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Research Article

Characterizing deformability and surface friction of cancer cells

Sangwon Byun, Sungmin Son, Dario Amodei, Nathan Cermak, Josephine Shaw, Joon Ho Kang, Vivian C. Hecht, Monte M. Winslow, Tyler Jacks, Parag Mallick, and Scott R. Manalis
  1. Departments of aBiological Engineering,
  2. bMechanical Engineering,
  3. dComputational and Systems Biology Initiative,
  4. ePhysics,
  5. hBiology, and
  6. fKoch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02139; and
  7. Departments of cRadiology and
  8. gGenetics, Stanford University School of Medicine, Stanford, CA 94305

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PNAS first published April 22, 2013; https://doi.org/10.1073/pnas.1218806110
Sangwon Byun
Departments of aBiological Engineering,
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Sungmin Son
bMechanical Engineering,
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Dario Amodei
Departments of cRadiology and
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Nathan Cermak
dComputational and Systems Biology Initiative,
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Josephine Shaw
Departments of aBiological Engineering,
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Joon Ho Kang
ePhysics,
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Vivian C. Hecht
Departments of aBiological Engineering,
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Monte M. Winslow
fKoch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02139; and
gGenetics, Stanford University School of Medicine, Stanford, CA 94305
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Tyler Jacks
fKoch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02139; and
hBiology, and
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Parag Mallick
Departments of cRadiology and
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Scott R. Manalis
Departments of aBiological Engineering,
bMechanical Engineering,
dComputational and Systems Biology Initiative,
fKoch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02139; and
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  • For correspondence: scottm@media.mit.edu
  1. Edited by David A. Weitz, Harvard University, Cambridge, MA, and approved April 1, 2013 (received for review October 28, 2012)

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Abstract

Metastasis requires the penetration of cancer cells through tight spaces, which is mediated by the physical properties of the cells as well as their interactions with the confined environment. Various microfluidic approaches have been devised to mimic traversal in vitro by measuring the time required for cells to pass through a constriction. Although a cell’s passage time is expected to depend on its deformability, measurements from existing approaches are confounded by a cell's size and its frictional properties with the channel wall. Here, we introduce a device that enables the precise measurement of (i) the size of a single cell, given by its buoyant mass, (ii) the velocity of the cell entering a constricted microchannel (entry velocity), and (iii) the velocity of the cell as it transits through the constriction (transit velocity). Changing the deformability of the cell by perturbing its cytoskeleton primarily alters the entry velocity, whereas changing the surface friction by immobilizing positive charges on the constriction's walls primarily alters the transit velocity, indicating that these parameters can give insight into the factors affecting the passage of each cell. When accounting for cell buoyant mass, we find that cells possessing higher metastatic potential exhibit faster entry velocities than cells with lower metastatic potential. We additionally find that some cell types with higher metastatic potential exhibit greater than expected changes in transit velocities, suggesting that not only the increased deformability but reduced friction may be a factor in enabling invasive cancer cells to efficiently squeeze through tight spaces.

  • cell mechanics
  • cell stiffness
  • biophysics
  • suspended microchannel resonator
  • biosensors

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: scottm{at}media.mit.edu.
  • Author contributions: S.B., S.S., N.C., J.S., J.H.K., V.C.H., M.M.W., T.J., P.M., and S.R.M. designed research; S.B., S.S., N.C., J.S., J.H.K., and V.C.H. performed research; M.M.W. and T.J. contributed mouse model cell lines; S.B., D.A., N.C., and J.S. analyzed data; and S.B., D.A., J.S., P.M., and S.R.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1218806110/-/DCSupplemental.

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Deformability and surface friction of cancer cells
Sangwon Byun, Sungmin Son, Dario Amodei, Nathan Cermak, Josephine Shaw, Joon Ho Kang, Vivian C. Hecht, Monte M. Winslow, Tyler Jacks, Parag Mallick, Scott R. Manalis
Proceedings of the National Academy of Sciences Apr 2013, 201218806; DOI: 10.1073/pnas.1218806110

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Deformability and surface friction of cancer cells
Sangwon Byun, Sungmin Son, Dario Amodei, Nathan Cermak, Josephine Shaw, Joon Ho Kang, Vivian C. Hecht, Monte M. Winslow, Tyler Jacks, Parag Mallick, Scott R. Manalis
Proceedings of the National Academy of Sciences Apr 2013, 201218806; DOI: 10.1073/pnas.1218806110
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