Three-Dimensional Characterization of Active Membrane Waves on Living Cells

Chen, Chien-Hong; Tsai, Feng-Ching; Wang, Chun‐Chieh; Lee, Chau‐Hwang

doi:10.1103/physrevlett.103.238101

Cited by 40 publications

(31 citation statements)

References 18 publications

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“…Very interestingly, membrane waves were described in the recent years and introduced as a new mechanistic component in the understanding of cell motility [13]–[16]. In fact, cells have the ability to produce centripetally propagating waves on their membranes, which are traveling membrane undulations that persist over microns.…”

Section: Introductionmentioning

confidence: 99%

“…Such membrane waves have been observed in a variety of cells [13], [17], [18]. For example, on fibroblasts, the amplitudes of these waves were shown to be smaller than 300 nm [16]. Furthermore, these waves are believed to play a key role in cellular motility but also in probing of the surrounding matrix, endocytosis and internalization of membrane receptors [19].…”

Section: Introductionmentioning

confidence: 99%

“…We perform this by using a superresolution in depth microscopy technique called “optical profilometry” [16], [24]–[26] which provides with our configuration [27], [28] a depth profiling accuracy of around 1,2 nm and lateral resolution of about 200 nm ( figure S1 ). Because the optical profilometry technique profiles sample surface by light waves, it does not induce variations of membrane topography.…”

Section: Introductionmentioning

confidence: 99%

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Membrane Nanowaves in Single and Collective Cell Migration

2014

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We report the characterization of three-dimensional membrane waves for migrating single and collective cells and describe their propagation using wide-field optical profiling technique with nanometer resolution. We reveal the existence of small and large membrane waves the amplitudes of which are in the range of ∼3–7 nm to ∼16–25 nm respectively, through the cell. For migrating single-cells, the amplitude of these waves is about 30 nm near the cell edge. Two or more different directions of propagation of the membrane nanowaves inside the same cell can be observed. After increasing the migration velocity by BMP-2 treatment, only one wave direction of propagation exists with an increase in the average amplitude (more than 80 nm near the cell edge). Furthermore for collective-cell migration, these membrane nanowaves are attenuated on the leader cells and poor transmission of these nanowaves to follower cells was observed. After BMP-2 treatment, the membrane nanowaves are transmitted from the leader cell to several rows of follower cells. Surprisingly, the vast majority of the observed membrane nanowaves is shared between the adjacent cells. These results give a new view on how single and collective-cells modulate their motility. This work has significant implications for the therapeutic use of BMPs for the regeneration of skin tissue.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Membrane Nanowaves in Single and Collective Cell Migration

2014

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“…Other details of NIWOP measurement on cell membrane roughness can be found in our previous publications. [15][16][17] The NIWOP system was constructed on an upright microscope, and we used a spatial light modulator to generate the pattern for structured illumination. The microscope and the piezoelectric transducer (PZT)-driven vertical stage were placed in a temperature-controlled incubator, which kept the temperature at 37 AE 1°C during the experiment.…”

Section: Setup Of Niwopmentioning

confidence: 99%

“…The NIWOP technique has been used to measure the dynamical membrane ripples on live cells. [15][16][17] Compared with atomic force microscopy, the NIWOP technique is faster and noncontact, and therefore the membrane topography as well as the cell viability is not perturbed during the measurement. In addition, because the NIWOP setup is constructed on a conventional optical microscope, it is compatible with current cell culture devices and easy to conduct various treatments during the observation.…”

Section: Introductionmentioning

confidence: 99%

Using optical profilometry to characterize cell membrane roughness influenced by amyloid-beta 42 aggregates and electric fields

et al. 2013

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Abstract. The membrane roughness of Neuro-2a neroblastoma cells is measured by using noninterferometric widefield optical profilometry. The cells are treated with the fibril and oligomer conformers of amyloid-beta (Aβ) 42, which is a peptide of 42 amino acids related to the development of Alzheimer's disease. We find that both the Aβ42 fibrils and Aβ42 oligomers reduced the cell membrane roughness, but the effect of Aβ42 oligomers was faster and stronger than that of the fibrils. We also apply direct-current electric field (dcEF) stimulations on the cells. A dcEF of 300 mV∕mm can increase the membrane roughness under the treatment of Aβ42. These results suggest that Aβ42 can decrease the membrane compliance of live neuroblastoma cells, and dcEFs may counteract this effect. © The Authors. Published by SPIE under a Creative Commons Attribution 3.0 Unported License. Distribution or reproduction of this work in whole or in part requires full attribution of the original publication, including its DOI.

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A review of models of fluctuating protrusion and retraction patterns at the leading edge of motile cells

2012

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A characteristic feature of motile cells as they undergo a change in motile behavior is the development of fluctuating exploratory motions of the leading edge, driven by actin polymerization. We review quantitative models of these protrusion and retraction phenomena. Theoretical studies have been motivated by advances in experimental and computational methods that allow controlled perturbations, single molecule imaging, and analysis of spatiotemporal correlations in microscopic images. To explain oscillations and waves of the leading edge, most theoretical models propose nonlinear interactions and feedback mechanisms among different components of the actin cytoskeleton system. These mechanisms include curvature-sensing membrane proteins, myosin contraction, and autocatalytic biochemical reaction kinetics. We discuss how the combination of experimental studies with modeling promises to quantify the relative importance of these biochemical and biophysical processes at the leading edge and to evaluate their generality across cell types and extracellular environments. V C 2012 Wiley Periodicals, Inc Key Words: actin, cell motility, lamellipodium dynamics, mathematical modeling, single molecule microscopy Introduction E ukaryotic cell motility is driven by actin protrusions at the leading edge, formation of adhesions, and myosin-driven contraction at the trailing edge. Understanding the function of these three motility components has inspired a huge body of biological, biochemical, and modeling work [Mogilner and Keren, 2009;Pollard and Cooper, 2009;Carlsson, 2010a;Watanabe, 2010]. Prior work has addressed many of the underlying molecular mechanisms of protrusion, adhesion, and retraction, as well as their combined influence in determining cell shape and motion. Many works have also examined the mechanisms of control of cell motility: how cells respond to stimuli in order to reorganize their cytoskeleton and move along a preferred direction [Jilkine and Edelstein-Keshet, 2010].In this review, we focus on a dynamical pattern of motile cells that involves cycles of protrusion-and-retraction (CPAR) of the leading edge. This type of motion consists of back and forth movements of the leading edge over a few microns over a few minutes. It is usually more pronounced as cells change polarization states, for example, during cell spreading or cell stimulation (Fig. 1). CPAR dynamics occur reproducibly in experiments and are easy to quantify as compared to other more complex features of cell shape. Statistical analysis of these repeated motions can provide insight into the regulatory mechanisms of motility. For this reason, in addition to novel experimental work, they have motivated mathematical and computational modeling studies and development of image analysis methods. We discuss some of the conceptual contributions of these quantitative studies to cell motility research and challenges for future feedback between experiment and theory.One of the best examples of CPAR occurs during cell spreading [Dobereiner et al., , 2006Du...

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Three-Dimensional Characterization of Active Membrane Waves on Living Cells

Cited by 40 publications

References 18 publications

Membrane Nanowaves in Single and Collective Cell Migration

Membrane Nanowaves in Single and Collective Cell Migration

Using optical profilometry to characterize cell membrane roughness influenced by amyloid-beta 42 aggregates and electric fields

A review of models of fluctuating protrusion and retraction patterns at the leading edge of motile cells

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