Portal de Periódicos da CAPES

The respiratory epithelium and airway smooth muscle homeostasis: its relevance to asthma

1994; Wiley; Volume: 24; Issue: 8 Linguagem: Inglês

10.1111/j.1365-2222.1994.tb00980.x

1365-2222

Darryl A. Knight, Geoffrey A. Stewart, Philip J. Thompson,

Neuroscience of respiration and sleep

Clinical & Experimental AllergyVolume 24, Issue 8 p. 698-706 The respiratory epithelium and airway smooth muscle homeostasis: its relevance to asthma D. A. KNIGHT, D. A. KNIGHT University Department of Medicine. Queen Elizabeth II. Medical Centre. NedlandsSearch for more papers by this authorG. A. STEWART, G. A. STEWART Institute for Child Health Research. Subiaco. Western Australia. AustraliaSearch for more papers by this authorP. J. THOMPSON, Corresponding Author P. J. THOMPSON University Department of Medicine. Queen Elizabeth II. Medical Centre. NedlandsDr P. J. Thompson, University Department of Medicine, Queen Elizabeth II Medical Centre, Nedlands 6009, Western Australia, AustraliaSearch for more papers by this author D. A. KNIGHT, D. A. KNIGHT University Department of Medicine. Queen Elizabeth II. Medical Centre. NedlandsSearch for more papers by this authorG. A. STEWART, G. A. STEWART Institute for Child Health Research. Subiaco. Western Australia. AustraliaSearch for more papers by this authorP. J. THOMPSON, Corresponding Author P. J. THOMPSON University Department of Medicine. Queen Elizabeth II. Medical Centre. NedlandsDr P. J. Thompson, University Department of Medicine, Queen Elizabeth II Medical Centre, Nedlands 6009, Western Australia, AustraliaSearch for more papers by this author First published: August 1994 https://doi.org/10.1111/j.1365-2222.1994.tb00980.xCitations: 18AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat References 1 Nadel JA. Cell to cell communication. Am Rev Respir Dis 1988; 138: s22–s23. 10.1164/ajrccm/138.6_Pt_2.S22 CASPubMedWeb of Science®Google Scholar 2 Widdicombe JH. Physiology of airway epithelium. In SG Farmer & DWP Hay eds. Airway epithelium: physiology, pathophysiology and pharmacology. New York , Marcel Dekker, 1991: 41–64. Google Scholar 3 Boushey HA Holtzman MJ, Sheller JR, Nadel JA. Bronchial hyperreactivity. Am Rev Respir Dis 1980; 121: 389–413. CASPubMedWeb of Science®Google Scholar 4 Beasley R, Roche WR. Roberts JA. Holgate ST. Cellular events in the bronchi in mild asthma and after bronchial provocation. Am Rev Respir Dis 1989; 139: 806–17. 10.1164/ajrccm/139.3.806 CASPubMedWeb of Science®Google Scholar 5 Laitinen LA, Heino M, Laitinen A, Kava T, Haahtela F. Damage to the airway epithelium and bronchial reactivity in patients with asthma. Am Rev Respir Dis 1985: 131: 599–606. CASPubMedWeb of Science®Google Scholar 6 Chung KF. Role of inflammation in the hyperreactivity of the airways in asthma. Thorax 1986; 41: 657–62. 10.1136/thx.41.9.657 CASPubMedWeb of Science®Google Scholar 7 Jeffery PK, Wardlaw AJ, Nelson FC. Collins JA. Kay AB. Bronchial biopsies in asthma; an ultrastructural quantitative study and correlation with hyperreactivity. Am Rev Respir Dis 1989; 140: 1745–53. 10.1164/ajrccm/140.6.1745 PubMedWeb of Science®Google Scholar 8 Flavahan NA, Aarhus LL, Rimele TJ, Vanhoutte PM. The respiratory epithelium inhibits bronchial smooth muscle tone. J Appl Physiol 1985; 58: 834–8. CASPubMedWeb of Science®Google Scholar 9 Hay DWP. Raeburn D, Farmer SG, Fleming WW. Fedan JS. Epithelium modulates the reactivity of ovalbuminsensitised guinea-pig airway smooth muscle. Life Sci 1986; 38: 2461–8. 10.1016/0024-3205(86)90617-X CASPubMedWeb of Science®Google Scholar 10 Barnes PJ, Cuss FM. Palmer JB. The effect of airway epithelium on smooth muscle contractility of bovine trachea. Br J Pharmacol 1985; 86: 685–91. 10.1111/j.1476-5381.1985.tb08946.x CASPubMedWeb of Science®Google Scholar 11 Raeburn DR. Hay DWP. Robinson VA et al. The effect of verapamil is reduced in isolated airway smooth muscle preparations lacking the epithelium. Life Sci 1986; 38: 809–16. 10.1016/0024-3205(86)90597-7 CASPubMedWeb of Science®Google Scholar 12 Goldie RG. Papadimitriou JM, Paterson JW, Rigby PJ. Self HM. Spina D. Influence of the epithelium on responsiveness of guinea-pig isolated trachea to contractile and relaxant agonists. Br J Pharmacol 1986; 87: 5–14. 10.1111/j.1476-5381.1986.tb10150.x CASPubMedWeb of Science®Google Scholar 13 Preuss JMH, Henry PJ, Goldie RG. Influence of age on epithelium-dependent responsiveness of guinea-pig and rat tracheal smooth muscle to spasmogens. Eur J Pharmacol 1992; 228: 3–8. CASPubMedWeb of Science®Google Scholar 14 Stuart-Smith K, Vanhoutte PM. Heterogeneity in the-effects of epithelium-removal in the canine bronchial tree. J Appl Physiol 1987; 63: 2510–5. CASPubMedWeb of Science®Google Scholar 15 Ullman A, Lofdahl C-G, Svedmyr N. Skoogh BE. Nerve stimulation releases mucosa-derived inhibitory factors, both prostanoids and non-prostanoids. in isolated ferret trachea. Am Rev Respir Dis 1990; 141: 748–57. 10.1164/ajrccm/141.3.748 CASPubMedWeb of Science®Google Scholar 16 Stuart-Smith K, Vanhoutte PM. Airway epithelium modulates the responsiveness of porcine bronchial smooth muscle. J Appl Physiol 1988; 65: 721–7. 10.1152/jappl.1988.65.2.721 CASPubMedWeb of Science®Google Scholar 17 Fernandes LB, Preuss JMH, Paterson JW. Goldie RG. Epithelium-derived inhibitory factor in human bronchus. Eur J Pharmacol 1990; 187: 331–6. 10.1016/0014-2999(90)90360-I CASPubMedWeb of Science®Google Scholar 18 Raeburn D, Hay DWP, Farmer SG, Fedan JS. Epithelium removal increases the reactivity of human isolated tracheal muscle to methacholine and reduces the effect of verapamil. Eur J Pharmacol 1986; 123: 451–3. 10.1016/0014-2999(86)90722-3 CASPubMedWeb of Science®Google Scholar 19 Knight DA, Adcock JA. Stewart GA, Thompson PJ. The effect of epithelium removal on human bronchial smooth muscle responsiveness to acetylcholine and histamine. Pulm Pharmacol 1990; 3: 198–202. 10.1016/0952-0600(90)90017-D CASPubMedGoogle Scholar 20 Knight DA, Phillips MJ, Stewart GA, Thompson PJ. The interaction of acetylcholine and histamine on human bronchial smooth muscle contraction. Eur Respir J 1991; 4: 985–91. CASPubMedWeb of Science®Google Scholar 21 Aizawa H, Miyaki N. Shigematsu N, Tomooka M. A possible role of airway epithelium in modulating hyperresponsiveness. Br J Pharmacol 1988; 93: 139–45. 10.1111/j.1476-5381.1988.tb11414.x CASPubMedWeb of Science®Google Scholar 22 Naline E, Devillier P, Drapeau G, Toty LF, Bakdach H, Regoli D. Advenier C. Characterisation of neurokinin effects and receptor selectivity in human isolated bronchi. Am Rev Respir Dis 1989; 140: 679–86. 10.1164/ajrccm/140.3.679 CASPubMedWeb of Science®Google Scholar 23 DeJongste JC, Mons H, Bonta IL, Kerrebijn KF. Non-neural components on the response of fresh human airways to electrical field stimulation. J Appl Physiol 1987; 63: 1558–66. CASPubMedWeb of Science®Google Scholar 24 Knight DA. The modulation of human bronchial smooth muscle contraction: Role of the epithelium and mediators of asthma. Ph.D. thesis, 1993: University of Western Australia, Perth , Western Australia . Google Scholar 25 Hay DWP. Raeburn D. Fedan JS. Regional differences in reactivity and in the influence of epithelium removal on canine intrapulmonary bronchial smooth muscle responsiveness. Eur J Pharmacol 1987; 141: 363–70. 10.1016/0014-2999(87)90553-X CASPubMedWeb of Science®Google Scholar 26 Farmer SG, Hay DWP. Airway epithelial modulation of smooth muscle function. The evidence for epithelium-derived inhibitory factor. In: SG Farmer & DWP Hay, eds. Airway epithelium: Physiology, pathophysiology and pharmacology. New York , Marcel Dekker, 1991: 437–83. Google Scholar 27 Advenier C, Devillier P, Matran R. Naline E. Influence of the epithelium on the responsiveness of guinea-pig isolated trachea to adenosine. Br J Pharmacol 1988; 93: 295–302. 10.1111/j.1476-5381.1988.tb11434.x CASPubMedWeb of Science®Google Scholar 28 Busk M, Vanhoutte PM. Theophylline causes the release of an epithelium-derived relaxing factor. FASEB J 1989; 3: A274. Google Scholar 29 Lundblad KAL, Persson CGA. The epithelium and the pharmacology of guinea-pig tracheal tone in vitro. Br J pharmacol 1988; 93: 909–17. 10.1111/j.1476-5381.1988.tb11479.x PubMedWeb of Science®Google Scholar 30 Farmer SG, Togo J. Effects of epithelium removal on relaxation of airway smooth muscle induced by vasoactive intestinal peptide and electrical field stimulation. Br J Pharmacol 1990; 100: 73–8. 10.1111/j.1476-5381.1990.tb12054.x CASPubMedWeb of Science®Google Scholar 31 Hulsmann AR, Jongejan RC, Raatgeep HR, Stijnen T, Bonta IL, Kerrebijn KF. DeJongste JC. Epithelium removal and peptidase inhibition enhance relaxation of human airways to vasoactive intestinal peptide. Am Rev Respir Dis 1993; 147: 1483–6. 10.1164/ajrccm/147.6_Pt_1.1483 CASPubMedWeb of Science®Google Scholar 32 Sparrow MP, Mitchell HW. Modulation by the epithelium of the extent of bronchial narrowing produced by substances perfused through the lumen. Br J Pharmacol 1991; 103: 1160–4. 10.1111/j.1476-5381.1991.tb12317.x CASPubMedWeb of Science®Google Scholar 33 Holroyde MC. The influence of the epithelium on the responsiveness of guinea-pig isolated trachea. Br J Pharmacol 1986; 87: 501–7. 10.1111/j.1476-5381.1986.tb10192.x CASPubMedWeb of Science®Google Scholar 34 Montefort S, Baker J, Roche WR, Holgate ST. The distribution of adhesive mechanisms in the normal bronchial epithelium. Eur Respir J 1993; 6: 1257–63. PubMedWeb of Science®Google Scholar 35 Undem BJ. Raible DG, Adkinson NF, Adams GK III. Effect of epithelium removal on antigen-induced smooth muscle contraction and mediator release from guinea-pig isolated trachea. J Pharmacol Exp Ther 1988; 244: 659–65. CASPubMedWeb of Science®Google Scholar 36 Gao Y, Vanhoutte PM. Removal of the epithelium potentiates acetylcholine in depolarizing canine bronchial smooth muscle. J Appl Physiol 1988; 65: 2400–5. CASPubMedWeb of Science®Google Scholar 37 Laitinen A. Ultrastructural organisation of intra-epithelial nerves in the human airway tract. Thorax 1985: 40: 488–92. 10.1136/thx.40.7.488 PubMedWeb of Science®Google Scholar 38 Barnes PJ. Asthma as an axon reflex. Lancet 1986; 1: 242–5. 10.1016/S0140-6736(86)90777-4 CASPubMedWeb of Science®Google Scholar 39 Ollerenshaw SL, Jarvis D, Sullivan CE, Woolcock AJ. Substance-P immunoreactive nerves in airways from asthmatics and non-asthmatics. Eur Respir J 1991; 4: 673–82. PubMedWeb of Science®Google Scholar 40 MacDonald DM. Neurogenic inflammation in the respiratory tract: Actions of sensory nerve mediators on blood vessels and epithelium of airway mucosa. Am Rev Respir Dis 1987; 136: s65–s72. 10.1164/ajrccm/136.6_Pt_2.S65 PubMedWeb of Science®Google Scholar 41 Frossard N, Rhoden KJ, Barnes PJ. Influence of the epithelium on airway responses to tachykinins: role of endopeptidase and cyclooxygenase. J Pharmacol Exp Ther 1989: 248: 292–8. CASPubMedWeb of Science®Google Scholar 42 Devillier P, Advenier C. Drapeau G, Marsac J, Regoli D. Comparison of the effects of epithelium removal and of an enkephalinase inhibitor on the neurokinin-induced contraction of guinea-pig bronchus. Br J Pharmacol 1988; 94: 675–84. 10.1111/j.1476-5381.1988.tb11575.x CASPubMedWeb of Science®Google Scholar 43 Sekizawa K, Tamioki J, Graf PD, Basbaum CB, Borson DB, Nadel JA. Enkephalinase inhibitor potentiates mammalian tachykinin-induced contraction in ferret trachea. J Pharmacol Exp Ther 1987; 243: 1211–17. CASPubMedWeb of Science®Google Scholar 44 Honda I. Kohrogi H, Yamaguchi T, Ando M, Araki S. Enkephalinase inhibitor potentiates substance P and capsaicin-induced bronchial smooth muscle contractions in humans. Am Rev Respir Dis 1991; 143: 1416–18. 10.1164/ajrccm/143.6.1416 CASPubMedWeb of Science®Google Scholar 45 Lindstrom FG, Andersson RGG, Granerus G. Grundstrom N. Is the airway epithelium responsible for histamine metabolism in the trachea of guinea pigs Agents and Actions 1991; 33: 170–2. 10.1007/BF01993158 CASPubMedWeb of Science®Google Scholar 46 Yamauchi K, Nakazawa H, Sekizawa K, Ohkawara Y, Hiroki H, Okayama M. Tamura G, Tanno Y, Suzuki H, Shibihara S, Maeyama K. Watanabe T, Takamura M, Sasaki H, Takishima T, Shirato K. The regulatory role of histamine-N-methyltransferase in allergic reactions m the human airways. Am Rev Respir Dis 1993; 147: A431. Web of Science®Google Scholar 47 Fernandes LB, Knight DA, Rigby PJ, Spina D, Paterson JW. Goldie RG. β-adrenoceptor desensitization in guinea-pig isolated trachea. Eur J Pharmacol 1988: 157: 135–45. 10.1016/0014-2999(88)90376-7 CASPubMedWeb of Science®Google Scholar 48 Goldie RG. Paterson JW, Spina D, Wade J. Classification of β-adrenoceptors in human isolated bronchus. Br J Pharmacol 1984; 81: 611–15. 10.1111/j.1476-5381.1984.tb16125.x CASPubMedWeb of Science®Google Scholar 49 Omini C, Abbracchio MP, Coen E, Daffonchio L, Fano M, Cattabeni F. Involvement of arachidonic acid metabolites in β-adrenoceptor desensitization: functional and biochemical studies. Eur J Pharmacol 1984; 106: 601–6. 10.1016/0014-2999(84)90064-5 CASPubMedWeb of Science®Google Scholar 50 Goldie RG, Spina D, Henry PJ, Lulich KM, Paterson JW. In vitro responsiveness of human asthmatic bronchus to carbachol, histamine, β-adrenoceptor agonists and theophylline. Br J Clin Pharmacol 1986; 22: 669–76. 10.1111/j.1365-2125.1986.tb02956.x CASPubMedWeb of Science®Google Scholar 51 Foreman JC, Norris JM, Rising TJ, Webber SE. The binding of 3H-tiotidine to homogenates of guinea-pig lung parenchyma. Br J Pharmacol 1985: 86: 475–82. 10.1111/j.1476-5381.1985.tb08917.x CASPubMedWeb of Science®Google Scholar 52 Knight DA, Stewart GA, Thompson PJ. Histamine tachyphylaxis in human airway smooth muscle: The role of H2 receptors and the epithelium. Am Rev Respir Dis 1992; 146: 137–40. 10.1164/ajrccm/146.1.137 CASPubMedWeb of Science®Google Scholar 53 Knight DA. Garlepp MJ, Peroni DJ. Stewart GA, Thompson PJ. Tissue distribution of histamine H2 receptor mRNA in human lung. XV meeting of The International Association of Allergology and Clinical Immunology, Stockholm, 1994. Published in proceedings. Google Scholar 54 Knight DA, Thompson PJ, Stewart GA. PGE2 but not PGI2 accounts for the inhibitory effect of prostaglandins in histamine tachyphylaxis on human bronchial smooth muscle. Am Rev Respir Dis 1993; 147: A449. Web of Science®Google Scholar 55 Abdolrasulnia R. Shepherd VL. Purification of Type I and Type II Tumor necrosis factor receptors from human lung tissue. Am J Respir Cell Mol Biol 1992; 7: 42–8. 10.1165/ajrcmb/7.1.42 CASPubMedWeb of Science®Google Scholar 56 Marini M, Soloperto M, Mezzetti M. Fasoli A, Mattoli S. Interleukin-1 binds to specific receptors on human bronchial epithelial cells and upregulates granulocyte-macrophage colony stimulating factor synthesis and release. Am J Respir Cell Mol Biol 1991: 4: 519–24. 10.1165/ajrcmb/4.6.519 CASPubMedWeb of Science®Google Scholar 57 Calhoun WJ, Kelley J. Cytokines in the respiratory tract. In KF Chung, PJ Barnes (eds). Pharmacology of the respiratory tract: Experimental and clinical research, New York : Marcel Dekker, 253–89. Google Scholar 58 Hollenberg SM, Cunnion RE, Purillo JE. The effect of tumour necrosis factor on Vascular smooth muscle: In vitro studies using rat aortic rings. Chest 1991; 100: 1133–7. 10.1378/chest.100.4.1133 CASPubMedWeb of Science®Google Scholar 59 Silberstein DS, Owen WF, Gasson JC, DiPersio JF, Golde DW, Bina JC, Soberman R, Austen KF, David JR. Enhancement of human eosinophil cytotoxicity and leukotriene synthesis by biosynthetic (recombinant) granulocyte/ macrophage colony stimulating factor. J Immunol 1986; 137: 3290–4. CASPubMedWeb of Science®Google Scholar 60 Kelley J. Transforming growth factor β. In J Kelley (ed), Cytokines of the lung. New York , Marcel Dekker, 101–37. Google Scholar 61 Gosset P, Tsciopoulos A, Wallaert B et al., Increased secretion of tumour necrosis factor α and interleukin-6 by alveolar macrophages consecutive to the late asthmatic reaction. J All Clin Immunol 1991; 88: 561–71. 10.1016/0091-6749(91)90149-I PubMedWeb of Science®Google Scholar 62 Marini M, Vittori E, Hllemborg J, Mattoli S. Expression of the potent inflammatory cytokines, granulocyte-macrophage-stimulating factor and interleukin-6 and interleukin-8 in bronchial epithelial cells of patients with asthma. J Allergy Clin Immunol 1992; 89: 1001–9. 10.1016/0091-6749(92)90223-O PubMedWeb of Science®Google Scholar 63 Frasier-Scott K. Hatzakis H, Seong D, Jones CM, Wu KK. Influence of natural and recombinant interleukin-2 on endothelial cell arachidonate metabolism. J Clin Invest 1988: 82: 1877–83. 10.1172/JCI113805 CASPubMedWeb of Science®Google Scholar 64 Holtzman MJ. Arachidonic acid metabolism: Implications of biological chemistry for lung function and disease. Am Rev Respir Dis 1991; 143: 188–203. 10.1164/ajrccm/143.1.188 CASPubMedWeb of Science®Google Scholar 65 Eling TE, Henke D, Danilowicz RM. Arachidonic acid metabolism in respiratory epithelial cells. Gen Pharmacol 1988; 19: 313–6. 10.1016/0306-3623(88)90022-5 CASPubMedWeb of Science®Google Scholar 66 Wills-Karp M, Jinot J, Lee F, Hirata F. Interleukin-1 alters guinea-pig tracheal smooth muscle responsiveness to β-adrenergic stimulation. Eur J Pharmacol 1990; 83: 1185. 10.1016/0014-2999(90)94275-3 Web of Science®Google Scholar 67 van Oosterhout AJM, Stam WB, Vanderschueren RGJRJ, Nijkamp FP. Effects of cytokines on β-adrenoceptor function of human peripheral blood mononuclear cells and guinea pig trachea. J Allergy Clin Immunol 1992; 90: 340–8. 10.1016/S0091-6749(05)80013-2 PubMedWeb of Science®Google Scholar 68 Bloomquist EI, Kream RM. The mucosa mediates tachyphylaxis to leukotrienes C4, D4, E4 in guinea pig trachea. Eur J Pharmacol 1988; 150: 185–8. 10.1016/0014-2999(88)90767-4 CASPubMedWeb of Science®Google Scholar 69 Anderson WH, Krzanowski .JJ, Polson JB, Szentivanyi A Effect of PGE2 on histamine-stimulated calcium mobilisation as a possible mechanism of histamine tachyphylaxis in canine tracheal smooth muscle. Naunyn-Schmeidebergs Arch Pharmacol 1983; 32: 72–7. 10.1007/BF00649355 Web of Science®Google Scholar 70 Farmer SG, Hay DWP, Raeburn D, Fedan JS. Relaxation of guinea-pig tracheal smooth muscle to arachidonate is converted to contraction following epithelium removal. Br J Pharmacol 1987; 92: 231–6. 10.1111/j.1476-5381.1987.tb11316.x CASPubMedWeb of Science®Google Scholar 71 Tschirhart E, Frossard N, Bertrand C, Landry Y. Arachidonic acid metabolites and airway epithelium-dependent relaxant factor. J Pharmacol Exp Ther 1987; 243: 310–16. CASPubMedWeb of Science®Google Scholar 72 Butler GB, Adler KB, Evans JN. Morgan DW, Szarek JL. Modulation of rabbit airway smooth muscle responsiveness by respiratory epithelium. Am Rev Respir Dis 1987; 135: 1099–104. CASPubMedWeb of Science®Google Scholar 73 Stuart-Smith K, Vanhoutte PM. Arachidonic acid evokes epithelium-dependent relaxations in canine airways. J Appl Physiol 1988: 65: 2170–80. CASPubMedWeb of Science®Google Scholar 74 Raeburn D, Sequeira DJ, Baekes WL. Possible involvement of cytochrome P450 in the epithelium modulated response to methacholine in guinea-pig trachea. Biochem Pharmacol 1988: 37: 573–6. 10.1016/0006-2952(88)90127-X CASPubMedWeb of Science®Google Scholar 75 Gray PR, Derksen FJ, Robinson NE, Slocombe RF, Peters-Golden ML. Epithelial strips: An alternative technique for examining arachidonate metabolism in equine tracheal epithelium. Am J Respir Cell Mol Biol 1992; 6: 29–36. 10.1165/ajrcmb/6.1.29 CASPubMedWeb of Science®Google Scholar 76 Tschirhart E, Landry Y. Airway epithelium releases a relaxant factor: Demonstration with substance-P. Eur J Pharmacol 1986; 132: 103–4. 10.1016/0014-2999(86)90020-8 CASPubMedWeb of Science®Google Scholar 77 Fernandes LB, Paterson JW, Goldie RG. Co-axial bioassay of a smooth muscle relaxant factor released from guinea-pig tracheal epithelium. Br J Pharmacol 1989; 96: 117–24. 10.1111/j.1476-5381.1989.tb11791.x CASPubMedWeb of Science®Google Scholar 78 Guc MO, Ilhan M. Kayaalp SO. The rat anococcygeus muscle is a convenient bioassay organ for epithelium-derived relaxing factor. Eur J Pharmacol 1988; 148: 405–9. 10.1016/0014-2999(88)90119-7 CASPubMedWeb of Science®Google Scholar 79 Munakata M, Mitzner W. Menkes H. Osmotic stimuli induces the epithelial-dependent relaxation of the guinea pig trachea. J Appl Physiol 1988; 64: 466–71. 10.1152/jappl.1988.64.1.466 PubMedWeb of Science®Google Scholar 80 Gunn LK, Piper PJ. Potential sources of artefact in the coaxial bioassay. Eur J Pharmacol 1991; 203: 405–552. 10.1016/0014-2999(91)90898-Z CASPubMedWeb of Science®Google Scholar 81 Spina D, Fernandas LB, Preuss JMH, Hay DWP, Muccitelli RM. Page CP, Goldie RG. Evidence that epithelium-dependent relaxation of vascular smooth muscle detected by coaxial bioassay is not attributable to hypoxia. Br J Pharmacol 1992; 105: 799–804. 10.1111/j.1476-5381.1992.tb09060.x CASPubMedWeb of Science®Google Scholar 82 Munakata M, Masaki Y, Sakuma I. Pharmacological differentiation of epithelium-derived relaxing factor from nitric oxide. J Appl Physiol 1990: 69: 665–70. 10.1152/jappl.1990.69.2.665 CASPubMedWeb of Science®Google Scholar 83 Palmer RJ, Ferridge AG, Moncada S. Nitric oxide accounts for the biological activity of endothelium-derived relaxant factor, Nature 1987; 327: 524–6. 10.1038/327524a0 CASPubMedWeb of Science®Google Scholar 84 Lorenz RR. Gao Y, Vanhoutte PM The effect of epithelium removal on airway contractility is not mediated by arachidonic acid metabolites or nitric oxide. Physiologist 1988; 31: A124. Google Scholar 85 Gao Y, Vanhoutte PM. Attenuation of contractions to acetylcholine in canine bronchi by an endogenous nitric oxide-like substance. Br J Pharmacol 1993; 109: 887–91. 10.1111/j.1476-5381.1993.tb13658.x CASPubMedWeb of Science®Google Scholar 86 Kobzik L, Bredt DS. Lowenstein CJ, Drazen J, Gaston B. Sugarbaker D, Stamler JS. Nitric oxide synthase in human and rat lung: Immunocytochemical and histochemical localisation. Am J Respir Cell Mol Biol 1993: 9: 371–77. 10.1165/ajrcmb/9.4.371 CASPubMedWeb of Science®Google Scholar 87 Hamid Q, Springall DR. Riveros-Moreno V et al. Induction of nitric oxide synthase in asthma. Lancet 1993: 342: 1510–13. 10.1016/S0140-6736(05)80083-2 CASPubMedWeb of Science®Google Scholar 88 Ellis JL. Undem BJ. Inhibition by L-NG-Nitro-L-Arginine of nonadrenergic-noncholinergic-mediated relaxations of human isolated central and peripheral airways. Am Rev Respir Dis 1992; 146: 1543–7. 10.1164/ajrccm/146.6.1543 PubMedWeb of Science®Google Scholar 89 Li CG, Rand MJ. Evidence that part of the NANC relaxant response of guinea-pig trachea to electrical field stimulation is mediated by nitric oxide. Br J Pharmacol 1991: 102: 91–4. 10.1111/j.1476-5381.1991.tb12137.x CASPubMedGoogle Scholar 90 Tucker JF, Brave SR. Charanlambous L, Hobbs AJ, Gibson A. L-NG-nitroarginine inhibits non-adrenergic non-cholinergic relaxations of guinea-pig isolated tracheal smooth muscle. Br J Pharmacol 1990; 100: 663–4. 10.1111/j.1476-5381.1990.tb14072.x CASPubMedWeb of Science®Google Scholar 91 Bai TR, Bramley AM, Schellenberg RR, Pare PD. Nitric oxide mediates non-adrenergic non-cholinergic inhibitory neural responses in human bronchial smooth muscle. Am Rev Respir Dis 1992; 145: A383. Google Scholar 92 Belvisi MG, Stretton D, Verleden GM, Yacoub MH, Barnes PJ. Nitric oxide is the endogenous neurotransmitter of bronchodilator nerves in humans. Eur J Pharmacol 1992; 210: 221–2. 10.1016/0014-2999(92)90676-U CASPubMedWeb of Science®Google Scholar 93 Jorens PG, Vermiere PA, Herman AG. L-arginine dependent nitric oxide synthase: A new metabolic pathway in the lung and airways. Eur Respir J 1993; 6: 258–66. CASPubMedWeb of Science®Google Scholar 94 Moncada S. Higgs A. The L-Arginine-Nitric oxide pathway. N Engl J Med 1993; 329: 2002–12. 10.1056/NEJM199312303292706 CASPubMedWeb of Science®Google Scholar Citing Literature Volume24, Issue8August 1994Pages 698-706 ReferencesRelatedInformation