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. 1991 Nov 15;88(22):9944–9948. doi: 10.1073/pnas.88.22.9944

Peritoneal B cells regulate the numbers of allotype-matched pre-B and B cells in bone marrow.

M A Marcos 1, A Sundblad 1, E Malenchère 1, A Coutinho 1
PMCID: PMC52843  PMID: 1946463

Abstract

The mechanisms regulating growth and differentiation of B-cell precursors in adult bone marrow (BM) and/or selecting immunocompetent cells for peripheral export are poorly understood. We report here that small numbers of activated peritoneal B cells selectively suppress the numbers of small pre-B (B220+IgM-) and B (B220+IgM+) cells in BM, if transferred into syngeneic adult mice. No significant alterations are detected in other BM cell lineages or in peripheral lymphocytes of recipient mice. Both CD5+ and CD5- peritoneal B cells display this activity, but the same or higher numbers of similarly activated splenic B cells have no effect. Suppression of B-lineage cells is independent of T lymphocytes but requires that both donor and recipient are matched for immunoglobulin allotypes. These findings provide evidence for regulation of BM B-cell production by peripheral B cells, especially when located in the peritoneal cavity, and ascribe regulatory roles to the peritoneal B-cell compartment. They also could contribute to understanding the control of total B-lymphocyte numbers in the organism.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altenburger W., Steinmetz M., Zachau H. G. Functional and non-functional joining in immunoglobulin light chain genes of a mouse myeloma. Nature. 1980 Oct 16;287(5783):603–607. doi: 10.1038/287603a0. [DOI] [PubMed] [Google Scholar]
  2. Cerny A., Heusser C., Sutter S., Huegin A. W., Bazin H., Hengartner H., Zinkernagel R. M. Generation of agammaglobulinaemic mice by prenatal and postnatal exposure to polyclonal or monoclonal anti-IgM antibodies. Scand J Immunol. 1986 Oct;24(4):437–445. doi: 10.1111/j.1365-3083.1986.tb02132.x. [DOI] [PubMed] [Google Scholar]
  3. Coffman R. L., Weissman I. L. A monoclonal antibody that recognizes B cells and B cell precursors in mice. J Exp Med. 1981 Feb 1;153(2):269–279. doi: 10.1084/jem.153.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cooper M. D., Mulvaney D., Coutinho A., Cazenave P. A. A novel cell surface molecule on early B-lineage cells. Nature. 1986 Jun 5;321(6070):616–618. doi: 10.1038/321616a0. [DOI] [PubMed] [Google Scholar]
  5. Coutinho A., Forni L., Bernabé R. R. The polyclonal expression of immunoglobulin variable region determinants on the membrane of B cells and their precursors. Springer Semin Immunopathol. 1980 Aug;3(2):171–211. doi: 10.1007/BF02053975. [DOI] [PubMed] [Google Scholar]
  6. Forni L., Cazenave P. A., Cosenza H., Forsbeck K., Coutinho A. Expression of V-region-like determinants on Ig-negative precursors in murine fetal liver and bone marrow. Nature. 1979 Jul 19;280(5719):241–243. doi: 10.1038/280241a0. [DOI] [PubMed] [Google Scholar]
  7. Freitas A. A., Andrade L., Lembezat M. P., Coutinho A. Selection of VH gene repertoires: differentiating B cells of adult bone marrow mimic fetal development. Int Immunol. 1990;2(1):15–23. doi: 10.1093/intimm/2.1.15. [DOI] [PubMed] [Google Scholar]
  8. Freitas A. A., Rocha B., Coutinho A. A. Lymphocyte population kinetics in the mouse. Immunol Rev. 1986 Jun;91:5–37. doi: 10.1111/j.1600-065x.1986.tb01482.x. [DOI] [PubMed] [Google Scholar]
  9. Freitas A. A., Viale A. C., Sundblad A., Heusser C., Coutinho A. Normal serum immunoglobulins participate in the selection of peripheral B-cell repertoires. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5640–5644. doi: 10.1073/pnas.88.13.5640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Förster I., Vieira P., Rajewsky K. Flow cytometric analysis of cell proliferation dynamics in the B cell compartment of the mouse. Int Immunol. 1989;1(4):321–331. doi: 10.1093/intimm/1.4.321. [DOI] [PubMed] [Google Scholar]
  11. Grandien A., Coutinho A., Andersson J. Selective peripheral expansion and activation of B cells expressing endogenous immunoglobulin in mu-transgenic mice. Eur J Immunol. 1990 May;20(5):991–998. doi: 10.1002/eji.1830200507. [DOI] [PubMed] [Google Scholar]
  12. Hayakawa K., Hardy R. R. Normal, autoimmune, and malignant CD5+ B cells: the Ly-1 B lineage? Annu Rev Immunol. 1988;6:197–218. doi: 10.1146/annurev.iy.06.040188.001213. [DOI] [PubMed] [Google Scholar]
  13. Herzenberg L. A., Stall A. M., Lalor P. A., Sidman C., Moore W. A., Parks D. R., Herzenberg L. A. The Ly-1 B cell lineage. Immunol Rev. 1986 Oct;93:81–102. doi: 10.1111/j.1600-065x.1986.tb01503.x. [DOI] [PubMed] [Google Scholar]
  14. Holmberg D., Freitas A. A., Portnoï D., Jacquemart F., Avrameas S., Coutinho A. Antibody repertoires of normal BALB/c mice: B lymphocyte populations defined by state of activation. Immunol Rev. 1986 Oct;93:147–169. doi: 10.1111/j.1600-065x.1986.tb01506.x. [DOI] [PubMed] [Google Scholar]
  15. Jyonouchi H., Kincade P. W., Good R. A., Gershwin M. E. B lymphocyte lineage cells in newborn and very young NZB mice: evidence for regulatory disorders affecting B cell formation. J Immunol. 1983 Nov;131(5):2219–2225. [PubMed] [Google Scholar]
  16. Kearney J. F., Vakil M. Idiotype-directed interactions during ontogeny play a major role in the establishment of the adult B cell repertoire. Immunol Rev. 1986 Dec;94:39–50. doi: 10.1111/j.1600-065x.1986.tb01163.x. [DOI] [PubMed] [Google Scholar]
  17. Kerr W. G., Cooper M. D., Feng L., Burrows P. D., Hendershot L. M. Mu heavy chains can associate with a pseudo-light chain complex (psi L) in human pre-B cell lines. Int Immunol. 1989;1(4):355–361. doi: 10.1093/intimm/1.4.355. [DOI] [PubMed] [Google Scholar]
  18. Kincade P. W., Lee G., Sun L., Watanabe T. Monoclonal rat antibodies to murine IgM determinants. J Immunol Methods. 1981;42(1):17–26. doi: 10.1016/0022-1759(81)90220-9. [DOI] [PubMed] [Google Scholar]
  19. Lalor P. A., Herzenberg L. A., Adams S., Stall A. M. Feedback regulation of murine Ly-1 B cell development. Eur J Immunol. 1989 Mar;19(3):507–513. doi: 10.1002/eji.1830190315. [DOI] [PubMed] [Google Scholar]
  20. Ledbetter J. A., Herzenberg L. A. Xenogeneic monoclonal antibodies to mouse lymphoid differentiation antigens. Immunol Rev. 1979;47:63–90. doi: 10.1111/j.1600-065x.1979.tb00289.x. [DOI] [PubMed] [Google Scholar]
  21. Marcos M. A., De la Hera A., Pereira P., Marquez C., Toribio M., Coutinho A., Martinez C. B cell participation in the recursive selection of T cell repertoires. Eur J Immunol. 1988 Jul;18(7):1015–1020. doi: 10.1002/eji.1830180707. [DOI] [PubMed] [Google Scholar]
  22. Marcos M. A., Huetz F., Pereira P., Andreu J. L., Martinez-A C., Coutinho A. Further evidence for coelomic-associated B lymphocytes. Eur J Immunol. 1989 Nov;19(11):2031–2035. doi: 10.1002/eji.1830191110. [DOI] [PubMed] [Google Scholar]
  23. Nemazee D. A., Bürki K. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature. 1989 Feb 9;337(6207):562–566. doi: 10.1038/337562a0. [DOI] [PubMed] [Google Scholar]
  24. Nishikawa S., Sasaki Y., Kina T., Amagai T., Katsura Y. A monoclonal antibody against Igh6-4 determinant. Immunogenetics. 1986;23(2):137–139. doi: 10.1007/BF00377976. [DOI] [PubMed] [Google Scholar]
  25. Nossal G. J. Cellular mechanisms of immunologic tolerance. Annu Rev Immunol. 1983;1:33–62. doi: 10.1146/annurev.iy.01.040183.000341. [DOI] [PubMed] [Google Scholar]
  26. Opstelten D., Osmond D. G. Pre-B cells in mouse bone marrow: immunofluorescence stathmokinetic studies of the proliferation of cytoplasmic mu-chain-bearing cells in normal mice. J Immunol. 1983 Dec;131(6):2635–2640. [PubMed] [Google Scholar]
  27. Opstelten D., Osmond D. G. Regulation of pre-B cell proliferation in bone marrow: immunofluorescence stathmokinetic studies of cytoplasmic mu chain-bearing cells in anti-IgM-treated mice, hematologically deficient mutant mice and mice given sheep red blood cells. Eur J Immunol. 1985 Jun;15(6):599–605. doi: 10.1002/eji.1830150613. [DOI] [PubMed] [Google Scholar]
  28. Osmond D. G. Population dynamics of bone marrow B lymphocytes. Immunol Rev. 1986 Oct;93:103–124. doi: 10.1111/j.1600-065x.1986.tb01504.x. [DOI] [PubMed] [Google Scholar]
  29. Raveche E. S., Lalor P., Stall A., Conroy J. In vivo effects of hyperdiploid Ly-1+ B cells of NZB origin. J Immunol. 1988 Dec 15;141(12):4133–4139. [PubMed] [Google Scholar]
  30. Schüppel R., Wilke J., Weiler E. Monoclonal anti-allotype antibody towards BALB/c IgM. Analysis of specificity and site of a V-C crossover in recombinant strain BALB-Igh-Va/Igh-Cb. Eur J Immunol. 1987 May;17(5):739–741. doi: 10.1002/eji.1830170527. [DOI] [PubMed] [Google Scholar]
  31. Sedgwick J. D., Holt P. G. A solid-phase immunoenzymatic technique for the enumeration of specific antibody-secreting cells. J Immunol Methods. 1983 Feb 25;57(1-3):301–309. doi: 10.1016/0022-1759(83)90091-1. [DOI] [PubMed] [Google Scholar]
  32. Springer T., Galfrè G., Secher D. S., Milstein C. Monoclonal xenogeneic antibodies to murine cell surface antigens: identification of novel leukocyte differentiation antigens. Eur J Immunol. 1978 Aug;8(8):539–551. doi: 10.1002/eji.1830080802. [DOI] [PubMed] [Google Scholar]
  33. Sundblad A., Marcos M., Huetz F., Freitas A., Heusser C., Portnoï D., Coutinho A. Normal serum immunoglobulins influence the numbers of bone marrow pre-B and B cells. Eur J Immunol. 1991 May;21(5):1155–1161. doi: 10.1002/eji.1830210510. [DOI] [PubMed] [Google Scholar]

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