Mechanical Stress Acts via Katanin to Amplify Differences in Growth Rate between Adjacent Cells in Arabidopsis

Uyttewaal, Magalie; Burian, Agata; Alim, Karen; Landrein, Benoi T.; Borowska-Wykręt, Dorota; Dedieu, Annick; Peaucelle, Alexis; Ludynia, Michał; Traas, Jan; Boudaoud, Arezki; Kwiatkowska, Dorota; Hamant, Olivier

doi:10.1016/j.cell.2012.02.048

Cited by 414 publications

(505 citation statements)

References 63 publications

(87 reference statements)

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“…Additionally, an overly stabilized and less dynamic MT network is a likely contributor to the acquisition of this abnormal size (up to 70 times larger than controls in our experiments). In Arabidopsis, cellular size and shape were found to be affected by katanin-dependent cortical MT dynamics and orientation influencing the ability of the cell to respond to mechanical stress [59]. A frequent observation in our live imaging recordings of Katnal2-silenced cell populations was the occurrence of large nuclei, ''rotating'' widely for prolonged periods.…”

Section: Discussionmentioning

confidence: 89%

A novel family of katanin-like 2 protein isoforms (KATNAL2), interacting with nucleotide-binding proteins Nubp1 and Nubp2, are key regulators of different MT-based processes in mammalian cells

Ververis

Christodoulou

Christoforou

et al. 2015

Cell. Mol. Life Sci.

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Katanins are microtubule (MT)-severing AAA proteins with high phylogenetic conservation throughout the eukaryotes. They have been functionally implicated in processes requiring MT remodeling, such as spindle assembly in mitosis and meiosis, assembly/disassembly of flagella and cilia and neuronal morphogenesis. Here, we uncover a novel family of katanin-like 2 proteins (KAT-NAL2) in mouse, consisting of five alternatively spliced isoforms encoded by the Katnal2 genomic locus. We further demonstrate that in vivo these isoforms are able to interact with themselves, with each other and moreover directly and independently with MRP/MinD-type P-loop NTPases Nubp1 and Nubp2, which are integral components of centrioles, negative regulators of ciliogenesis and implicated in centriole duplication in mammalian cells. We find KATNAL2 localized on interphase MTs, centrioles, mitotic spindle, midbody and the axoneme and basal body of sensory cilia in cultured murine cells. shRNAi of Katnal2 results in inefficient cytokinesis and severe phenotypes of enlarged cells and nuclei, increased numbers of centrioles and the manifestation of aberrant multipolar mitotic spindles, mitotic defects, chromosome bridges, multinuclearity, increased MT acetylation and an altered cell cycle pattern. Silencing or stable overexpression of KATNAL2 isoforms drastically reduces ciliogenesis. In conclusion, KATNAL2s are multitasking enzymes involved in the same cell type in critically important processes affecting cytokinesis, MT dynamics, and ciliogenesis and are also implicated in cell cycle progression.

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Section: Discussionmentioning

confidence: 89%

A novel family of katanin-like 2 protein isoforms (KATNAL2), interacting with nucleotide-binding proteins Nubp1 and Nubp2, are key regulators of different MT-based processes in mammalian cells

Ververis

Christodoulou

Christoforou

et al. 2015

Cell. Mol. Life Sci.

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“…Other experimental data suggest that katanin-mediated severing activity can be regulated through interactions between RIC1 and katanin p60 (30), and in a blue light-dependent manner through photoreceptors PHOT1/PHOT1 (26). Moreover, the MT array responds far less to mechanical perturbations in katanin loss-of-function mutants (25). All of these findings suggest that tuning MT severing is indeed an important target for responding to environmental stimuli and changing MT organization (40).…”

Section: Discussionmentioning

confidence: 99%

“…cortical array (23,24) as well as its reorientation upon external cues (25,26). At first sight, these findings seem at odds with the survival-of-the-aligned mechanism.…”

Section: Significancementioning

confidence: 99%

How selective severing by katanin promotes order in the plant cortical microtubule array

Deinum

Tindemans

Lindeboom

et al. 2017

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

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Plant morphogenesis requires differential and often asymmetric growth. A key role in controlling anisotropic expansion of individual cells is played by the cortical microtubule array. Although highly organized, the array can nevertheless rapidly change in response to internal and external cues. Experiments have identified the microtubule-severing enzyme katanin as a central player in controlling the organizational state of the array. Katanin action is required both for normal alignment and the adaptation of array orientation to mechanical, environmental, and developmental stimuli. How katanin fulfills its controlling role, however, remains poorly understood. On the one hand, from a theoretical perspective, array ordering depends on the "weeding out" of discordant microtubules through frequent catastrophe-inducing collisions among microtubules. Severing would reduce average microtubule length and lifetime, and consequently weaken the driving force for alignment. On the other hand, it has been suggested that selective severing at microtubule crossovers could facilitate the removal of discordant microtubules. Here we show that this apparent conflict can be resolved by systematically dissecting the role of all of the relevant interactions in silico. This procedure allows the identification of the sufficient and necessary conditions for katanin to promote array alignment, stresses the critical importance of the experimentally observed selective severing of the "crossing" microtubule at crossovers, and reveals a hitherto not appreciated role for microtubule bundling. We show how understanding the underlying mechanism can aid with interpreting experimental results and designing future experiments.katanin | cortical microtubule array | microtubule dynamics | self-organization | plant cell biology P lant cells are constrained by their cellulose-based cell walls.This fact poses two important requirements for development: (i) consistent cell wall anisotropy within tissues to ensure coherent growth and (ii) precise local controllability of cell wall properties to produce complex cell shapes (e.g., ref. 1) and accommodate the development of new plant organs (e.g., ref.2). The central organizing system that mediates these requirements is the plant cortical microtubule (MT) array. Individual MTs selforganize into this often strikingly ordered structure, which is known to regulate the insertion of cellulose synthase complexes into the plasma membrane (3) and subsequently guide their movement during cellulose microfibril deposition (4), thereby playing a key role in cell growth and development. The organizational state of the array, in turn, depends on cell type (5) and may change in response to mechanical (6), environmental stimuli, and developmental patterning processes (7). Acentrosomal and cortical MT arrays also occur in other eukaryotic systems, including protists and animals (e.g., refs. 8-10).The core mechanism behind the self-organization of the array is described by a consensus model that has been developed over the pa...

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“…Several models based on non-uniform cell growth across growing islets have emphasized the role of free edges [41][42][43][44][45] , some of them resulting in out-of-plane modulations 41 . Our results do not exclude these mechanisms by which more cells get to be produced at peripheral regions.…”

Section: Discussionmentioning

confidence: 99%

Emergence of collective modes and tri-dimensional structures from epithelial confinement

et al. 2014

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Many in vivo processes, including morphogenesis or tumour maturation, involve small populations of cells within a spatially restricted region. However, the basic mechanisms underlying the dynamics of confined cell assemblies remain largely to be deciphered and would greatly benefit from well-controlled in vitro experiments. Here we show that confluent epithelial cells cultured on finite population-sized domains, exhibit collective low-frequency radial displacement modes as well as stochastic global rotation reversals. A simple mathematical model, in which cells are described as persistent random walkers that adapt their motion to that of their neighbours, captures the essential characteristics of these breathing oscillations. As these epithelia mature, a tri-dimensional peripheral cell cord develops at the domain edge by differential extrusion, as a result of the additional degrees of freedom of the border cells. These results demonstrate that epithelial confinement alone can induce morphogenesis-like processes including spontaneous collective pulsations and transition from 2D to 3D.

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Mechanical Stress Acts via Katanin to Amplify Differences in Growth Rate between Adjacent Cells in Arabidopsis

Cited by 414 publications

References 63 publications

A novel family of katanin-like 2 protein isoforms (KATNAL2), interacting with nucleotide-binding proteins Nubp1 and Nubp2, are key regulators of different MT-based processes in mammalian cells

A novel family of katanin-like 2 protein isoforms (KATNAL2), interacting with nucleotide-binding proteins Nubp1 and Nubp2, are key regulators of different MT-based processes in mammalian cells

How selective severing by katanin promotes order in the plant cortical microtubule array

Emergence of collective modes and tri-dimensional structures from epithelial confinement

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