Efficient Front-Rear Coupling in Neutrophil Chemotaxis by Dynamic Myosin II Localization

Tony Y.C. Tsai, Sean Collins, Caleb K. Chan, Amalia Hadjitheodorou, Pui Ying Lam, Sunny S. Lou, Hee Won Yang, Julianne Jorgensen, Felix Ellett, Daniel Irimia, Michael W. Davidson, Robert S. Fischer, Anna Huttenlocher, Tobias Meyer, James E. Ferrell, Julie A. Theriot

Research output: Contribution to journalArticle

9 Scopus citations

Abstract

Efficient chemotaxis requires rapid coordination between different parts of the cell in response to changing directional cues. Here, we investigate the mechanism of front-rear coordination in chemotactic neutrophils. We find that changes in the protrusion rate at the cell front are instantaneously coupled to changes in retraction at the cell rear, while myosin II accumulation at the rear exhibits a reproducible 9–15-s lag. In turning cells, myosin II exhibits dynamic side-to-side relocalization at the cell rear in response to turning of the leading edge and facilitates efficient turning by rapidly re-orienting the rear. These manifestations of front-rear coupling can be explained by a simple quantitative model incorporating reversible actin-myosin interactions with a rearward-flowing actin network. Finally, the system can be tuned by the degree of myosin regulatory light chain (MRLC) phosphorylation, which appears to be set in an optimal range to balance persistence of movement and turning ability. Efficient chemotaxis requires close coordination between the front and the rear of a migrating cell. Tsai et al. identified a mechanical feedback between front protrusion and rear retraction, mediated by cell-scale retrograde flow, membrane tension, and dynamic myosin relocalization that is optimized to balance migration persistence with turning efficiency.

Original languageEnglish (US)
Pages (from-to)189-205.e6
JournalDevelopmental Cell
Volume49
Issue number2
DOIs
StatePublished - Apr 22 2019
Externally publishedYes

Keywords

  • actin network retrograde flow
  • actin-myosin interaction
  • cell mechanics
  • cell migration
  • cytoskeleton dynamics
  • myosin light chain phosphorylation
  • neutrophil chemotaxis

ASJC Scopus subject areas

  • Molecular Biology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Developmental Biology
  • Cell Biology

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  • Cite this

    Tsai, T. Y. C., Collins, S., Chan, C. K., Hadjitheodorou, A., Lam, P. Y., Lou, S. S., Yang, H. W., Jorgensen, J., Ellett, F., Irimia, D., Davidson, M. W., Fischer, R. S., Huttenlocher, A., Meyer, T., Ferrell, J. E., & Theriot, J. A. (2019). Efficient Front-Rear Coupling in Neutrophil Chemotaxis by Dynamic Myosin II Localization. Developmental Cell, 49(2), 189-205.e6. https://doi.org/10.1016/j.devcel.2019.03.025