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Three-dimensional actin-based protrusions of migrating neutrophils are intrinsically lamellar and facilitate direction changes

Lillian K. Fritz-Laylin, Megan Riel-Mehan, Bi-Chang Chen, Samuel J. Lord, Thomas D. Goddard, Thomas E. Ferrin, Graham Johnson, Eric Betzig, R. Dyche Mullins
doi: https://doi.org/10.1101/120444
Lillian K. Fritz-Laylin
aDepartment of Cellular and Molecular Pharmacology, Howard Hughes Medical Institute, University of California, San Francisco CA 94158, USA.
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Megan Riel-Mehan
bDepartment of Bioengineering and Therapeutic Sciences, University of California, San Francisco CA 94158, USA.
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Bi-Chang Chen
cJanelia Farms Research Campus, Howard Hughes Medical Institute, Ashburn VA, 20147, USA
dPresent address : Research Center for Applied Sciences, Academia Sinica, Taipei 11529, Taiwan.
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Samuel J. Lord
aDepartment of Cellular and Molecular Pharmacology, Howard Hughes Medical Institute, University of California, San Francisco CA 94158, USA.
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Thomas D. Goddard
eDepartment of Pharmaceutical Chemistry, University of California, San Francisco CA 94158, USA.
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Thomas E. Ferrin
eDepartment of Pharmaceutical Chemistry, University of California, San Francisco CA 94158, USA.
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Graham Johnson
fDepartment of Bioengineering and Therapeutic Science, University of California, San Francisco CA 94158, USA.
gAnimated Cell, Allen Institute for Cell Science, Seattle WA, 98109, USA
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Eric Betzig
cJanelia Farms Research Campus, Howard Hughes Medical Institute, Ashburn VA, 20147, USA
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R. Dyche Mullins
aDepartment of Cellular and Molecular Pharmacology, Howard Hughes Medical Institute, University of California, San Francisco CA 94158, USA.
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  • For correspondence: dyche@mullinslab.ucsf.edu
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Abstract

Leukocytes and other amoeboid cells change shape as they move, forming highly dynamic, actin-filled pseudopods. Although we understand much about the architecture and dynamics of thin lamellipodia made by slow-moving cells on flat surfaces, conventional light microscopy lacks the spatial and temporal resolution required to track complex pseudopods of cells moving in three dimensions. We therefore employed lattice light sheet microscopy to perform three-dimensional, time-lapse imaging of neutrophil-like HL-60 cells crawling through collagen matrices. To analyze three-dimensional pseudopods we: (i) developed fluorescent probe combinations that distinguish cortical actin from dynamic, pseudopod-forming actin networks, and (ii) adapted molecular visualization tools from structural biology to render and analyze complex cell surfaces. Surprisingly, three-dimensional pseudopods turn out to be composed of thin (<0.75 μm), flat sheets that sometimes interleave to form rosettes. Their laminar nature is not templated by an external surface, but likely reflects a linear arrangement of regulatory molecules. Although we find that pseudopods are dispensable for three-dimensional locomotion, their elimination dramatically decreases the frequency of cell turning, and pseudopod dynamics increase when cells change direction, highlighting the important role pseudopods play in pathfinding.

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  • ↵* Co-first author

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Posted March 24, 2017.
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Three-dimensional actin-based protrusions of migrating neutrophils are intrinsically lamellar and facilitate direction changes
Lillian K. Fritz-Laylin, Megan Riel-Mehan, Bi-Chang Chen, Samuel J. Lord, Thomas D. Goddard, Thomas E. Ferrin, Graham Johnson, Eric Betzig, R. Dyche Mullins
bioRxiv 120444; doi: https://doi.org/10.1101/120444
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Three-dimensional actin-based protrusions of migrating neutrophils are intrinsically lamellar and facilitate direction changes
Lillian K. Fritz-Laylin, Megan Riel-Mehan, Bi-Chang Chen, Samuel J. Lord, Thomas D. Goddard, Thomas E. Ferrin, Graham Johnson, Eric Betzig, R. Dyche Mullins
bioRxiv 120444; doi: https://doi.org/10.1101/120444

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