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Licensed Unlicensed Requires Authentication Published by De Gruyter March 23, 2019

Transient receptor potential channels in the context of nociception and pain – recent insights into TRPM3 properties and function

Marc Behrendt EMAIL logo
From the journal Biological Chemistry

Abstract

Potential harmful stimuli like heat, mechanical pressure or chemicals are detected by specialized cutaneous nerve fiber endings of nociceptor neurons in a process called nociception. Acute stimulation results in immediate protective reflexes and pain sensation as a normal, physiological behavior. However, ongoing (chronic) pain is a severe pathophysiological condition with diverse pathogeneses that is clinically challenging because of limited therapeutic options. Therefore, an urgent need exists for new potent and specific analgesics without afflicting adverse effects. Recently, TRPM3, a member of the superfamily of transient receptor potential (TRP) ion channels, has been shown to be expressed in nociceptors and to be involved in the detection of noxious heat (acute pain) as well as inflammatory hyperalgesia (acute and chronic pain). Current results in TRPM3 research indicate that this ion channel might not only be part of yet unraveled mechanisms underlying chronic pain but also has the potential to become a clinically relevant pharmacological target of future analgesic strategies. The aim of this review is to summarize and present the basic features of TRPM3 proteins and channels, to highlight recent findings and developments and to provide an outlook on emerging directions of TRPM3 research in the field of chronic pain.

Acknowledgments

The author would like to thank PD Dr. Richard Carr for critically reading the manuscript.

  1. Conflict of interest statement: The author declares no competing interests.

References

Aoki, R., Yokoyama, U., Ichikawa, Y., Taguri, M., Kumagaya, S., Ishiwata, R., Yanai, C., Fujita, S., Umemura, M., Fujita, T., et al. (2014). Decreased serum osmolality promotes ductus arteriosus constriction. Cardiovasc Res. 104, 326–336.10.1093/cvr/cvu199Search in Google Scholar PubMed

Autzen, H.E., Myasnikov, A.G., Campbell, M.G., Asarnow, D., Julius, D., and Cheng, Y. (2018). Structure of the human TRPM4 ion channel in a lipid nanodisc. Science 359, 228–232.10.1126/science.aar4510Search in Google Scholar PubMed PubMed Central

Badheka, D., Borbiro, I., and Rohacs, T. (2015). Transient receptor potential melastatin 3 is a phosphoinositide-dependent ion channel. J Gen Physiol. 146, 65–77.10.1085/jgp.201411336Search in Google Scholar PubMed PubMed Central

Badheka, D., Yudin, Y., Borbiro, I., Hartle, C.M., Yazici, A., Mirshahi, T., and Rohacs, T. (2017). Inhibition of transient receptor potential melastatin 3 ion channels by G-protein βγ subunits. eLife 6, e26147.10.7554/eLife.26147Search in Google Scholar PubMed PubMed Central

Behrendt, M., Mohr, F., Dembla, S., and Oberwinkler, J. (2014). Differential regulation of TRPM3 splice variants. Acta Physiol. 210(S695), 51.Search in Google Scholar

Behrendt, M., Dembla, S., Schneider, F.M., Bold, C., Goecke, C., and Oberwinkler, J. (2015).Characterization of a new TRPM3 agonist. Acta Physiol. 213(S699), 142–143.Search in Google Scholar

Bennett, T.M., Mackay, D.S., Siegfried, C.J., and Shiels, A. (2014). Mutation of the melastatin-related cation channel, TRPM3, underlies inherited cataract and glaucoma. PLoS One 9, e104000.10.1371/journal.pone.0104000Search in Google Scholar PubMed PubMed Central

Bevan, S., Quallo, T., and Andersson, D.A. (2014). TRPV1. Handb. Exp. Pharmacol. 222, 207–245.10.1007/978-3-642-54215-2_9Search in Google Scholar PubMed

Camacho Londono, J. and Philipp, S.E. (2016). A reliable method for quantification of splice variants using RT-qPCR. BMC Mol. Biol. 17, 8.10.1186/s12867-016-0060-1Search in Google Scholar PubMed PubMed Central

Cao, E., Liao, M., Cheng, Y., and Julius, D. (2013). TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504, 113–118.10.1038/nature12823Search in Google Scholar PubMed PubMed Central

Caterina, M.J., Schumacher, M.A., Tominaga, M., Rosen, T.A., Levine, J.D., and Julius, D. (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816–824.10.1038/39807Search in Google Scholar PubMed

Chen, L., Chen, W., Qian, X., Fang, Y., and Zhu, N. (2014). Liquiritigenin alleviates mechanical and cold hyperalgesia in a rat neuropathic pain model. Sci. Rep. 4, 5676.10.1038/srep05676Search in Google Scholar PubMed PubMed Central

Dembla, S., Behrendt, M., Goecke, C., and Oberwinkler, J. (2017a). Functional properties of TRPM3 channels in satellite glia cells of mouse dorsal root ganglia. Acta Physiol. 219(S711), 34.Search in Google Scholar

Dembla, S., Behrendt, M., Mohr, F., Goecke, C., Sondermann, J., Schneider, F.M., Schmidt, M., Stab, J., Enzeroth, R., Leitner, M.G., et al. (2017b). Anti-nociceptive action of peripheral mu-opioid receptors by G-βγ protein-mediated inhibition of TRPM3 channels. eLife 6, e26280.10.7554/eLife.26280Search in Google Scholar PubMed PubMed Central

Drews, A., Loch, S., Mohr, F., Rizun, O., Lambert, S., and Oberwinkler, J. (2010). The fractional calcium current through fast ligand-gated TRPM channels. Acta Physiol. 198(S677),P-TUE-115.Search in Google Scholar

Drews, A., Mohr, F., Rizun, O., Wagner, T.F., Dembla, S., Rudolph, S., Lambert, S., Konrad, M., Philipp, S.E., Behrendt, M., et al. (2014). Structural requirements of steroidal agonists of transient receptor potential melastatin 3 (TRPM3) cation channels. Br. J. Pharmacol. 171, 1019–1032.10.1111/bph.12521Search in Google Scholar PubMed PubMed Central

Duan, J., Li, Z., Li, J., Hulse, R.E., Santa-Cruz, A., Valinsky, W.C., Abiria, S.A., Krapivinsky, G., Zhang, J., and Clapham, D.E. (2018a). Structure of the mammalian TRPM7, a magnesium channel required during embryonic development. Proc. Natl. Acad. Sci. USA 115, E8201–E8210.10.1073/pnas.1810719115Search in Google Scholar PubMed PubMed Central

Duan, J., Li, Z., Li, J., Santa-Cruz, A., Sanchez-Martinez, S., Zhang, J., and Clapham, D.E. (2018b). Structure of full-length human TRPM4. Proc. Natl. Acad. Sci. USA 115, 2377–2382.10.1073/pnas.1722038115Search in Google Scholar PubMed PubMed Central

Fajardo, O., Meseguer, V., Belmonte, C., and Viana, F. (2008). TRPA1 channels: novel targets of 1,4-dihydropyridines. Channels (Austin) 2, 429–438.10.4161/chan.2.6.7126Search in Google Scholar PubMed

Fecher-Trost, C., Wissenbach, U., Beck, A., Schalkowsky, P.,Stoerger, C., Doerr, J., Dembek, A., Simon-Thomas, M., Weber, A., Wollenberg, P., et al. (2013). The in vivo TRPV6 protein starts at a non-AUG triplet, decoded as methionine, upstream of canonical initiation at AUG. J. Biol. Chem. 288, 16629–16644.10.1074/jbc.M113.469726Search in Google Scholar PubMed PubMed Central

Flockerzi, V. and Nilius, B. (2014). TRPs: truly remarkable proteins. Handb. Exp. Pharmacol. 222, 1–12.10.1007/978-3-642-54215-2_1Search in Google Scholar PubMed

Frühwald, J., Camacho Londono, J., Dembla, S., Mannebach, S., Lis, A., Drews, A., Wissenbach, U., Oberwinkler, J., and Philipp, S.E. (2012). Alternative splicing of a protein domain indispensable for function of transient receptor potential melastatin 3 (TRPM3) ion channels. J. Biol. Chem. 287, 36663–36672.10.1074/jbc.M112.396663Search in Google Scholar PubMed PubMed Central

Ghosh, D., Pinto, S., Danglot, L., Vandewauw, I., Segal, A., Van Ranst, N., Benoit, M., Janssens, A., Vennekens, R., Vanden Berghe, P., et al. (2016). VAMP7 regulates constitutive membrane incorporation of the cold-activated channel TRPM8. Nat. Commun. 7, 10489.10.1038/ncomms10489Search in Google Scholar PubMed PubMed Central

Gonzalez-Ramirez, R., Chen, Y., Liedtke, W.B., and Morales-Lazaro, S.L. (2017). TRP channels and pain. In: Neurobiology of TRP Channels. 2nd edition, T.L.R. Emir, ed. (Boca Raton, FL: CRC Press/Taylor & Francis); Chapter 8, pp. 125–147.10.4324/9781315152837-8Search in Google Scholar PubMed

Grimm, C., Kraft, R., Sauerbruch, S., Schultz, G., and Harteneck, C. (2003). Molecular and functional characterization of the melastatin-related cation channel TRPM3. J. Biol. Chem. 278, 21493–21501.10.1074/jbc.M300945200Search in Google Scholar PubMed

Grimm, C., Kraft, R., Schultz, G., and Harteneck, C. (2005). Activation of the melastatin-related cation channel TRPM3 by D-erythro-sphingosine [corrected]. Mol. Pharmacol. 67, 798–805.10.1124/mol.104.006734Search in Google Scholar PubMed

Guo, J., She, J., Zeng, W., Chen, Q., Bai, X.C., and Jiang, Y. (2017). Structures of the calcium-activated, non-selective cation channel TRPM4. Nature 552, 205–209.10.1038/nature24997Search in Google Scholar PubMed PubMed Central

Harteneck, C. (2013). Pregnenolone sulfate: from steroid metabolite to TRP channel ligand. Molecules 18, 12012–12028.10.3390/molecules181012012Search in Google Scholar PubMed PubMed Central

Harteneck, C. and Gollasch, M. (2011). Pharmacological modulation of diacylglycerol-sensitive TRPC3/6/7 channels. Curr. Pharm. Biotechnol. 12, 35–41.10.2174/138920111793937943Search in Google Scholar PubMed PubMed Central

Held, K., Kichko, T., De Clercq, K., Klaassen, H., Van Bree, R., Vanherck, J.C., Marchand, A., Reeh, P.W., Chaltin, P., Voets, T., et al. (2015a). Activation of TRPM3 by a potent synthetic ligand reveals a role in peptide release. Proc. Natl. Acad. Sci. USA 112, E1363–E1372.10.1073/pnas.1419845112Search in Google Scholar PubMed PubMed Central

Held, K., Voets, T., and Vriens, J. (2015b). TRPM3 in temperature sensing and beyond. Temperature (Austin) 2, 201–213.10.4161/23328940.2014.988524Search in Google Scholar PubMed PubMed Central

Held, K., Gruss, F., Aloi, V.D., Janssens, A., Ulens, C., Voets, T., and Vriens, J. (2018). Mutations in the voltage-sensing domain affect the alternative ion permeation pathway in the TRPM3 channel. J. Physiol. 596, 2413–2432.10.1113/JP274124Search in Google Scholar PubMed PubMed Central

Hoffmann, A., Grimm, C., Kraft, R., Goldbaum, O., Wrede, A., Nolte, C., Hanisch, U.K., Richter-Landsberg, C., Bruck, W., Kettenmann, H., et al. (2010). TRPM3 is expressed in sphingosine-responsive myelinating oligodendrocytes. J. Neurochem. 114, 654–665.10.1111/j.1471-4159.2010.06644.xSearch in Google Scholar PubMed

Holakovska, B., Grycova, L., Jirku, M., Sulc, M., Bumba, L., andTeisinger, J. (2012). Calmodulin and S100A1 protein interact with N terminus of TRPM3 channel. J. Biol. Chem. 287, 16645–16655.10.1074/jbc.M112.350686Search in Google Scholar PubMed PubMed Central

Holendova, B., Grycova, L., Jirku, M., and Teisinger, J. (2012). PtdIns(4,5)P2 interacts with CaM binding domains on TRPM3 N-terminus. Channels (Austin) 6, 479–482.10.4161/chan.22177Search in Google Scholar PubMed PubMed Central

Hsu, H.T., Tseng, Y.T., Lo, Y.C., and Wu, S.N. (2014). Ability of naringenin, a bioflavonoid, to activate M-type potassium current in motor neuron-like cells and to increase BKCa-channel activity in HEK293T cells transfected with α-hSlo subunit. BMC Neurosci. 15, 135.10.1186/s12868-014-0135-1Search in Google Scholar PubMed PubMed Central

Hu, H., Tian, J., Zhu, Y., Wang, C., Xiao, R., Herz, J.M., Wood, J.D., and Zhu, M.X. (2010). Activation of TRPA1 channels by fenamate nonsteroidal anti-inflammatory drugs. Pflüger’s Arch. 459, 579–592.10.1007/s00424-009-0749-9Search in Google Scholar PubMed PubMed Central

Huang, Y., Winkler, P.A., Sun, W., Lu, W., and Du, J. (2018). Architecture of the TRPM2 channel and its activation mechanism by ADP-ribose and calcium. Nature 562, 145–149.10.1038/s41586-018-0558-4Search in Google Scholar PubMed

Hughes, S., Pothecary, C.A., Jagannath, A., Foster, R.G., Hankins, M.W., and Peirson, S.N. (2012). Profound defects in pupillary responses to light in TRPM-channel null mice: a role for TRPM channels in non-image-forming photoreception. Eur. J. Neurosci. 35, 34–43.10.1111/j.1460-9568.2011.07944.xSearch in Google Scholar PubMed PubMed Central

Jia, S., Zhang, Y., and Yu, J. (2017). Antinociceptive effects of isosakuranetin in a rat model of peripheral neuropathy. Pharmacology 100, 201–207.10.1159/000478986Search in Google Scholar PubMed

Julius, D. (2013). TRP channels and pain. Annu. Rev. Cell Dev. Biol. 29, 355–384.10.1146/annurev-cellbio-101011-155833Search in Google Scholar PubMed

Kim, J., Williams, F.J., Dreger, D.L., Plassais, J., Davis, B.W., Parker, H.G., and Ostrander, E.A. (2018). Genetic selection of athletic success in sport-hunting dogs. Proc. Natl. Acad. Sci. USA 115, E7212–E7221.10.1073/pnas.1800455115Search in Google Scholar PubMed PubMed Central

Klose, C., Straub, I., Riehle, M., Ranta, F., Krautwurst, D., Ullrich, S., Meyerhof, W., and Harteneck, C. (2011). Fenamates as TRP channel blockers: mefenamic acid selectively blocks TRPM3. Br J Pharmacol. 162, 1757–1769.10.1111/j.1476-5381.2010.01186.xSearch in Google Scholar PubMed PubMed Central

Krügel, U., Straub, I., Beckmann, H., and Schaefer, M. (2017). Primidone inhibits TRPM3 and attenuates thermal nociception in vivo. Pain 158, 856–867.10.1097/j.pain.0000000000000846Search in Google Scholar PubMed PubMed Central

Kuner, R. and Flor, H. (2016). Structural plasticity and reorganisation in chronic pain. Nat. Rev. Neurosci. 18, 20–30.10.1038/nrn.2016.162Search in Google Scholar PubMed

Lambert, S., Drews, A., Rizun, O., Wagner, T.F., Lis, A., Mannebach, S., Plant, S., Portz, M., Meissner, M., Philipp, S.E., et al. (2011). Transient receptor potential melastatin 1 (TRPM1) is an ion-conducting plasma membrane channel inhibited by zinc ions. J. Biol. Chem. 286, 12221–12233.10.1074/jbc.M110.202945Search in Google Scholar PubMed PubMed Central

Lee, N., Chen, J., Sun, L., Wu, S., Gray, K.R., Rich, A., Huang, M., Lin, J.H., Feder, J.N., Janovitz, E.B., et al. (2003). Expression and characterization of human transient receptor potential melastatin 3 (hTRPM3). J. Biol. Chem. 278, 20890–20897.10.1074/jbc.M211232200Search in Google Scholar PubMed

Leitner, M.G., Michel, N., Behrendt, M., Dierich, M., Dembla, S., Wilke, B.U., Konrad, M., Lindner, M., Oberwinkler, J., and Oliver, D. (2016). Direct modulation of TRPM4 and TRPM3 channels by the phospholipase C inhibitor U73122. Br. J. Pharmacol. 173, 2555–2569.10.1111/bph.13538Search in Google Scholar PubMed PubMed Central

Liao, M., Cao, E., Julius, D., and Cheng, Y. (2013). Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504, 107–112.10.1038/nature12822Search in Google Scholar PubMed PubMed Central

Liman, E.R. (2014). TRP Channels: pain enters through the side door. Nat. Chem. Biol. 10, 171–172.10.1038/nchembio.1470Search in Google Scholar PubMed

Majeed, Y., Bahnasi, Y., Seymour, V.A., Wilson, L.A., Milligan, C.J., Agarwal, A.K., Sukumar, P., Naylor, J., and Beech, D.J. (2011). Rapid and contrasting effects of rosiglitazone on transient receptor potential TRPM3 and TRPC5 channels. Mol. Pharmacol. 79, 1023–1030.10.1124/mol.110.069922Search in Google Scholar PubMed PubMed Central

Majeed, Y., Tumova, S., Green, B.L., Seymour, V.A., Woods, D.M., Agarwal, A.K., Naylor, J., Jiang, S., Picton, H.M., Porter, K.E., et al. (2012). Pregnenolone sulphate-independent inhibition of TRPM3 channels by progesterone. Cell Calcium 51, 1–11.10.1016/j.ceca.2011.09.005Search in Google Scholar PubMed PubMed Central

Meng, L.M., Ma, H.J., Guo, H., Kong, Q.Q., and Zhang, Y. (2016). The cardioprotective effect of naringenin against ischemia-reperfusion injury through activation of ATP-sensitive potassium channel in rat. Can. J. Physiol. Pharmacol. 94, 973–978.10.1139/cjpp-2016-0008Search in Google Scholar PubMed

Mersereau, J.E., Levy, N., Staub, R.E., Baggett, S., Zogovic, T., Chow, S., Ricke, W.A., Tagliaferri, M., Cohen, I., Bjeldanes, L.F., et al. (2008). Liquiritigenin is a plant-derived highly selective estrogen receptor beta agonist. Mol. Cell Endocrinol. 283, 49–57.10.1016/j.mce.2007.11.020Search in Google Scholar PubMed PubMed Central

Moran, M.M. and Szallasi, A. (2018). Targeting nociceptive transient receptor potential channels to treat chronic pain: current state of the field. Br. J. Pharmacol. 175, 2185–2203.10.1111/bph.14044Search in Google Scholar PubMed PubMed Central

Naylor, J., Li, J., Milligan, C.J., Zeng, F., Sukumar, P., Hou, B., Sedo, A., Yuldasheva, N., Majeed, Y., Beri, D., et al. (2010). Pregnenolone sulphate- and cholesterol-regulated TRPM3 channels coupled to vascular smooth muscle secretion and contraction. Circ. Res. 106, 1507–1515.10.1161/CIRCRESAHA.110.219329Search in Google Scholar PubMed PubMed Central

Oberwinkler, J. and Philipp, S.E. (2014). Trpm3. Handb. Exp. Pharmacol. 222, 427–459.10.1007/978-3-642-54215-2_17Search in Google Scholar PubMed

Oberwinkler, J., Lis, A., Giehl, K.M., Flockerzi, V., and Philipp, S.E. (2005). Alternative splicing switches the divalent cation selectivity of TRPM3 channels. J. Biol. Chem. 280, 22540–22548.10.1074/jbc.M503092200Search in Google Scholar PubMed

Obreja, O. and Schmelz, M. (2010). Single-fiber recordings of unmyelinated afferents in pig. Neurosci. Lett. 470, 175–179.10.1016/j.neulet.2009.10.006Search in Google Scholar PubMed

Pafumi, I., Festa, M., Papacci, F., Lagostena, L., Giunta, C., Gutla, V., Cornara, L., Favia, A., Palombi, F., Gambale, F., et al. (2017). Naringenin impairs two-pore channel 2 activity and inhibits VEGF-induced angiogenesis. Sci. Rep. 7, 5121.10.1038/s41598-017-04974-1Search in Google Scholar PubMed PubMed Central

Paoletta, S., Steventon, G.B., Wildeboer, D., Ehrman, T.M., Hylands, P.J., and Barlow, D.J. (2008). Screening of herbal constituents for aromatase inhibitory activity. Bioorg. Med. Chem. 16, 8466–8470.10.1016/j.bmc.2008.08.034Search in Google Scholar PubMed

Patapoutian, A., Peier, A.M., Story, G.M., and Viswanath, V. (2003). ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat. Rev. Neurosci. 4, 529–539.10.1038/nrn1141Search in Google Scholar PubMed

Paulsen, C.E., Armache, J.P., Gao, Y., Cheng, Y., and Julius, D. (2015). Structure of the TRPA1 ion channel suggests regulatory mechanisms. Nature 520, 511–517.10.1038/nature14367Search in Google Scholar PubMed PubMed Central

Przibilla, J., Dembla, S., Rizun, O., Lis, A., Jung, M., Oberwinkler, J., Beck, A., and Philipp, S.E. (2018). Ca2+-dependent regulation and binding of calmodulin to multiple sites of Transient Receptor Potential Melastatin 3 (TRPM3) ion channels. Cell Calcium 73, 40–52.10.1016/j.ceca.2018.03.005Search in Google Scholar PubMed

Quallo, T., Alkhatib, O., Gentry, C., Andersson, D.A., and Bevan, S. (2017). G protein betagamma subunits inhibit TRPM3 ion channels in sensory neurons. eLife 6, e26138.10.7554/eLife.26138Search in Google Scholar PubMed PubMed Central

Rostock, C., Schrenk-Siemens, K., Pohle, J., and Siemens, J. (2018). Human vs. mouse nociceptors – similarities and differences. Neuroscience 387, 13–27.10.1016/j.neuroscience.2017.11.047Search in Google Scholar PubMed PubMed Central

Schneider, F.M., Mohr, F., Behrendt, M., and Oberwinkler, J. (2015). Properties and functions of TRPM1 channels in the dendritic tips of retinal ON-bipolar cells. Eur. J. Cell Biol. 94, 420–427.10.1016/j.ejcb.2015.06.005Search in Google Scholar PubMed

Shi, R., Xiao, Z.T., Zheng, Y.J., Zhang, Y.L., Xu, J.W., Huang, J.H., Zhou, W.L., Li, P.B., and Su, W.W. (2017). Naringenin regulates CFTR activation and expression in airway epithelial cells. Cell Physiol. Biochem. 44, 1146–1160.10.1159/000485419Search in Google Scholar PubMed

Son, G.Y., Yang, Y.M., Park, W.S., Chang, I., and Shin, D.M. (2015). Hypotonic stress induces RANKL via transient receptor potential melastatin 3 (TRPM3) and vaniloid 4 (TRPV4) in human PDL cells. J. Dent. Res. 94, 473–481.10.1177/0022034514567196Search in Google Scholar PubMed PubMed Central

Son, A., Kang, N., Kim, K.W., Yang, Y.M., and Shin, D.M. (2018). TRPM3/TRPV4 regulates Ca2+-mediated RANKL/NFATc1 expression in osteoblasts. J. Mol. Endocrinol. 61, 207–218.10.1530/JME-18-0051Search in Google Scholar PubMed

Staaf, S., Franck, M.C., Marmigere, F., Mattsson, J.P., and Ernfors, P. (2010). Dynamic expression of the TRPM subgroup of ion channels in developing mouse sensory neurons. Gene Expr, Patterns 10, 65–74.10.1016/j.gep.2009.10.003Search in Google Scholar PubMed

Straub, I., Mohr, F., Stab, J., Konrad, M., Philipp, S.E., Oberwinkler, J., and Schaefer, M. (2013a). Citrus fruit and fabacea secondary metabolites potently and selectively block TRPM3. Br. J. Pharmacol. 168, 1835–1850.10.1111/bph.12076Search in Google Scholar PubMed PubMed Central

Straub, I., Krügel, U., Mohr, F., Teichert, J., Rizun, O., Konrad, M., Oberwinkler, J., and Schaefer, M. (2013b). Flavanones that selectively inhibit TRPM3 attenuate thermal nociception in vivo. Mol. Pharmacol. 84, 736–750.10.1124/mol.113.086843Search in Google Scholar PubMed

Suzuki, H., Sasaki, E., Nakagawa, A., Muraki, Y., Hatano, N., and Muraki, K. (2016). Diclofenac, a nonsteroidal anti-inflammatory drug, is an antagonist of human TRPM3 isoforms. Pharmacol. Res. Perspect. 4, e00232.10.1002/prp2.232Search in Google Scholar PubMed PubMed Central

Tan, C.H. and McNaughton, P.A. (2016). The TRPM2 ion channel is required for sensitivity to warmth. Nature 536, 460–463.10.1038/nature19074Search in Google Scholar PubMed PubMed Central

Testai, L., Da Pozzo, E., Piano, I., Pistelli, L., Gargini, C., Breschi, M.C., Braca, A., Martini, C., Martelli, A., and Calderone, V. (2017). The citrus flavanone naringenin produces cardioprotective effects in hearts from 1 year old rat, through activation of mitoBK channels. Front Pharmacol. 8, 71.10.3389/fphar.2017.00071Search in Google Scholar PubMed PubMed Central

Toth, B.I., Konrad, M., Ghosh, D., Mohr, F., Halaszovich, C.R., Leitner, M.G., Vriens, J., Oberwinkler, J., and Voets, T. (2015). Regulation of the transient receptor potential channel TRPM3 by phosphoinositides. J. Gen. Physiol. 146, 51–63.10.1085/jgp.201411339Search in Google Scholar PubMed PubMed Central

Uchida, K., Demirkhanyan, L., Asuthkar, S., Cohen, A., Tominaga, M., and Zakharian, E. (2016). Stimulation-dependent gating of TRPM3 channel in planar lipid bilayers. FASEB J. 30, 1306–1316.10.1096/fj.15-281576Search in Google Scholar PubMed PubMed Central

Vandewauw, I., De Clercq, K., Mulier, M., Held, K., Pinto, S., Van Ranst, N., Segal, A., Voet, T., Vennekens, R., Zimmermann, K., et al. (2018). A TRP channel trio mediates acute noxious heat sensing. Nature 555, 662–666.10.1038/nature26137Search in Google Scholar PubMed

Vriens, J. and Voets, T. (2018). Sensing the heat with TRPM3. Pflüger’s Arch. 470, 799–807.10.1007/s00424-017-2100-1Search in Google Scholar PubMed PubMed Central

Vriens, J., Owsianik, G., Hofmann, T., Philipp, S.E., Stab, J., Chen, X., Benoit, M., Xue, F., Janssens, A., Kerselaers, S., et al. (2011). TRPM3 is a nociceptor channel involved in the detection of noxious heat. Neuron 70, 482–494.10.1016/j.neuron.2011.02.051Search in Google Scholar PubMed

Vriens, J., Held, K., Janssens, A., Toth, B.I., Kerselaers, S., Nilius, B., Vennekens, R., and Voets, T. (2014). Opening of an alternative ion permeation pathway in a nociceptor TRP channel. Nat. Chem. Biol. 10, 188–195.10.1038/nchembio.1428Search in Google Scholar PubMed

Wagner, T.F., Loch, S., Lambert, S., Straub, I., Mannebach, S., Mathar, I., Dufer, M., Lis, A., Flockerzi, V., Philipp, S.E., et al. (2008). Transient receptor potential M3 channels are ionotropic steroid receptors in pancreatic beta cells. Nat. Cell Biol. 10, 1421–1430.10.1038/ncb1801Search in Google Scholar PubMed

Wagner, T.F., Drews, A., Loch, S., Mohr, F., Philipp, S.E., Lambert, S., and Oberwinkler, J. (2010). TRPM3 channels provide a regulated influx pathway for zinc in pancreatic β cells. Pflüger’s Arch. 460, 755–765.10.1007/s00424-010-0838-9Search in Google Scholar PubMed

Yin, Y., Wu, M., Zubcevic, L., Borschel, W.F., Lander, G.C., and Lee, S.Y. (2018). Structure of the cold- and menthol-sensing ion channel TRPM8. Science 359, 237–241.10.1126/science.aan4325Search in Google Scholar PubMed PubMed Central

Zhang, Z., Toth, B., Szollosi, A., Chen, J., and Csanady, L. (2018). Structure of a TRPM2 channel in complex with Ca2+ explains unique gating regulation. eLife 7, e36409.10.7554/eLife.36409Search in Google Scholar PubMed PubMed Central

Zhao, P.Y., Gan, G., Peng, S., Wang, S.B., Chen, B., Adelman, R.A., and Rizzolo, L.J. (2015). TRP channels localize to subdomains of the apical plasma membrane in human Fetal retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 56, 1916–1923.10.1167/iovs.14-15738Search in Google Scholar PubMed PubMed Central

Received: 2018-12-07
Accepted: 2019-02-25
Published Online: 2019-03-23
Published in Print: 2019-06-26

©2019 Walter de Gruyter GmbH, Berlin/Boston

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