Collective dynamics of processive cytoskeletal motors

Abstract

Major cellular processes are supported by various biomolecular motors that usually operate together as teams. We present an overview of the collective dynamics of processive cytokeletal motor proteins based on recent experimental and theoretical investigations. Experimental studies show that multiple motors function with different degrees of cooperativity, ranging from negative to positive. This effect depends on the mechanical properties of individual motors, the geometry of their connections, and the surrounding cellular environment. Theoretical models based on stochastic approaches underline the importance of intermolecular interactions, the properties of single motors, and couplings with cellular medium in predicting the collective dynamics. We discuss several features that specify the cooperativity in motor proteins. Based on this approach a general picture of collective dynamics of motor proteins is formulated, and the future directions and challenges are discussed.

Fig. 1

A schematic view of synthetically engineered complexes of two myosin V motor proteins. A DNA linker system consisting of a short 50nm segment of double-stranded DNA and polymer connectors at both ends couples two molecular motors. Each motor protein molecule is bound to a quantum dot of different color, which helps to comprehensively monitor the dynamics of the system. Adapted with permission from Ref.

Fig. 2

Distributions of maximal observed forces before the detachment for single kinesins (top) and for two-kinesin assemblies (bottom). Adapted with permission from Ref.

Fig. 3

A fraction of time the cellular load is driven by one (downward-pointing triangles) or by two kinesin motors (upward-pointing triangles). Adapted with permission from Ref.

Fig. 4

A schematic view of the tag-of-war phenomenon when motor proteins with opposite polarity compete with each other to move the cellular cargo. Dyneins pull the cargo to the “minus” end of the microtubules, while kinesins tend to carry the cargo in the opposite direction. Adapted with permission from Ref.

Fig. 5

Stepping dynamics of the cellular cargo bound to motor protein complexes, which is driven by dyneins (minus direction) or kinesins (plus direction). Adapted with permission from Ref.

Fig. 6

Comparison of dynamic properties such as transition rates, velocities and fraction of load-shared states for two-kinesin complexes. Symbols are experimental results, and lines are theoretical predictions from cooperative models with different interactions. Reprinted with permission from Ref.. Copyright 2012, American Chemical Society.