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Synaptic cell adhesion molecule Cdh6 identifies a class of sensory neurons with novel functions in colonic motility.

ABSTRACT: Intrinsic sensory neurons are an essential part of the enteric nervous system (ENS) and play a crucial role in gastrointestinal tract motility and digestion. Neuronal subtypes in the ENS have been distinguished by their electrophysiological properties, morphology, and expression of characteristic markers, notably neurotransmitters and neuropeptides. Here we investigated synaptic cell adhesion molecules as novel cell type markers in the ENS. Our work identifies two Type II classic cadherins, Cdh6 and Cdh8, specific to sensory neurons in the mouse colon. We show that Cdh6+ neurons demonstrate all other distinguishing classifications of enteric sensory neurons including marker expression of Calcb and Nmu, Dogiel type II morphology and AH-type electrophysiology and I _H current. Optogenetic activation of Cdh6+ sensory neurons in distal colon evokes retrograde colonic motor complexes (CMCs), while pharmacologic blockade of rhythmicity-associated current I _H disrupts the spontaneous generation of CMCs. These findings provide the first demonstration of selective activation of a single neurochemical and functional class of enteric neurons, and demonstrate a functional and critical role for sensory neurons in the generation of CMCs.

SUBMITTER: Gomez-Frittelli J

PROVIDER: S-EPMC11326146 | biostudies-literature | 2024 Aug

REPOSITORIES: biostudies-literature

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Synaptic cell adhesion molecule <i>Cdh6</i> identifies a class of sensory neurons with novel functions in colonic motility.

Gomez-Frittelli Julieta J Devienne Gabrielle G Travis Lee L Kyloh Melinda A MA Duan Xin X Hibberd Tim J TJ Spencer Nick J NJ Huguenard John R JR Kaltschmidt Julia A JA

bioRxiv : the preprint server for biology 20241220

Intrinsic sensory neurons are an essential part of the enteric nervous system (ENS) and play a crucial role in gastrointestinal tract motility and digestion. Neuronal subtypes in the ENS have been distinguished by their electrophysiological properties, morphology, and expression of characteristic markers, notably neurotransmitters and neuropeptides. Here we investigated synaptic cell adhesion molecules as novel cell type markers in the ENS. Our work identifies two Type II classic cadherins, <i>C ...[more]

PMID: 39149241

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Project description:As the primary sites of synaptic or sensory input in the nervous system, dendrites play an essential role in processing neuronal and sensory information. Moreover, the specification of class specific dendrite arborization is critically important in establishing neural connectivity and the formation of functional networks. Cytoskeletal modulation provides a key mechanism for establishing, as well as reorganizing, dendritic morphology among distinct neuronal subtypes. While previous studies have established differential roles for the small GTPases Rac and Rho in mediating dendrite morphogenesis, little is known regarding the direct regulators of these genes in mediating distinct dendritic architectures.Here we demonstrate that the RhoGEF Trio is required for the specification of class specific dendritic morphology in dendritic arborization (da) sensory neurons of the Drosophila peripheral nervous system (PNS). Trio is expressed in all da neuron subclasses and loss-of-function analyses indicate that Trio functions cell-autonomously in promoting dendritic branching, field coverage, and refining dendritic outgrowth in various da neuron subtypes. Moreover, overexpression studies demonstrate that Trio acts to promote higher order dendritic branching, including the formation of dendritic filopodia, through Trio GEF1-dependent interactions with Rac1, whereas Trio GEF-2-dependent interactions with Rho1 serve to restrict dendritic extension and higher order branching in da neurons. Finally, we show that de novo dendritic branching, induced by the homeodomain transcription factor Cut, requires Trio activity suggesting these molecules may act in a pathway to mediate dendrite morphogenesis.Collectively, our analyses implicate Trio as an important regulator of class specific da neuron dendrite morphogenesis via interactions with Rac1 and Rho1 and indicate that Trio is required as downstream effector in Cut-mediated regulation of dendrite branching and filopodia formation.

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Synaptic cell adhesion molecule Cdh6 identifies a class of sensory neurons with novel functions in colonic motility.

Publications

Synaptic cell adhesion molecule <i>Cdh6</i> identifies a class of sensory neurons with novel functions in colonic motility.

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Dataset Information

Synaptic cell adhesion molecule Cdh6 identifies a class of sensory neurons with novel functions in colonic motility.

Publications

Synaptic cell adhesion molecule &lt;i&gt;Cdh6&lt;/i&gt; identifies a class of sensory neurons with novel functions in colonic motility.

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OmicsDI is part of the ELIXIR infrastructure

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Synaptic cell adhesion molecule <i>Cdh6</i> identifies a class of sensory neurons with novel functions in colonic motility.