Skip to main content
Immunology logoLink to Immunology
. 1996 Dec;89(4):547–552. doi: 10.1046/j.1365-2567.1996.d01-768.x

Interferon-gamma promotes the survival and Fc epsilon RI-mediated histamine release in cultured human mast cells.

M Yanagida 1, H Fukamachi 1, M Takei 1, T Hagiwara 1, H Uzumaki 1, T Tokiwa 1, H Saito 1, Y Iikura 1, T Nakahata 1
PMCID: PMC1456572  PMID: 9014819

Abstract

We examined the effects of interferon-gamma (IFN-gamma) on 100% pure human mast cells generated in suspension cultures of umbilical cord blood mononuclear cells in the presence of stem cell factor (SCF) and interleukin-6 (IL-6). When mast cells were suspended in serum-free medium without any cytokine after the withdrawal of SCF and IL-6, they died over a period of 5 days because of apoptosis. IFN-gamma in the cultures suppressed apoptosis and prolonged their survival in a dose-dependent manner. This survival-promoting effect of IFN-gamma was blocked by neutralizing antibodies to IFN-gamma or to IFN-gamma receptor (IFN-gamma R). When mast cells were incubated with IFN-gamma in serum-free medium for more than 4 hr during sensitization, immunoglobulin E (IgE)/anti-IgE antibody-induced histamine release was effectively enhanced. Polymerase chain reaction (PCR) amplification of the alpha-chain of IFN-gamma R (IFN-gamma R alpha) yielded products of the correct size predicted from the sequence of the receptor. In addition, flow cytometry using anti-IFN-gamma R monoclonal antibodies (mAbs) indicated that these mast cells bear IFN-gamma R on their surface. These findings suggested that IFN-gamma activates human mast cells via specific receptors in certain aspects of inflammatory reactions.

Full text

PDF
550

Images in this article

Selected References

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

  1. Bischoff S. C., Dahinden C. A. c-kit ligand: a unique potentiator of mediator release by human lung mast cells. J Exp Med. 1992 Jan 1;175(1):237–244. doi: 10.1084/jem.175.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bradding P., Feather I. H., Howarth P. H., Mueller R., Roberts J. A., Britten K., Bews J. P., Hunt T. C., Okayama Y., Heusser C. H. Interleukin 4 is localized to and released by human mast cells. J Exp Med. 1992 Nov 1;176(5):1381–1386. doi: 10.1084/jem.176.5.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bradding P., Feather I. H., Wilson S., Bardin P. G., Heusser C. H., Holgate S. T., Howarth P. H. Immunolocalization of cytokines in the nasal mucosa of normal and perennial rhinitic subjects. The mast cell as a source of IL-4, IL-5, and IL-6 in human allergic mucosal inflammation. J Immunol. 1993 Oct 1;151(7):3853–3865. [PubMed] [Google Scholar]
  4. Burd P. R., Rogers H. W., Gordon J. R., Martin C. A., Jayaraman S., Wilson S. D., Dvorak A. M., Galli S. J., Dorf M. E. Interleukin 3-dependent and -independent mast cells stimulated with IgE and antigen express multiple cytokines. J Exp Med. 1989 Jul 1;170(1):245–257. doi: 10.1084/jem.170.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coffman R. L., Carty J. A T cell activity that enhances polyclonal IgE production and its inhibition by interferon-gamma. J Immunol. 1986 Feb 1;136(3):949–954. [PubMed] [Google Scholar]
  6. Coleman J. W., Buckley M. G., Holliday M. R., Morris A. G. Interferon-gamma inhibits serotonin release from mouse peritoneal mast cells. Eur J Immunol. 1991 Oct;21(10):2559–2564. doi: 10.1002/eji.1830211037. [DOI] [PubMed] [Google Scholar]
  7. Columbo M., Horowitz E. M., Botana L. M., MacGlashan D. W., Jr, Bochner B. S., Gillis S., Zsebo K. M., Galli S. J., Lichtenstein L. M. The human recombinant c-kit receptor ligand, rhSCF, induces mediator release from human cutaneous mast cells and enhances IgE-dependent mediator release from both skin mast cells and peripheral blood basophils. J Immunol. 1992 Jul 15;149(2):599–608. [PubMed] [Google Scholar]
  8. Coussens L., Van Beveren C., Smith D., Chen E., Mitchell R. L., Isacke C. M., Verma I. M., Ullrich A. Structural alteration of viral homologue of receptor proto-oncogene fms at carboxyl terminus. Nature. 1986 Mar 20;320(6059):277–280. doi: 10.1038/320277a0. [DOI] [PubMed] [Google Scholar]
  9. Fierlbeck G., Rassner G., Müller C. Psoriasis induced at the injection site of recombinant interferon gamma. Results of immunohistologic investigations. Arch Dermatol. 1990 Mar;126(3):351–355. [PubMed] [Google Scholar]
  10. Grewe M., Gyufko K., Schöpf E., Krutmann J. Lesional expression of interferon-gamma in atopic eczema. Lancet. 1994 Jan 1;343(8888):25–26. doi: 10.1016/s0140-6736(94)90879-6. [DOI] [PubMed] [Google Scholar]
  11. Harvima I. T., Naukkarinen A., Harvima R. J., Aalto M. L., Neittaanmäki H., Horsmanheimo M. Quantitative enzyme-histochemical analysis of tryptase- and chymase-containing mast cells in psoriatic skin. Arch Dermatol Res. 1990;282(7):428–433. doi: 10.1007/BF00402617. [DOI] [PubMed] [Google Scholar]
  12. Hernandez-Asensio M., Hooks J. J., Ida S., Siraganian R. P., Notkins A. L. Interferon-induced enhancement of IgE-mediated histamine release from human basophils requires RNA synthesis. J Immunol. 1979 Apr;122(4):1601–1603. [PubMed] [Google Scholar]
  13. Ida S., Hooks J. J., Siraganian R. P., Notkins A. L. Enhancement of IgE-mediated histamine release from human basophils by viruses: role of interferon. J Exp Med. 1977 Apr 1;145(4):892–906. doi: 10.1084/jem.145.4.892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Igarashi Y., Kurosawa M., Ishikawa O., Miyachi Y., Saito H., Ebisawa M., Iikura Y., Yanagida M., Uzumaki H., Nakahata T. Characteristics of histamine release from cultured human mast cells. Clin Exp Allergy. 1996 May;26(5):597–602. [PubMed] [Google Scholar]
  15. Irani A. A., Schechter N. M., Craig S. S., DeBlois G., Schwartz L. B. Two types of human mast cells that have distinct neutral protease compositions. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4464–4468. doi: 10.1073/pnas.83.12.4464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ishizaka T., Ishizaka K. Activation of mast cells for mediator release through IgE receptors. Prog Allergy. 1984;34:188–235. [PubMed] [Google Scholar]
  17. Kataoka S., Naito M., Fujita N., Ishii H., Ishii S., Yamori T., Nakajima M., Tsuruo T. Control of apoptosis and growth of malignant T lymphoma cells by lymph node stromal cells. Exp Cell Res. 1993 Aug;207(2):271–276. doi: 10.1006/excr.1993.1193. [DOI] [PubMed] [Google Scholar]
  18. Mosmann T. R., Cherwinski H., Bond M. W., Giedlin M. A., Coffman R. L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol. 1986 Apr 1;136(7):2348–2357. [PubMed] [Google Scholar]
  19. Mosmann T. R., Coffman R. L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol. 1989;7:145–173. doi: 10.1146/annurev.iy.07.040189.001045. [DOI] [PubMed] [Google Scholar]
  20. Naukkarinen A., Harvima I. T., Aalto M. L., Horsmanheimo M. Mast cell tryptase and chymase are potential regulators of neurogenic inflammation in psoriatic skin. Int J Dermatol. 1994 May;33(5):361–366. doi: 10.1111/j.1365-4362.1994.tb01069.x. [DOI] [PubMed] [Google Scholar]
  21. Okayama Y., Petit-Frére C., Kassel O., Semper A., Quint D., Tunon-de-Lara M. J., Bradding P., Holgate S. T., Church M. K. IgE-dependent expression of mRNA for IL-4 and IL-5 in human lung mast cells. J Immunol. 1995 Aug 15;155(4):1796–1808. [PubMed] [Google Scholar]
  22. Plaut M., Pierce J. H., Watson C. J., Hanley-Hyde J., Nordan R. P., Paul W. E. Mast cell lines produce lymphokines in response to cross-linkage of Fc epsilon RI or to calcium ionophores. Nature. 1989 May 4;339(6219):64–67. doi: 10.1038/339064a0. [DOI] [PubMed] [Google Scholar]
  23. Pène J., Rousset F., Brière F., Chrétien I., Bonnefoy J. Y., Spits H., Yokota T., Arai N., Arai K., Banchereau J. IgE production by normal human lymphocytes is induced by interleukin 4 and suppressed by interferons gamma and alpha and prostaglandin E2. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6880–6884. doi: 10.1073/pnas.85.18.6880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Saito H., Ebisawa M., Sakaguchi N., Onda T., Iikura Y., Yanagida M., Uzumaki H., Nakahata T. Characterization of cord-blood-derived human mast cells cultured in the presence of Steel factor and interleukin-6. Int Arch Allergy Immunol. 1995 May-Jun;107(1-3):63–65. doi: 10.1159/000236932. [DOI] [PubMed] [Google Scholar]
  25. Saito H., Ebisawa M., Tachimoto H., Shichijo M., Fukagawa K., Matsumoto K., Iikura Y., Awaji T., Tsujimoto G., Yanagida M. Selective growth of human mast cells induced by Steel factor, IL-6, and prostaglandin E2 from cord blood mononuclear cells. J Immunol. 1996 Jul 1;157(1):343–350. [PubMed] [Google Scholar]
  26. Saito H., Hayakawa T., Mita H., Yui Y. S., Shida T. Augmentation of leukotriene C4 production by gamma interferon in leukocytes challenged with an allergen. Int Arch Allergy Appl Immunol. 1988;87(3):286–293. doi: 10.1159/000234687. [DOI] [PubMed] [Google Scholar]
  27. Siraganian R. P. An automated continuous-flow system for the extraction and fluorometric analysis of histamine. Anal Biochem. 1974 Feb;57(2):383–394. doi: 10.1016/0003-2697(74)90093-1. [DOI] [PubMed] [Google Scholar]
  28. Takagi M., Koike K., Nakahata T. Antiproliferative effect of IFN-gamma on proliferation of mouse connective tissue-type mast cells. J Immunol. 1990 Sep 15;145(6):1880–1884. [PubMed] [Google Scholar]
  29. Uyemura K., Yamamura M., Fivenson D. F., Modlin R. L., Nickoloff B. J. The cytokine network in lesional and lesion-free psoriatic skin is characterized by a T-helper type 1 cell-mediated response. J Invest Dermatol. 1993 Nov;101(5):701–705. doi: 10.1111/1523-1747.ep12371679. [DOI] [PubMed] [Google Scholar]
  30. Valerius T., Repp R., Kalden J. R., Platzer E. Effects of IFN on human eosinophils in comparison with other cytokines. A novel class of eosinophil activators with delayed onset of action. J Immunol. 1990 Nov 1;145(9):2950–2958. [PubMed] [Google Scholar]
  31. Wodnar-Filipowicz A., Heusser C. H., Moroni C. Production of the haemopoietic growth factors GM-CSF and interleukin-3 by mast cells in response to IgE receptor-mediated activation. Nature. 1989 May 11;339(6220):150–152. doi: 10.1038/339150a0. [DOI] [PubMed] [Google Scholar]
  32. Yanagida M., Fukamachi H., Ohgami K., Kuwaki T., Ishii H., Uzumaki H., Amano K., Tokiwa T., Mitsui H., Saito H. Effects of T-helper 2-type cytokines, interleukin-3 (IL-3), IL-4, IL-5, and IL-6 on the survival of cultured human mast cells. Blood. 1995 Nov 15;86(10):3705–3714. [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES