Crossref journal-article
Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences (341)
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.

Bibliography

Maly, I. V., & Borisy, G. G. (2001). Self-organization of a propulsive actin network as an evolutionary process. Proceedings of the National Academy of Sciences, 98(20), 11324–11329.

Authors 2
  1. Ivan V. Maly (first)
  2. Gary G. Borisy (additional)
References 29 Referenced 119
  1. 10.1146/annurev.biophys.29.1.545
  2. 10.1083/jcb.129.5.1275
  3. 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)
  4. 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)
  5. 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)
  6. 10.1038/35006635
  7. 10.1126/science.291.5501.114
  8. 10.1073/pnas.95.11.6181
  9. 10.1083/jcb.145.5.1009
  10. 10.1016/S0955-0674(99)00063-0
  11. 10.1038/35010008
  12. 10.1016/S0006-3495(96)79496-1
  13. 10.1016/S0960-9822(98)00015-3
  14. 10.1016/S0092-8674(00)80732-1
  15. 10.1016/S0960-9822(99)80243-7
  16. 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)
  17. 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)
  18. E Reif Fundamentals of Statistical and Thermal Physics (McGraw–Hill, New York, 1965). / Fundamentals of Statistical and Thermal Physics by Reif E (1965)
  19. 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)
  20. J V Small, J E Celis Eur J Cell Biol 16, 308–325 (1978). / Eur J Cell Biol by Small J V (1978)
  21. 10.1016/S0006-3495(99)77018-9
  22. 10.1007/978-1-4757-1463-0
  23. 10.1007/978-1-4471-1940-1
  24. 10.1109/TPAMI.1986.4767851
  25. 10.1083/jcb.135.1.169
  26. 10.1083/jcb.130.2.331
  27. 10.1083/jcb.103.6.2747
  28. 10.1038/347044a0
  29. 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)
Funders 0

None

@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} }