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Research Article| Volume 244, 103053, January 2023

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Expression of group II metabotropic glutamate receptors in rat superior cervical ganglion

  • Xixi Wei
    Affiliations
    Henan Key Laboratory of Neurorestoratology, Life Science Research Center, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiankang Road, Weihui 453100, Henan, China
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  • Chenlu Zhao
    Affiliations
    Henan Key Laboratory of Neurorestoratology, Life Science Research Center, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiankang Road, Weihui 453100, Henan, China
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  • Xinyun Jia
    Affiliations
    Henan Key Laboratory of Neurorestoratology, Life Science Research Center, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiankang Road, Weihui 453100, Henan, China
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  • Baosheng Zhao
    Affiliations
    Department of Thoracic Surgery, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiankang Road, Weihui 453100, Henan, China
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  • Yuzhen Liu
    Correspondence
    Corresponding author at: 88 Jiankang Road, Weihui, Henan 453100, China.
    Affiliations
    Henan Key Laboratory of Neurorestoratology, Life Science Research Center, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiankang Road, Weihui 453100, Henan, China

    Department of Thoracic Surgery, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiankang Road, Weihui 453100, Henan, China
    Search for articles by this author
Published:November 21, 2022DOI:https://doi.org/10.1016/j.autneu.2022.103053

      Abstract

      Background

      The superior cervical ganglion (SCG) plays critical roles in the regulation of blood pressure and cardiac output. Metabotropic glutamate receptors (mGluRs) in the SCG are not clearly elucidated yet. Most studies on the expression and functions of mGluRs in the SCG focused on the cultured SCG neurons, and yet little information has been reported in the SCG tissue. Chronic intermittent hypoxia (CIH), one of the major clinical features of obstructive sleep apnea (OSA) patients, is a critical pathological cause of secondary hypertension in OSA patients, but its impact on the level of mGluRs in the SCG is unknown.

      Objective

      To explore the expression and localization of mGluR2/3 and the effect of CIH on mGluR2/3 level in rat SCG tissue.

      Methods

      RT-PCR and immunostaining were conducted to examine the mRNA and protein expression of mGluR2/3 in rat SCG. Immunofluorescence staining was conducted to examine the distribution of mGluR2/3. Rats were divided into control and CIH group which the rats were exposed to CIH for 6 weeks. Western blots were performed to examine the level of mGluR2/3 in rat SCG.

      Results

      mRNAs of mGluR2/3 expressed in rat SCG. mGluR2 distributed in principal neurons and small intensely fluorescent cells but not in satellite glial cells, nerve fibers, and vascular endothelial cells; mGluR3 was detected in nerve fibers rather than in the cells mentioned above. CIH exposure reduced the protein level of mGluR2/3 in rat SCG.

      Conclusion

      mGluR2/3 exists in rat SCG with diverse distribution patterns, and may be involved in CIH-induced hypertension.

      Keywords

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      References

        • Chen T.J.
        • Kukley M.
        Glutamate receptors and glutamatergic signalling in the peripheral nerves.
        Neural Regen. Res. 2020; 15: 438-447https://doi.org/10.4103/1673-5374.266047
        • Cryan J.F.
        • Dev K.K.
        Chapter 4.4 The glutamatergic system as a potential therapeutic target for the treatment of anxiety disorders.
        in: Handb. Behav. Neurosci. 17. 2008: 269-301https://doi.org/10.1016/S1569-7339(07)00013-66
        • Dobó E.
        • Kása P.
        • Joó F.
        • Wenthold R.J.
        • Wolff J.R.
        Structures with GABA-like and GAD-like immunoreactivity in the cervical sympathetic ganglion complex of adult rats.
        Cell Tissue Res. 1900; 262: 351-361https://doi.org/10.1007/BF00309890
        • Dobó E.
        • Joó F.
        • Wolff J.R.
        Distinct subsets of neuropeptide Y-negative principal neurons receive basket-like innervation from enkephalinergic and gabaergic axons in the superior cervical ganglion of adult rats.
        Neuroscience. 1993; 57: 833-844https://doi.org/10.1016/0306-4522(93)90028-e
        • García-Bea A.
        • Walker M.A.
        • Hyde T.M.
        • Kleinman J.E.
        • Harrison P.J.
        • Lane T.A.
        Metabotropic glutamate receptor 3 (mGlu3; mGluR3; GRM3) in schizophrenia: antibody characterisation and a semi-quantitative western blot study.
        Schizophr. Res. 2016; 177: 18-27https://doi.org/10.1016/j.schres.2016.04.015
        • Gereau IV, R.W.
        • Conn P.J.
        Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1.
        J. Neurosci. 1995; 15: 6879-6889https://doi.org/10.1523/JNEUROSCI.15-10-06879.1995
        • Guimarães-Souza E.M.
        • Gardino P.F.
        • De Mello F.G.
        • Calaza K.C.
        A calcium-dependent glutamate release induced by metabotropic glutamate receptors I/II promotes GABA efflux from amacrine cells via a transporter-mediated process.
        Neuroscience. 2011; 179: 23-31https://doi.org/10.1016/j.neuroscience.2011.01.035
        • He Zongbao
        • Youkui Lu.
        • Chen Dongchang
        Overview of domestic research on abnormal cervical blood pressure.
        Chin. J. Phys. Med. Rehabil. 2006; 9 (637-628)
        • Ikeda S.R.
        • Lovinger D.M.
        • McCool B.A.
        • Lewis D.L.
        Heterologous expression of metabotropic glutamate receptors in adult rat sympathetic neurons: subtype-specific coupling to ion channels.
        Neuron. 1995; 14: 1029-1038https://doi.org/10.1016/0896-6273(95)90341-0
        • Ito T.
        • Iino S.
        • Nojyo Y.
        A part of cholinergic fibers in mouse superior cervical ganglia contain GABA or glutamate.
        Brain Res. 2005; 1046: 234-238https://doi.org/10.1016/j.brainres.2005.04.018
        • Jin L.E.
        • Wang M.
        • Yang S.T.
        • Yang Y.
        • Galvin V.C.
        • Lightbourne T.C.
        • Ottenheimer D.
        • Zhong Q.
        • Stein J.
        • Raja A.
        • Paspalas C.D.
        • Arnsten A.F.T.
        mGluR2/3 mechanisms in primate dorsolateral prefrontal cortex: evidence for both presynaptic and postsynaptic actions.
        Mol. Psychiatry. 2017; 22: 1615-1625https://doi.org/10.1038/mp.2016.129
        • Jin L.E.
        • Wang M.
        • Galvin V.C.
        • Lightbourne T.C.
        • Conn P.J.
        • Arnsten A.F.T.
        • Paspalas C.D.
        mGluR2 versus mGluR3 metabotropic glutamate receptors in primate dorsolateral prefrontal cortex: postsynaptic mGluR3 strengthen working memory networks.
        Cereb. Cortex. 2018; 28: 974-987https://doi.org/10.1093/cercor/bhx005
        • Jinliang Zuo
        • Jianlong Han
        • Yingwen Ma.
        Experimental study on the phase distribution of sympathetic nerve in rabbit vertebral artery capsule.
        J. Taishan Med. Coll. 2006; 27: 107-109
        • Kameda Y.
        Signaling molecules and transcription factors involved in the development of the sympathetic nervous system, with special emphasis on the superior cervical ganglion.
        Cell Tissue Res. 2014; 357: 527-548https://doi.org/10.1007/s00441-014-1847-3
        • Kammermeier P.J.
        The orthosteric agonist 2-chloro-5-hydroxyphenylglycine activates mGluR5 and mGluR1 with similar efficacy and potency.
        BMC Pharmacol. 2012; 12: 6https://doi.org/10.1186/1471-2210-12-6
        • Kammermeier P.J.
        Functional and pharmacological characteristics of metabotropic glutamate receptors 2/4 heterodimers.
        Mol. Pharmacol. 2012; 82: 438-447https://doi.org/10.1124/mol.112.078501
        • Kammermeier P.J.
        • Ikeda S.R.
        Metabotropic glutamate receptor expression in the rat superior cervical ganglion.
        Neurosci. Lett. 2002; 330: 260-264https://doi.org/10.1016/s0304-3940(02)00822-4
        • Kiyama H.
        • Sato K.
        • Kuba T.
        • Tohyama M.
        Sympathetic and parasympathetic ganglia express non-NMDA type glutamate receptors: distinct receptor subunit composition in the principle and SIF cells.
        Brain Res. Mol. Brain Res. 1993; 19: 345-348https://doi.org/10.1016/0169-328x(93)90137-e
        • Li C.
        • Zhao B.
        • Fan Y.N.
        • Jia X.
        • Liu Y.
        Expression of BACE1 in the rat carotid body.
        Front. Physiol. 2020; 11: 505https://doi.org/10.3389/fphys.2020.00505
        • Li C.
        • Zhao B.
        • Zhao C.
        • Huang L.
        • Liu Y.
        Metabotropic glutamate receptors 1 regulates rat carotid body response to acute hypoxia via presynaptic mechanism.
        Front. Neurosci. 2021; 15741214https://doi.org/10.3389/fnins.2021.741214
        • Liu Hongtao
        Research progress on the relationship between cervical spine and hypertension.
        J. Pract. Cardiovasc. Cerebrovasc. Dis. 2012; 20: 1214-1244
        • Liu Y.
        • Ji E.S.
        • Xiang S.
        • Tamisier R.
        • Tong J.
        • Huang J.
        • Weiss J.W.
        Exposure to cyclic intermittent hypoxia increases expression of functional NMDA receptors in the rat carotid body.
        J. Appl. Physiol. (1985). 2009; 106: 259-267https://doi.org/10.1152/japplphysiol.90626.2008
        • Liu Y.
        • Li C.
        • Jia X.
        • Huang L.
        • Weiss J.W.
        AMPA receptor-dependent glutamatergic signaling is present in the carotid chemoreceptor.
        Neuroscience. 2018; 382: 59-68https://doi.org/10.1016/j. neuroscience.2018.04.032
        • McCullock T.W.
        • Kammermeier P.J.
        Target validation: weak selectivity of LY341495 for mGluR2 over mGluR4 makes glutamate a less selective agonist.
        Pharmacol. Res. Perspect. 2019; 7: 00471https://doi.org/10.1002/prp2.471
        • McMullan S.
        • Pilowsky P.M.
        Sympathetic premotor neurones project to and are influenced by neurones in the contralateral rostral ventrolateral medulla of the rat in vivo.
        Brain Res. 2012; 1439: 34-43https://doi.org/10.1016/j.brainres.2011.12.058
        • Niswender C.M.
        • Conn P.J.
        Metabotropic glutamate receptors: physiology, pharmacology, and disease.
        Annu. Rev. Pharmacol. Toxicol. 2010; 50: 295-322https://doi.org/10.1146/annurev.pharmtox.011008.145533
        • Pan Zhiqing
        • Pan Xudong
        Forty years of research on cervicogenic hypertension.
        in: Proceedings of the 2008 academic conference of the Liaoyang rehabilitation professional committee of the Chinese association of rehabilitation medicine. 2008
        • Reiner A.
        • Levitz J.
        Glutamatergic signaling in the central nervous system: ionotropic and metabotropic receptors in concert.
        Neuron. 2018; 98: 1080-1098https://doi.org/10.1016/j. neuron.2018.05.018
        • Salman L.A.
        • Shulman R.
        • Cohen J.B.
        Obstructive sleep apnea, hypertension, and cardiovascular risk: epidemiology, pathophysiology, and management.
        Curr. Cardiol. Rep. 2020; 22: 6https://doi.org/10.1007/s11886-020-1257-y
        • Senba E.
        • Kaneko T.
        • Mizuno N.
        • Tohyama M.
        Somato-, branchio- and viscero-motor neurons contain glutaminase-like immunoreactivity.
        Brain Res. Bull. 1991; 26: 85-97https://doi.org/10.1016/0361-9230(91)90193-n
        • Seravalle G.
        • Mancia G.
        • Grassi G.
        Role of the sympathetic nervous system in hypertension and hypertension-related cardiovascular disease.
        High Blood Press. Cardiovasc. Prev. 2014; 21: 89-105https://doi.org/10.1007/s40292-014-0056-1
        • Sheng N.
        • Yang J.
        • Silm K.
        • Edwards R.H.
        • Nicoll R.A.
        A slow excitatory postsynaptic current mediated by a novel metabotropic glutamate receptor in CA1 pyramidal neurons.
        Neuropharmacology. 2017; 115: 4-9https://doi.org/10.1016/j. neuropharm.2016.08.028
        • Shigemoto R.
        • Kinoshita A.
        • Wada E.
        • Nomura S.
        • Ohishi H.
        • Takada M.
        • Flor P.J.
        • Neki A.
        • Abe T.
        • Nakanishi S.
        • Mizuno N.
        Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus.
        J. Neurosci. 1997; 17: 7503-7522https://doi.org/10.1523/JNEUROSCI.17-19-07503.1997
        • Sica A.L.
        • Greenberg H.E.
        • Ruggiero D.A.
        • Scharf S.M.
        Chronic-intermittent hypoxia: a model of sympathetic activation in the rat.
        Respir. Physiol. 2000; 121: 173-184https://doi.org/10.1016/s0034-5687(00)00126-2
        • Sladeczek F.
        • Momiyama A.
        • Takahashi T.
        Presynaptic inhibitory action of a metabotropic glutamate receptor agonist on excitatory transmission in visual cortical neurons.
        Proc. Biol. Sci. 1993; 253: 297-303https://doi.org/10.1098/rspb.1993.0117
        • Traynelis S.F.
        • Wollmuth L.P.
        • McBain C.J.
        • Menniti F.S.
        • Vance K.M.
        • Ogden K.K.
        • Hansen K.B.
        • Yuan H.
        • Myers S.J.
        • Dingledine R.
        Glutamate receptor ion channels: structure, regulation, and function.
        Pharmacol. Rev. 2010; 62: 405-496https://doi.org/10.1124/pr.109.002451
        • Tremolizzo L.
        • Sala G.
        • Zoia C.P.
        • Ferrarese C.
        Assessing glutamatergic function and dysfunction in peripheral tissues.
        Curr. Med. Chem. 2012; 19: 1310-1315https://doi.org/10.2174/092986712799462702
        • Turati J.
        • Rudi J.
        • Beauquis J.
        • Carniglia L.
        • López Couselo F.
        • Saba J.
        • Caruso C.
        • Saravia F.
        • Lasaga M.
        • Durand D.
        A metabotropic glutamate receptor 3 (mGlu3R) isoform playing neurodegenerative roles in astrocytes is prematurely up-regulated in an Alzheimer's model.
        J. Neurochem. 2022; 161: 366-382https://doi.org/10.1111/jnc.15610
        • Wang F.B.
        • Cheng P.M.
        • Chi H.C.
        • Kao C.K.
        • Liao Y.H.
        Axons of passage and inputs to superior cervical ganglion in rat.
        Anat. Rec. 2018; 301: 1906-1916https://doi.org/10.1002/ar.23953
        • Wolff J.R.
        • Kása P.
        • Dobó E.
        • Römgens H.J.
        • Párducz A.
        • Joó F.
        • Wolff A.
        Distribution of GABA-immunoreactive nerve fibers and cells in the cervical and thoracic paravertebral sympathetic trunk of adult rat: evidence for an ascending feed-forward inhibition system.
        J. Comp. Neurol. 1993; 334: 281-293https://doi.org/10.1002/cne.903340209