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Potential hydrodynamic cytoplasmic transfer between mammalian cells: Cell-projection pumping

View ORCID ProfileHans Zoellner, Navid Paknejad, James Cornwell, Belal Chami, Yevgeniy Romin, Vitaly Boyko, Sho Fujisawa, Elizabeth Kelly, Garry W. Lynch, Glynn Rogers, Katia Manova, Malcolm A.S. Moore
doi: https://doi.org/10.1101/531798
Hans Zoellner
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, NSW 2145, Australia
2Cell Biology, The Memorial Sloan Kettering Cancer Center, 430 E 67th St, RRL 717, New York, NY
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  • ORCID record for Hans Zoellner
  • For correspondence: hans.zoellner@sydney.edu.au
Navid Paknejad
3Molecular Cytology, The Memorial Sloan Kettering Cancer Center, 415-417 E 68 Street, ZRC 1962, New York, NY
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James Cornwell
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, NSW 2145, Australia
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Belal Chami
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, NSW 2145, Australia
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Yevgeniy Romin
3Molecular Cytology, The Memorial Sloan Kettering Cancer Center, 415-417 E 68 Street, ZRC 1962, New York, NY
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Vitaly Boyko
3Molecular Cytology, The Memorial Sloan Kettering Cancer Center, 415-417 E 68 Street, ZRC 1962, New York, NY
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Sho Fujisawa
3Molecular Cytology, The Memorial Sloan Kettering Cancer Center, 415-417 E 68 Street, ZRC 1962, New York, NY
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Elizabeth Kelly
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, NSW 2145, Australia
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Garry W. Lynch
4Sydney Medical School, Faculty of Medicine and Health, and Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, NSW, 2006, Australia
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Glynn Rogers
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, NSW 2145, Australia
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Katia Manova
3Molecular Cytology, The Memorial Sloan Kettering Cancer Center, 415-417 E 68 Street, ZRC 1962, New York, NY
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Malcolm A.S. Moore
2Cell Biology, The Memorial Sloan Kettering Cancer Center, 430 E 67th St, RRL 717, New York, NY
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ABSTRACT

We earlier reported cytoplasmic fluorescence exchange between cultured human fibroblasts (Fib) and malignant cells (MC). Others report similar transfer via either tunneling nanotubes (TNT) or shed membrane vesicles and this changes the phenotype of recipient cells. Our current time-lapse microscopy showed most exchange was from Fib into MC, with less in the reverse direction. Although TNT were seen, we were surprised transfer was not via TNT, but was instead via fine and often branching cell projections that defied direct visual resolution because of their size and rapid movement. Their structure was revealed nonetheless, by their organellar cargo and the grooves they formed indenting MC, while this was consistent with holotomography. Discrete, rapid and highly localized transfer events, evidenced against a role for shed vesicles. Transfer coincided with rapid retraction of the cell-projections, suggesting a hydrodynamic mechanism. Increased hydrodynamic pressure in retracting cell-projections normally returns cytoplasm to the cell body. We hypothesize ‘cell-projection pumping’ (CPP), where cytoplasm in retracting cell-projections partially equilibrates into adjacent recipient cells via micro-fusions that form temporary inter-cellular cytoplasmic continuities. We tested plausibility for CPP by combined mathematical modelling, comparison of predictions from the model with experimental results, and then computer simulations based on experimental data. The mathematical model predicted preferential CPP into cells with lower cell stiffness, expected from equilibration of pressure towards least resistance. Predictions from the model were satisfied when Fib were co-cultured with MC, and fluorescence exchange related with cell stiffness by atomic force microscopy. When transfer into 5000 simulated recipient MC or Fib was studied in computer simulations, inputting experimental cell stiffness and donor cell fluorescence values generated transfers to simulated recipient cells similar to those seen by experiment. We propose CPP as a potentially novel mechanism in mammalian inter-cellular cytoplasmic transfer and communication.

SIGNIFICANCE Time-lapse observations of co-cultured cells led us to hypothesize what we believe to be a novel hydrodynamic mechanism transferring cytoplasm between cells. Similar transfer by other mechanisms markedly affects cell behavior. Combined mathematical modelling, satisfaction of predictions from the mathematical model in cell culture experiments, and separate computer simulations that generate outcomes similar to experimental observations, support our hypothesized mechanism.

Footnotes

  • It was decided to slightly modify the title of the report. In addition, Supplementary movie S6 has been improved by addition of arrows marking cell-projections of interest. Further, original Matlab files that may be of use to colleagues wishing to perform computer simulations, or to explore the effect of changing variables with the data used in this study, are also now provided in compressed file format.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted January 10, 2020.
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Potential hydrodynamic cytoplasmic transfer between mammalian cells: Cell-projection pumping
Hans Zoellner, Navid Paknejad, James Cornwell, Belal Chami, Yevgeniy Romin, Vitaly Boyko, Sho Fujisawa, Elizabeth Kelly, Garry W. Lynch, Glynn Rogers, Katia Manova, Malcolm A.S. Moore
bioRxiv 531798; doi: https://doi.org/10.1101/531798
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Potential hydrodynamic cytoplasmic transfer between mammalian cells: Cell-projection pumping
Hans Zoellner, Navid Paknejad, James Cornwell, Belal Chami, Yevgeniy Romin, Vitaly Boyko, Sho Fujisawa, Elizabeth Kelly, Garry W. Lynch, Glynn Rogers, Katia Manova, Malcolm A.S. Moore
bioRxiv 531798; doi: https://doi.org/10.1101/531798

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