Marking and Measuring Single Microtubules by PRC1 and Kinesin-4

Subramanian, Radhika; Ti, Shih-Chieh; Tan, Lei; Darst, Seth A.; Kapoor, Tarun M.

doi:10.1016/j.cell.2013.06.021

Cited by 164 publications

(249 citation statements)

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“…Both of these motors have previously been implicated in opposing dynein-driven MT rotations in D. discoideum [38] and thus work synergistically with dynein to organize the MT array. Both motors are also known to participate in antiparallel MT-MT interactions [39–42]. Kinesin-8 has MT sliding and depolymerizing activities and has recently been modeled into a nuclear centering mechanism relevant to interphase [43].…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Organization of microtubule assemblies in Dictyostelium syncytia depends on the microtubule crosslinker, Ase1

Tikhonenko¹,

Irizarry²,

Khodjakov³

et al. 2015

Cell. Mol. Life Sci.

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It has long been known that the interphase microtubule (MT) array is a key cellular scaffold that provides structural support and directs organelle trafficking in eukaryotic cells. Although in animal cells, a combination of centrosome nucleating properties and polymer dynamics at the distal microtubule ends is generally sufficient to establish a radial, polar array of MTs, little is known about how effector proteins (motors and crosslinkers) are coordinated to produce the diversity of interphase MT array morphologies found in nature. This diversity is particularly important in multinucleated environments where multiple MT arrays must coexist and function. We initiate here a study to address the higher ordered coordination of multiple, independent MT arrays in a common cytoplasm. Deletion of a MT crosslinker of the MAP65/Ase1/PRC1 family disrupts the spatial integrity of multiple arrays in Dictyostelium discoideum, reducing the distance between centrosomes and increasing the intermingling of MTs with opposite polarity. This result, coupled with previous dynein disruptions suggest a robust mechanism by which interphase MT arrays can utilize motors and crosslinkers to sense their position and minimize overlap in a common cytoplasm.

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Section: Discussionmentioning

confidence: 99%

“…Kinesin-8 has MT sliding and depolymerizing activities and has recently been modeled into a nuclear centering mechanism relevant to interphase [43]. Kinesin-4 is further known to interact directly with human PRC1 [39,44,42] where it also functions to regulate MT length during mitosis.…”

Section: Discussionmentioning

confidence: 99%

Organization of microtubule assemblies in Dictyostelium syncytia depends on the microtubule crosslinker, Ase1

Tikhonenko¹,

Irizarry²,

Khodjakov³

et al. 2015

Cell. Mol. Life Sci.

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“…As seen in theoretical studies on the collective motion of molecular motors, resource limitation affects the density profile on the MT: regions of low and high motor density separate, as a localized domain wall emerges on the MT [16][17][18][19]. This is a direct result of resource limitation and does not rely on the existence of a motor density gradient, as necessary for domain wall localization in the presence of unlimited resources [20][21][22][23]. So far, most work on the role of limited resources has focused on single components of the relevant system [17][18][19][24][25][26][27][28].…”

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confidence: 99%

Limited Resources Induce Bistability in Microtubule Length Regulation

et al. 2018

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The availability of protein is an important factor for the determination of the size of the mitotic spindle. Involved in spindle-size regulation is kinesin-8, a molecular motor and microtubule (MT) depolymerase, which is known to tightly control MT length. Here, we propose and analyze a theoretical model in which kinesin-induced MT depolymerization competes with spontaneous polymerization while supplies of both tubulin and kinesin are limited. In contrast to previous studies where resources were unconstrained, we find that, for a wide range of concentrations, MT length regulation is bistable. We test our predictions by conducting in vitro experiments and find that the bistable behavior manifests in a bimodal MT length distribution. DOI: 10.1103/PhysRevLett.120.148101 The absolute and relative abundance of particular sets of proteins is important for a wide range of processes in cells. For example, during Xenopus laevis embryogenesis, importin α becomes progressively localized to the cell membrane [1]. As a consequence of importin's depletion from the cytoplasm, the protein kif2a escapes inactivation and decreases the size of the mitotic spindle. Similarly, formation of the mitotic spindle reduces the concentration of free tubulin dimers, the building blocks of microtubules (MTs). Thus, up to 60% of all tubulin heterodimers [2,3] may be incorporated into the spindle [4]. In addition, it has been shown in vivo and in vitro that both spindle size [4,5] and the lengths of its constituent MTs [6] scale with cytoplasmic volume.Assembly and disassembly of MTs are regulated by a set of proteins that interact with the plus ends of protofilaments [7,8]. One of these factors, the molecular motor kinesin-8, acts as a depolymerase [8,9]. As a consequence, spindle size increases in its absence [10] and decreases upon overexpression of the protein [11]. Moreover, the kinesin-8 homolog Kip3 from Saccharomyces cerevisiae has been shown to depolymerize MTs in a length-dependent fashion [9,12]. This is facilitated by a density gradient on the MT, caused by the interplay between the processive motion of Kip3 along the MT and its depolymerase activity at the plus end, which effectively enables the MT to "sense" its own length [12,13]. In combination with spontaneous MT polymerization, the Kip3 gradient leads to a length regulation mechanism [14,15].Here, we explore the combined effect of limited resources and Kip3-induced depolymerization on the length regulation of MTs. As seen in theoretical studies on the collective motion of molecular motors, resource limitation affects the density profile on the MT: regions of low and high motor density separate, as a localized domain wall emerges on the MT [16][17][18][19]. This is a direct result of resource limitation and does not rely on the existence of a motor density gradient, as necessary for domain wall localization in the presence of unlimited resources [20][21][22][23]. So far, most work on the role of limited resources has focused on single components of the relevant system [17][...

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“…In general, adapter proteins may sense the local configuration of microtubules to provide feedback on microtubule network layout. Examples are MAP65/Ase1/PRC1, which bind to antiparallel-oriented microtubules, and SPIRAL2, which is recruited to sites of microtubule cross-over (Janson et al 2007;Subramanian et al 2013;Wightman et al 2013). The use of such adapter proteins may enable a conserved set of proteins to be efficiently used in various network layouts and may facilitate fast switching between network architectures as observed in plant cell division.…”

Section: Discussionmentioning

confidence: 99%

Microtubule networks for plant cell division

2014

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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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Marking and Measuring Single Microtubules by PRC1 and Kinesin-4

Cited by 164 publications

References 31 publications

Organization of microtubule assemblies in Dictyostelium syncytia depends on the microtubule crosslinker, Ase1

Organization of microtubule assemblies in Dictyostelium syncytia depends on the microtubule crosslinker, Ase1

Limited Resources Induce Bistability in Microtubule Length Regulation

Microtubule networks for plant cell division

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