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Accurate information transmission through dynamic biochemical signaling networks
Open accessAbstract
Stochasticity inherent to biochemical reactions (intrinsic noise) and variability in cellular states (extrinsic noise) degrade information transmitted through signaling networks. We analyzed the ability of temporal signal modulation—that is, dynamics—to reduce noise-induced information loss. In the extracellular signal–regulated kinase (ERK), calcium (Ca 2+ ), and nuclear factor kappa-B (NF-κB) pathways, response dynamics resulted in significantly greater information transmission capacities compared to nondynamic responses. Theoretical analysis demonstrated that signaling dynamics has a key role in overcoming extrinsic noise. Experimental measurements of information transmission in the ERK network under varying signal-to-noise levels confirmed our predictions and showed that signaling dynamics mitigate, and can potentially eliminate, extrinsic noise–induced information loss. By curbing the information-degrading effects of cell-to-cell variability, dynamic responses substantially increase the accuracy of biochemical signaling networks.
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Cites
Information transfer by leaky, heterogeneous, protein kinase signaling systems
Voliotis, M., Perrett, R. M., McWilliams, C., McArdle, C. A., & Bowsher, C. G. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314446111 · Cited by 98
Cited by
Van Valen, D. A., Kudo, T., Lane, K. M., Macklin, D. N., Quach, N. T., DeFelice, M. M., Maayan, I., Tanouchi, Y., Ashley, E. A., & Covert, M. W. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005177 · Cited by 557
Robustness and Information Transfer within IL-6-induced JAK/STAT Signalling
Billing, U., Jetka, T., Nortmann, L., Wundrack, N., Komorowski, M., Waldherr, S., Schaper, F., & Dittrich, A. (2019) · Communications Biology · doi:10.1038/s42003-018-0259-4 · Cited by 64
Relaxation oscillations and hierarchy of feedbacks in MAPK signaling
Kochańczyk, M., Kocieniewski, P., Kozłowska, E., Jaruszewicz-Błońska, J., Sparta, B., Pargett, M., Albeck, J. G., Hlavacek, W. S., & Lipniacki, T. (2017) · Scientific Reports · doi:10.1038/srep38244 · Cited by 59
Self-citationFiebelkow, J., Guendel, A., Guendel, B., Mehwald, N., Jetka, T., Komorowski, M., Waldherr, S., Schaper, F., & Dittrich, A. (2021) · Cell Communication and Signaling · doi:10.1186/s12964-021-00770-7 · Cited by 53
Mathematical modeling of gonadotropin-releasing hormone signaling
Pratap, A., Garner, K. L., Voliotis, M., Tsaneva-Atanasova, K., & McArdle, C. A. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.08.022 · Cited by 35
Signaling pathways have an inherent need for noise to acquire information
Azpeitia, E., Balanzario, E. P., & Wagner, A. (2020) · BMC Bioinformatics · doi:10.1186/s12859-020-03778-x · Cited by 20
Modeling evolution of crosstalk in noisy signal transduction networks
Tareen, A., Wingreen, N. S., & Mukhopadhyay, R. (2018) · Physical Review E · doi:10.1103/physreve.97.020402 · Cited by 11
Nearly maximal information gain due to time integration in central dogma reactions
Sarkar, S., & Rammohan, J. (2023) · iScience · doi:10.1016/j.isci.2023.106767
Metadata
- Authors
- Selimkhanov, J., Taylor, B., Yao, J., Pilko, A., Albeck, J., Hoffmann, A., Tsimring, L., & Wollman, R.
- Venue
- Science
- Published
- 2014-12-12
- Volume
- 346
- Issue
- 6215
- Pages
- 1370-1373
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2021387539
- Cited by
- 378
- References
- 1
- FWCI
- 10.46
- Type
- journal article
- Language
- en
- Open access
- green
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