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A novel mechanism of nuclear envelope break-down in a fungus: nuclear migration strips off the envelope.

ABSTRACT: In animals, the nuclear envelope disassembles in mitosis, while budding and fission yeast form an intranuclear spindle. Ultrastructural data indicate that basidiomycetes, such as the pathogen Ustilago maydis, undergo an 'open mitosis'. Here we describe the mechanism of nuclear envelope break-down in U. maydis. In interphase, the nucleus resides in the mother cell and the spindle pole body is inactive. Prior to mitosis, it becomes activated and nucleates microtubules that reach into the daughter cell. Dynein appears at microtubule tips and exerts force on the spindle pole body, which leads to the formation of a long nuclear extension that reaches into the bud. Chromosomes migrate through this extension and together with the spindle pole bodies leave the old envelope, which remains in the mother cell until late telophase. Inhibition of nuclear migration or deletion of a Tem1p-like GTPase leads to a 'closed' mitosis, indicating that spindle pole bodies have to reach into the bud where MEN signalling participates in envelope removal. Our data indicate that dynein-mediated premitotic nuclear migration is essential for envelope removal in U. maydis.

SUBMITTER: Straube A

PROVIDER: S-EPMC1142577 | biostudies-literature | 2005 May

REPOSITORIES: biostudies-literature

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A novel mechanism of nuclear envelope break-down in a fungus: nuclear migration strips off the envelope.

Straube Anne A Weber Isabella I Steinberg Gero G

The EMBO journal 20050414 9

In animals, the nuclear envelope disassembles in mitosis, while budding and fission yeast form an intranuclear spindle. Ultrastructural data indicate that basidiomycetes, such as the pathogen Ustilago maydis, undergo an 'open mitosis'. Here we describe the mechanism of nuclear envelope break-down in U. maydis. In interphase, the nucleus resides in the mother cell and the spindle pole body is inactive. Prior to mitosis, it becomes activated and nucleates microtubules that reach into the daughter ...[more]

PMID: 15861140

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Project description:Recent in vitro and in vivo studies have highlighted the importance of the cell nucleus in governing migration through confined environments. Microfluidic devices that mimic the narrow interstitial spaces of tissues have emerged as important tools to study cellular dynamics during confined migration, including the consequences of nuclear deformation and nuclear envelope rupture. However, while image acquisition can be automated on motorized microscopes, the analysis of the corresponding time-lapse sequences for nuclear transit through the pores and events such as nuclear envelope rupture currently requires manual analysis. In addition to being highly time-consuming, such manual analysis is susceptible to person-to-person variability. Studies that compare large numbers of cell types and conditions therefore require automated image analysis to achieve sufficiently high throughput. Here, we present an automated image analysis program to register microfluidic constrictions and perform image segmentation to detect individual cell nuclei. The MATLAB program tracks nuclear migration over time and records constriction-transit events, transit times, transit success rates, and nuclear envelope rupture. Such automation reduces the time required to analyze migration experiments from weeks to hours, and removes the variability that arises from different human analysts. Comparison with manual analysis confirmed that both constriction transit and nuclear envelope rupture were detected correctly and reliably, and the automated analysis results closely matched a manual analysis gold standard. Applying the program to specific biological examples, we demonstrate its ability to detect differences in nuclear transit time between cells with different levels of the nuclear envelope proteins lamin A/C, which govern nuclear deformability, and to detect an increase in nuclear envelope rupture duration in cells in which CHMP7, a protein involved in nuclear envelope repair, had been depleted. The program thus presents a versatile tool for the study of confined migration and its effect on the cell nucleus.

Dataset Information

A novel mechanism of nuclear envelope break-down in a fungus: nuclear migration strips off the envelope.

Publications

A novel mechanism of nuclear envelope break-down in a fungus: nuclear migration strips off the envelope.

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