Gap junctions in <i>C. elegans</i>: Their roles in behavior and development

Hall, David H.

doi:10.1002/dneu.22408

Cited by 50 publications

(39 citation statements)

References 54 publications

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“…From these findings, the authors propose that the expression of a specific innexin paralog is sufficient for electrical coupling (Firme et al, 2012). In C. elegans, nearly every cell type expresses at least one paralog of innexin, allowing the formation of heterotypic and heteromeric gap junctions (Hall, 2017). Our results further support the theme of cell-specific innexin paralog expression and localization, which has potential for proper channel formation and changes in synaptic connection, ultimately leading to functional specificity of paralogs.…”

Section: Paralog-and Ganglion-specific Expression and Functionsupporting

confidence: 74%

“…Changes in gap junction expression are required for proper development, synaptic connections, and plasticity in invertebrates and vertebrates (Stebbings et al, 2002;Oyamada et al, 2005;Hall, 2017;Bhattacharya et al, 2019), and the differences in innexin expression levels found in L. stagnalis are likely required for proper organismal function under intrinsic, developmental and extrinsic, environmental regulations. Interestingly, Lst Inx7 was downregulated compared to the other innexins in most tissues.…”

Section: Paralog-and Ganglion-specific Expression and Functionmentioning

confidence: 99%

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Gap Junction Coding Innexin in Lymnaea stagnalis: Sequence Analysis and Characterization in Tissues and the Central Nervous System

Mersman

Jolly

Zhang

et al. 2020

Front. Synaptic Neurosci.

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Connections between neurons called synapses are the key components underlying all nervous system functions of animals and humans. However, important genetic information on the formation and plasticity of one type, the electrical (gap junctionmediated) synapse, is understudied in many invertebrates. In the present study, we set forth to identify and characterize the gap junction-encoding gene innexin in the central nervous system (CNS) of the mollusk pond snail Lymnaea stagnalis. With PCR, 3 and 5 RACE, and BLAST searches, we identified eight innexin genes in the L. stagnalis genome, named Lst Inx1-Lst Inx8. Phylogenetic analysis revealed that the L. stagnalis innexin genes originated from a single copy in the common ancestor of molluskan species by multiple gene duplication events and have been maintained in L. stagnalis since they were generated. The paralogous innexin genes demonstrate distinct expression patterns among tissues. In addition, one paralog, Lst Inx1, exhibits heterogeneity in cells and ganglia, suggesting the occurrence of functional diversification after gene duplication. These results introduce possibilities to study an intriguing potential relationship between innexin paralog expression and cell-specific functional outputs such as heterogenic ability to form channels and exhibit synapse plasticity. The L. stagnalis CNS contains large neurons and functionally defined networks for behaviors; with the introduction of L. stagnalis in the gap junction gene field, we are providing novel opportunities to combine genetic research with direct investigations of functional outcomes at the cellular, synaptic, and behavioral levels.

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Section: Paralog-and Ganglion-specific Expression and Functionsupporting

confidence: 74%

Section: Paralog-and Ganglion-specific Expression and Functionmentioning

confidence: 99%

Gap Junction Coding Innexin in Lymnaea stagnalis: Sequence Analysis and Characterization in Tissues and the Central Nervous System

Mersman

Jolly

Zhang

et al. 2020

Front. Synaptic Neurosci.

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“…While there is a general appreciation of the importance of establishing synaptic connectivity diagrams, much of past and present analysis of connectomes focuses on chemical synapses, even though the importance of electrical synapses in nervous system function has been made apparent by a number of genetic loss of function studies (Abrams and Scherer, 2012;Hall, 2017;Hasegawa and Turnbull, 2014;Marder et al, 2017;Song et al, 2016;White and Paul, 1999). Through the establishment of a nervous system wide map of innexin expression, as well its dynamic modulation under specific environmental conditions;…”

Section: Discussionmentioning

confidence: 99%

“…While the role of chemical synapses in nervous system function has been widely studied, electrical synapses have received much less attention. The importance of electrical synapses is, however, well documented through genetic analysis in invertebrate and vertebrate nervous system, in which the loss of constituent components of electrical synapses result in obvious dysfunctions of the nervous system (Abrams and Scherer, 2012;Hall, 2017;Hasegawa and Turnbull, 2014;Marder et al, 2017;Song et al, 2016;White and Paul, 1999).…”

Section: Introductionmentioning

confidence: 99%

Plasticity of the electrical connectome ofC. elegans

Bhattacharya

Aghayeva

Berghoff

et al. 2018

Preprint

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The patterns of electrical synapses of an animal nervous system ("electrical connectome"), as well as the functional properties and plasticity of electrical synapses, are defined by the neuron type-specific complement of electrical synapse constituents. We systematically examine here properties of the electrical connectome of the nematode C. elegans through a genome-and nervous system-wide analysis of the expression pattern of the central components of invertebrate electrical synapses, the innexins, revealing highly complex combinatorial patterns of innexin expression throughout the nervous system. We find that the complex expression patterns of 12 out of 14 neuronally expressed innexins change in a strikingly neuron type-specific manner throughout most of the nervous system, if animals encounter harsh environmental conditions and enter the dauer arrest stage. We systematically describe the plasticity of locomotory patterns of dauer stage animals and, by analyzing several individual electrical synapses, we demonstrate that dauer stage-specific electrical synapse remodeling is responsible for specific aspects of the altered locomotory patterns as well as altered chemosensory behavior of dauer stage animals. We describe an intersectional gene regulatory mechanism, involving terminal selector and FoxO transcription factors that are responsible for inducing innexin expression changes in a neuron type-and environment-specific manner. Taken together, our studies illustrate the remarkably dynamic nature of electrical synapses on a nervous system-wide level and describe regulatory strategies for how these alterations are achieved.

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“…1d) others can be very simple. For example, electrical synapses or gap junctions (GJs) are intercellular channels formed by two matching hemi-channels consisting of a subset of 25 innexin proteins [41]. In order to maintain a GJ, the innexins forming the hemi-channels must be expressed on the surface of adjacent neurons.…”

Section: Introductionmentioning

confidence: 99%

Uncovering the genetic blueprint of theC. elegansnervous system

Kovács

Barabási

2020

Preprint

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Despite rapid advances in connectome mapping and neuronal genetics, we lack theoretical and computational tools to unveil, in an experimentally testable fashion, the genetic mechanisms that govern neuronal wiring. Here we introduce a computational framework to link the adjacency matrix of a connectome to the expression patterns of its neurons, helping us uncover a set of genetic rules that govern the interactions between adjacent neurons. The method incorporates the biological realities of the system, accounting for noise from data collection limitations, as well as spatial restrictions. The resulting methodology allows us to infer a network of 19 innexin interactions that govern the formation of gap junctions in C. elegans, five of which are already supported by experimental data. As advances in singlecell gene expression profiling increase the accuracy and the coverage of the data, the developed framework will allow researchers to systematically infer experimentally testable connection rules, o↵ering mechanistic predictions for synapse and gap junction formation.

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Gap junctions in C. elegans: Their roles in behavior and development

Cited by 50 publications

References 54 publications

Gap Junction Coding Innexin in Lymnaea stagnalis: Sequence Analysis and Characterization in Tissues and the Central Nervous System

Gap Junction Coding Innexin in Lymnaea stagnalis: Sequence Analysis and Characterization in Tissues and the Central Nervous System

Plasticity of the electrical connectome ofC. elegans

Uncovering the genetic blueprint of theC. elegansnervous system

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