Interaction of NHE1 and TRPA1 Activity in DRG Neurons Isolated from Adult Rats and its Role in Inflammatory Nociception

Neuroscience - Tập 465 - Trang 154-165 - 2021
Vladimir A. Martínez-Rojas1, Ana B. Salinas-Abarca2, Norma L. Gómez-Víquez1, Vinicio Granados-Soto2, Francisco Mercado3, Janet Murbartián1
1Departamento de Farmacobiología, Cinvestav, South Campus, Mexico City, Mexico
2Neurobiology of Pain Laboratory, Departamento de Farmacobiología, Cinvestav, South Campus, Mexico City, Mexico
3Dirección de Investigaciones en Neurociencias, Instituto Nacional de Psiquiatría Ramón de la Fuente Muñiz, Mexico City, Mexico

Tài liệu tham khảo

Akopian, 2007, Transient receptor potential TRPA1 channel desensitization in sensory neurons is agonist dependent and regulated by TRPV1-directed internalization, J Physiol, 583, 175, 10.1113/jphysiol.2007.133231 Almanza, 2019, Cellular mechanism for specific mechanical antinociception by D2-like receptor at the spinal cord level, Neuroscience, 417, 81, 10.1016/j.neuroscience.2019.08.019 Asgar, 2015, The role of TRPA1 in muscle pain and mechanical hypersensitivity under inflammatory conditions in rats, Neuroscience, 310, 206, 10.1016/j.neuroscience.2015.09.042 Barabas ME, Kossyreva EA, Stucky CL. TRPA1 is functionally expressed primarily by IB4-binding, non-peptidergic mouse and rat sensory neurons. PLoS One 2012;7:e47988. doi: 10.1371/journal.pone.0047988. Bayliss, 2015, The role of pH-sensitive TASK channels in central respiratory chemoreception, Pflugers Arch., 467, 917, 10.1007/s00424-014-1633-9 Bravo-Hernández M, Corleto JA, Barragán-Iglesias P, González-Ramírez R, Pineda-Farias JB, Felix R, Calcutt NA, Delgado-Lezama R, et al. The α5 subunit containing GABAA receptors contribute to chronic pain. Pain 2016;157:613–26. doi: 10.1097/j.pain.0000000000000410. Brisson, 2011, NaV1.5 enhances breast cancer cell invasiveness by increasing NHE1-dependent H+ efflux in caveolae, Oncogene, 30, 2070, 10.1038/onc.2010.574 Carpenter, 2006, Cell Profiler: image analysis software for identifying and quantifying cell phenotypes, Genome Biol, 7, R100, 10.1186/gb-2006-7-10-r100 Castañeda-Corral, 2012, Blockade of peripheral and spinal Na+/H+ exchanger increases formalin-induced long-lasting mechanical allodynia and hyperalgesia in rats, Brain Res, 1475, 19, 10.1016/j.brainres.2012.08.001 Castañeda-Corral, 2011, Role of the spinal Na+/H+ exchanger in formalin-induced nociception, Neurosci Lett, 501, 4, 10.1016/j.neulet.2011.06.048 Chaplan, 1994, Quantitative assessment of tactile allodynia in the rat paw, J Neurosci Meth, 53, 55, 10.1016/0165-0270(94)90144-9 Chen J, Joshi SK, DiDomenico S, Perner RJ, Mikusa JP, Gauvin DM, Segreti JA, Han P, et al. Selective blockade of TRPA1 channel attenuates pathological pain without altering noxious cold sensation or body temperature regulation. Pain 2011;152:1165–72. doi: 10.1016/j.pain.2011.01.049. Cheng, 2019, The Na+/H+ -exchanger NHE1 regulates extra- and intracellular pH and nimodipine-sensitive [Ca2+]i in the suprachiasmatic nucleus, Sci Rep, 9, 6430, 10.1038/s41598-019-42872-w Cox, 1997, Sodium/hydrogen exchanger gene defect in slow-wave epilepsy mutant mice, Cell, 91, 139, 10.1016/S0092-8674(01)80016-7 da Costa, 2010, The involvement of the transient receptor potential A1 (TRPA1) in the maintenance of mechanical and cold hyperalgesia in persistent inflammation, Pain, 148, 431, 10.1016/j.pain.2009.12.002 de Curtis, 1998, Activity-dependent pH shifts and periodic recurrence of spontaneous interictal spikes in a model of focal epileptogenesis, J Neurosci, 18, 7543, 10.1523/JNEUROSCI.18-18-07543.1998 Dunn, 2011, A practical guide to evaluating colocalization in biological microscopy, Am J Physiol Cell Physiol, 300, C723, 10.1152/ajpcell.00462.2010 Fuchs, 2007, Contribution of calcium channel subtypes to the intracellular calcium signal in sensory neurons: the effect of injury, Anesthesiology, 107, 117, 10.1097/01.anes.0000267511.21864.93 Fujita, 2008, Intracellular alkalization causes pain sensation through activation of TRPA1 in mice, J Clin Invest, 118, 4049, 10.1172/JCI35957 Gómez-Viquez, 2003, SERCA pump optimizes Ca2+ release by a mechanism independent of store filling in smooth muscle cells, Biophys J, 85, 370, 10.1016/S0006-3495(03)74481-6 Govea, 2016, Group III mGluR8 negatively modulates TRPA1, Neuroscience, 334, 134, 10.1016/j.neuroscience.2016.07.047 Guzman-Perez, 2001, Discovery of zoniporide: a potent and selective sodium-hydrogen exchanger type 1 (NHE-1) inhibitor with high aqueous solubility, Bioorganic Med Chem Lett, 11, 803, 10.1016/S0960-894X(01)00059-2 Hellwig, 2004, TRPV1 acts as proton channel to induce acidification in nociceptive neurons, J Biol Chem, 279, 34553, 10.1074/jbc.M402966200 Hwang, 2011, Intracellular acidification is associated with changes in free cytosolic calcium and inhibition of action potentials in rat trigeminal ganglion, J Biol Chem, 286, 1719, 10.1074/jbc.M109.090951 Iorio, 2020, KV11.1 potassium channel and the Na+/H+ antiporter NHE1 modulate adhesion-dependent intracellular pH in colorectal cancer cells, Front Pharmacol, 11, 848, 10.3389/fphar.2020.00848 James-Kracke, 1992, Quick and accurate method to convert BCECF fluorescence to pHi: Calibration in three different types of cell preparations, J Cell Physiol, 151, 596, 10.1002/jcp.1041510320 Ji, 2008, Intact Aδ-fibers up-regulate transient receptor potential A1 and contribute to cold hypersensitivity in neuropathic rats, Neuroscience, 154, 1054, 10.1016/j.neuroscience.2008.04.039 Kang, 2006, TREK-2 (K2P10.1) and TRESK (K2P18.1) are major background K+ channels in dorsal root ganglion neurons, Am J Physiol Cell Physiol, 291, C138, 10.1152/ajpcell.00629.2005 Khan, 2003, Role of Na+/H+ exchanger isoform-1 in human inflammatory bowel disease, Can J Gastroenterol, 17, 31, 10.1155/2003/673819 Kiss, 1999, Modulation of N-type Ca2+ channels by intracellular pH in chick sensory neurons, J Neurophysiol, 81, 1839, 10.1152/jn.1999.81.4.1839 Kistner, 2016, Systemic desensitization through TRPA1 channels by capsazepine and mustard oil-a novel strategy against inflammation and pain, Sci Rep, 6, 10.1038/srep28621 Liu, 2008, Na+/H+ exchanger-1 inhibitors reduce neuronal excitability and alter Na+ channel inactivation properties in rat primary sensory neurons, Toxicol Sci, 103, 346, 10.1093/toxsci/kfn045 Martínez-Rojas, 2018, Peripheral and spinal TRPA1 channels contribute to formalin-induced long-lasting mechanical hypersensitivity, J Pain Res, 11, 51, 10.2147/JPR.S153671 Nagata, 2005, Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing, J Neurosci, 25, 4052, 10.1523/JNEUROSCI.0013-05.2005 Odem, 2018, Isolated nociceptors reveal multiple specializations for generating irregular ongoing activity associated with ongoing pain, Pain, 159, 2347, 10.1097/j.pain.0000000000001341 Orlowski, 2004, Diversity of the mammalian sodium/proton exchanger SLC9 gene family, Pflügers Arch, 447, 549, 10.1007/s00424-003-1110-3 Orlowski, 1992, Molecular cloning of putative members of the Na+/H+ exchanger gene family. cDNA cloning, deduced amino acid sequence, and mRNA tissue expression of the rat Na+/H+ exchanger NHE-1 and two structurally related proteins, J Biol Chem, 267, 9331, 10.1016/S0021-9258(19)50428-8 Pettersen, 2008, Neurotoxic effects of zoniporide: a selective inhibitor of the Na+/H+ exchanger isoform 1, Toxicol Pathol, 36, 608, 10.1177/0192623308318215 Riva, 2018, Oxaliplatin induces pH acidification in dorsal root ganglia neurons, Sci Rep, 8, 10.1038/s41598-018-33508-6 Rocha-González, 2009, Identification of the Na+/H+ exchanger 1 in dorsal root ganglion and spinal cord: Its possible role in inflammatory nociception, Neuroscience, 160, 156, 10.1016/j.neuroscience.2009.02.033 Schmidt, 2009, Nociceptive signals induce trafficking of TRPA1 to the plasma membrane, Neuron, 64, 498, 10.1016/j.neuron.2009.09.030 Steen, 1999, The pH response of rat cutaneous nociceptors correlates with extracellular [Na+] and is increased under amiloride, Eur J Neurosci, 11, 2783, 10.1046/j.1460-9568.1999.00695.x Story, 2003, ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures, Cell, 112, 819, 10.1016/S0092-8674(03)00158-2 Talavera, 2020, Mammalian transient receptor potential TRPA1 channels: from structure to disease, Physiol Rev, 100, 725, 10.1152/physrev.00005.2019 Takahashi, 2008, Molecular characterization of TRPA1 channel activation by cysteine-reactive inflammatory mediators, Channels, 2, 287, 10.4161/chan.2.4.6745 Thomas, 1979, Intracellular pH measurements in ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ, Biochemistry, 18, 2210, 10.1021/bi00578a012 Usoskin, 2015, Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing, Nat Neurosci, 18, 145, 10.1038/nn.3881 Viana, 2016, TRPA1 channels: molecular sentinels of cellular stress and tissue damage, J Physiol, 594, 4151, 10.1113/JP270935 Viatchenko-Karpinski, 2018, Characterization of temperature-sensitive leak K+ currents and expression of TRAAK, TREK-1, and TREK2 channels in dorsal root ganglion neurons of rats, Mol Brain, 11, 40, 10.1186/s13041-018-0384-5 Wang, 2011, A TRPA1-dependent mechanism for the pungent sensationof weak acids, J Gen Physiol, 137, 493, 10.1085/jgp.201110615 Wang, 2010, TRPA1 is a component of the nociceptive response to CO2, J Neurosci, 30, 12958, 10.1523/JNEUROSCI.2715-10.2010 Weng, 2015, Tmem100 is a regulator of TRPA1-TRPV1 complex and contributes to persistent pain, Neuron, 85, 833, 10.1016/j.neuron.2014.12.065 Zhang, 2016, Clustering and functional coupling of diverse ion channels and signaling proteins revealed by superresolution STORM microscopy in neurons, Neuron, 92, 461, 10.1016/j.neuron.2016.09.014 Zhang, 2014, Nitro-oleic acid desensitizes TRPA1 and TRPV1 agonist responses in adult rat DRG neurons, Exp Neurol, 251, 12, 10.1016/j.expneurol.2013.10.020 Zimmermann, 1983, Ethical guidelines for investigations on experimental pain in conscious animals, Pain, 16, 109, 10.1016/0304-3959(83)90201-4