Adaptive braking by Ase1 prevents overlapping microtubules from sliding completely apart

Braun, Marcus; Lánský, Zdeněk; Fink, Gero; Ruhnow, Felix; Diez, Stefan; Janson, Marcel E.

doi:10.1038/ncb2323

Cited by 113 publications

(185 citation statements)

References 31 publications

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“…If we take for ξ the rough hydrodynamic estimate ξ H given above, an energy barrier E a ≅ 10 k B T (15) brings channel friction to a level compatible with our experiments. Internal friction resulting from barrier crossing is thought to influence many processes in biology, including protein folding (22), protein-protein interactions (23,24), cell adhesion (25), and the speed and efficiency of motor proteins (16,26). Our work shows that this general concept of barrier friction also applies to mechanosensory ion channels and is thus relevant for the detection of sound-evoked vibrations by hair-cell bundles in the ear.…”

Section: Discussionmentioning

confidence: 82%

Transduction channels’ gating can control friction on vibrating hair-cell bundles in the ear

Bormuth

Barral

Joanny

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Hearing starts when sound-evoked mechanical vibrations of the hair-cell bundle activate mechanosensitive ion channels, giving birth to an electrical signal. As for any mechanical system, friction impedes movements of the hair bundle and thus constrains the sensitivity and frequency selectivity of auditory transduction. Friction is generally thought to result mainly from viscous drag by the surrounding fluid. We demonstrate here that the opening and closing of the transduction channels produce internal frictional forces that can dominate viscous drag on the micrometer-sized hair bundle. We characterized friction by analyzing hysteresis in the force-displacement relation of single hair-cell bundles in response to periodic triangular stimuli. For bundle velocities high enough to outrun adaptation, we found that frictional forces were maximal within the narrow region of deflections that elicited significant channel gating, plummeted upon application of a channel blocker, and displayed a sublinear growth for increasing bundle velocity. At low velocity, the slope of the relation between the frictional force and velocity was nearly fivefold larger than the hydrodynamic friction coefficient that was measured when the transduction machinery was decoupled from bundle motion by severing tip links. A theoretical analysis reveals that channel friction arises from coupling the dynamics of the conformational change associated with channel gating to tip-link tension. Varying channel properties affects friction, with faster channels producing smaller friction. We propose that this intrinsic source of friction may contribute to the process that sets the hair cell's characteristic frequency of responsiveness.mechanosensitive channels | protein friction | hair-bundle mechanosensitivity | cell mechanics | auditory system S ound evokes vibrations in the inner ear that are detected by sensory hair cells. Mechanosensitivity stems from mechanical activation of ion channels by tension changes in tip links that interconnect neighboring stereocilia of the hair-cell bundle (1). The acute sensitivity and sharp frequency selectivity of auditory detection rely on efficient transmission of the energy derived from the acoustic stimulus to the apparatus that mediates mechanoelectrical transduction. However, at least three sources of friction threaten to dissipate the energy of the vibrating hair bundle. First, viscous drag by the surrounding fluid provides a minimum source of damping (2, 3). Second, viscoelasticity of the tip links, or of proteins in series with these links, may result in additional dissipation during hair-bundle deflections (4). Third, an intrinsic source of friction-called "channel friction" in the following-is related to thermal fluctuations of the transduction channels between their open and closed states (5). The fluctuation-dissipation theorem dictates that this source of mechanical noise be related to friction forces on the hair bundle.To circumvent the fundamental challenge posed by friction, hair cells mobilize internal ...

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Section: Discussionmentioning

confidence: 82%

Transduction channels’ gating can control friction on vibrating hair-cell bundles in the ear

Bormuth

Barral

Joanny

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Other forms of feedback may be more physical in origin (Fig. 3d, e), such as the packing of bundling proteins within the overlaps of sliding microtubules or the induction of catastrophes through collisions with neighbouring microtubules (Allard et al 2010a;Braun et al 2011). Cell geometry plays an additional role as shown by local cell wall curvature which may invoke microtubule catastrophes (Ambrose and Wasteneys 2012).…”

Section: Discussionmentioning

confidence: 99%

Microtubule networks for plant cell division

2014

Self Cite

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During cytokinesis the cytoplasm of a cell is divided to form two daughter cells. In animal cells, the existing plasma membrane is first constricted and then abscised to generate two individual plasma membranes. Plant cells on the other hand divide by forming an interior dividing wall, the so-called cell plate, which is constructed by localized deposition of membrane and cell wall material. Construction starts in the centre of the cell at the locus of the mitotic spindle and continues radially towards the existing plasma membrane. Finally the membrane of the cell plate and plasma membrane fuse to form two individual plasma membranes. Two microtubule-based cytoskeletal networks, the phragmoplast and the pre-prophase band (PPB), jointly control cytokinesis in plants. The bipolar microtubule array of the phragmoplast regulates cell plate deposition towards a cortical position that is templated by the ring-shaped microtubule array of the PPB. In contrast to most animal cells, plants do not use centrosomes as foci of microtubule growth initiation. Instead, plant microtubule networks are striking examples of selforganizing systems that emerge from physically constrained interactions of dispersed microtubules. Here we will discuss how microtubule-based activities including growth, shrinkage, severing, sliding, nucleation and bundling interrelate to jointly generate the required ordered structures. Evidence mounts that adapter proteins sense the local geometry of microtubules to locally modulate the activity of proteins involved in microtubule growth regulation and severing. Many of the proteins and mechanisms involved have roles in other microtubule assemblies as well, bestowing broader relevance to insights gained from plants.

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“…The forces generated by Ase1-driven expansion of the overlapping microtubule-region are large enough to counterbalance kinesin-14 mediated sliding forces in vitro 28,29 . In cells, Ase1/PRC1 is required for stable formation of overlapping microtubule regions in the spindle midzone [25][26][27]30 , suggesting that the forces generated by diffusible cross-linkers can significantly contribute to spindle organization.…”

Section: Introductionmentioning

confidence: 99%

Reconstitution of Basic Mitotic Spindles in Spherical Emulsion Droplets

Vleugel

Roth

Groenendijk

et al. 2016

JoVE

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Mitotic spindle assembly, positioning and orientation depend on the combined forces generated by microtubule dynamics, microtubule motor proteins and cross-linkers. Growing microtubules can generate pushing forces, while depolymerizing microtubules can convert the energy from microtubule shrinkage into pulling forces, when attached, for example, to cortical dynein or chromosomes. In addition, motor proteins and diffusible cross-linkers within the spindle contribute to spindle architecture by connecting and sliding anti-parallel microtubules. In vivo, it has proven difficult to unravel the relative contribution of individual players to the overall balance of forces. Here we present the methods that we recently developed in our efforts to reconstitute basic mitotic spindles bottom-up in vitro. Using microfluidic techniques, centrosomes and tubulin are encapsulated in water-in-oil emulsion droplets, leading to the formation of geometrically confined (double) microtubule asters. By additionally introducing cortically anchored dynein, plus-end directed microtubule motors and diffusible cross-linkers, this system is used to reconstitute spindle-like structures. The methods presented here provide a starting point for reconstitution of more complete mitotic spindles, allowing for a detailed study of the contribution of each individual component, and for obtaining an integrated quantitative view of the force-balance within the mitotic spindle.

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Adaptive braking by Ase1 prevents overlapping microtubules from sliding completely apart

Cited by 113 publications

References 31 publications

Transduction channels’ gating can control friction on vibrating hair-cell bundles in the ear

Transduction channels’ gating can control friction on vibrating hair-cell bundles in the ear

Microtubule networks for plant cell division

Reconstitution of Basic Mitotic Spindles in Spherical Emulsion Droplets

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