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Disentangling Membrane Dynamics and Cell Migration; Differential Influences of F-actin and Cell-Matrix Adhesions

Author

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  • Jacob M Kowalewski
  • Hamdah Shafqat-Abbasi
  • Mehrdad Jafari-Mamaghani
  • Bereket Endrias Ganebo
  • Xiaowei Gong
  • Staffan Strömblad
  • John G Lock

Abstract

Cell migration is heavily interconnected with plasma membrane protrusion and retraction (collectively termed “membrane dynamics”). This makes it difficult to distinguish regulatory mechanisms that differentially influence migration and membrane dynamics. Yet such distinctions may be valuable given evidence that cancer cell invasion in 3D may be better predicted by 2D membrane dynamics than by 2D cell migration, implying a degree of functional independence between these processes. Here, we applied multi-scale single cell imaging and a systematic statistical approach to disentangle regulatory associations underlying either migration or membrane dynamics. This revealed preferential correlations between membrane dynamics and F-actin features, contrasting with an enrichment of links between cell migration and adhesion complex properties. These correlative linkages were often non-linear and therefore context-dependent, strengthening or weakening with spontaneous heterogeneity in cell behavior. More broadly, we observed that slow moving cells tend to increase in area, while fast moving cells tend to shrink, and that the size of dynamic membrane domains is independent of cell area. Overall, we define macromolecular features preferentially associated with either cell migration or membrane dynamics, enabling more specific interrogation and targeting of these processes in future.

Suggested Citation

  • Jacob M Kowalewski & Hamdah Shafqat-Abbasi & Mehrdad Jafari-Mamaghani & Bereket Endrias Ganebo & Xiaowei Gong & Staffan Strömblad & John G Lock, 2015. "Disentangling Membrane Dynamics and Cell Migration; Differential Influences of F-actin and Cell-Matrix Adhesions," PLOS ONE, Public Library of Science, vol. 10(8), pages 1-23, August.
  • Handle: RePEc:plo:pone00:0135204
    DOI: 10.1371/journal.pone.0135204
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    References listed on IDEAS

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    1. Kinneret Keren & Zachary Pincus & Greg M. Allen & Erin L. Barnhart & Gerard Marriott & Alex Mogilner & Julie A. Theriot, 2008. "Mechanism of shape determination in motile cells," Nature, Nature, vol. 453(7194), pages 475-480, May.
    2. John G Lock & Mehrdad Jafari Mamaghani & Hamdah Shafqat-Abbasi & Xiaowei Gong & Joanna Tyrcha & Staffan Strömblad, 2014. "Plasticity in the Macromolecular-Scale Causal Networks of Cell Migration," PLOS ONE, Public Library of Science, vol. 9(2), pages 1-17, February.
    3. Pablo Hernández-Varas & Ulrich Berge & John G. Lock & Staffan Strömblad, 2015. "A plastic relationship between vinculin-mediated tension and adhesion complex area defines adhesion size and lifetime," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
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