Abstract
The leading edge of motile cells is propelled by polymerization of actin filaments according to a dendritic nucleation/array treadmilling mechanism. However, little attention has been given to the origin and maintenance of the dendritic array. Here we develop and test a population–kinetics model that explains the organization of actin filaments in terms of the reproduction of dendritic units. The life cycle of an actin filament consists of dendritic nucleation on another filament (birth), elongation by addition of actin subunits and, finally, termination of filament growth by capping protein (death). The regularity of branch angle between daughter and mother filaments endows filaments with heredity of their orientation. Fluctuations of branch angle that become fixed in the actin network create errors of orientation (mutations) that may be inherited. In our model, birth and death rates depend on filament orientation, which then becomes a selectable trait. Differential reproduction and elimination of filaments, or natural selection, leads to the evolution of a filament pattern with a characteristic distribution of filament orientations. We develop a procedure based on the Radon transform for quantitatively analyzing actin networksin situand show that the experimental results are in agreement with the distribution of filament orientations predicted by our model. We conclude that the propulsive actin network can be understood as a self-organizing supramolecular ensemble shaped by the evolution of dendritic lineages through natural selection of their orientation.
References
29
Referenced
119
10.1146/annurev.biophys.29.1.545
10.1083/jcb.129.5.1275
- R E Michod Darwinian Dynamics: Evolutionary Transitions in Fitness and Individuality (Princeton Univ. Press, Princeton, NJ, 1999). / Darwinian Dynamics: Evolutionary Transitions in Fitness and Individuality by Michod R E (1999)
- V Grant The Evolutionary Process: A Critical Review of Evolutionary Theory (Columbia Univ. Press, New York, 1985). / The Evolutionary Process: A Critical Review of Evolutionary Theory by Grant V (1985)
-
G W Rowe Theoretical Models in Biology: The Origin of Life, the Immune System, and the Brain (Oxford Univ. Press, New York, 1994).
(
10.1093/oso/9780198596882.001.0001
) / Theoretical Models in Biology: The Origin of Life, the Immune System, and the Brain by Rowe G W (1994) 10.1038/35006635
10.1126/science.291.5501.114
10.1073/pnas.95.11.6181
10.1083/jcb.145.5.1009
10.1016/S0955-0674(99)00063-0
10.1038/35010008
10.1016/S0006-3495(96)79496-1
10.1016/S0960-9822(98)00015-3
10.1016/S0092-8674(00)80732-1
10.1016/S0960-9822(99)80243-7
-
R A Fisher The Genetical Theory of Natural Selection (Oxford Univ. Press, Oxford, U.K., 1999).
(
10.1093/oso/9780198504405.001.0001
) / The Genetical Theory of Natural Selection by Fisher R A (1999) - J F Crow, M Kimura An Introduction to Population Genetics Theory (Harper & Row, New York, 1970). / An Introduction to Population Genetics Theory by Crow J F (1970)
- E Reif Fundamentals of Statistical and Thermal Physics (McGraw–Hill, New York, 1965). / Fundamentals of Statistical and Thermal Physics by Reif E (1965)
- C T H Baker The Numerical Treatment of Integral Equations (Clarendon Press, Oxford, U.K., 1977). / The Numerical Treatment of Integral Equations by Baker C T H (1977)
- J V Small, J E Celis Eur J Cell Biol 16, 308–325 (1978). / Eur J Cell Biol by Small J V (1978)
10.1016/S0006-3495(99)77018-9
10.1007/978-1-4757-1463-0
10.1007/978-1-4471-1940-1
10.1109/TPAMI.1986.4767851
10.1083/jcb.135.1.169
10.1083/jcb.130.2.331
10.1083/jcb.103.6.2747
10.1038/347044a0
10.1038/362167a0
Dates
Type | When |
---|---|
Created | 23 years, 1 month ago (July 26, 2002, 10:34 a.m.) |
Deposited | 1 year, 7 months ago (Jan. 3, 2024, 11:48 p.m.) |
Indexed | 2 months, 3 weeks ago (June 5, 2025, 6:48 a.m.) |
Issued | 23 years, 11 months ago (Sept. 25, 2001) |
Published | 23 years, 11 months ago (Sept. 25, 2001) |
Published Online | 23 years, 11 months ago (Sept. 25, 2001) |
Published Print | 23 years, 11 months ago (Sept. 25, 2001) |
@article{Maly_2001, title={Self-organization of a propulsive actin network as an evolutionary process}, volume={98}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.181338798}, DOI={10.1073/pnas.181338798}, number={20}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Maly, Ivan V. and Borisy, Gary G.}, year={2001}, month=sep, pages={11324–11329} }