Literature DB >> 24882814

Endogenous bioelectrical networks store non-genetic patterning information during development and regeneration.

Michael Levin1.   

Abstract

Pattern formation, as occurs during embryogenesis or regeneration, is the crucial link between genotype and the functions upon which selection operates. Even cancer and aging can be seen as challenges to the continuous physiological processes that orchestrate individual cell activities toward the anatomical needs of an organism. Thus, the origin and maintenance of complex biological shape is a fundamental question for cell, developmental, and evolutionary biology, as well as for biomedicine. It has long been recognized that slow bioelectrical gradients can control cell behaviors and morphogenesis. Here, I review recent molecular data that implicate endogenous spatio-temporal patterns of resting potentials among non-excitable cells as instructive cues in embryogenesis, regeneration, and cancer. Functional data have implicated gradients of resting potential in processes such as limb regeneration, eye induction, craniofacial patterning, and head-tail polarity, as well as in metastatic transformation and tumorigenesis. The genome is tightly linked to bioelectric signaling, via ion channel proteins that shape the gradients, downstream genes whose transcription is regulated by voltage, and transduction machinery that converts changes in bioelectric state to second-messenger cascades. However, the data clearly indicate that bioelectric signaling is an autonomous layer of control not reducible to a biochemical or genetic account of cell state. The real-time dynamics of bioelectric communication among cells are not fully captured by transcriptomic or proteomic analyses, and the necessary-and-sufficient triggers for specific changes in growth and form can be physiological states, while the underlying gene loci are free to diverge. The next steps in this exciting new field include the development of novel conceptual tools for understanding the anatomical semantics encoded in non-neural bioelectrical networks, and of improved biophysical tools for reading and writing electrical state information into somatic tissues. Cracking the bioelectric code will have transformative implications for developmental biology, regenerative medicine, and synthetic bioengineering.
© 2014 The Author. The Journal of Physiology © 2014 The Physiological Society.

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Year:  2014        PMID: 24882814      PMCID: PMC4048089          DOI: 10.1113/jphysiol.2014.271940

Source DB:  PubMed          Journal:  J Physiol        ISSN: 0022-3751            Impact factor:   5.182


  118 in total

1.  The effects of regeneration upon retention of a conditioned response in the planarian.

Authors:  J V McCONNELL; A L JACOBSON; D P KIMBLE
Journal:  J Comp Physiol Psychol       Date:  1959-02

2.  "Nanosized voltmeter" enables cellular-wide electric field mapping.

Authors:  Katherine M Tyner; Raoul Kopelman; Martin A Philbert
Journal:  Biophys J       Date:  2007-05-18       Impact factor: 4.033

3.  Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis.

Authors:  Scott P Fraser; James K J Diss; Athina-Myrto Chioni; Maria E Mycielska; Huiyan Pan; Rezan F Yamaci; Filippo Pani; Zuzanna Siwy; Monika Krasowska; Zbigniew Grzywna; William J Brackenbury; Dimis Theodorou; Meral Koyutürk; Handan Kaya; Esra Battaloglu; Manuela Tamburo De Bella; Martin J Slade; Robert Tolhurst; Carlo Palmieri; Jie Jiang; David S Latchman; R Charles Coombes; Mustafa B A Djamgoz
Journal:  Clin Cancer Res       Date:  2005-08-01       Impact factor: 12.531

4.  Depolarization alters phenotype, maintains plasticity of predifferentiated mesenchymal stem cells.

Authors:  Sarah Sundelacruz; Michael Levin; David L Kaplan
Journal:  Tissue Eng Part A       Date:  2013-06-05       Impact factor: 3.845

Review 5.  Role of membrane potential in the regulation of cell proliferation and differentiation.

Authors:  Sarah Sundelacruz; Michael Levin; David L Kaplan
Journal:  Stem Cell Rev Rep       Date:  2009-06-27       Impact factor: 5.739

Review 6.  Electric fields at the plasma membrane level: a neglected element in the mechanisms of cell signalling.

Authors:  M Olivotto; A Arcangeli; M Carlà; E Wanke
Journal:  Bioessays       Date:  1996-06       Impact factor: 4.345

Review 7.  Spirals, chaos, and new mechanisms of wave propagation.

Authors:  P S Chen; A Garfinkel; J N Weiss; H S Karagueuzian
Journal:  Pacing Clin Electrophysiol       Date:  1997-02       Impact factor: 1.976

8.  Induction of vertebrate regeneration by a transient sodium current.

Authors:  Ai-Sun Tseng; Wendy S Beane; Joan M Lemire; Alessio Masi; Michael Levin
Journal:  J Neurosci       Date:  2010-09-29       Impact factor: 6.167

Review 9.  Molecular bioelectricity in developmental biology: new tools and recent discoveries: control of cell behavior and pattern formation by transmembrane potential gradients.

Authors:  Michael Levin
Journal:  Bioessays       Date:  2012-01-11       Impact factor: 4.345

Review 10.  Modeling planarian regeneration: a primer for reverse-engineering the worm.

Authors:  Daniel Lobo; Wendy S Beane; Michael Levin
Journal:  PLoS Comput Biol       Date:  2012-04-26       Impact factor: 4.475

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  76 in total

1.  Transcriptional profiling of intramembranous and endochondral ossification after fracture in mice.

Authors:  Brandon A Coates; Jennifer A McKenzie; Evan G Buettmann; Xiaochen Liu; Paul M Gontarz; Bo Zhang; Matthew J Silva
Journal:  Bone       Date:  2019-07-29       Impact factor: 4.398

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

Authors:  Vaibhav P Pai; Joan M Lemire; Jean-François Paré; Gufa Lin; Ying Chen; Michael Levin
Journal:  J Neurosci       Date:  2015-03-11       Impact factor: 6.167

Review 3.  The Cognitive Lens: a primer on conceptual tools for analysing information processing in developmental and regenerative morphogenesis.

Authors:  Santosh Manicka; Michael Levin
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-06-10       Impact factor: 6.237

4.  Inwardly rectifying potassium channels influence Drosophila wing morphogenesis by regulating Dpp release.

Authors:  Giri Raj Dahal; Sarala Joshi Pradhan; Emily Anne Bates
Journal:  Development       Date:  2017-07-06       Impact factor: 6.868

5.  Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish.

Authors:  Jeremy S Rabinowitz; Aaron M Robitaille; Yuliang Wang; Catherine A Ray; Ryan Thummel; Haiwei Gu; Danijel Djukovic; Daniel Raftery; Jason D Berndt; Randall T Moon
Journal:  Proc Natl Acad Sci U S A       Date:  2017-01-17       Impact factor: 11.205

6.  Sustained Depolarization of the Resting Membrane Potential Regulates Muscle Progenitor Cell Growth and Maintains Stem Cell Properties In Vitro.

Authors:  Colin Fennelly; Zhan Wang; Tracy Criswell; Shay Soker
Journal:  Stem Cell Rev Rep       Date:  2016-12       Impact factor: 5.739

Review 7.  Top-down models in biology: explanation and control of complex living systems above the molecular level.

Authors:  Giovanni Pezzulo; Michael Levin
Journal:  J R Soc Interface       Date:  2016-11       Impact factor: 4.118

8.  Evolution evolves: physiology returns to centre stage.

Authors:  Denis Noble; Eva Jablonka; Michael J Joyner; Gerd B Müller; Stig W Omholt
Journal:  J Physiol       Date:  2014-06-01       Impact factor: 5.182

9.  A conceptual model of morphogenesis and regeneration.

Authors:  A Tosenberger; N Bessonov; M Levin; N Reinberg; V Volpert; N Morozova
Journal:  Acta Biotheor       Date:  2015-03-31       Impact factor: 1.774

Review 10.  Re-membering the body: applications of computational neuroscience to the top-down control of regeneration of limbs and other complex organs.

Authors:  G Pezzulo; M Levin
Journal:  Integr Biol (Camb)       Date:  2015-11-16       Impact factor: 2.192

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