Timescale Separation of Positive and Negative Signaling Creates History-Dependent Responses to IgE Receptor Stimulation

Harmon, Brooke; Chylek, Lily A.; Liu, Yanli; Mitra, Eshan D.; Mahajan, Avanika; Saada, Edwin A.; Schudel, Benjamin R.; Holowka, David A.; Baird, Barbara A.; Wilson, Bridget S.; Hlavacek, William S.; Singh, Anup K.

doi:10.1038/s41598-017-15568-2

Title: Timescale Separation of Positive and Negative Signaling Creates History-Dependent Responses to IgE Receptor Stimulation

Journal Article · Tue Nov 14 00:00:00 EST 2017 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-017-15568-2· OSTI ID:1457302

Harmon, Brooke ^[1]; Chylek, Lily A. ^[2]; Liu, Yanli ^[3]; Mitra, Eshan D. ^[4]; Mahajan, Avanika ^[5]; Saada, Edwin A. ^[1]; Schudel, Benjamin R. ^[3]; Holowka, David A. ^[2]; Baird, Barbara A. ^[2]; Wilson, Bridget S. ^[5];

^[4]; Singh, Anup K. ^[6]

Sandia National Lab. (SNL-CA), Livermore, CA (United States). Dept. of Systems Biology. Biological and Material Sciences
Cornell Univ., Ithaca, NY (United States). Dept. of Chemistry and Chemical Biology
Sandia National Lab. (SNL-CA), Livermore, CA (United States). Dept. of Biotechnology and Bioengineering. Biological and Material Sciences
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Univ. of New Mexico, Albuquerque, NM (United States). School of Medicine. Dept. of Pathology
Sandia National Lab. (SNL-CA), Livermore, CA (United States). Biological and Material Sciences

Abstract not provided.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States); Cornell Univ., Ithaca, NY (United States); Univ. of New Mexico, Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE National Nuclear Security Administration (NNSA); National Inst. of Health (NIH) (United States); National Institutes of Health (NIH)

Grant/Contract Number:: AC52-06NA25396; NA0003525; R01DE020891; R01GM111510; P50GM085273; AC04-94AL85000

OSTI ID:: 1457302

Alternate ID(s):: OSTI ID: 1481886

Report Number(s):: LA-UR-15-28484; SAND-2018-11800J

Journal Information:: Scientific Reports, Vol. 7; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 9 works

Citation information provided by
Web of Science

References (41)

p66Shc Is a Negative Regulator of FcεRI-Dependent Signaling in Mast Cells Ulivieri, Cristina; Fanigliulo, Daniela; Masi, Giulia The Journal of Immunology, Vol. 186, Issue 9 https://doi.org/10.4049/jimmunol.1001391	journal	March 2011
Desensitization of mast cells’ secretory response to an immuno-receptor stimulus Barbu, Alina E.; Pecht, Israel Immunology Letters, Vol. 100, Issue 1 https://doi.org/10.1016/j.imlet.2005.06.009	journal	August 2005
Modeling for (physical) biologists: an introduction to the rule-based approach Chylek, Lily A.; Harris, Leonard A.; Faeder, James R. Physical Biology, Vol. 12, Issue 4 https://doi.org/10.1088/1478-3975/12/4/045007	journal	July 2015
Subthreshold and Suboptimal Desensitization of Human Basophils Mendoza, Guillermo R.; Minagawa, Kiminobu International Archives of Allergy and Immunology, Vol. 69, Issue 3 https://doi.org/10.1159/000233185	journal	January 1982
Optimizing ring assembly reveals the strength of weak interactions Deeds, E. J.; Bachman, J. A.; Fontana, W. Proceedings of the National Academy of Sciences, Vol. 109, Issue 7 https://doi.org/10.1073/pnas.1113095109	journal	January 2012
Phosphoinositide lipid phosphatase SHIP1 and PTEN coordinate to regulate cell migration and adhesion Mondal, Subhanjan; Subramanian, Kulandayan K.; Sakai, Jiro Molecular Biology of the Cell, Vol. 23, Issue 7 https://doi.org/10.1091/mbc.E11-10-0889	journal	April 2012
NF-κB signalling and cell fate decisions in response to a short pulse of tumour necrosis factor Lee, Robin E. C.; Qasaimeh, Mohammad A.; Xia, Xianfang Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep39519	journal	December 2016
Syk and pTyr'd: Signaling through the B cell antigen receptor Geahlen, Robert L. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1793, Issue 7 https://doi.org/10.1016/j.bbamcr.2009.03.004	journal	July 2009
New developments in FcεRI regulation, function and inhibition Kraft, Stefan; Kinet, Jean-Pierre Nature Reviews Immunology, Vol. 7, Issue 5 https://doi.org/10.1038/nri2072	journal	May 2007
SUNDIALS: Suite of nonlinear and differential/algebraic equation solvers Hindmarsh, Alan C.; Brown, Peter N.; Grant, Keith E. ACM Transactions on Mathematical Software, Vol. 31, Issue 3 https://doi.org/10.1145/1089014.1089020	journal	September 2005
Modeling the Effect of APC Truncation on Destruction Complex Function in Colorectal Cancer Cells Barua, Dipak; Hlavacek, William S. PLoS Computational Biology, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pcbi.1003217	journal	September 2013
SHIP1 Inhibition Increases Immunoregulatory Capacity and Triggers Apoptosis of Hematopoietic Cancer Cells Brooks, Robert; Fuhler, Gwenny M.; Iyer, Sonia The Journal of Immunology, Vol. 184, Issue 7 https://doi.org/10.4049/jimmunol.0902844	journal	March 2010
Subthreshold and Suboptimal Desensitization of Human Basophils Mendoza, Guillermo R.; Minagawa, Kiminobu International Archives of Allergy and Immunology, Vol. 68, Issue 2 https://doi.org/10.1159/000233076	journal	January 1982
Structural and Biophysical Characterization of the Syk Activation Switch Grädler, Ulrich; Schwarz, Daniel; Dresing, Verena Journal of Molecular Biology, Vol. 425, Issue 2 https://doi.org/10.1016/j.jmb.2012.11.007	journal	January 2013
Signal processing by the HOG MAP kinase pathway Hersen, P.; McClean, M. N.; Mahadevan, L. Proceedings of the National Academy of Sciences, Vol. 105, Issue 20 https://doi.org/10.1073/pnas.0710770105	journal	May 2008
The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Damen, J. E.; Liu, L.; Rosten, P. Proceedings of the National Academy of Sciences, Vol. 93, Issue 4 https://doi.org/10.1073/pnas.93.4.1689	journal	February 1996
Ramipril and metoprolol intake aggravate human and murine anaphylaxis: Evidence for direct mast cell priming Nassiri, Maria; Babina, Magda; Dölle, Sabine Journal of Allergy and Clinical Immunology, Vol. 135, Issue 2 https://doi.org/10.1016/j.jaci.2014.09.004	journal	February 2015
The src homology 2-containing inositol phosphatase (SHIP) is the gatekeeper of mast cell degranulation Huber, M.; Helgason, C. D.; Damen, J. E. Proceedings of the National Academy of Sciences, Vol. 95, Issue 19 https://doi.org/10.1073/pnas.95.19.11330	journal	September 1998
Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data Bischoff, Stephan C. Nature Reviews Immunology, Vol. 7, Issue 2 https://doi.org/10.1038/nri2018	journal	February 2007
Regulation of mast-cell and basophil function and survival by IgE Kawakami, Toshiaki; Galli, Stephen J. Nature Reviews Immunology, Vol. 2, Issue 10 https://doi.org/10.1038/nri914	journal	October 2002
Differential mast cell outcomes are sensitive to FcεRI-Syk binding kinetics Schwartz, Samantha L.; Cleyrat, Cédric; Olah, Mark J. Molecular Biology of the Cell, Vol. 28, Issue 23 https://doi.org/10.1091/mbc.E17-06-0350	journal	November 2017
BioNetFit: a fitting tool compatible with BioNetGen, NFsim and distributed computing environments Thomas, Brandon R.; Chylek, Lily A.; Colvin, Joshua Bioinformatics, Vol. 32, Issue 5 https://doi.org/10.1093/bioinformatics/btv655	journal	November 2015
In Vitro Desensitization of Human Skin Mast Cells Zhao, Wei; Gomez, Gregorio; Macey, Matthew Journal of Clinical Immunology, Vol. 32, Issue 1 https://doi.org/10.1007/s10875-011-9605-8	journal	October 2011
Multi-state Modeling of Biomolecules Stefan, Melanie I.; Bartol, Thomas M.; Sejnowski, Terrence J. PLoS Computational Biology, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pcbi.1003844	journal	September 2014
Diverse Sensitivity Thresholds in Dynamic Signaling Responses by Social Amoebae Wang, C. J.; Bergmann, A.; Lin, B. Science Signaling, Vol. 5, Issue 213 https://doi.org/10.1126/scisignal.2002449	journal	February 2012
Rift Valley Fever Virus Strain MP-12 Enters Mammalian Host Cells via Caveola-Mediated Endocytosis Harmon, B.; Schudel, B. R.; Maar, D. Journal of Virology, Vol. 86, Issue 23 https://doi.org/10.1128/JVI.02242-12	journal	September 2012
Rule-based modeling: a computational approach for studying biomolecular site dynamics in cell signaling systems: Computational approach for studying biomolecular site dynamics in cell signaling systems Chylek, Lily A.; Harris, Leonard A.; Tung, Chang-Shung Wiley Interdisciplinary Reviews: Systems Biology and Medicine, Vol. 6, Issue 1 https://doi.org/10.1002/wsbm.1245	journal	September 2013
Single-Cell Measurements of IgE-Mediated FcεRI Signaling Using an Integrated Microfluidic Platform Liu, Yanli; Barua, Dipak; Liu, Peng PLoS ONE, Vol. 8, Issue 3, Article No. e60159 https://doi.org/10.1371/journal.pone.0060159	journal	March 2013
Proline-rich Akt substrate of 40kDa (PRAS40): A novel downstream target of PI3k/Akt signaling pathway Wang, Haitao; Zhang, Qishan; Wen, Qiang Cellular Signalling, Vol. 24, Issue 1 https://doi.org/10.1016/j.cellsig.2011.08.010	journal	January 2012
BioNetGen: software for rule-based modeling of signal transduction based on the interactions of molecular domains Blinov, M. L.; Faeder, J. R.; Goldstein, B. Bioinformatics, Vol. 20, Issue 17 https://doi.org/10.1093/bioinformatics/bth378	journal	June 2004
Optimal Aggregation of FcεRI with a Structurally Defined Trivalent Ligand Overrides Negative Regulation Driven by Phosphatases Mahajan, Avanika; Barua, Dipak; Cutler, Patrick ACS Chemical Biology, Vol. 9, Issue 7 https://doi.org/10.1021/cb500134t	journal	May 2014
Tyr130 phosphorylation triggers Syk release from antigen receptor by long-distance conformational uncoupling Zhang, Y.; Oh, H.; Burton, R. A. Proceedings of the National Academy of Sciences, Vol. 105, Issue 33 https://doi.org/10.1073/pnas.0708583105	journal	August 2008
Characterization of protein-tyrosine phosphatases that dephosphorylate the high affinity IgE receptor. Mao, Su-Yau; Metzger, Henry Journal of Biological Chemistry, Vol. 272, Issue 38 https://doi.org/10.1016/s0021-9258(19)65897-7	journal	September 1997
The Frequency Dependence of Osmo-Adaptation in Saccharomyces cerevisiae Mettetal, J. T.; Muzzey, D.; Gomez-Uribe, C. Science, Vol. 319, Issue 5862 https://doi.org/10.1126/science.1151582	journal	January 2008
The FcϵRIβ Immunoreceptor Tyrosine-based Activation Motif Exerts Inhibitory Control on MAPK and IκB Kinase Phosphorylation and Mast Cell Cytokine Production Furumoto, Yasuko; Nunomura, Satoshi; Terada, Tomoyoshi Journal of Biological Chemistry, Vol. 279, Issue 47 https://doi.org/10.1074/jbc.M404730200	journal	September 2004
Phosphatase regulation of immunoreceptor signaling in T cells, B cells and mast cells Bounab, Yacine; Getahun, Andrew; Cambier, John C. Current Opinion in Immunology, Vol. 25, Issue 3 https://doi.org/10.1016/j.coi.2013.04.001	journal	June 2013
Characterization of Protein-tyrosine Phosphatases That Dephosphorylate the High Affinity IgE Receptor Mao, Su-Yau; Metzger, Henry Journal of Biological Chemistry, Vol. 272, Issue 22 https://doi.org/10.1074/jbc.272.22.14067	journal	May 1997
BioNetGen 2.2: advances in rule-based modeling Harris, Leonard A.; Hogg, Justin S.; Tapia, José-Juan Bioinformatics, Vol. 32, Issue 21 https://doi.org/10.1093/bioinformatics/btw469	journal	July 2016
Digital signaling decouples activation probability and population heterogeneity Kellogg, Ryan A.; Tian, Chengzhe; Lipniacki, Tomasz eLife, Vol. 4 https://doi.org/10.7554/eLife.08931	journal	October 2015
Induction of Basophil Desensitization in Physiological Medium: Enhancement after IgE-Dependent Upregulation of Surface IgE Binding on Basophils Komiya, Akiko; Hirai, Koichi; Iikura, Motoyasu International Archives of Allergy and Immunology, Vol. 130, Issue 1 https://doi.org/10.1159/000068374	journal	January 2003
Investigation of Early Events in FcεRI-Mediated Signaling Using a Detailed Mathematical Model Faeder, James R.; Hlavacek, William S.; Reischl, Ilona The Journal of Immunology, Vol. 170, Issue 7 https://doi.org/10.4049/jimmunol.170.7.3769	journal	April 2003

Cited By (3)

The Autoimmune Skin Disease Bullous Pemphigoid: The Role of Mast Cells in Autoantibody-Induced Tissue Injury Fang, Hui; Zhang, Yang; Li, Ning Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.00407	journal	March 2018
Parameter estimation and uncertainty quantification for systems biology models Mitra, Eshan D.; Hlavacek, William S. Current Opinion in Systems Biology, Vol. 18 https://doi.org/10.1016/j.coisb.2019.10.006	journal	December 2019
PyBioNetFit and the Biological Property Specification Language Mitra, Eshan D.; Suderman, Ryan; Colvin, Joshua iScience, Vol. 19 https://doi.org/10.1016/j.isci.2019.08.045	journal	September 2019

Similar Records

Single-Cell Measurements of IgE-Mediated FcεRI Signaling Using an Integrated Microfluidic Platform

Journal Article · Wed Mar 27 00:00:00 EDT 2013 · PLoS ONE · OSTI ID:1457302

Liu, Yanli; Barua, Dipak; Liu, Peng; +4 more

Cross-linking of surface Ig receptors on murine B lymphocytes stimulates the expression of nuclear tetradecanoyl phorbol acetate-response element-binding proteins

Journal Article · Fri Mar 15 00:00:00 EST 1991 · Journal of Immunology; (USA) · OSTI ID:1457302

Chiles, T C; Liu, J L; Rothstein, T L

Quantitative relationships between aggregation of IgE receptors, generation of intracellular signals, and histamine secretion in rat basophilic leukemia (2H3) cells. Enhanced responses with heavy water

Journal Article · Tue Feb 25 00:00:00 EST 1986 · J. Biol. Chem.; (United States) · OSTI ID:1457302

Maeyama, K; Hohman, R J; Metzger, H; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
computational models
lab-on-a-chip
signal processing

Title: Timescale Separation of Positive and Negative Signaling Creates History-Dependent Responses to IgE Receptor Stimulation

Citation Formats

References (41)

Cited By (3)

Similar Records

Related Subjects