Abstract
Autonomic nerves regulate several aspects of airway function [1]. However, for the purposes of this chapter, we will focus on the role of nitric oxide (NO)-containing nerves in the control of airway smooth muscle function. Neural control of airway smooth muscle is very complex since in addition to cholinergic and adrenergic innervation there is a non-adrenergic non-cholinergic (NANC) innervation. The existence of a NANC nervous system in the gastrointestinal tract, which controls gut motility, sphincters and secretions had previously been established in vertebrates from fish to humans [2]. The airways develop embryologically from the foregut and so the existence of NANC nerves in the respiratory tract was not an unexpected finding.
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References
Barnes PJ (1992) Modulation of neurotransmission in airways. Physiological Reviews 72: 699–729
Burnstock G (1972) Purinergic nerves. Pharmacol Rev 24: 247–324
Belvisi MG, Bai TR (1994) Inhibitory non-adrenergic non-cholinergic innervation of airways smooth muscle: Role of nitric oxide. In: Raeburn D, Giemybycz MA (eds) Airways Smooth Muscle: Structure, Innervation and Neurotransmission. Basel: Birkhauser Verlag, 157–187
Belvisi MG, Ward JK, Mitchell JA, Barnes PJ (1995) Nitric oxide as neurotransmitter in human airways. Archives Internationales de Pharmacodynamie et Therapie 329: 97–110
Ellis JL, Undem BJ (1994) Pharmacology of non-adrenergic, non-cholinergic nerves in airway smooth muscle. Pulmonary Pharmacology 7: 205–223
Mann SP (1971) The innervation of mammalian bronchial smooth muscle, the localisation of catechol amines and cholinesterases. Histochem J 3: 319–331
Richardson J, Beland J (1976) Non-adrenergic inhibitory nervous system in human airways. J Appl Physiol 41: 764–771
Barnes PJ (1986) Neural control in health and disease. Am Rev Respir Dis 134: 1289–1314
Burnstock G, Wood MJ (1967) Innervation of the lungs of the sleepy lizard (Trachysaurus regosus). II. Physiology and pharmacology. Comp Biochem Physiol 22: 815–831
Wood MJ, Burnstock G (1967) Innervation of the lungs of the toad (Bufo marinus). I. Physiology and Pharmacology. Comp Biochem Physiol 22: 755–766
Robinson PM, Mclean JR, Burnstock G (1971) Ultrastructural identification of nonadrenergic inhibitory nerve fibres. J Pharmacol Exp Ther 179: 149–160
Berger PJ (1973) Autonomic innervation of the visceral and vascular smooth muscle of the lizard lung. Comp Gen Pharmacol 4: 1–10
Burnstock G (1975) Comparative studies of purinergic nerves. J Exp Zool 194: 103–134
Fedde MR, Burger RE, Kitchell R (1961) The influence of the vagus nerve on respiration. Poult Sci 40: 1401–1407
Cook RD, King AS (1969) Observations on the ultrastructure of the smooth muscle and its innervation in the avian lung. J Anat 105: 202–208
Richardson JB (1979) Nerve supply to the lungs. Am Rev Respir Dis 119: 785–802
Richardson JB, Beland J (1976) Nonadrenergic inhibitory nervous system in human airways. J Appl Physiol 41: 764–771
Bando TX, Shindo N, Shimo Y (1973) Non-adrenergic inhibitory nerves in tracheal smooth muscle in guinea-pig. Proc J Physiol Soc Jpn 35: 508–509
Coburn RF, Tomita T (1973) Evidence for nonadrenergic inhibitory nerves in the guinea-pig trachealis muscle. Am J Physiol 224: 1072–1080
Coleman RA (1973) Evidence for a non-adrenergic inhibitory nervous pathway in guinea-pig trachea. Br J Pharmacol 48: 360–361
Coleman RA, Levy GP (1974) A non-adrenergic inhibitory nervous pathway in guinea-pig trachea. Br J Pharmacol 52: 167–174
O’Donnell SR, Saar N (1973) Histochemical localisation of adrenergic nerves in the guinea-pig trachea. Br J Pharmacol 47: 707–710
Kalenburg S, Satchell DG (1979) The inhibitory innervation of the guinea-pig trachea: a study of its adrenergic and non-adrenergic components. Clin Exp Pharmacol Physiol 6: 53–64
Richardson JB, Bouchard T (1975) Demonstration of a non-adrenerigc inhibitory nervous system in the trachea of the guinea-pig. J Allergy Clin Immunol 56: 473–480
Yip P, Palambini B, Coburn RF (1981) Inhibitory innervation of the guinea-pig trachealis muscle. J Appl Physiol 50: 373–382
Hammarström M, Sjöstrand NO (1979) Pathways for excitatory and inhibitory innervation to the guinea-pig tracheal smooth muscle. Experimentia 35: 64–65
Taylor JF, Paré PD, Schellenburg RR (1984) Cholinergic and non-adrenergic mechanisms in human and guinea-pig airways. J Appl Physiol 56: 958–965
Chesrown SE, Venugoplan CS, Gold WM, Drazen JM (1980) In vivo demonstration of non-adrenergic inhibitory innervation of the guinea-pig trachea. J Clin Invest 65: 314–320
Canning BJ, Undem BJ (1993) Relaxant innervation of the guinea-pig trachealis: demonstration of capsaicin-sensitive and insensitive vagal pathways. JPhysiol 460: 719–739
Satchell D (1982) Non-adrenergic non-cholinergic nerves in mammalian airways: their function and the role of purines. Comp Biochem Physiol 72: 189–196
Doidge JM, Satchell DG (1982) Adrenergic and nonadrenergic inhibitory nerves in mammalian airways. J Autonomic Nervous System 5: 83–99
Suzuki H, Morita K, Kuriyama H (1976) Innervation and properties of the smooth muscle of the dog trachea. Jpn JPhysiol 26: 303–320
Russell J (1980) Noradrenergic inhibitory innervation of canine airways. J Appl Physiol 48: 16–22
Kannan MS, Daniel EE (1980) Structural and functional study of control of canine tracheal smooth muscle. Am JPhysiol 238: C27–C33
Altiere RJ, Szarek JL, Diamond L (1984) Neural control of relaxation in cat airways smooth muscle. J Appl Physiol 57: 1536–1544
Diamond L, O’Donnell M (1980) A non-adrenergic vagal inhibitory pathway to feline airway. Science 208: 185–188
Irvin CG, Boileau R, Tremblay J, Martin RR, Macklem PT (1980) Bronchodilatation: Noncholinergic, nonadrenergic mediation demonstrated in vivo in the cat. Science 207: 791–792
Szarek JL, Gillespie MN, Altiere RJ, Diamond L (1986) Reflex activation of the nonadrenergic non-cholinergic inhibitory system in feline airway. Am Rev Respir Dis 133: 159–162
Inoue H, Ichinose M, Miura M, Katsumata U, Takishima T (1989) Sensory receptors and reflex pathways of non-adrenergic inhibitory nervous system in feline airway. Am Rev Respir Dis 139: 1175–1178
Sheller JR, Brigham KL (1982) Bronchomotor responses of isolated sheep airways to electrical field stimulation. J Appl Physiol 53: 1088–1093
Leff AR, Munoz NM, Tallet J, David AC, Cavigelli MA, Garrity ER (1985) Autonomic response characteristics of porcine airway smooth muscle in vivo. J Appl Physiol 58: 1176–1188
Kannan MS, Johnson DE (1992) Functional innervation of pig tracheal smooth muscle: neural and non-neural mechanisms of relaxation. J Pharmacol Exp Ther 260: 1180–1184
Cameron AR, Johnston CF, Kirkpatrick CT, Kirkpatrick MCA (1983) The quest for the inhibitory neurotransmitter in bovine tracheal smooth muscle. Q J Exp Physiol 68: 413–426
Broadstone RV, Leblanc PH, Derksen FJ, Robinson NE (1991) In vitro responses of airway smooth muscle from horses with recurrent airway obstruction. Pulm Pharmacol 4: 191–202
Yu M, Wang Z, Robinson NE, Leblanc PH (1994) Inhibitory nerve distribution and media-tion of NANC relaxation by nitric oxide in horse airways. J Appl Physiol 76: 339–344
Middendorf WF, Russell JA (1980) Innervation of airway smooth muscle in the baboon: evidence for a nonadrenergic inhibitory system. J Appl Physiol Respir Environ Exercise Physiol 48: 947–956
Richardson JB (1981) Nonadrenergic inhibitory innervation of the lung. Lung 159: 315–322
Rikimaru A, Sudoh M (1971) Innervation of the smooth muscle of the guinea-pig trachea. Jpn J Smooth Muscle Res 7: 35–44
Foster RW, O’Donnell SR (1975) Evidence that adrenergic nerves are responsible for the active uptake of norepinephrine in the guinea-pig isolated trachea. Br J Pharmacol 53: 109–112
Ind PW (1994) Role of the sympathetic nervous system and endogenous catecholamines in the regulation of airways smooth muscle tone. In: Raeburn D, Giembycz MA (eds) Airway Smooth Muscle: Structure, Innervation and Neurotransmission. Basel: Birkhauser Verlag, 29–41
Davis C, Kannan MS, Jones TR, Daniel EE (1982) Control of human enzyme smooth muscle: in vitro studies. J Appl Physiol 53: 1080–1087
Palmer JBD, Cuss FMC, Barnes PJ (1986) VIP and PHM and their role in non-adrenergic inhibitory responses in isolated human airways. J Appl Physiol 61: 1322–1328
Ellis JL, Undem BJ (1992) Inhibition by L-NG-nitro-L-arginine of nonadrenergic noncholinergic relaxations of human isolated central and peripheral airways. Am Rev Respir Dis 146: 1543–1547
Ward JK, Barnes PJ, Springall DR, Abelli L, Tadjkarimi S, Yacoub MH et al (1995) Distribution of human i-NANC bronchodilator and nitric oxide-immunoreactive nerves. Am J Respir Cell Mol Biol 13: 175–184
Michoud M-C, Amyot R, Jeanneret-Grosjean A, Couture J (1988) Reflex decrease of histamine-induced bronchoconstriction after laryngeal stimulation in humans. Am Rev Respir Dis 136: 616–622
Lammers J-W, Minette M, McCusker M, Chung KF, Barnes PJ (1988) Nonadrenergic bronchodilator mechanisms in normal human subjects in vivo. J Appl Physiol 64: 1817–1822
Ichinose M, Inoue H, Miura M, Takishima T (1988) Nonadrenergic bronchodilation in normal subjects. Am Rev Respir Dis 138: 31–34
Fuller RW, Dixon CMS, Barnes PJ (1985) The bronchoconstrictor response to inhaled capsaicin in humans. J Appl Physiol 85: 1080–1085
Irvin CG, Martin RR, Macklem PT (1982) Nonpurinergic nature and efficacy of nonadrenergic bronchodilation. J Appl Physiol 52: 562–569
Hutás I, Hádhazy P, Debreczeni L, Vizi ES (1981) Relaxation of human isolated bronchial smooth muscle. Lung 159: 153–161
Barnes PJ, Baraniuk JN, Belvisi MG (1991) Neuropeptides in the respiratory tract. Am Rev Respir Dis 144: 1187–1198
Burnstock G, Campbell G, Satchell DG, Smythe A (1970) Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut. Br J Pharmacol 40: 668–675
Sundler F, Ekblad E, Grunditz T, Håkanson R, Uddman R (1988) Vasoactive intestinal peptide in the peripheral nervous system. Ann New York Acad Sci 527: 143–167
Uddman R, Alumets J, Densert O, Hålånson R, Sundler F (1978) Occurrence and distribution of VIP nerves in the nasal mucosa and tracheobronchial wall. Acta Otolaryngol 86: 443–448
Dey RD, Shannon WA, Said SI (1981) Localisation of VIP-immunoreactive nerves in airways and pulmonary vessels of dogs, cats and human subjects. Cell Tissue Res 220: 231–238
Ghatei MA, Sheppard MN, 0’ Shaughnessy DJ, Adrian TE, McGregor GP, Polak JM et al (1982) Regulatory peptides in the mammalian respiratory tract. Endocrinology 111: 1248–1254
Lundberg JM, Fahrenkrug J, Hökfelt T (1984) Co-existence of peptide histidine isoleucine (PHI) and VIP in nerves regulating blood flow and bronchial smooth muscle tone in various mammals including man. Peptides 5: 593–598
Laitinen A, Partanen M, Hervonen A, Pelto-Huikko M, Laitinen LA (1985) VIP-like immunoreactive nerves in human respiratory tract. Histochemistry 82: 313–319
Uddman R, Sundler F (1987) Neuropeptides in the airways: a review. Am Rev Respir Dis 136: S3–8
Dey RD, Hoffpauir J, Said SI (1988) Co-localisation of vasoactive intestinal peptide-and substance P-containing nerves in cat bronchi. Neuroscience 24: 275–281
Dey RD, Altemus JB, Michalkiewicz M (1991) Distribution of vasoactive intestinal peptide-and substance P-containing nerves originating nerves originating from neurons of airway ganglia in cat bronchi. J Comp Neurol 304: 330–340
Bowden JJ, Gibbins IL (1992) Vasoactive intestinal peptide and neuropeptide Y co-exist in non-noradrenergic sympathetic neurons to guinea-pig trachea. J Autonomic Nervous System 38: 1–20
Belvisi MG, Stretton CD, Miura M, Verleden GM, Tadjkarimi S, Yacoub MH et al (1992) Inhibitory NANC nerves in human tracheal smooth muscle: a quest for the neurotransmitter. J Appl Physiol 73: 2505–2510
Ito Y, Takeda K (1982) Non-adrenergic inhibitory nerves and putative neurotransmitters in the smooth muscle of cat trachea. J Physiol 330: 497–511
Altiere RJ, Diamond L (1984) Comparison of vasoactive intestinal peptide and isoproterenol relaxant effects in isolated cat airways. J Appl Physiol 56: 986–992
Bai TR, Bramley AM (1993) Effect of an inhibitor of nitric oxide synthase on neural relaxation of human bronchi. Am J Physiol: Lung Cell Mol Physiol 8: L425–L430
Waelbroeck M, Robberecht P, Coy DH, Camus J-C, De Neef P, Christophe J (1985) Interaction of growth hormone-releasing factor (GRF) and 14 GRF analogues with vasoactive intestinal peptide (VIP) receptors of rat pancreas. Discovery of [AC-Tyr1, D-Phe2]GRF(1–29)-NH2 as a VIP antagonist. Endocrinol 116: 2643–2649
Pandol SJ, Dharmsathaphorn K, Schoeffield MS, Vale W, Rivier J (1986) Vasoactive intestinal peptide receptor antagonist [4-C1-D-Phe6, Leu17]-VIP. Am J Physiol 250: G553–G557
Ellis JL, Farmer SG (1989) The effects of vasoactive intestinal (VIP) antagonists, and VIP and peptide histidine isoleucine antisera on non-adrenergic, non-cholinergic relaxations of tracheal smooth muscle. Br J Pharmacol 96: 513–520
Li CG, Rand MJ (1991) Evidence that part of the NANC relaxant response of guinea-pig trachea to electrical field stimulation is mediated by nitric oxide. Br J Pharmacol 102: 91–94
Hakoda H, Xie ZQ, Aizawa H, Inoue H, Hirata M, Ito Y (1991) Effects of immunisation against VIP on neurotransmission in cat trachea. Am J Physiol 261: L341–L348
Altiere RJ, Diamond L (1984) Relaxation of cat tracheobronchial and pulmonary arterial smooth muscle by vasoactive intestinal peptide: lack of influence of peptidase inhibitors. Br J Pharmacol 82: 321–328
Altiere RJ, Diamond L (1985) Effect of a-chymotrypsin on the non-adrenergic noncholinergic inhibitory system in cat airways. Eur J Pharmacol 114: 75–78
Fisher JT, Anderson JW, Waldron MA (1993) Nonadrenergic noncholinergic neurotransmitter of feline trachealis: VIP or nitric oxide. J Appl Physiol 74: 31–39
Takahashi N, Tanaka H, Abdullah N, Jing L, Inoue R, Ito Y (1995) Regional difference in the distribution of L-NAME-sensitive and -insensitive NANC relaxations in cat airway. J Physiol 488: 709–720
Raffestin B, Cerrina J, Boullet C, Labat C, Benveniste J, Brink C (1985) Response and sensitivity of isolated human pulmonary muscle preparations to pharmacological agents. J Pharmacol Exp Ther 233: 186–194
Belvisi MG, Stretton CD, Yacoub MH, Barnes PJ (1992) Nitric oxide is the endogenous neurotransmitter of bronchodilator nerves in humans. Eur J Pharmacol 210: 221–222
Nathan CF (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J 6: 3051–3064
Forstermann U, Schmidt HHHW, Pollock JS, Sheng H, Mitchell JA, Warner TD et al (1991) Isoforms of nitric oxide synthase: Characterisation and purification from different cell types. Biochem Pharmacol 42: 1849–1857
Pollock JS, Forstermann U, Mitchell JA, Warner TD, Schmidt HH, Nakane M et al (1991) Purification and characterisation of particulate endothelium-derived relaxant factor synthase from cultured and native bovine aortic endothelial cells. Proc Nall Acad Sci (USA) 88: 10480–10484
Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci (USA) 87: 682–685
Schmidt HHHW, Pollock JS, Nakane M, Gorsky LD, Forstermann U, Murad F (1991) Purification of a soluble isoform of guanylyl cyclase-activating-factor synthase. Proc Natl Acad Sci 88: 365–369
Mitchell JA, Sheng H, Forstermann U, Murad F (1991) Characterisation of NO synthase in non-adrenergic non-cholinergic nerve containing anoccocygeus. Br J Pharmacol 104: 289–291
Hamid Q, Springall DR, Riveros-Moreno V, Chanez P, Howarth P, Redington A et al (1993) Induction of nitric oxide synthase in asthma. Lancet 342: 1510–1513
Robbins RA, Barnes PJ, Springall DR, Warren JB, Kwon OJ, Buttery LD et al (1994) Expression of inducible nitric oxide synthase in human bronchial epithelial cells. Biochem Biophys Res Commun 203: 209–218
Barnes PJ, Belvisi MG (1993) Nitric oxide and lung disease. Thorax 48: 1034–1043
Tucker JF, Brave SR, Charalambous L, Hobbs A, Gibson AJ (1990) L-NG-nitro arginine inhibits nonadrenergic, noncholinergic relaxations of guinea-pig tracheal smooth muscle. Br J Pharmacol 100: 663–664
Hecker M, Mitchell JA, Harris Hi, Katsura M, Thiemermann C, Vane JR (1990) Endothelial cells metabolize NG-monomethyl-L-arginine to L-citrulline and subsequently to L-arginine. Biochem Biophys Res Commun 167: 1037–1043
Bogle RG, Moncada S, Pearson JD, Mann GE (1993) Identification of inhibitors of nitric oxide synthase that do not interact with the endothelial cell L-arginine transporter. Br J Pharmacol 105: 768–770
Li CG, Rand MJ (1989) Evidence for a role of nitric oxide in the NANC-mediated relaxations in rat anococcygeus muscle. Clin Exp Physiol Pharmacol 16: 933–938
Li CG, Rand MJ (1990) Nitric oxide and vasoactive intestinal polypeptide mediate nonadrenergic, non-cholinergic inhibitory transmission to smooth muscle of the rat gastric fundus. Eur J Pharmacol 191: 303–309
Grider JJ, Murthy KS, Jin JG, Makhlouf GM (1992) Stimulation of nitric oxide from muscle cells by VIP: Pre-junctional enhancement of VIP release. Am J Physiol 262: G774–G778
Fischer A, Mundel P, Mayer B, Preissler U, Philippin B, Kummer W (1993) Nitric oxide synthase in guinea-pig lower airway innervation. Neurosci Letts 149: 157–160
De Luca A, Li CG, Rand J, Reid JJ, Thaina P, Wong-Dusting HK (1990) Effects of co-conotoxin GVIA on autonomic neuroeffector transmission in various tissues. Br J Pharmacol 101: 437–447
Diamond L, Lantta J, Thompson D, Altiere RJ (1992) Nitric oxide synthase inhibitors fail to affect cat airway nonadrenergic noncholinergic inhibitory (NANCI) responses. Am Rev Re.sp Dis 145: A382
Jing L, Inoue R, Tashiro K, Takahashi S, Ito Y (1995) Role of nitric oxide in inhibitory and modulation of excitatory neuroeffector transmission in cat airway. J Physiol 481: 225–237
Kannan MS, Johnson DE (1992) Nitric oxide mediated the neural non-adrenergic, non-cholinergic relaxation of pig tracheal smooth muscle. Am J Physiol 262: L511–L514
Fame TM, Loader JE, Graves J, Colasurdo GN, Larsen GL (1993) Decrease in the airways’ non-adrenergic, non-cholinergic inhibitory system in allergen sensitised rabbit. Am Rev Respir Dis 147: A285
Dey RD, Mayer B, Said SI (1993) Colocalisation of vasoactive intestinal peptide and nitric oxide synthase in neurons of the ferret trachea. Neurosci 54: 839–843
Rapoport RM, Murad F (1983) Agonist induced endothelium-dependent relaxation in rat thoracic aorta may be mediated through cGMP. Circ Res 52: 352–357
Ward JK, Barnes Pi, Tadjkarimi S, Yacoub MH, Belvisi MG (1995) Neural relaxation in human tracheal smooth muscle (HTSM) is mediated by an increase in cGMP: further evidence for the role of nitric oxide. J Physiol 483: 525–536
Watson NJ, Maclagan J, Barnes PJ (1993) Vagal control of guinea-pig tracheal smooth muscle: lack of involvement of VIP or nitric oxide. J Appl Physiol 74: 1964–1971
Rhoden KJ, Barnes PJ (1989) Epithelial modulation of NANC and VIP-induced responses: role of neutral endopeptidase. Eur JPharmacol 171: 247–250
Fischer A, Hoffman B (1996) Nitric oxide synthase in neurons and nerve fibres of lower airways and vagal sensory ganglia of man. Am J Respir Crit Care Med 154: 209–216
Hassall CJS, Saffrey MJ, Burnstock G (1993) NADPH-diaphorase activity by guinea-pig paratracheal neurons. Neuro Report 4: 49–52
Yu M, Robinson NE, Wang Z (1993) Regional distribution of nitroxidergic and adrenergic nerves in equine airway smooth muscle. Am Rev Respir Dis 147: A286
Grundstrom N, Andersson RGG, Wikberg JES (1981) Pharmacological characterisation of the autonomous innervation of guinea-pig tracheobronchial smooth muscle. Acta Pharmacol Scand 49: 150–157
Undem BJ, Myers AC, Barthlow H et al (1990) Vagal innervation of the guinea-pig bronchus. J Appl Physiol 69: 1336–1346
Ellis JL, Undem BJ (1990) Non-adrenergic, non-cholinergic contractions in the electrically field stimulated guinea-pig trachea. Br J Pharmacol 101: 875–880
Palmer JBD, Sampson AP, Barnes PJ (1985) Cholinergic and non-adrenergic inhibitory responses in bovine airways: distribution and functional association. Am Rev Respir Dis A283
Rand MJ, Li CG (1995) Nitric oxide as a neurotransmitter in peripheral nerves: Nature of transmitter and mechanism of transmission. Annu Rev Physiol 57: 659–682
Rand MJ, Li CG (1995) Nitric oxide in the autonomic and enteric nervous systems. In: Vincent SR (ed) Nitric oxide in the nervous system. London: Academic Press 229–279
Langley JN, Anderson HK (1895) The innervation of the pelvic and adjoining viscera. J Physiol 19: 71–139
Gillespie JS, Sheng H (1990) The effects of pyrogalol and hydroquinone on the response to NANC nerve stimulation in the rat anococcygeus and the bovine retractor penis. Br J Pharmacol 99: 194–196
Hobbs AJ, Tucker JF, Gibson A (1991) Differentiation by hydroquinone of relaxations induced by exogenous and endogenous nitrates in non-vascular smooth muscle: Role of superoxide anions. Br J Pharmacol 104: 645–650
Barbier AJM, Lefebvre RA (1992) Effect of LY83583 on relaxation induced by nonadrenergic, non-cholinergic nerve stimulation and exogenous nitric oxide in the rat gastric fundus. Eur J Pharmacol 219: 331–334
Knudsen MA, Svane D, Tottrup A (1992) Action profiles of nitric oxide, S-nitroso-Lcysteine, SNP, and NANC responses in oppossum lower esophageal sphincter. Amer J Physiol 262: G840–846
Liu X, Gillespie JS, Martin W (1994) Non-adrenergic, non-cholinergic relaxation of the bovine retractor penis muscle: Role of S-nitrosothiols. Br J Pharmacol 111: 1287–1295
Tanaka H, Jing L, Takahashi S, Ito Y (1996) The possible role of nitric oxide in relaxations and excitatory neuroeffector transmission in the cat airway. J Physiol 493: 785–791
Gibson A, Brave SR, McFadzean I, Tucker JF, Wayman C (1995) The nitrergic transmitter of the anococcygeus — NO or not? Arch Int Pharmacodyn Ther 329: 39–51
Gibson A, Babbedge R, Brave SR, Hart SL, Hobbs AJ, Tucker JF et al (1992) An investigation of some S-nitrosothiols, and of hydroxy-arginine, on the mouse anococcygeus. Br JPharmacol 107: 715–721
Barbier AJM, Lefebvre RA (1994) Influence of S-nitrosothiols and nitrate tolerance in the rat gastric fundus. Br JPharmacol 111: 1280–1286
Rand MJ, Li CG (1993) Differential effects of hydroxocobalamin on relaxations induced by nitrosothiols in rat aorta and anococcygeus muscle. Eur J Pharmacol 241: 249–254
Jansen A, Drazen J, Osborne JA, Brown R, Loscalzo JP, Stamler JS (1992) The relaxant properties in guinea-pig airways of S-nitrosothiols. J Pharmacol Exp Ther 261: 154–160
Mathews WR, Kerr SW (1993) Biological activity of S-nitrosothiols — The role of nitric oxide. JPharmacol Exp Ther 267: 1529–1537
Wood J, Garthwaite J (1994) Models of the diffusional spread of nitric oxide: implications for neural nitric oxide signalling and its pharmacological properties. Neuropharmacology 33: 1235–1244
Rand MJ, Li CG (1995) Discrimination by the NO-trapping agent, carboxy-PTIO, between NO and the nitrergic transmitter but not between NO and EDRF. Br J Pharmacol 116: 1906–1910
Brave SR, Gibson A, Tucker JF (1993) The inhibitory effects of hydroquinone on nitric oxide-induced relaxation of the mouse anococcygeus are prevented by native thiols. Br J Pharmacol 109:10P
Martin W, McAllister KHM, Paisley K (1994) NANC neurotransmission in the bovine retractor penis muscle is blocked by superoxide anion following inhibition of superoxide dismutase with diethyldithiocarbamate. Neuropharmacology 33: 1293–1301
Lilley E, Gibson A (1995) Inhibition of relaxations to nitrergic stimulation of the mouse anococcygeus by duroquinone. Br J Pharmacol 116: 3231–3236
Lilley E, Gibson A (1996) Antioxidant protection of NO-induced relaxations of the mouse anococcygeus against inhibition by superoxide anions, hydroquinone and carboxy-PTIO. Br J Pharmacol 119: 432–438
Radi R, Beckman JS, Bush KM, Freemans BA (1991) Peroxynitrite oxidation of sulfhydryls. J Biol Chem 266: 4244–4250
van der Vliet A, Smith D, O’Neil CA, Kaur H, Darley-Usmar V, Cross CE et al (1994) Interactions of peroxynitrite with human plasma and its constituents: oxidative damage and antioxidant depletion. Biochem J 303: 295–301
Villa LM, Salas E, Darley-Usmar V, Radomski MW, Moncada S (1994) Peroxynitrite induces both vasodilatation and impaired vascular relaxation in the isolated perfused rat heart. Proc NatlAcad Sci USA 91: 12383–123887
Bolanos JP, Heales SJR, Land JM, Clark JB (1995) Effect of peroxynitrite on the mitochondria] respiratory chain: differential susceptibility of neurons and astrocytes in primary culture. J Neurochem 64: 1965–1972
Diamond L, Altiere RJ (1989) Airway nonadrenergic noncholinergic inhibitory nervous system. In Kaliner M, Barnes PJ (eds) Lung Biology in Health and Disease. The Airways: neural control in health and disease. Marcel Dekker: New York, 343–394
Lammers J-WJ, Barnes PJ, Chung KF (1992) Nonadrenergic, non-cholinergic airway inhibitory nerves. Eur Respir J 5: 239–246
Miura M, Inoue H, Ichinose M, Kimura K, Katsumata U, Takishima T (1990) Effect of nonadrenergic, noncholinergic inhibitory nerve stimulation on the allergic reaction in cat airways. A m Rev Respir Dis 141: 29–32
Undem BJ, Dick EC, Buckner CK (1983) Inhibition by vasoactive intestinal peptide of antigen-induced histamine release from guinea-pig minced lung. Eur J Pharmacol 88: 247–250
Miura M, Kimura K, Takahashi T, Inoue H, Takishima T (1990) Possible mechanisms of the antigen-induced dysfunction of nonadrenergic, noncholinergic inhibitory nervous system. Am Rev Respir Dis 141: A387
Tam EK, Caughey GH (1990) Degradation of airway neuropeptides by human lung typtase. Am J Respir Cell Mol Biol 3: 27–32
O11erensha Jarvis D, Woolcock A, Sullivan C, Scheibner T (1989) Absence of immunoreactive vasoactive intestinal polypeptide in tissue from the lungs of patients with asthma. N Engl J Med 320: 1244–1248
Kakuta Y, Stead RH, Perdue MH, Marshall JS, Bienenstock J (1989) Micro-anatomical relationship of mast cells and nerves in rat lung and trachea. Am Rev Respir Dis 139: A118
Miura M, Yamauchi H, Ichinose M, Ohuchi Y, Kageyama N, Tomaki Metal (1997) Impairment of neural nitric oxide-mediated relaxation after antigen exposure in guinea-pig airways in vitro. Am JRespir Grit Care Med 156: 217–222
Taylor SM, Paré P, Armour CL, Hogg JC, Schellenburg RR (1985) Airway reactivity in chronic obstructive pulmonary disease. Failure of in vivo methacholine responsiveness to correlate with cholinergic, adrenergic, or non-adrenergic responses in vitro. Am Rev Respir Dis 132: 30–35
Belvisi MG, Ward JK, Tadjkarimi S, Yacoub MH, Barnes PJ (1993) Inhibitory NANC nerves in human airways: differences in disease and after extrinsic denervation. Am Rev Respir Dis 147: A286
Bai TR (1990) Abnormalities in airway smooth muscle in fatal asthma. Am Rev Respir Dis 141: 552–557
Howarth P, Springall DR, Redington AE, Djukanovic R, Holgate ST, Polak JM (1995) Neuropeptide-containing nerves in endobronchial biopsies from asthmatic and non-asthmatic subjects. Am J Respir Cell Mol Biol 13: 288–296
Belvisi MG, Ward JK, Springall DR, Tadjkarimi S, Yacoub MH, Polak JM et al (1994) Nitrergic innervation in the airways of patients with cystic fibrosis. Am JRespir Med and Grit Care Med 149: A675
Belvisi MG, Miura M, Stretton CD, Barnes PJ (1993) Endogenous vasoactive intestinal peptide and nitric oxide modulate cholinergic neurotransmission in guinea-pig trachea. Eur J Pharmacol 231: 97–102
Brave SR, Hobbs AJ, Gibson A, Tucker JF (1991) The influence of L-NG-nitro-arginine on field stimulation-induced contractions and acetylcholine release in guinea-pig isolated smooth muscle. Biochem Biophys Res Commun 179: 1017–1022
Belvisi MG, Stretton CD, Barnes PJ (1991) Nitric oxide as an endogenous modulator of cholinergic neurotransmission in guinea-pig airways. Eur J Pharmacol 198: 219–221
Ward JK, Belvisi MG, Fox AJ, Miura M, Tadjkarimi S, Yacoub MH et al (1993) Modulation of cholinergic bronchoconstrictor responses by endogenous nitric oxide and vasoactive intestinal peptide in human airways in vitro. J Clin Invest 92: 736–742
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Belvisi, M.G., Gibson, A. (2000). Non-Adrenergic Non-Cholinergic Neurotransmission in the Airways: Role of Nitric Oxide. In: Belvisi, M.G., Mitchell, J.A. (eds) Nitric Oxide in Pulmonary Processes. Respiratory Pharmacology and Pharmacotherapy. Birkhäuser, Basel. https://doi.org/10.1007/978-3-0348-8474-7_3
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DOI: https://doi.org/10.1007/978-3-0348-8474-7_3
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