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Cited by 187Cellular Mechanics and InteractionsProtein Kinase Regulation and GTPase SignalingCellular transport and secretion

Membrane Tension Acts Through PLD2 and mTORC2 to Limit Actin Network Assembly During Neutrophil Migration

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Diz-Muñoz, Alba, Thurley, Kevin, Chintamen, Sana, Altschuler, Steven J., Wu, Lani F., Fletcher, Daniel A., Weiner, Orion D.·2016·PLOS Biology
DOI 10.1371/journal.pbio.1002474PMC PMC4900667
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Abstract

For efficient polarity and migration, cells need to regulate the magnitude and spatial distribution of actin assembly. This process is coordinated by reciprocal interactions between the actin cytoskeleton and mechanical forces. Actin polymerization-based protrusion increases tension in the plasma membrane, which in turn acts as a long-range inhibitor of actin assembly. These interactions form a negative feedback circuit that limits the magnitude of membrane tension in neutrophils and prevents expansion of the existing front and the formation of secondary fronts. It has been suggested that the plasma membrane directly inhibits actin assembly by serving as a physical barrier that opposes protrusion. Here we show that efficient control of actin polymerization-based protrusion requires an additional mechanosensory feedback cascade that indirectly links membrane tension with actin assembly. Specifically, elevated membrane tension acts through phospholipase D2 (PLD2) and the mammalian target of rapamycin complex 2 (mTORC2) to limit actin nucleation. In the absence of this pathway, neutrophils exhibit larger leading edges, higher membrane tension, and profoundly defective chemotaxis. Mathematical modeling suggests roles for both the direct (mechanical) and indirect (biochemical via PLD2 and mTORC2) feedback loops in organizing cell polarity and motility-the indirect loop is better suited to enable competition between fronts, whereas the direct loop helps spatially organize actin nucleation for efficient leading edge formation and cell movement. This circuit is essential for polarity, motility, and the control of membrane tension.

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Authors
Diz-Muñoz, A., Thurley, K., Chintamen, S., Altschuler, S. J., Wu, L. F., Fletcher, D. A., & Weiner, O. D.
Affiliations
  • University of California, San Francisco (US)
  • University of California, Berkeley (US)
Corresponding author
  • Diz-Muñoz, Alba
  • Thurley, Kevin
  • Altschuler, Steven J.
  • Wu, Lani F.
  • Fletcher, Daniel A.
  • Weiner, Orion D.
ORCID
Venue
PLOS Biology
Publisher
Public Library of Science (PLoS)
Published
2016-06-09
Volume
14
Issue
6
Pages
e1002474
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
DOI
10.1371/journal.pbio.1002474
PMC
PMC4900667
OpenAlex
W2414012998
Cited by
187
References
3
Citations by year
2026: 15 · 2025: 12 · 2024: 19 · 2023: 16 · 2022: 27 · 2021: 19 · 2020: 26 · 2019: 18 · 2018: 17 · 2017: 16 · 2016: 1
FWCI
9.91
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Institute of General Medical Sciences (GM084040, GM118167, GM074751, GM112690)
  • National Cancer Institute (CA185404)
  • Damon Runyon Cancer Research Foundation (DRG 2157-12)
  • Research Fellowship of the Deutsche Forschungsgemeinschaft (Postdoctoral Fellowship)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Keywords
membrane tension, neutrophil migration, chemotaxis, actin polymerization, actin nucleation, phospholipase D2, mTORC2, mechanosensing, cell polarity, leading edge, protrusions, negative feedback loop, mathematical modeling
MeSH terms
Mechanistic Target of Rapamycin Complex 2, Actins, Cell Membrane, Cell Movement, Humans, Actin Cytoskeleton, Microscopy, Fluorescence, Models, Biological, Neutrophils, Phospholipase D, Blotting, Western, Cell Polarity, HL-60 Cells, RNA Interference, Mechanotransduction, Cellular, Multiprotein Complexes, HEK293 Cells, Polymerization, TOR Serine-Threonine Kinases

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