Optical volume and mass measurements show that mammalian cells swell during mitosis

Zlotek-Zlotkiewicz, Ewa; Monnier, Sylvain; Cappello, Giovanni; Berre, Maël Le; Piel, Matthieu

doi:10.1083/jcb.201505056

Cited by 209 publications

(262 citation statements)

References 31 publications

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“…Simultaneously, the mixing of cytoplasm and nucleoplasm induced by the loss of the nuclear compartment is likely to induce a sudden drop in the concentration of proteins localized to only one of the two compartments -inducing profound changes in cellular biochemistry and cytoarchitecture. This is augmented by osmotic swelling 59 and a sudden influx of water, leading to a significant (>10%) increase in cell volume that is independent of the actin cytoskeleton 60,61 and a dramatic increase in cell height 59,62,63 . In combin ation, changes in cell architecture, actin remodelling, cell-substrate adhesion and osmotic swelling, cause cells to assume a spherical shape by the time they have assembled a metaphase plate (FIGS 1,3a).…”

Section: Non-muscle Myosin IImentioning

confidence: 99%

Coupling changes in cell shape to chromosome segregation

Ramkumar

Baum

2016

Nat Rev Mol Cell Biol

129

132

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Animal cells undergo dramatic changes in shape, mechanics and polarity as they progress through the different stages of cell division. These changes begin at mitotic entry, with cell-substrate adhesion remodelling, assembly of a cortical actomyosin network and osmotic swelling, which together enable cells to adopt a near spherical form even when growing in a crowded tissue environment. These shape changes, which probably aid spindle assembly and positioning, are then reversed at mitotic exit to restore the interphase cell morphology. Here, we discuss the dynamics, regulation and function of these processes, and how cell shape changes and sister chromatid segregation are coupled to ensure that the daughter cells generated through division receive their fair inheritance.

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Section: Non-muscle Myosin IImentioning

confidence: 99%

Coupling changes in cell shape to chromosome segregation

Ramkumar

Baum

2016

Nat Rev Mol Cell Biol

129

132

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“…In fact, the sensitivity of weak complex populations to cellular volume changes suggests a class of protein complexes whose association strongly depends on cellular crowding conditions. Such complexes imbue the cell with the ability to detect, signal, and/or directly initiate regulatory processes quickly and effectively in response to external stresses or internal signals, such as the rapid volume increase that occurs upon entry to mitosis (20,23).…”

Section: Discussionmentioning

confidence: 99%

“…Our model predicts that this sensitivity is particularly high when the dissociation constant K d is of the order of the protein's cellular concentration. It is known that the cell changes its volume as part of an internal regulatory process, or in response to environmental duress (20,23). We propose that such cellular volume change can trigger regulatory responses rapidly and reversibly, purely by altering the concentrations of complexed proteins, an effect that is amplified because the free volume (the volume that is occupied by water and other small, permeable solutes) in the cell is less than the overall cellular volume.…”

mentioning

confidence: 99%

“…Volume change is a mild perturbation that happens routinely: Cells change their volume by up to 30% in both routine cell-cycle changes and in response to deleterious conditions (19)(20)(21). Rapid volume changes (approximately 1-100 s) are driven by water influx or efflux, altering the concentration of all molecular species contained within the cellular matrix (19,22,23).…”

mentioning

confidence: 99%

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Weak protein–protein interactions in live cells are quantified by cell-volume modulation

Sukenik

Ren

Gruebele

2017

Proc. Natl. Acad. Sci. U.S.A.

104

123

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Weakly bound protein complexes play a crucial role in metabolic, regulatory, and signaling pathways, due in part to the high tunability of their bound and unbound populations. This tunability makes weak binding (micromolar to millimolar dissociation constants) difficult to quantify under biologically relevant conditions. Here, we use rapid perturbation of cell volume to modulate the concentration of weakly bound protein complexes, allowing us to detect their dissociation constant and stoichiometry directly inside the cell. We control cell volume by modulating media osmotic pressure and observe the resulting complex association and dissociation by FRET microscopy. We quantitatively examine the interaction between GAPDH and PGK, two sequential enzymes in the glycolysis catalytic cycle. GAPDH and PGK have been shown to interact weakly, but the interaction has not been quantified in vivo. A quantitative model fits our experimental results with log K d = −9.7 ± 0.3 and a 2:1 prevalent stoichiometry of the GAPDH:PGK complex. Cellular volume perturbation is a widely applicable tool to detect transient protein interactions and other biomolecular interactions in situ. Our results also suggest that cells could use volume change (e.g., as occurs upon entry to mitosis) to regulate function by altering biomolecular complex concentrations.quinary interactions | protein-protein interactions | cell volume | FRET | live-cell microscopy F rom forming active enzymatic complexes to facilitating signal transduction in regulatory networks, protein interactions are pivotal to cell function. Strong interactions, with dissociation constants (K d ) of nanomolar and lower (1, 2), can be measured accurately both in vitro and in vivo (3, 4). These interactions are ideal in cases where the complex should form with high fidelity and persist. The downside of strong binding is that its regulation in the cellular environment is limited: Once a complex is formed, it seldom dissociates.Another type of protein complexes relies on weak, transient interactions, collectively termed quinary interactions (5-7). Such interactions, with a K d in the micromolar to millimolar range, are emerging as important components of the cell's signaling, regulatory, and stress adaptation mechanisms (6,8,9). Their transient nature is key to their function: Unlike tightly bound complexes, quinary interactions are highly sensitive to variations in their environment and respond rapidly to changes in temperature, pressure, pH, or the local concentration of surrounding molecules. The sensitivity of quinary interactions makes them important in fine-tuning cellular processes. For example, it has been proposed that sequential metabolic enzymes could associate to improve substrate transfer between catalytic enzymes (10), that weak protein association can mediate cytokine release (11), or that phase-separated protein droplets held together by quinary interactions could serve for cellular storage or stress response (12, 13).Despite growing interest, quantification of quinary inte...

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“…There is experimental evidence that mammalian cells swell prior to cell division 24 and that centrosomes may also change size 25 . Additionally, a correlation between cell and centrosome sizes has been demonstrated in C. Elegans 26 .…”

Section: Shapes With Two Defects: Bipolar Divisionmentioning

confidence: 99%

Defect driven shapes in nematic droplets: analogies with cell division

et al. 2017

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Building on the striking similarity between the structure of the spindle during mitosis in living cells and nematic textures in confined liquid crystals, we use a continuum model of two-dimensional nematic liquid crystal droplets, to examine the physical aspects of cell division. The model investigates the interplay between bulk elasticity of the microtubule assembly, described as a nematic liquid crystal, and surface elasticity of the cell cortex, modelled as a bounding flexible membrane, in controlling cell shape and division. The centrosomes at the spindle poles correspond to the cores of the topological defects required to accommodate nematic order in a closed geometry. We map out the progression of both healthy bipolar and faulty multi-polar division as a function of an effective parameter that incorporates active processes and controls centrosome separation. A robust prediction, independent of energetic considerations, is that the transition from a single cell to daughters cells occurs at critical value of this parameter. Our model additionally suggests that microtubule anchoring at the cell cortex may play an important role for successful bipolar division. This can be tested experimentally by regulating microtubule anchoring.Comment: 10 pages, 7 figure

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Optical volume and mass measurements show that mammalian cells swell during mitosis

Abstract: Mammalian cells display a significant increase in volume during mitosis, which corresponds to a decrease in cell density, is linked to the mitotic state and not to the cell shape, and is independent of the actomyosin cortex.

Cited by 209 publications

References 31 publications

Coupling changes in cell shape to chromosome segregation

Coupling changes in cell shape to chromosome segregation

Weak protein–protein interactions in live cells are quantified by cell-volume modulation

Defect driven shapes in nematic droplets: analogies with cell division

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