Defective in Vitro Production of Gamma-interferon and Tumor Necrosis Factor-alpha by Circulating T Cells from Patients with the Hyper-immunoglobulin E Syndrome

Overview

Journal J Clin Invest

Specialty General Medicine

Date 1989 Dec 1

PMID 2531758

Citations 23

Authors

G Del Prete

A Tiri

E Maggi

M De Carli

D Macchia

P Parronchi

M E Rossi

M C Pietrogrande

M Ricci

S Romagnani

Affiliations

Soon will be listed here.

Abstract

Circulating T cells from four patients with the hyper-IgE syndrome were found to produce significantly lower concentrations of interferon-gamma (IFN-gamma) in response to stimulation with phytohemagglutinin (PHA) than did T cells from eight age-matched healthy controls, three patients with atopic dermatitis and one patient with chronic granulomatous disease. A clonal analysis revealed that patients with hyper-IgE syndrome had markedly lower proportions of circulating T cells able to produce IFN-gamma and tumor necrosis factor-alpha (TNF-alpha) in comparison with controls. In contrast, the proportions of peripheral blood T cells able to produce IL-4 or IL-2 were not significantly different in patients and controls. All the four patients with hyper-IgE syndrome showed high proportions of circulating CD4+ helper T cells able to induce IgE synthesis in allogeneic B cells, as well. Such an activity for IgE synthesis appeared to be positively correlated with IL-4 production by T cells and inversely related to the ability of the same T cells to produce IFN-gamma. Since IFN-gamma exerts an inhibitory effect on the synthesis of IgE and both IFN-gamma and TNF-alpha play an important role in inflammatory reactions, we suggest that the defective production of IFN-gamma may be responsible for hyperproduction of IgE and the combined defect of IFN-gamma and TNF-alpha may contribute to the undue susceptibility to infections seen in patients with hyper-IgE syndrome.

Citing Articles

Infection in Humans With STAT3-Deficiency Is Associated With Defective Interferon-Gamma and Th17 Responses.

Danion F, Aimanianda V, Bayry J, Dureault A, Wong S, Bougnoux M Front Immunol. 2020; 11:38.

PMID: 32047500 PMC: 6997434. DOI: 10.3389/fimmu.2020.00038.

Functional Defects in Type 3 Innate Lymphoid Cells and Classical Monocytes in a Patient with Hyper-IgE Syndrome.

Chang Y, Kang S, Kim J, Kang H, Kim H Immune Netw. 2017; 17(5):352-364.

PMID: 29093656 PMC: 5662784. DOI: 10.4110/in.2017.17.5.352.

Collaborative Interferon-γ and Interleukin-17 Signaling Protects the Oral Mucosa from Staphylococcus aureus.

Barin J, Talor M, Schaub J, Diny N, Hou X, Hoyer M Am J Pathol. 2016; 186(9):2337-52.

PMID: 27470712 PMC: 5012512. DOI: 10.1016/j.ajpath.2016.07.001.

Genetic origins of hyper-IgE syndrome.

Minegishi Y, Karasuyama H Curr Allergy Asthma Rep. 2008; 8(5):386-91.

PMID: 18682102 DOI: 10.1007/s11882-008-0075-x.

In vitro interleukin 4 and interferon-gamma production by mononuclear cells from atopic dermatitis patients.

Well S, Diel F Mediators Inflamm. 1993; 2(6):411-5.

PMID: 18475556 PMC: 2365435. DOI: 10.1155/S0962935193000584.

References

Djeu J, Stocks N, Zoon K, STANTON G, Timonen T, Herberman R . Positive self regulation of cytotoxicity in human natural killer cells by production of interferon upon exposure to influenza and herpes viruses. J Exp Med. 1982; 156(4):1222-34. PMC: 2186820. DOI: 10.1084/jem.156.4.1222. View

Steeg P, Moore R, Johnson H, Oppenheim J . Regulation of murine macrophage Ia antigen expression by a lymphokine with immune interferon activity. J Exp Med. 1982; 156(6):1780-93. PMC: 2186868. DOI: 10.1084/jem.156.6.1780. View

Ringden O, Persson U, JOHANSSON S, Wilczek H, Gahrton G, Groth C . Markedly elevated serum IgE levels following allogeneic and syngeneic bone marrow transplantation. Blood. 1983; 61(6):1190-5. View

Romagnani S, Del Prete G, Maggi E, Bellesi G, Biti G, Ferrini P . Abnormalities of in vitro immunoglobulin synthesis by peripheral blood lymphocytes from untreated patients with Hodgkin's disease. J Clin Invest. 1983; 71(5):1375-82. PMC: 437001. DOI: 10.1172/jci110890. View

Nathan C, Murray H, Wiebe M, Rubin B . Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med. 1983; 158(3):670-89. PMC: 2187114. DOI: 10.1084/jem.158.3.670. View

Perussia B, Dayton E, Fanning V, Thiagarajan P, HOXIE J, Trinchieri G . Immune interferon and leukocyte-conditioned medium induce normal and leukemic myeloid cells to differentiate along the monocytic pathway. J Exp Med. 1983; 158(6):2058-80. PMC: 2187172. DOI: 10.1084/jem.158.6.2058. View

Pennica D, Nedwin G, Hayflick J, Seeburg P, Derynck R, Palladino M . Human tumour necrosis factor: precursor structure, expression and homology to lymphotoxin. Nature. 1984; 312(5996):724-9. DOI: 10.1038/312724a0. View

Coffman R, Carty J . A T cell activity that enhances polyclonal IgE production and its inhibition by interferon-gamma. J Immunol. 1986; 136(3):949-54. View

Del Prete G, Maggi E, Macchia D, Tiri A, Parronchi P, Ricci M . Human T cell clones can induce in vitro IgE synthesis in normal B cells regardless of alloantigen recognition or specificity for peculiar antigens. Eur J Immunol. 1986; 16(12):1509-14. DOI: 10.1002/eji.1830161207. View

10.

Romagnani S, Del Prete G, Maggi E, Ricci M . Activation through CD3 molecule leads a number of human T cell clones to induce IgE synthesis in vitro by B cells from allergic and nonallergic individuals. J Immunol. 1987; 138(6):1744-9. View

11.

Snapper C, Paul W . Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science. 1987; 236(4804):944-7. DOI: 10.1126/science.3107127. View

12.

PARKIN J, Eales L, Galazka A, Pinching A . Atopic manifestations in the acquired immune deficiency syndrome: response to recombinant interferon gamma. Br Med J (Clin Res Ed). 1987; 294(6581):1185-6. PMC: 1246352. DOI: 10.1136/bmj.294.6581.1185. View

13.

Del Prete G, Maggi E, Parronchi P, Chretien I, Tiri A, Macchia D . IL-4 is an essential factor for the IgE synthesis induced in vitro by human T cell clones and their supernatants. J Immunol. 1988; 140(12):4193-8. View

14.

Paliard X, de Waal Malefijt R, Yssel H, Blanchard D, Chretien I, Abrams J . Simultaneous production of IL-2, IL-4, and IFN-gamma by activated human CD4+ and CD8+ T cell clones. J Immunol. 1988; 141(3):849-55. View

15.

Maggi E, Del Prete G, Macchia D, Parronchi P, Tiri A, Chretien I . Profiles of lymphokine activities and helper function for IgE in human T cell clones. Eur J Immunol. 1988; 18(7):1045-50. DOI: 10.1002/eji.1830180712. View

16.

Chretien I, van Kimmenade A, Pearce M, Banchereau J, Abrams J . Development of polyclonal and monoclonal antibodies for immunoassay and neutralization of human interleukin-4. J Immunol Methods. 1989; 117(1):67-81. DOI: 10.1016/0022-1759(89)90120-8. View

17.

Buckley R, Wray B, Belmaker E . Extreme hyperimmunoglobulinemia E and undue susceptibility to infection. Pediatrics. 1972; 49(1):59-70. View

18.

Buckley R, Fiscus S . Serum IgD and IgE concentrations in immunodeficiency diseases. J Clin Invest. 1975; 55(1):157-65. PMC: 301727. DOI: 10.1172/JCI107906. View

19.

Buckley R, Becker W . Abnormalities in the regulation of human IgE synthesis. Immunol Rev. 1978; 41:288-314. DOI: 10.1111/j.1600-065x.1978.tb01469.x. View

20.

Taswell C . Limiting dilution assays for the determination of immunocompetent cell frequencies. I. Data analysis. J Immunol. 1981; 126(4):1614-9. View