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Distribution of proteins for synaptic release in nerve endings associated with the trachealis muscle of rats

Published:November 07, 2022DOI:https://doi.org/10.1016/j.autneu.2022.103042

      Abstract

      The immunohistochemical localization of proteins for synaptic release was examined in smooth muscle-associated sensory nerve endings using whole-mount preparations of the rat trachea. Plant-like smooth muscle-associated nerve endings with immunoreactivity for Na+-K+-ATPase, α3-subunit were identified in the trachealis muscle. VGLUT1, synapsin1, t-SNARE proteins (SNAP25 and syntaxin1), v-SNARE proteins (VAMP1 and VAMP2), and a presynaptic active zone-related protein (piccolo) were detected in the terminal parts of these endings. These results suggest that smooth muscle-associated nerve endings secrete glutamate to modulate sensorimotor functions in the lung deflation reflex.

      Keywords

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      References

        • Anaparti V.
        • Ilarraza R.
        • Orihara K.
        • Stelmack G.L.
        • Ojo O.O.
        • Mahood T.H.
        • Unruh H.
        • Halayko A.J.
        • Moqbel R.
        NMDA receptors mediate contractile responses in human airway smooth muscle cells.
        Am. J. Physiol. Lung Cell. Mol. Physiol. 2015; 308: 1253-1264https://doi.org/10.1152/ajplung.00402.2014
        • Banks R.W.
        • Cahusac P.M.B.
        • Graca A.
        • Kain N.
        • Shenton F.
        • Singh P.
        • Njå A.
        • Simon A.
        • Watson S.
        • Slater C.R.
        • Bewick G.S.
        Glutamatergic modulation of synaptic-like vesicle recycling in mechanosensory lanceolate nerve terminals of mammalian hair follicles.
        J. Physiol. 2013; 591: 2523-2540https://doi.org/10.1113/jphysiol.2012.243659
        • Bewick G.S.
        • Reid B.
        • Richardson C.
        • Banks R.W.
        Autogenic modulation of mechanoreceptor excitability by glutamate release from synaptic-like vesicles: evidence from the rat muscle spindle primary sensory ending.
        J. Physiol. 2005; 562: 381-394https://doi.org/10.1113/jphysiol.2004.074799
        • Brouns I.
        • de Proost I.
        • Pintelon I.
        • Timmermans J.P.
        • Adriaensen D.
        Sensory receptors in the airways: neurochemical coding of smooth muscle-associated airway receptors and pulmonary neuroepithelial body innervation.
        Auton. Neurosci. 2006; 126–127: 307-319https://doi.org/10.1016/j.autneu.2006.02.006
        • Cahusac P.M.B.
        • Senok S.S.
        • Hitchcock I.S.
        • Genever P.G.
        • Baumann K.I.
        Are unconventional NMDA receptors involved in slowly adapting type I mechanoreceptor responses?.
        Neuroscience. 2005; 133: 763-773https://doi.org/10.1016/j.neuroscience.2005.03.018
        • Cesca F.
        • Baldelli P.
        • Valtorta F.
        • Benfenati F.
        The synapsins: key actors of synapse function and plasticity.
        Prog. Neurobiol. 2010; 91: 313-348https://doi.org/10.1016/j.pneurobio.2010.04.006
        • Duman J.G.
        • Forte J.G.
        What is the role of SNARE proteins in membrane fusion?.
        Am. J. Physiol. Cell Physiol. 2003; 285 (54-52)https://doi.org/10.1152/ajpcell.00091.2003
        • Honma S.
        • Kato A.
        • Shi L.
        • Yatani H.
        • Wakisaka S.
        Vesicular glutamate transporter immunoreactivity in the periodontal ligament of the rat incisor.
        Anat. Rec. 2012; 295: 160-166https://doi.org/10.1002/ar.21465
        • Honma S.
        • Kadono K.
        • Kawano A.
        • Wakisaka S.
        Immunohistochemical localization of SNARE core proteins in intrapulpal and intradentinal nerve fibers of rat molar teeth.
        Arch. Oral Biol. 2017; 73: 248-252https://doi.org/10.1016/j.archoralbio.2016.10.025
        • Lee L.-Y.
        • Yu J.
        Sensory nerves in lung and airways.
        Compr. Physiol. 2014; 4: 287-324https://doi.org/10.1002/cphy.c130020
        • Liu J.
        • Song N.
        • Guardiola J.
        • Roman J.
        • Yu J.
        Slowly adapting sensory units have more receptors in large airways than in small airways in rabbits.
        Front. Physiol. 2016; 7: 1-7https://doi.org/10.3389/fphys.2016.00588
        • Liu C.
        • Kershberg L.
        • Wang J.
        • Schneeberger S.
        • Kaeser P.S.
        Dopamine secretion is mediated by sparse active zone-like release sites.
        Cell. 2018; 172e15https://doi.org/10.1016/j.cell.2018.01.008
        • Liu J.
        • Song N.
        • Wang Y.
        • Walker J.
        • Yu J.
        A single baroreceptor unit consists of multiple sensors.
        Sci. Rep. 2021; 11: 23111https://doi.org/10.1038/S41598-021-02563-X
        • Mazzone S.B.
        • Undem B.J.
        Vagal afferent innervation of the airways in health and disease.
        Physiol. Rev. 2016; 96: 975-1024https://doi.org/10.1152/physrev.00039.2015
        • Pintelon I.
        • Brouns I.
        • de Proost I.
        • van Meir F.
        • Timmermans J.P.
        • Adriaensen D.
        Sensory receptors in the visceral pleura: neurochemical coding and live staining in whole mounts.
        Am. J. Resp. Cell Mol. Biol. 2007; 36: 541-551https://doi.org/10.1165/rcmb.2006-0256OC
        • Schoch S.
        • Gundelfinger E.D.
        Molecular organization of the presynaptic active zone.
        Cell Tissue Res. 2006; 326: 379-391https://doi.org/10.1007/S00441-006-0244-Y
        • Soda Y.
        • Yamamoto Y.
        Morphology and chemical characteristics of subepithelial laminar nerve endings in the rat epiglottic mucosa.
        Histochem. Cell Biol. 2012; 138: 25-39https://doi.org/10.1007/s00418-012-0939-y
        • Than K.
        • Kim E.
        • Navarro C.
        • Chu S.
        • Klier N.
        • Occiano A.
        • Ortiz S.
        • Salazar A.
        • Valdespino S.R.
        • Villegas N.K.
        • Wilkinson K.A.
        Vesicle-released glutamate is necessary to maintain muscle spindle afferent excitability but not dynamic sensitivity in adult mice.
        J. Physiol. 2021; 599: 2953-2967https://doi.org/10.1113/JP281182
        • Wu S.X.
        • Koshimizu Y.
        • Feng Y.P.
        • Okamoto K.
        • Fujiyama F.
        • Hioki H.
        • Li Y.Q.
        • Kaneko T.
        • Mizuno N.
        Vesicular glutamate transporter immunoreactivity in the central and peripheral endings of muscle-spindle afferents.
        Brain Res. 2004; 1011: 247-251https://doi.org/10.1016/j.brainres.2004.03.047
        • Yamamoto Y.
        • Hayashi M.
        • Atoji Y.
        • Suzuki Y.
        Vagal afferent nerve endings in the trachealis muscle of the dog.
        Arch. Histol. Cytol. 1994; 57: 473-480
        • Yamamoto Y.
        • Atoji Y.
        • Suzuki Y.
        Calretinin immunoreactive nerve endings in the trachea and bronchi of the rat.
        J. Vet. Med. Sci. 1999; 61: 267-269
        • Yamamoto Y.
        • Moriai H.
        • Yokoyama T.
        • Nakamuta N.
        Immunohistochemical distribution of proteins involved in glutamate release in subepithelial sensory nerve endings of rat epiglottis.
        Histochem. Cell Biol. 2022; 157: 51-63https://doi.org/10.1007/S00418-021-02038-0
        • Yokoyama T.
        • Nakamuta N.
        • Kusakabe T.
        • Yamamoto Y.
        Vesicular glutamate transporter 2-immunoreactive afferent nerve terminals in the carotid body of the rat.
        Cell Tissue Res. 2014; 358: 271-275https://doi.org/10.1007/s00441-014-1921-x
        • Yokoyama T.
        • Settai K.
        • Nakamuta N.
        • Yamamoto Y.
        Vesicular glutamate transporter 2-immunoreactive afferent nerve terminals in rat carotid sinus baroreceptors.
        Acta Histochem. 2020; 122151469https://doi.org/10.1016/j.acthis.2019.151469
        • Yu J.
        • Wang Y.F.
        • Zhang J.W.
        Structure of slowly adapting pulmonary stretch receptors in the lung periphery.
        J. Appl. Physiol. 2003; 95: 385-393https://doi.org/10.1152/japplphysiol.00137.2003