V-ATPase Proton Pumping Activity Is Required for Adult Zebrafish Appendage Regeneration

Monteiro, Joana F.; Aires, Rita; Becker, Jörg; Jacinto, António; Certal, Ana C.; Rodríguez-León, Joaquín

doi:10.1371/journal.pone.0092594

Cited by 33 publications

(44 citation statements)

References 49 publications

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“…Bioelectric and, more recently, redox activities have been shown, independently, to modulate regeneration in widespread models: planaria (Beane et al, 2011;Pirotte et al, 2015), zebrafish (Gauron et al, 2013;Monteiro et al, 2014) and amphibians (Love et al, 2013;Reid et al, 2009). Seeking a biochemical and biophysical integration, we aimed to determine whether and how these pervasive activities interact during regeneration.…”

Section: Discussionmentioning

confidence: 99%

“…V-ATPase-mediated repolarization of membrane potential (V m ) and voltage-gated Na + channel (VGSC or Na V ) 1.2-mediated sodium influx are necessary for and sufficient to induce X. laevis tadpole tail regeneration (Adams et al, 2007;Tseng et al, 2010). V-ATPase proton efflux activity correlates with regeneration rate and ability in zebrafish caudal fin regeneration (Monteiro et al, 2014). H + /K + -ATPase-mediated V m depolarization modulates planarian head regeneration (Beane et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…Interestingly, redox and bioelectric activities control the expression and activity of signaling pathways, such as Wnt, FGF, BMP and Notch, in addition to cell behaviors, such as proliferation, apoptosis and innervation, which are required for regeneration (Adams et al, 2007;Gauron et al, 2013;Han et al, 2014;Love et al, 2013;Monteiro et al, 2014;Tseng et al, 2010). Redox (ROS) and bioelectric [V m , TEP, electric fields (EF) and J I ] states therefore affect regeneration.…”

Section: Introductionmentioning

confidence: 99%

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Early bioelectric activities mediate redox-modulated regeneration

et al. 2016

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Reactive oxygen species (ROS) and electric currents modulate regeneration; however, the interplay between biochemical and biophysical signals during regeneration remains poorly understood. We investigate the interactions between redox and bioelectric activities during tail regeneration in Xenopus laevis tadpoles. We show that inhibition of NADPH oxidase-mediated production of ROS, or scavenging or blocking their diffusion into cells, impairs regeneration and consistently regulates the dynamics of membrane potential, transepithelial potential (TEP) and electric current densities (J I ) during regeneration. Depletion of ROS mimics the altered TEP and J I observed in the non-regenerative refractory period. Short-term application of hydrogen peroxide (H 2 O 2 ) rescues (from depleted ROS) and induces (from the refractory period) regeneration, TEP increase and J I reversal. H 2 O 2 is therefore necessary for and sufficient to induce regeneration and to regulate TEP and J I . Epistasis assays show that voltage-gated Na + channels act downstream of H 2 O 2 to modulate regeneration. Altogether, these results suggest a novel mechanism for regeneration via redoxbioelectric orchestration.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Early bioelectric activities mediate redox-modulated regeneration

et al. 2016

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“…Our observation that prolonged depolarization blocks ependymoglial cell proliferation conflicts with a, previous study that shows that ivermectin treatment of developing Xenopus embryos leads to a hyperproliferation of melanocyte-producing neural crest cells in a cell non-autonomous manner (Blackiston et al, 2011). Interestingly, other studies report that global perturbation of the electrical response of damage tissue blocks cell proliferation and subsequent regenerative outgrowth after Xenopus tadpole tail amputation and zebra fish fin amputation (Adams et al, 2007; Tseng et al, 2010; Monteiro et al, 2014). Taken together, these observations suggest that Vmem-sensitive changes in cell proliferation are cell type and context specific.…”

Section: Discussionmentioning

confidence: 99%

Dynamic membrane depolarization is an early regulator of ependymoglial cell response to spinal cord injury in axolotl

Sabin

Santos-Ferreira

Essig

et al. 2015

Developmental Biology

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Salamanders, such as the Mexican axolotl, are some of the few vertebrates fortunate in their ability to regenerate diverse structures after injury. Unlike mammals they are able to regenerate a fully functional spinal cord after injury. However, the molecular circuitry required to initiate a pro-regenerative response after spinal cord injury is not well understood. To address this question we developed a spinal cord injury model in axolotls and used in vivo imaging of labeled ependymoglial cells to characterize the response of these cells to injury. Using in vivo imaging of ion sensitive dyes we identified that spinal cord injury induces a rapid and dynamic change in the resting membrane potential of ependymoglial cells. Prolonged depolarization of ependymoglial cells after injury inhibits ependymoglial cell proliferation and subsequent axon regeneration. Using transcriptional profiling we identified c-Fos as a key voltage sensitive early response gene that is expressed specifically in the ependymoglial cells after injury. This data establishes that dynamic changes in the membrane potential after injury are essential for regulating the specific spatiotemporal expression of c-Fos that is critical for promoting faithful spinal cord regeneration in axolotl.

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“…Recently, bioelectric signalling has also been found to regulate fin growth rate (Monteiro et al. ), pattern and size (Perathoner et al. ), opening new avenues of research.…”

Section: Introductionmentioning

confidence: 99%

Widening control of fin inter‐rays in zebrafish and inferences about actinopterygian fins

et al. 2018

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The amputation of a teleost fin rapidly triggers an intricate maze of hierarchically regulated signalling processes which ultimately reconstruct the diverse tissues of the appendage. Whereas the generation of the fin pattern along the proximodistal axis brings with it several well-known developmental regulators, the mechanisms by which the fin widens along its dorsoventral axis remain poorly understood. Utilizing the zebrafish as an experimental model of fin regeneration and studying more than 1000 actinopterygian species, we hypothesized a connection between specific inter-ray regulatory mechanisms and the morphological variability of inter-ray membranes found in nature. To tackle these issues, both cellular and molecular approaches have been adopted and our results suggest the existence of two distinguishable inter-ray areas in the zebrafish caudal fin, a marginal and a central region. The present work associates the activity of the cell membrane potassium channel kcnk5b, the fibroblast growth factor receptor 1 and the sonic hedgehog pathway to the control of several cell functions involved in inter-ray wound healing or dorsoventral regeneration of the zebrafish caudal fin. This ray-dependent regulation controls cell migration, cell-type patterning and gene expression. The possibility that modifications of these mechanisms are responsible for phenotypic variations found in euteleostean species, is discussed.

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V-ATPase Proton Pumping Activity Is Required for Adult Zebrafish Appendage Regeneration

Cited by 33 publications

References 49 publications

Early bioelectric activities mediate redox-modulated regeneration

Early bioelectric activities mediate redox-modulated regeneration

Dynamic membrane depolarization is an early regulator of ependymoglial cell response to spinal cord injury in axolotl

Widening control of fin inter‐rays in zebrafish and inferences about actinopterygian fins

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