The bioelectric code: An ancient computational medium for dynamic control of growth and form

Levin, Michael; Martyniuk, Christopher J.

doi:10.1016/j.biosystems.2017.08.009

Cited by 171 publications

(188 citation statements)

References 201 publications

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“…In this perspective, we focus on closing the loop with mechanical processes. Similar ideas apply to electrical processes . There are several known transduction processes that can couple mechanical and electrical processes to each other and to other biochemical processes.…”

Section: Discussionmentioning

confidence: 97%

“…Broadly defined, patterning during morphogenesis involves three types of processes: biochemical, mechanical, and electrical . These processes involve fields; continuous space‐time dependent properties, that are being shaped by the dynamics at the different levels of organization while simultaneously influencing them.…”

Section: Morphogenesis As An Integrated Processmentioning

confidence: 99%

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HydraRegeneration: Closing the Loop with Mechanical Processes in Morphogenesis

Braun

Keren

2018

BioEssays

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The convergence of morphogenesis into viable organisms under variable conditions suggests closed-loop dynamics involving multiscale functional feedback. We develop the idea that morphogenesis is based on synergy between mechanical and bio-signaling processes, spanning all levels of organization: molecular, cellular, tissue, up to the whole organism. This synergy provides feedback within and between all levels of organization, to close the loop between the dynamics of the morphogenesis process and its robust functional outcome. Hydra offer a powerful platform to explore this direction, thanks to their simple body plan, extraordinary regeneration capabilities, and the accessibility and flexibility of their tissues. Our recent experiments show that structural inheritance of the actomyosin organization directs body-axis formation during Hydra regeneration. Morphogenesis is then stabilized through dynamic cytoskeletal reorganization induced by the inherited structure. The observed cytoskeletal stability and reorganization capabilities suggest that mechanical feedback integrates with biochemical processes to establish viable patterns and ensure canalization.

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Section: Discussionmentioning

confidence: 97%

Section: Morphogenesis As An Integrated Processmentioning

confidence: 99%

HydraRegeneration: Closing the Loop with Mechanical Processes in Morphogenesis

Braun

Keren

2018

BioEssays

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“…The pathophysiological importance of membrane voltage is becoming increasingly recognized in many fields such as development (Bates, 2015, Levin andMartyniuk, 2018), regeneration (Zhao, 2009, McLaughlin and, and cancer (Chernet andLevin, 2013, Onkal andDjamgoz, 2009) (Payne S.L., 2019). This increased recognition prompts the need for simple standardized methods to quantify and precisely manipulate the RMP and to identify the contribution of specific ions to the RMP.…”

Section: Discussionmentioning

confidence: 99%

Defined extracellular ionic solutions to study and manipulate the cellular resting membrane potential

Bonzanni

Payne

Adelfio

et al. 2019

Preprint

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Statement:We describe simplified roadmap to study the role of bioelectricity, in particular individual ions, in cell biological processes. Abstract:All cells possess an electric potential across their plasma membranes. While familiar in the context of excitable cells such as neurons, healthy non-excitable cells are also able to generate and receive bioelectric signals. The cellular resting membrane potential (RMP) regulates many factors in cell homeostasis, such as cell proliferation, differentiation and apoptosis. It is therefore critical to develop simple strategies to measure, manipulate and characterize this feature. Current studies to evaluate RMP rely on the patch clamp approach, which is technically challenging, low-throughput and not widely available to the scientific community. Here, we present a relatively simple methodology to functionally study the role of RMP in non-excitable cells by modulating it pharmacologically, and using a voltage-sensitive dye to characterize the contribution of individual ions to the RMP. Specifically, we define protocols for using extracellular solutions in which permeable ions (Na + , Cland K + ) are substituted with non-permeable ions (N-Methyl-D-glucamine (NMDG), gluconate, choline, SO4 2-) to study and manipulate RMP in vitro. The resulting RMP modifications were assessed with both patch clamp and a voltage sensitive dye. Using an epithelial and cancer cell line, we demonstrate that the proposed ionic solutions can determine the relative contribution of ionic species in setting the RMP and be used to actively and selectively modify the RMP. The proposed method is simple and reproducible and will make the study of bioelectricity more readily available to the cell biology community by enabling functional modulation of RMP in most cellular assays.

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“…How organs and tissues develop in concert to form a functional organism is still largely an open question. Morphogenesis results from the dynamic interplay of three types of processes: biochemical (1-3), mechanical (2,4) and electrical (5,6), which span all scales from the molecular to the entire organism (7,8). While there has been a great progress in understanding the role of each of these processes in morphogenesis, how they are coordinated and integrated towards a robust functional animal remains elusive.…”

Section: Introductionmentioning

confidence: 99%

Electric-induced reversal of morphogenesis inHydra

Braun

Ori

2019

Preprint

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Morphogenesis involves the dynamic integration of biochemical, mechanical and electricalprocesses. We show that an external electric field can halt morphogenesis in Hydra.Moreover, above a critical field morphogenesis exhibits reversal dynamics: a fully developed animal folds back into its incipient spheroid morphology. The potential to renew morphogenesis is re-exposed when the field is reduced back to amplitudes below criticality. These dynamics are accompanied by modulations of the Wnt3 activity, a central component of the head organizer in Hydra. Reversal of morphogenesis is shown to be triggered by enhanced electrical excitations in the Hydra tissue, leading to intensified calcium activity. The controlled backward-forward cycle of morphogenesis can be repeated several times. These results indicate that electrical processes are tightly integrated with biochemical and mechanical processes in morphogenesis, and play an instructive role to a level that can direct developmental trajectories. The capability to reverse the dynamics of morphogenesis calls for extending the study of development beyond forward-driven hierarchical processes.

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The bioelectric code: An ancient computational medium for dynamic control of growth and form

Cited by 171 publications

References 201 publications

HydraRegeneration: Closing the Loop with Mechanical Processes in Morphogenesis

HydraRegeneration: Closing the Loop with Mechanical Processes in Morphogenesis

Defined extracellular ionic solutions to study and manipulate the cellular resting membrane potential

Electric-induced reversal of morphogenesis inHydra

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