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. 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.

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Selected References

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  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]

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