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WAVE complex self-organization templates lamellipodial formation

View ORCID ProfileAnne Pipathsouk, Rachel M. Brunetti, Jason P. Town, Artù Breuer, Patrina A. Pellett, Kyle Marchuk, Ngoc-Han T. Tran, Matthew F. Krummel, Dimitrios Stamou, Orion D. Weiner
doi: https://doi.org/10.1101/836585
Anne Pipathsouk
1Cardiovascular Research Institute, University of California, San Francisco, CA, USA
2Department of Biochemistry and Biophysics, University of California, San Francisco, CA, USA
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  • ORCID record for Anne Pipathsouk
Rachel M. Brunetti
1Cardiovascular Research Institute, University of California, San Francisco, CA, USA
2Department of Biochemistry and Biophysics, University of California, San Francisco, CA, USA
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Jason P. Town
1Cardiovascular Research Institute, University of California, San Francisco, CA, USA
2Department of Biochemistry and Biophysics, University of California, San Francisco, CA, USA
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Artù Breuer
3Nano-Science Center and Department of Chemistry, University of Copenhagen, Copenhagen, Denmark
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Patrina A. Pellett
4GE Healthcare, Life Sciences, Cell Analysis Division, Marlborough, MA, USA
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Kyle Marchuk
5Department of Pathology and Biological Imaging Development CoLab, University of California, San Francisco, CA, USA
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Ngoc-Han T. Tran
2Department of Biochemistry and Biophysics, University of California, San Francisco, CA, USA
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Matthew F. Krummel
5Department of Pathology and Biological Imaging Development CoLab, University of California, San Francisco, CA, USA
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Dimitrios Stamou
3Nano-Science Center and Department of Chemistry, University of Copenhagen, Copenhagen, Denmark
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Orion D. Weiner
1Cardiovascular Research Institute, University of California, San Francisco, CA, USA
2Department of Biochemistry and Biophysics, University of California, San Francisco, CA, USA
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  • For correspondence: orion.weiner@ucsf.edu
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ABSTRACT

How local interactions of actin regulators yield large-scale organization of cell shape and movement is not well understood. For example, why does the WAVE complex build lamellipodia, the broad sheet-like protrusions that power cell migration, whereas the homologous actin regulator N-WASP forms spiky finger-like actin networks? N-WASP is known to oligomerize into focal condensates that generate an actin finger. In contrast, the WAVE complex exhibits the linear distribution needed to generate an actin sheet. This linear organization of the WAVE complex could either arise from interactions with the actin cytoskeleton or could represent an ability of the complex to self-organize into a linear template. Using super-resolution microscopy, we find that the WAVE complex forms higher-order linear oligomers that curve into 270 nanometer-wide ring structures in the absence of actin polymer. These rings localize to the necks of membrane invaginations, which display saddle point geometries with positive curvature in one axis and negative curvature in the orthogonal axis. To investigate the molecular mechanism of saddle curvature enrichment, we show that the WAVE complex and IRSp53, a membrane curvature-sensitive protein, collaborate to recognize saddle curvature that IRSp53 cannot sense alone. This saddle preference for the WAVE complex could explain emergent cell behaviors, such as expanding and self-straightening lamellipodia as well as the ability of endothelial cells to recognize and seal transcellular holes. Our work highlights how partnering protein interactions enable complex shape sensing and how feedback between cell shape and actin regulators yields self-organized cell morphogenesis.

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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-ND 4.0 International license.
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Posted November 09, 2019.
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WAVE complex self-organization templates lamellipodial formation
Anne Pipathsouk, Rachel M. Brunetti, Jason P. Town, Artù Breuer, Patrina A. Pellett, Kyle Marchuk, Ngoc-Han T. Tran, Matthew F. Krummel, Dimitrios Stamou, Orion D. Weiner
bioRxiv 836585; doi: https://doi.org/10.1101/836585
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WAVE complex self-organization templates lamellipodial formation
Anne Pipathsouk, Rachel M. Brunetti, Jason P. Town, Artù Breuer, Patrina A. Pellett, Kyle Marchuk, Ngoc-Han T. Tran, Matthew F. Krummel, Dimitrios Stamou, Orion D. Weiner
bioRxiv 836585; doi: https://doi.org/10.1101/836585

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