Advertisement

Differences in Human B Cell Differentiation

  • Peter D. Burrows
  • Hiromi Kubagawa
  • Norihiro Nishimoto
  • William G. Kerr
  • Gary V. Borzillo
  • Linda M. Hendershot
  • Max D. Cooper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 292)

Abstract

A comparative approach to the study of immune system development has been extremely useful in our understanding of this complex process. For example, it was first experimentally demonstrated in chickens that the immune system had two antigen specific components, T and B cells. This dichotomy was subsequently found to exist in organisms as diverse as humans and frogs.1,2 Extrapolation of many findings in mammalian B cell differentiation can often be readily made between humans and mice. However, we will discuss several instances where models of B cell development that have been derived from murine systems do not appear to be directly applicable to humans. In some cases the apparent differences may simply be due to the experimental systems employed, but in others there may be fundamental differences between the two species. Since our purpose is not to minimize the value of comparative analysis, recent data concerning early B cell development in humans that most likely is true in mice will also be discussed.

Keywords

Heavy Chain Staphylococcus Aureus Isotype Switching Light Chain Gene Heavy Chain Locus 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    M. D. Cooper and A. R. Lawton, The development of the immune system, Sci. Am. 231:58 (1974).PubMedCrossRefGoogle Scholar
  2. 2.
    L. Du-Pasquier, J. Schwager and M. F. Flajnik, The immune system of Xenopus, Ann. Rev. Immunol. 7:251 (1989).CrossRefGoogle Scholar
  3. 3.
    M. D. Cooper and P. D. Burrows, B cell differentiation, in “Immunoglobulin Genes” T. Honjo, F. W. Alt, and T. H. Rabbitts, eds., Academic Press, London (1989).Google Scholar
  4. 4.
    F. W. Alt, T. K. Blackwell, R. A. DePinho, and M. Reth, Regulation of genome rearrangement events during lymphocyte differentiation, Immunol. Rev. 89:5 (1986).PubMedCrossRefGoogle Scholar
  5. 5.
    U. Storb, Immunoglobulin gene analysis in transgenic mice, in “Immunoglobulin Genes”, T. Honjo, F. W. Alt and T. H. Rabbitts, eds., Academic Press, London, (1989).Google Scholar
  6. 6.
    S. M. Fu, J. N. Hurley, J. M. McCune, H. G. Kunkel, and R. A. Good, Pre-B cells and other possible precursor lymphoid cell lines derived from patients with X-linked agammaglobulinemia, J. Exp. Med. 152:1519 (1980).PubMedCrossRefGoogle Scholar
  7. 7.
    S. Katamine, M. Otsu, K. Tada, S. Tsuchiya, T. Sato, N. Ishida, T. Honjo, and Y. Ohno, Epstein-Barr virus transforms precursor B cells even before immunoglobulin gene rearrangements, Nature 309:368 (1984).CrossRefGoogle Scholar
  8. 8.
    T. F. Tedder, L. T. Clement, and M. D. Cooper, Expression of C3d receptors during human B cell differentiation: Immunofluorescence analysis with the HB-5 monoclonal antibody. J. Immunol. 133:678 (1984).PubMedGoogle Scholar
  9. 9.
    G. R. Nemerow, M. D. Moore, and N. R. Cooper, Structure and function of the B lymphocyte Epstein-Barr virus/C3d receptor, Adv. Cancer. Res. 54:273 (1990).PubMedCrossRefGoogle Scholar
  10. 10.
    H. Kubagawa, M. D. Cooper, A. J. Carroll, and P. D. Burrows, Light chain gene expression before heavy chain gene rearrangement in pre-B cells transformed by Epstein-Barr virus, Proc. Natl. Acad. Sci. USA 86:2356 (1989).PubMedCrossRefGoogle Scholar
  11. 11.
    S. Tonegawa, Somatic generation of antibody diversity, Nature 302:575 (1983).PubMedCrossRefGoogle Scholar
  12. 12.
    G. D. Yancopoulos and F. W. Alt, Regulation of the assembly and expression of variable-region genes, Ann. Rev. Immunol. 4:339 (1986).CrossRefGoogle Scholar
  13. 13.
    B. Lange, M. Valtieri, D. Santoli, D. Caracciola, F. Mavilio, I. Gemperlein, C. Griffin, B. Emanuel, J. Finan, P. Nowell, and G. Rovera, Growth factor requirements of childhood acute leukemia: establishment of GM-CSF-dependent cell lines, Blood 70:192 (1987).PubMedGoogle Scholar
  14. 14.
    K. Sheibani, A. Wu, J. Ben-Erza, R. Stroup, H. Rappaport, and C. Winberg, Rearrangement of kappa-chain and T-cell receptor beta-chain genes in malignant lymphomas of “T-cell” phenotype, Am. J. Path. 129:201 (1987).PubMedGoogle Scholar
  15. 15.
    D. Delia, M. G. Borrello, E. Berti, M. A. Pierotti, D. Biassoni, R. Gianotti, I. Alessi, M. G. Rizzetti, R. Caputo, and G. Delia Porta, Clonal immunoglobulin gene rearrangements and normal T-cell receptor, bcl-2, and c-myc genes in primary cutaneous B-cell lymphomas, Cancer Res. 49:4901 (1989).Google Scholar
  16. 16.
    M. D. Schlissel and D. Baltimore, Activation of immunoglobulin kappa gene rearrangement correlates with induction of germline kappa gene transcription, Cell 58:1001 (1989).PubMedCrossRefGoogle Scholar
  17. 17.
    E. J. Siden, D. Baltimore, D. Clark, and N. Rosenberg, Immunoglobulin synthesis by lymphoid cells transformed in vitro by Abelson Murine leukemic virus, Cell 16:389 (1979).PubMedCrossRefGoogle Scholar
  18. 18.
    J. Sen, N. Rosenberg, and S. J. Burakoft, Expression and ontogeny of CD2 on murine B cells, J. Immunol. 144:2925 (1990).PubMedGoogle Scholar
  19. 19.
    H. Kubagawa, P. D. Burrows, C. E. Grossi, J. Mestecky, and M. D. Cooper, Precursor B cells transformed by Epstein-Barr virus undergo sterile plasma cell differentiation: J chain expression without immunoglobulin, Proc. Natl. Acad. Sci. USA 85:875 (1988).PubMedCrossRefGoogle Scholar
  20. 20.
    P. A. Scherle, K. Dorshkind, and O. N. Witte, Clonal lymphoid progenitor cell lines expressing the BCR/ABL oncogene retain full differentiative function, Proc. Natl. Acad. Sci. USA 87:1908 (1990).PubMedCrossRefGoogle Scholar
  21. 21.
    R. Wall. M. Birskin, C. Carter, H. Govan, A. Taylor, and P. Kincade, A labile inhibitor blocks immunoglobulin k light chain gene transcription in a pre-B leukemic cell line, Proc. Natl. Acad. Sci. USA 83:295 (1986).PubMedCrossRefGoogle Scholar
  22. 22.
    P. A. Baeuerle and D. Baltimore, IkB: a specific inhibitor of the NF-/cB transcription factor, Science 242:540 (1988).PubMedCrossRefGoogle Scholar
  23. 23.
    M. J. Lenardo and D. Baltimore, NFkB: a pleiotropic mediator of inducible and tissue-specific gene control, Cell 58:227 (1989).PubMedCrossRefGoogle Scholar
  24. 24.
    C. Jamieson, F. Mauxion, and R. Sen, Identification of a functional NFkB binding site in the murine T cell receptor 2 locus, J. Exp. Med. 170:1737 (1989).PubMedCrossRefGoogle Scholar
  25. 25.
    P. D. Burrows, J. F. Kearney, A. R. Lawton, and M. D. Cooper, Pre-B cells: Bone marrow persistence in anti-suppressed mice, conversion to B lymphocytes and recovery after destruction by cyclophosphamide, J. Immunol. 120:1526 (1978).PubMedGoogle Scholar
  26. 26.
    G. M. Fulop and D. G. Osmond, Regulation of bone marrow lymphocyte production. IV. Cells mediating the stimulation of marrow lymphocyte production by sheep red blood cells: studies in anti-IgM-suppressed mice, athymic mice, and silica-treated mice, Cell. Immunol. 75:91 (1983).PubMedCrossRefGoogle Scholar
  27. 27.
    I. G. Haas and M. R. Wabl, Immunoglobulin heavy chain binding protein, Nature 306:387 (1983).PubMedCrossRefGoogle Scholar
  28. 28.
    L. M. Hendershot, D. Bole, and J. F. Kearney, The role of immunoglobulin heavy chain binding protein, Immunol. Today 8:111 (1987).CrossRefGoogle Scholar
  29. 29.
    S. Munro and H. R. B. Pelham, An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein, Cell 46:291 (1986).PubMedCrossRefGoogle Scholar
  30. 30.
    L. B. Vogler, W. Crist, D. E. Bockman, E. R. Pearl, A. R. Lawton, and M. D. Cooper, Pre-B cell leukemia: a new phenotype of childhood lymphoblastic leukemia, New Engl. J. Med. 298:872 (1978).PubMedCrossRefGoogle Scholar
  31. 31.
    H. W. Findley, Jr., M. D. Cooper, T. H. Kim, C. Alvarodo, and A. H. Ragab, Two new acute lymphoblastic leukemia cell lines with early B cell phenotype, Blood 60:1305 (1982).PubMedGoogle Scholar
  32. 32.
    N. Sakaguchi and F. Melchers, 5, a new light chain related locus selectively expressed in pre-B lymphocytes, Nature 324:579 (1986).CrossRefGoogle Scholar
  33. 33.
    A. Kudo and F. Melchers, A second gene, Vpre-B, in the 5 locus of the mouse which appears to be selectively expressed in pre-B lymphocytes, EMBO J. 6:2267 (1987).PubMedGoogle Scholar
  34. 34.
    S. Pillai and D. Baltimore, Formation of disulphide-linked 22tetramers in pre-B cells by the 18 K -immunoglobulin light chain, Nature 329:172 (1987).PubMedCrossRefGoogle Scholar
  35. 35.
    S. Pillai and D. Baltimore, The omega and iota surrogate immunological light chains, Curr. Top. Microbiol. Immunol. 137:136 (1988).PubMedGoogle Scholar
  36. 36.
    W. G. Kerr, M. D. Cooper, L. Feng, P. D. Burrows, and L. M. Hendershot, Mu heavy chains can associate with a pseudo-light chain complex (L) in human pre-B cells, Inter. Immunol. 1:355 (1989).CrossRefGoogle Scholar
  37. 37.
    H. Kubagawa, T. Ohno, P. D. Burrows, and M. D. Cooper, Putative human -L complex defined by a monoclonal antibody (MAb) with reactivity to an IgM conformational determinant, 7th Inter. Congress of Immunol ,p. 180, A34–13 (1989).Google Scholar
  38. 38.
    S. Bauer, A. Kudo, and F. Melchers, Structure and pre-B lymphocyte expression of the Vpre-B gene in humans and conservation of its structure in other mammalian species, EMBO J. 7:111 (1988).PubMedGoogle Scholar
  39. 39.
    F. Mami, P. A. Cazenave, and T. J. Kindt, Conservation of the immunoglobulin C5 gene in the Mus genus, EMBO J. 7:117 (1988).PubMedGoogle Scholar
  40. 40.
    C. Schiff, M. Milili, and M. Fougereau, Isolation of early immunoglobulin -like gene transcripts in human fetal liver, Eur. J. Immunol. 19:1873 (1989).PubMedCrossRefGoogle Scholar
  41. 41.
    G. F. Hollis, R. J. Evans, J. M. Stafford-Hollis, S. J. Korsmeyer, and J. P. McKearn, Immunoglobulin light-chain-related genes 14.1 and 16.1 are expressed in pre-B cells and may encode the human immunoglobulin light chain protein, Proc. Natl. Acad. Sci. USA 86:5552 (1989).PubMedCrossRefGoogle Scholar
  42. 42.
    T. Ohno, M. D. Cooper, M. C. Sekar, P. D. Burrows, L. M. Hendershot, and H. Kuba\gawa, Biochemical and functional characterization of the heavy chain and the surrogate light chain complex expressed on human pre-B cell lines, Fed. Proc. 4:A1846 (1990).Google Scholar
  43. 43.
    N. Nishimoto, H. Kubagawa, T. Ohno, G. L. Gartland, A. K. Stankovic, and M. D. Cooper, Normal pre-B cells can express theheavy chain and surrogate light chain complex on their surface, Fed. Proc. 4.A2885 (1990).Google Scholar
  44. 44.
    P. W. Kincade, G. Lee, C. E. Pietrangeli, S. Hayashi, and G. M. Gimble, Cells and molecules that regulate B lymphopoiesis in bone marrow, Ann. Rev. Immunol. 7:111 (1989).CrossRefGoogle Scholar
  45. 45.
    G. Moller, Immunoglobulin D: Structure, synthesis, membrane representation and function, Immunol. Rev. 37:1 (1977).Google Scholar
  46. 46.
    F. R. Blattner and P. W. Tucker, The molecular biology of immunoglobulin D, Nature 307:417 (1984).PubMedCrossRefGoogle Scholar
  47. 47.
    E. L. Mather, K. J. Nelson, J. Haimovich, and R. P. Perry, Mode of regulation of immunoglobulin - and -chain expression varies during B lymphocyte maturation, Cell 36:329 (1984).PubMedCrossRefGoogle Scholar
  48. 48.
    D. Yuan and P. W. Tucker, Transcriptional regulation of the -6 heavy chain locus in normal murine B lymphocytes, J. Exp. Med. 160:564 (1984).PubMedCrossRefGoogle Scholar
  49. 49.
    D. S. Rowe and J. L. Fahey, A new class of human immunoglobulins. I. A unique myeloma protein, J. Exp. Med. 121:171 (1965).PubMedCrossRefGoogle Scholar
  50. 50.
    A. Bargelles, G. Corte, E. E. Cosulich, and M. Ferrarini, Presence of serum IgD and IgD-containing plasma cells in the mouse, Eur. J. Immunol. 9:490 (1979).CrossRefGoogle Scholar
  51. 51.
    W. G. Kerr, L. M. Hendershot, arid P. D. Burrows, Regulation of -and -chain expression in human B-lineage cells, J. Immunol ,(in press, 1990).Google Scholar
  52. 52.
    D. Yuan and P. W. Tucker, Regulation of IgM and IgD synthesis in B lymphocytes. I. Changes in biosynthesis of mRNA for -and -chains, J. Immunol. 132:1561 (1984).PubMedGoogle Scholar
  53. 53.
    W. A. Kuziel, C. J. Word, D.. Yuan, M. B. White, J. F. Mushinski, F. R. Blattner, and P. W. Tucker, The human immunoglobulin C-Clocus: regulation of and RNA expression during B cell development, Inter. Immunol. 1:310 (1989).CrossRefGoogle Scholar
  54. 54.
    A. Iglesias, M. Lamers, and G. Kohler, Expression of immunoglobulin 8 chains causes allelic exclusion in transgenic mice, Nature 330:482 (1987).PubMedCrossRefGoogle Scholar
  55. 55.
    R. F. Coico, G. W. Siskind, and G. J. Thorbecke, Role of IgD and T delta cells in the regulation of the humoral immune response, Immunol. Rev. 105:45–67 (1988).PubMedCrossRefGoogle Scholar
  56. 56.
    W. E. Gathings, A. R. Lawton, and M. D. Cooper, Immunofluorescent studies of the development of pre-B cells, B lymphocytes and immunoglobulin isotype diversity in humans, Eur. J. Immunol. 7:804 (1977).PubMedCrossRefGoogle Scholar
  57. 57.
    E. R. Abney, M. D. Cooper, J. F. Cooper, A. R. Lawton, and R. M. E. Parkhouse, Sequential expression of immunoglobulin on developing mouse B lymphocytes. A systematic survey which suggests a model for the generation of immunoglobulin isotype diversity, J. Immunol. 120:2041 (1978).PubMedGoogle Scholar
  58. 58.
    T. Honjo, A. Shimizu, and Y. Yaoita, Constant-region genes of the immunoglobulin heavy chain and the molecular mechanism of class switching, in , T. Honjo, F. W. Alt, and T. H. Rabbitts, eds., Academic Press, London (1989).Google Scholar
  59. 59.
    C. Esser and A. Radbruch, Immunoglobulin class switching: molecular and cellular analysis, Ann. Rev. Immunol. 8:717 (1990).CrossRefGoogle Scholar
  60. 60.
    Y. Yaoita, Y. Kumagai, K. Okumura, and T. Honjo, Expression of lymphocyte surface IgE does not require switch recombination, Nature 297:697 (1982).PubMedCrossRefGoogle Scholar
  61. 61.
    A. P. Perlmutter and W. Gilbert, Antibodies of the secondary response can be expressed without switch recombination in normal mouse B cells, Proc. Natl. Acad. Sci. USA 81:7189 (1984).PubMedCrossRefGoogle Scholar
  62. 62.
    E. A. Weiss, P. W. Tucker, and D. Yuan, The C gene is transcribed in IgG-bearing B lymphocytes, J. Molec. Cell. Immunol. 3:69 (1987).Google Scholar
  63. 63.
    Y. W. Chen, C. Word, V. Dev, J. W. Uhr, E. S. Vitetta, and P. W. Tucker, Double isotype production by a neoplastic B cells lines. II. Allelically excluded production of ; and 51 heavy chians without CH gene rearrangement, J. Exp. Med. 164:562 (1986).PubMedCrossRefGoogle Scholar
  64. 64.
    T. Miyawaki, J. L. Butler, A. Radbruch, G. L. Gartland, and M. D. Cooper, Isotype commitment of human B cells that are transformed by Epstein-Barr virus, submitted.Google Scholar
  65. 65.
    A. Shimizu, M. C. Nussenzweig, T. R. Mizuta, P. Leder, and T. Honjo, Immunoglobulin double isotype expression by trans-mRNA in a human immunoglobulin transgenic mouse, Proc. Natl. Acad. Sci. USA 86:8020 (1989).PubMedCrossRefGoogle Scholar
  66. 66.
    G. B. Borzillo, M. D. Cooper, H. Kubagawa, A. Landay, and P. D. Burrows, Isotype switching in human B lymphocyte malignancies occurs by DNA deletion: evidence for nonspecific switch recombination, J. Immunol. 139:1326 (1987).PubMedGoogle Scholar
  67. 67.
    G. V. Borzillo, M. D. Cooper, L. F. Bertoli, A. Landay, R. Castleberry, and P. D. Burrows, Lineage and stage specificity of isotype switching in humans, J. Immunol. 141:3625 (1988).PubMedGoogle Scholar
  68. 68.
    C. Schultz, J. Petrini, J. Collins, J. L. Claflin, K. A. Denis, P. Gearhart, C. Gritzmacher, T. Manser, M. Shulman, and W. Dunnick, Patterns and extent of isotype-specificity in the murine H chain switch DNA rearrangement, J. Immmunol. 144:363 (1990).Google Scholar
  69. 69.
    W. G. Kerr and P. D. Burrows, Stage-specific transcription of human Cand C; loci during human B cell differentiation, submitted.Google Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • Peter D. Burrows
    • 1
  • Hiromi Kubagawa
    • 1
  • Norihiro Nishimoto
    • 1
  • William G. Kerr
    • 3
  • Gary V. Borzillo
    • 4
  • Linda M. Hendershot
    • 4
  • Max D. Cooper
    • 1
    • 2
  1. 1.Division of Developmental and Clinical Immunology, Departments of Pediatrics, Medicine and MicrobiologyUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.The Howard Hughes Medical InstituteBirminghamUSA
  3. 3.Department of GeneticsStanford University School of MedicineStanfordUSA
  4. 4.Department of Tumor Cell BiologySt. Jude Children’s Research HospitalMemphisUSA

Personalised recommendations