Complementary roles of murine Na


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
11 02 2020
Historique:
received: 06 11 2019
accepted: 17 01 2020
entrez: 13 2 2020
pubmed: 13 2 2020
medline: 30 3 2021
Statut: epublish

Résumé

Acute pruritus occurs in various disorders. Despite severe repercussions on quality of life treatment options remain limited. Voltage-gated sodium channels (Na

Identifiants

pubmed: 32047194
doi: 10.1038/s41598-020-59092-2
pii: 10.1038/s41598-020-59092-2
pmc: PMC7012836
doi:

Substances chimiques

NAV1.7 Voltage-Gated Sodium Channel 0
NAV1.8 Voltage-Gated Sodium Channel 0
NAV1.9 Voltage-Gated Sodium Channel 0
Scn10a protein, mouse 0
Scn11a protein, mouse 0
Scn9a protein, mouse 0
Histamine 820484N8I3

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2326

Références

Weisshaar, E. et al. European guideline on chronic pruritus: In cooperation with the European dermatology forum (EDF) and the European academy of dermatology and venereology (EADV). Acta Derm. Venereol. 92, 563–581 (2012).
pubmed: 22790094 doi: 10.2340/00015555-1400 pmcid: 22790094
Simone, D. A. et al. The magnitude and duration of itch produced by intracutaneous injections of histamine. Somatosens. Res. 5, 81–92 (1987).
pubmed: 3423533 doi: 10.3109/07367228709144620 pmcid: 3423533
Rossbach, K. et al. Histamine H1, H3 and H4 receptors are involved in pruritus. Neuroscience 190, 89–102 (2011).
pubmed: 21689731 doi: 10.1016/j.neuroscience.2011.06.002 pmcid: 21689731
Sikand, P., Dong, X. & LaMotte, R. H. BAM8-22 Peptide Produces Itch and Nociceptive Sensations in Humans Independent of Histamine Release. J. Neurosci. 31, 7563–7567 (2011).
pubmed: 21593341 pmcid: 3111068 doi: 10.1523/JNEUROSCI.1192-11.2011
Liu, Q. et al. Sensory Neuron-Specific GPCR Mrgprs Are Itch Receptors Mediating Chloroquine-Induced Pruritus. Cell 139, 1353–1365 (2009).
pubmed: 20004959 pmcid: 2989405 doi: 10.1016/j.cell.2009.11.034
Liu, Q. et al. Mechanisms of itch evoked by β-alanine. J. Neurosci. 32, 14532–7 (2012).
pubmed: 23077038 pmcid: 3491570 doi: 10.1523/JNEUROSCI.3509-12.2012
Liu, Q. et al. The distinct roles of two GPCRs, MrgprC11 and PAR2, in itch and hyperalgesia. Sci. Signal. 4, ra45 (2011).
pubmed: 21775281 pmcid: 3144551
Yamaguchi, T., Nagasawa, T., Satoh, M. & Kuraishi, Y. Itch-associated response induced by intradermal serotonin through 5-HT2 receptors in mice. Neurosci. Res. 35, 77–83 (1999).
pubmed: 10616911 doi: 10.1016/S0168-0102(99)00070-X pmcid: 10616911
Kremer, A. E. et al. Lysophosphatidic acid is a potential mediator of cholestatic pruritus. Gastroenterology 139, 1018.e1–1018 (2010).
doi: 10.1053/j.gastro.2010.05.009
Chen, Y. et al. Luciferase reporter gene assay on human 5-HT receptor: which response element should be chosen? Sci. Rep. 5, 8060 (2015).
pubmed: 25622827 pmcid: 4306921 doi: 10.1038/srep08060
Han, S.-K. et al. Orphan G protein-coupled receptors MrgA1 and MrgC11 are distinctively activated by RF-amide-related peptides through the G q/11 pathway. Proc. Natl. Acad. Sci. 99, 14740–14745 (2002).
pubmed: 12397184 doi: 10.1073/pnas.192565799 pmcid: 12397184
Shinohara, T. et al. Identification of a G protein-coupled receptor specifically responsive to beta-alanine. J. Biol. Chem. 279, 23559–64 (2004).
pubmed: 15037633 doi: 10.1074/jbc.M314240200 pmcid: 15037633
Lembo, P. M. C. et al. Proenkephalin A gene products activate a new family of sensory neuron–specific GPCRs. Nat. Neurosci. 5, 201–9 (2002).
pubmed: 11850634 doi: 10.1038/nn815 pmcid: 11850634
Sun, S. & Dong, X. Trp channels and itch. Semin. Immunopathol. 38, 293–307 (2016).
pubmed: 26385480 doi: 10.1007/s00281-015-0530-4 pmcid: 26385480
Eijkelkamp, N. et al. Neurological perspectives on voltage-gated sodium channels. Brain 135, 2585–612 (2012).
pubmed: 22961543 pmcid: 3437034 doi: 10.1093/brain/aws225
Lai, J., Porreca, F., Hunter, J. C. & Gold, M. S. Voltage-gated sodium channels and hyperalgesia. Annu. Rev. Pharmacol. Toxicol. 44, 371–97 (2004).
pubmed: 14744251 doi: 10.1146/annurev.pharmtox.44.101802.121627 pmcid: 14744251
Harriott, A. M. & Gold, M. S. Contribution of primary afferent channels to neuropathic pain. Curr. Pain Headache Rep. 13, 197–207 (2009).
pubmed: 19457280 pmcid: 2859626 doi: 10.1007/s11916-009-0034-9
Jurcakova, D. et al. Voltage-Gated Sodium Channels Regulating Action Potential Generation in Itch-, Nociceptive-, and Low-Threshold Mechanosensitive Cutaneous C-Fibers. Mol. Pharmacol. 94, 1047–1056 (2018).
pubmed: 29941667 doi: 10.1124/mol.118.112839 pmcid: 29941667
Usoskin, D. et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Publ. Gr. 18, 145–153 (2014).
Zimmermann, K. et al. Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature 447, 855–8 (2007).
pubmed: 17568746 doi: 10.1038/nature05880 pmcid: 17568746
Nassar, M. A. et al. Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain. Proc. Natl. Acad. Sci. 101, 12706–12711 (2004).
pubmed: 15314237 doi: 10.1073/pnas.0404915101 pmcid: 15314237
Dib-Hajj, S. D. et al. Voltage-gated sodium channels in pain states: Role in pathophysiology and targets for treatment. Brain Res. Rev. 60, 65–83 (2009).
pubmed: 19150627 doi: 10.1016/j.brainresrev.2008.12.005 pmcid: 19150627
Emery, E. C., Luiz, A. P. & Wood, J. N. Nav 1. 7 and other voltage-gated sodium channels as drug targets for pain relief. Expert Opin. Ther. Targets 20, 975–983 (2016).
pubmed: 26941184 pmcid: 4950419 doi: 10.1517/14728222.2016.1162295
Zakrzewska, J. M. et al. Novel design for a phase IIa placebo-controlled, double-blind randomized withdrawal study to evaluate the safety and efficacy of CNV1014802 in patients with trigeminal neuralgia. Trials 14, 402 (2013).
pubmed: 24267010 pmcid: 4222641 doi: 10.1186/1745-6215-14-402
McDonnell, A. et al. Efficacy of the Nav1.7 blocker PF-05089771 in a randomised, placebo-controlled, double-blind clinical study in subjects with painful diabetic peripheral neuropathy. Pain 159, 1465–1476 (2018).
pubmed: 29578944 doi: 10.1097/j.pain.0000000000001227 pmcid: 29578944
Devigili, G. et al. Paroxysmal itch caused by gain-of-function Nav1.7 mutation. Pain 155, 1702–1707 (2014).
pubmed: 24820863 doi: 10.1016/j.pain.2014.05.006 pmcid: 24820863
Faber, C. G. et al. Gain-of-function Nav1.8 mutations in painful neuropathy. Proc. Natl. Acad. Sci. USA 109, 19444–9 (2012).
pubmed: 23115331 doi: 10.1073/pnas.1216080109 pmcid: 23115331
Salvatierra, J. et al. A disease mutation reveals a role for NaV1.9 in acute itch. J. Clin. Invest. 128, 5434–5447 (2018).
pubmed: 30395542 pmcid: 6264633 doi: 10.1172/JCI122481
Woods, C. G., Babiker, M. O. E., Horrocks, I., Tolmie, J. & Kurth, I. The phenotype of congenital insensitivity to pain due to the NaV1.9 variant p.L811P. Eur. J. Hum. Genet. 23, 1434 (2015).
pubmed: 26376683 pmcid: 4592096 doi: 10.1038/ejhg.2015.163
Lee, J. H. et al. A monoclonal antibody that targets a NaV1.7 channel voltage sensor for pain and itch relief. Cell 157, 1393–1404 (2014).
pubmed: 24856969 pmcid: 4098795 doi: 10.1016/j.cell.2014.03.064
Graceffa, R. F. et al. Sulfonamides as Selective NaV1.7 Inhibitors: Optimizing Potency, Pharmacokinetics, and Metabolic Properties to Obtain Atropisomeric Quinolinone (AM-0466) that Affords Robust in Vivo Activity. J. Med. Chem. 60, 5990–6017 (2017).
pubmed: 28324649 doi: 10.1021/acs.jmedchem.6b01850 pmcid: 28324649
Kornecook, T. J. et al. Pharmacologic Characterization of AMG8379, a Potent and Selective Small Molecule Sulfonamide Antagonist of the Voltage-Gated Sodium Channel Na
pubmed: 28473457 doi: 10.1124/jpet.116.239590
La, D. S. et al. The discovery of benzoxazine sulfonamide inhibitors of NaV1.7: Tools that bridge efficacy and target engagement. Bioorganic Med. Chem. Lett. 27, 3477–3485 (2017).
doi: 10.1016/j.bmcl.2017.05.070
Theile, J. W., Fuller, M. D. & Chapman, M. L. The Selective Nav1.7 Inhibitor, PF-05089771, Interacts Equivalently with Fast and Slow Inactivated Nav1.7 Channels. Mol. Pharmacol. 90, 540–548 (2016).
pubmed: 27587537 doi: 10.1124/mol.116.105437 pmcid: 27587537
Swain, N. A. et al. Discovery of Clinical Candidate 4-[2-(5-Amino-1H-pyrazol-4-yl)-4-chlorophenoxy]-5-chloro-2-fluoro-N-1,3-thiazol-4-ylbenzenesulfonamide (PF-05089771): Design and Optimization of Diaryl Ether Aryl Sulfonamides as Selective Inhibitors of NaV1.7. J. Med. Chem. 60, 7029–7042 (2017).
pubmed: 28682065 doi: 10.1021/acs.jmedchem.7b00598 pmcid: 28682065
Jarvis, M. F. et al. A-803467, a potent and selective Nav1.8 sodium channel blocker, attenuates neuropathic and inflammatory pain in the rat. Proc. Natl. Acad. Sci. 104, 8520–8525 (2007).
pubmed: 17483457 doi: 10.1073/pnas.0611364104 pmcid: 17483457
Reich, A., Ständer, S. & Szepietowski, J. C. Drug-induced pruritus: A review. Acta Derm. Venereol. 89, 236–244 (2009).
pubmed: 19479118 doi: 10.2340/00015555-0650 pmcid: 19479118
Shields, S. D. et al. Insensitivity to Pain upon Adult-Onset Deletion of Nav1.7 or Its Blockade with Selective Inhibitors. J. Neurosci. 38, 10180–10201 (2018).
pubmed: 30301756 pmcid: 6596201 doi: 10.1523/JNEUROSCI.1049-18.2018
Klugbauer, N., Lacinova, L., Flockerzi, V. & Hofmann, F. Structure and functional expression of a new member of the tetrodotoxin-sensitive voltage-activated sodium channel family from human neuroendocrine cells. EMBO J. 14, 1084–90 (1995).
pubmed: 7720699 pmcid: 398185 doi: 10.1002/j.1460-2075.1995.tb07091.x
Cummins, T. R., Sheets, P. L. & Waxman, S. G. The roles of sodium channels in nociception: Implications for mechanisms of pain. Pain 131, 243–57 (2007).
pubmed: 17766042 pmcid: 2055547 doi: 10.1016/j.pain.2007.07.026
Choi, J.-S., Dib-Hajj, S. D. & Waxman, S. G. Inherited erythermalgia: limb pain from an S4 charge-neutral Na channelopathy. Neurology 67, 1563–7 (2006).
pubmed: 16988069 doi: 10.1212/01.wnl.0000231514.33603.1e pmcid: 16988069
Cummins, T. R., Dib-Hajj, S. D. & Waxman, S. G. Electrophysiological properties of mutant Nav1.7 sodium channels in a painful inherited neuropathy. J. Neurosci. 24, 8232–6 (2004).
pubmed: 15385606 pmcid: 6729696 doi: 10.1523/JNEUROSCI.2695-04.2004
Sheets, P. L., Jackson, J. O., Waxman, S. G., Dib-Hajj, S. D. & Cummins, T. R. A Nav1.7 channel mutation associated with hereditary erythromelalgia contributes to neuronal hyperexcitability and displays reduced lidocaine sensitivity. J. Physiol. 581, 1019–31 (2007).
pubmed: 17430993 pmcid: 2170829 doi: 10.1113/jphysiol.2006.127027
McDermott, L. A. et al. Defining the Functional Role of NaV1.7 in Human Nociception. Neuron 101, 905–919.e8 (2019).
pubmed: 30795902 pmcid: 6424805 doi: 10.1016/j.neuron.2019.01.047
Gingras, J. et al. Global Nav1.7 knockout mice recapitulate the phenotype of human congenital indifference to pain. PLoS One 9, (2014).
pubmed: 25188265 pmcid: 4154897 doi: 10.1371/journal.pone.0105895
Han, C., Huang, J. & Waxman, S. G. Sodium channel Nav1.8: Emerging links to human disease. Neurology 86, 473–83 (2016).
pubmed: 26747884 doi: 10.1212/WNL.0000000000002333 pmcid: 26747884
Sangameswaran, L. et al. Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J. Biol. Chem. 271, 5953–6 (1996).
pubmed: 8626372 doi: 10.1074/jbc.271.11.5953 pmcid: 8626372
Elliott, A. A. & Elliott, J. R. Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia. J. Physiol. 463, 39–56 (1993).
pubmed: 8246189 pmcid: 1175332 doi: 10.1113/jphysiol.1993.sp019583
Hoffmann, T. et al. Reduced excitability and impaired nociception in peripheral unmyelinated fibers from Nav1.9-null mice. Pain 158, 58–67 (2017).
pubmed: 27780178 doi: 10.1097/j.pain.0000000000000723 pmcid: 27780178
Nicol, N. H. Anatomy and physiology of the skin. Dermatology Nurs. 17, 62 (2005).
Akopian, A. N. et al. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat. Neurosci. 2, 541–8 (1999).
pubmed: 10448219 doi: 10.1038/9195 pmcid: 10448219
Matsutomi, T., Nakamoto, C., Zheng, T., Kakimura, J.-I. & Ogata, N. Multiple types of Na(+) currents mediate action potential electrogenesis in small neurons of mouse dorsal root ganglia. Pflugers Arch. 453, 83–96 (2006).
pubmed: 16838161 doi: 10.1007/s00424-006-0104-3 pmcid: 16838161
Weiss, J. et al. Loss-of-function mutations in sodium channel Nav1.7 cause anosmia. Nature 472, 186–90 (2011).
pubmed: 21441906 pmcid: 3674497 doi: 10.1038/nature09975
Ostman, J. A. R., Nassar, M. A., Wood, J. N. & Baker, M. D. GTP up-regulated persistent Na+ current and enhanced nociceptor excitability require NaV1.9. J. Physiol. 586, 1077–87 (2008).
pubmed: 18096591 doi: 10.1113/jphysiol.2007.147942 pmcid: 18096591
Cummins, T. R., Howe, J. R. & Waxman, S. G. Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/PN1 sodium channel. J. Neurosci. 18, 9607–19 (1998).
pubmed: 9822722 pmcid: 6793269 doi: 10.1523/JNEUROSCI.18-23-09607.1998
Herzog, R. I., Cummins, T. R., Ghassemi, F., Dib-Hajj, S. D. & Waxman, S. G. Distinct repriming and closed-state inactivation kinetics of Nav1.6 and Nav1.7 sodium channels in mouse spinal sensory neurons. J. Physiol. 551, 741–750 (2003).
pubmed: 12843211 pmcid: 2343279 doi: 10.1113/jphysiol.2003.047357
Isensee, J. et al. Synergistic regulation of serotonin and opioid signaling contributes to pain insensitivity in Nav1.7 knockout mice. Sci. Signal. 10, (2017).
pubmed: 28074005 pmcid: 6711404 doi: 10.1126/scisignal.aah4874
Liu, X.-Y. et al. Unidirectional cross-activation of GRPR by MOR1D uncouples itch and analgesia induced by opioids. Cell 147, 447–58 (2011).
pubmed: 22000021 pmcid: 3197217 doi: 10.1016/j.cell.2011.08.043
Ringkamp, M. et al. A role for nociceptive, myelinated nerve fibers in itch sensation. J. Neurosci. 31, 14841–9 (2011).
pubmed: 22016517 pmcid: 3218799 doi: 10.1523/JNEUROSCI.3005-11.2011
Minett, M. S. et al. Distinct Nav1.7-dependent pain sensations require different sets of sensory and sympathetic neurons. Nat. Commun. 3, 791–799 (2012).
pubmed: 22531176 pmcid: 3337979 doi: 10.1038/ncomms1795
Faul, F., Erdfelder, E., Lang, A.-G. & Buchner, A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 39, 175–91 (2007).
doi: 10.3758/BF03193146
Dittert, I. et al. A technique for fast application of heated solutions of different composition to cultured neurones. J. Neurosci. Methods 82, 195–201 (1998).
pubmed: 9700692 doi: 10.1016/S0165-0270(98)00051-X pmcid: 9700692
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–8 (2001).
doi: 10.1006/meth.2001.1262

Auteurs

Helen Kühn (H)

Department of Medicine 1, Friedrich-Alexander-University Erlangen-Nürnberg, Ulmenweg 18, Erlangen, Germany. helen.kuehn@fau.de.

Leonie Kappes (L)

Department of Medicine 1, Friedrich-Alexander-University Erlangen-Nürnberg, Ulmenweg 18, Erlangen, Germany.

Katharina Wolf (K)

Department of Medicine 1, Friedrich-Alexander-University Erlangen-Nürnberg, Ulmenweg 18, Erlangen, Germany.

Lisa Gebhardt (L)

Department of Medicine 1, Friedrich-Alexander-University Erlangen-Nürnberg, Ulmenweg 18, Erlangen, Germany.
Institute of Physiology and Pathophysiology, Friedrich-Alexander-University Erlangen-Nürnberg, Universitätsstrasse 17, Erlangen, Germany.

Markus F Neurath (MF)

Department of Medicine 1, Friedrich-Alexander-University Erlangen-Nürnberg, Ulmenweg 18, Erlangen, Germany.

Peter Reeh (P)

Institute of Physiology and Pathophysiology, Friedrich-Alexander-University Erlangen-Nürnberg, Universitätsstrasse 17, Erlangen, Germany.

Michael J M Fischer (MJM)

Center for Physiology and Pharmacology, Medical University of Vienna, Schwarzspanierstrasse 17, Vienna, Austria.

Andreas E Kremer (AE)

Department of Medicine 1, Friedrich-Alexander-University Erlangen-Nürnberg, Ulmenweg 18, Erlangen, Germany. andreas.kremer@uk-erlangen.de.

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