» Articles » PMID: 38421867

Neuron Cilia Restrain Glial KCC-3 to a Microdomain to Regulate Multisensory Processing

Overview
Journal Cell Rep
Publisher Cell Press
Date 2024 Feb 29
PMID 38421867
Authors
Affiliations
Soon will be listed here.
Abstract

Glia interact with multiple neurons, but it is unclear whether their interactions with each neuron are different. Our interrogation at single-cell resolution reveals that a single glial cell exhibits specificity in its interactions with different contacting neurons. Briefly, C. elegans amphid sheath (AMsh) glia apical-like domains contact 12 neuron-endings. At these ad-neuronal membranes, AMsh glia localize the K/Cl transporter KCC-3 to a microdomain exclusively around the thermosensory AFD neuron to regulate its properties. Glial KCC-3 is transported to ad-neuronal regions, where distal cilia of non-AFD glia-associated chemosensory neurons constrain it to a microdomain at AFD-contacting glial membranes. Aberrant KCC-3 localization impacts both thermosensory (AFD) and chemosensory (non-AFD) neuron properties. Thus, neurons can interact non-synaptically through a shared glial cell by regulating microdomain localization of its cues. As AMsh and glia across species compartmentalize multiple cues like KCC-3, we posit that this may be a broadly conserved glial mechanism that modulates information processing across multimodal circuits.

Citing Articles

The AFD-expressed SRTX-1 GPCR does not contribute to AFD thermosensory functions.

Chen L, Harris N, Sengupta P MicroPubl Biol. 2024; 2024.

PMID: 39611104 PMC: 11603155. DOI: 10.17912/micropub.biology.001382.


Molecular profiling of invertebrate glia.

Purice M, Lago-Baldaia I, Fernandes V, Singhvi A Glia. 2024; 73(3):632-656.

PMID: 39415317 PMC: 11784859. DOI: 10.1002/glia.24623.


Glia in Invertebrate Models: Insights from Caenorhabditis elegans.

Purice M, Severs L, Singhvi A Adv Neurobiol. 2024; 39:19-49.

PMID: 39190070 DOI: 10.1007/978-3-031-64839-7_2.


Epithelial UNC-23 limits mechanical stress to maintain glia-neuron architecture in C. elegans.

Martin C, Bent J, Hill T, Topalidou I, Singhvi A Dev Cell. 2024; 59(13):1668-1688.e7.

PMID: 38670103 PMC: 11233253. DOI: 10.1016/j.devcel.2024.04.005.


Glia Development and Function in the Nematode .

Singhvi A, Shaham S, Rapti G Cold Spring Harb Perspect Biol. 2024; 16(12.

PMID: 38565269 PMC: 11445397. DOI: 10.1101/cshperspect.a041346.

References
1.
Raiders S, Black E, Bae A, Macfarlane S, Klein M, Shaham S . Glia actively sculpt sensory neurons by controlled phagocytosis to tune animal behavior. Elife. 2021; 10. PMC: 8079151. DOI: 10.7554/eLife.63532. View

2.
Armenti S, Lohmer L, Sherwood D, Nance J . Repurposing an endogenous degradation system for rapid and targeted depletion of C. elegans proteins. Development. 2014; 141(23):4640-7. PMC: 4302935. DOI: 10.1242/dev.115048. View

3.
Mello C, Kramer J, Stinchcomb D, Ambros V . Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991; 10(12):3959-70. PMC: 453137. DOI: 10.1002/j.1460-2075.1991.tb04966.x. View

4.
Bacaj T, Lu Y, Shaham S . The conserved proteins CHE-12 and DYF-11 are required for sensory cilium function in Caenorhabditis elegans. Genetics. 2008; 178(2):989-1002. PMC: 2248344. DOI: 10.1534/genetics.107.082453. View

5.
Payne J, Rivera C, Voipio J, Kaila K . Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci. 2003; 26(4):199-206. DOI: 10.1016/S0166-2236(03)00068-7. View