Granulocyte-macrophage Colony-stimulating Factor Antagonizes the Transforming Growth Factor-beta-induced Expression of Fc Gamma RIII (CD16) on Human Monocytes

Overview

Journal Immunology

Specialty Allergy & Immunology

Date 1996 Jan 1

PMID 8666430

Citations 7

Authors

M Kruger

L Coorevits

T P De Wit

M Casteels-Van Daele

J G van de Winkel

J L Ceuppens

Affiliations

Soon will be listed here.

Abstract

Fc-gamma receptor III (Fc gamma RIII, CD16) type A is expressed on natural killer cells, on a small subset of peripheral blood monocytes and on mature macrophages. Along with differentiation into macrophages, monocytes will express Fc gamma RIII when cultured with transforming growth factor-beta (TGF-beta). In view of the involvement of granulocyte-macrophage colony-stimulating factor (GM-CSF) in myeloid cell differentiation, we investigated the effect of this cytokine on Fc gamma RIII expression in cultures of peripheral blood monocytes. GM-CSF antagonized TGF-beta-induced expression of Fc gamma RIII on monocytes in vitro in a dose-dependent way. The effect of GM-CSF persisted in cultures until at least day 7. The suppression was at the mRNA level, as shown by Northern analyses with a CD16 specific probe, and the signalling pathway involved tyrosine kinase activity. Interferon-gamma and interleukin-2 had no effect on the induced expression of Fc gamma RIII by TGF-beta, while interleukin-4, similar to GM-CSF, antagonized this induction. Our findings suggest that regulatory cytokine networks can drive monocytes into different effector functions and differentiation pathways.

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References

Perussia B, Trinchieri G . Antibody 3G8, specific for the human neutrophil Fc receptor, reacts with natural killer cells. J Immunol. 1984; 132(3):1410-5. View

de Waal Malefyt R, Figdor C, Huijbens R, Bennett B, Culpepper J, Dang W . Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes. Comparison with IL-4 and modulation by IFN-gamma or IL-10. J Immunol. 1993; 151(11):6370-81. View

Clarkson S, Kimberly R, Valinsky J, Witmer M, Bussel J, Nachman R . Blockade of clearance of immune complexes by an anti-Fc gamma receptor monoclonal antibody. J Exp Med. 1986; 164(2):474-89. PMC: 2188226. DOI: 10.1084/jem.164.2.474. View

Munker R, Gasson J, Ogawa M, Koeffler H . Recombinant human TNF induces production of granulocyte-monocyte colony-stimulating factor. Nature. 1986; 323(6083):79-82. DOI: 10.1038/323079a0. View

Broudy V, Kaushansky K, Harlan J, Adamson J . Interleukin 1 stimulates human endothelial cells to produce granulocyte-macrophage colony-stimulating factor and granulocyte colony-stimulating factor. J Immunol. 1987; 139(2):464-8. View

Clarkson S, Ory P . CD16. Developmentally regulated IgG Fc receptors on cultured human monocytes. J Exp Med. 1988; 167(2):408-20. PMC: 2188855. DOI: 10.1084/jem.167.2.408. View

Czarniecki C, Chiu H, Wong G, McCabe S, Palladino M . Transforming growth factor-beta 1 modulates the expression of class II histocompatibility antigens on human cells. J Immunol. 1988; 140(12):4217-23. View

FISCHER H, Frosch S, Reske K, Reske-Kunz A . Granulocyte-macrophage colony-stimulating factor activates macrophages derived from bone marrow cultures to synthesis of MHC class II molecules and to augmented antigen presentation function. J Immunol. 1988; 141(11):3882-8. View

Thompson C, LINDSTEN T, Ledbetter J, Kunkel S, Young H, Emerson S . CD28 activation pathway regulates the production of multiple T-cell-derived lymphokines/cytokines. Proc Natl Acad Sci U S A. 1989; 86(4):1333-7. PMC: 286684. DOI: 10.1073/pnas.86.4.1333. View

10.

Wodnar-Filipowicz A, Heusser C, 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; 339(6220):150-2. DOI: 10.1038/339150a0. View

11.

Ravetch J, Perussia B . Alternative membrane forms of Fc gamma RIII(CD16) on human natural killer cells and neutrophils. Cell type-specific expression of two genes that differ in single nucleotide substitutions. J Exp Med. 1989; 170(2):481-97. PMC: 2189395. DOI: 10.1084/jem.170.2.481. View

12.

Passlick B, Flieger D . Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood. 1989; 74(7):2527-34. View

13.

Anderson C, Shen L, Eicher D, Wewers M, Gill J . Phagocytosis mediated by three distinct Fc gamma receptor classes on human leukocytes. J Exp Med. 1990; 171(4):1333-45. PMC: 2187839. DOI: 10.1084/jem.171.4.1333. View

14.

Welch G, Wong H, Wahl S . Selective induction of Fc gamma RIII on human monocytes by transforming growth factor-beta. J Immunol. 1990; 144(9):3444-8. View

15.

Smith P, Lamerson C, Wong H, Wahl L, Wahl S . Granulocyte-macrophage colony-stimulating factor stimulates human monocyte accessory cell function. J Immunol. 1990; 144(10):3829-34. View

16.

Young D, Lowe L, Clark S . Comparison of the effects of IL-3, granulocyte-macrophage colony-stimulating factor, and macrophage colony-stimulating factor in supporting monocyte differentiation in culture. Analysis of macrophage antibody-dependent cellular cytotoxicity. J Immunol. 1990; 145(2):607-15. View

17.

Connor R, Shen L, Fanger M . Evaluation of the antibody-dependent cytotoxic capabilities of individual human monocytes. Role of Fc gamma RI and Fc gamma RII and the effects of cytokines at the single cell level. J Immunol. 1990; 145(5):1483-9. View

18.

TREZZINI C, Jungi T, Spycher M, Maly F, Rao P . Human monocytes CD36 and CD16 are signaling molecules. Evidence from studies using antibody-induced chemiluminescence as a tool to probe signal transduction. Immunology. 1990; 71(1):29-37. PMC: 1384217. View

19.

Gasson J . Molecular physiology of granulocyte-macrophage colony-stimulating factor. Blood. 1991; 77(6):1131-45. View

20.

Nelson B, Ralph P, Green S, Nacy C . Differential susceptibility of activated macrophage cytotoxic effector reactions to the suppressive effects of transforming growth factor-beta 1. J Immunol. 1991; 146(6):1849-57. View