Trends in Cell Biology
Volume 15, Issue 2, February 2005, Pages 92-101
Journal home page for Trends in Cell Biology

Cytokinesis series
Membrane traffic: a driving force in cytokinesis

https://doi.org/10.1016/j.tcb.2004.12.008Get rights and content

Dividing animal and plant cells maintain a constant chromosome content through temporally separated rounds of replication and segregation. Until recently, the mechanisms by which animal and plant cells maintain a constant surface area have been considered to be distinct. The prevailing view was that surface area was maintained in dividing animal cells through temporally separated rounds of membrane expansion and membrane invagination. The latter event, known as cytokinesis, produces two physically distinct daughter cells and has been thought to be primarily driven by actomyosin-based constriction. By contrast, membrane addition seems to be the primary mechanism that drives cytokinesis in plants and, thus, the two events are linked mechanistically and temporally. In this article (which is part of the Cytokinesis series), we discuss recent studies of a variety of organisms that have made a convincing case for membrane trafficking at the cleavage furrow being a key component of both animal and plant cytokinesis.

Introduction

Basic light-microscopic observations highlight the differences between plant and animal cytokinesis. During plant cell division, a specialized structure known as the phragmoplast forms at the cell center. The phragmoplast consists of membrane, microtubules and microfilaments, and promotes the concentration and fusion of secretory vesicles [1]. Thus, plant cytokinesis proceeds from the cell center towards the cortex, relying primarily on vesicle fusion. This process involves delivery of cell wall and membrane components, and requires actomyosin for expansion and fusion of the newly formed membrane with the plasma membrane. By contrast, cytokinesis in animal cells relies on a pronounced actomyosin contractile ring that drives plasma membrane invagination from the cortex. An important feature of this ‘purse-string’ model is that, with the exception of the terminal sealing event, it does not require cleavage furrow ingression and membrane addition to be linked temporally and spatially. According to this basic model, additional membrane could be incorporated at any time and anywhere along the plasma membrane before the terminal events of cytokinesis. Reinforcing the distinction between plant and animal cytokinesis is the fact that secretion remains active throughout the cell cycle in plants but is dramatically downregulated during mitosis in animal cells 2, 3.

Recent advances in microscopy, a new generation of fluorescent probes and sophisticated functional approaches have begun to highlight the similarities between plant and animal cytokinesis. Specifically, studies of a variety of animal systems have revealed that, like plants, membrane trafficking has an important role during animal cytokinesis (Figure 1, Figure 2 and Table 1, Table 2). These studies demonstrate that targeted membrane addition during cleavage furrow formation is a fundamental and widely conserved mechanism of animal cytokinesis. This insight has opened new avenues of investigation that are now rapidly being addressed: what are the sources of membrane; when and where is membrane added and removed during cytokinesis; how do membrane-trafficking pathways regulate membrane delivery to and from the cleavage furrow; what role does the cytoskeleton have in this process; and why are the distinct protein and lipid compositions at the furrow important for cytokinesis? In this article, we highlight recent progress in these areas (for further reviews about specific aspects of plant and animal cytokinesis, see Refs 3, 4, 5, 6, 7, 8, 9).

Section snippets

Cytokinesis in animal cells often requires on-time delivery of Golgi-derived membrane

The additional membrane required for cytokinesis has several possible origins such as excess membrane stored within the plasma membrane, and internal membrane derived from secretory, endocytic or recycling pathways (Figure 2). In amphibian embryos, microvilli observed during the initiation of cytokinesis might provide the required membrane [10]. In cellularizing Drosophila embryos, excess membrane stored as microprojections is a possible source [11]. Studies have also emphasized the role of

Golgi disassembly is required for cytokinesis

Golgi have at least two distinct roles in promoting cytokinesis: supplying membrane through Golgi-mediated vesicle addition and supplying cytokinetic regulatory proteins through cell-cycle-mediated release of Golgi-associated proteins [14] (Figure 2). In many cell types, Golgi undergo an ordered stepwise disassembly as the cells enter mitosis [25]. A recent study has identified the small GTPase Arf1 as being a regulator of Golgi mitotic disassembly [26]. As cells enter mitosis, Arf1 becomes

Endocytosis and cytokinesis

Considering that cytokinesis requires the incorporation of additional membrane, it is surprising that endocytosis-based membrane trafficking is also required for cytokinesis (Figure 2, Table 1). In Dictyostelium discoideum, the completion of cytokinesis is dependent upon clathrin and dynamin, which are membrane-associated proteins that promote vesicle budding from the plasma membrane [30]. Other studies support a role for endocytosis-associated proteins in promoting animal cytokinesis. In

Cytokinesis involves homotypic and heterotypic membrane fusion

EM analysis of cleaving Xenopus embryos provides dramatic visual evidence that vesicle fusion has a role in cytokinesis [17] (Figure 3a). The region immediately behind the leading edge of the cleavage furrow is heavily pockmarked with fusion pores. Vesicle fusion is central to many membrane-based cellular processes, including synaptic transmission, organelle inheritance and epithelial polarity, and much is known about the underlying molecular mechanisms. Membrane fusions are classified as being

Cytokinesis is linked to establishment and maintenance of distinct cortical domains

Cortical domains, which contain a distinct protein and lipid composition, represent functionally specialized regions of the plasma membrane that are necessary for several biological processes. Establishment and maintenance of cortical domains require: (i) the site-specific targeting of proteins and lipids; (ii) the restriction of cortical proteins and lipids within the domain; and (iii) the exclusion of protein and lipid diffusion from adjacent domains and the cytoplasm. Animal cells use

Concluding remarks

The realization that membrane dynamics have an active role in animal cytokinesis forces us to reconsider many of the outstanding issues in the field. Foremost among these is the identification of the factors and mechanisms responsible for establishing cleavage furrow position. Influenced by developmental biologists and their successful hunt for morphogens, the field has been anticipating that a protein will prove to be the mythical cleavage furrow determinant. It is likely that the plasma

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