Dendritic Actin Filament Nucleation Causes Traveling Waves and Patches

Overview

Journal Phys Rev Lett

Publisher American Physical Society

Specialty Biophysics

Date 2010 Sep 28

PMID 20867207

Citations 30

Authors

Anders E Carlsson

Affiliations

Soon will be listed here.

Abstract

The polymerization of actin via branching at a cell membrane containing nucleation-promoting factors is simulated using a stochastic-growth methodology. The polymerized-actin distribution displays three types of behavior: (a) traveling waves, (b) moving patches, and (c) random fluctuations. Increasing actin concentration causes a transition from patches to waves. The waves and patches move by a treadmilling mechanism not involving myosin II. The effects of downregulation of key proteins on actin wave behavior are evaluated.

Citing Articles

Supramolecular fibrillation in coacervates and other confined systems towards biomimetic function.

Sanchez-Fernandez A, Insua I, Montenegro J Commun Chem. 2024; 7(1):223.

PMID: 39349583 PMC: 11442845. DOI: 10.1038/s42004-024-01308-x.

Supramolecular fibrillation of peptide amphiphiles induces environmental responses in aqueous droplets.

Booth R, Insua I, Ahmed S, Rioboo A, Montenegro J Nat Commun. 2021; 12(1):6421.

PMID: 34741043 PMC: 8571317. DOI: 10.1038/s41467-021-26681-2.

Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality.

Bonilla-Quintana M, Worgotter F, DEste E, Tetzlaff C, Fauth M Sci Rep. 2021; 11(1):4012.

PMID: 33597561 PMC: 7889935. DOI: 10.1038/s41598-021-83331-9.

Why a Large-Scale Mode Can Be Essential for Understanding Intracellular Actin Waves.

Beta C, Gov N, Yochelis A Cells. 2020; 9(6).

PMID: 32585983 PMC: 7349605. DOI: 10.3390/cells9061533.

Quasi-periodic migration of single cells on short microlanes.

Zhou F, Schaffer S, Schreiber C, Segerer F, Goychuk A, Frey E PLoS One. 2020; 15(4):e0230679.

PMID: 32282802 PMC: 7153896. DOI: 10.1371/journal.pone.0230679.

References

Vicker M . Eukaryotic cell locomotion depends on the propagation of self-organized reaction-diffusion waves and oscillations of actin filament assembly. Exp Cell Res. 2002; 275(1):54-66. DOI: 10.1006/excr.2001.5466. View

Pantaloni D, Boujemaa R, Didry D, Gounon P, Carlier M . The Arp2/3 complex branches filament barbed ends: functional antagonism with capping proteins. Nat Cell Biol. 2000; 2(7):385-91. DOI: 10.1038/35017011. View

Yamaguchi H, Condeelis J . Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta. 2006; 1773(5):642-52. PMC: 4266238. DOI: 10.1016/j.bbamcr.2006.07.001. View

Pollard T, Borisy G . Cellular motility driven by assembly and disassembly of actin filaments. Cell. 2003; 112(4):453-65. DOI: 10.1016/s0092-8674(03)00120-x. View

Carlsson A . Growth of branched actin networks against obstacles. Biophys J. 2001; 81(4):1907-23. PMC: 1301666. DOI: 10.1016/S0006-3495(01)75842-0. View

Bretschneider T, Anderson K, Ecke M, Muller-Taubenberger A, Schroth-Diez B, Ishikawa-Ankerhold H . The three-dimensional dynamics of actin waves, a model of cytoskeletal self-organization. Biophys J. 2009; 96(7):2888-900. PMC: 3325131. DOI: 10.1016/j.bpj.2008.12.3942. View

Carlsson A . Growth velocities of branched actin networks. Biophys J. 2003; 84(5):2907-18. PMC: 1302854. DOI: 10.1016/S0006-3495(03)70018-6. View

Whitelam S, Bretschneider T, Burroughs N . Transformation from spots to waves in a model of actin pattern formation. Phys Rev Lett. 2009; 102(19):198103. DOI: 10.1103/PhysRevLett.102.198103. View

Gerisch G, Bretschneider T, Muller-Taubenberger A, Simmeth E, Ecke M, Diez S . Mobile actin clusters and traveling waves in cells recovering from actin depolymerization. Biophys J. 2004; 87(5):3493-503. PMC: 1304815. DOI: 10.1529/biophysj.104.047589. View

10.

Guyader H, Hyver C . Periodic activity of the cortical cytoskeleton of the lymphoblast: modelling by a reaction-diffusion system. C R Acad Sci III. 1997; 320(1):59-65. DOI: 10.1016/s0764-4469(99)80087-0. View

11.

Krischer , MIKHAILOV . Bifurcation to traveling spots in reaction-diffusion systems. Phys Rev Lett. 1994; 73(23):3165-3168. DOI: 10.1103/PhysRevLett.73.3165. View

12.

Hug C, Jay P, Reddy I, McNally J, Bridgman P, Elson E . Capping protein levels influence actin assembly and cell motility in dictyostelium. Cell. 1995; 81(4):591-600. DOI: 10.1016/0092-8674(95)90080-2. View

13.

Vicker M . F-actin assembly in Dictyostelium cell locomotion and shape oscillations propagates as a self-organized reaction-diffusion wave. FEBS Lett. 2002; 510(1-2):5-9. DOI: 10.1016/s0014-5793(01)03207-0. View

14.

Young M, Cooper J, Bridgman P . Yeast actin patches are networks of branched actin filaments. J Cell Biol. 2004; 166(5):629-35. PMC: 2172413. DOI: 10.1083/jcb.200404159. View

15.

Akin O, Mullins R . Capping protein increases the rate of actin-based motility by promoting filament nucleation by the Arp2/3 complex. Cell. 2008; 133(5):841-51. PMC: 2576297. DOI: 10.1016/j.cell.2008.04.011. View

16.

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

17.

Mullins R, Heuser J, Pollard T . The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci U S A. 1998; 95(11):6181-6. PMC: 27619. DOI: 10.1073/pnas.95.11.6181. View

18.

Samarin S, Romero S, Kocks C, Didry D, Pantaloni D, Carlier M . How VASP enhances actin-based motility. J Cell Biol. 2003; 163(1):131-42. PMC: 2173428. DOI: 10.1083/jcb.200303191. View

19.

Bretschneider T, Diez S, Anderson K, Heuser J, Clarke M, Muller-Taubenberger A . Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. Curr Biol. 2004; 14(1):1-10. DOI: 10.1016/j.cub.2003.12.005. View

20.

Padrick S, Cheng H, Ismail A, Panchal S, Doolittle L, Kim S . Hierarchical regulation of WASP/WAVE proteins. Mol Cell. 2008; 32(3):426-38. PMC: 2680354. DOI: 10.1016/j.molcel.2008.10.012. View