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Feedback Regulation Between Plasma Membrane Tension and Membrane-bending Proteins Organizes Cell Polarity During Leading Edge Formation

Overview
Journal Nat Cell Biol
Specialty Cell Biology
Date 2015 May 5
PMID 25938814
Citations 75
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Abstract

Tension applied to the plasma membrane (PM) is a global mechanical parameter involved in cell migration. However, how membrane tension regulates actin assembly is unknown. Here, we demonstrate that FBP17, a membrane-bending protein and an activator of WASP/N-WASP-dependent actin nucleation, is a PM tension sensor involved in leading edge formation. In migrating cells, FBP17 localizes to short membrane invaginations at the leading edge, while diminishing from the cell rear in response to PM tension increase. Conversely, following reduced PM tension, FBP17 dots randomly distribute throughout the cell, correlating with loss of polarized actin assembly on PM tension reduction. Actin protrusive force is required for the polarized accumulation, indicating a role for FBP17-mediated activation of WASP/N-WASP in PM tension generation. In vitro experiments show that FBP17 membrane-bending activity depends on liposomal membrane tension. Thus, FBP17 is the local activator of actin polymerization that is inhibited by PM tension in the feedback loop that regulates cell migration.

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References
1.
Graziano B, Weiner O . Self-organization of protrusions and polarity during eukaryotic chemotaxis. Curr Opin Cell Biol. 2014; 30:60-7. PMC: 4177965. DOI: 10.1016/j.ceb.2014.06.007. View

2.
Itoh T, Erdmann K, Roux A, Habermann B, Werner H, De Camilli P . Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell. 2005; 9(6):791-804. DOI: 10.1016/j.devcel.2005.11.005. View

3.
Weiner O, Marganski W, Wu L, Altschuler S, Kirschner M . An actin-based wave generator organizes cell motility. PLoS Biol. 2007; 5(9):e221. PMC: 1945041. DOI: 10.1371/journal.pbio.0050221. View

4.
Chander H, Truesdell P, Meens J, Craig A . Transducer of Cdc42-dependent actin assembly promotes breast cancer invasion and metastasis. Oncogene. 2012; 32(25):3080-90. DOI: 10.1038/onc.2012.317. View

5.
Malet-Engra G, Viaud J, Ysebaert L, Farce M, Lafouresse F, Laurent G . CIP4 controls CCL19-driven cell steering and chemotaxis in chronic lymphocytic leukemia. Cancer Res. 2013; 73(11):3412-24. DOI: 10.1158/0008-5472.CAN-12-3564. View