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Membrane and organelle dynamics during cell division

Nature Reviews Molecular Cell Biology volume 21, pages 151–166 (2020)Cite this article

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Abstract

During division, eukaryotic cells undergo a dramatic, complex and coordinated remodelling of their cytoskeleton and membranes. For cell division to occur, chromosomes must be segregated and new cellular structures, such as the spindle apparatus, must be assembled. Pre-existing organelles, such as the nuclear envelope, endoplasmic reticulum and Golgi apparatus, must be disassembled or remodelled, distributed and reformed. Smaller organelles such as mitochondria as well as cytoplasmic content must also be properly distributed between daughter cells. This mixture of organelles and cytoplasm is bound by a plasma membrane that is itself subject to remodelling as division progresses. The lipids resident in these different membrane compartments play important roles in facilitating the division process. In recent years, we have begun to understand how membrane remodelling is coordinated during division; however, there is still much to learn. In this Review, we discuss recent insights into how these important cellular events are performed and regulated.

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Fig. 1: Overview of organelle dynamics during division.
Fig. 2: Restructuring of the ER and nuclear envelope during cell division.
Fig. 3: Rearrangement of the Golgi during cell division.
Fig. 4: Mitochondrial dynamics during cell division.

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Acknowledgements

Work on membrane dynamics in the authors’ laboratories is funded by Wellcome Trust Investigator Award 110060/Z/15/Z (to U.E.) and Wellcome Trust Senior Fellowship 206346/Z/17/Z (to J.G.C). The Francis Crick Institute receives core funding from Cancer Research UK (FC001092), the UK Medical Research Council (FC001092) and the Wellcome Trust (FC001092).

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Authors and Affiliations

  1. School of Cancer and Pharmaceutical Sciences, King’s College London, London, UK

    Jeremy G. Carlton & Hannah Jones

  2. The Francis Crick Institute, London, UK

    Jeremy G. Carlton & Hannah Jones

  3. Randall Centre for Cell and Molecular Biophysics, School of Basic and Medical Biosciences and Department of Chemistry, King’s College London, London, UK

    Ulrike S. Eggert

Authors
  1. Jeremy G. Carlton
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  2. Hannah Jones
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  3. Ulrike S. Eggert
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Contributions

J.G.C. and U.S.E. contributed to all aspects of the article. H.J. researched data for the article and contributed to the writing, reviewing and editing of the manuscript.

Corresponding authors

Correspondence to Jeremy G. Carlton or Ulrike S. Eggert.

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The authors declare no competing interests.

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Related links

HUGO Gene Nomenclature Committee: https://www.genenames.org/

Supplementary information

Glossary

Mitotic spindle

A cytoskeletal structure, consisting primarily of microtubules, built during division to enable the segregation of duplicated chromatids into daughter cells.

Midbody

A transient microtubule-rich structure in mammalian cells that forms from the condensed spindle and represents the final connection between daughter cells.

Cytokinetic abscission

The terminal phase of cytokinesis, where the midbody is severed to produce two daughter cells.

Phosphoinositides

Also known as phosphatidylinositol phosphates. Differentially phosphorylated signalling lipids with many roles, involved in defining the identities of different membrane compartments and vesicles.

Cyclin proteins

Cell cycle regulatory proteins, the levels of which vary in a cyclical fashion to enable specific biochemical events to occur in different phases of the cell cycle.

Cyclin-dependent kinases

(CDKs). Protein kinases, the activity of which is strictly dependent upon association with a cyclin protein and is thus responsible for driving specific biochemical events in each phase of the cell cycle.

Aurora A

A mitotic serine/threonine protein kinase, the activity of which peaks during G2–M transition and is essential for spindle formation.

Aurora B

A mitotic serine/threonine protein kinase that complexes with members of the chromosome passenger complex and coordinates a number of events necessary for completion of cell division.

Polo-like kinase 1

(PLK1). A mitotic serine/threonine protein kinase that plays important roles in triggering M-phase entry, activation of the APC/C and later cytokinetic events.

Regulated proteolysis

The intentional destruction of proteins through ubiquitylation and proteasomal or lysosomal degradation.

Ubiquitin

A small 8.6 kDa protein that can be post-translationally attached to lysine residues on proteins of interest by E3 ubiquitin ligases, often resulting in its recognition by the proteasome for degradation.

Anaphase-promoting complex/cyclosome

(APC/C). A multiprotein E3 ubiquitin ligase that targets cell cycle proteins for proteasomal degradation.

Skp, cullin, F-box-containing complex

(SCF-containing complex). A multiprotein E3 ubiquitin ligase that targets cell cycle proteins for proteasomal degradation.

Cortex

An actin-rich layer immediately underneath the plasma membrane that plays important roles in cell shape control.

Membrane blebbing

The bulging of the cell membrane that protrudes into the extracellular environment when cortical connections are uncoupled.

G protein-coupled receptors

A receptor with seven transmembrane domains that can initiate intracellular signalling cascades in response to ligand binding.

Septin proteins

A group of filament-forming GTP-binding proteins that can function to recruit target proteins, scaffold complex assemblies or create diffusion barriers to restrict protein mobility.

Lipid modifications

Post-translational covalent attachment of a lipid group to specific residues within a protein, commonly to increase the affinity of the protein for membranes.

Nuclear pore complexes

(NPCs). A multi-subunit protein complex comprised of nucleoporin proteins that spans the nuclear envelope and allows regulated exchange of material between the nucleoplasm and cytoplasm.

Linker of nucleoskeleton and cytoskeleton complex

(LINC complex). A multi-subunit protein complex comprised of KASH and SUN domain proteins that spans the nuclear envelope and links the nuclear lamina to the cytoplasmic microtubule, actin and intermediate filament networks.

Morphometric proteins

A group of proteins that can shape organelles by inserting into, stabilizing or remodelling organellar membranes.

Dynamin

A GTPase involved in membrane fission reactions. Part of a larger superfamily of dynamin-like proteins.

Dynein

A microtubule-based molecular motor that travels towards the minus end of microtubules.

Nucleoporins

(NUPs). A family of proteins that help build the NPC.

Barrier-to-autointegration factor

(BAF). A small 10 kDa chromatin-binding protein that binds LEM domain-containing inner membrane proteins and participates in nuclear, and nuclear envelope, regeneration.

ESCRT-III

A membrane remodelling machinery that performs a topologically unique membrane fission activity called reverse topology membrane fission. See also Box 3.

Golgi reassembly and stacking proteins

(GRASPs). Myristoylated peripheral membrane proteins that localize to Golgi cisternae and trans-oligomerize to facilitate cisternal stacking.

C-terminal-binding protein 1/brefeldin A ADP-ribosylated substrate

(CtBP1/BARS). A dual function protein that regulates both transcriptional repression in the nucleus and membrane fission reactions in the cytoplasm.

SNARE

Membrane-embedded and soluble proteins that can oligomerize to mediate the fusion of vesicles with cellular membranes.

Sumoylated

A protein that has been post-translationally modified with a ubiquitin-like protein known as SUMO (small ubiquitin-related modifier). SUMO alters the protein’s function rather than targeting it for degradation.

Centromere protein F

(CENPF). A protein that associates with kinetochores in the G2 phase of the cell cycle and then localizes to the spindle midzone and midbody during cytokinesis.

Kinesin

Members of a family of microtubule-based molecular motors that typically travel towards the plus end of microtubules.

Clathrin

A lattice-like protein that forms a coat around vesicles during the endocytic budding process.

Exocyst

An octameric protein complex involved in tethering secretory vesicles to the plasma membrane.

Rab proteins

Members of the Ras superfamily of small GTPases that are specifically involved in membrane trafficking events.

Secondary ingression

A constriction generated in the midbody that specifies the site of cytokinetic abscission.

Autophagy

A catabolic process involving intentional sequestration of cytoplasm, organelles and/or foreign material and their targeting to the lysosome for proteolytic degradation and reutilization of cellular materials.

Centralspindlin complex

A protein complex involved in spindle assembly, microtubule bundling to form a midbody, cleavage furrow ingression, anchoring the midbody to the plasma membrane and recruitment of the ESCRT machinery to allow completion of cytokinesis.

Super-resolution

Forms of light microscopy that allow resolution to be achieved beyond the diffraction limit.

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Carlton, J.G., Jones, H. & Eggert, U.S. Membrane and organelle dynamics during cell division. Nat Rev Mol Cell Biol 21, 151–166 (2020). https://doi.org/10.1038/s41580-019-0208-1

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