Parasympathetic control of airway submucosal glands: Central reflexes and the airway intrinsic nervous system

Autonomic Neuroscience: Basic and Clinical

Volumn 133, Issue 1, 2007, Pages 35-54

  Wine, Jeffrey J ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; SODIUM CHLORIDE; TACHYKININ; VASOACTIVE INTESTINAL POLYPEPTIDE;

AIRWAY CONDUCTANCE; ANATOMY; BACTERIUM; CHOLINERGIC SYSTEM; CYSTIC FIBROSIS; FUNGUS; HUMAN; IMMUNOPATHOGENESIS; INNATE IMMUNITY; LUNG CLEARANCE; LUNG TRANSPLANTATION; MUCOCILIARY CLEARANCE; MUCUS; MUCUS GLAND; MUCUS SECRETION; NERVE TRACT; NONHUMAN; PARASYMPATHETIC INNERVATION; PHAGOCYTE; PRIORITY JOURNAL; RESPIRATORY FUNCTION; RESPIRATORY TRACT MUCOSA; REVIEW; UPPER RESPIRATORY TRACT; VAGUS NERVE STIMULATION; VAGUS REFLEX;

ANIMALS; EXOCRINE GLANDS; HUMANS; MUCUS; NERVE NET; PARASYMPATHETIC NERVOUS SYSTEM; RESPIRATORY MUCOSA;

EID: 33947724811     PISSN: 15660702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.autneu.2007.01.008     Document Type: Review

References (149)

1. Allen T.G., and Burnstock G. A voltage-clamp study of the electrophysiological characteristics of the intramural neurones of the rat trachea. J. Physiol. 423 (1990) 593-614
2. Atoji Y., Kusindarta D.L., Hamazaki N., and Kaneko A. Innervation of the rat trachea by bilateral cholinergic projections from the nucleus ambiguous and direct motor fibers from the cervical spinal cord: a retrograde and anterograde tracer study. Brain Res. 1031 1 (2005) 90-100
3. Baker D.G., McDonald D.M., Basbaum C.B., and Mitchell R.A. The architecture of nerves and ganglia of the ferret trachea as revealed by acetylcholinesterase histochemistry. J. Comp. Neurol. 246 4 (1986) 513-526
4. Ballard S.T., and Inglis S.K. Liquid secretion properties of airway submucosal glands. J. Physiol. 556 Pt 1 (2004) 1-10
5. Ballard S.T., Trout L., Bebok Z., Sorscher E.J., and Crews A. CFTR involvement in chloride, bicarbonate, and liquid secretion by airway submucosal glands. Am. J. Physiol. 277 4 Pt 1 (1999) L694-L699
6. Ballard S.T., Trout L., Garrison J., and Inglis S.K. Ionic mechanism of forskolin-induced liquid secretion by porcine bronchi. Am. J. Physiol. Lung Cell Mol. Physiol. 290 1 (2006) L97-L104
7. Baluk P., and Gabella G. Innervation of the guinea pig trachea: a quantitative morphological study of intrinsic neurons and extrinsic nerves. J. Comp. Neurol. 285 1 (1989) 117-132
8. Baraniuk J.N., Lundgren J.D., Okayama M., Mullol J., Merida M., Shelhamer J.H., and Kaliner M.A. Vasoactive intestinal peptide in human nasal mucosa. J. Clin. Invest. 86 3 (1990) 825-831
9. Beisswenger C., and Bals R. Antimicrobial peptides in lung inflammation. Chem. Immunol. Allergy 86 (2005) 55-71
10. Bredt D.S., Hwang P.M., and Snyder S.H. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347 6295 (1990) 768-770
11. Burnstock G. Autonomic neural control mechanisms with special reference to the airways. The Airways: Neural Control in Health and Disease. In: Kaliner M.A., and Barnes P.J. (Eds). Lung Biology in Health and Disease vol. 33 (1988) 1-22
12. Canning B.J. Anatomy and neurophysiology of the cough reflex: ACCP evidence-based clinical practice guidelines. Chest 129 1 Suppl (2006) 33S-47S
13. Canning B.J., Reynolds S.M., Anukwu L.U., Kajekar R., and Myers A.C. Endogenous neurokinins facilitate synaptic transmission in guinea pig airway parasympathetic ganglia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283 2 (2002) R320-R330
14. Canning B.J., Mazzone S.B., Meeker S.N., Mori N., Reynolds S.M., and Undem B.J. Identification of the tracheal and laryngeal afferent neurones mediating cough in anaesthetized guinea-pigs. J. Physiol. 557 Pt 2 (2004) 543-558
15. Canning B.J., Farmer D.G., and Mori N. Mechanistic studies of acid-evoked coughing in anesthetized guinea pigs. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 2 (2006) R454-R463
16. Chiang C.H., and Gabella G. Quantitative study of the ganglion neurons of the mouse trachea. Cell Tissue Res. 246 2 (1986) 243-252
17. Choi H.K., Finkbeiner W.E., and Widdicombe J.H. A comparative study of mammalian tracheal mucous glands. J. Anat. 197 Pt 3 (2000) 361-372
18. Choi J.Y., Ianowski J.P., Hanrahan J.W., and Wine J.J. Mucus secretion by mouse airway submucosal glands. Pediatr. Pulmonol., Suppl. 29 (2006) 238
19. Choi J.Y., Joo N.S., Wu J.V., Krouse M.E., and Wine J.J. Human submucosal gland secretion: synergic stimulation by low levels of vip and carbachol is lost in cystic fibrosis. Pediatr. Pulmonol., Suppl. 29 (2006) 238
20. Choi J.Y., Joo N.S., Wu J.V., Krouse M.E., and Wine J.J. Submucosal gland secretion in pig airways: synergistic stimulation by low levels of vip and carbachol. Pediatr. Pulmonol., Suppl. 29 (2006) 238
21. Coburn R.F. The anatomy of the ferret paratracheal parasympathetic nerve-ganglion plexus. Exp. Lung Res. 7 1 (1984) 1-9
22. Coburn R.F., and Kalia M.P. Morphological features of spiking and nonspiking cells in the paratracheal ganglion of the ferret. J. Comp. Neurol. 254 3 (1986) 341-351
23. Cole A.M., and Waring A.J. The role of defensins in lung biology and therapy. Am. J. Respir. Med. 1 4 (2002) 249-259
24. Coleridge H.M., and Coleridge J.C. Pulmonary reflexes: neural mechanisms of pulmonary defense. Annu. Rev. Physiol. 56 (1994) 69-91
25. Coles S.J., Neill K.H., and Reid L.M. Potent stimulation of glycoprotein secretion in canine trachea by substance P. J. Appl. Physiol. 57 5 (1984) 1323-1327
26. Crews A., Taylor A.E., and Ballard S.T. Liquid transport properties of porcine tracheal epithelium. J. Appl. Physiol. 91 2 (2001) 797-802
27. Dajani R., Zhang Y., Taft P.J., Travis S.M., Starner T.D., Olsen A., Zabner J., Welsh M.J., and Engelhardt J.F. Lysozyme secretion by submucosal glands protects the airway from bacterial infection. Am. J. Respir. Cell Mol. Biol. 32 6 (2005) 548-552
28. Davis B., and Tseng H.C. Neural regulation of lysozyme secretion from tracheal submucosal glands of ferrets in vivo. J. Appl. Physiol. 71 3 (1991) 939-944
29. Davis B., Chinn R., Gold J., Popovac D., Widdicombe J.G., and Nadel J.A. Hypoxemia reflexly increases secretion from tracheal submucosal glands in dogs. J. Appl. Physiol. 52 6 (1982) 1416-1419
30. Davis B., Roberts A.M., Coleridge H.M., and Coleridge J.C. Reflex tracheal gland secretion evoked by stimulation of bronchial C-fibers in dogs. J. Appl. Physiol. 53 4 (1982) 985-991
31. Devor D.C., Singh A.K., Lambert L.C., DeLuca A., Frizzell R.A., and Bridges R.J. Bicarbonate and chloride secretion in Calu-3 human airway epithelial cells. J. Gen. Physiol. 113 5 (1999) 743-760
32. Dey R.D. Controlling from within: neurophysiological plasticity of parasympathetic airway neurons. Am. J. Physiol. Lung Cell Mol. Physiol. 284 4 (2003) L578-L580
33. Dey R.D., and Zhu W. Origin of galanin in nerves of cat airways and colocalization with vasoactive intestinal peptide. Cell Tissue Res. 273 1 (1993) 193-200
34. Dey R.D., Shannon Jr. W.A., and Said S.I. Localization of VIP-immunoreactive nerves in airways and pulmonary vessels of dogs, cat, and human subjects. Cell Tissue Res. 220 2 (1981) 231-238
35. Dey R.D., Hoffpauir J., and Said S.I. Co-localization of vasoactive intestinal peptide- and substance P-containing nerves in cat bronchi. Neuroscience 24 1 (1988) 275-281
36. Dey R.D., Altemus J.B., and Michalkiewicz M. Distribution of vasoactive intestinal peptide- and substance P-containing nerves originating from neurons of airway ganglia in cat bronchi. J. Comp. Neurol. 304 2 (1991) 330-340
37. Dey R.D., Mayer B., and Said S.I. Colocalization of vasoactive intestinal peptide and nitric oxide synthase in neurons of the ferret trachea. Neuroscience 54 4 (1993) 839-843
38. Dey R.D., Altemus J.B., Rodd A., Mayer B., Said S.I., and Coburn R.F. Neurochemical characterization of intrinsic neurons in ferret tracheal plexus. Am. J. Respir. Cell Mol. Biol. 14 3 (1996) 207-216
39. Dey R.D., Satterfield B., and Altemus J.B. Innervation of tracheal epithelium and smooth muscle by neurons in airway ganglia. Anat. Rec. 254 2 (1999) 166-172
40. Duszyk M. CFTR and lysozyme secretion in human airway epithelial cells. Pflugers Arch. 443 Suppl 1 (2001) S45-S49
41. Elkins M.R., Robinson M., Rose B.R., Harbour C., Moriarty C.P., Marks G.B., Belousova E.G., Xuan W., and Bye P.T. A controlled trial of long-term inhaled hypertonic saline in patients with cystic fibrosis. N. Engl. J. Med. 354 3 (2006) 229-240
42. Emmelin N., Garrett J.R., and Gjorstrup P. Supporting effects of myoepithelial cells in submandibular glands of dogs when acting against increased intraluminal pressure. J. Physiol. 268 1 (1977) 73-85
43. Finkbeiner W.E., Carrier S.D., and Teresi C.E. Reverse transcription-polymerase chain reaction (RT-PCR) phenotypic analysis of cell cultures of human tracheal epithelium, tracheobronchial glands, and lung carcinomas. Am. J. Respir. Cell Mol. Biol. 9 5 (1993) 547-556
44. Fisher A.W. The intrinsic innervation of the trachea. J. Anat. 98 (1964) 117-124
45. Fischer A., and Hoffmann B. Nitric oxide synthase in neurons and nerve fibers of lower airways and in vagal sensory ganglia of man. Correlation with neuropeptides. Am. J. Respir. Crit. Care Med. 154 1 (1996) 209-216
46. Fischer A., Canning B.J., and Kummer W. Correlation of vasoactive intestinal peptide and nitric oxide synthase with choline acetyltransferase in the airway innervation. Ann. N.Y. Acad. Sci. 805 (1996) 717-722
47. Fischer A., Canning B.J., Undem B.J., and Kummer W. Evidence for an esophageal origin of VIP-IR and NO synthase-IR nerves innervating the guinea pig trachealis: a retrograde neuronal tracing and immunohistochemical analysis. J. Comp. Neurol. 394 3 (1998) 326-334
48. Fontan J.J., Cortright D.N., Krause J.E., Velloff C.R., Karpitskyi V.V., Carver Jr. T.W., Shapiro S.D., and Mora B.N. Substance P and neurokinin-1 receptor expression by intrinsic airway neurons in the rat. Am. J. Physiol. Lung Cell Mol. Physiol. 278 2 (2000) L344-L355
49. Ganz T. Antimicrobial polypeptides. J. Leukoc. Biol. 75 1 (2004) 34-38
50. Gashi A.A., Borson D.B., Finkbeiner W.E., Nadel J.A., and Basbaum C.B. Neuropeptides degranulate serous cells of ferret tracheal glands. Am. J. Physiol. 251 2 Pt 1 (1986) C223-C229
51. German V.F., Ueki I.F., and Nadel J.A. Micropipette measurement of airway submucosal gland secretion: laryngeal reflex. Am. Rev. Respir. Dis. 122 3 (1980) 413-416
52. German V.F., Corrales R., Ueki I.F., and Nadel J.A. Reflex stimulation of tracheal mucus gland secretion by gastric irritation in cats. J. Appl. Physiol. 52 5 (1982) 1153-1155
53. Gerson C., Sabater J., Scuri M., Torbati A., Coffey R., Abraham J.W., Lauredo I., Forteza R., Wanner A., Salathe M., Abraham W.M., and Conner G.E. The lactoperoxidase system functions in bacterial clearance of airways. Am. J. Respir. Cell Mol. Biol. 22 6 (2000) 665-671
54. Goetz D.H., Holmes M.A., Borregaard N., Bluhm M.E., Raymond K.N., and Strong R.K. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol. Cell 10 5 (2002) 1033-1043
55. Haws C., Finkbeiner W.E., Widdicombe J.H., and Wine J.J. CFTR in Calu-3 human airway cells: channel properties and role in cAMP-activated Cl-conductance. Am. J. Physiol. 266 5 Pt 1 (1994) L502-L512
56. Haxhiu M.A., Haxhiu-Poskurica B., Moracic V., Carlo W.A., and Martin R.J. Reflex and chemical responses of tracheal submucosal glands in piglets. Respir. Physiol. 82 3 (1990) 267-277
57. Haxhiu M.A., Cherniack N.S., and Strohl K.P. Reflex responses of laryngeal and pharyngeal submucosal glands in dogs. J. Appl. Physiol. 71 5 (1991) 1669-1673
58. Haxhiu M.A., van Lunteren E., and Cherniack N.S. Central effects of tachykinin peptide on tracheal secretion. Respir. Physiol. 86 3 (1991) 405-414
59. Haxhiu M.A., Van Lunteren E., and Cherniack N.S. Influence of ventrolateral surface of medulla on tracheal gland secretion. J. Appl. Physiol. 71 5 (1991) 1663-1668
60. Haxhiu M.A., Chavez J.C., Pichiule P., Erokwu B., and Dreshaj I.A. The excitatory amino acid glutamate mediates reflexly increased tracheal blood flow and airway submucosal gland secretion. Brain Res. 883 1 (2000) 77-86
61. Haxhiu M.A., Kc P., Moore C.T., Acquah S.S., Wilson C.G., Zaidi S.I., Massari V.J., and Ferguson D.G. Brain stem excitatory and inhibitory signaling pathways regulating bronchoconstrictive responses. J. Appl. Physiol. 98 6 (2005) 1961-1982
62. Hejal R., Strohl K.P., Erokwu B., Cherniack N.S., and Haxhiu M.A. Pathways and mechanisms involved in neural control of laryngeal submucosal gland secretion. J. Appl. Physiol. 75 6 (1993) 2347-2352
63. Hejal R., Strohl K.P., Erokwu B., Cherniack N.S., and Haxhiu M.A. Effect of hypoxia on reflex responses of tracheal submucosal glands. J. Appl. Physiol. 78 5 (1995) 1651-1656
64. Hunter D.D., and Undem B.J. Identification and substance P content of vagal afferent neurons innervating the epithelium of the guinea pig trachea. Am. J. Respir. Crit. Care Med. 159 6 (1999) 1943-1948
65. Hutchings H.A., Morris S., Eccles R., and Jawad M.S. Voluntary suppression of cough induced by inhalation of capsaicin in healthy volunteers. Respir. Med. 87 5 (1993) 379-382
66. Ianowski J.P., Choi J.Y., Wine J.J., and Hanrahan J.W. Mucus secretion by CFTR-/-mouse airway submucosal glands. Pediatr. Pulmonol., Suppl. 29 (2006) 264
67. Ianowski, J.P., Choi, J.Y., Wine, J.J., Hanrahan, J.W., in press. Mucus secretion by CFTR-/-mouse airway submucosal glands. J. Physiol. doi:10.1113/JPHYSIOL.2006.123653 (Published online Jan 4, 2007).
68. Inglis S.K., Corboz M.R., Taylor A.E., and Ballard S.T. Effect of anion transport inhibition on mucus secretion by airway submucosal glands. Am. J. Physiol. 272 2 Pt 1 (1997) L372-L377
69. Inglis S.K., Corboz M.R., Taylor A.E., and Ballard S.T. In situ visualization of bronchial submucosal glands and their secretory response to acetylcholine. Am. J. Physiol. 272 2 Pt 1 (1997) L203-L210
70. Inglis S.K., Corboz M.R., and Ballard S.T. Effect of anion secretion inhibitors on mucin content of airway submucosal gland ducts. Am. J. Physiol. 274 5 Pt 1 (1998) L762-L766
71. Irokawa T., Krouse M.E., Joo N.S., Wu J.V., and Wine J.J. A "virtual gland" method for quantifying epithelial fluid secretion. Am. J. Physiol. Lung Cell Mol. Physiol. 287 4 (2004) L784-L793
72. Jayaraman S., Joo N.S., Reitz B., Wine J.J., and Verkman A.S. Submucosal gland secretions in airways from cystic fibrosis patients have normal [Na+] and pH but elevated viscosity. Proc. Natl. Acad. Sci. U. S. A. 98 14 (2001) 8119-8123
73. Joo N.S., Krouse M.E., Wu J.V., Saenz Y., Jayaraman S., Verkman A.S., and Wine J.J. HCO(3)(-) transport in relation to mucus secretion from submucosal glands. Jop 2 4 Suppl (2001) 280-284
74. Joo N.S., Wu J.V., Krouse M.E., Saenz Y., and Wine J.J. Optical method for quantifying rates of mucus secretion from single submucosal glands. Am. J. Physiol. Lung Cell Mol. Physiol. 281 2 (2001) L458-L468
75. Joo N.S., Irokawa T., Wu J.V., Robbins R.C., Whyte R.I., and Wine J.J. Absent secretion to vasoactive intestinal peptide in cystic fibrosis airway glands. J. Biol. Chem. 277 52 (2002) 50710-50715
76. Joo N.S., Saenz Y., Krouse M.E., and Wine J.J. Mucus secretion from single submucosal glands of pig. Stimulation by carbachol and vasoactive intestinal peptide. J. Biol. Chem. 277 31 (2002) 28167-28175
77. Joo N.S., Lee D.J., Winges K.M., Rustagi A., and Wine J.J. Regulation of antiprotease and antimicrobial protein secretion by airway submucosal gland serous cells. J. Biol. Chem. 279 37 (2004) 38854-38860
78. Joo N.S., Irokawa T., Robbins R.C., and Wine J.J. Hyposecretion, not hyperabsorption, is the basic defect of cystic fibrosis airway glands. J. Biol. Chem. 281 11 (2006) 7392-7398
79. Kajekar R., Rohde H.K., and Myers A.C. The integrative membrane properties of human bronchial parasympathetic ganglia neurons. Am. J. Respir. Crit. Care Med. 164 10 Pt 1 (2001) 1927-1932
80. Kajekar R., Undem B.J., and Myers A.C. Role of cyclooxygenase activation and prostaglandins in antigen-induced excitability changes of bronchial parasympathetic ganglia neurons. Am. J. Physiol. Lung Cell Mol. Physiol. 284 4 (2003) L581-L587
81. Kc P., Mayer C.A., and Haxhiu M.A. Chemical profile of vagal preganglionic motor cells innervating the airways in ferrets: the absence of noncholinergic neurons. J. Appl. Physiol. 97 4 (2004) 1508-1517
82. Khakh B.S., and North R.A. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442 7102 (2006) 527-532
83. Kim J.S., Okamoto K., Arima S., and Rubin B.K. Vasoactive intestinal peptide stimulates mucus secretion, but nitric oxide has no effect on mucus secretion in the ferret trachea. J. Appl. Physiol. (2006)
84. Kirchgessner A.L., Liu M.T., and Gershon M.D. In situ identification and visualization of neurons that mediate enteric and enteropancreatic reflexes. J. Comp. Neurol. 371 2 (1996) 270-286
85. Knowles M.R., and Boucher R.C. Mucus clearance as a primary innate defense mechanism for mammalian airways. J. Clin. Invest. 109 5 (2002) 571-577
86. Kubin L., Alheid G.F., Zuperku E.J., and McCrimmon D.R. Central pathways of pulmonary and lower airway vagal afferents. J. Appl. Physiol. 101 2 (2006) 618-627
87. Kuder T., Szczurkowski A., Kuchinka J., and Nowak E. The AChE-positive ganglia in the trachea and bronchi of the cat. Folia Morphol. (Warsz.) 62 2 (2003) 99-106
88. Kusindarta D.L., Atoji Y., and Yamamoto Y. Nerve plexuses in the trachea and extrapulmonary bronchi of the rat. Arch. Histol. Cytol. 67 1 (2004) 41-55
89. Laitinen A. Ultrastructural organisation of intraepithelial nerves in the human airway tract. Thorax 40 7 (1985) 488-492
90. Lamb D., and Reid L. The tracheobronchial submucosal glands in cystic fibrosis: a qualitative and quantitative histochemical study. Br. J. Dis. Chest 66 4 (1972) 239-247
91. Landois L. A Textbook of Human Physiology (1885), Charles Griffin, London
92. Lee M.C., Penland C.M., Widdicombe J.H., and Wine J.J. Evidence that Calu-3 human airway cells secrete bicarbonate. Am. J. Physiol. 274 3 Pt 1 (1998) L450-L453
93. Levin M.H., Sullivan S., Nielson D., Yang B., Finkbeiner W.E., and Verkman A.S. Hypertonic saline therapy in cystic fibrosis: evidence against the proposed mechanism involving aquaporins. J. Biol. Chem. 281 35 (2006) 25803-25812
94. Lundberg J.M., Hokfelt T., Martling C.R., Saria A., and Cuello C. Substance P-immunoreactive sensory nerves in the lower respiratory tract of various mammals including man. Cell Tissue Res. 235 2 (1984) 251-261
95. Mazzone S.B., and Canning B.J. Central nervous system control of the airways: pharmacological implications. Curr. Opin. Pharmacol. 2 3 (2002) 220-228
96. Meyrick B., and Reid L. Ultrastructure of cells in the human bronchial submucosal glands. J. Anat. 107 2 (1970) 281-299
97. Meyrick B., Sturgess J.M., and Reid L. A reconstruction of the duct system and secretory tubules of the human bronchial submucosal gland. Thorax 24 6 (1969) 729-736
98. Mitchell R.A., Herbert D.A., Baker D.G., and Basbaum C.B. In vivo activity of tracheal parasympathetic ganglion cells innervating tracheal smooth muscle. Brain Res. 437 1 (1987) 157-160
99. Myers A.C. Anatomical characteristics of tonic and phasic postganglionic neurons in guinea pig bronchial parasympathetic ganglia. J. Comp. Neurol. 419 4 (2000) 439-450
100. Myers A.C. Transmission in autonomic ganglia. Respir. Physiol. 125 1-2 (2001) 99-111
101. Myers A.C., and Undem B.J. Electrophysiological effects of tachykinins and capsaicin on guinea-pig bronchial parasympathetic ganglion neurones. J. Physiol. 470 (1993) 665-679
102. Myers A.C., and Undem B.J. Antigen depolarizes guinea pig bronchial parasympathetic ganglion neurons by activation of histamine H1 receptors. Am. J. Physiol. 268 6 Pt 1 (1995) L879-L884
103. Myers A.C., and Undem B.J. Muscarinic receptor regulation of synaptic transmission in airway parasympathetic ganglia. Am. J. Physiol. 270 4 Pt 1 (1996) L630-L636
104. Myers A., Undem B., and Kummer W. Anatomical and electrophysiological comparison of the sensory innervation of bronchial and tracheal parasympathetic ganglion neurons. J. Auton. Nerv. Syst. 61 2 (1996) 162-168
105. Myers A.C., Goldie R.G., and Hay D.W. A novel role for tachykinin neurokinin-3 receptors in regulation of human bronchial ganglia neurons. Am. J. Respir. Crit. Care Med. 171 3 (2005) 212-216
106. Nadel J.A., Davis B., and Phipps R.J. Control of mucus secretion and ion transport in airways. Annu. Rev. Physiol. 41 (1979) 369-381
107. Newhouse M., Sanchis J., and Bienenstock J. Lung defense mechanisms (first of two parts). N. Engl. J. Med. 295 18 (1976) 990-998
108. Oh E.J., Mazzone S.B., Canning B.J., and Weinreich D. Reflex regulation of airway sympathetic nerves in guinea-pigs. J. Physiol. 573 Pt 2 (2006) 549-564
109. Pastor L.M., Ferran A., Calvo A., Sprekelsen C., Horn R., and Marin J.A. Morphological and histochemical study of human submucosal laryngeal glands. Anat. Rec. 239 4 (1994) 453-467
110. Peatfield A.C., Barnes P.J., Bratcher C., Nadel J.A., and Davis B. Vasoactive intestinal peptide stimulates tracheal submucosal gland secretion in ferret. Am. Rev. Respir. Dis. 128 1 (1983) 89-93
111. Pedersen K.E., Meeker S.N., Riccio M.M., and Undem B.J. Selective stimulation of jugular ganglion afferent neurons in guinea pig airways by hypertonic saline. J. Appl. Physiol. 84 2 (1998) 499-506
112. Perez Fontan J.J., and Velloff C.R. Labeling of vagal motoneurons and central afferents after injection of cholera toxin B into the airway lumen. Am. J. Physiol. Lung Cell Mol. Physiol. 280 1 (2001) L152-L164
113. Petersen O.H., and Sutton R. Ca2+ signalling and pancreatitis: effects of alcohol, bile and coffee. Trends Pharmacol. Sci. 27 2 (2006) 113-120
114. Phillips J.E., Hey J.A., and Corboz M.R. Computer assisted measurement of airway gland secretions by the hillocks technique. Comput. Methods Programs Biomed. 68 3 (2002) 215-222
115. Phillips J.E., Hey J.A., and Corboz M.R. Effects of ion transport inhibitors on MCh-mediated secretion from porcine airway submucosal glands. J. Appl. Physiol. 93 3 (2002) 873-881
116. Phillips J.E., Hey J.A., and Corboz M.R. Tachykinin NK3 and NK1 receptor activation elicits secretion from porcine airway submucosal glands. Br. J. Pharmacol. 138 1 (2003) 254-260
117. Pisarri T.E., Jonzon A., Coleridge H.M., and Coleridge J.C. Vagal afferent and reflex responses to changes in surface osmolarity in lower airways of dogs. J. Appl. Physiol. 73 6 (1992) 2305-2313
118. Pisarri T.E., Coleridge H.M., and Coleridge J.C. Reflex bronchial vasodilation in dogs evoked by injection of a small volume of water into a bronchus. J. Appl. Physiol. 75 5 (1993) 2195-2202
119. Quinton P.M. Composition and control of secretions from tracheal bronchial submucosal glands. Nature 279 5713 (1979) 551-552
120. Robinson M., Regnis J.A., Bailey D.L., King M., Bautovich G.J., and Bye P.T. Effect of hypertonic saline, amiloride, and cough on mucociliary clearance in patients with cystic fibrosis. Am. J. Respir. Crit. Care Med. 153 5 (1996) 1503-1509
121. Salinas D., Haggie P.M., Thiagarajah J.R., Song Y., Rosbe K., Finkbeiner W.E., Nielson D.W., and Verkman A.S. Submucosal gland dysfunction as a primary defect in cystic fibrosis. FASEB J. 19 3 (2005) 431-433
122. Schultz H.D., Roberts A.M., Bratcher C., Coleridge H.M., Coleridge J.C., and Davis B. Pulmonary C-fibers reflexly increase secretion by tracheal submucosal glands in dogs. J. Appl. Physiol. 58 3 (1985) 907-910
123. Schultz H.D., Davis B., Coleridge H.M., and Coleridge J.C. Cigarette smoke in lungs evokes reflex increase in tracheal submucosal gland secretion in dogs. J. Appl. Physiol. 71 3 (1991) 900-909
124. Shen B.Q., Finkbeiner W.E., Wine J.J., Mrsny R.J., and Widdicombe J.H. Calu-3: a human airway epithelial cell line that shows cAMP-dependent Cl-secretion. Am. J. Physiol. 266 5 Pt 1 (1994) L493-L501
125. Shimura S., Sasaki T., Okayama H., Sasaki H., and Takishima T. Effect of substance P on mucus secretion of isolated submucosal gland from feline trachea. J. Appl. Physiol. 63 2 (1987) 646-653
126. Shimura S., Sasaki T., Ikeda K., Sasaki H., and Takishima T. VIP augments cholinergic-induced glycoconjugate secretion in tracheal submucosal glands. J. Appl. Physiol. 65 6 (1988) 2537-2544
127. Song Y., Salinas D., Nielson D.W., and Verkman A.S. Hyperacidity of secreted fluid from submucosal glands in early cystic fibrosis. Am. J. Physiol. Cell Physiol. 290 3 (2006) C741-C749
128. Thiagarajah J.R., Song Y., Haggie P.M., and Verkman A.S. A small molecule CFTR inhibitor produces cystic fibrosis-like submucosal gland fluid secretions in normal airways. FASEB J. 18 7 (2004) 875-877
129. Tos M. Development of the tracheal glands in man. Number, density, structure, shape, and distribution of mucous glands elucidated by quantitative studies of whole mounts. Acta Pathol. Microbiol. Scand. 68 Suppl 185 (1966) 1-130
130. Trout L., Gatzy J.T., and Ballard S.T. Acetylcholine-induced liquid secretion by bronchial epithelium: role of Cl- and HCO3- transport. Am. J. Physiol. 275 6 Pt 1 (1998) L1095-L1099
131. Trout L., King M., Feng W., Inglis S.K., and Ballard S.T. Inhibition of airway liquid secretion and its effect on the physical properties of airway mucus. Am. J. Physiol. 274 2 Pt 1 (1998) L258-L263
132. Trout L., Corboz M.R., and Ballard S.T. Mechanism of substance P-induced liquid secretion across bronchial epithelium. Am. J. Physiol. Lung Cell Mol. Physiol. 281 3 (2001) L639-L645
133. Trout L., Townsley M.I., Bowden A.L., and Ballard S.T. Disruptive effects of anion secretion inhibitors on airway mucus morphology in isolated perfused pig lung. J. Physiol. 549 Pt 3 (2003) 845-853
134. Uddman R., Alumets J., Densert O., Hakanson R., and Sundler F. Occurrence and distribution of VIP nerves in the nasal mucosa and tracheobronchial wall. Acta Otolaryngol. 86 5-6 (1978) 443-448
135. Undem B.J., Chuaychoo B., Lee M.G., Weinreich D., Myers A.C., and Kollarik M. Subtypes of vagal afferent C-fibres in guinea-pig lungs. J. Physiol. 556 Pt 3 (2004) 905-917
136. Van Genechten J., Brouns I., Scheuermann D.W., Timmermans J.P., and Adriaensen D. Reduced number of intrinsic pulmonary nitrergic neurons in Fawn-Hooded rats as compared to control rat strains. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 272 1 (2003) 446-453
137. Verkman A.S., Song Y., and Thiagarajah J.R. Role of airway surface liquid and submucosal glands in cystic fibrosis lung disease. Am. J. Physiol. Cell Physiol. 284 1 (2003) C2-C15
138. Wagner U., Fehmann H.C., Bredenbroker D., Yu F., Barth P.J., and von Wichert P. Galanin and somatostatin inhibition of substance P-induced airway mucus secretion in the rat. Neuropeptides 28 1 (1995) 59-64
139. Weichselbaum M., Sparrow M.P., Hamilton E.J., Thompson P.J., and Knight D.A. A confocal microscopic study of solitary pulmonary neuroendocrine cells in human airway epithelium. Respir. Res. 6 (2005) 115
140. Widdicombe J.G. Action potentials in parasympathetic and sympathetic efferent fibres to the trachea and lungs of dogs and cats. J. Physiol. 186 1 (1966) 56-88
141. Widdicombe, J.G. 1977. Defensive mechanisms of the respiratory system. International Review of Physiology: Respiratory Physiology II. J.G. Widdicombe. Baltimore, Univ. Park Press. 14: 291-315.
142. Widdicombe J.H., and Pecson I.S. Distribution and numbers of mucous glands in the horse trachea. Equine Vet. J. 34 6 (2002) 630-633
143. Widdicombe J.H., Chen L.L., Sporer H., Choi H.K., Pecson I.S., and Bastacky S.J. Distribution of tracheal and laryngeal mucous glands in some rodents and the rabbit. J. Anat. 198 Pt 2 (2001) 207-221
144. Worlitzsch D., Tarran R., Ulrich M., Schwab U., Cekici A., Meyer K.C., Birrer P., Bellon G., Berger J., Weiss T., Botzenhart K., Yankaskas J.R., Randell S., Boucher R.C., and Doring G. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 109 3 (2002) 317-325
145. Wu Z.X., and Dey R.D. Nerve growth factor-enhanced airway responsiveness involves substance P in ferret intrinsic airway neurons. Am. J. Physiol. Lung Cell Mol. Physiol. 291 1 (2006) L111-L118
146. Wu Z.X., Maize Jr. D.F., Satterfield B.E., Frazer D.G., Fedan J.S., and Dey R.D. Role of intrinsic airway neurons in ozone-induced airway hyperresponsiveness in ferret trachea. J. Appl. Physiol. 91 1 (2001) 371-378
147. Yamamoto Y., Ootsuka T., Atoji Y., and Suzuki Y. Morphological and quantitative study of the intrinsic nerve plexuses of the canine trachea as revealed by immunohistochemical staining of protein gene product 9.5. Anat. Rec. 250 4 (1998) 438-447
148. Yu J., Schultz H.D., Goodman J., Coleridge J.C., Coleridge H.M., and Davis B. Pulmonary rapidly adapting receptors reflexly increase airway secretion in dogs. J. Appl. Physiol. 67 2 (1989) 682-687
149. Zhu W., and Dey R.D. Projections and pathways of VIP- and nNOS-containing airway neurons in ferret trachea. Am. J. Respir. Cell Mol. Biol. 24 1 (2001) 38-43