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基于细胞离子通道和细胞间缝隙连接的头尾模式生物电模型。

Bioelectrical model of head-tail patterning based on cell ion channels and intercellular gap junctions.

机构信息

Dept. de Termodinàmica, Facultat de Física, Universitat de València, E-46100 Burjassot, Spain.

Laboratory of Immunobiology, Centro de Investigación Príncipe Felipe, Valencia 46012, Spain.

出版信息

Bioelectrochemistry. 2020 Apr;132:107410. doi: 10.1016/j.bioelechem.2019.107410. Epub 2019 Nov 29.


DOI:10.1016/j.bioelechem.2019.107410
PMID:31821903
Abstract

Robust control of anterior-posterior axial patterning during regeneration is mediated by bioelectric signaling. However, a number of systems-level properties of bioelectrochemical circuits, including stochastic outcomes such as seen in permanently de-stabilized "cryptic" flatworms, are not completely understood. We present a bioelectrical model for head-tail patterning that combines single-cell characteristics such as membrane ion channels with multicellular community effects via voltage-gated gap junctions. It complements the biochemically-focused models by describing the effects of intercellular electrochemical coupling, cutting plane, and gap junction blocking of the multicellular ensemble. We provide qualitative insights into recent experiments concerning planarian anterior/posterior polarity by showing that: (i) bioelectrical signals can help separated cell domains to know their relative position after injury and contribute to the transitions between the abnormal double-head state and the normal head-tail state; (ii) the bioelectrical phase-space of the system shows a bi-stability region that can be interpreted as the cryptic system state; and (iii) context-dependent responses are obtained depending on the cutting plane position, the initial bioelectrical state of the multicellular system, and the intercellular connectivity. The model reveals how simple bioelectric circuits can exhibit complex tissue-level patterning and suggests strategies for regenerative control in vivo and in synthetic biology contexts.

摘要

生物电信号在再生过程中对前后轴模式的稳健控制。然而,生物电化学电路的许多系统级特性,包括永久性不稳定的“隐匿”扁形虫中出现的随机结果,还不完全清楚。我们提出了一个用于头尾模式的生物电模型,该模型将细胞膜离子通道等单细胞特性与电压门控间隙连接的多细胞群落效应相结合。它通过描述细胞间电化学耦合、切割面和多细胞集合的间隙连接阻断的影响,补充了以生物化学为重点的模型。我们通过展示以下内容,为最近有关扁形虫前后极性的实验提供了定性的见解:(i)生物电信号可以帮助分离的细胞区域在受伤后了解它们的相对位置,并有助于异常双头状态和正常头尾状态之间的转变;(ii)系统的生物电相空间显示出双稳定性区域,可以解释为隐匿系统状态;(iii)根据切割面位置、多细胞系统的初始生物电状态和细胞间连接性,获得了上下文相关的响应。该模型揭示了简单的生物电路如何表现出复杂的组织级模式,并为体内和合成生物学背景下的再生控制提供了策略。

相似文献

[1]
Bioelectrical model of head-tail patterning based on cell ion channels and intercellular gap junctions.

Bioelectrochemistry. 2019-11-29

[2]
Bioelectrical coupling in multicellular domains regulated by gap junctions: A conceptual approach.

Bioelectrochemistry. 2018-4-21

[3]
From non-excitable single-cell to multicellular bioelectrical states supported by ion channels and gap junction proteins: Electrical potentials as distributed controllers.

Prog Biophys Mol Biol. 2019-6-27

[4]
Bioelectrical Signals and Ion Channels in the Modeling of Multicellular Patterns and Cancer Biophysics.

Sci Rep. 2016-2-4

[5]
MicroRNA Intercellular Transfer and Bioelectrical Regulation of Model Multicellular Ensembles by the Gap Junction Connectivity.

J Phys Chem B. 2017-8-2

[6]
Gap Junctional Blockade Stochastically Induces Different Species-Specific Head Anatomies in Genetically Wild-Type Girardia dorotocephala Flatworms.

Int J Mol Sci. 2015-11-24

[7]
Transplantation of fragments from different planaria: A bioelectrical model for head regeneration.

J Theor Biol. 2023-2-7

[8]
Characterization of innexin gene expression and functional roles of gap-junctional communication in planarian regeneration.

Dev Biol. 2005-11-15

[9]
Oscillatory phenomena in electrophysiological networks: The coupling between cell bioelectricity and transcription.

Comput Biol Med. 2024-9

[10]
Cell Systems Bioelectricity: How Different Intercellular Gap Junctions Could Regionalize a Multicellular Aggregate.

Cancers (Basel). 2021-10-22

引用本文的文献

[1]
Stability and robustness properties of bioelectric networks: A computational approach.

Biophys Rev (Melville). 2021-9-28

[2]
Information integration during bioelectric regulation of morphogenesis of the embryonic frog brain.

iScience. 2023-11-4

[3]
REAC Neurobiological Modulation as a Precision Medicine Treatment for Fibromyalgia.

J Pers Med. 2023-5-27

[4]
Technological Approach to Mind Everywhere: An Experimentally-Grounded Framework for Understanding Diverse Bodies and Minds.

Front Syst Neurosci. 2022-3-24

[5]
Comparative Proteome Analysis Indicates The Divergence between The Head and Tail Regeneration in Planarian.

Cell J. 2021-11

[6]
Bistability of somatic pattern memories: stochastic outcomes in bioelectric circuits underlying regeneration.

Philos Trans R Soc Lond B Biol Sci. 2021-3-29

[7]
Precise control of ion channel and gap junction expression is required for patterning of the regenerating axolotl limb.

Int J Dev Biol. 2020

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