Self-organization of a propulsive actin network as an evolutionary process

Area of Science:

• Cell Biology
• Biophysics
• Systems Biology

Background:

• The leading edge of motile cells uses actin filament polymerization for propulsion via dendritic nucleation and array treadmilling.
• The origin and maintenance of these dendritic actin networks remain poorly understood.

Purpose of the Study:

• To develop and test a population-kinetics model explaining actin filament organization through the reproduction of dendritic units.
• To investigate the role of natural selection in shaping actin network patterns based on filament orientation.

Main Methods:

• Developed a population-kinetics model where actin filament life cycles (birth, elongation, death) are influenced by orientation.
• Introduced concepts of heredity and mutation (orientation errors) within filament lineages.
• Utilized a Radon transform-based procedure for quantitative in situ analysis of actin networks.

Main Results:

• The model predicts that differential reproduction and elimination of filaments based on orientation lead to a characteristic distribution of filament orientations.
• Experimental results align with the model's predictions for filament orientation distributions.
• Demonstrated that actin networks can be viewed as self-organizing ensembles shaped by evolutionary principles.

Conclusions:

• The organization of propulsive actin networks can be understood through the evolution of dendritic lineages via natural selection of filament orientation.
• Filament orientation acts as a selectable trait, driving the self-organization of the actin cytoskeleton.
• This evolutionary framework provides a novel perspective on the structure and function of cellular motility machinery.