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PMID: 8454323 Published · ppublish English Journal Article

Temporal relationship of cytokine release by peripheral blood mononuclear cells stimulated by the streptococcal superantigen pep M5.

Infection and immunity ·Vol. 61 ·No. 4 ·1993-04-00 ·Pages 1194-201

Kotb M, Ohnishi H, Majumdar G, Hackett S, Bryant A, Higgins G, Stevens D

Abstract

We undertook this study to determine the quality, quantity, and temporal relationship of pep M5-induced cytokine release. The ability of pep M5 to stimulate interleukin-1 (IL-1) and tumor necrosis factor alpha (TNF-alpha) production by a T-cell-depleted, monocyte- and B-cell-enriched cell population was dependent on the presence of T cells. The requirement for T cells could be met by addition of exogenous gamma interferon (IFN-gamma). In the presence of IFN-gamma, pep M5 induced the release of TNF-alpha, IL-1, and IL-6, TNF-alpha levels peaked at 24 h, while IL-1 and IL-6 levels peaked at 48 h. pep M5 induced T cells to produce IFN-gamma, which may have accounted for the ability of the super antigen to induce the production of IL-1, IL-6, TNF-alpha, and TNF-beta by peripheral blood mononuclear cells (PBMC). The addition of excess IFN-gamma to cultures of pep M5 and PBMC did not further increase the release of these cytokines at 24 and 48 h but resulted in sustained higher levels at 72 h. Interestingly, TNF-beta production occurred only in the presence of pep M5 and exogenous IFN-gamma. The ability of pep M5 to induce cytokine production was compared with that of a potent super antigen, staphylococcal enterotoxin B (SEB). SEB was a 2- to 14-fold-more-potent inducer of IFN-gamma production. Furthermore, the profile of cytokine released by PBMC in response to this super antigen mimicked that seen with pep M5 in the presence of exogenous IFN-gamma. In conclusion, pep M5 induces the production of cytokines that are involved in immune regulation and inflammation. These cytokines also play a major role in human T-cell responses to this super antigen.

MeSH Terms
Adult Antigen-Presenting Cells/immunology Antigens, Bacterial/immunology Bacterial Outer Membrane Proteins Bacterial Proteins/immunology Carrier Proteins Cells, Cultured Cytokines/metabolism Enterotoxins/immunology Humans In Vitro Techniques Interferon-gamma/pharmacology Leukocytes, Mononuclear/immunology Streptococcus pyogenes/immunology T-Lymphocytes/immunology Time Factors
Chemicals
Antigens, Bacterial Bacterial Outer Membrane Proteins Bacterial Proteins Carrier Proteins Cytokines Enterotoxins streptococcal M protein enterotoxin B, staphylococcal Interferon-gamma
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Kotb M
Veterans Affairs Medical Center, Memphis, Tennessee 38104.
Ohnishi H
Majumdar G
Hackett S
Bryant A
Higgins G
Stevens D
References (55)
55 references, click to expand
  1. Regulation of tumor necrosis factor/cachectin and IL-1 secretion in human mononuclear phagocytes.
    J Immunol. 1988 May 15;140(10):3473-81 PMID: 3258884
  2. Group A streptococcal M proteins: virulence factors and protective antigens.
    Immunol Today. 1992 Sep;13(9):362-7 PMID: 1281632
  3. Correlation of plasma interleukin 1 levels with disease activity in rheumatoid arthritis.
    Lancet. 1988 Sep 24;2(8613):706-9 PMID: 2901567
  4. Failure of hydrocortisone to suppress the interferon-gamma-induced augmentation of interleukin 1 secretion of aged human monocytes.
    Immunobiology. 1988 Jul;177(3):245-53 PMID: 3139548
  5. Production of tumor necrosis factor by human monocytes in response to toxic-shock-syndrome toxin-1.
    J Infect Dis. 1988 Nov;158(5):1026-33 PMID: 3263447
  6. The glomerular permeability determined by dextran clearance using Sephadex gel filtration.
    Scand J Clin Lab Invest. 1968;21(1):77-82 PMID: 5637478
  7. An improved rosetting assay for detection of human T lymphocytes.
    J Immunol Methods. 1974 Jul;5(2):131-5 PMID: 4600315
  8. Human immune response to immunization with a structurally defined polypeptide fragment of streptococcal M protein.
    J Exp Med. 1979 Oct 1;150(4):862-77 PMID: 390084
  9. Blastogenic responses of human lymphocytes to structurally defined polypeptide fragments of streptococcal M protein.
    J Immunol. 1981 Apr;126(4):1499-505 PMID: 7009743
  10. Antiopsonic activity of fibrinogen bound to M protein on the surface of group A streptococci.
    J Clin Invest. 1982 Apr;69(4):1042-5 PMID: 7042754
  11. Induction of human interleukin-1 by a product of Staphylococcus aureus associated with toxic shock syndrome.
    J Clin Invest. 1984 May;73(5):1312-20 PMID: 6609169
  12. 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):1339-45 PMID: 6235287
  13. Resurgence of acute rheumatic fever in the intermountain area of the United States.
    N Engl J Med. 1987 Feb 19;316(8):421-7 PMID: 3807984
  14. Clinical and bacteriologic observations of a toxic shock-like syndrome due to Streptococcus pyogenes.
    N Engl J Med. 1987 Jul 16;317(3):146-9 PMID: 3299086
  15. Toxic shock syndrome-associated staphylococcal and streptococcal pyrogenic toxins are potent inducers of tumor necrosis factor production.
    Infect Immun. 1989 Jan;57(1):291-4 PMID: 2642470
  16. Role of toxic shock syndrome toxin 1 in toxic shock syndrome: overview.
    Rev Infect Dis. 1989 Jan-Feb;11 Suppl 1:S107-9 PMID: 2648535
  17. Stimulation of T cells and induction of interferon by toxic shock syndrome toxin 1.
    Rev Infect Dis. 1989 Jan-Feb;11 Suppl 1:S305-12 PMID: 2494690
  18. Defective T-cell activation by Mycoplasma arthritidis mitogen is restored by interferon-gamma.
    Cell Immunol. 1989 Apr 15;120(1):188-94 PMID: 2495188
  19. Downregulation of tumor necrosis factor receptors of macrophages by interferons and interleukin-1. Role of protein kinase C activation.
    J Biol Regul Homeost Agents. 1988 Oct-Dec;2(4):166-72 PMID: 2471393
  20. Severe group A streptococcal infections associated with a toxic shock-like syndrome and scarlet fever toxin A.
    N Engl J Med. 1989 Jul 6;321(1):1-7 PMID: 2659990
  21. IL-6 inhibits lipopolysaccharide-induced tumor necrosis factor production in cultured human monocytes, U937 cells, and in mice.
    J Immunol. 1989 Dec 1;143(11):3517-23 PMID: 2584704
  22. Regulation of expression of human IL-1 alpha and IL-1 beta genes.
    J Immunol. 1989 Dec 1;143(11):3556-61 PMID: 2511244
  23. Down regulation of the receptors for tumor necrosis factor by interleukin 1 and 4 beta-phorbol-12-myristate-13-acetate.
    J Immunol. 1987 Aug 15;139(4):1161-7 PMID: 3038998
  24. Toxic shock syndrome toxin 1 as an inducer of human tumor necrosis factors and gamma interferon.
    J Exp Med. 1988 Mar 1;167(3):752-61 PMID: 3127526
  25. Cytokines and immunoglobulin in rheumatic heart disease: production by blood and tonsillar mononuclear cells.
    J Rheumatol. 1989 Nov;16(11):1436-42 PMID: 2600943
  26. Rheumatogenic group A streptococci and the return of rheumatic fever.
    Adv Intern Med. 1990;35:1-25 PMID: 2405590
  27. Endothelial cell production of nitrogen oxides in response to interferon gamma in combination with tumor necrosis factor, interleukin-1, or endotoxin.
    J Natl Cancer Inst. 1990 May 2;82(9):772-6 PMID: 2109093
  28. The staphylococcal enterotoxins and their relatives.
    Science. 1990 May 11;248(4956):705-11 PMID: 2185544
  29. Production of TNF-alpha and TNF-beta by staphylococcal enterotoxin A activated human T cells.
    J Immunol. 1990 Jun 15;144(12):4663-9 PMID: 1972165
  30. Superantigenicity of streptococcal M protein.
    J Exp Med. 1990 Jul 1;172(1):359-62 PMID: 2358781
  31. Cytokine regulation of human monocyte interleukin-1 (IL-1) production in vitro. Enhancement of IL-1 production by interferon (IFN) gamma, tumour necrosis factor-alpha, IL-2 and IL-1, and inhibition by IFN-alpha.
    Clin Exp Immunol. 1990 Jun;80(3):435-43 PMID: 2115419
  32. IFN-gamma regulates the expression of the adhesion molecule ELAM-1 and IL-6 production by human endothelial cells in vitro.
    J Immunol. 1990 Oct 1;145(7):2110-4 PMID: 1697876
  33. In vivo induction of anergy in peripheral V beta 8+ T cells by staphylococcal enterotoxin B.
    J Exp Med. 1990 Oct 1;172(4):1091-100 PMID: 2212944
  34. Aberrant regulation of IL-1 expression in macrophages from young autoimmune-prone mice.
    J Immunol. 1990 Nov 15;145(10):3231-9 PMID: 2230116
  35. Induction of specific clonal anergy in human T lymphocytes by Staphylococcus aureus enterotoxins.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):8884-8 PMID: 1978940
  36. Dissociation of the stimulatory activities of staphylococcal enterotoxins for T cells and monocytes.
    J Exp Med. 1990 Dec 1;172(6):1831-41 PMID: 2258710
  37. Programmed cell death and extrathymic reduction of Vbeta8+ CD4+ T cells in mice tolerant to Staphylococcus aureus enterotoxin B.
    Nature. 1991 Jan 17;349(6306):245-8 PMID: 1670963
  38. A potential role for microbial superantigens in the pathogenesis of systemic autoimmune disease.
    Arthritis Rheum. 1991 Apr;34(4):468-80 PMID: 1826427
  39. Interleukin 1 alpha, tumor necrosis factor alpha, and interferon gamma in psoriasis.
    Arch Dermatol. 1991 Jun;127(6):827-30 PMID: 1903629
  40. T cell receptor V gene usage by human T cells stimulated with the superantigen streptococcal M protein.
    J Exp Med. 1991 Jul 1;174(1):285-8 PMID: 1711564
  41. Streptococcal M protein.
    Sci Am. 1991 Jun;264(6):58-65 PMID: 1857955
  42. Group A streptococcal infections and acute rheumatic fever.
    N Engl J Med. 1991 Sep 12;325(11):783-93 PMID: 1870652
  43. Staphylococcal exotoxins stimulate nitric oxide-dependent murine macrophage tumoricidal activity.
    Infect Immun. 1991 Sep;59(9):2987-93 PMID: 1908828
  44. Induction of interleukin-1 in human monocytes by the superantigen staphylococcal enterotoxin A requires the participation of T cells.
    Cell Immunol. 1991 Oct 1;137(1):61-71 PMID: 1884398
  45. The Mycoplasma arthritidis T-cell mitogen, MAM: a model superantigen.
    Immunol Today. 1991 Aug;12(8):271-6 PMID: 1910449
  46. Superantigens: mechanism of T-cell stimulation and role in immune responses.
    Annu Rev Immunol. 1991;9:745-72 PMID: 1832875
  47. Staphylococcal enterotoxin microbial superantigens.
    FASEB J. 1991 Sep;5(12):2706-12 PMID: 1916093
  48. IL-6 and IL-6 receptor modulation by IFN-gamma and tumor necrosis factor-alpha in human monocytic cell line (THP-1). Priming effect of IFN-gamma.
    J Immunol. 1991 Oct 15;147(8):2630-7 PMID: 1918983
  49. Modulating activity of interferon-gamma on endotoxin-induced cytokine production in cancer patients.
    Blood. 1991 Dec 15;78(12):3254-8 PMID: 1720701
  50. Distinct T-cell receptor V beta gene usage by human T lymphocytes stimulated with the streptococcal pyrogenic exotoxins and pep M5 protein.
    Infect Immun. 1992 Feb;60(2):701-5 PMID: 1530928
  51. Separation of T-cell-stimulating activity from streptococcal M protein.
    Infect Immun. 1992 May;60(5):1767-70 PMID: 1563763
  52. Invasive group A streptococcus infections.
    Clin Infect Dis. 1992 Jan;14(1):2-11 PMID: 1571429
  53. Induction of tumor necrosis factor and interleukin-1 by purified staphylococcal toxic shock syndrome toxin 1 requires the presence of both monocytes and T lymphocytes.
    Infect Immun. 1992 Jul;60(7):2612-8 PMID: 1612731
  54. Bacterial toxin-induced cytokine production studied at the single-cell level.
    Immunol Rev. 1992 Jun;127:69-96 PMID: 1506008
  55. Changing group A streptococci. The reappearance of streptococcal 'toxic shock'.
    Arch Intern Med. 1988 Jun;148(6):1268-70 PMID: 3288156
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1993-04-00
Pages
1194-201
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC281348
Subset
IM
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