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. 1988 May;64(1):147–153.

A role for mature B cells in bone marrow transplantation.

T Yoshio 1, K Saito 1, F L Adler 1, L T Adler 1
PMCID: PMC1385200  PMID: 3290093

Abstract

The proliferative potential of membrane Ig (mIg)-bearing B lymphocytes was assessed in an adoptive transfer system based on the use of non-inbred rabbits matched for major histocompatibility (MHC) antigens and mismatched for immunoglobulin (Ig) allotypes. Cell suspensions made from spleens (SP), mesenteric lymph nodes (LN), or bone marrow (BM) of allotype b4b5 rabbits were deprived of B cells with mIg of the b4 type by adherence to plastic dishes coated with affinity-purified anti-b4. When such b4-depleted cell populations were injected into newborn hosts of allotype b6b6, stable and lasting chimerism promptly resulted, in which donor-derived products were almost entirely of the b5 allotype. Chimeras formed by transfer of unfractionated cells from b4b5 donors, on the other hand, exhibited a predominance of the b4 allotype, as seen in the living donors. BM but not SP or LN contained precursors capable of differentiating into mIg+ lymphocytes in culture, but no evidence was obtained for engraftment and differentiation by such B-cell precursors or more primitive stem cells in vivo. These studies suggest a potentially significant role for mature B cells in reconstituting the immune system of human transplant recipients.

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Selected References

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

  1. Adler F. L., Adler L. T. Immunocompetence of chimeric rabbits. II. Persistence of memory and antigen-driven responses of donor cells. Transplantation. 1984 Oct;38(4):387–391. [PubMed] [Google Scholar]
  2. Adler F. L., Adler L. T. Immunocompetence of chimeric rabbits. III. Serial passage and persistence of B-lymphocyte memory. Cell Immunol. 1985 Apr 1;91(2):385–396. doi: 10.1016/0008-8749(85)90236-9. [DOI] [PubMed] [Google Scholar]
  3. Adler F. L., Adler L. T. Passive hemagglutination and hemolysis for estimation of antigens and antibodies. Methods Enzymol. 1980;70(A):455–466. doi: 10.1016/s0076-6879(80)70069-1. [DOI] [PubMed] [Google Scholar]
  4. Adler L. T., Adler F. L., Cohen C., Tissot R. G. Induction of lymphoid cell chimerism in noninbred, histocompatible rabbits. A new model for studying allotype suppression in the rabbit. J Exp Med. 1981 Oct 1;154(4):1085–1099. doi: 10.1084/jem.154.4.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Adler L. T., Adler F. L., Cohen C., Tissot R. G., Lancki D. Stable chimerism induced in noninbred rabbits by neonatal injection of spleen cells from allotype-suppressed adult donors. I. Replacement of hemopoietic tissue by donor cells. Transplantation. 1977 Nov;24(5):338–348. doi: 10.1097/00007890-197711000-00005. [DOI] [PubMed] [Google Scholar]
  6. Adler L. T., LeBeau M. M., Adler F. L. Characterization of donor-derived lymphocytes in chimeric rabbits. Transplantation. 1983 Jun;35(6):530–534. doi: 10.1097/00007890-198306000-00003. [DOI] [PubMed] [Google Scholar]
  7. Adler L. T., Rehg J. E., Cohen C., LeBeau M. M. Graft-versus-host reactions and abrogation of allotype suppression following histoincompatible lymphoid cell transfers in rabbits. Transplantation. 1984 Jun;37(6):606–611. doi: 10.1097/00007890-198406000-00016. [DOI] [PubMed] [Google Scholar]
  8. Askonas B. A., Williamson A. R., Wright B. E. Selection of a single antibody-forming cell clone and its propagation in syngeneic mice. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1398–1403. doi: 10.1073/pnas.67.3.1398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Buckley R. H., Schiff S. E., Sampson H. A., Schiff R. I., Markert M. L., Knutsen A. P., Hershfield M. S., Huang A. T., Mickey G. H., Ward F. E. Development of immunity in human severe primary T cell deficiency following haploidentical bone marrow stem cell transplantation. J Immunol. 1986 Apr 1;136(7):2398–2407. [PubMed] [Google Scholar]
  10. Champlin R. Bone marrow transplantation for leukemia: effects of T lymphocyte depletion of donor bone marrow. Transplant Proc. 1987 Feb;19(1 Pt 1):157–159. [PubMed] [Google Scholar]
  11. Craig S. W., Cebra J. J. Peyer's patches: an enriched source of precursors for IgA-producing immunocytes in the rabbit. J Exp Med. 1971 Jul 1;134(1):188–200. doi: 10.1084/jem.134.1.188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Deeg H. J., Storb R. Graft-versus-host disease: pathophysiological and clinical aspects. Annu Rev Med. 1984;35:11–24. doi: 10.1146/annurev.me.35.020184.000303. [DOI] [PubMed] [Google Scholar]
  13. Förster I., Rajewsky K. Expansion and functional activity of Ly-1+ B cells upon transfer of peritoneal cells into allotype-congenic, newborn mice. Eur J Immunol. 1987 Apr;17(4):521–528. doi: 10.1002/eji.1830170414. [DOI] [PubMed] [Google Scholar]
  14. Gathings W. E., Mage R. G., Cooper M. D., Young-Cooper G. O. A subpopulation of small pre-B cells in rabbit bone marrow expresses kappa light chains and exhibits allelic exclusion of b locus allotypes. Eur J Immunol. 1982 Jan;12(1):76–81. doi: 10.1002/eji.1830120114. [DOI] [PubMed] [Google Scholar]
  15. Grant P. R. Dispersal in relation to carrying capacity. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2854–2858. doi: 10.1073/pnas.75.6.2854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hayakawa K., Hardy R. R., Stall A. M., Herzenberg L. A., Herzenberg L. A. Immunoglobulin-bearing B cells reconstitute and maintain the murine Ly-1 B cell lineage. Eur J Immunol. 1986 Oct;16(10):1313–1316. doi: 10.1002/eji.1830161021. [DOI] [PubMed] [Google Scholar]
  17. Inoue T., Adler L. T. Selective suppressive effects of anti-allotype antibodies on spleen cells of adult rabbits. Cell Immunol. 1982 Jan 15;66(2):277–288. doi: 10.1016/0008-8749(82)90179-4. [DOI] [PubMed] [Google Scholar]
  18. Kincade P. W. Formation of B lymphocytes in fetal and adult life. Adv Immunol. 1981;31:177–245. doi: 10.1016/s0065-2776(08)60921-9. [DOI] [PubMed] [Google Scholar]
  19. Kindt T. J. Rabbit immunoglobulin allotypes: structure, immunology, and genetics. Adv Immunol. 1975;21:35–86. doi: 10.1016/s0065-2776(08)60218-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Korngold R., Sprent J. Lethal graft-versus-host disease after bone marrow transplantation across minor histocompatibility barriers in mice. Prevention by removing mature T cells from marrow. J Exp Med. 1978 Dec 1;148(6):1687–1698. doi: 10.1084/jem.148.6.1687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kurland J. I., Ziegler S. F., Witte O. N. Long-term cultured B lymphocytes and their precursors reconstitute the B-lymphocyte lineage in vivo. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7554–7558. doi: 10.1073/pnas.81.23.7554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Leventon G. S., Kulkarni S. S., White R. A., Zander A. R. Enhanced recovery of gut-associated lymphoid tissue by infusion of buffy coat cells and gut leukocytes in the murine syngeneic bone marrow transplantation model. Blood. 1986 Nov;68(5):1003–1007. [PubMed] [Google Scholar]
  23. Lum L. G., Seigneuret M. C., Storb R. The transfer of antigen-specific humoral immunity from marrow donors to marrow recipients. J Clin Immunol. 1986 Sep;6(5):389–396. doi: 10.1007/BF00915378. [DOI] [PubMed] [Google Scholar]
  24. Mage M. G., McHugh L. L., Rothstein T. L. Mouse lymphocytes with and without surface immunoglobulin: preparative scale separation in polystyrene tissue culture dishes coated with specifically purified anti-immunoglobulin. J Immunol Methods. 1977;15(1):47–56. doi: 10.1016/0022-1759(77)90016-3. [DOI] [PubMed] [Google Scholar]
  25. Martin P. J., Hansen J. A., Buckner C. D., Sanders J. E., Deeg H. J., Stewart P., Appelbaum F. R., Clift R., Fefer A., Witherspoon R. P. Effects of in vitro depletion of T cells in HLA-identical allogeneic marrow grafts. Blood. 1985 Sep;66(3):664–672. [PubMed] [Google Scholar]
  26. NOSSAL G. J. Studies on the transfer of antibody-producing capacty. II. The serial transfer of antibody-producing cells. Immunology. 1960 Apr;3:109–116. [PMC free article] [PubMed] [Google Scholar]
  27. Ohama Y., Adler L. T., Saito K. Impaired lymphocyte functions in heterozygous rabbits recovering from neonatal allotype suppression. Cell Immunol. 1985 Feb;90(2):416–425. doi: 10.1016/0008-8749(85)90206-0. [DOI] [PubMed] [Google Scholar]
  28. Ohama Y., Adler L. T. Suppression of rabbit lymphocyte functions by antibodies specific for allotypic membrane determinants. Cell Immunol. 1984 Jul;86(2):429–438. doi: 10.1016/0008-8749(84)90398-8. [DOI] [PubMed] [Google Scholar]
  29. Paige C. J., Kincade P. W., Moore M. A., Lee G. The fate of fetal and adult B-cell progenitors grafted into immunodeficient CBA/N mice. J Exp Med. 1979 Sep 19;150(3):548–563. doi: 10.1084/jem.150.3.548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Patterson J., Prentice H. G., Brenner M. K., Gilmore M., Janossy G., Ivory K., Skeggs D., Morgan H., Lord J., Blacklock H. A. Graft rejection following HLA matched T-lymphocyte depleted bone marrow transplantation. Br J Haematol. 1986 Jun;63(2):221–230. doi: 10.1111/j.1365-2141.1986.tb05544.x. [DOI] [PubMed] [Google Scholar]
  31. Pink J. R., Ratcliffe M. J., Vainio O. Immunoglobulin-bearing stem cells for clones of B (bursa-derived) lymphocytes. Eur J Immunol. 1985 Jun;15(6):617–620. doi: 10.1002/eji.1830150616. [DOI] [PubMed] [Google Scholar]
  32. Prentice H. G., Blacklock H. A., Janossy G., Gilmore M. J., Price-Jones L., Tidman N., Trejdosiewicz L. K., Skeggs D. B., Panjwani D., Ball S. Depletion of T lymphocytes in donor marrow prevents significant graft-versus-host disease in matched allogeneic leukaemic marrow transplant recipients. Lancet. 1984 Mar 3;1(8375):472–476. doi: 10.1016/s0140-6736(84)92848-4. [DOI] [PubMed] [Google Scholar]
  33. Reisner Y., Kapoor N., Kirkpatrick D., Pollack M. S., Dupont B., Good R. A., O'Reilly R. J. Transplantation for acute leukaemia with HLA-A and B nonidentical parental marrow cells fractionated with soybean agglutinin and sheep red blood cells. Lancet. 1981 Aug 15;2(8242):327–331. doi: 10.1016/s0140-6736(81)90647-4. [DOI] [PubMed] [Google Scholar]
  34. Saito K., Adler L. T. Selective suppression of allotype expression induced in vitro: maintenance of suppression following adoptive transfer. Cell Immunol. 1986 Apr 15;99(1):209–219. doi: 10.1016/0008-8749(86)90229-7. [DOI] [PubMed] [Google Scholar]
  35. Seferian P. G., Rodkey L. S., Adler F. L. Selective survival and expression of B-lymphocyte memory cells during long-term serial transplantation. Cell Immunol. 1987 Dec;110(2):226–232. doi: 10.1016/0008-8749(87)90118-3. [DOI] [PubMed] [Google Scholar]
  36. Shiobara S., Lum L. G., Witherspoon R. P., Storb R. Antigen-specific antibody responses of lymphocytes to tetanus toxoid after human marrow transplantation. Transplantation. 1986 May;41(5):587–592. doi: 10.1097/00007890-198605000-00007. [DOI] [PubMed] [Google Scholar]
  37. Tseng J. Transfer of lymphocytes of Peyer's patches between immunoglobulin allotype congenic mice: repopulation of the IgA plasma cells in the gut lamina propria. J Immunol. 1981 Nov;127(5):2039–2043. [PubMed] [Google Scholar]
  38. Vallera D. A., Soderling C. C., Carlson G. J., Kersey J. H. Bone marrow transplantation across major histocompatibility barriers in mice. Effect of elimination of T cells from donor grafts by treatment with monoclonal Thy-1.2 plus complement or antibody alone. Transplantation. 1981 Mar;31(3):218–222. doi: 10.1097/00007890-198103000-00015. [DOI] [PubMed] [Google Scholar]
  39. Waldmann H., Polliak A., Hale G., Or R., Cividalli G., Weiss L., Weshler Z., Samuel S., Manor D., Brautbar C. Elimination of graft-versus-host disease by in-vitro depletion of alloreactive lymphocytes with a monoclonal rat anti-human lymphocyte antibody (CAMPATH-1). Lancet. 1984 Sep 1;2(8401):483–486. doi: 10.1016/s0140-6736(84)92564-9. [DOI] [PubMed] [Google Scholar]
  40. Wimperis J. Z., Brenner M. K., Prentice H. G., Reittie J. E., Karayiannis P., Griffiths P. D., Hoffbrand A. V. Transfer of a functioning humoral immune system in transplantation of T-lymphocyte-depleted bone marrow. Lancet. 1986 Feb 15;1(8477):339–343. doi: 10.1016/s0140-6736(86)92315-9. [DOI] [PubMed] [Google Scholar]
  41. Wimperis J. Z., Brenner M. K., Prentice H. G., Thompson E. J., Hoffbrand A. V. B cell development and regulation after T cell-depleted marrow transplantation. J Immunol. 1987 Apr 15;138(8):2445–2450. [PubMed] [Google Scholar]
  42. Witherspoon R. P., Storb R., Ochs H. D., Fluornoy N., Kopecky K. J., Sullivan K. M., Deeg J. H., Sosa R., Noel D. R., Atkinson K. Recovery of antibody production in human allogeneic marrow graft recipients: influence of time posttransplantation, the presence or absence of chronic graft-versus-host disease, and antithymocyte globulin treatment. Blood. 1981 Aug;58(2):360–368. [PubMed] [Google Scholar]

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