Physiological Parameters Affecting the Modulatory Role of Airway Epithelium on Airway Smooth Muscle Responsiveness
DOI:
https://doi.org/10.17140/PRRMOJ-1-101Keywords:
Airways, Epithelium, Nitric oxideAbstract
Numerous studies have revealed the significant action of airway epithelium as a non-specific defence mechanism in airways. In addition, epithelial cells release biologically active agents, which modulate airway tone. Importantly, airway epithelium function is influenced by physiological parameters, including the release of endogenous factors, age, gender, load, and bronchi size. The primary goal of this review is to summarize knowledge concerning the effect of the aforementioned parameters on the modulatory role of airway epithelium on airway smooth muscle responsiveness. These effects may be implicated in the pathophysiology of airway diseases like asthma and Chronic Obstructive Pulmonary Disease (COPD).
References
Ricciardolo FL. Multiple roles of nitric oxide in the airways. Thorax. 2003; 58(2): 175-182. doi: 10.1136/thorax.58.2.175
Holgate ST. The airway epithelium is central to the patho-genesis of asthma. Allergol Int. 2008; 57(1): 1-10. doi: 10.2332/ allergolint.R-07-154
Knight DA, Stewart GA, Thompson PJ. Histamine tachyphy-laxis in human airway smooth muscle. The role of H2-receptors and the bronchial epithelium. Am Rev Respir Dis. 1992; 146(1): 137-140. doi: 10.1164/ajrccm/146.1.137
Knight DA, Holgate ST. The airway epithelium: structural and functional properties in health and disease. Respirology 2003; 8(4): 432-446. doi: 10.1046/j.1440-1843.2003.00493.x
de Marco R, Locatelli F, Sunyer J, Burney P. Differences in incidence of reported asthma related to age in men and women. A retrospective analysis of the data of the European Respiratory Health Survey. Am J Respir Crit Care Med. 2000; 162(1): 68- 74. doi: 10.1164/ajrccm.162.1.9907008
Papagianni M, HatziefthimiouA, Chachami G, Gourgoulianis K, Molyvdas PA, Paraskeva E. Insulin causes a transient induc-tion of proliferation via activation of the PI3-kinase pathway in airway smooth muscle cells. Exp Clin Endocrinol Diabetes. 2007; 115(2): 118-123. doi: 10.1055/s-2007-967094
Gosens R, Nelemans SA, Hiemstra M, Grootte Bromhaar MM, Meurs H, Zaagsma J. Insulin induces a hypercontractile airway smooth muscle phenotype. Eur J Pharmacol. 2003; 481(1): 125-131. doi: 10.1016/j.ejphar.2003.08.081
Dekkers BG, Schaafsma D, Tran T, Zaagsma J, Meurs H. In-sulin-induced laminin expression promotes a hypercontractile airway smooth muscle phenotype. Am J Respir Cell Mol Biol. 2009; 41(4): 494-504. doi: 10.1165/rcmb.2008-0251OC
Schaafsma D, McNeill KD, Stelmack GL, et al. Insulin in-creases the expression of contractile phenotypic markers in air-way smooth muscle. Am J Physiol Cell Physiol. 2007; 293(1): C429- C439. doi: 10.1152/ajpcell.00502.2006
Schaafsma D, Gosens R, Ris JM, Zaagsma J, Meurs H, Nelemans SA. Insulin induces airway smooth muscle contrac-tion. Br J Pharmacol. 2007; 150(2): 136-142. doi: 10.1038/ sj.bjp.0706985
Numata T, Araya J, Fujii S, et al. Insulin-dependent phos-phatidylinositol 3-kinase/Akt and ERK signaling pathways inhibit TLR3-mediated human bronchial epithelial cell apop-tosis. J Immunol. 2011; 187(1): 510-519. doi: 10.4049/jimmu-nol.1004218
Romberger DJ, Pladsen P, Claassen L, Yoshida M, Beck-mann JD, Rennard SI. Insulin modulation of bronchial epithe-lial cell fibronectin in vitro. Am J Physiol. 1995; 268(2 Pt 1): L230-L238.
Papayianni M, Gourgoulianis KI, Molyvdas PA. Insulin NO-dependent action on airways smooth muscles. Nitric Ox-ide. 2001; 5(1): 72-76. doi: 10.1006/niox.2000.0317
Sadeghi-Hashjin G, Folkerts G, Henricks PA, et al. Induc-tion of guinea pig airway hyperresponsiveness by inactivation of guanylate cyclase. Eur J Pharmacol. 1996; 302(1-3): 109- 115.
Rada B, Boudreau HE, Park JJ, Leto TL. Histamine stimu-lates hydrogen peroxide production by bronchial epithelial cells via histamine H1 receptor and dual oxidase. Am J Respir Cell Mol Biol. 2014; 50(1): 125-134. doi: 10.1165/rcmb.2013-0254- OC
Huang HT, Guo JJ, Huang YH, Fu YS. Histamine-induced changes in rat tracheal goblet cell mucin store and mucosal ede-ma. Histochem Cell Biol. 2013; 139(5): 717-726. doi: 10.1007/ s00418-012-1060-y
Spicuzza L, Basile L, Belvisi MG, et al. The protective role of epithelium-derived nitric oxide in isolated bovine trachea. Pulm Pharmacol Ther. 2002; 15(4): 357-362. doi: 10.1006/ pupt.2002.0377
Gourgoulianis K, Iliodromitis Z, Hatziefthimiou A, Molyvdas PA. Epithelium-dependent regulation of airways smooth muscle function. A histamine-nitric oxide pathway. Mediators Inflamm. 1998; 7(6): 409-411. doi: http://dx.doi.org/10.1248/bpb.33.58
Sun P, Jin X, Koyama T, Li S, Kitamura Y, Kawasaki H. R-(-)-alpha-methylhistamine, a histamine H3 receptor agonist, induces endothelium-dependent vasodilation in rat mesenteric resistance arteries. Biol Pharm Bull. 2010; 33(1): 58-63. doi: http://dx.doi. org/10.1248/bpb.33.58
Thors B, Halldórsson H, Thorgeirsson G. eNOS activation me-diated by AMPK after stimulation of endothelial cells with hista-mine or thrombin is dependent on LKB1. Biochim Biophys Acta. 2011; 1813(2): 322-331. doi: 10.1016/j.bbamcr.2010.12.001
Gourgoulianis KI, Chatziparasidis G, Chatziefthimiou A, Molyvdas PA. Magnesium as a relaxing factor of airway smooth muscles. J Aerosol Med. 2001; 14(3): 301-307. doi: 10.1089/089426801316970259
Kitsiopoulou E, Hatziefthimiou AA, Gourgoulianis KI, Mo-lyvdas PA. Resting tension affects eNOS activity in a calcium-dependent way in airways. Mediators Inflamm. 2007; 24174.
Proskocil BJ, Sekhon HS, Jia Y et al. Acetylcholine is an au-tocrine or paracrine hormone synthesized and secreted by airway bronchial epithelial cells. Endocrinology. 2004; 145(5): 2498- 2506. doi: http://dx.doi.org/10.1210/en.2003-1728
Koyama S, Rennard SI, Robbins RA. Acetylcholine stimu-lates bronchial epithelial cells to release neutrophil and mono-cyte chemotactic activity. Am J Physiol. 1992; 262 (4 Pt 1): L466-L471.
Koyama S, Sato E, Nomura H, Kubo K, Nagai S, Izumi T. Acetylcholine and substance P stimulate bronchial epithelial cells to release eosinophil chemotactic activity. J Appl Physiol (1985). 1998; 84(5): 1528-1534.
Profita M, Bonanno A, Siena L, et al. Acetylcholine medi-ates the release of IL-8 in human bronchial epithelial cells by a NFkB/ERK-dependent mechanism Eur J Pharmacol. 2008; 582(1-3): 145-153. doi: 10.1016/j.ejphar.2007.12.029
Barnes PJ. Muscarinic receptors subtypes in airways. Eur Respir J. 1993; 6(3): 328-331.
Stamatiou R, Paraskeva E, Vasilaki A, Mylonis I, Molyvdas PA, Gourgoulianis K, Hatziefthimiou A. Long-term exposure to muscarinic agonists decreases expression of contractile pro-teins and responsiveness of rabbit tracheal smooth muscle cells. BMC Pulm Med. 2014;14: 39.
Gosens R, Zaagsma J, Meurs H, Halayko AJ. Muscarinic re-ceptor signaling in the pathophysiology of asthma and COPD. Respir Res. 2006; 7: e73. doi: 10.1186/1465-9921-7-73
Folkerts G, Kloek J, Geppetti P, Van der Linde HJ, Nijkamp FP. Factors that determine acetylcholine responsiveness of guinea pig tracheal tubes. Eur J Pharmacol. 2001; 420(2-3): 151-157. doi: 10.1016/S0014-2999(01)01016-0
Spicuzza L, Basile L, Belvisi MG, Bellofiore S, Matera MG, Cazzola M, Di Maria GU. The protective role of epithelium-de-rived nitric oxide in isolated bovine trachea. Pulm Pharmacol Ther. 2002; 15(4): 357-362.
Sparrow MP, Mitchell HW. Contraction of smooth muscle of pig airway tissues from before birth to maturity. J Appl Phys-iol (1985). 1990; 68(2): 468-477.
Chitano P, Cox CM, Murphy TM. Relaxation of guinea pig trachealis during electrical field stimulation increases with age. J Appl Physiol (1985). 2002; 92(5): 1835-1842. doi: 10.1152/ japplphysiol.00688.2001
Grunstein MM, Rosenberg SM, Schramm CM, Pawlowski NA. Mechanisms of action of endothelin 1 in maturing rabbit airway smooth muscle. Am J Physiol. 1991; 260(6 Pt 1): L434- 443.
Deoras KS, Wolfson MR, Searls RL, Hifler SR, Shaffer TH. Developmental changes in tracheal structure. Pediatr Res. 1991; 30(2): 170-175.doi: 10.1203/00006450-199108000-00010
Ramchandani R, Shen X, Elmsley CL, Ambrosius WT, Gunst SJ, Tepper RS. Differences in airway structure in im-mature and mature rabbits. J Appl Physiol (1985). 2000; 89(4): 1310-1316.
Colasurdo GN, Loader JE, Graves JP, Larsen GL. Matura-tion of nonadrenergic noncholinergic inhibitory system in nor-mal and allergen-sensitized rabbits. Am J Physiol. 1994; 267(6 Pt 1): L739-L744.
Murphy TM, Mitchell RW, Phillips IJ, Leff AR. Ontogenic expression of acetylcholinesterase activity in trachealis of young swine. Am J Physiol. 1991; 261(4 Pt 1): L322-L326
Jakupaj M, Martin RG, Dreshaj IA, Potter CF, Haxhiu MA, Ernsberger P. Role of endogenous NO in modulating airway con-traction mediated by muscarinic receptors during development. Am J Physiol. 1997; 273(3 Pt 1): L531-L536.
Sherman TS, Chen Z, Yuahanna IS, Lau KS, Margraf LR, Shaul PW. Nitric oxide synthase isoform expression in the de-veloping lung epithelium. Am J Physiol.1999; 276(2 Pt 1): L383- L390.
KouloumentaV,HatziefthimiouA,ParaskevaE,Gourgoulianis K, Molyvdas PA. Sexual dimorphism in airway responsiveness to sex hormones in rabbits Am J Physiol Lung Cell Mol Physiol. 2007; 293(2): L516.
Dahlman-Wright K, Cavailles V, Fuqua SA, et al. Interna-tional Union of Pharmacology. LXIV. Estrogen receptors. Phar-macol Rev. 2006; 58(4): 773-781.
Hibbert M, Lannigan A, Raven J, Landau L, Phelan P. Gen-der differences in lung growth. Pediatr Pulmonol. 1995; 19(2): 129-134.
Torday JS, Nielsen HC, Fencl Mde M, Avery ME. Sex differ-ences in fetal lung maturation. Am Rev Respir Dis. 1981; 123(2): 205-208.
Osman M. Therapeutic implications of sex differences in asthma and atopy. Arch Dis Child. 2003; 88(7): 587-590. doi: 10.1136/adc.88.7.587
Levesque BM, Vosatka RJ, Nielsen HC. Dihydrotestosterone stimulates branching morphogenesis, cell proliferation and pro-grammed cell death in mouse embryonic lung explants. Pediatr Res. 2000; 47(4 Pt 1): 481-491.
Wilson CM, McPhaul MJ. A and B forms of androgen receptor are expressed in a variety of human tissues. Mol Cell Endocrinol. 1996; 120(1): 51-57. doi: 10.1016/0303-7207(96)03819-1
Dashtaki R, Whorton AR, Murphy TM, Chitano P, Reed W, Kennedy TP. Dehydroepiandrosterone and analogs inhibit DNA binding of AP-1 and airway smooth muscle proliferation. J Phar-macol Exp Ther. 1998; 285(2): 876-883.
Stamatiou R, Paraskeva E, Papagianni M, Molyvdas PA, Hatziefthimiou A. The mitogenic effect of testosterone and 17β-estradiol on airway smooth muscle cells. Steroids. 2011; 76(4): 400-408. doi: 10.1016/j.steroids.2010.12.010
Pang JJ, Xu XB, Li HF, Zhang XY, Zheng TZ, Qu SY. Inhibition of beta-estradiol on trachea smooth muscle contraction in vitro and in vivo. Acta Pharmacol Sin. 2002; 23(3): 273-277.
Card JW, Voltz JW, Ferguson CD, et al. Male sex hormones promote vagally mediated reflex airway responsiveness to cho-linergic stimulation. Am J Physiol Lung Cell Mol Physiol. 2007; 292(4): L908-L914. doi: 10.1152/ajplung.00407.2006
Kouloumenta V, Hatziefthimiou A, Paraskeva E, Gourgoulianis K, Molyvdas PA. Non-genomic effect of tes-tosterone on airway smooth muscle. Br J Pharmacol. 2006; 149(8): 1083-1091. doi: 10.1038/sj.bjp.0706936
Bordallo J, de Boto MJ, Meana C, et al. Modulatory role of endogenous androgens on airway smooth muscle tone in isolated guinea-pig and bovine trachea; involvement of β2- adrenoceptors, the polyamine system and external calcium. Eur J Pharmacol. 2008; 601(1-3): 154-162. doi: 10.1016/j. ejphar.2008.10.039
Suárez L, Pipa M, Granda J, et al. Sex hormones modu-late salbutamol-elicited long-term relaxation in isolated bovine tracheal strips. Pharmacology. 2011; 87(5-6): 249-256. doi: 10.1159/000324315
Ma X, Li W, Stephens NL. Detection of two clusters of mechanical properties of smooth muscle along the airway tree. J Appl Physiol (1985). 1996; 80(3): 857-861.
Bai Y, Zhang M, Sanderson MJ. Contractility and Ca2+ sig-naling of smooth muscle cells in different generations of mouse airways. Am J Respir Cell Mol Biol. 2007; 36(1): 122-130. doi: 10.1165/rcmb.2006-0036OC
McKay KO, Wiggs BR, Paré PD, Kamm RD. Zero-stress state of intra- and extraparenchymal airways from human, pig, rabbit, and sheep lung. J Appl Physiol (1985). 2002; 92(3): 1261-1266. doi: 10.1152/japplphysiol.00131.2001
Goroumaru-Shinkai M, Yamamoto R, Funayama N, Ta-kayanagi I. Regional differences of the contractile responses to acetylcholine and neurokinin A in rabbit airway: heterogeneous distribution of the metabolic enzymes. Gen Pharmacol. 1992; 23(6): 1057-1061.
Maize DF, Fedan JS, Dey RD. Characterization of neural control and contractile function in airway smooth muscle of the ferret. Pulm Pharmacol Ther. 1998; 11(1): 57-64. doi: 10.1006/ pupt.1998.0117
Boucher RC Jr, Bromberg PA, Gatzy JT. Airway transepi-thelial electric potential in vivo: species and regional differenc-es. J Appl Physiol Respir Environ Exerc Physiol. 1980; 48(l): 169-176.
Mariassy AT, Plopper CG. Tracheobronchial epithelium of the sheep: I. Quantitative light-microscopic study of epithelial cell abundance, and distribution. Anat Rec. 1983; 205(3): 263-275.
Ballard ST, Schepens SM, Falcone JC, Meininger GA, Taylor AE. Regional bioelectric properties of porcine airway epithelium. J Appl Physiol (1985). 1992; 73(5): 2021-2027.
Al-Bazzaz FJ, Hafez N, Tyagi S, et al. Detection of Cl--HCO3- and Na+-H+ exchangers in human airways epithelium. JOP. 2001; 2(4 Suppl): 285-290.
Hay DW, Raeburn D, Fedan JS. Regional differences in re-activity and in the influence of the epithelium on canine intrapul-monary bronchial smooth muscle responsiveness. Eur J Pharma-col. 1987; 141(3): 363-370.
Hatziefthimiou A, Kiritsi M, Kiropoulou C, Vasilaki A, Sakellaridis N, Molyvdas PA. Regional differences in the mod-ulatory role of the epithelium in sheep airway. Clin Exp Phar-macol Physiol. 2009; 36(7): 668-674. doi: 10.1111/j.1440-1681- .2008.05131.x
Pratusevich VR, Seow CY, Ford LE. Plasticity in canine air-way smooth muscle. J Gen Physiol. 1995; 105(1): 73-94.
Kuo KH, Herrera AM, Wang L, Paré PD, Ford LE, Stephens NL, Seow CY. Structure-function correlation in airway smooth muscle adapted to different lengths. Am J Physiol Cell Physiol. 2003; 285(2): C384-C390. doi: 10.1152/ajpcell.00095.2003
Hatziefthimiou AA, Karetsi E, Pratzoudis E, Gourgoulianis KI, Molyvdas PA. Resting tension effect on airway smooth mus-cle: the involvement of epithelium. Respir Physiol Neurobiol. 2005; 145(2-3): 201-208. doi: 10.1016/j.resp.2004.06.004
Mehta D, Wu MF, Gunst SJ. Role of contractile protein ac-tivation in the lenght-dependent modulation of tracheal smooth muscle force. Am J Physiol. 1996; 270(1 Pt 1): C243-C252.
Gilbert EK, Weaver BA, Rembold CM. Depolarisation dec-reaces the [Ca2+]i sensitivity of myocin light-chain kinase in ar-terial smooth muscle: comparison of aequorin and fura 2 [Ca2+] i estimates. FASEB J. 1991; 5(11): 2593-2599.
Mandal TK. Inhaled insulin for diabetes mellitus. Am J Health Syst Pharm. 2005; 62(13): 1359-1364. doi: 10.1002/14651858. CD003890
Szczeklik A, Pieton R, Sieradzki J. Alternation in both insulin release and its hypoglycemic effects in atopic bronchial asthma. J Allergy Clin Immunol. 1980; 66(5): 424-427.
Gosens R, Zaagsma J, Meurs H, Halayko AJ. Muscarinic re-ceptor signaling in the pathophysiology of asthma and COPD. Respir Res. 2006; 7: 73.
Sherman TS, Chen Z, Yuahanna IS, Lau KS, Margraf LR, Shaul PW. Nitric oxide synthase isoform expression in the de-veloping lung epithelium. Am J Physiol. 1999; 276 (2 Pt 1): L383-L390.
Mhanna MJ, Dreshaj IA, Haxhiu MA, Martin RJ. Mecha-nism for subsance induced relaxation of precontracted airway smooth muscle during development. Am J Physiol. 1999; 276 (1 Pt 1): L51-L56. doi: 10.1203/00006450-199804001-01992
Semple PD, Beastall GH, Watson WS, Hume R. Serum testosterone depression associated with hypoxia in respiratory failure. Clin Sci (Lond). 1980; 58(1): 105-106.
Leifke E, Friemert M, Heilmann M, Puvogel N, Smaczny C, von zur Muhlen A, Brabant G. Sex steroids and body com-position in men with cystic fibrosis. Eur J Endocrinol. 2003; 148(5): 551-557. doi: 10.1530/eje.0.1480551
Semple PD, Beastall GH, Brown TM, Stirling KW, Mills RJ, Watson WS. Sex hormone suppression and sexual impo-tence in hypoxic pulmonary fibrosis. Thorax. 1984; 39(1): 46- 51.
Creutzberg EC, Casaburi R. Endocrinological disturbances in chronic obstructive pulmonary disease. Eur Respir J Suppl. 2003; 46: 76s-80s. doi: 10.1183/09031936.03.00004610
Kapsali T, Permutt S, Laube B, Scichilone N, Togias A. Potent bronchoprotective effect of deep inspiration and its ab-sence in asthma. J Appl Physiol (1985). 2000; 89(2): 711-720.
Scichilone N, Kapsali T, Permutt S, Togias A. Deep inspi-ration-induced bronchoprotection is stronger than bronchodila-tion. Am J Respir Crit Care Med. 2000; 162(3 Pt 1): 910-916. doi: 10.1164/ajrccm.162.3.9907048
Scichilone N, Permutt S, Togias A. The lack of the bron-choprotective and not the bronchodilatory ability of deep in-spiration is associated with airway hyperresponsiveness. Am J Respir Crit Care Med. 2001; 163(2): 413-419. doi: 10.1164/ ajrccm.163.2.2003119
Scichilone N, Marchese R, Catalano F, Vignola AM, Togias A, Bellia V. Bronchodilatory effect of deep inspiration is absent in subjects with mild COPD. Chest. 2004; 125(6): 2029-2035.
Downloads
Published
How to Cite
Issue
Section
License
This work is licensed under a Creative Commons Attribution 4.0 International License.
All content published in Pulmonary Research and Respiratory Medicine (PRRM) is licensed under the Creative Commons Attribution 4.0 International License (CC BY 4.0). This license allows anyone to copy, distribute, transmit, and adapt the work — including for commercial purposes — provided appropriate credit is given to the original author(s) and source.
