Compression and dilation of the membrane-cortex layer generates rapid changes in cell shape

Kapustina, Maryna; Elston, Timothy C.; Jacobson, Ken

doi:10.1085/jgp1411oia3

Cited by 6 publications

(10 citation statements)

References 15 publications

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“…A laterally propagating compression/dilation wave of the coupled actin cortex and plasma membrane is the major feature of the periodic protrusive phenotype. This wave, first discovered in [Kapustina et al, 2013], and the associated cell morphological behavior [Pletjushkina et al, 2001;Costigliola et al, 2010] has many similarities to the blebby type of amoeboid migration. Thus, for example both phenotypes exhibit rounded protrusions, low adhesion and strong dependence on RhoA activation [Friedl and Wolf, 2010; Blanchoin et al, 2014).…”

Section: Discussionmentioning

confidence: 94%

“…In our previous work [Kapustina et al, 2013] we suggested that the compression (folding) and dilation (unfolding) of the coupled plasma membrane-actin cortex layer may be used as a general mechanism for rapid transformations of rounded cells. We investigated the periodic protrusions that can be exhibited spontaneously by many cells following rapid detachment from a substrate.…”

Section: Introductionmentioning

confidence: 99%

“…1B. The propagating wave of cortex density is likely to be only sustainable in cells with rounded morphology, where the available plasma membrane area is greater than is required to contain the cell volume [Kapustina et al, 2013].…”

Section: Introductionmentioning

confidence: 99%

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Spatiotemporal relationships between the cell shape and the actomyosin cortex of periodically protruding cells

et al. 2015

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We investigate the dynamics of cell shape and analyze the actin and myosin distributions of cells exhibiting cortical density traveling waves. These waves propagate by repeated cycles of cortical compression (folding) and dilation (unfolding) that lead to periodic protrusions (oscillations) of the cell boundary. The focus of our detailed analysis is the remarkable periodicity of this phenotype, in which both the overall shape transformation and distribution of actomyosin density are repeated from cycle to cycle even though the characteristics of the shape transformation vary significantly for different regions of the cell. We show, using correlation analysis, that during traveling wave propagation cortical actin and plasma membrane densities are tightly coupled at each point along the cell periphery. We also demonstrate that the major protrusion appears at the wave trailing edge just after the actin cortex density has reached a maximum. Making use of the extraordinary periodicity, we employ latrunculin to demonstrate that sequestering actin monomers can have two distinct effects: low latrunculin concentrations can trigger and enhance traveling waves but higher concentrations of this drug retard the waves. The fundamental mechanism underlying this periodically protruding phenotype, involving folding and unfolding of the cortex-membrane couple, is likely to hold important clues for diverse phenomena including cell division and amoeboid-type migration.

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Section: Discussionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

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Spatiotemporal relationships between the cell shape and the actomyosin cortex of periodically protruding cells

et al. 2015

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“…In contrast to cytochalasin D, membrane blebbing was increased, suggesting that bleb retraction rather than bleb formation was impaired. At first glance this result is in contrast to the observations made on continuously blebbing cells, where blebbistatin blocks membrane blebbing (Charras et al 2005(Charras et al , 2006Kapustina et al 2013). Continuous blebbing is based on oscillating fluctuations of Ca 2+ that trigger rhythmic actomyosin cortex contractions followed by bleb formation in the plasma membrane and subsequent bleb retraction (Charras et al 2006).…”

Section: Discussionmentioning

confidence: 79%

“…Finally membrane blebs retract by myosin II contraction mediated by myosin II kinase and the small GTPase Rho (Charras et al 2006). Some authors suggest that the formation of membrane blebs could function as a mechanism for directed cell migration to chemoattractants (Blaser et al 2006;Kapustina et al 2013).…”

Section: Introductionmentioning

confidence: 99%

Bradykinin enhances invasion of malignant glioma into the brain parenchyma by inducing cells to undergo amoeboid migration

Seifert

Sontheimer

2014

The Journal of Physiology

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Key pointsr Glioma multiforme is a fast expanding and aggressive type of brain tumour that invades healthy brain tissue by migration of single glioma cells along blood vessels.r We show that bradykinin, a neuropeptide of the vasculature, induces the formation of small bleb-like protrusions at the plasma membrane of glioma cells in vitro, which are regulated by intracellular Ca 2+ , resulting in contraction of the cytoskeleton, cytoplasmatic flow and activation of Ca 2+ -dependent K + and Cl − channels.r From our in vitro experiments we conclude that bradykinin facilitates glioma invasion by stimulating an amoeboid phenotype of migration.r In situ experiments confirmed that bradykinin increases the speed of glioma cell migration, which we have been able to block with blebbistatin, an inhibitor of membrane blebbing, and with the B2 receptor agonist Hoe-140.r The study reveals novel mechanisms of bradykinin-induced glioma migration and suggests pharmacological targets to reduce glioma invasion.Abstract The molecular and cellular mechanisms governing cell motility and directed migration in response to the neuropeptide bradykinin are largely unknown. Here, we demonstrate that human glioma cells whose migration is guided by bradykinin generate bleb-like protrusions. We found that activation of the B2 receptor leads to a rise in free Ca 2+ from internal stores that activates actomyosin contraction and subsequent cytoplasmic flow into protrusions forming membrane blebs. Furthermore Ca 2+ activates Ca 2+ -dependent K + and Cl − channels, which participate in bleb regulation. Treatment of gliomas with bradykinin in situ increased glioma growth by increasing the speed of cell migration at the periphery of the tumour mass. To test if bleb formation is related to bradykinin-promoted glioma invasion we blocked glioma migration with blebbistatin, a blocker of myosin kinase II, which is necessary for proper bleb retraction. Our findings suggest a pivotal role of bradykinin during glioma invasion by stimulating amoeboid migration of glioma cells.

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Actin shells control buckling and wrinkling of biomembranes

et al. 2019

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Compression and dilation of the membrane-cortex layer generates rapid changes in cell shape

Cited by 6 publications

References 15 publications

Spatiotemporal relationships between the cell shape and the actomyosin cortex of periodically protruding cells

Spatiotemporal relationships between the cell shape and the actomyosin cortex of periodically protruding cells

Bradykinin enhances invasion of malignant glioma into the brain parenchyma by inducing cells to undergo amoeboid migration

Actin shells control buckling and wrinkling of biomembranes

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