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Collective oscillatory signaling in Dictyostelium discoideum acts as a developmental timer initiated by weak coupling of a noisy pulsatile signal

Brimson, Christopher A; Baines, Robert; Sams-Dodd, Elisabeth; Stefanescu, Ioanina; Evans, Bethany; Kuwana, Satoshi; Hashimura, Hidenori; ... Thompson, Christopher RL; + view all (2024) Collective oscillatory signaling in Dictyostelium discoideum acts as a developmental timer initiated by weak coupling of a noisy pulsatile signal. Developmental Cell 10.1016/j.devcel.2024.11.016. (In press). Green open access

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Abstract

Oscillatory phenomena play widespread roles in the control of biological systems. In D. discoideum, oscillatory cyclic adenosine monophosphate (cAMP) signaling drives collective behavior and induces a temporal developmental gene expression program. How collective cAMP oscillations emerge or how they encode temporal transcriptional information is still poorly understood. To address this, we identified a transcription factor required for the initiation of collective behavior. Hbx5 activity is cAMP dependent and provides a sensitive single-cell readout for cAMP signaling. Extensive stochastic pulsatile cAMP signaling is found to precede collective oscillations. Stochastic signaling induces Hbx5-dependent transcriptional feedback, which enhances signal sensitivity and cell-cell coupling. This results in the emergence of synchronized collective oscillations, which subsequently activates the GtaC transcription factor and triggers shifts in developmental gene expression. Our results suggest this temporal coordination is encoded by changes in the amplitude of cAMP oscillations and differential sensitivity of these transcription factors to the cAMP-regulated kinase ErkB.

Type: Article
Title: Collective oscillatory signaling in Dictyostelium discoideum acts as a developmental timer initiated by weak coupling of a noisy pulsatile signal
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1016/j.devcel.2024.11.016
Publisher version: https://doi.org/10.1016/j.devcel.2024.11.016
Language: English
Additional information: Copyright © 2024 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Keywords: Dictyostelium, Erk activity, cAMP signaling, collective behavior, coupled oscillations, developmental time, oscillatory signaling, stochastic signaling, subcellular localization, transcription factors
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Genetics, Evolution and Environment
URI: https://discovery.ucl.ac.uk/id/eprint/10203005
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