Cell surface control of the multiubiquitination and deubiquitination of high-affinity immunoglobulin E receptors.
EMBO J. 1993 Feb;12(2):779–786. doi:
10.1002/j.1460-2075.1993.tb05712.x
Cell surface control of the multiubiquitination and deubiquitination of high-affinity immunoglobulin E receptors.
R Paolini
1Molecular Allergy and Immunology Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD 20852.Find articles by
1,
J P Kinet
1Molecular Allergy and Immunology Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD 20852.Find articles by
1Author information
Copyright and License information
1Molecular Allergy and Immunology Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD 20852.
PMCID: PMC413265 PMID:
Abstract
Multiubiquitination of proteins is a critical step leading to selective degradation for many polypeptides. Therefore, activation-induced multiubiquitination of cell surface receptors, such as the platelet-derived growth factor (PDGF) receptor and the T cell antigen (TCR) receptor, may correspond to a degradation pathway for ligand-receptor complexes. Here we show that the antigen-induced engagement of high-affinity immunoglobulin E receptors (Fc epsilon RI) results in the immediate multiubiquitination of Fc epsilon RI beta and gamma chains. This ubiquitination is independent of receptor phosphorylation and is restricted to activated receptors. Surprisingly, receptor multiubiquitination is immediately reversible when receptors are disengaged. Therefore, multiubiquitination and deubiquitination of Fc epsilon RI receptors is controlled at the cell surface by receptor engagement and disengagement. The rapidity, specificity and, most importantly, the reversibility of the activation-induced receptor multiubiquitination suggest that this process may turn on/off a cell surface receptor signaling function thus far unsuspected.
Full text
…
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
Adamczewski M., Paolini R., Kinet J. P. Evidence for two distinct phosphorylation pathways activated by high affinity immunoglobulin E receptors. J Biol Chem. 1992 Sep 5;267(25):18126–18132. [
] [
]
Alber G., Miller L., Jelsema C. L., Varin-Blank N., Metzger H. Structure-function relationships in the mast cell high affinity receptor for IgE. Role of the cytoplasmic domains and of the beta subunit. J Biol Chem. 1991 Nov 25;266(33):22613–22620. [
] [
]
Amigorena S., Salamero J., Davoust J., Fridman W. H., Bonnerot C. Tyrosine-containing motif that transduces cell activation signals also determines internalization and antigen presentation via type III receptors for IgG. Nature. 1992 Jul 23;358(6384):337–341. doi: 10.1038/358337a0. [
] [
] [
]
Anderson P., Caligiuri M., O'Brien C., Manley T., Ritz J., Schlossman S. F. Fc gamma receptor type III (CD16) is included in the zeta NK receptor complex expressed by human natural killer cells. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2274–2278. doi: 10.1073/pnas.87.6.2274. [
] [
] [
] [
]
Benhamou M., Gutkind J. S., Robbins K. C., Siraganian R. P. Tyrosine phosphorylation coupled to IgE receptor-mediated signal transduction and histamine release. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5327–5330. doi: 10.1073/pnas.87.14.5327. [
] [
] [
] [
]
Benhamou M., Stephan V., Robbins K. C., Siraganian R. P. High-affinity IgE receptor-mediated stimulation of rat basophilic leukemia (RBL-2H3) cells induces early and late protein-tyrosine phosphorylations. J Biol Chem. 1992 Apr 15;267(11):7310–7314. [
] [
]
Bonnerot C., Amigorena S., Choquet D., Pavlovich R., Choukroun V., Fridman W. H. Role of associated gamma-chain in tyrosine kinase activation via murine Fc gamma RIII. EMBO J. 1992 Jul;11(7):2747–2757. doi: 10.1002/j.1460-2075.1992.tb05340.x. [
] [
] [
] [
]
Boyle W. J., van der Geer P., Hunter T. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 1991;201:110–149. doi: 10.1016/0076-6879(91)01013-r. [
] [
] [
]
Cenciarelli C., Hou D., Hsu K. C., Rellahan B. L., Wiest D. L., Smith H. T., Fried V. A., Weissman A. M. Activation-induced ubiquitination of the T cell antigen receptor. Science. 1992 Aug 7;257(5071):795–797. doi: 10.1126/science.1323144. [
] [
] [
]
Chau V., Tobias J. W., Bachmair A., Marriott D., Ecker D. J., Gonda D. K., Varshavsky A. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science. 1989 Mar 24;243(4898):1576–1583. doi: 10.1126/science.2538923. [
] [
] [
]
Finley D., Chau V. Ubiquitination. Annu Rev Cell Biol. 1991;7:25–69. doi: 10.1146/annurev.cb.07.110191.000325. [
] [
] [
]
Gregori L., Poosch M. S., Cousins G., Chau V. A uniform isopeptide-linked multiubiquitin chain is sufficient to target substrate for degradation in ubiquitin-mediated proteolysis. J Biol Chem. 1990 May 25;265(15):8354–8357. [
] [
]
Hershko A., Ciechanover A. The ubiquitin system for protein degradation. Annu Rev Biochem. 1992;61:761–807. doi: 10.1146/annurev.bi.61.070192.003553. [
] [
] [
]
Hershko A., Heller H., Elias S., Ciechanover A. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J Biol Chem. 1983 Jul 10;258(13):8206–8214. [
] [
]
Hershko A. Ubiquitin-mediated protein degradation. J Biol Chem. 1988 Oct 25;263(30):15237–15240. [
] [
]
Hibbs M. L., Selvaraj P., Carpén O., Springer T. A., Kuster H., Jouvin M. H., Kinet J. P. Mechanisms for regulating expression of membrane isoforms of Fc gamma RIII (CD16). Science. 1989 Dec 22;246(4937):1608–1611. doi: 10.1126/science.2531918. [
] [
] [
]
Hsi E. D., Siegel J. N., Minami Y., Luong E. T., Klausner R. D., Samelson L. E. T cell activation induces rapid tyrosine phosphorylation of a limited number of cellular substrates. J Biol Chem. 1989 Jun 25;264(18):10836–10842. [
] [
]
Irving B. A., Weiss A. The cytoplasmic domain of the T cell receptor zeta chain is sufficient to couple to receptor-associated signal transduction pathways. Cell. 1991 Mar 8;64(5):891–901. doi: 10.1016/0092-8674(91)90314-o. [
] [
] [
]
Jentsch S. Ubiquitin-dependent protein degradation: a cellular perspective. Trends Cell Biol. 1992 Apr;2(4):98–103. doi: 10.1016/0962-8924(92)90013-d. [
] [
] [
]
June C. H., Fletcher M. C., Ledbetter J. A., Samelson L. E. Increases in tyrosine phosphorylation are detectable before phospholipase C activation after T cell receptor stimulation. J Immunol. 1990 Mar 1;144(5):1591–1599. [
] [
]
Kinet J. P. The gamma-zeta dimers of Fc receptors as connectors to signal transduction. Curr Opin Immunol. 1992 Feb;4(1):43–48. doi: 10.1016/0952-7915(92)90122-u. [
] [
] [
]
Kinet J. P. The high-affinity receptor for IgE. Curr Opin Immunol. 1989;2(4):499–505. doi: 10.1016/0952-7915(90)90002-x. [
] [
] [
]
Kong S. K., Chock P. B. Protein ubiquitination is regulated by phosphorylation. An in vitro study. J Biol Chem. 1992 Jul 15;267(20):14189–14192. [
] [
]
Lanier L. L., Yu G., Phillips J. H. Co-association of CD3 zeta with a receptor (CD16) for IgG Fc on human natural killer cells. Nature. 1989 Dec 14;342(6251):803–805. doi: 10.1038/342803a0. [
] [
] [
]
Letourneur F., Klausner R. D. Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3 epsilon. Science. 1992 Jan 3;255(5040):79–82. doi: 10.1126/science.1532456. [
] [
] [
]
Letourneur F., Klausner R. D. T-cell and basophil activation through the cytoplasmic tail of T-cell-receptor zeta family proteins. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):8905–8909. doi: 10.1073/pnas.88.20.8905. [
] [
] [
] [
]
Letourneur O., Kennedy I. C., Brini A. T., Ortaldo J. R., O'Shea J. J., Kinet J. P. Characterization of the family of dimers associated with Fc receptors (Fc epsilon RI and Fc gamma RIII). J Immunol. 1991 Oct 15;147(8):2652–2656. [
] [
]
Leung D. W., Spencer S. A., Cachianes G., Hammonds R. G., Collins C., Henzel W. J., Barnard R., Waters M. J., Wood W. I. Growth hormone receptor and serum binding protein: purification, cloning and expression. Nature. 1987 Dec 10;330(6148):537–543. doi: 10.1038/330537a0. [
] [
] [
]
Li W., Deanin G. G., Margolis B., Schlessinger J., Oliver J. M. Fc epsilon R1-mediated tyrosine phosphorylation of multiple proteins, including phospholipase C gamma 1 and the receptor beta gamma 2 complex, in RBL-2H3 rat basophilic leukemia cells. Mol Cell Biol. 1992 Jul;12(7):3176–3182. doi: 10.1128/mcb.12.7.3176-3182.1992. [
] [
] [
] [
]
Liu F. T., Bohn J. W., Ferry E. L., Yamamoto H., Molinaro C. A., Sherman L. A., Klinman N. R., Katz D. H. Monoclonal dinitrophenyl-specific murine IgE antibody: preparation, isolation, and characterization. J Immunol. 1980 Jun;124(6):2728–2737. [
] [
]
Mori S., Heldin C. H., Claesson-Welsh L. Ligand-induced polyubiquitination of the platelet-derived growth factor beta-receptor. J Biol Chem. 1992 Mar 25;267(9):6429–6434. [
] [
]
Orloff D. G., Ra C. S., Frank S. J., Klausner R. D., Kinet J. P. Family of disulphide-linked dimers containing the zeta and eta chains of the T-cell receptor and the gamma chain of Fc receptors. Nature. 1990 Sep 13;347(6289):189–191. doi: 10.1038/347189a0. [
] [
] [
]
Paolini R., Jouvin M. H., Kinet J. P. Phosphorylation and dephosphorylation of the high-affinity receptor for immunoglobulin E immediately after receptor engagement and disengagement. Nature. 1991 Oct 31;353(6347):855–858. doi: 10.1038/353855a0. [
] [
] [
]
Park D. J., Min H. K., Rhee S. G. IgE-induced tyrosine phosphorylation of phospholipase C-gamma 1 in rat basophilic leukemia cells. J Biol Chem. 1991 Dec 25;266(36):24237–24240. [
] [
]
Ra C., Jouvin M. H., Blank U., Kinet J. P. A macrophage Fc gamma receptor and the mast cell receptor for IgE share an identical subunit. Nature. 1989 Oct 26;341(6244):752–754. doi: 10.1038/341752a0. [
] [
] [
]
Ravetch J. V., Kinet J. P. Fc receptors. Annu Rev Immunol. 1991;9:457–492. doi: 10.1146/annurev.iy.09.040191.002325. [
] [
] [
]
Reth M. Antigen receptor tail clue. Nature. 1989 Mar 30;338(6214):383–384. doi: 10.1038/338383b0. [
] [
] [
]
Rivera J., Kinet J. P., Kim J., Pucillo C., Metzger H. Studies with a monoclonal antibody to the beta subunit of the receptor with high affinity for immunoglobulin E. Mol Immunol. 1988 Jul;25(7):647–661. doi: 10.1016/0161-5890(88)90100-9. [
] [
] [
]
Romeo C., Amiot M., Seed B. Sequence requirements for induction of cytolysis by the T cell antigen/Fc receptor zeta chain. Cell. 1992 Mar 6;68(5):889–897. doi: 10.1016/0092-8674(92)90032-8. [
] [
] [
]
Romeo C., Seed B. Cellular immunity to HIV activated by CD4 fused to T cell or Fc receptor polypeptides. Cell. 1991 Mar 8;64(5):1037–1046. doi: 10.1016/0092-8674(91)90327-u. [
] [
] [
]
Schneider H., Cohen-Dayag A., Pecht I. Tyrosine phosphorylation of phospholipase C gamma 1 couples the Fc epsilon receptor mediated signal to mast cells secretion. Int Immunol. 1992 Apr;4(4):447–453. doi: 10.1093/intimm/4.4.447. [
] [
] [
]
Siegelman M., Bond M. W., Gallatin W. M., St John T., Smith H. T., Fried V. A., Weissman I. L. Cell surface molecule associated with lymphocyte homing is a ubiquitinated branched-chain glycoprotein. Science. 1986 Feb 21;231(4740):823–829. doi: 10.1126/science.3003913. [
] [
] [
]
Wegener A. M., Letourneur F., Hoeveler A., Brocker T., Luton F., Malissen B. The T cell receptor/CD3 complex is composed of at least two autonomous transduction modules. Cell. 1992 Jan 10;68(1):83–95. doi: 10.1016/0092-8674(92)90208-t. [
] [
] [
]
Weissman A. M., Baniyash M., Hou D., Samelson L. E., Burgess W. H., Klausner R. D. Molecular cloning of the zeta chain of the T cell antigen receptor. Science. 1988 Feb 26;239(4843):1018–1021. doi: 10.1126/science.3278377. [
] [
] [
]
Wilkinson K. D., Lee K. M., Deshpande S., Duerksen-Hughes P., Boss J. M., Pohl J. The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science. 1989 Nov 3;246(4930):670–673. doi: 10.1126/science.2530630. [
] [
] [
]
Williams A. F., Barclay A. N. The immunoglobulin superfamily--domains for cell surface recognition. Annu Rev Immunol. 1988;6:381–405. doi: 10.1146/annurev.iy.06.040188.002121. [
] [
] [
]
Wirthmueller U., Kurosaki T., Murakami M. S., Ravetch J. V. Signal transduction by Fc gamma RIII (CD16) is mediated through the gamma chain. J Exp Med. 1992 May 1;175(5):1381–1390. doi: 10.1084/jem.175.5.1381. [
] [
] [
] [
]
Wu R. S., Kohn K. W., Bonner W. M. Metabolism of ubiquitinated histones. J Biol Chem. 1981 Jun 10;256(11):5916–5920. [
] [
]
Yarden Y., Escobedo J. A., Kuang W. J., Yang-Feng T. L., Daniel T. O., Tremble P. M., Chen E. Y., Ando M. E., Harkins R. N., Francke U. Structure of the receptor for platelet-derived growth factor helps define a family of closely related growth factor receptors. Nature. 1986 Sep 18;323(6085):226–232. doi: 10.1038/323226a0. [
] [
] [
]
———
Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group