Cellular Na+ handling mechanisms involved in airway smooth muscle contraction (Review)
- Authors:
- Bettina Sommer
- Edgar Flores-Soto
- Georgina Gonzalez-Avila
-
Affiliations: Department of Bronchial Hyperreactivity, National Institute of Respiratory Diseases ‘Ismael Cosio Villegas’, CP 14080 Mexico City, Mexico, Department of Pharmacology, Faculty of Medicine, National Autonomous University of Mexico, CP 04510 Mexico City, Mexico, Biomedical Oncology Laboratory, Department of Chronic‑Degenerative Diseases, National Institute of Respiratory Diseases ‘Ismael Cosio Villegas’, CP 14080 Mexico City, Mexico - Published online on: May 17, 2017 https://doi.org/10.3892/ijmm.2017.2993
- Pages: 3-9
-
Copyright: © Sommer et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Woloski JR, Heston S and Escobedo Calderon SP: Respiratory Allergic Disorders. Prim Care. 43:401–415. 2016. View Article : Google Scholar : PubMed/NCBI | |
Bostantzoglou C, Delimpoura V, Samitas K, Zervas E, Kanniess F and Gaga M: Clinical asthma phenotypes in the real world: Opportunities and challenges. Breathe Sheff. 11:186–193. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lommatzsch M and Stoll P: Novel strategies for the treatment of asthma. Allergo J Int. 25:11–17. 2016. View Article : Google Scholar : PubMed/NCBI | |
Koopmans T, Anaparti V, Castro-Piedras I, Yarova P, Irechukwu N, Nelson C, Perez-Zoghbi J, Tan X, Ward JP and Wright DB: Ca2+ handling and sensitivity in airway smooth muscle: Emerging concepts for mechanistic understanding and therapeutic targeting. Pulm Pharmacol Ther. 29:108–120. 2014. View Article : Google Scholar : PubMed/NCBI | |
Carbajal V, Vargas MH, Flores-Soto E, Martínez-Cordero E, Bazán-Perkins B and Montaño LM: LTD4 induces hyperrespon-siveness to histamine in bovine airway smooth muscle: Role of SR-ATPase Ca2+ pump and tyrosine kinase. Am J Physiol Lung Cell Mol Physiol. 288:L84–L92. 2005. View Article : Google Scholar | |
Liu C, Tazzeo T and Janssen LJ: Isoprostane-induced airway hyperresponsiveness is dependent on internal Ca2+ handling and Rho/ROCK signaling. Am J Physiol Lung Cell Mol Physiol. 291:L1177–L1184. 2006. View Article : Google Scholar : PubMed/NCBI | |
Morin C and Rousseau E: Enhanced Ca2+ sensitivity in hyper-responsive cultured bronchi is mediated by TNFalpha and NF-kappaB. Can J Physiol Pharmacol. 84:1029–1041. 2006. View Article : Google Scholar | |
Sweeney D, Hollins F, Gomez E, Saunders R, Challiss RA and Brightling CE: [Ca2+]i oscillations in ASM: Relationship with persistent airflow obstruction in asthma. Respirology. 19:763–766. 2014. View Article : Google Scholar : PubMed/NCBI | |
Fleischmann BK, Washabau RJ and Kotlikoff MI: Control of resting membrane potential by delayed rectifier potassium currents in ferret airway smooth muscle cells. J Physiol. 469:625–638. 1993. View Article : Google Scholar : PubMed/NCBI | |
Blaustein MP: Sodium ions, calcium ions, blood pressure regulation, and hypertension: A reassessment and a hypothesis. Am J Physiol. 232:C165–C173. 1977.PubMed/NCBI | |
Orrenius S, Zhivotovsky B and Nicotera P: Regulation of cell death: The calcium-apoptosis link. Nat Rev Mol Cell Biol. 4:552–565. 2003. View Article : Google Scholar : PubMed/NCBI | |
Eder P, Poteser M, Romanin C and Groschner K: Na(+) entry and modulation of Na(+)/Ca(2+) exchange as a key mechanism of TRPC signaling. Pflugers Arch. 451:99–104. 2005. View Article : Google Scholar : PubMed/NCBI | |
Blaustein MP and Lederer WJ: Sodium/calcium exchange: Its physiological implications. Physiol Rev. 79:763–854. 1999.PubMed/NCBI | |
Blaustein MP and Wier WG: Local sodium, global reach: Filling the gap between salt and hypertension. Circ Res. 101:959–961. 2007. View Article : Google Scholar : PubMed/NCBI | |
Poburko D, Fameli N, Kuo KH and van Breemen C: Ca2+ signaling in smooth muscle: TRPC6, NCX and LNats in nanodomains. Channels (Austin). 2:10–12. 2008. View Article : Google Scholar | |
Dai JM, Kuo KH, Leo JM, Paré PD, van Breemen C and Lee CH: Acetylcholine-induced asynchronous calcium waves in intact human bronchial muscle bundle. Am J Respir Cell Mol Biol. 36:600–608. 2007. View Article : Google Scholar | |
Flores-Soto E, Reyes-García J, Sommer B and Montaño LM: Sarcoplasmic reticulum Ca(2+) refilling is determined by L-type Ca(2+) and store operated Ca(2+) channels in guinea pig airway smooth muscle. Eur J Pharmacol. 721:21–28. 2013. View Article : Google Scholar : PubMed/NCBI | |
Perusquía M, Flores-Soto E, Sommer B, Campuzano-González E, Martínez-Villa I, Martínez-Banderas AI and Montaño LM: Testosterone-induced relaxation involves L-type and store-operated Ca2+ channels blockade, and PGE2 in guinea pig airway smooth muscle. Pflugers Arch. 467:767–777. 2015. View Article : Google Scholar | |
Sommer B, Flores-Soto E, Reyes-García J, Díaz-Hernández V, Carbajal V and Montaño LM: Na(+) permeates through L-type Ca(2+) channel in bovine airway smooth muscle. Eur J Pharmacol. 782:77–88. 2016. View Article : Google Scholar : PubMed/NCBI | |
Lingrel JB: The physiological significance of the cardiotonic steroid/ouabain-binding site of the Na, K-ATPase. Annu Rev Physiol. 72:395–412. 2010. View Article : Google Scholar | |
Agrawal A, Agrawal KP, Ram A, Sondhi A, Chhabra SK, Gangal SV and Mehta D: Basis of rise in intracellular sodium in airway hyperresponsiveness and asthma. Lung. 183:375–387. 2005. View Article : Google Scholar | |
Chhabra SK, Khanduja A and Jain D: Increased intracellular calcium and decreased activities of leucocyte Na+, K+-ATPase and Ca2+-ATPase in asthma. Clin Sci (Lond). 97:595–601. 1999. View Article : Google Scholar | |
Gentile DA and Skoner DP: The relationship between airway hyperreactivity (AHR) and sodium, potassium adenosine triphosphatase (Na+, K+ ATPase) enzyme inhibition. J Allergy Clin Immunol. 99:367–373. 1997. View Article : Google Scholar : PubMed/NCBI | |
Skoner DP, Gentile D and Evans RW: A circulating inhibitor of the platelet Na+, K+ adenosine triphosphatase (ATPase) enzyme in allergy. J Allergy Clin Immunol. 87:476–482. 1991. View Article : Google Scholar : PubMed/NCBI | |
Tribe RM, Barton JR, Poston L and Burney PG: Dietary sodium intake, airway responsiveness, and cellular sodium transport. Am J Respir Crit Care Med. 149:1426–1433. 1994. View Article : Google Scholar : PubMed/NCBI | |
Van Deusen MA, Gentile DA and Skoner DP: Inhibition of the sodium, potassium adenosine triphosphatase enzyme in peripheral blood mononuclear cells of subjects with allergic rhinitis. Ann Allergy Asthma Immunol. 78:259–264. 1997. View Article : Google Scholar : PubMed/NCBI | |
Hamlyn JM, Blaustein MP, Bova S, DuCharme DW, Harris DW, Mandel F, Mathews WR and Ludens JH: Identification and characterization of a ouabain-like compound from human plasma. Proc Natl Acad Sci USA. 88:6259–6263. 1991. View Article : Google Scholar : PubMed/NCBI | |
Ferrandi M, Manunta P, Balzan S, Hamlyn JM, Bianchi G and Ferrari P: Ouabain-like factor quantification in mammalian tissues and plasma: Comparison of two independent assays. Hypertension. 30:886–896. 1997. View Article : Google Scholar : PubMed/NCBI | |
Laredo J, Hamilton BP and Hamlyn JM: Ouabain is secreted by bovine adrenocortical cells. Endocrinology. 135:794–797. 1994. View Article : Google Scholar : PubMed/NCBI | |
Schoner W: Ouabain, a new steroid hormone of adrenal gland and hypothalamus. Exp Clin Endocrinol Diabetes. 108:449–454. 2000. View Article : Google Scholar : PubMed/NCBI | |
Komiyama Y, Nishimura N, Munakata M, Mori T, Okuda K, Nishino N, Hirose S, Kosaka C, Masuda M and Takahashi H: Identification of endogenous ouabain in culture supernatant of PC12 cells. J Hypertens. 19:229–236. 2001. View Article : Google Scholar : PubMed/NCBI | |
el-Masri MA, Clark BJ, Qazzaz HM and Valdes R Jr: Human adrenal cells in culture produce both ouabain-like and dihydroouabain-like factors. Clin Chem. 48:1720–1730. 2002.PubMed/NCBI | |
Murrell JR, Randall JD, Rosoff J, Zhao JL, Jensen RV, Gullans SR and Haupert GT Jr: Endogenous ouabain: Upregulation of steroidogenic genes in hypertensive hypothalamus but not adrenal. Circulation. 112:1301–1308. 2005. View Article : Google Scholar : PubMed/NCBI | |
Laredo J, Shah JR, Lu ZR, Hamilton BP and Hamlyn JM: Angiotensin II stimulates secretion of endogenous ouabain from bovine adrenocortical cells via angiotensin type 2 receptors. Hypertension. 29:401–407. 1997. View Article : Google Scholar : PubMed/NCBI | |
Shah JR, Laredo J, Hamilton BP and Hamlyn JM: Effects of angiotensin II on sodium potassium pumps, endogenous ouabain, and aldosterone in bovine zona glomerulosa cells. Hypertension. 33:373–377. 1999. View Article : Google Scholar : PubMed/NCBI | |
Saklani P and Skanes A: Novel anti-arrhythmic medications in the treatment of atrial fibrillation. Curr Cardiol Rev. 8:302–309. 2012. View Article : Google Scholar : PubMed/NCBI | |
Cortijo J, Sarria B, Mata M, Naline E, Advenier C and Morcillo EJ: Effects of ouabain on human bronchial muscle in vitro. Naunyn Schmiedebergs Arch Pharmacol. 368:393–403. 2003. View Article : Google Scholar : PubMed/NCBI | |
Blaustein MP and Hamlyn JM: Signaling mechanisms that link salt retention to hypertension: Endogenous ouabain, the Na(+) pump, the Na(+)/Ca(2+) exchanger and TRPC proteins. Biochim Biophys Acta. 1802:1219–1229. 2010. View Article : Google Scholar : PubMed/NCBI | |
Katz A, Lifshitz Y, Bab-Dinitz E, Kapri-Pardes E, Goldshleger R, Tal DM and Karlish SJ: Selectivity of digitalis glycosides for isoforms of human Na, K-ATPase. J Biol Chem. 285:19582–19592. 2010. View Article : Google Scholar : PubMed/NCBI | |
Floyd R and Wray S: Calcium transporters and signalling in smooth muscles. Cell Calcium. 42:467–476. 2007. View Article : Google Scholar : PubMed/NCBI | |
DiPolo R and Beaugé L: Sodium/calcium exchanger: Influence of metabolic regulation on ion carrier interactions. Physiol Rev. 86:155–203. 2006. View Article : Google Scholar | |
Kofuji P, Lederer WJ and Schulze DH: Mutually exclusive and cassette exons underlie alternatively spliced isoforms of the Na/Ca exchanger. J Biol Chem. 269:5145–5149. 1994.PubMed/NCBI | |
Quednau BD, Nicoll DA and Philipson KD: Tissue specificity and alternative splicing of the Na+/Ca2+ exchanger isoforms NCX1, NCX2, and NCX3 in rat. Am J Physiol. 272:C1250–C1261. 1997.PubMed/NCBI | |
Mejía-Elizondo R, Espinosa-Tanguma R and Saavedra-Alanis VM: Molecular identification of the NCX isoform expressed in tracheal smooth muscle of guinea pig. Ann NY Acad Sci. 976:73–76. 2002. View Article : Google Scholar : PubMed/NCBI | |
Philipson KD, Nicoll DA, Ottolia M, Quednau BD, Reuter H, John S and Qiu Z: The Na+/Ca2+ exchange molecule: An overview. Ann NY Acad Sci. 976:1–10. 2002. View Article : Google Scholar | |
Pitt A and Knox AJ: Molecular characterization of the human airway smooth muscle Na+/Ca2+ exchanger. Am J Respir Cell Mol Biol. 15:726–730. 1996. View Article : Google Scholar : PubMed/NCBI | |
Janssen LJ, Walters DK and Wattie J: Regulation of [Ca2+] in canine airway smooth muscle by Ca(2+)-ATPase and Na+/Cai2+ exchange mechanisms. Am J Physiol. 273:L322–L330. 1997.PubMed/NCBI | |
Flores-Soto E, Carbajal V, Reyes-García J, García-Hernández LM, Figueroa A, Checa M, Barajas-López C and Montaño LM: In airways ATP refills sarcoplasmic reticulum via P2X smooth muscle receptors and induces contraction through P2Y epithelial receptors. Pflugers Arch. 461:261–275. 2011. View Article : Google Scholar | |
Liu B, Peel SE, Fox J and Hall IP: Reverse mode Na+/Ca2+ exchange mediated by STIM1 contributes to Ca2+ influx in airway smooth muscle following agonist stimulation. Respir Res. 11:1682010. View Article : Google Scholar | |
Putney JW and Tomita T: Phospholipase C signaling and calcium influx. Adv Biol Regul. 52:152–164. 2012. View Article : Google Scholar | |
Pedersen SF, Owsianik G and Nilius B: TRP channels: An overview. Cell Calcium. 38:233–252. 2005. View Article : Google Scholar : PubMed/NCBI | |
Trebak M, Lemonnier L, Smyth JT, Vazquez G and Putney JW Jr: Phospholipase C-coupled receptors and activation of TRPC channels. Handb Exp Pharmacol. 179:593–614. 2007. View Article : Google Scholar | |
Trebak M, Vazquez G, Bird GS and Putney JW Jr: The TRPC3/6/7 subfamily of cation channels. Cell Calcium. 33:451–461. 2003. View Article : Google Scholar : PubMed/NCBI | |
Vazquez G, Wedel BJ, Aziz O, Trebak M and Putney JW Jr: The mammalian TRPC cation channels. Biochim Biophys Acta. 1742:21–36. 2004. View Article : Google Scholar : PubMed/NCBI | |
Ong HL and Ambudkar IS: The dynamic complexity of the TRPC1 channelosome. Channels (Austin). 5:424–431. 2011. View Article : Google Scholar | |
Yuan JP, Lee KP, Hong JH and Muallem S: The closing and opening of TRPC channels by Homer1 and STIM1. Acta Physiol (Oxf). 204:238–247. 2012. View Article : Google Scholar | |
Cheng KT, Liu X, Ong HL, Swaim W and Ambudkar IS: Local Ca2+ entry via Orai1 regulates plasma membrane recruitment of TRPC1 and controls cytosolic Ca2+ signals required for specific cell functions. PLoS Biol. 9:e10010252011. View Article : Google Scholar | |
Soboloff J, Madesh M and Gill DL: Sensing cellular stress through STIM proteins. Nat Chem Biol. 7:488–492. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zhu X, Jiang M, Peyton M, Boulay G, Hurst R, Stefani E and Birnbaumer L: Trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry. Cell. 85:661–671. 1996. View Article : Google Scholar : PubMed/NCBI | |
Kiselyov K, Xu X, Mozhayeva G, Kuo T, Pessah I, Mignery G, Zhu X, Birnbaumer L and Muallem S: Functional interaction between InsP3 receptors and store-operated Htrp3 channels. Nature. 396:478–482. 1998. View Article : Google Scholar : PubMed/NCBI | |
McKay RR, Szymeczek-Seay CL, Lievremont JP, Bird GS, Zitt C, Jüngling E, Lückhoff A and Putney JW Jr: Cloning and expression of the human transient receptor potential 4 (TRP4) gene: Localization and functional expression of human TRP4 and TRP3. Biochem J. 351:735–746. 2000. View Article : Google Scholar : PubMed/NCBI | |
Kiselyov K, Mignery GA, Zhu MX and Muallem S: The N-terminal domain of the IP3 receptor gates store-operated hTrp3 channels. Mol Cell. 4:423–429. 1999. View Article : Google Scholar : PubMed/NCBI | |
Xiao JH, Zheng YM, Liao B and Wang YX: Functional role of canonical transient receptor potential 1 and canonical transient receptor potential 3 in normal and asthmatic airway smooth muscle cells. Am J Respir Cell Mol Biol. 43:17–25. 2010. View Article : Google Scholar : | |
Putney JW: The physiological function of store-operated calcium entry. Neurochem Res. 36:1157–1165. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bradley E, Webb TI, Hollywood MA, Sergeant GP, McHale NG and Thornbury KD: The cardiac sodium current Na(v)1.5 is functionally expressed in rabbit bronchial smooth muscle cells. Am J Physiol Cell Physiol. 305:C427–C435. 2013. View Article : Google Scholar : PubMed/NCBI | |
Snetkov VA, Hirst SJ and Ward JP: Ion channels in freshly isolated and cultured human bronchial smooth muscle cells. Exp Physiol. 81:791–804. 1996. View Article : Google Scholar : PubMed/NCBI | |
Jo T, Nagata T, Iida H, Imuta H, Iwasawa K, Ma J, Hara K, Omata M, Nagai R, Takizawa H, et al: Voltage-gated sodium channel expressed in cultured human smooth muscle cells: Involvement of SCN9A. FEBS Lett. 567:339–343. 2004. View Article : Google Scholar : PubMed/NCBI | |
Nakajima T, Jo T, Meguro K, Oonuma H, Ma J, Kubota N, Imuta H, Takano H, Iida H, Nagase T, et al: Effect of dexamethasone on voltage-gated Na+ channel in cultured human bronchial smooth muscle cells. Life Sci. 82:1210–1215. 2008. View Article : Google Scholar : PubMed/NCBI | |
Knox AJ, Ajao P, Britton JR and Tattersfield AE: Effect of sodium-transport inhibitors on airway smooth muscle contractility in vitro. Clin Sci (Lond). 79:315–323. 1990. View Article : Google Scholar | |
Knudsen T, Bertelsen H and Johansen T: Ouabain enhancement of compound 48/80 induced histamine secretion from rat peritoneal mast cells: Dependence on extracellular sodium. Pharmacol Toxicol. 70:412–418. 1992. View Article : Google Scholar : PubMed/NCBI | |
de Vasconcelos DI, Leite JA, Carneiro LT, Piuvezam MR, de Lima MR, de Morais LC, Rumjanek VM and Rodrigues-Mascarenhas S: Anti-inflammatory and antinociceptive activity of ouabain in mice. Mediators Inflamm. 2011:9129252011. View Article : Google Scholar : PubMed/NCBI | |
Choi JP, Kim YS, Kim OY, Kim YM, Jeon SG, Roh TY, Park JS, Gho YS and Kim YK: TNF-alpha is a key mediator in the development of Th2 cell response to inhaled allergens induced by a viral PAMP double-stranded RNA. Allergy. 67:1138–1148. 2012. View Article : Google Scholar : PubMed/NCBI | |
Hallstrand TS: New insights into pathogenesis of exercise-induced bronchoconstriction. Curr Opin Allergy Clin Immunol. 12:42–48. 2012. View Article : Google Scholar : | |
Anderson SD: Indirect challenge tests: Airway hyperresponsiveness in asthma: its measurement and clinical significance. Chest. 138(Suppl): 25S–30S. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hallstrand TS, Moody MW, Wurfel MM, Schwartz LB, Henderson WR Jr and Aitken ML: Inflammatory basis of exercise-induced bronchoconstriction. Am J Respir Crit Care Med. 172:679–686. 2005. View Article : Google Scholar : PubMed/NCBI | |
Hallstrand TS, Lai Y, Ni Z, Oslund RC, Henderson WR Jr, Gelb MH and Wenzel SE: Relationship between levels of secreted phospholipase A2 groups IIA and X in the airways and asthma severity. Clin Exp Allergy. 41:801–810. 2011. View Article : Google Scholar : PubMed/NCBI | |
Schmitt L, Wiebel M, Frese F, Dehnert C, Zugck C, Bärtsch P and Mairbäurl H: Exercise reduces airway sodium ion reabsorption in cystic fibrosis but not in exercise asthma. Eur Respir J. 37:342–348. 2011. View Article : Google Scholar | |
Aneiros E, Philipp S, Lis A, Freichel M and Cavalié A: Modulation of Ca2+ signaling by Na+/Ca2+ exchangers in mast cells. J Immunol. 174:119–130. 2005. View Article : Google Scholar | |
Praetorius HA, Friis UG, Praetorius J and Johansen T: Evidence for a Na+/Ca2+ exchange mechanism in rat peritoneal mast cells. Pflugers Arch. 437:86–93. 1998. View Article : Google Scholar : PubMed/NCBI | |
Rundell KW and Jenkinson DM: Exercise-induced bronchospasm in the elite athlete. Sports Med. 32:583–600. 2002. View Article : Google Scholar : PubMed/NCBI | |
Gotshall RW, Mickleborough TD and Cordain L: Dietary salt restriction improves pulmonary function in exercise-induced asthma. Med Sci Sports Exerc. 32:1815–1819. 2000. View Article : Google Scholar : PubMed/NCBI | |
McKeever TM, Lewis SA, Smit HA, Burney P, Cassano PA and Britton J: A multivariate analysis of serum nutrient levels and lung function. Respir Res. 9:67–89. 2008. View Article : Google Scholar : PubMed/NCBI | |
Mickleborough TD, Lindley MR and Ray S: Dietary salt, airway inflammation, and diffusion capacity in exercise-induced asthma. Med Sci Sports Exerc. 37:904–914. 2005.PubMed/NCBI | |
Pogson Z and McKeever T: Dietary sodium manipulation and asthma. Cochrane Database Syst Rev. 3:CD0004362011. | |
Ardern KD and Ardern KD: Dietary salt reduction or exclusion for allergic asthma. Cochrane Database Syst Rev. 2:CD0004362004. |