Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1989 Apr;57(4):1151–1157. doi: 10.1128/iai.57.4.1151-1157.1989

Brucella abortus regulates bovine macrophage-T-cell interaction by major histocompatibility complex class II and interleukin-1 expression.

G A Splitter 1, K M Everlith 1
PMCID: PMC313244  PMID: 2494112

Abstract

T-cell activation is dependent on nominal antigen associated with major histocompatibility complex (MHC) class II molecules and interleukin-1 (IL-1), both provided by antigen-presenting cells. We have studied the effects of Brucella abortus and recombinant bovine gamma interferon (IFN-gamma) on bovine macrophage expression of MHC class II and IL-1 molecules and subsequent T-cell proliferation in response to B. abortus. When peripheral blood mononuclear cells were cocultured with B. abortus and IFN-gamma, increasing amounts of IFN-gamma, from 1 to 100 U/ml, down regulated T-cell proliferation. Expression of MHC class II molecules on macrophages was increased independently by IFN-gamma or B. abortus treatment. Thus, class II molecule expression was not the cause of down regulation of T-cell proliferation as observed in other systems. However, B. abortus-IFN-gamma-treated macrophages obtained from overnight cultures had minimal membrane IL-1 compared with macrophages treated with B. abortus alone. Loss of membrane IL-1 required IFN-gamma and the o-polysaccharide of the lipopolysaccharide. IFN-gamma at 1 U/ml in combination with B. abortus produced a 32% decrease in T-cell response, while IFN-gamma at 100 U/ml added to B. abortus-treated cultures produced an 82% reduction in T-cell response. Membrane IL-1 levels were not altered when recombinant bovine IFN-alpha or the rough strain 45/20 of B. abortus, which lacks the o-polysaccharide, was used. Secreted IL-1 levels were unaffected by IFN-gamma and B. abortus treatment. The addition of recombinant bovine IL-1 beta (0.001 to 0.1 ng/ml) to B. abortus- and IFN-gamma-treated cultures failed to provide a signal necessary for T-cell proliferation. These data suggest that membrane IL-1 has a key role in T-cell activation in response to B. abortus. When the o-polysaccharide of B. abortus lipopolysaccharide is combined with IFN-gamma at an inappropriate time during an immune response, T-cell proliferation is prevented and cannot be restored by the addition of exogenous IL-1.

Full text

PDF
1157

Selected References

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

  1. Bakouche O., Brown D. C., Lachman L. B. Subcellular localization of human monocyte interleukin 1: evidence for an inactive precursor molecule and a possible mechanism for IL 1 release. J Immunol. 1987 Jun 15;138(12):4249–4255. [PubMed] [Google Scholar]
  2. Beller D. I., Ho K. Regulation of macrophage populations. V. Evaluation of the control of macrophage Ia expression in vitro. J Immunol. 1982 Sep;129(3):971–976. [PubMed] [Google Scholar]
  3. Berman M. A., Sandborg C. I., Calabia B. S., Andrews B. S., Friou G. J. Studies of an interleukin 1 inhibitor: characterization and clinical significance. Clin Exp Immunol. 1986 Apr;64(1):136–145. [PMC free article] [PubMed] [Google Scholar]
  4. Blanchard D. K., Djeu J. Y., Klein T. W., Friedman H., Stewart W. E., 2nd Interferon-gamma induction by lipopolysaccharide: dependence on interleukin 2 and macrophages. J Immunol. 1986 Feb 1;136(3):963–970. [PubMed] [Google Scholar]
  5. Bonney R. J., Humes J. L. Physiological and pharmacological regulation of prostaglandin and leukotriene production by macrophages. J Leukoc Biol. 1984 Jan;35(1):1–10. doi: 10.1002/jlb.35.1.1. [DOI] [PubMed] [Google Scholar]
  6. Browning J. L., Ribolini A. Interferon blocks interleukin 1-induced prostaglandin release from human peripheral monocytes. J Immunol. 1987 May 1;138(9):2857–2863. [PubMed] [Google Scholar]
  7. Chen B. D., Lin H. S., Hsu S. Lipopolysaccharide inhibits the binding of colony-stimulating factor (CSF-1) to murine peritoneal exudate macrophages. J Immunol. 1983 May;130(5):2256–2260. [PubMed] [Google Scholar]
  8. Conlon P. J., Grabstein K. H., Alpert A., Prickett K. S., Hopp T. P., Gillis S. Localization of human mononuclear cell interleukin 1. J Immunol. 1987 Jul 1;139(1):98–102. [PubMed] [Google Scholar]
  9. Economou J. S., Shin H. S. Lymphocyte-activating factor. I. Generation and physicochemical characterization. J Immunol. 1978 Oct;121(4):1446–1452. [PubMed] [Google Scholar]
  10. Jerrells T. R., Dean J. H., Richardson G. L., Herberman R. B. Depletion of monocytes from human peripheral blood mononuclear leukocytes: comparison of the sephadex G-10 column method with other commonly used techniques. J Immunol Methods. 1980;32(1):11–29. doi: 10.1016/0022-1759(80)90113-1. [DOI] [PubMed] [Google Scholar]
  11. Kaye J., Gillis S., Mizel S. B., Shevach E. M., Malek T. R., Dinarello C. A., Lachman L. B., Janeway C. A., Jr Growth of a cloned helper T cell line induced by a monoclonal antibody specific for the antigen receptor: interleukin 1 is required for the expression of receptors for interleukin 2. J Immunol. 1984 Sep;133(3):1339–1345. [PubMed] [Google Scholar]
  12. Koerner T. J., Hamilton T. A., Adams D. O. Suppressed expression of surface Ia on macrophages by lipopolysaccharide: evidence for regulation at the level of accumulation of mRNA. J Immunol. 1987 Jul 1;139(1):239–243. [PubMed] [Google Scholar]
  13. Kurt-Jones E. A., Beller D. I., Mizel S. B., Unanue E. R. Identification of a membrane-associated interleukin 1 in macrophages. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1204–1208. doi: 10.1073/pnas.82.4.1204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kurt-Jones E. A., Kiely J. M., Unanue E. R. Conditions required for expression of membrane IL 1 on B cells. J Immunol. 1985 Sep;135(3):1548–1550. [PubMed] [Google Scholar]
  15. Kurt-Jones E. A., Virgin H. W., 4th, Unanue E. R. In vivo and in vitro expression of macrophage membrane interleukin 1 in response to soluble and particulate stimuli. J Immunol. 1986 Jul 1;137(1):10–14. [PubMed] [Google Scholar]
  16. Kurt-Jones E. A., Virgin H. W., 4th, Unanue E. R. Relationship of macrophage Ia and membrane IL 1 expression to antigen presentation. J Immunol. 1985 Dec;135(6):3652–3654. [PubMed] [Google Scholar]
  17. Le J. M., Weinstein D., Gubler U., Vilcek J. Induction of membrane-associated interleukin 1 by tumor necrosis factor in human fibroblasts. J Immunol. 1987 Apr 1;138(7):2137–2142. [PubMed] [Google Scholar]
  18. Lewin H. A., Calvert C. C., Bernoco D. Cross-reactivity of a monoclonal antibody with bovine, equine, ovine, and porcine peripheral blood B lymphocytes. Am J Vet Res. 1985 Apr;46(4):785–788. [PubMed] [Google Scholar]
  19. Liao Z., Haimovitz A., Chen Y., Chan J., Rosenstreich D. L. Characterization of a human interleukin 1 inhibitor. J Immunol. 1985 Jun;134(6):3882–3886. [PubMed] [Google Scholar]
  20. Loppnow H., Brade L., Brade H., Rietschel E. T., Kusumoto S., Shiba T., Flad H. D. Induction of human interleukin 1 by bacterial and synthetic lipid A. Eur J Immunol. 1986 Oct;16(10):1263–1267. doi: 10.1002/eji.1830161013. [DOI] [PubMed] [Google Scholar]
  21. Marshall R. L., Rodriguez L. L., Letchworth G. J., 3rd Characterization of envelope proteins of infectious bovine rhinotracheitis virus (bovine herpesvirus 1) by biochemical and immunological methods. J Virol. 1986 Mar;57(3):745–753. doi: 10.1128/jvi.57.3.745-753.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mizel S. B., Oppenheim J. J., Rosentreich D. L. Characterization of lymphocyte-activating factor (LAF) produced by a macrophage cell line, P388D1. II. Biochemical characterization of LAF induced by activated T cells and LPS. J Immunol. 1978 May;120(5):1504–1508. [PubMed] [Google Scholar]
  23. Moreno E., Jones L. M., Berman D. T. Immunochemical characterization of rough Brucella lipopolysaccharides. Infect Immun. 1984 Mar;43(3):779–782. doi: 10.1128/iai.43.3.779-782.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Moreno E., Kurtz R. S., Berman D. T. Induction of immune and adjuvant immunoglobulin G responses in mice by Brucella lipopolysaccharide. Infect Immun. 1984 Oct;46(1):74–80. doi: 10.1128/iai.46.1.74-80.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moreno E., Pitt M. W., Jones L. M., Schurig G. G., Berman D. T. Purification and characterization of smooth and rough lipopolysaccharides from Brucella abortus. J Bacteriol. 1979 May;138(2):361–369. doi: 10.1128/jb.138.2.361-369.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nagelkerken L. M., van Breda Vriesman P. J. Membrane-associated IL 1-like activity on rat dendritic cells. J Immunol. 1986 Mar 15;136(6):2164–2170. [PubMed] [Google Scholar]
  27. Noma T., Dorf M. E. Modulation of suppressor T cell induction with gamma-interferon. J Immunol. 1985 Dec;135(6):3655–3660. [PubMed] [Google Scholar]
  28. Roberts N. J., Jr, Prill A. H., Mann T. N. Interleukin 1 and interleukin 1 inhibitor production by human macrophages exposed to influenza virus or respiratory syncytial virus. Respiratory syncytial virus is a potent inducer of inhibitor activity. J Exp Med. 1986 Mar 1;163(3):511–519. doi: 10.1084/jem.163.3.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rodgers B. C., Scott D. M., Mundin J., Sissons J. G. Monocyte-derived inhibitor of interleukin 1 induced by human cytomegalovirus. J Virol. 1985 Sep;55(3):527–532. doi: 10.1128/jvi.55.3.527-532.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Scala G., Kuang Y. D., Hall R. E., Muchmore A. V., Oppenheim J. J. Accessory cell function of human B cells. I. Production of both interleukin 1-like activity and an interleukin 1 inhibitory factor by an EBV-transformed human B cell line. J Exp Med. 1984 Jun 1;159(6):1637–1652. doi: 10.1084/jem.159.6.1637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Splitter G. A., Everlith K. M. Collaboration of bovine T lymphocytes and macrophages in T-lymphocyte response to Brucella abortus. Infect Immun. 1986 Mar;51(3):776–783. doi: 10.1128/iai.51.3.776-783.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Splitter G., Burkholder J., O'Reilly K., Janzer A. Anti-BoLA-w8 monoclonal antibody: production of a tissue typing reagent after blocking monomorphic sites on bovine mononuclear cells. Tissue Antigens. 1987 Sep;30(3):122–127. doi: 10.1111/j.1399-0039.1987.tb01608.x. [DOI] [PubMed] [Google Scholar]
  33. Srikumaran S., Guidry A. J., Goldsby R. A. Production and characterization of monoclonal bovine immunoglobulins G1, G2 and M from bovine x murine hybridomas. Vet Immunol Immunopathol. 1984 Mar;5(4):323–342. doi: 10.1016/0165-2427(84)90002-3. [DOI] [PubMed] [Google Scholar]
  34. Steeg P. S., Johnson H. M., Oppenheim J. J. Regulation of murine macrophage Ia antigen expression by an immune interferon-like lymphokine: inhibitory effect of endotoxin. J Immunol. 1982 Dec;129(6):2402–2406. [PubMed] [Google Scholar]
  35. Steeg P. S., Moore R. N., Johnson H. M., Oppenheim J. J. Regulation of murine macrophage Ia antigen expression by a lymphokine with immune interferon activity. J Exp Med. 1982 Dec 1;156(6):1780–1793. doi: 10.1084/jem.156.6.1780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Takacs L., Berzofsky J. A., York-Jolley J., Akahoshi T., Blasi E., Durum S. K. IL 1 induction by murine T cell clones: detection of an IL 1-inducing lymphokine. J Immunol. 1987 Apr 1;138(7):2124–2131. [PubMed] [Google Scholar]
  37. Unanue E. R., Allen P. M. The basis for the immunoregulatory role of macrophages and other accessory cells. Science. 1987 May 1;236(4801):551–557. doi: 10.1126/science.2437650. [DOI] [PubMed] [Google Scholar]
  38. Unanue E. R., Beller D. I., Lu C. Y., Allen P. M. Antigen presentation: comments on its regulation and mechanism. J Immunol. 1984 Jan;132(1):1–5. [PubMed] [Google Scholar]
  39. Wentworth P. A., Ziegler H. K. Induction of macrophage Ia expression by lipopolysaccharide and Listeria monocytogenes in congenitally athymic nude mice. J Immunol. 1987 May 15;138(10):3167–3173. [PubMed] [Google Scholar]
  40. Windle J. J., Shin H. S., Morrow J. F. Induction of interleukin 1 messenger RNA and translation in oocytes. J Immunol. 1984 Mar;132(3):1317–1322. [PubMed] [Google Scholar]
  41. Ziegler H. K., Staffileno L. K., Wentworth P. Modulation of macrophage Ia-expression by lipopolysaccharide. I. Induction of Ia expression in vivo. J Immunol. 1984 Oct;133(4):1825–1835. [PubMed] [Google Scholar]

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

RESOURCES