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Review
. 2009 Dec;25(12):545-54.
doi: 10.1016/j.tig.2009.10.005. Epub 2009 Oct 29.

Double duty for nuclear proteins--the price of more open forms of mitosis

Colin P De Souza  1 , Stephen A Osmani
Affiliations
Review

Double duty for nuclear proteins--the price of more open forms of mitosis

Colin P De Souza et al. Trends Genet. 2009 Dec.

Abstract

During cell division, eukaryotic cells pass on their genetic material to the next generation by undergoing mitosis, which segregates their chromosomes. During mitosis, the nuclear envelope, nuclear pore complexes and nucleolus must also be segregated. Cells achieve this in a range of different forms of mitosis, from closed, in which these nuclear structures remain intact, to open, in which these nuclear structures are disassembled. In between lies a smorgasbord of intermediate forms of mitosis, displaying varying degrees of nuclear disassembly. Gathering evidence is revealing links between the extent of nuclear disassembly and the evolution of new roles for nuclear proteins during mitosis. We propose that proteins with such double duties help coordinate reassembly of the nucleus with chromosomal segregation.

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Figures

Figure I
Figure I
Figure 1
Figure 1
Variant forms of mitosis occur in different organisms. Although a spindle forms in all these forms of mitosis, other mitotic events are distinct. (a) During S. cerevisiae closed mitosis, the spindle forms within an intact nuclear envelope containing intact NPCs. (b) In A. nidulans semi-open mitosis, although the nuclear envelope remains intact, NPCs undergo a partial disassembly, permeabilizing the nuclear envelope. (c) In Ustilago maydis, the spindle pole bodies are extracted from the nuclear envelope resulting in a cytoplasmic spindle and a form of open mitosis. (d) During mitotic entry in Drosophila early embryos, partial breakdown of the nuclear envelope allows centrosomally nucleated microtubules to attach to kinetochores and at this stage mitosis is semi-open. The remaining nuclear envelope does not completely breakdown until after metaphase. (e) Open mitosis in which the nuclear envelope completely breaks down prior to metaphase.
Figure 2
Figure 2
Mad1 and Mad2 SAC protein localization by Mlp proteins in different forms of mitosis. Examples shown are for S. cerevisiae, A. nidulans and human cells. In all cases, during interphase Mlp proteins are part of the nuclear basket of NPCs and tether Mad1 and Mad2 to NPCs. (a) During the closed mitosis of S. cerevisiae, Mlp proteins continue to localize Mad1 and Mad2 to NPCs [36,37]. (b) During the semi-open mitosis of A. nidulans, the nuclear basket is disassembled and Mlp is part of a spindle matrix. Mlp localizes Mad1 and Mad2 to this spindle matrix which might serve to keep these SAC proteins in close proximity to the spindle [33]. (c) Prometaphase in the open mitosis of mammalian cells. Microtubules nucleated from the centrosomes are beginning to gain access to the kinetochores as the nuclear envelope disassembles. The SAC is active, as indicated by the kinetochore association of Mad1 and Mad2, as all bipolar attachments have yet to be accomplished. Mlp (Tpr in human cells) has a facilitatory role in SAC activation and displays a spindle like localization which is likely analogous to the Drosophila Mlp (Mtor) and A. nidulans spindle matrix [53,56,98].
Figure 3
Figure 3
Specialized mitotic nuclear envelope and spindle matrix functions. (a) During entry into mitosis in Drosophila early embryos, localized nuclear envelope breakdown occurs in the region of the centrosomes allowing access of spindle microtubules to kinetochores. The remaining nuclear envelope persists until after bipolar spindle assembly in metaphase and contains partially disassembled NPC intermediates [3,4]. As many nuclei enter mitosis synchronously within the syncytium of early embryos, the late breakdown of the nuclear envelope provides a physical barrier which might help prevent microtubules interacting with kinetochores of inappropriate nuclei. The Mlp (Mtor) spindle matrix (purple) might also help guide spindle formation within individual nuclei during mitotic entry. (b) Schematic showing double restriction of the nuclear envelope during A. nidulans telophase [84]. Each nuclear envelope restriction occurs at the junctions between the nucleolus and the daughter nuclei. At this stage of A. nidulans mitosis, the NORs have been removed from the nucleolus. Nuclear envelope fission at the two sites of nuclear envelope restriction then results in the exclusion of the nucleolus to the cytoplasm [84]. Mlp in the telophase spindle matrix localizes the Mad1 and Mad2 SAC proteins in between the daughter nuclei [33]. The localization to Mad1 and Mad2 to this region of the mitotic apparatus might locally inhibit APC/C activation, potentially providing spatiotemporal regulation of mitosis.
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