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Potential Hydrodynamic Cytoplasmic Transfer between Mammalian Cells: Cell-Projection Pumping.

Hans Zoellner1, Navid Paknejad2, James A Cornwell3

  • 1The Cellular and Molecular Pathology Research Unit, Oral Pathology and Oral Medicine, School of Dentistry, Faculty of Medicine and Health, The University of Sydney, Westmead Hospital, Westmead, Australia; Cell Biology, The Memorial Sloan Kettering Cancer Center, New York, New York.

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Cytoplasmic transfer between human fibroblasts and malignant cells occurs via cell-projection pumping (CPP), a novel hydrodynamic mechanism, not tunneling nanotubes or vesicles. This process is influenced by cell stiffness.

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Area of Science:

  • Cell Biology
  • Biophysics

Background:

  • Intercellular cytoplasmic transfer influences cell phenotype.
  • Previous studies suggested transfer via tunneling nanotubes or shed vesicles.

Purpose of the Study:

  • Investigate the mechanism of cytoplasmic fluorescence exchange between human fibroblasts (Fibs) and malignant cells (MCs).
  • Propose and validate a novel mechanism termed cell-projection pumping (CPP).

Main Methods:

  • Time-lapse microscopy to observe cytoplasmic exchange.
  • Holotomography to visualize fine cell projections.
  • Atomic force microscopy to measure cell stiffness.
  • Mathematical modeling and computer simulations to test the CPP hypothesis.

Main Results:

  • Cytoplasmic transfer predominantly occurred from Fibs to MCs.
  • Transfer was mediated by fine, rapidly retracting cell projections, not tunneling nanotubes or vesicles.
  • Cell stiffness influenced the direction and extent of cytoplasmic transfer.
  • Mathematical modeling and simulations supported the CPP mechanism, predicting preferential transfer into less stiff cells.

Conclusions:

  • Cell-projection pumping (CPP) is proposed as a novel mechanism for mammalian intercellular cytoplasmic transfer.
  • CPP involves hydrodynamic forces during cell projection retraction and microfusion events.
  • The findings highlight the role of biophysical properties like cell stiffness in regulating intercellular communication.