediation of immune and hemopoietic progenitor cell functions. Int Rev Cytol 45: 155–290PubMedCrossRefGoogle Scholar
  52. Scheid MP, Landreth KS, Tung JS, Kincade PW (1982) Preferential but nonexclusive expression of macromolecular antigens on B-lineage cells. Immunol Rev 69: 141–159PubMedCrossRefGoogle Scholar
  53. Schrader JW, 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: 823–828PubMedCrossRefGoogle Scholar
  54. Schrader JW, Goldschneider I, Bollum FJ, Schrader S (1979) In vitro studies in lymphocyte differentiation. II. Generation of terminal deoxynucleotidyl transferase-positive cells in long-term cultures of mouse bone marrow. J Immunol 122: 2337–2339PubMedGoogle Scholar
  55. Song ZX, Quesenberry PJ (1984) Radioresistant murine marrow stromal cells: a morphologic and functional characterization. Exp Hematol 12: 523–533PubMedGoogle Scholar
  56. Song ZX, Shadduck RK, Innes DJ, Waheed A, Quesenberry PJ (1985) Hematopoietic factor production by a cell line (TC-1) derived from adherent murine marrow cells. Blood 66: 273–281PubMedGoogle Scholar
  57. Tavassoli M (1982) Ultrastructural and radiobiological characterization of stromal cells in continuous, long-term marrow cell line. In: Johari O (ed) Scanning electron mcirosocpy. SEM, AMF O’Hare, Chicago, p 349Google Scholar
  58. Van der Putten H, Botteri FM, Miller AD, Rosenfeld MG, Fan H, Evans RM, Verma IM (1985) Efficient insertion of genes into the mouse germ-line via retroviral vectors. Proc Natl Acad Sci USA 82: 6148–6152PubMedCrossRefGoogle Scholar
  59. Weiss L (1970) Transmural cellular passage in vascular sinuses of rat bone marrow. Blood 36: 189–208PubMedGoogle Scholar
  60. Whitlock CA, Witte ON (1982) Long-term culture of B lymphocytes and their precursors from murine bone marrow. Proc Natl Acad Sci USA 79: 3608–3612PubMedCrossRefGoogle Scholar
  61. Whitlock CA, Ziegler SF, Treiman LJ, Stafford JI, Witte ON (1983) Differentiation of cloned populations of immature B cells after transformation with Abelson murine leukemia virus. Cell 32: 903–911PubMedCrossRefGoogle Scholar
  62. Whitlock CA, Robertson D, Witte ON (1984) Murine B cell lymphopoiesis in long-term culture. J Immunol Methods 16: 353–369CrossRefGoogle Scholar
  63. Williams N, Jackson H, Sheridan APC, Murphy MJ, Eisle A, Moore MAS (1978) Regulation of megakaryopoiesis in long-term murine bone marrow cultures. Blood 51: 245–255PubMedGoogle Scholar
  64. Williams DA, Lemischka IR, Nathans DG, Mulligan RC (1984) Induction of new genetic material into pluripotent haemopoietic stem cells of the mouse. Nature 310: 476–480PubMedCrossRefGoogle Scholar
  65. Wolf NS, Trentin JJ (1968) Hemopoietic colony studies. V. Effect of hemopoietic organ stroma on differentiation. J Exp Med 127: 205–214CrossRefGoogle Scholar
  66. Ziegler SF, Treiman LJ, Witte ON (1984) K gene diversity among the clonal progeny of pre-B lymphocytes. Proc Natl Acad Sci USA 81: 1529–1533PubMedCrossRefGoogle Scholar
  67. Zipori D, Duskin D, Tamir M, Argaman A, Toledo J, Malik Z (1985) Cultured mouse marrow stromal cell lines. II. Distinct subtypes differing in morphology, collagen types, myelopoietic factors, and leukemic cell growth modulating activities. J Cell Physiol 122: 81–90PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1987

Authors and Affiliations

  • K. Dorshkind
    • 1
  • O. N. Witte
    • 2
  1. 1.Division of Biomedical SciencesUniversity of CaliforniaRiversideUSA
  2. 2.Department of Microbiology and Molecular Biology InstituteUniversity Of CaliforniaLos AngelesUSA

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