Abstract
Recently, it has been appreciated that cultured mast cells are significant sources of cytokines. However, the role of interkeukin-1 (IL-1) on mast cells and/or basophil degranulation is still unclear. In this report we provide evidence that rat basophilic leukemia cells (RBLC) cultured with a natural inhibitor of IL-1, interleukin-1 receptor antagonist (IL-1RA) (500 ng/ml) for 48 h, strongly inhibited the spontaneous release of serotonin (5HT) and histamine (from 22.50 to 43.49%), compared to untreated cells (control). When IL-1RA-treated and untreated RBLC were stimulated with a secretagogue (anti-IgE), no difference was found in the percent of 5HT and histamine release. Moreover, in another set of experiments using rat peritoneal mast cells (RPMC) treated and untreated with IL-1RA, we found that IL-1RA did not affect the release of 5HT or histamine, even when the secretagogue anti-IgE or compound 48/80 (C48/80) were used. The present studies describe an additional biological activity of IL-1RA, inhibiting histamine and 5HT release from RBLC cultures.
Similar content being viewed by others
Abbreviations
- IL-1:
-
interleukin-1
- RA:
-
receptor antagonist
- 5HT:
-
serotonin
- RBLC:
-
rat basophilic leukemia cells
- RPMC:
-
rat peritoneal mast cells
- IgE:
-
immunoglobulin E
- FcΣ :
-
immunoglobulin E receptor
- CPM:
-
counts per minute
- BSA:
-
bovine serum albumin
- C48/80:
-
compound 48/80
- TNF:
-
tumor necrosis factor
References
Serafin E, Austen KF: Mediators of immediate hypersensitivity reactions. N Engl J Med 317: 87–138, 1987
Theoharides TC, Bondy PK, Tsakalos ND, Askenase PW: Differential release of serotonin and histamine from mast cells. Nature 297: 229, 1982
Plaut M, Pierce JH, Watson CJ, Hanley-Hyde J, Nordan RP, Paul WE: Mast cell lines produce lymphokines in response to cross-linkage of FcΣRI or to calcium ionophores. Nature 339: 64–67, 1989
Sieghart W, Theoharides TC, Alper DS, Douglas WW, Greengard P: Calcium dependent protein phosphorylation during exocytotic release of mast cell secretory granules. Nature 275: 329–331, 1978
Lewis RA, Austen KF: Mediation of local homeostasis and inflammatory by leukotrienes and other mast cell-dependent compounds. Nature 293: 103, 1981
Conti P, Reale M, Barbacane RC, Panara MR, Bongrazio M, Theoharides TO Role of lipoxin A4 and B4 in the generation of arachidonic acid metabolites by rat mast cells and their effect on [3H]serotonin release. Immunol Lett 32: 117–124, 1992
Kulczycki A, Isersky C, Metzgze H: The interaction of IgE with rat basophilic leukemia cells. I. Evidence for specific binding of IgE. J Exp Med 139: 600, 1974
Conrad DH, Berczi I, Froese A: Characterization of the target cell receptor for IgE-I. Solubilization of IgE-receptor complexes from rat mast cells and rat basophilic leukemia cells. J Immunol 13: 320–332, 1976
Bonifacino JS, Perez P, Klausner RD, Sandoval IV: Study of the transit of an integral membrane protein from secretory granules through the plasma membrane of secreting rat basophilic leukemia cells using a specific monoclonal antibody. J Cell Biol 102: 516–522, 1986
Theoharides TC, Douglas WW: Secretion in mast cells induced by calcium entrapped within phospholipid vescicles. Science 201: 1143–1145, 1978
Isersky C, Metzger H, Buell DN: Cell cycle-associated changes in receptors for IgE during growth and differentiation of a rat basophilic leukemia cell line. J Exp Med 141: 1147–1162, 1975
Williams ME, Chang TL, Burke SK, Lichtman AH, Abbas AK: Activation of functionally distinct subset of CD4+ T lymphocytes. Res Immunol Inst Pasteur 142: 23–28, 1991
Chang TL, Shea CM, Urioste S, Thompson RC, Boom WH, Abbas AK: Heterogeneity of helper/inducer T lymphocytes. III. Response of IL-2 and IL-4 production (TH1 and TH2) clones to antigen presented by different accessory cells. J Immunol 145: 2803–2808, 1990
Mizel SB: The interleukins. Faseb J 3: 2379–2388, 1989
Seckinger P, Lowenthal JW, Williamson K, Dayer J-M, McDonald HR: A urine inhibitor of interleukin-1 activity that blocks ligand binding. J Immunol 139: 1546–1549, 1987
Dinarello CA, Rosenwasser LJ, Wolff SM: Demonstration of a circulating thymocytes suppressor factor during endotoxin fever in humans. J Immunol 127: 2517–2519, 1982
Hannum CH, Wilcox CJ, Arend WP, Joslin FG, Dripps DJ, Heimdal PLet al.: Interleukin-1 receptor antagonist activity of a human interleukin-1 inhibitor. Nature 343: 336–340, 1990
Carter DB, Deibel MR, Dunn CJ, Tomich CSC, Laborde AL, Slightom JLet al.: Purification, cloning, expression and biological characterization of interleukin-1 receptor antagonist protein. Nature 344: 633–637, 1990
Eisenberg SP, Evans RJ, Arend WP, Verderber E, Brewer MT, Hannum CH, Thompson, RC: Primary structure and functional expression from complementary DNA of a human interleukin-1 receptor antagonist. Nature 343: 341–346, 1990
Arend WP, Welgus HG, Thompson RC, Eisenberg, SP: Biological properties of recombinant human monocyte-derived interleukin-1 receptor anagonist. J Clin Invest 85: 1694–1697, 1990
Dinarello CA: Strategies for anti- interleukin-1 therapy. Int J Immunopathol Pharmacol 2: 203–211, 1989
Wakabayashi G, Gelfand JA, Jung WK, Connolly RJ, Burke JF, Dinarello CA: Staphylococcus epidermis induces complement activation, tumor necrosis factor and interleukin-1, a shock-like state and tissue injury in rabbits without endotoxemia. J Clin Invest 87: 1925–1935, 1991
Conti P, Feliciani C, Barbacane RC, Panara MR, Reale M, Placido FC, Sander DN, Dempsey RA, Amerio P: Inhibition of interleukin1-β mRNA expression and interleukin-1α and β secretion by a specific human recombiant interleukin-1 receptor antagonist in human peripheral blood mononuclear cells. Immunology 77: 245–250, 1992
Conti P, Dempsey R: Macrophage down-regulation by interleukin-1 receptor antagonist. Am J Hematol 39/4: 310–311, 1991
Dinarello CA: Interleukin-1 and its biologically related cytokines. Adv Immunol 44: 153, 1989
Conti P, Panara MR, Barbacane RC, Placido FC, Bongrazio M, Reale M, Dempsey RA, Fiore S: Blocking the interleukin-1 receptor inhibits leukotriene B4 (LTB4) and prostaglandin E2 (PGE2) generation in human monocyte cultures. Cell Immunol 145: 199–209, 1992
Conti P, Panara MR, Fridas S, Barbacane RC, Reale M, Dempsey RA, Placido FC: Inhibition ofin vivo induced chronic inflammation by human recombinant interleukin-1 receptor antagonisyt (hrIL-Ira). New Adv Cytokines, Raven Press, NY 92: 361–365, 1992
Haak-Frendscho M, Dinarello C, Kaplan AP: Recombinant interleukin-1β causes histamine release from human basophils. JAllergy Clin Immunol 82: 218–223, 1988
Subramanian N, Bray MA: Interleukin-1 releases histamine from human basophils and mast cellsin vitro. J Immunol 138: 271–275, 1987
Kaplan AP, Haak-Frendscho M, Fauci A, Dinarello CA, Malbert E: A histamine releasing factor from activated human mononuclear cells. J Immunol 135: 2027–2032, 1985
Plaut M, Pierce JH, Watson CJ, Hanley-Hyde J, Nordon RP, Paul WE: Mast cell lines produce lymphokines in response to cross linkage of FcΣRI or calcium ionophore. Nature 339: 64, 1989
Wodnar-Filipowicz A, Heusser CH, Moroni C: Production of hematopoietic growth factor GM-CSF and interleukin-3 by mast cells in response to IgE receptor-mediated activation. Nature 39: 150, 1989
Burd PR, Rogers HW, Gordon JR, Martin CA, Jayaraman S, Wilson D, Dvorak AM, Galli SJ, Dorf ME: Interleukin 3-dependent and -independent mast cells stimulated with IgE and antigen express multiple cytokines. J Exp Med 170: 245, 1989
Ansel JC, Brown JR, Payan DG, Brown MA: Substance P selectively activates TNF-α gene expression in murine mast cells. J Immunol 150: 4478–4485, 1993
Tung R, Lichtenstein LM:In vitro histamine release from basophils of asthmatica and atopic individuals in D20. J Immunol 128: 2067–2072, 1980
Kobayashi Y, Matsushima K, Oppenheim JJ: In: R. Bomford, B. Henderson (eds). Interleukin-1, Inflammation and Disease. Elsevier, Amsterdam, 1989, pp. 47–62
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Conti, P., Bouchet, W., Feliciani, C. et al. Effect of interleukin-1 receptor antagonist (IL-1RA) on histamine and serotonin release by rat basophilic leukemia cells (RBL-2H3) and peritoneal mast cells. Mol Cell Biochem 155, 61–68 (1996). https://doi.org/10.1007/BF00714334
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00714334