Myosin-driven actin-microtubule networks exhibit self-organized contractile dynamics

Abstract

The cytoskeleton is a dynamic network of proteins, including actin, microtubules, and their associated motor proteins, that enables essential cellular processes such as motility, division, and growth. While actomyosin networks are extensively studied, how interactions between actin and microtubules, ubiquitous in the cytoskeleton, influence actomyosin activity remains an open question. Here, we create a network of co-entangled actin and microtubules driven by myosin II. We combine dynamic differential microscopy, particle image velocimetry, and particle tracking to show that both actin and microtubules undergo ballistic contraction with unexpectedly indistinguishable characteristics. This contractility is distinct from faster disordered motion and rupturing that active actin networks exhibit. Our results suggest that microtubules enable self-organized myosin-driven contraction by providing flexural rigidity and enhanced connectivity to actin networks. Beyond the immediate relevance to cytoskeletal dynamics, our results shed light on the design of active materials that can be precisely tuned by the network composition.

Extensile to contractile transition in active microtubule–actin composites generates layered asters with programmable lifetimes

“…These dual observations challenge existing theoretical models. They are also different from previous work with myosin-driven MT–actin composites, which showed that the viscoelastic response could be tuned by the addition of a second material component, but the symmetry of the active stress did not change ( 43 ). However, they are broadly consistent with previous experimental work in which the deformations of rigid filaments changed from extensile to contractile through the addition of passive cross-linkers ( 52 ).…”

“…Our work builds on the previous studies of active composites ( 42 , 43 ). So far, we have described how increasing F-actin concentrations induce transitions from the extensile fluid to layered asters and then, to global contractions.…”

“…With notable exceptions from two-dimensional motility assay geometries ( 49 , 50 ), cytoskeletal active matter typically exhibits either uniform contractile or extensile dynamics, which implies the existence of a single type of self-organized active stress ( 13 , 16 , 20 , 43 , 51 – 53 ). It remains a challenge to predict the nature of the mesoscopic active stresses given known microscopic dynamics.…”

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“…Microtubules are cytoskeletal filaments that permeate the cytoplasm of all eukaryotic cells and play a pivotal role in numerous biological processes, including intracellular transport, cell motility, cell morphology maintenance and formation of mitotic spindle to facilitate chromosome separation during cell division [133][134][135][136][137]. Microtubules are inherently dynamic and capable of organizing and restructuring into different architectures in precise timing and location to facilitate various cellular functions [138,139]. During mitosis, the microtubule dynamics are increased by 20-100-fold [140].…”

DataSheet1.PDF

“…The corresponding correlation length ξ is obtained by curve-fitting autocorrelation curves to g(r) g o exp(−r/ξ). This approach is based on previous studies that have applied SIA to confocal images of cytoskeleton networks to determine correlation lengthscales [58,59]. Because many of the curves exhibit non-exponential tails at large distances due to flat-field noise, as in these prior studies, we restrict curvefitting to g(r ≤ 2 μm).…”