Electrochemical Control of Cell and Tissue Polarity

Chang, Fred; Minc, Nicolas

doi:10.1146/annurev-cellbio-100913-013357

Cited by 75 publications

(65 citation statements)

References 148 publications

(202 reference statements)

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“…, 2011; Maiuri et al. , 2015), and electrical (Homble and Leonetti, 2007; Chang and Minc, 2014) forces can also drive symmetry breaking when coupled with nonlinear chemical reactions, with each other, or even on their own.…”

Section: Symmetry Breaking: From Physics To Biologymentioning

confidence: 99%

Many roads to symmetry breaking: molecular mechanisms and theoretical models of yeast cell polarity

Goryachev

Leda

2017

MBoC

115

111

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Mathematical modeling has been instrumental in identifying common principles of cell polarity across diverse systems. These principles include positive feedback loops that are required to destabilize a spatially uniform state of the cell. The conserved small G-protein Cdc42 is a master regulator of eukaryotic cellular polarization. Here we discuss recent developments in studies of Cdc42 polarization in budding and fission yeasts and demonstrate that models describing symmetry-breaking polarization can be classified into six minimal classes based on the structure of positive feedback loops that activate and localize Cdc42. Owing to their generic system-independent nature, these model classes are also likely to be relevant for the G-protein–based symmetry-breaking systems of higher eukaryotes. We review experimental evidence pro et contra different theoretically plausible models and conclude that several parallel and non–mutually exclusive mechanisms are likely involved in cellular polarization of yeasts. This potential redundancy needs to be taken into consideration when interpreting the results of recent cell-rewiring studies.

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Section: Symmetry Breaking: From Physics To Biologymentioning

confidence: 99%

Many roads to symmetry breaking: molecular mechanisms and theoretical models of yeast cell polarity

Goryachev

Leda

2017

MBoC

115

111

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“…Considering that PIPKI isoforms may be highly activated during egg fertilization (44-47), we could envision why previous studies found PI(4,5)P 2 increases following the rapid membrane depolarization (42) during fertilization (48)(49)(50)(51). Taken together, VSPs possibly regulate the spatial and temporal distribution of phosphoinositides in a cell membrane in response to voltage (52) or pH changes in the cell (7,53). If the distribution is localized and dynamic, VSPs may determine binding of target proteins at specific regions and time, resulting in, for example, cell migration or polarization (54)(55)(56).…”

Section: Discussionmentioning

confidence: 95%

Phosphoinositide 5- and 3-phosphatase activities of a voltage-sensing phosphatase in living cells show identical voltage dependence

Keum

Kruse

Kim

et al. 2016

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

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Voltage-sensing phosphatases (VSPs) are homologs of phosphatase and tensin homolog (PTEN), a phosphatidylinositol 3,4-bisphosphate [PI(3,4)P2] and phosphatidylinositol 3,4,5-trisphosphate [PI(3,4,5)P3] 3-phosphatase. However, VSPs have a wider range of substrates, cleaving 3-phosphate from PI(3,4)P2 and probably PI(3,4,5)P3 as well as 5-phosphate from phosphatidylinositol 4,5-bisphosphate [PI(4,5)P2] and PI(3,4,5)P3 in response to membrane depolarization. Recent proposals say these reactions have differing voltage dependence. Using Förster resonance energy transfer probes specific for different PIs in living cells with zebrafish VSP, we quantitate both voltage-dependent 5- and 3-phosphatase subreactions against endogenous substrates. These activities become apparent with different voltage thresholds, voltage sensitivities, and catalytic rates. As an analytical tool, we refine a kinetic model that includes the endogenous pools of phosphoinositides, endogenous phosphatase and kinase reactions connecting them, and four exogenous voltage-dependent 5- and 3-phosphatase subreactions of VSP. We show that apparent voltage threshold differences for seeing effects of the 5- and 3-phosphatase activities in cells are not due to different intrinsic voltage dependence of these reactions. Rather, the reactions have a common voltage dependence, and apparent differences arise only because each VSP subreaction has a different absolute catalytic rate that begins to surpass the respective endogenous enzyme activities at different voltages. For zebrafish VSP, our modeling revealed that 3-phosphatase activity against PI(3,4,5)P3 is 55-fold slower than 5-phosphatase activity against PI(4,5)P2; thus, PI(4,5)P2 generated more slowly from dephosphorylating PI(3,4,5)P3 might never accumulate. When 5-phosphatase activity was counteracted by coexpression of a phosphatidylinositol 4-phosphate 5-kinase, there was accumulation of PI(4,5)P2 in parallel to PI(3,4,5)P3 dephosphorylation, emphasizing that VSPs can cleave the 3-phosphate of PI(3,4,5)P3.

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“…More recent work showed that imposed external electric fields are in some instances sufficient to change cellular orientation, expansion, proliferation, migration, and differentiation in Dyctostelium discoideum , fission yeast, and animal tissues (Chang & Minc 2014). These studies clearly indicate that electric fields are capable of perturbing cellular and developmental processes in a wide spectrum of tissues and organisms.…”

Section: Discussionmentioning

confidence: 99%

“…Although there is a long tradition of exploring the effects of electric stimulation on the regeneration of animal tissues and organs (Smith 1974; McCaig et al. 2005; Levin 2007; Chang & Minc 2014), little attention has been focused on similar perturbations applied to organ regeneration in planta .…”

Section: Introductionmentioning

confidence: 99%

Externally imposed electric field enhances plant root tip regeneration

2016

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In plants, shoot and root regeneration can be induced in the distinctive conditions of tissue culture (in vitro) but is also observed in intact individuals (in planta) recovering from tissue damage. Roots, for example, can regenerate their fully excised meristems in planta, even in mutants with impaired apical stem cell niches. Unfortunately, to date a comprehensive understanding of regeneration in plants is still missing. Here, we provide evidence that an imposed electric field can perturb apical root regeneration in Arabidopsis. Crucially, we explored both spatial and temporal competences of the stump to respond to electrical stimulation, by varying respectively the position of the cut and the time interval between excision and stimulation. Our data indicate that a brief pulse of an electric field parallel to the root is sufficient to increase by up to two‐fold the probability of its regeneration, and to perturb the local distribution of the hormone auxin, as well as cell division regulation. Remarkably, the orientation of the root towards the anode or the cathode is shown to play a role.

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Electrochemical Control of Cell and Tissue Polarity

Cited by 75 publications

References 148 publications

Many roads to symmetry breaking: molecular mechanisms and theoretical models of yeast cell polarity

Many roads to symmetry breaking: molecular mechanisms and theoretical models of yeast cell polarity

Phosphoinositide 5- and 3-phosphatase activities of a voltage-sensing phosphatase in living cells show identical voltage dependence

Externally imposed electric field enhances plant root tip regeneration

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