Endogenous gradients of resting potential instructively pattern embryonic neural tissue via Notch signaling and regulation of proliferation

The Journal of Neuroscience : the Official Journal of the Society for Neuroscience
Vaibhav P PaiMichael Levin

Abstract

Biophysical forces play important roles throughout embryogenesis, but the roles of spatial differences in cellular resting potentials during large-scale brain morphogenesis remain unknown. Here, we implicate endogenous bioelectricity as an instructive factor during brain patterning in Xenopus laevis. Early frog embryos exhibit a characteristic hyperpolarization of cells lining the neural tube; disruption of this spatial gradient of the transmembrane potential (Vmem) diminishes or eliminates the expression of early brain markers, and causes anatomical mispatterning of the brain, including absent or malformed regions. This effect is mediated by voltage-gated calcium signaling and gap-junctional communication. In addition to cell-autonomous effects, we show that hyperpolarization of transmembrane potential (Vmem) in ventral cells outside the brain induces upregulation of neural cell proliferation at long range. Misexpression of the constitutively active form of Notch, a suppressor of neural induction, impairs the normal hyperpolarization pattern and neural patterning; forced hyperpolarization by misexpression of specific ion channels rescues brain defects induced by activated Notch signaling. Strikingly, hyperpolarizing posterior ...Continue Reading

Citations

Jul 23, 2016·Frontiers in Psychology·František Baluška, Michael Levin
Jul 28, 2016·Frontiers in Bioengineering and Biotechnology·Alexis Pietak, Michael Levin
Nov 18, 2017·Wiley Interdisciplinary Reviews. Systems Biology and Medicine·Chris Fields, Michael Levin
Dec 11, 2019·Scientific Reports·Santosh Manicka, Michael Levin
Aug 31, 2016·Communicative & Integrative Biology·Kelly G SullivanMichael Levin
Nov 17, 2015·Integrative Biology : Quantitative Biosciences From Nano to Macro·G Pezzulo, M Levin
Jan 6, 2018·Npj Regenerative Medicine·Jean-François ParéMichael Levin
Mar 3, 2018·Communicative & Integrative Biology·Celia Herrera-Rincon, Michael Levin
Jul 21, 2020·Bioelectricity·Vaibhav P Pai, Dany Spencer Adams
Oct 17, 2015·Theoretical Biology & Medical Modelling·Robert Law, Michael Levin
Jun 22, 2017·Annual Review of Biomedical Engineering·Michael LevinJoshua M Finkelstein
Jul 18, 2017·Biology & Philosophy·Fred Keijzer, Argyris Arnellos
Jun 13, 2020·Frontiers in Cellular Neuroscience·Vaibhav P PaiMichael Levin
Mar 10, 2018·Nature Communications·Vaibhav P PaiMichael Levin
Jan 30, 2020·BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology·Michael Levin
Feb 9, 2021·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Giovanni PezzuloMichael Levin
Feb 26, 2021·EMBO Reports·Maya Emmons-Bell, Iswar K Hariharan
Apr 24, 2018·Current Opinion in Biotechnology·Juanita Mathews, Michael Levin
Mar 6, 2016·Cell Calcium·Michelle K TuLaura N Borodinsky
Aug 16, 2019·Progress in Biophysics and Molecular Biology·William B MillerFrantišek Baluška
Aug 24, 2019·Current Opinion in Genetics & Development·Jessica L Whited, Michael Levin
Apr 13, 2021·Frontiers in Molecular Neuroscience·Michael Levin, Angeles B Ribera
Sep 1, 2017·Bio Systems·Michael Levin, Christopher J Martyniuk
May 8, 2021·Progress in Biophysics and Molecular Biology·Michael Levin
Apr 8, 2018·Progress in Biophysics and Molecular Biology·Alexis Pietak, Michael Levin

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