Published October 14, 2022 | Version v1
Journal article Open

Activated I-BAR IRSp53 clustering controls the formation of VASP-actin–based membrane protrusions

Description

Filopodia are actin-rich membrane protrusions essential for cell morphogenesis, motility, and cancer invasion. How cells control filopodium initiation on the plasma membrane remains elusive. We performed experiments in cellulo, in vitro, and in silico to unravel the mechanism of filopodium initiation driven by the membrane curvature sensor IRSp53 (insulin receptor substrate protein of 53 kDa). We showed that full-length IRSp53 self-assembles into clusters on membranes depending on PIP2. Using well-controlled in vitro reconstitution systems, we demonstrated that IRSp53 clusters recruit the actin polymerase VASP (vasodilator-stimulated phosphoprotein) to assemble actin filaments locally on membranes, leading to the generation of actin-filled membrane protrusions reminiscent of filopodia. By pulling membrane nanotubes from live cells, we observed that IRSp53 can only be enriched and trigger actin assembly in nanotubes at highly dynamic membrane regions. Our work supports a regulation mechanism of IRSp53 in its attributes of curvature sensation and partner recruitment to ensure a precise spatial-temporal control of filopodium initiation.

Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials.

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Additional details

Identifiers

DOI
10.1126/sciadv.abp8677
Other
oai:uchicago.tind.io:10910

Funding

National Institute of General Medical Sciences
R01-GM063796
Takeda Science Foundation
European Commission
RGP0005/2016
Wesco Science Foundation
Marie Curie Actions
H2020-MSCA-IF-2014
EMBO
long-term fellowship
Human Frontier Science Program
RGP0005/2016
Institut Curie and the Centre National de la Recherche Scientifique
Agence Nationale Pour La Recherche
ANR-20-CE13-0032
Université Paris Sciences et Lettres-QLife Institute
ANR-17-CONV-0005 Q-LIFE
Agence Nationale Pour La Recherche
ANR-18-CE13-0026-01
Agence Nationale Pour La Recherche
ANR-21-CE13-0010-03
Cancer Society Finland
4705949
Japan Society for the Promotion of Science and Academy of Finland
FY 2015 Researcher Exchange Program
Wesco Scientific Promotion Foundation
Pasteur Foundation
Fellowship

UChicago Information

Division(s)
Physical Sciences Division, Pritzker School of Molecular Engineering
Department(s)
Chemistry
Center(s) or Institute(s)
Institute for Biophysical Dynamics, James Franck Institute