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Dev Cell. 2019 Mar 11;48(5):646-658.e6. doi: 10.1016/j.devcel.2018.12.024. Epub 2019 Jan 31.

Heat Oscillations Driven by the Embryonic Cell Cycle Reveal the Energetic Costs of Signaling.

Author information

1
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06520, USA. Electronic address: jonathan.rodenfels@gmail.com.
2
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06520, USA. Electronic address: karla.neugebauer@yale.edu.
3
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06520, USA.

Abstract

All living systems function out of equilibrium and exchange energy in the form of heat with their environment. Thus, heat flow can inform on the energetic costs of cellular processes, which are largely unknown. Here, we have repurposed an isothermal calorimeter to measure heat flow between developing zebrafish embryos and the surrounding medium. Heat flow increased over time with cell number. Unexpectedly, a prominent oscillatory component of the heat flow, with periods matching the synchronous early reductive cleavage divisions, persisted even when DNA synthesis and mitosis were blocked by inhibitors. Instead, the heat flow oscillations were driven by the phosphorylation and dephosphorylation reactions catalyzed by the cell-cycle oscillator, the biochemical network controlling mitotic entry and exit. We propose that the high energetic cost of cell-cycle signaling reflects the significant thermodynamic burden of imposing accurate and robust timing on cell proliferation during development.

KEYWORDS:

cell cycle; cell cycle oscillator; cell proliferation; energetics; energy dissipation; heat flow; isothermal calorimetry; zebrafish embryogenesis

PMID:
30713074
PMCID:
PMC6414255
[Available on 2020-03-11]
DOI:
10.1016/j.devcel.2018.12.024
[Indexed for MEDLINE]

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