4.5 Article

Intercellular water exchanges trigger soliton-like waves in multicellular systems

Journal

BIOPHYSICAL JOURNAL
Volume 121, Issue 9, Pages 1610-1618

Publisher

CELL PRESS
DOI: 10.1016/j.bpj.2022.04.005

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Funding

  1. National Natural Science Foundation of China [12002338, 12025207, 11872357, 11622222]
  2. USTC Research Funds of the Double First-Class Initiative [YD2480002001]
  3. Anhui Provincial Natural Science Foundation [2008085QA24]
  4. Fundamental Research Funds for the Central Universities [WK2090000017, WK2090050048, WK2480000006, WK2480000005]
  5. Strategic Priority Research Program of the Chinese Academy of Sciences [XDB22040403]

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Oscillations and waves in living cellular systems are often attributed to mechanochemical feedbacks. However, this study reveals that osmotic shocks can trigger self-sustained cell oscillations and result in long-range waves. These waves propagate along the intercellular osmotic pressure gradient and their speed is proportional to the magnitude of intercellular water flows. Additionally, the waves exhibit characteristics of solitary waves. These findings predict a new mechanism of wave generation in living multicellular systems and suggest its relevance to a broad class of systems.
Oscillations and waves are ubiquitous in living cellular systems. Generations of these spatiotemporal patterns are generally attributed to some mechanochemical feedbacks. Here, we treat cells as open systems, i.e., water and ions can pass through the cell membrane passively or actively, and reveal a new origin of wave generation. We show that osmotic shocks above a shock threshold will trigger self-sustained cell oscillations and result in long-range waves propagating without decrement, a phenomenon that is analogous to the excitable medium. The traveling wave propagates along the intercellular osmotic pressure gradient, and its wave speed scales with the magnitude of intercellular water flows. Furthermore, we also find that the traveling wave exhibits several hallmarks of solitary waves. Together, our findings predict a new mechanism of wave generation in living multicellular systems. The ubiquity of intercellular water exchanges implies that this mechanism may be relevant to a broad class of systems.

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