Home LiteratureArticle Details
PMID: 17440042 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Self-organization of actin filament orientation in the dendritic-nucleation/array-treadmilling model.

Schaus TE, Taylor EW, Borisy GG

Abstract

The dendritic-nucleation/array-treadmilling model provides a conceptual framework for the generation of the actin network driving motile cells. We have incorporated it into a 2D, stochastic computer model to study lamellipodia via the self-organization of filament orientation patterns. Essential dendritic-nucleation submodels were incorporated, including discretized actin monomer diffusion, Monte-Carlo filament kinetics, and flexible filament and plasma membrane mechanics. Model parameters were estimated from the literature and simulation, providing values for the extent of the leading edge-branching/capping-protective zone (5.4 nm) and the autocatalytic branch rate (0.43/sec). For a given set of parameters, the system evolved to a steady-state filament count and velocity, at which total branching and capping rates were equal only for specific orientations; net capping eliminated others. The standard parameter set evoked a sharp preference for the +/-35 degree filaments seen in lamellipodial electron micrographs, requiring approximately 12 generations of successive branching to adapt to a 15 degree change in protrusion direction. This pattern was robust with respect to membrane surface and bending energies and to actin concentrations but required protection from capping at the leading edge and branching angles >60 degrees. A +70/0/-70 degree pattern was formed with flexible filaments approximately 100 nm or longer and with velocities < approximately 20% of free polymerization rates.

MeSH Terms
Actin Cytoskeleton/chemistry,metabolism Biological Evolution Biopolymers/chemistry,metabolism Computer Simulation Dendrites/chemistry,metabolism Diffusion Models, Biological Pseudopodia/chemistry,metabolism
Chemicals
Biopolymers
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Schaus Thomas E
Department of Cell and Molecular Biology, Northwestern University Feinberg School of Medicine, 303 East Chicago Avenue, Chicago, IL 60611, USA.
Taylor Edwin W
Borisy Gary G
References (26)
26 references, click to expand
  1. Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins.
    Nature. 2000 Apr 27;404(6781):1007-11 PMID: 10801131
  2. Protein complexes regulating Arp2/3-mediated actin assembly.
    Curr Opin Cell Biol. 2006 Feb;18(1):4-10 PMID: 16343889
  3. Growth of branched actin networks against obstacles.
    Biophys J. 2001 Oct;81(4):1907-23 PMID: 11566765
  4. Self-organization of a propulsive actin network as an evolutionary process.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11324-9 PMID: 11572984
  5. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility.
    Cell. 2002 May 17;109(4):509-21 PMID: 12086607
  6. Cellular motility driven by assembly and disassembly of actin filaments.
    Cell. 2003 Feb 21;112(4):453-65 PMID: 12600310
  7. Force generation by actin polymerization II: the elastic ratchet and tethered filaments.
    Biophys J. 2003 Mar;84(3):1591-605 PMID: 12609863
  8. Growth velocities of branched actin networks.
    Biophys J. 2003 May;84(5):2907-18 PMID: 12719223
  9. How capping protein binds the barbed end of the actin filament.
    Curr Biol. 2003 Sep 2;13(17):1531-7 PMID: 12956956
  10. Orientational order of the lamellipodial actin network as demonstrated in living motile cells.
    Mol Biol Cell. 2003 Nov;14(11):4667-75 PMID: 13679520
  11. Engineering complex systems.
    Nature. 2004 Jan 29;427(6973):399 PMID: 14749808
  12. Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end.
    Cell. 2004 Aug 6;118(3):363-73 PMID: 15294161
  13. Quantitative analysis of the effect of Acanthamoeba profilin on actin filament nucleation and elongation.
    Biochemistry. 1984 Dec 18;23(26):6631-41 PMID: 6543322
  14. Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments.
    J Cell Biol. 1986 Dec;103(6 Pt 2):2747-54 PMID: 3793756
  15. Morphological changes in liposomes caused by polymerization of encapsulated actin and spontaneous formation of actin bundles.
    Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11547-51 PMID: 1454846
  16. Flexibility of actin filaments derived from thermal fluctuations. Effect of bound nucleotide, phalloidin, and muscle regulatory proteins.
    J Biol Chem. 1995 May 12;270(19):11437-44 PMID: 7744781
  17. Dynamics of capping protein and actin assembly in vitro: uncapping barbed ends by polyphosphoinositides.
    J Cell Biol. 1996 Oct;135(1):169-79 PMID: 8858171
  18. Cell motility driven by actin polymerization.
    Biophys J. 1996 Dec;71(6):3030-45 PMID: 8968574
  19. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility.
    J Cell Biol. 1997 Mar 24;136(6):1307-22 PMID: 9087445
  20. 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 May 26;95(11):6181-6 PMID: 9600938
  21. Simultaneous measurements of actin filament turnover, filament fraction, and monomer diffusion in endothelial cells.
    Biophys J. 1998 Oct;75(4):2070-8 PMID: 9746549
  22. Mechanism of interaction of Acanthamoeba actophorin (ADF/Cofilin) with actin filaments.
    J Biol Chem. 1999 May 28;274(22):15538-46 PMID: 10336448
  23. The actin-based nanomachine at the leading edge of migrating cells.
    Biophys J. 1999 Sep;77(3):1721-32 PMID: 10465781
  24. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins.
    Nature. 1999 Oct 7;401(6753):613-6 PMID: 10524632
  25. Morphology of the lamellipodium and organization of actin filaments at the leading edge of crawling cells.
    Biophys J. 2005 Nov;89(5):3589-602 PMID: 16085776
  26. Interactions of ADF/cofilin, Arp2/3 complex, capping protein and profilin in remodeling of branched actin filament networks.
    Curr Biol. 2000 Oct 19;10(20):1273-82 PMID: 11069108
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2007-04-24
Epub
2007-00-17
Pages
7086-91
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1855413
Subset
IM
Grants
NIGMS NIH HHS · R01 GM062431 · United States
NIGMS NIH HHS · GM 62431 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com