Augmin-dependent microtubule nucleation at microtubule walls in the spindle

Kamasaki, Tomoko; O’Toole, Eileen; Kita, Shigeo; Osumi, Masako; Usukura, Jiro; McIntosh, J. Richard; Goshima, Gohta

doi:10.1083/jcb.201304031

Cited by 107 publications

(123 citation statements)

References 40 publications

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“…However, unlike other cases, the branch angle utilized in this cell type was highly variable. Branching nucleation with a fixed angle has been thought to be an excellent cellular approach to not only amplify MT numbers, but also polarize the MT network (Janson et al, 2005;Murata et al, 2005;Kamasaki et al, 2013;Petry et al, 2013). Our observation suggests that protonemal cells utilize this mode of MT nucleation simply to increase MT numbers.…”

Section: Mechanism Of Branching Nucleationmentioning

confidence: 57%

“…In this mechanism, a conserved eight-subunit complex, augmin, binds to spindle/ phragmoplast MTs, recruits the g-tubulin ring complex (g-TuRC), and thereby nucleates new MTs. Studies in animal systems have shown that daughter MTs are nucleated predominantly at <20°a ngles from mother MTs during this process, indicating that this mechanism is suitable for generating the parallel MT arrays commonly seen in the spindle and phragmoplast (Kamasaki et al, 2013;Petry et al, 2013). A recent report has shown that augmin also plays a role in MT-dependent MT nucleation by recruiting the g-TuRC in the cortical MT arrays (Liu et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Cytoplasmic Nucleation and Atypical Branching Nucleation Generate Endoplasmic Microtubules inPhyscomitrella patens

et al. 2015

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The mechanism underlying microtubule (MT ) generation in plants has been primarily studied using the cortical MT array, in which fixed-angled branching nucleation and katanin-dependent MT severing predominate. However, little is known about MT generation in the endoplasm. Here, we explored the mechanism of endoplasmic MT generation in protonemal cells of Physcomitrella patens. We developed an assay that utilizes flow cell and oblique illumination fluorescence microscopy, which allowed visualization and quantification of individual MT dynamics. MT severing was infrequently observed, and disruption of katanin did not severely affect MT generation. Branching nucleation was observed, but it showed markedly variable branch angles and was occasionally accompanied by the transport of nucleated MTs. Cytoplasmic nucleation at seemingly random locations was most frequently observed and predominated when depolymerized MTs were regrown. The MT nucleator g-tubulin was detected at the majority of the nucleation sites, at which a single MT was generated in random directions. When g-tubulin was knocked down, MT generation was significantly delayed in the regrowth assay. However, nucleation occurred at a normal frequency in steady state, suggesting the presence of a g-tubulin-independent backup mechanism. Thus, endoplasmic MTs in this cell type are generated in a less ordered manner, showing a broader spectrum of nucleation mechanisms in plants.

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Section: Mechanism Of Branching Nucleationmentioning

confidence: 57%

Section: Introductionmentioning

confidence: 99%

Cytoplasmic Nucleation and Atypical Branching Nucleation Generate Endoplasmic Microtubules inPhyscomitrella patens

et al. 2015

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“…Such a nucleation pattern is now recognized to be shared by animal cells and recapitulated by electron microscopy [14,23]. The augmin complex interacts with the gTuRC and likely recruits the latter to MT walls to initiate branching nucleation with shallow angles (<30 ); such a nucleation event has been reconstituted in vitro using frog egg extracts [24].…”

Section: Augmin Is Specifically Associated With Mt-dependent Mt Nuclementioning

confidence: 96%

Augmin Triggers Microtubule-Dependent Microtubule Nucleation in Interphase Plant Cells

et al. 2014

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Microtubule (MT)-dependent MT nucleation by γ-tubulin is required for interphase plant cells to establish a highly dynamic cortical MT network underneath the plasma membrane, which influences the deposition of cell wall materials and consequently governs patterns of directional cell expansion. Newly formed MTs either assume 40° angles or are parallel to the extant ones. To date, it has been enigmatic how the γ-tubulin complex is recruited to the sidewall of cortical MTs and initiates MT nucleation. Here, we discovered that the augmin complex was recruited to cortical MTs and initiated MT nucleation in both branching and parallel forms. The augmin complex overwhelmingly colocalized with the γ-tubulin complex. When the function of the augmin complex was compromised, MT nucleation frequency was drastically reduced, most obviously for the branching nucleation. Consequently, the augmin knockdown cells displayed highly parallel and bundled MTs, replacing the fine and mesh-like MT network in the wild-type cells. Our findings uncovered a mechanism by which the augmin complex functions in recruiting the γ-tubulin complex to cortical MTs and initiating MT nucleation, and they shifted the paradigm of the commonly perceived mitotic-specific function of augmin and established its crucial function in MT-dependent MT nucleation in interphase plant cells.

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“…Existing microtubules for example trigger nucleation of new microtubules through augmin-mediated recruitment of microtubule nucleation complexes leading to local microtubule amplification (Clausen and Ribbeck 2007;Petry et al 2013). Directionally biased microtubule-dependent nucleation can reinforce an existing polarity (Smertenko et al 2011;Kamasaki et al 2013). Another example of feedback involves the dynamic instability of microtubules in bundles, which is adapted locally through recruitment of CLASP or KIF4 by bundling proteins (Bratman and Chang 2007;Bieling et al 2010).…”

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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Augmin-dependent microtubule nucleation at microtubule walls in the spindle

Abstract: Electron tomography and 3D modeling identifies augmin-dependent connections between the wall of one microtubule and the minus end of a neighboring one in the spindle.

Cited by 107 publications

References 40 publications

Cytoplasmic Nucleation and Atypical Branching Nucleation Generate Endoplasmic Microtubules inPhyscomitrella patens

Cytoplasmic Nucleation and Atypical Branching Nucleation Generate Endoplasmic Microtubules inPhyscomitrella patens

Augmin Triggers Microtubule-Dependent Microtubule Nucleation in Interphase Plant Cells

Microtubule networks for plant cell division

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