Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1979 Aug;76(8):4056–4060. doi: 10.1073/pnas.76.8.4056

Thymus-derived lymphocytes control the expression of immunogenic properties of peritoneal macrophages.

E Tzehoval, S Segal, M Feldman
PMCID: PMC383976  PMID: 91174

Abstract

Macrophages, given keyhole limpet hemocyanin in vitro, from normal mice initiate in culture antigen-specific T cell-mediated immune reactions. On the other hand, macrophages from nude, from adult-thymectomized, or from neonatal-thymectomized mice are impaired with respect to their capacity to signal such an antigen-specific T cell reaction. Thymocytes from hydrocortisone-treated donors, added in culture to such impaired macrophages, rendered them immunologically potent. The capacity of macrophages from adult thymectomized mice to promote the activation of antigen-specific "helper" T cells which, cooperating with B lymphocytes, would lead to antibody production, was also impaired. Thus, it appears that short-lived T lymphocytes control the maturation of macrophages up to a stage at which they can present antigen-specific T cells with antigen in an immunogenic form. We found that such T lymphocytes also control the phagocytic properties of macrophages, yet the impairment of their immunogenic properties does not seem to be derived from decreased phagocytosis.

Full text

PDF
4056

Selected References

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

  1. Baehner R. L., Nathan D. G. Quantitative nitroblue tetrazolium test in chronic granulomatous disease. N Engl J Med. 1968 May 2;278(18):971–976. doi: 10.1056/NEJM196805022781801. [DOI] [PubMed] [Google Scholar]
  2. Beller D. I., Farr A. G., Unanue E. R. Regulation of lymphocyte proliferation and differentiation by macrophages. Fed Proc. 1978 Jan;37(1):91–96. [PubMed] [Google Scholar]
  3. Beller D. I., Unanue E. R. Thymic maturation in vitro by a secretory product from macrophages. J Immunol. 1977 May;118(5):1780–1787. [PubMed] [Google Scholar]
  4. Brownstone A., Mitchison N. A., Pitt-Rivers R. Chemical and serological studies with an iodine-containing synthetic immunological determinant 4-hydroxy-3-iodo-5-nitrophenylacetic acid (NIP) and related compounds. Immunology. 1966 May;10(5):465–479. [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. Cantor H., Boyse E. A. Regulation of cellular and humoral immune responses by T-cell subclasses. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 1):23–32. doi: 10.1101/sqb.1977.041.01.006. [DOI] [PubMed] [Google Scholar]
  7. Casazza A. R., Duvall C. P., Carbone P. P. Summary of infectious complications occurring in patients with Hodgkin's disease. Cancer Res. 1966 Jun;26(6):1290–1296. [PubMed] [Google Scholar]
  8. Cohen I. R., Livnat S. The cell-mediated immune response: interactions of initiator and recruited T lymphocytes. Transplant Rev. 1976;29:24–58. doi: 10.1111/j.1600-065x.1976.tb00196.x. [DOI] [PubMed] [Google Scholar]
  9. Farr A. G., Dorf M. E., Unanue E. R. Secretion of mediators following T lymphocyte-macrophage interaction is regulated by the major histocompatibility complex. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3542–3546. doi: 10.1073/pnas.74.8.3542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fridkin M., Stabinsky Y., Zakuth V., Spirer Z. Tuftsin and some analogs: synthesis and interaction with human polymorphonuclear leukocytes. Biochim Biophys Acta. 1977 Jan 24;496(1):203–211. doi: 10.1016/0304-4165(77)90129-5. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Gordon D., Bray M. A., Morley J. Control of lymphokine secretion by prostaglandins. Nature. 1976 Jul 29;262(5567):401–402. doi: 10.1038/262401a0. [DOI] [PubMed] [Google Scholar]
  13. Gordon S., Cohn Z. A. Bacille Calmette-Guérin infection in the mouse. Regulation of macrophage plasminogen activator by T lymphocytes and specific antigen. J Exp Med. 1978 Apr 1;147(4):1175–1188. doi: 10.1084/jem.147.4.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gougerot M. A., Descamps A., Dimitriu A. Facteur lymphocytaire d'activation des macrophages. Comparaison du mode de production chez l'Homme et chez la souris. C R Acad Sci Hebd Seances Acad Sci D. 1976 Jun 14;282(22):2011–2014. [PubMed] [Google Scholar]
  15. Hadden J. W., Sadlik J. R., Hadden E. M. Macrophage proliferation induced in vitro by a lymphocyte factor. Nature. 1975 Oct 9;257(5526):483–485. doi: 10.1038/257483a0. [DOI] [PubMed] [Google Scholar]
  16. Haimovich J., Sela M. Inactivation of poly-DL-alanyl bacteriophage T4 with antisera specific toward poly-DL-alanine. J Immunol. 1966 Sep;97(3):338–343. [PubMed] [Google Scholar]
  17. Hirsch M. S., Ellis D. A., Proffitt M. R., Black P. H. Effects of interferon on leukaemia virus activation in graft versus host disease. Nat New Biol. 1973 Jul 25;244(134):102–103. doi: 10.1038/newbio244102a0. [DOI] [PubMed] [Google Scholar]
  18. Ishizaka K., Adachi T. Generation of specific helper cells and suppressor cells in vitro for the IgE and IgG antibody responses. J Immunol. 1976 Jul;117(1):40–47. [PubMed] [Google Scholar]
  19. KAPLAN H. S., SMITHERS D. W. Auto-immunity in man and homologous disease in mice in relation to the malignant lymphomas. Lancet. 1959 Jul 4;2(7088):1–4. doi: 10.1016/s0140-6736(59)92106-3. [DOI] [PubMed] [Google Scholar]
  20. Lane F. C., Unanue E. R. Requirement of thymus (T) lymphocytes for resistance to listeriosis. J Exp Med. 1972 May 1;135(5):1104–1112. doi: 10.1084/jem.135.5.1104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lindahl-Magnusson P., Leary P., Gresser I. Interferon inhibits DNA synthesis induced in mouse lymphocyte suspensions by phytohaemagglutinin or by allogeneic cells. Nat New Biol. 1972 May 24;237(73):120–121. doi: 10.1038/newbio237120a0. [DOI] [PubMed] [Google Scholar]
  22. MACKANESS G. B. THE IMMUNOLOGICAL BASIS OF ACQUIRED CELLULAR RESISTANCE. J Exp Med. 1964 Jul 1;120:105–120. doi: 10.1084/jem.120.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mauel J., Defendi V. Regulation of DNA synthesis in mouse macrophages. I. Sources, action and purification of the macrophage growing factor (MGF). Exp Cell Res. 1971 Mar;65(1):33–42. doi: 10.1016/s0014-4827(71)80047-2. [DOI] [PubMed] [Google Scholar]
  24. McGregor D. D., Logie P. S. The mediator of cellular immunity. X. Interaction of macrophages and specifically sensitized lymphocytes. Cell Immunol. 1975 Aug;18(2):454–465. doi: 10.1016/0008-8749(75)90072-6. [DOI] [PubMed] [Google Scholar]
  25. Mäkelä O. Assay of anti-hapten antibody with the aid of hapten-coupled bacteriophage. Immunology. 1966 Jan;10(1):81–86. [PMC free article] [PubMed] [Google Scholar]
  26. Nogueira N., Gordon S., Cohn Z. Trypanosoma cruzi: the immunological induction of macrophage plasminogen activator requires thymus-derived lymphocytes. J Exp Med. 1977 Jul 1;146(1):172–183. doi: 10.1084/jem.146.1.172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. North R. J. Importance of thymus-derived lymphocytes in cell-mediated immunity to infection. Cell Immunol. 1973 Apr;7(1):166–176. doi: 10.1016/0008-8749(73)90193-7. [DOI] [PubMed] [Google Scholar]
  28. Okudaira H., Ishizaka K. Reaginic antibody formation in the mouse. IV. Adoptive anti-hapten IgE antibody response in irradiated recipients of hapten-primed cells and carrier-specific cells. J Immunol. 1974 Aug;113(2):563–573. [PubMed] [Google Scholar]
  29. Rao G. R., Rawls W. E., Perey D. Y., Tompkins W. A. Macrophage activation in congenitally athymic mice raised under conventional or germ-free conditions. J Reticuloendothel Soc. 1977 Jan;21(1):13–20. [PubMed] [Google Scholar]
  30. Rode H. N., Gordon J. Macrophages in the mixed leukocyte culture reaction (MLC). Cell Immunol. 1974 Jul;13(1):87–94. doi: 10.1016/0008-8749(74)90229-9. [DOI] [PubMed] [Google Scholar]
  31. SVEHAG S. E., MANDEL B. THE FORMATION AND PROPERTIES OF POLIOVIRUS-NEUTRALIZING ANTIBODY. I. 19S AND 7S ANTIBODY FORMATION: DIFFERENCES IN KINETICS AND ANTIGEN DOSE REQUIREMENT FOR INDUCTION. J Exp Med. 1964 Jan 1;119:1–19. doi: 10.1084/jem.119.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Segal S., Cohen I. R., Feldman M. Thymus-derived lymphocytes: humoral and cellular reactions distinguished by hydrocortisone. Science. 1972 Mar 10;175(4026):1126–1128. doi: 10.1126/science.175.4026.1126. [DOI] [PubMed] [Google Scholar]
  33. Shire J. G., Pantelouris E. M. Comparison of endocrine function in normal and genetically athymic mice. Comp Biochem Physiol A Comp Physiol. 1974 Jan;47(1):93–100. doi: 10.1016/0300-9629(74)90055-3. [DOI] [PubMed] [Google Scholar]
  34. Simpson E., Cantor H. Regulation of the immune response by subclasses of T lymphocytes. II. The effect of adult thymectomy upon humoral and cellular responses in mice. Eur J Immunol. 1975 May;5(5):337–343. doi: 10.1002/eji.1830050509. [DOI] [PubMed] [Google Scholar]
  35. Smith T. J., Wagner R. R. Rabbit macrophage interferons. I. Conditions for biosynthesis by virus-infected and uninfected cells. J Exp Med. 1967 Apr 1;125(4):559–577. doi: 10.1084/jem.125.4.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Steinman L., Tzehoval E., Cohen I. R., Segal S., Glickman E. Sequential interaction of macrophages, initiator T lymphocytes and recruited T lymphocytes in a cell-mediated immune response to soluble antigen. Eur J Immunol. 1978 Jan;8(1):29–34. doi: 10.1002/eji.1830080107. [DOI] [PubMed] [Google Scholar]
  37. Tzehoval E., Segal S., Stabinsky Y., Fridkin M., Spirer Z., Feldman M. Tuftsin (an Ig-associated tetrapeptide) triggers the immunogenic function of macrophages: implications for activation of programmed cells. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3400–3404. doi: 10.1073/pnas.75.7.3400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Unanue E. R. The regulation of lymphocyte functions by the macrophage. Immunol Rev. 1978;40:227–255. doi: 10.1111/j.1600-065x.1978.tb00408.x. [DOI] [PubMed] [Google Scholar]
  39. Unanue E. R. Thymus dependency of the immune response to hemocyanin: an evaluation of the role of macrophages in thymectomized mice. J Immunol. 1970 Dec;105(6):1339–1343. [PubMed] [Google Scholar]
  40. Vadas M. A., Miller J. F., McKenzie I. F., Chism S. E., Shen F. W., Boyse E. A., Gamble J. R., Whitelaw A. M. Ly and Ia antigen phenotypes of T cells involved in delayed-type hypersensitivity and in suppression. J Exp Med. 1976 Jul 1;144(1):10–19. doi: 10.1084/jem.144.1.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. ZIMMERMAN L. E., RAPPAPORT H. Occurrence of Cryptococcosis in patients with malignant disease of reticuloendothelial system. Am J Clin Pathol. 1954 Sep;24(9):1050–1072. doi: 10.1093/ajcp/24.9.1050. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES