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. 1977 May 1;145(5):1299–1315. doi: 10.1084/jem.145.5.1299

Regulation of B-cell proliferative responses to lipopolysaccharide by a subclass of thymus T cells

PMCID: PMC2180647  PMID: 300782

Abstract

When thymus cells which are unresponsive to LPS are combined with numbers of peripheral lymphoid cells giving minimal responses to LPS, synergistic incorporation of [3H]thymidine occurs. Synergy requires that both components proliferate, but most of the augmented response is the result of peripheral cell proliferation. The thymus cell is a T cell of variable density, low in thy-1.2 antigen, not concanavalin A responsive, present in the major thymus subpopulation, and may be from lipopolysaccharide (LPS)-unresponsive strains. The peripheral cell is sensitive to anti-IgG or IgM plus complement (C'), resistant to anti- Thy-1.2 and C', exhibits adherence properties of B lymphocytes, and must be from LPS-responsive strains. Synergistic responses depend on critical thymus/peripheral cell ratios, inhibition occurring at high peripheral cell numbers. The data provide evidence that B-cell proliferative responses to LPS may be regulated by a subclass of thymus T cells.

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Selected References

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

  1. Allison A. C., Davies A. J. Requirement of thymus-dependent lymphocytes for potentiation by adjuvants of antibody formation. Nature. 1971 Oct 1;233(5318):330–332. doi: 10.1038/233330a0. [DOI] [PubMed] [Google Scholar]
  2. Andersson J., Möller G., Sjöberg O. Selective induction of DNA synthesis in T and B lymphocytes. Cell Immunol. 1972 Aug;4(4):381–393. doi: 10.1016/0008-8749(72)90040-8. [DOI] [PubMed] [Google Scholar]
  3. Andersson J., Sjöberg O., Möller G. Mitogens as probes for immunocyte activation and cellular cooperation. Transplant Rev. 1972;11:131–177. doi: 10.1111/j.1600-065x.1972.tb00048.x. [DOI] [PubMed] [Google Scholar]
  4. Armerding D., Katz D. H. Activation of T and B lymphocytes in vitro. I. Regulatory influence of bacterial lipopolysaccharide (LPS) on specific T-cell helper function. J Exp Med. 1974 Jan 1;139(1):24–43. doi: 10.1084/jem.139.1.24. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Calderon J., Kiely J. M., Lefko J. L., Unanue E. R. The modulation of lymphocyte functions by molecules secreted by macrophages. I. Description and partial biochemical analysis. J Exp Med. 1975 Jul 1;142(1):151–164. doi: 10.1084/jem.142.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Di Sabato G., Chen D. M., Erickson J. W. Production by murine spleen cells of an activity stimulating the PHA-responsiveness of thymus lymphocytes. Cell Immunol. 1975 Jun;17(2):495–504. doi: 10.1016/s0008-8749(75)80053-0. [DOI] [PubMed] [Google Scholar]
  7. Forbes J. T., Nakao Y., Smith R. T. T mitogens trigger LPS responsiveness in mouse thymus cells. J Immunol. 1975 Mar;114(3):1004–1007. [PubMed] [Google Scholar]
  8. Gery I., Gershon R. K., Waksman B. H. Potentiation of the T-lymphocyte response to mitogens. I. The responding cell. J Exp Med. 1972 Jul 1;136(1):128–142. doi: 10.1084/jem.136.1.128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gery I., Krüger J., Spiesel S. Z. Stimulation of B-lymphocytes by endotoxin. Reactions of thymus-deprived mice and karyotypic analysis of dividing cells in mice bearing T 6 T 6 thymus grafts. J Immunol. 1972 Apr;108(4):1088–1091. [PubMed] [Google Scholar]
  10. Gery I., Waksman B. H. Potentiation of the T-lymphocyte response to mitogens. II. The cellular source of potentiating mediator(s). J Exp Med. 1972 Jul 1;136(1):143–155. doi: 10.1084/jem.136.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Glode L. M., Scher I., Osborne B., Rosenstreich D. L. Cellular mechanism of endotoxin unresponsiveness in C3H/HeJ mice. J Immunol. 1976 Feb;116(2):454–461. [PubMed] [Google Scholar]
  12. Handwerger B. S., Schwartz R. H. Separation of murine lymphoid cells using nylon wool columns. Recovery of the B cell-enriched population. Transplantation. 1974 Dec;18(6):544–548. doi: 10.1097/00007890-197412000-00013. [DOI] [PubMed] [Google Scholar]
  13. Hoffmann M. K., Weiss O., Koenig S., Hirst J. A., Oettgen H. F. Suppression and enhancement of the T cell-dependent production of antibody to SRBC in vitro by bacterial lipopolysaccharide. J Immunol. 1975 Feb;114(2 Pt 2):738–741. [PubMed] [Google Scholar]
  14. Howe M. L., Cohen L. Lymphoid cell subpopulations. I. Synergy between lymph node cells and thymocytes in response to alloantigens and mitogens. J Immunol. 1975 Nov;115(5):1227–1232. [PubMed] [Google Scholar]
  15. Julius M. H., Simpson E., Herzenberg L. A. A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur J Immunol. 1973 Oct;3(10):645–649. doi: 10.1002/eji.1830031011. [DOI] [PubMed] [Google Scholar]
  16. Kadish J. L., Basch R. S. Hematopoietic thymocyte precursors. I. Assay and kinetics of the appearance of progeny. J Exp Med. 1976 May 1;143(5):1082–1099. doi: 10.1084/jem.143.5.1082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Konda S., Nakao Y., Smith R. T. Immunologic properties of mouse thymus cells. Identification of T cell functions within a minor, low-density subpopulation. J Exp Med. 1972 Dec 1;136(6):1461–1477. doi: 10.1084/jem.136.6.1461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Konda S., Stockert E., Smith R. T. Immunologic properties of mouse thymus cells: membrane antigen patterns associated with various cell subpopulations. Cell Immunol. 1973 May;7(2):275–289. doi: 10.1016/0008-8749(73)90250-5. [DOI] [PubMed] [Google Scholar]
  19. Kyminski J. W., Smith R. T. Evidence for a B-cell -like helper function in mixed lymphocyte culture between immunocompetent thymus cells. J Exp Med. 1975 Feb 1;141(2):360–373. doi: 10.1084/jem.141.2.360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lemke H., Coutinho A., Opitz H. G., Gronowicz E. Macrophages suppress direct B-cell activation by lipopolysaccharide. Scand J Immunol. 1975;4(7):707–720. doi: 10.1111/j.1365-3083.1975.tb02679.x. [DOI] [PubMed] [Google Scholar]
  21. Nakano M., Uchiyama T., Saito K. Adjuvant effect of endotoxin; antibody response to sheep erythrocytes in mice after transfer of syngeneic lymphoid cells treated with bacterial lipopolysaccharide in vitro. J Immunol. 1973 Feb;110(2):408–413. [PubMed] [Google Scholar]
  22. Ness D. B., Smith S., Talcott J. A., Grumet F. C. T cell requirements for the expression of the lipopolysaccharide adjuvant effect in vivo: evidence for a T cell-dependent and a T cell-independent mode of action. Eur J Immunol. 1976 Sep;6(9):650–654. doi: 10.1002/eji.1830060911. [DOI] [PubMed] [Google Scholar]
  23. Newburger P. E., Hamaoka T., Katz D. H. Potentiation of helper T cell function in IgE antibody responses by bacterial lipolysaccharide (LPS). J Immunol. 1974 Sep;113(3):824–829. [PubMed] [Google Scholar]
  24. Ozato K., Adler W. H., Ebert J. D. Synergism of bacterial lipopolysaccharides and concanavalin A in the activation of thymic lymphocytes. Cell Immunol. 1975 Jun;17(2):532–541. doi: 10.1016/s0008-8749(75)80057-8. [DOI] [PubMed] [Google Scholar]
  25. Peavy D. L., Adler W. H., Smith R. T. The mitogenic effects of endotoxin and staphylococcal enterotoxin B on mouse spleen cells and human peripheral lymphocytes. J Immunol. 1970 Dec;105(6):1453–1458. [PubMed] [Google Scholar]
  26. Peavy D. L., Shands J. W., Jr, Adler W. H., Smith R. T. Mitogenicity of bacterial endotoxins: characterization of the mitogenic principle. J Immunol. 1973 Aug;111(2):352–357. [PubMed] [Google Scholar]
  27. Roelants G. E., Loor F., von Boehmer H., Sprent J., Hägg L. B., Mayor K. S., Rydén A. Five types of lymphocytes (Ig-theta-, Ig-theta+weak, Ig-theta+strong, Ig+theta- and Ig+theta+) characterized by double immunofluorescence and electrophoretic mobility. Organ distribution in normal and nude mice. Eur J Immunol. 1975 Feb;5(2):127–131. doi: 10.1002/eji.1830050211. [DOI] [PubMed] [Google Scholar]
  28. Rosenstreich D. L., Nowotny A., Chused T., Mergenhagen S. E. In vitro transformation of mouse bone-marrow-derived (B) lymphocytes induced by the lipid component of endotoxin. Infect Immun. 1973 Sep;8(3):406–411. doi: 10.1128/iai.8.3.406-411.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Scheid M. P., Hoffmann M. K., Komuro K., Hämmerling U., Abbott J., Boyse E. A., Cohen G. H., Hooper J. A., Schulof R. S., Goldstein A. L. Differentiation of T cells induced by preparations from thymus and by nonthymic agents. J Exp Med. 1973 Oct 1;138(4):1027–1032. doi: 10.1084/jem.138.4.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schmidtke J. R., Najarian J. S. Synergistic effects on DNA synthesis of phytohemagglutinin or concanavalin A and lipopolysaccharide in human peripheral blood lymphocytes. J Immunol. 1975 Feb;114(2 Pt 2):742–746. [PubMed] [Google Scholar]
  31. Shinohara N., Kern M. Differentiation of lymphoid cells: B cell as a direct target and T cell as a regulator in lipopolysaccharide-enhanced induction of immunoglobulin production. J Immunol. 1976 Jun;116(6):1607–1612. [PubMed] [Google Scholar]
  32. Smith R. T. Specific recognition reactions at the cellular level in mouse lymphoreticular cell subpopulations. Transplant Rev. 1972;11:178–216. doi: 10.1111/j.1600-065x.1972.tb00049.x. [DOI] [PubMed] [Google Scholar]
  33. Sultzer B. M. Genetic analysis of lymphocyte activation by lipopolysaccharide Endotoxin. Infect Immun. 1976 Jun;13(6):1579–1584. doi: 10.1128/iai.13.6.1579-1584.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Takiguchi T., Adler W. H., Smith R. T. Identification of mouse thymus antigen recognition function in a minor, low-density, low-theta cell subpopulation. Cell Immunol. 1971 Aug;2(4):373–380. doi: 10.1016/0008-8749(71)90072-4. [DOI] [PubMed] [Google Scholar]

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