Switching direction in electric-signal-induced cell migration by cyclic guanosine monophosphate and phosphatidylinositol signaling

Sato, Masayuki; Kuwayama, Hidekazu; Egmond, Wouter N. van; Takayama, Airi; Takagi, Hiroaki; Haastert, Peter J.M. van; Yanagida, Toshio; Ueda, Masahiro

doi:10.1073/pnas.0809974106

Cited by 87 publications

(89 citation statements)

References 37 publications

(68 reference statements)

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“…Similarly to chemotaxing cells, several studies have reported activation and/or localization of typical leading edge markers, including actin polymerization, phosphatidylinositol 3,4,5-trisphosphate (PIP3), and/or extracellular signal-regulated kinase (ERK) 1/2, at the front of cells undergoing either shear-flowmediated migration or electrotaxis (4)(5)(6)(7). However, these activities were observed under steady-state conditions and, because these activities are associated with random projections, their appearance at the leading edge most likely merely reflects the abundance of projections at the front induced by mechanical or electrical forces.…”

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confidence: 99%

Chemical and mechanical stimuli act on common signal transduction and cytoskeletal networks

Artemenko

Axiotakis

Borleis

et al. 2016

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

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Signal transduction pathways activated by chemoattractants have been extensively studied, but little is known about the events mediating responses to mechanical stimuli. We discovered that acute mechanical perturbation of cells triggered transient activation of all tested components of the chemotactic signal transduction network, as well as actin polymerization. Similarly to chemoattractants, the shear flow-induced signal transduction events displayed features of excitability, including the ability to mount a full response irrespective of the length of the stimulation and a refractory period that is shared with that generated by chemoattractants. Loss of G protein subunits, inhibition of multiple signal transduction events, or disruption of calcium signaling attenuated the response to acute mechanical stimulation. Unlike the response to chemoattractants, an intact actin cytoskeleton was essential for reacting to mechanical perturbation. These results taken together suggest that chemotactic and mechanical stimuli trigger activation of a common signal transduction network that integrates external cues to regulate cytoskeletal activity and drive cell migration.biochemical excitability | shear stress | motility | biomechanics | inflammation

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confidence: 99%

Chemical and mechanical stimuli act on common signal transduction and cytoskeletal networks

Artemenko

Axiotakis

Borleis

et al. 2016

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

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“…Several other pathways may also contribute to chemotaxis (9,22). We demonstrated that Dictyostelium cells also show robust electrotaxis and are a good model for dissecting the molecular/genetic basis of electrotaxis (19,29). Extracellular pH, [K ϩ ], and electroporation significantly affected V m and correspondingly reduced or abolished electrotaxis.…”

Section: Discussionmentioning

confidence: 81%

Different Roles of Membrane Potentials in Electrotaxis and Chemotaxis of Dictyostelium Cells

et al. 2011

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Many types of cells migrate directionally in direct current (DC) electric fields (EFs), a phenomenon termed galvanotaxis or electrotaxis. The directional sensing mechanisms responsible for this response to EFs, however, remain unknown. Exposing cells to an EF causes changes in plasma membrane potentials (V m ). Exploiting the ability of Dictyostelium cells to tolerate drastic V m changes, we investigated the role of V m in electrotaxis and, in parallel, in chemotaxis. We used three independent factors to control V m : extracellular pH, extracellular [K ؉ ], and electroporation. Changes in V m were monitored with microelectrode recording techniques. Depolarized V m was observed under acidic (pH 5.0) and alkaline (pH 9.0) conditions as well as under higher extracellular [K ؉ ] conditions. Electroporation permeabilized the cell membrane and significantly reduced the V m , which gradually recovered over 40 min. We then recorded the electrotactic behaviors of Dictyostelium cells with a defined V m using these three techniques. The directionality (directedness of electrotaxis) was quantified and compared to that of chemotaxis (chemotactic index). We found that a reduced V m significantly impaired electrotaxis without significantly affecting random motility or chemotaxis. We conclude that extracellular pH, [K ؉ ], and electroporation all significantly affected electrotaxis, which appeared to be mediated by the changes in V m . The initial directional sensing mechanisms for electrotaxis therefore differ from those of chemotaxis and may be mediated by changes in resting V m .Cells migrate directionally in response to many extracellular cues including chemical gradients (chemotaxis), topography, mechanical forces (mechanotaxis/durataxis), and electrical fields (EFs) (electrotaxis/galvanotaxis) (1,3,8,15,27). Electric fields have long been suggested to be a candidate directional signal for cell migration in development, wound healing, and regeneration. The mechanisms used by cells to sense the weak direct current (DC) EFs, however, have remained very poorly understood.One of the immediate effects felt by a cell upon exposure to an EF is a change in the cell membrane potentials (V m ). In an EF, the plasma membrane facing the cathode depolarizes while the membrane facing the anode hyperpolarizes (17, 18). It has been proposed that the changes in V m may underlie electrotaxis. In a cell with negligible voltage-gated conductance, the hyperpolarized membrane facing the anode attracts Ca 2ϩ by passive electrochemical diffusion. This side of the cell then contracts, thereby propelling the cell toward the cathode. In a cell with voltage-gated Ca 2ϩ channels, channels near the cathodal (depolarized) side open, thereby allowing Ca 2ϩ influx. Intracellular Ca 2ϩ levels will rise both on the anodal side and on the cathodal side in such a cell. The direction of cell movement in this situation will depend on the balance between the opposing contractile forces (17). The role of V m in electrotaxis has not yet been directly tested.In thi...

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“…This probabilistic view of chemotaxis might also hold true for other modes of oriented cell movement, such as electrotaxis or thermotaxis. In electric fields, signalling molecules such as PI3K and sGC translocate to the anode or cathode side of the applied electric field and increase the probability of pseudopod formation, thereby inducing directed movement (Sato et al, 2009;Zhao et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

Chemotaxis: insights from the extending pseudopod

Haastert

2010

Journal of Cell Science

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SummaryChemotaxis is one of the most fascinating processes in cell biology. Shallow gradients of chemoattractant direct the movement of cells, and an intricate network of signalling pathways somehow instructs the movement apparatus to induce pseudopods in the direction of these gradients. Exciting new experiments have approached chemotaxis from the perspective of the extending pseudopod. These recent studies have revealed that, in the absence of external cues, cells use endogenous signals for the highly ordered extension of pseudopods, which appear mainly as alternating right and left splits. In addition, chemoattractants activate other signalling molecules that induce a positional bias of this basal system, such that the extending pseudopods are oriented towards the gradient. In this Commentary, I review the findings of these recent experiments, which together provide a new view of cell movement and chemotaxis.

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Switching direction in electric-signal-induced cell migration by cyclic guanosine monophosphate and phosphatidylinositol signaling

Cited by 87 publications

References 37 publications

Chemical and mechanical stimuli act on common signal transduction and cytoskeletal networks

Chemical and mechanical stimuli act on common signal transduction and cytoskeletal networks

Different Roles of Membrane Potentials in Electrotaxis and Chemotaxis of Dictyostelium Cells

Chemotaxis: insights from the extending pseudopod

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