Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1991 Sep;59(9):3053–3059. doi: 10.1128/iai.59.9.3053-3059.1991

Increase of T-cell receptor gamma/delta-bearing T cells in cord blood of newborn babies obtained by in vitro stimulation with mycobacterial cord factor.

I Tsuyuguchi 1, H Kawasumi 1, C Ueta 1, I Yano 1, S Kishimoto 1
PMCID: PMC258134  PMID: 1652559

Abstract

Cord blood T lymphocytes proliferated in vitro in response to mycobacterial organisms but did not proliferate in the presence of tuberculin purified protein derivative. Components recognized by cord blood T cells were resistant to protease digestion. In contrast, T lymphocytes derived from tuberculin-positive adult peripheral blood proliferated when stimulated by the protease-sensitive component of mycobacterial organisms or purified protein derivative, confirming that adult T cells respond to protein components whereas cord blood T cells respond to the nonpeptide component of mycobacteria. In vitro culture of cord blood lymphocytes stimulated by either mycobacterial lysates or the lipid fraction showed increases in the numbers of T-cell receptor (TcR) gamma/delta T lymphocytes with no changes in the numbers of TcR alpha/beta T lymphocytes in contrast to the in vitro cultures of adult blood lymphocytes stimulated with mycobacterial ligands in which no increase of TcR gamma/delta cells was observed. Interleukin-2 receptor (CD25) and Ia antigen (HLA-DR) analyses evidenced the activation of a large proportion of cord blood gamma/delta T cells which had increased after stimulation with mycobacteria in vitro. Further characterization of mycobacterial ligand suggested that the lipid fraction of mycobacterial lysate or trehalose dimycolate-cord factor was the most plausible cause for T-cell proliferation in cord blood. These results suggest that when the gamma/delta T cells in a newborn infant not yet sensitized to any pathogenic organisms are confronted by a mycobacterium, they respond nonspecifically to the mycobacterial organism or its lipid component (cord factor). gamma/delta T cells may therefore play a distinct role in forming the first line of the host defense system against certain microorganisms.

Full text

PDF
3054

Selected References

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

  1. Augustin A., Kubo R. T., Sim G. K. Resident pulmonary lymphocytes expressing the gamma/delta T-cell receptor. Nature. 1989 Jul 20;340(6230):239–241. doi: 10.1038/340239a0. [DOI] [PubMed] [Google Scholar]
  2. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  3. Born W., Hall L., Dallas A., Boymel J., Shinnick T., Young D., Brennan P., O'Brien R. Recognition of a peptide antigen by heat shock--reactive gamma delta T lymphocytes. Science. 1990 Jul 6;249(4964):67–69. doi: 10.1126/science.1695022. [DOI] [PubMed] [Google Scholar]
  4. Born W., Happ M. P., Dallas A., Reardon C., Kubo R., Shinnick T., Brennan P., O'Brien R. Recognition of heat shock proteins and gamma delta cell function. Immunol Today. 1990 Feb;11(2):40–43. doi: 10.1016/0167-5699(90)90015-2. [DOI] [PubMed] [Google Scholar]
  5. Brenner M. B., McLean J., Dialynas D. P., Strominger J. L., Smith J. A., Owen F. L., Seidman J. G., Ip S., Rosen F., Krangel M. S. Identification of a putative second T-cell receptor. Nature. 1986 Jul 10;322(6075):145–149. doi: 10.1038/322145a0. [DOI] [PubMed] [Google Scholar]
  6. Fisch P., Malkovsky M., Braakman E., Sturm E., Bolhuis R. L., Prieve A., Sosman J. A., Lam V. A., Sondel P. M. Gamma/delta T cell clones and natural killer cell clones mediate distinct patterns of non-major histocompatibility complex-restricted cytolysis. J Exp Med. 1990 May 1;171(5):1567–1579. doi: 10.1084/jem.171.5.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fujita T., Sugimoto N., Yokoi F., Ohtsubo Y., Ikutoh M., Kato Y., Natsuhara Y., Oka S., Yano I. Induction of interferons (IFNs) and tumor necrosis factor (TNF) in mice by a novel glycolipid trehalose 2,3,6'-trimycolate from Rhodococcus aurantiacus (Gordona aurantiaca). Microbiol Immunol. 1990;34(6):523–532. doi: 10.1111/j.1348-0421.1990.tb03169.x. [DOI] [PubMed] [Google Scholar]
  8. Goren M. B. Mycobacterial lipids: selected topics. Bacteriol Rev. 1972 Mar;36(1):33–64. doi: 10.1128/br.36.1.33-64.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Happ M. P., Kubo R. T., Palmer E., Born W. K., O'Brien R. L. Limited receptor repertoire in a mycobacteria-reactive subset of gamma delta T lymphocytes. Nature. 1989 Dec 7;342(6250):696–698. doi: 10.1038/342696a0. [DOI] [PubMed] [Google Scholar]
  10. Haregewoin A., Soman G., Hom R. C., Finberg R. W. Human gamma delta+ T cells respond to mycobacterial heat-shock protein. Nature. 1989 Jul 27;340(6231):309–312. doi: 10.1038/340309a0. [DOI] [PubMed] [Google Scholar]
  11. Holoshitz J., Koning F., Coligan J. E., De Bruyn J., Strober S. Isolation of CD4- CD8- mycobacteria-reactive T lymphocyte clones from rheumatoid arthritis synovial fluid. Nature. 1989 May 18;339(6221):226–229. doi: 10.1038/339226a0. [DOI] [PubMed] [Google Scholar]
  12. Janeway C. A., Jr, Jones B., Hayday A. Specificity and function of T cells bearing gamma delta receptors. Immunol Today. 1988 Mar;9(3):73–76. doi: 10.1016/0167-5699(88)91267-4. [DOI] [PubMed] [Google Scholar]
  13. Janis E. M., Kaufmann S. H., Schwartz R. H., Pardoll D. M. Activation of gamma delta T cells in the primary immune response to Mycobacterium tuberculosis. Science. 1989 May 12;244(4905):713–716. doi: 10.1126/science.2524098. [DOI] [PubMed] [Google Scholar]
  14. Kabelitz D., Bender A., Schondelmaier S., Schoel B., Kaufmann S. H. A large fraction of human peripheral blood gamma/delta + T cells is activated by Mycobacterium tuberculosis but not by its 65-kD heat shock protein. J Exp Med. 1990 Mar 1;171(3):667–679. doi: 10.1084/jem.171.3.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaufmann S. H. Heat shock proteins and the immune response. Immunol Today. 1990 Apr;11(4):129–136. doi: 10.1016/0167-5699(90)90050-j. [DOI] [PubMed] [Google Scholar]
  16. Modlin R. L., Pirmez C., Hofman F. M., Torigian V., Uyemura K., Rea T. H., Bloom B. R., Brenner M. B. Lymphocytes bearing antigen-specific gamma delta T-cell receptors accumulate in human infectious disease lesions. Nature. 1989 Jun 15;339(6225):544–548. doi: 10.1038/339544a0. [DOI] [PubMed] [Google Scholar]
  17. Munk M. E., Gatrill A. J., Kaufmann S. H. Target cell lysis and IL-2 secretion by gamma/delta T lymphocytes after activation with bacteria. J Immunol. 1990 Oct 15;145(8):2434–2439. [PubMed] [Google Scholar]
  18. Natsuhara Y., Yoshinaga J., Shogaki T., Sumi-Nishikawa Y., Kurano S., Kato Y., Kaneda K., Oka S., Yano I. Granuloma-forming activity and antitumor activity of newly isolated mycoloyl glycolipid from Rhodococcus terrae 70012 (Rt. GM-2). Microbiol Immunol. 1990;34(1):45–53. doi: 10.1111/j.1348-0421.1990.tb00990.x. [DOI] [PubMed] [Google Scholar]
  19. O'Brien R. L., Happ M. P., Dallas A., Palmer E., Kubo R., Born W. K. Stimulation of a major subset of lymphocytes expressing T cell receptor gamma delta by an antigen derived from Mycobacterium tuberculosis. Cell. 1989 May 19;57(4):667–674. doi: 10.1016/0092-8674(89)90135-9. [DOI] [PubMed] [Google Scholar]
  20. Ohga S., Yoshikai Y., Takeda Y., Hiromatsu K., Nomoto K. Sequential appearance of gamma/delta- and alpha/beta-bearing T cells in the peritoneal cavity during an i.p. infection with Listeria monocytogenes. Eur J Immunol. 1990 Mar;20(3):533–538. doi: 10.1002/eji.1830200311. [DOI] [PubMed] [Google Scholar]
  21. Parker C. M., Groh V., Band H., Porcelli S. A., Morita C., Fabbi M., Glass D., Strominger J. L., Brenner M. B. Evidence for extrathymic changes in the T cell receptor gamma/delta repertoire. J Exp Med. 1990 May 1;171(5):1597–1612. doi: 10.1084/jem.171.5.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pfeffer K., Schoel B., Gulle H., Kaufmann S. H., Wagner H. Primary responses of human T cells to mycobacteria: a frequent set of gamma/delta T cells are stimulated by protease-resistant ligands. Eur J Immunol. 1990 May;20(5):1175–1179. doi: 10.1002/eji.1830200534. [DOI] [PubMed] [Google Scholar]
  23. Saito T., Weiss A., Miller J., Norcross M. A., Germain R. N. Specific antigen-Ia activation of transfected human T cells expressing murine Ti alpha beta-human T3 receptor complexes. Nature. 1987 Jan 8;325(7000):125–130. doi: 10.1038/325125a0. [DOI] [PubMed] [Google Scholar]
  24. Shiratsuchi H., Tsuyuguchi I. Tuberculin purified protein derivative-reactive T cells in cord blood lymphocytes. Infect Immun. 1981 Sep;33(3):651–657. doi: 10.1128/iai.33.3.651-657.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Smith M. D., Worman C., Yüksel F., Yüksel B., Moretta L., Ciccone E., Grossi C. E., MacKenzie L., Lydyard P. M. T gamma delta-cell subsets in cord and adult blood. Scand J Immunol. 1990 Nov;32(5):491–495. doi: 10.1111/j.1365-3083.1990.tb03189.x. [DOI] [PubMed] [Google Scholar]
  26. Söderström K., Halapi E., Nilsson E., Grönberg A., van Embden J., Klareskog L., Kiessling R. Synovial cells responding to a 65-kDa mycobacterial heat shock protein have a high proportion of a TcR gamma delta subtype uncommon in peripheral blood. Scand J Immunol. 1990 Nov;32(5):503–515. doi: 10.1111/j.1365-3083.1990.tb03191.x. [DOI] [PubMed] [Google Scholar]
  27. Tsuyuguchi I., Kawasumi H., Takashima T., Tsuyuguchi T., Kishimoto S. Mycobacterium avium-Mycobacterium intracellular complex-induced suppression of T-cell proliferation in vitro by regulation of monocyte accessory cell activity. Infect Immun. 1990 May;58(5):1369–1378. doi: 10.1128/iai.58.5.1369-1378.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yano I., Tomiyasu I., Kaneda K., Kato Y., Sumi Y., Kurano S., Sugimoto N., Sawai H. Isolation of mycolic acid-containing glycolipids in Nocardia rubra and their granuloma forming activity in mice. J Pharmacobiodyn. 1987 Mar;10(3):113–123. doi: 10.1248/bpb1978.10.113. [DOI] [PubMed] [Google Scholar]
  29. Yoshikai Y., Matsuzaki G., Inoue T., Nomoto K. An increase in number of T-cell receptor gamma/delta-bearing T cells in athymic nude mice treated with complete Freund's adjuvants. Immunology. 1990 May;70(1):61–65. [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES