Biomimetism of Cellular Movement

Team Publications

Year of publication 2019

Simon C*, Kusters R*, Caorsi V*, Allard A, Abou-Ghali M, Manzi J, Di Cicco A, Lévy D, Lenz M, Joanny J-F, Campillo C, Plastino J, Sens P*, Sykes C* (2019 Mar 18)

Actin dynamics drive cell-like membrane deformation

Nature Physics : DOI : 10.1038/s41567-019-0464-1 Learn more
Summary

Cell membrane deformations are crucial for proper cell function. Specialized protein assemblies initiate inward or outward membrane deformations that the cell uses respectively to uptake external substances or probe the environment. The assembly and dynamics of the actin cytoskeleton are involved in this process, although their detailed role remains controversial. We show here that a dynamic, branched actin network is sufficient to initiate both inward and outward membrane deformation. The polymerization of a dense actin network at the membrane of liposomes produces inward membrane bending at low tension, while outward deformations are robustly generated regardless of tension. Our results shed light on the mechanism cells use to internalize material, both in mammalian cells, where actin polymerization forces are required when membrane tension is increased, and in yeast, where those forces are necessary to overcome the opposing turgor pressure. By combining experimental observations with physical modelling, we propose a mechanism that explains how membrane tension and the architecture of the actin network regulate cell-like membrane deformations.

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Dreier J, Castello M, Coceano G, Cáceres R, Plastino J, Vicidomini G, Testa I (2019 Feb 1)

Smart scanning for low-illumination and fast RESOLFT nanoscopy in vivo

Nature Communications : 10 : 556 : DOI : 10.1038/s41467-019-08442-4 Learn more
Summary

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Kelley LC, Chi Q, Cáceres R, Hastie E, Schindler AJ, Jiang Y, Matus DQ, Plastino J, Sherwood DR (2019 Jan 24)

Adaptive F-actin polymerization and localized ATP production drive basement membrane invasion in the absence of MMPs

Developmental Cell : 48 : 313-328 : DOI : 10.1016/j.devcel.2018.12.018 Learn more
Summary

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Year of publication 2018

Cáceres R, Bojanala N, Kelley LC, Dreier J, Manzi J, Di Federico F, Chi Q, Risler T, Testa I, Sherwood DR, Plastino J (2018 Nov 6)

Forces drive basement membrane invasion in Caenorhabditis elegans

Proceedings of the National Academy of Sciences USA : 115 : 11537-11542 : DOI : 10.1073/pnas.1808760115 Learn more
Summary

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Plastino J, Blanchoin L (2018 Aug 13)

Dynamic stability of the actin ecosystem

Journal of Cell Science : 132 : pii: jcs219832 : DOI : 10.1242/jcs.219832 Learn more
Summary

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Simon C, Caorsi V, Campillo C, Sykes C (2018 Jul 30)

Interplay between membrane tension and the actin cytoskeleton determines shape changes

Physical Biology : 5 : 065004 : DOI : 10.1088/1478-3975/aad1ab Learn more
Summary

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Patricia Bassereau, Rui Jin, Tobias Baumgart, Markus Deserno, Rumiana Dimova, Vadim A. Frolov, Pavel V. Bashkirov, Helmut Grubmüller, Reinhard Jahn, H. Jelger Risselada, Ludger Johannes, Michael M. Kozlov, Reinhard Lipowsky, Thomas J. Pucadyil, Wade F. Zeno, Jeanne C. Stachowiak, Dimitrios Stamou, Artù Breuer, Line Lauritsen, Camille Simon, Cécile Sykes, Gregory A. Voth, Thomas R Weikl (2018 Jul 20)

The 2018 biomembrane curvature and remodeling roadmap.

Journal of Physics D: Applied Physics : 51 : 343001 : DOI : 10.1088/1361-6463/aacb98 Learn more
Summary

The importance of curvature as a structural feature of biological membranes has been recognized for many years and has fascinated scientists from a wide range of different backgrounds. On the one hand, changes in membrane morphology are involved in a plethora of phenomena involving the plasma membrane of eukaryotic cells, including endo- and exocytosis, phagocytosis and filopodia formation. On the other hand, a multitude of intracellular processes at the level of organelles rely on generation, modulation, and maintenance of membrane curvature to maintain the organelle shape and functionality. The contribution of biophysicists and biologists is essential for shedding light on the mechanistic understanding and quantification of these processes.

Given the vast complexity of phenomena and mechanisms involved in the coupling between membrane shape and function, it is not always clear in what direction to advance to eventually arrive at an exhaustive understanding of this important research area. The 2018 Biomembrane Curvature and Remodeling Roadmap of Journal of Physics D: Applied Physics addresses this need for clarity and is intended to provide guidance both for students who have just entered the field as well as established scientists who would like to improve their orientation within this fascinating area.

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Sherwood DR, Plastino J (2018 Jan 1)

Invading, leading and navigating cells in Caenorhabditis elegans: insights into cell movement in vivo

Genetics : 208 : 53-78 : DOI : 10.1534/genetics.117.300082 Learn more
Summary

Highly regulated cell migration events are crucial during animal tissue formation and the trafficking of cells to sites of infection and injury. Misregulation of cell movement underlies numerous human diseases, including cancer. Although originally studied primarily in two-dimensional in vitro assays, most cell migrations in vivo occur in complex three-dimensional tissue environments that are difficult to recapitulate in cell culture or ex vivo Further, it is now known that cells can mobilize a diverse repertoire of migration modes and subcellular structures to move through and around tissues. This review provides an overview of three distinct cellular movement events in Caenorhabditis eleganscell invasion through basement membrane, leader cell migration during organ formation, and individual cell migration around tissues-which together illustrate powerful experimental models of diverse modes of movement in vivo We discuss new insights into migration that are emerging from these in vivo studies and important future directions toward understanding the remarkable and assorted ways that cells move in animals.

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Year of publication 2017

Plastino J, Blanchoin L (2017 Sep 25)

Adaptive actin networks

Developmental Cell : 42 : 565-566 : DOI : 10.1016/j.devcel.2017.09.005 Learn more
Summary

Despite their fundamental importance in the regulation of cell physiology, the mechanisms that confer cell adaptability to changes in the microenvironment are poorly understood. A recent study in Cell (Mueller et al., 2017) examines the capability of branched actin networks to respond and adapt to mechanical load in vivo.

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Rückerl F, Lenz M, Betz T, Manzi J, Martiel J-L, Safouane M, Paterski-Boujemaa R, Blanchoin L, Sykes C (2017 Sep 5)

Adaptive response of actin bundles under mechanical stress

Biophysical Journal : 113 : 1072-1079 : DOI : 10.1016/j.bpj.2017.07.017 Learn more
Summary

Actin is one of the main components of the architecture of cells. Actin filaments form different polymer networks with versatile mechanical properties that depend on their spatial organization and the presence of cross-linkers. Here, we investigate the mechanical properties of actin bundles in the absence of cross-linkers. Bundles are polymerized from the surface of mDia1-coated latex beads, and deformed by manipulating both ends through attached beads held by optical tweezers, allowing us to record the applied force. Bundle properties are strikingly different from the ones of a homogeneous isotropic beam. Successive compression and extension leads to a decrease in the buckling force that we attribute to the bundle remaining slightly curved after the first deformation. Furthermore, we find that the bundle is solid, and stiff to bending, along the long axis, whereas it has a liquid and viscous behavior in the transverse direction. Interpretation of the force curves using a Maxwell visco-elastic model allows us to extract the bundle mechanical parameters and confirms that the bundle is composed of weakly coupled filaments. At short times, the bundle behaves as an elastic material, whereas at long times, filaments flow in the longitudinal direction, leading to bundle restructuring. Deviations from the model reveal a complex adaptive rheological behavior of bundles. Indeed, when allowed to anneal between phases of compression and extension, the bundle reinforces. Moreover, we find that the characteristic visco-elastic time is inversely proportional to the compression speed. Actin bundles are therefore not simple force transmitters, but instead, complex mechano-transducers that adjust their mechanics to external stimulation. In cells, where actin bundles are mechanical sensors, this property could contribute to their adaptability.

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Cáceres R, Plastino J (2017 Apr 17)

Cytoskeleton dynamics: actin in cell invasion

Encyclopedia of Life Sciences : DOI : 10.1002/9780470015902.a0001254.pub2 Learn more
Summary

Basement membrane (BM) is a dense sheet of specialised extracellular matrix that separates epithelial layers of cells from the underlying tissue. The penetration of cells through BM barriers, called ‘invasion’, is an important process during normal tissue development and in cancer metastasis. To enable invasion, the cell adopts different shapes and creates different protrusive structures powered mainly by actin cytoskeleton dynamics. However, the exact cytoskeletal strategy that the cell uses to cross the physical BM barrier depends on the physiological context and the physical environment, as observed by examining actin structures in invading cancer and immune cells, and in cells that invade during developmental processes such as angiogenesis and anchor cell invasion in Caenorhabditis elegans.

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Year of publication 2016

Valentino F, Sens P, Lemière J, Allard A, Betz T, Campillo C, Sykes C (2016 Nov 28)

Fluctuations of a membrane nanotube revealed by high-resolution force measurements

Soft Matter : 12 : 9429-9435 : DOI : 10.1039/c6sm02117d Learn more
Summary

Pulling membrane nanotubes from liposomes presents a powerful method to gain access to membrane mechanics. Here we extend classical optical tweezers studies to infer membrane nanotube dynamics with high spatial and temporal resolution. We first validate our force measurement setup by accurately measuring the bending modulus of EPC membrane in tube pulling experiments. Then we record the position signal of a trapped bead when it is connected, or not, to a tube. We derive the fluctuation spectrum of these signals and find that the presence of a membrane nanotube induces higher fluctuations, especially at low frequencies (10-1000 Hz). We analyse these spectra by taking into account the peristaltic modes of nanotube fluctuations. This analysis provides a new experimental framework for a quantitative study of the fluctuations of nanotubular membrane structures that are present in living cells, and now classically used for in vitro biomimetic approaches.

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Lemière J, Valentino F, Campillo C, Sykes C (2016 Nov 1)

How cellular membrane properties are affected by the actin cytoskeleton.

Biochimie : 130 : 33-40 : DOI : 10.1016/j.biochi.2016.09.019 Learn more
Summary

Lipid membranes define the boundaries of living cells and intracellular compartments. The dynamic remodelling of these membranes by the cytoskeleton, a very dynamic structure made of active biopolymers, is crucial in many biological processes such as motility or division. In this review, we present some aspects of cellular membranes and how they are affected by the presence of the actin cytoskeleton. We show that, in parallel with the direct study of membranes and cytoskeleton in vivo, biomimetic in vitro systems allow reconstitution of biological processes in a controlled environment. In particular, we show that liposomes, or giant unilamellar vesicles, encapsulating a reconstituted actin network polymerizing at their membrane are suitable models of living cells and can be used to decipher the relative contributions of membrane and actin on the mechanical properties of the cellular interface.

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Caorsi V, Lemière J, Campillo C, Bussonnier M, Manzi J, Betz T, Plastino J, Carvalho K, Sykes C (2016 Jul 20)

Cell-sized liposome doublets reveal active tension build-up driven by acto-myosin dynamics

Soft Matter : 12 : 6223-31 : DOI : 10.1039/c6sm00856a Learn more
Summary

Cells modulate their shape to fulfill specific functions, mediated by the cell cortex, a thin actin shell bound to the plasma membrane. Myosin motor activity, together with actin dynamics, contributes to cortical tension. Here, we examine the individual contributions of actin polymerization and myosin activity to tension increase with a non-invasive method. Cell-sized liposome doublets are covered with either a stabilized actin cortex of preformed actin filaments, or a dynamic branched actin network polymerizing at the membrane. The addition of myosin II minifilaments in both cases triggers a change in doublet shape that is unambiguously related to a tension increase. Preformed actin filaments allow us to evaluate the effect of myosin alone while, with dynamic actin cortices, we examine the synergy of actin polymerization and myosin motors in driving shape changes. Our assay paves the way for a quantification of tension changes triggered by various actin-associated proteins in a cell-sized system.

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Chaigne A, Campillo C, Voituriez R, Gov NS, Sykes C, Verlhac MH, Terret ME (2016 Jan 4)

F-actin mechanics control spindle centring in the mouse zygote

Nature Communications : 7 : 10253 : DOI : 10.1038/ncomms10253 Learn more
Summary

Mitotic spindle position relies on interactions between astral microtubules nucleated by centrosomes and a rigid cortex. Some cells, such as mouse oocytes, do not possess centrosomes and astral microtubules. These cells rely only on actin and on a soft cortex to position their spindle off-centre and undergo asymmetric divisions. While the first mouse embryonic division also occurs in the absence of centrosomes, it is symmetric and not much is known on how the spindle is positioned at the exact cell centre. Using interdisciplinary approaches, we demonstrate that zygotic spindle positioning follows a three-step process: (1) coarse centring of pronuclei relying on the dynamics of an F-actin/Myosin-Vb meshwork; (2) fine centring of the metaphase plate depending on a high cortical tension; (3) passive maintenance at the cell centre. Altogether, we show that F-actin-dependent mechanics operate the switch between asymmetric to symmetric division required at the oocyte to embryo transition.

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