Differential mast cell outcomes are sensitive to FcεRI-Syk binding kinetics
Abstract
Cross-linking of immunoglobulin E–bound FcεRI triggers multiple cellular responses, including degranulation and cytokine production. Signaling is dependent on recruitment of Syk via docking of its dual SH2 domains to phosphorylated tyrosines within the FcεRI immunoreceptor tyrosine-based activation motifs. Using single-molecule imaging in live cells, we directly visualized and quantified the binding of individual mNeonGreen-tagged Syk molecules as they associated with the plasma membrane after FcεRI activation. We found that Syk colocalizes transiently to FcεRI and that Syk-FcεRI binding dynamics are independent of receptor aggregate size. Substitution of glutamic acid for tyrosine between the Syk SH2 domains (Syk-Y130E) led to an increased Syk-FcεRI off-rate, loss of site-specific Syk autophosphorylation, and impaired downstream signaling. Genome edited cells expressing only Syk-Y130E were deficient in antigen-stimulated calcium release, degranulation, and production of some cytokines (TNF-a, IL-3) but not others (MCP-1, IL-4). We propose that kinetic discrimination along the FcεRI signaling pathway occurs at the level of Syk-FcεRI interactions, with key outcomes dependent upon sufficiently long-lived Syk binding events.
- Authors:
-
- Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Pathology; Univ. of New Mexico, Albuquerque, NM (United States). Comprehensive Cancer Center
- Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Physics
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Division. Theoretical Biology and Biophysics Group
- Publication Date:
- Research Org.:
- Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1625243
- Grant/Contract Number:
- AC52-06NA25396
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Biology of the Cell
- Additional Journal Information:
- Journal Volume: 28; Journal Issue: 23; Journal ID: ISSN 1059-1524
- Publisher:
- American Society for Cell Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Cell Biology
Citation Formats
Schwartz, Samantha L., Cleyrat, Cédric, Olah, Mark J., Relich, Peter K., Phillips, Genevieve K., Hlavacek, William S., Lidke, Keith A., Wilson, Bridget S., and Lidke, Diane S. Differential mast cell outcomes are sensitive to FcεRI-Syk binding kinetics. United States: N. p., 2017.
Web. doi:10.1091/mbc.e17-06-0350.
Schwartz, Samantha L., Cleyrat, Cédric, Olah, Mark J., Relich, Peter K., Phillips, Genevieve K., Hlavacek, William S., Lidke, Keith A., Wilson, Bridget S., & Lidke, Diane S. Differential mast cell outcomes are sensitive to FcεRI-Syk binding kinetics. United States. https://doi.org/10.1091/mbc.e17-06-0350
Schwartz, Samantha L., Cleyrat, Cédric, Olah, Mark J., Relich, Peter K., Phillips, Genevieve K., Hlavacek, William S., Lidke, Keith A., Wilson, Bridget S., and Lidke, Diane S. Wed .
"Differential mast cell outcomes are sensitive to FcεRI-Syk binding kinetics". United States. https://doi.org/10.1091/mbc.e17-06-0350. https://www.osti.gov/servlets/purl/1625243.
@article{osti_1625243,
title = {Differential mast cell outcomes are sensitive to FcεRI-Syk binding kinetics},
author = {Schwartz, Samantha L. and Cleyrat, Cédric and Olah, Mark J. and Relich, Peter K. and Phillips, Genevieve K. and Hlavacek, William S. and Lidke, Keith A. and Wilson, Bridget S. and Lidke, Diane S.},
abstractNote = {Cross-linking of immunoglobulin E–bound FcεRI triggers multiple cellular responses, including degranulation and cytokine production. Signaling is dependent on recruitment of Syk via docking of its dual SH2 domains to phosphorylated tyrosines within the FcεRI immunoreceptor tyrosine-based activation motifs. Using single-molecule imaging in live cells, we directly visualized and quantified the binding of individual mNeonGreen-tagged Syk molecules as they associated with the plasma membrane after FcεRI activation. We found that Syk colocalizes transiently to FcεRI and that Syk-FcεRI binding dynamics are independent of receptor aggregate size. Substitution of glutamic acid for tyrosine between the Syk SH2 domains (Syk-Y130E) led to an increased Syk-FcεRI off-rate, loss of site-specific Syk autophosphorylation, and impaired downstream signaling. Genome edited cells expressing only Syk-Y130E were deficient in antigen-stimulated calcium release, degranulation, and production of some cytokines (TNF-a, IL-3) but not others (MCP-1, IL-4). We propose that kinetic discrimination along the FcεRI signaling pathway occurs at the level of Syk-FcεRI interactions, with key outcomes dependent upon sufficiently long-lived Syk binding events.},
doi = {10.1091/mbc.e17-06-0350},
journal = {Molecular Biology of the Cell},
number = 23,
volume = 28,
place = {United States},
year = {Wed Aug 30 00:00:00 EDT 2017},
month = {Wed Aug 30 00:00:00 EDT 2017}
}
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Kinetic proofreading in T-cell receptor signal transduction.
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Syk Is Activated by Phosphotyrosine-containing Peptides Representing the Tyrosine-based Activation Motifs of the High Affinity Receptor for IgE
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Observing Fcεri Signaling from the Inside of the Mast Cell Membrane
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