Balancing limited resources in actin network competition

被引:3
作者
Guerin, Christophe [1 ]
N'Diaye, Anne-Betty [1 ]
Gressin, Laurene [1 ]
Mogilner, Alex [2 ,3 ]
Thery, Manuel [4 ]
Blanchoin, Laurent [1 ,4 ]
Colin, Alexandra [1 ]
机构
[1] Univ Grenoble Alpes, Lab Physiol Cellulaire & Vegetale, Interdisciplinary Res Inst Grenoble, CEA,CNRS,INRA,Cytomorpholab, 17 Ave Martyrs, F-38054 Grenoble, France
[2] NYU, Courant Inst Math Sci, 251 Mercer St, New York, NY 10012 USA
[3] NYU, Dept Biol, 251 Mercer St, New York, NY 10012 USA
[4] Univ Paris Sci & Lettres, Inst Chim Biol Innovat, Inst Pierre Gilles Gennes, Cytomorpholab,CEA,ESPCI, 6 Rue Jean Calvin, F-75005 Paris, France
基金
欧洲研究理事会;
关键词
CELL COMPETITION; ARP2/3; COMPLEX; DYNAMICS; MOTILITY; YEAST; CYTOSKELETON; FILAMENTS; PROFILIN; REVEALS; MAINTENANCE;
D O I
10.1016/j.cub.2024.11.067
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
In cells, multiple actin networks coexist in a dynamic manner. These networks compete for a common pool of actin monomers and actin-binding proteins. Interestingly, all of these networks manage to coexist despite the strong competition for resources. Moreover, the coexistence of networks with various strengths is key to cell adaptation to external changes. However, a comprehensive view of how these networks coexist in this competitive environment, where resources are limited, is still lacking. To address this question, we used a reconstituted system, in closed microwells, consisting of beads propelled by actin polymerization or micro- patterns functionalized with lipids capable of initiating polymerization close to a membrane. This system enabled us to build dynamic actin architectures, competing for a limited pool of proteins, over a period of hours. We demonstrated the importance of protein turnover for the coexistence of actin networks, showing that it ensures resource distribution between weak and strong networks. However, when competition becomes too intense, turnover alone is insufficient, leading to a selection process that favors the strongest networks. Consequently, we emphasize the importance of competition strength, which is defined by the turnover rate, the amount of available protein, and the number of competing structures. More generally, this work illustrates how turnover allows biological populations with various competition strengths to coexist despite resource constraints.
引用
收藏
页码:500 / 513.e5
页数:20
相关论文
共 102 条
[1]   A "Primer"-Based Mechanism Underlies Branched Actin Filament Network Formation and Motility [J].
Achard, Verane ;
Martiel, Jean-Louis ;
Michelot, Alphee ;
Guerin, Christophe ;
Reymann, Anne-Cecile ;
Blanchoin, Laurent ;
Boujemaa-Paterski, Rajaa .
CURRENT BIOLOGY, 2010, 20 (05) :423-428
[2]   Capping protein increases the rate of actin-based motility by promoting filament nucleation by the Arp2/3 complex [J].
Akin, Orkun ;
Mullins, R. Dyche .
CELL, 2008, 133 (05) :841-851
[3]   PURIFICATION, CHARACTERIZATION AND CRYSTALLIZATION OF ACANTHAMOEBA PROFILIN EXPRESSED IN ESCHERICHIA-COLI [J].
ALMO, SC ;
POLLARD, TD ;
WAY, M ;
LATTMAN, EE .
JOURNAL OF MOLECULAR BIOLOGY, 1994, 236 (03) :950-952
[4]   Resource allocation in mammalian systems [J].
Baghdassarian, Hratch M. ;
Lewis, Nathan E. .
BIOTECHNOLOGY ADVANCES, 2024, 71
[5]   Size regulation of multiple organelles competing for a limiting subunit pool [J].
Banerjee, Deb Sankar ;
Banerjee, Shiladitya .
PLOS COMPUTATIONAL BIOLOGY, 2022, 18 (06)
[6]   Emergence and maintenance of variable-length actin filaments in a limiting pool of building blocks [J].
Banerjee, Deb Sankar ;
Banerjee, Shiladitya .
BIOPHYSICAL JOURNAL, 2022, 121 (12) :2436-2448
[7]   γ-Actin is required for cytoskeletal maintenance but not development [J].
Belyantseva, Inna A. ;
Perrin, Benjamin J. ;
Sonnemann, Kevin J. ;
Zhu, Mei ;
Stepanyan, Ruben ;
McGee, JoAnn ;
Frolenkov, Gregory I. ;
Walsh, Edward J. ;
Friderici, Karen H. ;
Friedman, Thomas B. ;
Ervasti, James M. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2009, 106 (24) :9703-9708
[8]   The dynamics of actin-based motility depend on surface parameters [J].
Bernheim-Groswasser, A ;
Wiesner, S ;
Golsteyn, RM ;
Carlier, MF ;
Sykes, C .
NATURE, 2002, 417 (6886) :308-311
[9]   Force Feedback Controls Motor Activity and Mechanical Properties of Self-Assembling Branched Actin Networks [J].
Bieling, Peter ;
Li, Tai-De ;
Weichsel, Julian ;
McGorty, Ryan ;
Jreij, Pamela ;
Huang, Bo ;
Fletcher, Daniel A. ;
Mullins, R. Dyche .
CELL, 2016, 164 (1-2) :115-127
[10]   Capping Protein Insulates Arp2/3-Assembled Actin Patches from Formins [J].
Billault-Chaumartin, Ingrid ;
Martin, Sophie G. .
CURRENT BIOLOGY, 2019, 29 (19) :3165-+