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Volume 13
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Article

Quantitative Spatial Analysis of Neuroligin-3 mRNA Expression in the Enteric Nervous System Reveals a Potential Role in Neuronal–Glial Synapses and Reduced Expression in Nlgn3R451C Mice

by
Madushani Herath
1,†,‡,
Ellie Cho
2,
Ulrika Marklund
3,
Ashley E. Franks
4,
Joel C. Bornstein
1 and
Elisa L. Hill-Yardin
5,*
1
Department of Anatomy & Physiology, University of Melbourne, Parkville, VIC 3010, Australia
2
Biological Optical Microscopy Platform, University of Melbourne, Parkville, VIC 3010, Australia
3
Division of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Karolinska Institute, 171 77 Stockholm, Sweden
4
Department of Microbiology, Anatomy Physiology & Pharmacology, School of Agriculture, Biomedicine and Environment, La Trobe University, Bundoora, VIC 3086, Australia
5
School of Health and Biomedical Sciences, STEM College, RMIT University, Bundoora, VIC 3083, Australia
*
Author to whom correspondence should be addressed.
†
Current address: Department of Pathology and Immunology, Baylor College of Medicine, Houston, TX 77030, USA.
‡
Current address: Texas Children’s Microbiome Center, Department of Pathology, Texas Children’s Hospital, Houston, TX 77030, USA.
Biomolecules 2023, 13(7), 1063; https://doi.org/10.3390/biom13071063
Submission received: 2 June 2023 / Revised: 23 June 2023 / Accepted: 25 June 2023 / Published: 30 June 2023
(This article belongs to the Special Issue Neuroimmune Interactions in Neuropsychiatric Diseases)
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Abstract

Mutations in the Neuroligin-3 (Nlgn3) gene are implicated in autism spectrum disorder (ASD) and gastrointestinal (GI) dysfunction, but cellular Nlgn3 expression in the enteric nervous system remains to be characterised. We combined RNAScope in situ hybridization and immunofluorescence to measure Nlgn3 mRNA expression in cholinergic and VIP-expressing submucosal neurons, nitrergic and calretinin-containing myenteric neurons and glial cells in both WT and Nlgn3R451C mutant mice. We measured Nlgn3 mRNA neuronal and glial expression via quantitative three-dimensional image analysis. To validate dual RNAScope/immunofluorescence data, we interrogated available single-cell RNA sequencing (scRNASeq) data to assess for Nlgn3, Nlgn1, Nlgn2 and their binding partners, Nrxn1-3, MGDA1 and MGDA2, in enteric neural subsets. Most submucosal and myenteric neurons expressed Nlgn3 mRNA. In contrast to other Nlgns and binding partners, Nlgn3 was strongly expressed in enteric glia, suggesting a role for neuroligin-3 in mediating enteric neuron–glia interactions. The autism-associated R451C mutation reduces Nlgn3 mRNA expression in cholinergic but not in VIPergic submucosal neurons. In the myenteric plexus, Nlgn3 mRNA levels are reduced in calretinin, nNOS-labelled neurons and S100 β -labelled glia. We provide a comprehensive cellular profile for neuroligin-3 expression in ileal neuronal subpopulations of mice expressing the R451C autism-associated mutation in Nlgn3, which may contribute to the understanding of the pathophysiology of GI dysfunction in ASD.
Keywords: neuroligin-3; autism; enteric nervous system; glia; ileum; RNAScope; immunocytochemistry; scRNASeq neuroligin-3; autism; enteric nervous system; glia; ileum; RNAScope; immunocytochemistry; scRNASeq

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MDPI and ACS Style

Herath, M.; Cho, E.; Marklund, U.; Franks, A.E.; Bornstein, J.C.; Hill-Yardin, E.L. Quantitative Spatial Analysis of Neuroligin-3 mRNA Expression in the Enteric Nervous System Reveals a Potential Role in Neuronal–Glial Synapses and Reduced Expression in Nlgn3R451C Mice. Biomolecules 2023, 13, 1063. https://doi.org/10.3390/biom13071063

AMA Style

Herath M, Cho E, Marklund U, Franks AE, Bornstein JC, Hill-Yardin EL. Quantitative Spatial Analysis of Neuroligin-3 mRNA Expression in the Enteric Nervous System Reveals a Potential Role in Neuronal–Glial Synapses and Reduced Expression in Nlgn3R451C Mice. Biomolecules. 2023; 13(7):1063. https://doi.org/10.3390/biom13071063

Chicago/Turabian Style

Herath, Madushani, Ellie Cho, Ulrika Marklund, Ashley E. Franks, Joel C. Bornstein, and Elisa L. Hill-Yardin. 2023. "Quantitative Spatial Analysis of Neuroligin-3 mRNA Expression in the Enteric Nervous System Reveals a Potential Role in Neuronal–Glial Synapses and Reduced Expression in Nlgn3R451C Mice" Biomolecules 13, no. 7: 1063. https://doi.org/10.3390/biom13071063

APA Style

Herath, M., Cho, E., Marklund, U., Franks, A. E., Bornstein, J. C., & Hill-Yardin, E. L. (2023). Quantitative Spatial Analysis of Neuroligin-3 mRNA Expression in the Enteric Nervous System Reveals a Potential Role in Neuronal–Glial Synapses and Reduced Expression in Nlgn3R451C Mice. Biomolecules, 13(7), 1063. https://doi.org/10.3390/biom13071063

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