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      An Atlas of Vagal Sensory Neurons and Their Molecular Specialization

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          Summary

          Sensory functions of the vagus nerve are critical for conscious perceptions and for monitoring visceral functions in the cardio-pulmonary and gastrointestinal systems. Here, we present a comprehensive identification, classification, and validation of the neuron types in the neural crest (jugular) and placode (nodose) derived vagal ganglia by single-cell RNA sequencing (scRNA-seq) transcriptomic analysis. Our results reveal major differences between neurons derived from different embryonic origins. Jugular neurons exhibit fundamental similarities to the somatosensory spinal neurons, including major types, such as C-low threshold mechanoreceptors (C-LTMRs), A-LTMRs, Aδ-nociceptors, and cold-, and mechano-heat C-nociceptors. In contrast, the nodose ganglion contains 18 distinct types dedicated to surveying the physiological state of the internal body. Our results reveal a vast diversity of vagal neuron types, including many previously unanticipated types, as well as proposed types that are consistent with chemoreceptors, nutrient detectors, baroreceptors, and stretch and volume mechanoreceptors of the respiratory, gastrointestinal, and cardiovascular systems.

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          Highlights

          • A comprehensive molecular identification of neuronal types in vagal ganglion complex

          • Prdm12 + jugular ganglion neurons share features with spinal somatosensory neurons

          • Phox2b + viscerosensory nodose neurons are molecularly versatile and highly specialized

          • Nodose neuron types are consistent with chemo-, baro-, stretch-, tension-, and volume-sensors

          Abstract

          Visceral sensory neurons are necessary for the control of organ functions, but knowledge on the complexity of neuron types involved is missing. Kupari et al. molecularly identify jugular and nodose ganglion neurons and find a large diversity of neuron types that are consistent with the numerous sensory functions of the vagus nerve.

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          Most cited references43

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          Bias, robustness and scalability in single-cell differential expression analysis

          Many methods have been used to determine differential gene expression from single-cell RNA (scRNA)-seq data. We evaluated 36 approaches using experimental and synthetic data and found considerable differences in the number and characteristics of the genes that are called differentially expressed. Prefiltering of lowly expressed genes has important effects, particularly for some of the methods developed for bulk RNA-seq data analysis. However, we found that bulk RNA-seq analysis methods do not generally perform worse than those developed specifically for scRNA-seq. We also present conquer, a repository of consistently processed, analysis-ready public scRNA-seq data sets that is aimed at simplifying method evaluation and reanalysis of published results. Each data set provides abundance estimates for both genes and transcripts, as well as quality control and exploratory analysis reports.
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            The vagus nerve and the inflammatory reflex--linking immunity and metabolism.

            The vagus nerve has an important role in regulation of metabolic homeostasis, and efferent vagus nerve-mediated cholinergic signalling controls immune function and proinflammatory responses via the inflammatory reflex. Dysregulation of metabolism and immune function in obesity are associated with chronic inflammation, a critical step in the pathogenesis of insulin resistance and type 2 diabetes mellitus. Cholinergic mechanisms within the inflammatory reflex have, in the past 2 years, been implicated in attenuating obesity-related inflammation and metabolic complications. This knowledge has led to the exploration of novel therapeutic approaches in the treatment of obesity-related disorders.
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              The functional organization of cutaneous low-threshold mechanosensory neurons.

              Innocuous touch of the skin is detected by distinct populations of neurons, the low-threshold mechanoreceptors (LTMRs), which are classified as Aβ-, Aδ-, and C-LTMRs. Here, we report genetic labeling of LTMR subtypes and visualization of their relative patterns of axonal endings in hairy skin and the spinal cord. We found that each of the three major hair follicle types of trunk hairy skin (guard, awl/auchene, and zigzag hairs) is innervated by a unique and invariant combination of LTMRs; thus, each hair follicle type is a functionally distinct mechanosensory end organ. Moreover, the central projections of Aβ-, Aδ-, and C-LTMRs that innervate the same or adjacent hair follicles form narrow LTMR columns in the dorsal horn. These findings support a model of mechanosensation in which the activities of Aβ-, Aδ-, and C-LTMRs are integrated within dorsal horn LTMR columns and processed into outputs that underlie the perception of myriad touch sensations. Copyright © 2011 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Cell Rep
                Cell Rep
                Cell Reports
                Cell Press
                2211-1247
                21 May 2019
                21 May 2019
                21 May 2019
                : 27
                : 8
                : 2508-2523.e4
                Affiliations
                [1 ]Division of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, 17177 Stockholm, Sweden
                [2 ]Ming Wai Lau Centre for Reparative Medicine, Stockholm node, Karolinska Institutet, Stockholm, Sweden
                Author notes
                []Corresponding author patrik.ernfors@ 123456ki.se
                [3]

                Lead Contact

                Article
                S2211-1247(19)30576-5
                10.1016/j.celrep.2019.04.096
                6533201
                31116992
                d350e6c6-569c-4b61-9295-3d93b7d55b5b
                © 2019 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 14 January 2019
                : 25 March 2019
                : 22 April 2019
                Categories
                Article

                Cell biology
                single cell rna-sequencing,vagus nerve,sensory neurons,viscerosensory,somatosensory,transcriptome,jugular ganglion,nodose ganglion,mechanoreceptor,nociceptor

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