Physical Association Between the High-affinity IgG Receptor (Fc Gamma RI) and the Gamma Subunit of the High-affinity IgE Receptor (Fc Epsilon RI Gamma)

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1993 Oct 1

PMID 8415618

Citations 21

Authors

P R Scholl

R S Geha

Affiliations

Soon will be listed here.

Abstract

To investigate the structural basis of transmembrane signaling via the high-affinity IgG receptor (Fc gamma RI), the identity of Fc gamma RI-associated proteins in THP-1 human monocytic cells was examined. Anti-Fc gamma RI monoclonal antibody (mAb) 197 immunoprecipitates from 125I-labeled THP-1 cells solubilized in 1% digitonin buffer were found to contain a protein migrating at 12 kDa on reduction. This protein comigrated with the 12-kDa protein precipitated by the anti-high-affinity IgE receptor gamma chain (Fc epsilon RI gamma) mAb 4D8. Similarly, a 70-kDa band immunoprecipitated by mAb 4D8 comigrated with the 70-kDa protein band corresponding to Fc gamma RI in mAb 197 immunoprecipitates. On two-dimensional nonreducing-reducing gel analysis, the 12-kDa protein present in both mAb 197 and mAb 4D8 immunoprecipitates migrated as a disulfide-linked homodimer. Analysis of 1% Nonidet P-40 eluates of the digitonin immunoprecipitates under reducing conditions demonstrated the presence of a 12-kDa band in the mAb 197 immunoprecipitate that could be reprecipitated with mAb 4D8. Conversely, a 70-kDa band in the mAb 4D8 immunoprecipitate could be reprecipitated with mAb 197. Similar to these findings, both mAb 197 and mAb 4D8 precipitated a 12-kDa disulfide-linked homodimeric protein from digitonin lysates of 125I-labeled human neutrophils after induction of Fc gamma RI expression with interferon gamma but not from unstimulated neutrophils. Northern blot analysis confirmed the presence of Fc epsilon RI gamma mRNA in interferon gamma-induced human neutrophils. We conclude that Fc epsilon RI gamma, a member of a family of proteins implicated in transmembrane signaling via immune recognition receptors, associates with Fc gamma RI in human cells.

Citing Articles

A Molecular Signature in Blood Reveals a Role for p53 in Regulating Malaria-Induced Inflammation.

Tran T, Guha R, Portugal S, Skinner J, Ongoiba A, Bhardwaj J Immunity. 2019; 51(4):750-765.e10.

PMID: 31492649 PMC: 7163400. DOI: 10.1016/j.immuni.2019.08.009.

Mind the Gap: How Interspecies Variability in IgG and Its Receptors May Complicate Comparisons of Human and Non-human Primate Effector Function.

Crowley A, Ackerman M Front Immunol. 2019; 10:697.

PMID: 31024542 PMC: 6463756. DOI: 10.3389/fimmu.2019.00697.

Vectors for Expression of Signal Peptide-Dependent Proteins in Baculovirus/Insect Cell Systems and Their Application to Expression and Purification of the High-Affinity Immunoglobulin Gamma Fc Receptor I in Complex with Its Gamma Chain.

Le L, Nyengaard J, Golas M, Sander B Mol Biotechnol. 2017; 60(1):31-40.

PMID: 29143175 DOI: 10.1007/s12033-017-0041-8.

DC subset-specific induction of T cell responses upon antigen uptake via Fcγ receptors in vivo.

Lehmann C, Baranska A, Heidkamp G, Heger L, Neubert K, Luhr J J Exp Med. 2017; 214(5):1509-1528.

PMID: 28389502 PMC: 5413326. DOI: 10.1084/jem.20160951.

An fc gamma receptor-mediated upregulation of the production of interleukin 10 by intravenous immunoglobulin in bone-marrow-derived mouse dendritic cells stimulated with lipopolysaccharide in vitro.

Fujii A, Kase Y, Suzuki C, Kamizono A, Imada T J Signal Transduct. 2013; 2013:239320.

PMID: 23853721 PMC: 3703884. DOI: 10.1155/2013/239320.

References

Vivier E, Rochet N, Kochan J, Presky D, Schlossman S, Anderson P . Structural similarity between Fc receptors and T cell receptors. Expression of the gamma-subunit of Fc epsilon RI in human T cells, natural killer cells and thymocytes. J Immunol. 1991; 147(12):4263-70. View

Indik Z, Kelly C, Chien P, Levinson A, Schreiber A . Human Fc gamma RII, in the absence of other Fc gamma receptors, mediates a phagocytic signal. J Clin Invest. 1991; 88(5):1766-71. PMC: 295724. DOI: 10.1172/JCI115496. View

Kurosaki T, Gander I, Wirthmueller U, Ravetch J . The beta subunit of the Fc epsilon RI is associated with the Fc gamma RIII on mast cells. J Exp Med. 1992; 175(2):447-51. PMC: 2119115. DOI: 10.1084/jem.175.2.447. View

Schoneich J, Wilkinson V, Presky D, Kochan J . Association of the human Fc epsilon RI gamma subunit with novel cell surface polypeptides. J Immunol. 1992; 148(7):2181-5. View

Scholl P, Trede N, Chatila T, Geha R . Role of protein tyrosine phosphorylation in monokine induction by the staphylococcal superantigen toxic shock syndrome toxin-1. J Immunol. 1992; 148(7):2237-41. View

Romeo C, Amiot M, Seed B . Sequence requirements for induction of cytolysis by the T cell antigen/Fc receptor zeta chain. Cell. 1992; 68(5):889-97. DOI: 10.1016/0092-8674(92)90032-8. View

Liao F, Shin H, Rhee S . Tyrosine phosphorylation of phospholipase C-gamma 1 induced by cross-linking of the high-affinity or low-affinity Fc receptor for IgG in U937 cells. Proc Natl Acad Sci U S A. 1992; 89(8):3659-63. PMC: 48928. DOI: 10.1073/pnas.89.8.3659. View

Neuman E, Huleatt J, Vargas H, Rupp E, Jack R . Regulation of MHC class I synthesis and expression by human neutrophils. J Immunol. 1992; 148(11):3520-7. View

Kinet J . The gamma-zeta dimers of Fc receptors as connectors to signal transduction. Curr Opin Immunol. 1992; 4(1):43-8. DOI: 10.1016/0952-7915(92)90122-u. View

10.

Oettgen H, Pettey C, Maloy W, Terhorst C . A T3-like protein complex associated with the antigen receptor on murine T cells. Nature. 1986; 320(6059):272-5. DOI: 10.1038/320272a0. View

11.

Thompson J, Lau A, Cunningham D . Selective radiolabeling of cell surface proteins to a high specific activity. Biochemistry. 1987; 26(3):743-50. DOI: 10.1021/bi00377a014. View

12.

Kuster H, Zhang L, Brini A, MacGlashan D, Kinet J . The gene and cDNA for the human high affinity immunoglobulin E receptor beta chain and expression of the complete human receptor. J Biol Chem. 1992; 267(18):12782-7. View

13.

Scholl P, Ahern D, Geha R . Protein tyrosine phosphorylation induced via the IgG receptors Fc gamma Ri and Fc gamma RII in the human monocytic cell line THP-1. J Immunol. 1992; 149(5):1751-7. View

14.

Ernst L, Duchemin A, Anderson C . Association of the high-affinity receptor for IgG (Fc gamma RI) with the gamma subunit of the IgE receptor. Proc Natl Acad Sci U S A. 1993; 90(13):6023-7. PMC: 46859. DOI: 10.1073/pnas.90.13.6023. View

15.

Blank U, Ra C, Miller L, White K, Metzger H, Kinet J . Complete structure and expression in transfected cells of high affinity IgE receptor. Nature. 1989; 337(6203):187-9. DOI: 10.1038/337187a0. View

16.

Reth M . Antigen receptor tail clue. Nature. 1989; 338(6214):383-4. DOI: 10.1038/338383b0. View

17.

Scholl P, Diez A, Mourad W, Parsonnet J, Geha R, Chatila T . Toxic shock syndrome toxin 1 binds to major histocompatibility complex class II molecules. Proc Natl Acad Sci U S A. 1989; 86(11):4210-4. PMC: 287420. DOI: 10.1073/pnas.86.11.4210. View

18.

Ra C, Jouvin M, Blank U, Kinet J . A macrophage Fc gamma receptor and the mast cell receptor for IgE share an identical subunit. Nature. 1989; 341(6244):752-4. DOI: 10.1038/341752a0. View

19.

Kuster H, Thompson H, Kinet J . Characterization and expression of the gene for the human Fc receptor gamma subunit. Definition of a new gene family. J Biol Chem. 1990; 265(11):6448-52. View

20.

Thompson H, Metcalfe D, Kinet J . Early expression of high-affinity receptor for immunoglobulin E (Fc epsilon RI) during differentiation of mouse mast cells and human basophils. J Clin Invest. 1990; 85(4):1227-33. PMC: 296556. DOI: 10.1172/JCI114557. View