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01.12.2014

Differential Regulation of ASICs and TRPV1 by Zinc in Rat Bronchopulmonary Sensory Neurons

verfasst von: Zhanna V. Vysotskaya, Charles R. Moss II, Qihai Gu

Erschienen in: Lung | Ausgabe 6/2014

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Abstract

Purpose

Zinc has been known to act as a signaling molecule that regulates a variety of neuronal functions. In this study, we aimed to study the effect of zinc on two populations of acid-sensitive ion channels, acid-sensing ion channels (ASICs), and transient receptor potential vanilloid receptor-1 (TRPV1), in vagal bronchopulmonary sensory neurons.

Methods

Rat vagal sensory neurons innervating lungs and airways were retrogradely labeled with a fluorescent tracer. Whole-cell perforated patch-clamp recordings were carried out in primarily cultured bronchopulmonary sensory neurons. The acid-evoked ASIC and TRPV1 currents were measured and compared between before and after the zinc pretreatment.

Results

ASIC currents were induced by a pH drop from 7.4 to 6.8 or 6.5 in the presence of capsazepine (10 µM), a specific TRPV1 antagonist. Pretreatment with zinc (50 or 300 µM, 2 min) displayed different effects on the two distinct phenotypes of ASIC currents: a marked potentiation on ASIC channels with fast kinetics of activation and inactivation or no significant effect on ASIC currents with slow activation and inactivation. On the other hand, pretreatment with zinc significantly inhibited the acid (pH 5.5 or 5.3)-induced TRPV1 currents. The inhibition was abolished by intracellular chelation of zinc by TPEN (25 µM), indicating that intracellular accumulation of zinc was likely required for its inhibitory effect on TRPV1 channels.

Conclusions

Our study showed that zinc differentially regulates the activities of ASICs and TRPV1 channels in rat vagal bronchopulmonary sensory neurons.

Weiss JH, Sensi SL, Koh JY (2000) Zn(2+): a novel ionic mediator of neural injury in brain disease. Trends Pharmacol Sci 21:395–401CrossRefPubMed

Baron A, Schaefer L, Lingueglia E, Champigny G, Lazdunski M (2001) Zn²⁺ and H⁺ are coactivators of acid-sensing ion channels. J Biol Chem 276:35361–35367CrossRefPubMed

Frassinetti S, Bronzetti G, Caltavuturo L, Cini M, Croce CD (2006) The role of zinc in life: a review. J Environ Pathol Toxicol Oncol 25:597–610CrossRefPubMed

Nozaki C, Vergnano AM, Filliol D, Ouagazzal AM, Le Goff A, Carvalho S, Reiss D, Gaveriaux-Ruff C, Neyton J, Paoletti P, Kieffer BL (2009) Zinc alleviates pain through high-affinity binding to the NMDA receptor NR2A subunit. Nat Neurosci 14:1017–1022CrossRef

Gu Y, Barry J, Gu C (2013) Kv3 channel assembly, trafficking and activity are regulated by zinc through different binding sites. J Physiol 591:2491–2507PubMedCentralCrossRefPubMed

Sun HS, Hui K, Lee DW, Feng ZP (2007) Zn²⁺ sensitivity of high- and low-voltage activated calcium channels. Biophys J 93:1175–1183PubMedCentralCrossRefPubMed

Mathie A, Sutton GL, Clarke CE, Veale EL (2006) Zinc and copper: pharmacological probes and endogenous modulators of neuronal excitability. Pharmacol Ther 111:567–583CrossRefPubMed

Sensi SL, Paoletti P, Bush AI, Sekler I (2009) Zinc in the physiology and pathology of the CNS. Nat Rev Neurosci 10:780–791CrossRefPubMed

Hunt JF, Fang K, Malik R, Snyder A, Malhotra N, Platts-Mills TA, Gaston B (2000) Endogenous airway acidification. Implications for asthma pathophysiology. Am J Respir Crit Care Med 161:694–699CrossRefPubMed

10.

Kostikas K, Papatheodorou G, Ganas K, Psathakis K, Panagou P, Loukides S (2002) pH in expired breath condensate of patients with inflammatory airways diseases. Am J Respir Crit Care Med 165:1364–1370CrossRefPubMed

11.

Kodric M, Shah AN, Fabbri LM, Confalonieri M (2007) An investigation of airway acidification in asthma using induced sputum: a study of feasibility and correlation. Am J Respir Crit Care Med 175:905–910CrossRefPubMed

12.

Reeh PW, Steen KH (1996) Tissue acidosis in nociception and pain. Prog Brain Res 113:143–151CrossRefPubMed

13.

Mantyh PW, Clohisy DR, Koltzenburg M, Hunt SP (2002) Molecular mechanisms of cancer pain. Nat Rev Cancer 2:201–209CrossRefPubMed

14.

Krishtal O (2003) The ASICs: signaling molecules? Modulators? Trends Neurosci 26:477–483CrossRefPubMed

15.

Geppetti P, Materazzi S, Nicoletti P (2006) The transient receptor potential vanilloid 1: role in airway inflammation and disease. Eur J Pharmacol 533:207–214CrossRefPubMed

16.

Lee LY, Gu Q (2009) Role of TRPV1 in inflammation-induced airway hypersensitivity. Curr Opin Pharmacol 9:243–249PubMedCentralCrossRefPubMed

17.

Ricciardolo FL, Gaston B, Hunt J (2004) Acid stress in the pathology of asthma. J Allergy Clin Immunol 113:610–619CrossRefPubMed

18.

Kollarik M, Ru F, Undem BJ (2007) Acid-sensitive vagal sensory pathways and cough. Pulm Pharmacol Ther 20:402–411PubMedCentralCrossRefPubMed

19.

Gu Q, Lee LY (2011) Airway irritation and cough evoked by acid: from humans to ion channels. Curr Opin Pharmacol 11:238–247PubMedCentralCrossRefPubMed

20.

Gu Q, Vysotskaya ZV, Moss CR 2nd, Kagira MK, Gilbert CA (2013) Calcium-sensing receptor in rat vagal bronchopulmonary sensory neurons regulates the function of the capsaicin receptor TRPV1. Exp Physiol 98:1631–1642CrossRefPubMed

21.

Jiang Q, Li MH, Papasian CJ, Branigan D, Xiong ZG, Wang JQ, Chu XP (2009) Characterization of acid-sensing ion channels in medium spiny neurons of mouse striatum. Neuroscience 162:55–66CrossRefPubMed

22.

Jiang Q, Inoue K, Wu X, Papasian CJ, Wang JQ, Xiong ZG, Chu XP (2011) Cysteine 149 in the extracellular finger domain of acid-sensing ion channel 1b subunit is critical for zinc-mediated inhibition. Neuroscience 193:89–99PubMedCentralCrossRefPubMed

23.

Gu Q, Lin RL (2010) Heavy metals zinc, cadmium, and copper stimulate pulmonary sensory neurons via direct activation of TRPA1. J Appl Physiol 108:891–897PubMedCentralCrossRefPubMed

24.

Gu Q, Lee LY (2006) Characterization of acid-signaling in rat vagal pulmonary sensory neurons. Am J Physiol Lung Cell Mol Physiol 291:L58–L65PubMedCentralCrossRefPubMed

25.

Gu Q, Lee LY (2010) Regulation of acid signaling in rat pulmonary sensory neurons by protease-activated receptor-2. Am J Physiol Lung Cell Mol Physiol 298:L454–L461PubMedCentralCrossRefPubMed

26.

Bessac BF, Jordt SE (2008) Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensation and reflex control. Physiology 23:360–370PubMedCentralCrossRefPubMed

27.

Akopian AN (2011) Regulation of nociceptive transmission at the periphery via TRPA1-TRPV1 interactions. Curr Pharm Biotechnol 12:89–94CrossRefPubMed

28.

Wemmie JA, Price MP, Welsh MJ (2006) Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci 29:578–586CrossRefPubMed

29.

Xu TL, Xiong ZG (2007) Dynamic regulation of acid-sensing ion channels by extracellular and intracellular modulators. Curr Med Chem 14:1753–1763CrossRefPubMed

30.

Sherwood TW, Frey EN, Askwith CC (2012) Structure and activity of the acid-sensing ion channels. Am J Physiol Cell Physiol 303:C699–C710PubMedCentralCrossRefPubMed

31.

Holzer P (2009) Acid-sensitive ion channels and receptors. Handb Exp Pharmacol 194:283–332CrossRefPubMed

32.

Benson CJ, Xie J, Wemmie JA, Price MP, Henss JM, Welsh MJ, Snyder PM (2002) Heteromultimers of DEG/ENaC subunits form H⁺-gated channels in mouse sensory neurons. Proc Natl Acad Sci USA 99:2338–2343PubMedCentralCrossRefPubMed

33.

Chu XP, Wemmie JA, Wang WZ, Zhu XM, Saugstad JA, Price MP, Simon RP, Xiong ZG (2004) Subunit-dependent high-affinity zinc inhibition of acid-sensing ion channels. J Neurosci 24:8678–8689PubMedCentralCrossRefPubMed

34.

Poirot O, Berta T, Decosterd I, Kellenberger S (2006) Distinct ASIC currents are expressed in rat putative nociceptors and are modulated by nerve injury. J Physiol 576:215–234PubMedCentralCrossRefPubMed

35.

Jiang Q, Papasian CJ, Wang JQ, Xiong ZG, Chu XP (2010) Inhibitory regulation of acid-sensing ion channel 3 by zinc. Neuroscience 169:574–583CrossRefPubMed

36.

Caterina MJ, Julius D (2001) The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24:487–517CrossRefPubMed

37.

Lee LY, Pisarri TE (2001) Afferent properties and reflex functions of bronchopulmonary C-fibers. Respir Physiol 125:47–65CrossRefPubMed

38.

Pecze L, Winter Z, Jósvay K, Ötvös F, Kolozsi C, Vizler C, Budai D, Letoha T, Dombi G, Szakonyi G, Oláh Z (2013) Divalent heavy metal cations block the TRPV1 Ca(2+)channel. Biol Trace Elem Res 151:451–461PubMedCentralCrossRefPubMed

39.

Welch JM, Simon SA, Reinhart PH (2000) The activation mechanism of rat vanilloid receptor 1 by capsaicin involves the pore domain and differs from the activation by either acid or heat. Proc Natl Acad Sci USA 97:13889–13894PubMedCentralCrossRefPubMed

40.

Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to “hot” chili peppers. Cell 108:421–430CrossRefPubMed

41.

Sugiura T, Kasai M, Katsuya H, Mizumura K (2003) Thermal properties of acid-induced depolarization in cultured rat small primary afferent neurons. Neurosci Lett 350:109–112CrossRefPubMed

42.

Ni D, Lee LY (2008) Lack of potentiating effect of increasing temperature on responses to chemical activators in vagal sensory neurons isolated from TRPV1-null mice. Am J Physiol Lung Cell Mol Physiol 295:L897–L904PubMedCentralCrossRefPubMed

43.

Júnior WB, Alexandre-Moreira MS, Alves MA, Perez-Rebolledo A, Parrilha GL, Castellano EE, Piro OE, Barreiro EJ, Lima LM, Beraldo H (2011) Analgesic and anti-inflammatory activities of salicylaldehyde 2-chlorobenzoyl hydrazine (H(2)LASSBio-466), salicylaldehyde 4-chlorobenzoyl hydrazone (H(2)LASSBio-1064) and their zinc(II) complexes. Molecules 16:6902–6915CrossRefPubMed

44.

Tamba BI, Leon MM, Petreus T (2013) Common trace elements alleviate pain in an experimental mouse model. J Neurosci Res 91:554–561CrossRefPubMed

Titel: Differential Regulation of ASICs and TRPV1 by Zinc in Rat Bronchopulmonary Sensory Neurons
verfasst von: Zhanna V. Vysotskaya
Charles R. Moss II
Qihai Gu
Publikationsdatum: 01.12.2014
Verlag: Springer US
Erschienen in: Lung / Ausgabe 6/2014
Print ISSN: 0341-2040
Elektronische ISSN: 1432-1750
DOI: https://doi.org/10.1007/s00408-014-9634-1

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Differential Regulation of ASICs and TRPV1 by Zinc in Rat Bronchopulmonary Sensory Neurons

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Purpose

Methods

Results

Conclusions

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