Nuclear envelope remodelling during mitosis

Abstract

The defining feature of the eukaryotic cell, the nucleus, is bounded by a double envelope. This envelope and the nuclear pores within it play a critical role in separating the genome from the cytoplasm. It also presents cells with a challenge. How are cells to remodel the nuclear compartment boundary during mitosis without compromising nuclear function? In the two billion years since the emergence of the first cells with a nucleus, eukaryotes have evolved a range of strategies to do this. At one extreme, the nucleus is disassembled upon entry into mitosis and then reassembled anew in the two daughter cells. At the other, cells maintain an intact nuclear compartment boundary throughout the division process. In this review, we discuss common features of the division process that underpin remodelling mechanisms, the topological challenges involved and speculate on the selective pressures that may drive the evolution of distinct modes of division.

Keywords: Eukaryogenesis; Lamina; Mitosis; Nuclear division; Nuclear envelope; Nuclear pore complex.

Figure 1

A schematic illustrating the full range of possible mitotic nuclear remodelling strategies, starting from completely open at the top to completely closed at the bottom. The compartment barrier is highlighted by labelling the nucleoplasm in blue and the cytoplasm in white; chromosomes are in dark grey and spindle microtubules in brown; other key cellular structures are labelled on the diagram. The two theoretical extremes have not been experimentally observed in any eukaryote to date. The blue bars indicate either local or global fenestration or ‘opening’ of the nuclear envelope, leading to a disruption of the barrier between the nucleoplasm and cytoplasm. In closed or semiclosed mitosis, the first local opening event allows the microtubule-nucleating centres to access the nucleoplasm; the second local opening drives nuclear division.

Figure 2

Plasticity in nuclear remodelling across well-studied model systems. The compartment barrier is highlighted by labelling the nucleoplasm in blue and the cytoplasm in white; chromosomes are in dark grey and spindle microtubules in brown; other key cellular structures are labelled on the diagram. The presence (blue) or absence (grey) of homologues of an illustrative subset of the key protein or domain families involved in controlling nuclear remodelling is shown as a phylogenetic profile (filled circles) for each species. Differences in mitotic mode (closed or open) can be observed at large evolutionary distances, for example, between humans and fission yeast (illustrated by distance on the tree and low phylogenetic profile similarity), but also between closely related species, for example, S. pombe and S. japonicus (illustrated by proximity on the tree and high phylogenetic profile similarity). A divergence in lipin phosphorylation during mitosis [19] is thought to be responsible for the tearing of the nuclear envelope and loss of integrity in S. japonicus mitosis that is not observed during local NE breakdown [16,17] in its sister species S. pombe.