Differential immunostaining patterns of transient receptor potential (TRP) ion channels in the rat nodose ganglion
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
Fulbright Scholarship from the Fulbright Commission (HK)
Case Western Reserve University
Czech Academy of Sciences
Czech Science Foundation
PubMed
35396708
PubMed Central
PMC9296033
DOI
10.1111/joa.13656
Knihovny.cz E-zdroje
- Klíčová slova
- TRPA1, TRPC1, TRPM3, TRPM8, TRPV1, TRPV4, autonomic nervous system, blood vessels, confocal microscopy, immunohistochemistry, nodose ganglion, vagus nerve,
- MeSH
- ganglion inferius metabolismus MeSH
- kationtové kanály TRP * metabolismus MeSH
- kationtové kanály TRPM * metabolismus MeSH
- kationtové kanály TRPV MeSH
- krysa rodu Rattus MeSH
- nervus vagus metabolismus MeSH
- potkani Sprague-Dawley MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- kationtové kanály TRP * MeSH
- kationtové kanály TRPM * MeSH
- kationtové kanály TRPV MeSH
- TRPM3 protein, rat MeSH Prohlížeč
- Trpv4 protein, rat MeSH Prohlížeč
Vagal afferents regulate numerous physiological functions including arterial blood pressure, heart rate, breathing, and nociception. Cell bodies of vagal afferents reside in the inferior vagal (nodose) ganglia and their stimulation by various means is being considered as a way to regulate cardiorespiratory responses and control pain sensations. Stimulation of the nodose by exposure to infrared light is recently being considered as a precise way to elicit responses. These responses would likely involve the activity of temperature-sensitive membrane-bound channels. While papers have been published to track the expression of these transient receptor potential ion channels (TRPs), further studies are warranted to determine the in situ expression of the endogenous TRP proteins in the nodose ganglia to fully understand their pattern of expression, subcellular locations, and functions in this animal model. TRP ion channels are a superfamily of Na+ /Ca2+ -channels whose members are temperature- and/or mechano-sensitive and therefore represent a potential set of proteins that will be activated directly or indirectly by infrared light. Here, we report the spatial localization of six TRP channels, TRPV1, TRPV4, TRPM3, TRPM8, TRPA1, and TRPC1, from nodose ganglia taken from juvenile male Sprague-Dawley rats. The channels were detected using immunohistology with fluorescent tags on cryosections and imaged using confocal microscopy. All six TRP channels were detected with different levels of intensity in neuronal cell bodies and some were also detected in axonal fibers and blood vessels. The TRP receptors differed in their prevalence, in their patterns of expression, and in subcellular expression/localization. More specifically, TRPV1, TRPV4, TRPA1, TRPM8, TRPC1, and TRPM3 were found in vagal afferent cell bodies with a wide range of immunostaining intensity from neuron to neuron. Immunostaining for TRPV1, TRPV4, and TRPA1 appeared as fine particles scattered throughout the cytoplasm of the cell body. Intense TRPV1 immunostaining was also evident in a subset of axonal fibers. TRPM8 and TRPC1 were expressed in courser particles suggesting different subcellular compartments than for TRPV1. The localization of TRPM3 differed markedly from the other TRP channels with an immunostaining pattern that was localized to the periphery of a subset of cell bodies, whereas a scattering or no immunostaining was detected within the bulk of the cytoplasm. TRPV4 and TRPC1 were also expressed on the walls of blood vessels. The finding that all six TRP channels (representing four subfamilies) were present in the nodose ganglia provides the basis for studies designed to understand the roles of these channels in sensory transmission within vagal afferent fibers and in the responses elicited by exposure of nodose ganglia to infrared light and other stimuli. Depending on the location and functionality of the TRP channels, they may regulate the flux of Na+ /Ca2+ -across the membranes of cell bodies and axons of sensory afferents, efferent (motor) fibers coursing through the ganglia, and in vascular smooth muscle.
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Alonso‐Carbajo, L. , Kecskes, M. , Jacobs, G. , Pironet, A. , Syam, N. , Talavera, K. et al. (2017) Muscling in on TRP channels in vascular smooth muscle cells cardiomyocytes. Cell Calcium, 66, 48–61. 10.1016/j.ceca.2017.06.004 PubMed DOI
Baker, C. (2005) The embryology of vagal sensory neurons. In: Undem, B.J. & Weinreich, D. (Eds.) Advances in neurobiology. Boca Raton, FL: CRC.
Baker, C.V.H. & Bronner‐Fraser, M. (2001) Vertebrate cranial placodes I. Embryonic induction. Developmental Biology, 232, 1–61. 10.1006/dbio.2001.0156 PubMed DOI
Benemei, S. , Patacchini, R. , Trevisani, M. & Geppetti, P. (2015) TRP channels. Current Opinion in Pharmacology, 22, 18–23. 10.1016/j.coph.2015.02.006 PubMed DOI
Ben‐Menachem, E. (2012) Neurostimulation‐past, present, and beyond. Epilepsy Currents, 12(5), 188–191. 10.5698/1535-7511-12.5.188 PubMed DOI PMC
Berrout, J. , Jin, M. , Mamenko, M. , Zaika, O. , Pochynyuk, O. & O’Neil, R.G. (2012) Function of transient receptor potential cation channel subfamily V member 4 (TRPV4) as a mechanical transducer in flow‐sensitive segments of renal collecting duct system. Journal of Biological Chemistry, 287(12), 8782–8791. 10.1074/jbc.M111.308411 PubMed DOI PMC
Bezzerides, V.J. , Ramsey, I.S. , Kotecha, S. , Greka, A. & Clapham, D.E. (2004) Rapid vesicular translocation and insertion of TRP channels. Nature Cell Biology, 6, 709–720. 10.1038/ncb1150 PubMed DOI
Bidaux, G. , Borowiec, A.‐S. , Gordienko, D. , Beck, B. , Shapovalov, G.G. , Lemonnier, L. et al. (2015) Epidermal TRPM8 channel isoform controls the balance between keratinocyte proliferation and differentiation in a cold‐dependent manner. Proceedings of the National Academy of Sciences of the USA, 112(26), E3345–E3354. 10.1073/pnas.1423357112 PubMed DOI PMC
Bidaux, G. , Gordienko, D. , Shapovalov, G. , Farfariello, V. , Borowiec, A.‐S. , Iamshanova, O. et al. (1865) 4TM‐TRPM8 channels are new gatekeepers of the ER‐mitochondria Ca2+ transfer. Biochimica Et Biophysica Acta (BBA) – Molecular Cell Research, 981–994, 2018. 10.1016/j.bbamcr.2018.04.007 PubMed DOI
Boisseau, S. , Kunert‐Keil, C. , Lucke, S. & Bouron, A. (2009) Heterogeneous distribution of TRPC proteins in the embryonic cortex. Histochemistry and Cell Biology, 131, 355–363. 10.1007/s00418-008-0532-6 PubMed DOI
Castillo, K. , Diaz‐Franulic, I. , Canan, J. , Gonzalez‐Nilo, F. & Latorre, R. (2018) Thermally activated TRP channels: molecular sensors for temperature detection. Physical Biology, 15, 021001. 10.1088/1478-3975/aa9a6f PubMed DOI
Cavanaugh, D.J. , Chesler, A.T. , Jackson, A.C. , Sigal, Y.M. , Yamanaka, H. , Grant, R. et al. (2011) Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. Journal of Neuroscience, 31, 5067–5077. 10.1523/JNEUROSCI.6451-10.2011 PubMed DOI PMC
Cayce, J.M. , Wells, J.D. , Malphrus, J.D. , Kao, C. , Thomsen, S. , Tulipan, N.B. et al. (2015) Infrared neural stimulation of human spinal nerve roots in vivo. Neurophotonics, 2, 015007. 10.1117/1.NPh.2.1.015007 PubMed DOI PMC
Chen, H.‐C. , Wang, C. , Shih, C. , Chueh, S. , Liu, S. , Chen, H. et al. (2015) TRPC1 is required for survival and proliferation of cochlear spiral ganglion stem/progenitor cells. International Journal of Pediatric Otorhinolaryngology, 79, 2290–2294. 10.1016/j.ijporl.2015.10.027 PubMed DOI
Conklin, D.J. , Guo, Y. , Nystoriak, M.A. , Jagatheesan, G. , Obal, D. , Kilfoil, P.J. et al. (2019) TRPA1 channel contributes to myocardial ischemia–reperfusion injury. American Journal of Physiology‐Heart and Circulatory Physiology, 316(4), H889–H899. 10.1152/ajpheart.00106.2018 PubMed DOI PMC
Dhaka, A. , Earley, T.J. , Watson, J. & Patapoutian, A. (2008) Visualizing cold spots: TRPM8‐expressing sensory neurons and their projections. Journal of Neuroscience, 28, 566–575. 10.1523/JNEUROSCI.3976-07.2008 PubMed DOI PMC
Duke, A.R. , Lu, H. , Jenkins, M.W. , Chiel, H.J. & Jansen, E.D. (2012) Spatial and temporal variability in response to hybrid electro‐optical stimulation. Journal of Neural Engineering, 9, 036003. 10.1088/1741-2560/9/3/036003 PubMed DOI PMC
Duke, A.R. , Jenkins, M.W. , Lu, H. , McManus, J.M. , Chiel, H.J. & Jansen, E.D. (2013) Transient and selective suppression of neural activity with infrared light. Scientific Reports, 3, 2600. 10.1038/srep02600 PubMed DOI PMC
Earley, S. (2010) Vanilloid and melastatin transient receptor potential channels in vascular smooth muscle. Microcirculation, 17, 237–249. 10.1111/j.1549-8719.2010.00026.x PubMed DOI PMC
Elg, S. , Marmigere, F. , Mattsson, J.P. & Ernfors, P. (2007) Cellular subtype distribution and developmental regulation of TRPC channel members in the mouse dorsal root ganglion. The Journal of Comparative Neurology, 503, 35–46. 10.1002/cne.21351 PubMed DOI
Elokely, K. , Velisetty, P. , Delemotte, L. , Palovcak, E. , Klein, M.L. , Rohacs, T. et al. (2016) Understanding TRPV1 activation by ligands: Insights from the binding modes of capsaicin and resiniferatoxin. Proceedings of the National Academy of Sciences of the USA, 113, E137–E145. 10.1073/pnas.1517288113 PubMed DOI PMC
Ferrandiz‐Huertas, C. , Mathivanan, S. , Wolf, C. , Devesa, I. & Ferrer‐Montiel, A. (2014) Trafficking of ThermoTRP channels. Membranes, 4(3), 525–564. 10.3390/membranes4030525 PubMed DOI PMC
Ford, S.M. , Watanabe, M. & Jenkins, M.W. (2018) A review of optical pacing with infrared light. Journal of Neural Engineering, 15, 011001. 10.1088/1741-2552/aa795f PubMed DOI PMC
Fujita, M. , Sato, T. , Yajima, T. , Masaki, E. & Ichikawa, H. (2017) TRPC1, TRPC3, and TRPC4 in rat orofacial structures. Cells Tissues Organs, 204, 293–303. 10.1159/000477665 PubMed DOI
Gasperini, R. , Choi‐Lundberg, D. , Thompson, M.J. , Mitchell, C.B. & Foa, L. (2009) Homer regulates calcium signalling in growth cone turning. Neural Development, 4, 29. 10.1186/1749-8104-4-29 PubMed DOI PMC
Gees, M. , Colsoul, B. & Nilius, B. (2010) The role of transient receptor potential cation channels in Ca2+ signaling. Cold Spring Harbor Perspectives in Biology, 2, a003962. 10.1101/cshperspect.a003962 PubMed DOI PMC
Gerritsen, R.J.S. & Band, G.P.H. (2018) Breath of life: The respiratory vagal stimulation model of contemplative activity. Frontiers in Human Neuroscience, 12, 397. 10.3389/fnhum.2018.00397 PubMed DOI PMC
Glazebrook, P.A. , Schilling, W.P. & Kunze, D.L. (2005) TRPC channels as signal transducers. Pflügers Archiv – European Journal of Physiology, 451, 125–130. 10.1007/s00424-005-1468-5 PubMed DOI
Goswami, C. , Rademacher, N. , Smalla, K.‐H. , Kalscheuer, V. , Ropers, H.‐H. , Gundelfinger, E.D. et al. (2010) TRPV1 acts as a synaptic protein and regulates vesicle recycling. Journal of Cell Science, 123, 2045–2057. 10.1242/jcs.065144 PubMed DOI
Hanani, M. (2010) Satellite glial cells: More than just rings around the neuron. Neuron Glia Biology, 6, 1–2. PubMed
Hanani, M. (2010) Satellite glial cells in sympathetic and parasympathetic ganglia: In search of function. Brain Research Reviews, 64, 304–327. 10.1016/j.brainresrev.2010.04.009 PubMed DOI
Hoffstaetter, L.J. , Bagriantsev, S.N. & Gracheva, E.O. (2018) TRPs et al.: a molecular toolkit for thermosensory adaptations. Pflügers Archiv – European Journal of Physiology, 470, 745–759. 10.1007/s00424-018-2120-5 PubMed DOI PMC
Holzer, P. (2008) The pharmacological challenge to tame the transient receptor potential vanilloid‐1 (TRPV1) nocisensor. British Journal of Pharmacology, 155, 1145–1162. 10.1038/bjp.2008.351 PubMed DOI PMC
Hondoh, A. , Ishida, Y. , Ugawa, S. , Ueda, T. , Shibata, Y. , Yamada, T. et al. (2010) Distinct expression of cold receptors (TRPM8 and TRPA1) in the rat nodose‐petrosal ganglion complex. Brain Research, 1319, 60–69. 10.1016/j.brainres.2010.01.016 PubMed DOI
Jardín, I. , López, J.J. , Diez, R. , Sánchez‐Collado, J. , Cantonero, C. , Albarrán, L. et al. (2017) TRPs in pain sensation. Frontiers in Physiology, 8, 392. doi: 10.3389/fphys.2017.00392 PubMed DOI PMC
Jeon, S. & Caterina, M.J. (2018) Molecular basis of peripheral innocuous warmth sensitivity. In: Handbook of clinical neurology, pp. 69–82. Amsterdam, Netherlands: Elsevier; PubMed
Katz, D.M. , Erb, M. , Lillis, R. & Neet, K. (1990) Trophic regulation of nodose ganglion cell development: evidence for an expanded role of nerve growth factor during embryogenesis in the rat. Experimental Neurology, 110, 1–10. 10.1016/0014-4886(90)90046-U PubMed DOI
Kotagal, P. (2011) Neurostimulation: Vagus nerve stimulation and beyond. Seminars in Pediatric Neurology, 18, 186–194. 10.1016/j.spen.2011.06.005 PubMed DOI
Lacolley, P. , Owen, J.R. , Sandock, K. , Lewis, T.H.J. , Bates, J.N. , Robertson, T.P. et al. (2006) Occipital artery injections of 5‐HT may directly activate the cell bodies of vagal and glossopharyngeal afferent cell bodies in the rat. Neuroscience, 143, 289–308. 10.1016/j.neuroscience.2006.08.047 PubMed DOI
Lee, S.W. , Kulkarni, K. , Annoni, E.M. , Libbus, I. , KenKnight, B.H. & Tolkacheva, E.G. (2018) Stochastic vagus nerve stimulation affects acute heart rate dynamics in rats. PLoS One, 13, e0194910. 10.1371/journal.pone.0194910 PubMed DOI PMC
Lindsay, R.M. , Thoenen, H. & Barde, Y.‐A. (1985) Placode and neural crest‐derived sensory neurons are responsive at early developmental stages to brain‐derived neurotrophic factor. Developmental Biology, 112, 319–328. 10.1016/0012-1606(85)90402-6 PubMed DOI
Lothet, E.H. , Kilgore, K.L. , Bhadra, N. , Bhadra, N. , Vrabec, T. , Wang, Y.T. et al. (2014) Alternating current and infrared produce an onset‐free reversible nerve block. Neurophotonics, 1, 011010. 10.1117/1.NPh.1.1.011010 PubMed DOI PMC
Lothet, E.H. , Shaw, K.M. , Lu, H. , Zhuo, J. , Wang, Y.T. , Gu, S. et al. (2017) Selective inhibition of small‐diameter axons using infrared light. Scientific Reports, 7, 3275. 10.1038/s41598-017-03374-9 PubMed DOI PMC
Mahieu, F. , Owsianik, G. , Verbert, L. , Janssens, A. , De Smedt, H. , Nilius, B. et al. (2007) TRPM8‐independent menthol‐induced Ca2+ release from endoplasmic reticulum and Golgi. Journal of Biological Chemistry, 282, 3325–3336. 10.1074/jbc.M605213200 PubMed DOI
Martínez‐García, M.C. , Martínez, T. , Pañeda, C. , Gallego, P. , Jimenez, A.I. & Merayo, J. (2013) Differential expression and localization of transient receptor potential vanilloid 1 in rabbit and human eyes. Histology and Histopathology, 28, 1507–1516. 10.14670/HH-28.1507 PubMed DOI
Mazzone, S.B. & Undem, B.J. (2016) Vagal afferent innervation of the airways in health and disease. Physiological Reviews, 96, 975–1024. 10.1152/physrev.00039.2015 PubMed DOI PMC
Meng, Q. , Fang, P. , Hu, Z. , Ling, Y. & Liu, H. (2015) Mechanotransduction of trigeminal ganglion neurons innervating inner walls of rat anterior eye chambers. American Journal of Physiology‐Cell Physiology, 309, C1–C10. 10.1152/ajpcell.00028.2015 PubMed DOI
Menigoz, A. & Boudes, M. (2011) The expression pattern of TRPV1 in brain. Journal of Neuroscience, 31, 13025–13027. 10.1523/JNEUROSCI.2589-11.2011 PubMed DOI PMC
Premkumar, L.S. Methods used for studying TRP channel functions in sensory neurons [Online]. http://www.ncbi.nlm.nih.gov/pubmed/22593954 PubMed
Ragozzino, F.J. , Arnold, R.A. , Fenwick, A.J. , Riley, T.P. , Lindberg, J.E.M. , Peterson, B.A. et al. (2021) TRPM3 expression and control of glutamate release from primary vagal afferent neurons. Journal of Neurophysiology, 125, 199–210. 10.1152/jn.00229.2020 PubMed DOI PMC
Ruggiero, D.A. , Mtui, E.P. , Otake, K. & Anwar, M. (1996) Central and primary visceral afferents to nucleus tractus solitarii may generate nitric oxide as a membrane‐permeant neuronal messenger. The Journal of Comparative Neurology, 364, 51–67. 10.1002/(SICI)1096-9861(19960101)364:1<51:AID-CNE5>3.0.CO;2-R PubMed DOI
Sand, C.A. , Grant, A.D. & Nandi, M. (2015) Vascular expression of transient receptor potential vanilloid 1 (TRPV1). Journal of Histochemistry & Cytochemistry, 63(6), 449–453. 10.1369/0022155415581014 PubMed DOI PMC
Shin, S.M. , Itson‐Zoske, B. , Cai, Y. , Qiu, C. , Pan, B. , Stucky, C.L. et al. (2020) Satellite glial cells in sensory ganglia express functional transient receptor potential ankyrin 1 that is sensitized in neuropathic and inflammatory pain. Molecular Pain, 16, 1–19. 10.1177/1744806920925425 PubMed DOI PMC
Staaf, S. , Franck, M.C.M. , Marmigère, F. , Mattsson, J.P. & Ernfors, P. (2010) Dynamic expression of the TRPM subgroup of ion channels in developing mouse sensory neurons. Gene Expression Patterns, 10, 65–74. 10.1016/j.gep.2009.10.003 PubMed DOI
Sun, Y. , Zhang, H. , Selvaraj, S. , Sukumaran, P. , Lei, S. , Birnbaumer, L. et al. (2017) Inhibition of L‐type Ca2+ channels by TRPC1‐STIM1 complex is essential for the protection of dopaminergic neurons. The Journal of Neuroscience, 37(12), 3364–3377. 10.1523/JNEUROSCI.3010-16.2017 PubMed DOI PMC
Takumida, M. & Anniko, M. (2009) Expression of canonical transient receptor potential channel (TRPC) 1–7 in the mouse inner ear. Acta Oto‐Laryngologica, 129, 1351–1358. 10.3109/00016480902798350 PubMed DOI
Thiel, G. , Rubil, S. , Lesch, A. , Guethlein, L.A. & Rössler, O.G. (2017) Transient receptor potential TRPM3 channels: Pharmacology, signaling, and biological functions. Pharmacological Research, 124, 92–99. 10.1016/j.phrs.2017.07.014 PubMed DOI
Throckmorton, G. , Cayce, J. , Ricks, Z. , Adams, W.R. , Jansen, E.D. & Mahadevan‐Jansen, A. (2021) Identifying optimal parameters for infrared neural stimulation in the peripheral nervous system. Neurophotonics, 8, 015012. 10.1117/1.NPh.8.1.015012 PubMed DOI PMC
Tolstykh, G.P. , Ibey, B.L. , Sedelnikova, A.V. , Valdez, C.M. , Cantu, J.C. & Echchgadda, I. Infrared laser‐induced fast thermal gradient affects the excitability of primary hippocampal neurons. In: Optical interactions with tissue and cells XXXI, edited by Ibey, B.L. & Linz, N. . SPIE conference abstract book, p. 34.
Tominaga, M. , Caterina, M.J. , Malmberg, A.B. , Rosen, T.A. , Gilbert, H. , Skinner, K. et al. (1998) The cloned capsaicin receptor integrates multiple pain‐producing stimuli. Neuron, 21, 531–543. 10.1016/S0896-6273(00)80564-4 PubMed DOI
Toro, C.A. , Arias, L.A. & Brauchi, S. (2011) Sub‐cellular distribution and translocation of TRP channels. Current Pharmaceutical Biotechnology, 12, 12–23. 10.2174/138920111793937899 PubMed DOI
Trancikova, A. , Kovacova, E. , Ru, F. , Varga, K. , Brozmanova, M. , Tatar, M. et al. (2018) Distinct expression of phenotypic markers in placodes‐ and neural crest‐derived afferent neurons innervating the rat stomach. Digestive Diseases and Sciences, 63, 383–394. 10.1007/s10620-017-4883-5 PubMed DOI
Tsuzuki, K. , Xing, H. , Ling, J. & Gu, J.G. (2004) Menthol‐induced Ca2+ release from presynaptic Ca2+ stores potentiates sensory synaptic transmission. Journal of Neuroscience, 24, 762–771. 10.1523/JNEUROSCI.4658-03.2004 PubMed DOI PMC
Venkatachalam, K. & Montell, C. (2007) TRP channels. Annual Review of Biochemistry, 76(1), 387–417. 10.1146/annurev.biochem.75.103004.142819 PubMed DOI PMC
Vriens, J. , Owsianik, G. , Hofmann, T. , Philipp, S.E. , Stab, J. , Chen, X. , Benoit, M. , Xue, F. , Janssens, A. , Kerselaers, S. , Oberwinkler, J. , Vennekens, R. , Gudermann, T. , Nilius, B. & Voets, T. TRPM3 Is a nociceptor channel involved in the detection of noxious heat. Neuron, 70(3), 482–494 PubMed
Wani, A. , Trevino, K. , Marnell, P. & Husain, M.M. (2013) Advances in brain stimulation for depression. Annals of Clinical Psychiatry, 25(3), 217–224. PubMed
Wells, J. , Kao, C. , Jansen, E.D. , Konrad, P. & Mahadevan‐Jansen, A. (2005) Application of infrared light for in vivo neural stimulation. Journal of Biomedical Optics, 10, 064003.10.1117/1.2121772 PubMed DOI
Wolfrum, C. , Kiehlmann, E. & Pelczar, P. (2018) TRPC1 regulates brown adipose tissue activity in a PPARγ‐dependent manner. American Journal of Physiology‐Endocrinology and Metabolism, 315, E825–E832. 10.1152/ajpendo.00170.2017 PubMed DOI
Xie, M.‐X. , Cao, X.‐Y. , Zeng, W.‐A. , Lai, R.‐C. , Guo, L. , Wang, J.‐C. et al. (2021) ATF4 selectively regulates heat nociception and contributes to kinesin‐mediated TRPM3 trafficking. Nature Communications, 12(1), 1401. 10.1038/s41467-021-21,731-1 PubMed DOI PMC
Yajima, T. , Sato, T. , Shimazaki, K. & Ichikawa, H. (2019) Transient receptor potential melastatin‐3 in the rat sensory ganglia of the trigeminal, glossopharyngeal and vagus nerves. Journal of Chemical Neuroanatomy, 96, 116–125. 10.1016/j.jchemneu.2019.01.005 PubMed DOI
Yao, X. & Garland, C.J. (2005) Recent developments in vascular endothelial cell transient receptor potential channels. Circulation Research, 97, 853–863. 10.1161/01.RES.0000187473.85419.3e PubMed DOI
Yao, J. , Liu, B. & Qin, F. Rapid temperature jump by infrared diode laser irradiation for patch‐clamp studies. Biophysical Journal, 96(9), P3611–3619. PubMed PMC
Zhang, L. , Jones, S. , Brody, K. , Costa, M. & Brookes, S.J.H. (2004) Thermosensitive transient receptor potential channels in vagal afferent neurons of the mouse. American Journal of Physiology. Gastrointestinal and Liver Physiology, 286, G983–G991. 10.1152/ajpgi.00441.2003 PubMed DOI
Zhuo, H. (1997) Neurochemistry of the nodose ganglion. Progress in Neurobiology, 52, 79–107. 10.1016/S0301-0082(97)00003-8 PubMed DOI