Dataset Information

Expansion and concatenation of non-muscle myosin IIA filaments drive cellular contractile system formation during interphase and mitosis.

ABSTRACT: Cell movement and cytokinesis are facilitated by contractile forces generated by the molecular motor, non-muscle myosin II (NMII). NMII molecules form a filament (NMII-F) through interactions of their C-terminal rod domains, positioning groups of N-terminal motor domains on opposite sides. The NMII motors then bind and pull actin filaments toward the NMII-F, thus driving contraction. Inside of crawling cells, NMIIA-Fs form large macromolecular ensembles (i.e., NMIIA-F stacks) but how this occurs is unknown. Here we show NMIIA-F stacks are formed through two non-mutually exclusive mechanisms: expansion and concatenation. During expansion, NMIIA molecules within the NMIIA-F spread out concurrent with addition of new NMIIA molecules. Concatenation occurs when multiple NMIIA-F/NMIIA-F stacks move together and align. We found NMIIA-F stack formation was regulated by both motor-activity and the availability of surrounding actin filaments. Furthermore, our data showed expansion and concatenation also formed the contractile ring in dividing cells. Thus, interphase and mitotic cells share similar mechanisms for creating large contractile units, and these are likely to underlie how other myosin II-based contractile systems are assembled.

SUBMITTER: Fenix AM

PROVIDER: S-EPMC4850034 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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Expansion and concatenation of non-muscle myosin IIA filaments drive cellular contractile system formation during interphase and mitosis.

Fenix Aidan M AM Taneja Nilay N Buttler Carmen A CA Lewis John J Van Engelenburg Schuyler B SB Ohi Ryoma R Burnette Dylan T DT

Molecular biology of the cell 20160309

Cell movement and cytokinesis are facilitated by contractile forces generated by the molecular motor, non-muscle myosin II (NMII). NMII molecules form a filament (NMII-F) through interactions of their C-terminal rod domains, positioning groups of N-terminal motor domains on opposite sides. The NMII motors then bind and pull actin filaments toward the NMII-F, thus driving contraction. Inside of crawling cells, NMIIA-Fs form large macromolecular ensembles (i.e., NMIIA-F stacks) but how this occurs ...[more]

PMID: 26960797

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Project description:The contractile system of nonmuscle cells consists of interconnected actomyosin networks and bundles anchored to focal adhesions. The initiation of the contractile system assembly is poorly understood structurally and mechanistically, whereas system's maturation heavily depends on nonmuscle myosin II (NMII). Using platinum replica electron microscopy in combination with fluorescence microscopy, we characterized the structural mechanisms of the contractile system assembly and roles of NMII at early stages of this process. We show that inhibition of NMII by a specific inhibitor, blebbistatin, in addition to known effects, such as disassembly of stress fibers and mature focal adhesions, also causes transformation of lamellipodia into unattached ruffles, loss of immature focal complexes, loss of cytoskeleton-associated NMII filaments and peripheral accumulation of activated, but unpolymerized NMII. After blebbistatin washout, assembly of the contractile system begins with quick and coordinated recovery of lamellipodia and focal complexes that occurs before reappearance of NMII bipolar filaments. The initial formation of focal complexes and subsequent assembly of NMII filaments preferentially occurred in association with filopodial bundles and concave actin bundles formed by filopodial roots at the lamellipodial base. Over time, accumulating NMII filaments help to transform the precursor structures, focal complexes and associated thin bundles, into stress fibers and mature focal adhesions. However, semi-sarcomeric organization of stress fibers develops at much slower rate. Together, our data suggest that activation of NMII motor activity by light chain phosphorylation occurs at the cell edge and is uncoupled from NMII assembly into bipolar filaments. We propose that activated, but unpolymerized NMII initiates focal complexes, thus providing traction for lamellipodial protrusion. Subsequently, the mechanical resistance of focal complexes activates a load-dependent mechanism of NMII polymerization in association with attached bundles, leading to assembly of stress fibers and maturation of focal adhesions.

Dataset Information

Expansion and concatenation of non-muscle myosin IIA filaments drive cellular contractile system formation during interphase and mitosis.

Publications

Expansion and concatenation of non-muscle myosin IIA filaments drive cellular contractile system formation during interphase and mitosis.

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