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A three-dimensional computer simulation model reveals the mechanisms for self-organization of plant cortical microtubules into oblique arrays.

ABSTRACT: The noncentrosomal cortical microtubules (CMTs) of plant cells self-organize into a parallel three-dimensional (3D) array that is oriented transverse to the cell elongation axis in wild-type plants and is oblique in some of the mutants that show twisted growth. To study the mechanisms of CMT array organization, we developed a 3D computer simulation model based on experimentally observed properties of CMTs. Our computer model accurately mimics transverse array organization and other fundamental properties of CMTs observed in rapidly elongating wild-type cells as well as the defective CMT phenotypes observed in the Arabidopsis mor1-1 and fra2 mutants. We found that CMT interactions, boundary conditions, and the bundling cutoff angle impact the rate and extent of CMT organization, whereas branch-form CMT nucleation did not significantly impact the rate of CMT organization but was necessary to generate polarity during CMT organization. We also found that the dynamic instability parameters from twisted growth mutants were not sufficient to generate oblique CMT arrays. Instead, we found that parameters regulating branch-form CMT nucleation and boundary conditions at the end walls are important for forming oblique CMT arrays. Together, our computer model provides new mechanistic insights into how plant CMTs self-organize into specific 3D arrangements.

SUBMITTER: Eren EC

PROVIDER: S-EPMC2912353 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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A three-dimensional computer simulation model reveals the mechanisms for self-organization of plant cortical microtubules into oblique arrays.

Eren Ezgi Can EC Dixit Ram R Gautam Natarajan N

Molecular biology of the cell 20100602 15

The noncentrosomal cortical microtubules (CMTs) of plant cells self-organize into a parallel three-dimensional (3D) array that is oriented transverse to the cell elongation axis in wild-type plants and is oblique in some of the mutants that show twisted growth. To study the mechanisms of CMT array organization, we developed a 3D computer simulation model based on experimentally observed properties of CMTs. Our computer model accurately mimics transverse array organization and other fundamental p ...[more]

PMID: 20519434

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Project description:Nowadays, in vitro three-dimensional (3D) neuronal networks are becoming a consolidated experimental model to overcome most of the intrinsic limitations of bi-dimensional (2D) assemblies. In the 3D environment, experimental evidence revealed a wider repertoire of activity patterns, characterized by a modulation of the bursting features, than the one observed in 2D cultures. However, it is not totally clear and understood what pushes the neuronal networks towards different dynamical regimes. One possible explanation could be the underlying connectivity, which could involve a larger number of neurons in a 3D rather than a 2D space and could organize following well-defined topological schemes. Driven by experimental findings, achieved by recording 3D cortical networks organized in multi-layered structures coupled to Micro-Electrode Arrays (MEAs), in the present work we developed a large-scale computational network model made up of leaky integrate-and-fire (LIF) neurons to investigate possible structural configurations able to sustain the emerging patterns of electrophysiological activity. In particular, we investigated the role of the number of layers defining a 3D assembly and the spatial distribution of the connections within and among the layers. These configurations give rise to different patterns of activity that could be compared to the ones emerging from real in vitro 3D neuronal populations. Our results suggest that the introduction of three-dimensionality induced a global reduction in both firing and bursting rates with respect to 2D models. In addition, we found that there is a minimum number of layers necessary to obtain a change in the dynamics of the network. However, the effects produced by a 3D organization of the cells is somewhat mitigated if a scale-free connectivity is implemented in either one or all the layers of the network. Finally, the best matching of the experimental data is achieved supposing a 3D connectivity organized in structured bundles of links located in different areas of the 2D network.

Project description:Differentiated mammalian cells and tissues, such as skeletal muscle fibers, acquire an organization of Golgi complex and microtubules profoundly different from that in proliferating cells and still poorly understood. In adult rodent skeletal muscle, the multinucleated muscle fibers have hundreds of Golgi elements (GE), small stacks of cisternae that serve as microtubule-organizing centers. We are interested in the role of the GE in organizing a peculiar grid of microtubules located in the fiber cortex, against the sarcolemma. Modifications of this grid in the mdx mouse model of Duchenne muscular dystrophy have led to identifying dystrophin, the protein missing in both human disease and mouse model, as a microtubule guide. Compared to wild-type (WT), mdx microtubules are disordered and more dense and they have been linked to the dystrophic pathology. GE themselves are disordered in mdx. Here, to identify the causes of GE and microtubule alterations in the mdx muscle, we follow GFP-tagged microtubule markers in live mdx fibers and investigate the recovery of GE and microtubules after treatment with nocodazole. We find that mdx microtubules grow 10% faster but in 30% shorter bouts and that they begin to form a tangled network, rather than an orthogonal grid, right after nucleation from GE. Strikingly, a large fraction of microtubules in mdx muscle fibers seem to dissociate from GE after nucleation. Moreover, we report that mdx GE are mispositioned and increased in number and size. These results were replicated in WT fibers overexpressing the beta-tubulin tubb6, which is elevated in Duchenne muscular dystrophy, in mdx and in regenerating muscle. Finally, we examine the association of GE with ER exit sites and ER-to-Golgi intermediate compartment, which starts during muscle differentiation, and find it persisting in mdx and tubb6 overexpressing fibers. We conclude that GE are full, small, Golgi complexes anchored, and positioned through ER Exit Sites. We propose a model in which GE mispositioning, together with the absence of microtubule guidance due to the lack of dystrophin, determines the differences in GE and microtubule organization between WT and mdx muscle fibers.

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A three-dimensional computer simulation model reveals the mechanisms for self-organization of plant cortical microtubules into oblique arrays.

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A three-dimensional computer simulation model reveals the mechanisms for self-organization of plant cortical microtubules into oblique arrays.

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