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Collective Mechanical Memory Encoded by Long-Lasting Supracellular Cytoskeletal Structures in Multicellular

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Area of Science:

  • Cell Biology
  • Biophysics
  • Cancer Research

Background:

  • Animal cells exhibit "mechanical memory," altering form and function based on environmental stiffness.
  • Previous studies attributed this memory to individual cell epigenetic and transcriptional changes.
  • The retention of mechanical memory across collective cells remained largely unexplored.

Purpose of the Study:

  • To investigate if collective cells retain mechanical memory.
  • To elucidate the mechanisms underlying collective cell mechanical memory.
  • To explore the role of collective mechanical memory in cancer metastasis.

Main Methods:

  • Modeling ovarian cancer metastasis.
  • Culturing cells on substrates of varying stiffness (soft-primed vs. stiff-primed).
  • Analyzing multicellular spheroid formation and cytoskeletal structures (actin-CK18 networks).
  • Investigating the role of gap junctions in maintaining collective memory.

Main Results:

  • Collective cells sustained mechanical memory through self-organized actin-CK18 networks.
  • Soft-primed cells showed stronger cell-cell adhesions and formed peripheral cytoskeletal cages in spheroids.
  • These cages impeded collective invasion, confining spheroid movement.
  • Gap junction inhibition disrupted cytoskeletal cage formation, highlighting the role of intercellular communication.

Conclusions:

  • Collective cells possess a mechanical memory mechanism independent of solely epigenetic/transcriptional factors.
  • Supracellular actin-CK18 networks and intercellular communication are crucial for collective mechanical memory.
  • This finding advances understanding of tumor cell cluster behavior in metastatic processes.