The Bimodal Role of Filamin in Controlling the Architecture and Mechanics of F-actin Networks

Yiider Tseng, Kwang M. An, Osigwe Esue, Denis Wirtz

Research output: Contribution to journalArticle

Abstract

Reconstituted actin filament networks have been used extensively to understand the mechanics of the actin cortex and decipher the role of actin cross-linking proteins in the maintenance and deformation of cell shape. However, studies of the mechanical role of the F-actin cross-linking protein filamin have led to seemingly contradictory conclusions, in part due to the use of ill-defined mechanical assays. Using quantitative rheological methods that avoid the pitfalls of previous studies, we systematically tested the complex mechanical response of reconstituted actin filament networks containing a wide range of filamin concentrations and compared the mechanical function of filamin with that of the cross-linking/bundling proteins α-actinin and fascin. At steady state and within a well defined linear regime of small non-destructive deformations, F-actin solutions behave as highly dynamic networks (actin polymers are still sufficiently mobile to relax the stress) below the cross-linking-to-bundling threshold filamin concentration, and they behave as covalently cross-linked gels above that threshold. Under large deformations, F-actin networks soften at low filamin concentrations and strain-harden at high filamin concentrations. Filamin cross-links F-actin into networks that are more resilient, stiffer, more solid-like, and less dynamic than α-actinin and fascin. These results resolve the controversy by showing that F-actin/filamin networks can adopt diametrically opposed rheological behaviors depending on the concentration in cross-linking proteins.

Original languageEnglish (US)
Pages (from-to)1819-1826
Number of pages8
JournalJournal of Biological Chemistry
Volume279
Issue number3
DOIs
StatePublished - Jan 16 2004

Fingerprint

Filamins
Mechanics
Actins
Actinin
Actin Cytoskeleton
Proteins
Cell Shape
Polymers
Gels
Maintenance
Assays

ASJC Scopus subject areas

  • Biochemistry

Cite this

The Bimodal Role of Filamin in Controlling the Architecture and Mechanics of F-actin Networks. / Tseng, Yiider; An, Kwang M.; Esue, Osigwe; Wirtz, Denis.

In: Journal of Biological Chemistry, Vol. 279, No. 3, 16.01.2004, p. 1819-1826.

Research output: Contribution to journalArticle

Tseng, Yiider ; An, Kwang M. ; Esue, Osigwe ; Wirtz, Denis. / The Bimodal Role of Filamin in Controlling the Architecture and Mechanics of F-actin Networks. In: Journal of Biological Chemistry. 2004 ; Vol. 279, No. 3. pp. 1819-1826.
@article{82574b17d48c4a78a958a4705f14854d,
title = "The Bimodal Role of Filamin in Controlling the Architecture and Mechanics of F-actin Networks",
abstract = "Reconstituted actin filament networks have been used extensively to understand the mechanics of the actin cortex and decipher the role of actin cross-linking proteins in the maintenance and deformation of cell shape. However, studies of the mechanical role of the F-actin cross-linking protein filamin have led to seemingly contradictory conclusions, in part due to the use of ill-defined mechanical assays. Using quantitative rheological methods that avoid the pitfalls of previous studies, we systematically tested the complex mechanical response of reconstituted actin filament networks containing a wide range of filamin concentrations and compared the mechanical function of filamin with that of the cross-linking/bundling proteins α-actinin and fascin. At steady state and within a well defined linear regime of small non-destructive deformations, F-actin solutions behave as highly dynamic networks (actin polymers are still sufficiently mobile to relax the stress) below the cross-linking-to-bundling threshold filamin concentration, and they behave as covalently cross-linked gels above that threshold. Under large deformations, F-actin networks soften at low filamin concentrations and strain-harden at high filamin concentrations. Filamin cross-links F-actin into networks that are more resilient, stiffer, more solid-like, and less dynamic than α-actinin and fascin. These results resolve the controversy by showing that F-actin/filamin networks can adopt diametrically opposed rheological behaviors depending on the concentration in cross-linking proteins.",
author = "Yiider Tseng and An, {Kwang M.} and Osigwe Esue and Denis Wirtz",
year = "2004",
month = "1",
day = "16",
doi = "10.1074/jbc.M306090200",
language = "English (US)",
volume = "279",
pages = "1819--1826",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "3",

}

TY - JOUR

T1 - The Bimodal Role of Filamin in Controlling the Architecture and Mechanics of F-actin Networks

AU - Tseng, Yiider

AU - An, Kwang M.

AU - Esue, Osigwe

AU - Wirtz, Denis

PY - 2004/1/16

Y1 - 2004/1/16

N2 - Reconstituted actin filament networks have been used extensively to understand the mechanics of the actin cortex and decipher the role of actin cross-linking proteins in the maintenance and deformation of cell shape. However, studies of the mechanical role of the F-actin cross-linking protein filamin have led to seemingly contradictory conclusions, in part due to the use of ill-defined mechanical assays. Using quantitative rheological methods that avoid the pitfalls of previous studies, we systematically tested the complex mechanical response of reconstituted actin filament networks containing a wide range of filamin concentrations and compared the mechanical function of filamin with that of the cross-linking/bundling proteins α-actinin and fascin. At steady state and within a well defined linear regime of small non-destructive deformations, F-actin solutions behave as highly dynamic networks (actin polymers are still sufficiently mobile to relax the stress) below the cross-linking-to-bundling threshold filamin concentration, and they behave as covalently cross-linked gels above that threshold. Under large deformations, F-actin networks soften at low filamin concentrations and strain-harden at high filamin concentrations. Filamin cross-links F-actin into networks that are more resilient, stiffer, more solid-like, and less dynamic than α-actinin and fascin. These results resolve the controversy by showing that F-actin/filamin networks can adopt diametrically opposed rheological behaviors depending on the concentration in cross-linking proteins.

AB - Reconstituted actin filament networks have been used extensively to understand the mechanics of the actin cortex and decipher the role of actin cross-linking proteins in the maintenance and deformation of cell shape. However, studies of the mechanical role of the F-actin cross-linking protein filamin have led to seemingly contradictory conclusions, in part due to the use of ill-defined mechanical assays. Using quantitative rheological methods that avoid the pitfalls of previous studies, we systematically tested the complex mechanical response of reconstituted actin filament networks containing a wide range of filamin concentrations and compared the mechanical function of filamin with that of the cross-linking/bundling proteins α-actinin and fascin. At steady state and within a well defined linear regime of small non-destructive deformations, F-actin solutions behave as highly dynamic networks (actin polymers are still sufficiently mobile to relax the stress) below the cross-linking-to-bundling threshold filamin concentration, and they behave as covalently cross-linked gels above that threshold. Under large deformations, F-actin networks soften at low filamin concentrations and strain-harden at high filamin concentrations. Filamin cross-links F-actin into networks that are more resilient, stiffer, more solid-like, and less dynamic than α-actinin and fascin. These results resolve the controversy by showing that F-actin/filamin networks can adopt diametrically opposed rheological behaviors depending on the concentration in cross-linking proteins.

UR - http://www.scopus.com/inward/record.url?scp=0347087487&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0347087487&partnerID=8YFLogxK

U2 - 10.1074/jbc.M306090200

DO - 10.1074/jbc.M306090200

M3 - Article

C2 - 14594947

AN - SCOPUS:0347087487

VL - 279

SP - 1819

EP - 1826

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 3

ER -