Transduction mechanisms in airway sensory nerves

Journal of Applied Physiology

Volumn 101, Issue 3, 2006, Pages 950-959

  Taylor Clark, Thomas ^a   Undem, Bradley J ^a  

^a JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

Author keywords

Bronchopulmonary; C fiber; Chemosensitivity; Neuromodulation; Vagus

Indexed keywords

ACID; ADENOSINE; ADENOSINE TRIPHOSPHATE; BRADYKININ; CAPSAICIN; CATION CHANNEL; METABOTROPIC RECEPTOR; NEUROTROPHIN; NICOTINE; SEROTONIN; SODIUM CHLORIDE; WATER;

ACTION POTENTIAL; AIRWAY; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION; INFLAMMATION; INOTROPISM; MEDIATOR RELEASE; MEMBRANE DEPOLARIZATION; NERVE CONDUCTION; NERVE ENDING; NERVE EXCITABILITY; NEUROMODULATION; NONHUMAN; OSMOLARITY; PH; PRIORITY JOURNAL; REFLEX; REVIEW; SENSORY NERVE; SIGNAL TRANSDUCTION; TEMPERATURE;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; FEEDBACK; HUMANS; LUNG; RECEPTORS, SENSORY; RESPIRATORY MECHANICS; SIGNAL TRANSDUCTION;

EID: 33748445549     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00222.2006     Document Type: Review

References (107)

1. Adriaensen D, Timmermans JP, Brouns I, Berthoud HR, Neuhuber WL, and Scheuermann DW. Pulmonary intraepithelial vagal nodose afferent nerve terminals are confined to neuroepithelial bodies: an anterograde tracing and confocal microscopy study in adult rats. Cell Tissue Res 293: 395-405, 1998.
2. Alessandri-Haber N, Yeh JJ, Boyd AE, Parada CA, Chen X, Reichling DB, and Levine JD. Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39: 497-511, 2003.
3. Baker CV and Bronner-Fraser M. Vertebrate cranial placodes. I. Embryonic induction. Dev Biol 232: 1-61, 2001.
4. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, and Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124: 1269-1282, 2006.
5. Bergren DR. Sensory receptor activation by mediators of defense reflexes in guinea-pig lungs. Respir Physiol 108: 195-204, 1997.
6. Bolser DC, McLeod RL, Tulshian DB, and Hey JA. Antitussive action of nociceptin in the cat. Eur J Pharmacol 430: 107-111, 2001.
7. Bonini S, Lambiase A, Angelucci F, Magrini L, Manni L, and Aloe L. Circulating nerve growth factor levels are increased in humans with allergic diseases and asthma. Proc Natl Acad Sci USA 93: 10955-10960, 1996.
8. Brouns I, Pintelon I, De Proost I, Alewaters R, Timmermans JP, and Adriaensen D. Neurochemical characterisation of sensory receptors in airway smooth muscle: comparison with pulmonary neuroepithelial bodies. Histochem Cell Biol: 1-17, 2005.
9. Buck LB. Olfactory receptors and odor coding in mammals. Nutr Rev 62: S184-S188; discussion S224-S141, 2004.
10. Canning BJ, Mazzone SB, Meeker SN, Mori N, Reynolds SM, and Undem BJ. Identification of the tracheal and laryngeal afferent neurones mediating cough in anaesthetized guinea-pigs. J Physiol 557: 543-558, 2004.
11. Carr MJ, Gover TD, Weinreich D, and Undem BJ. Inhibition of mechanical activation of guinea-pig airway afferent neurons by amiloride analogues. Br J Pharmacol 133: 1255-1262, 2001.
12. Carr MJ, Hunter DD, Jacoby DB, and Undem BJ. Expression of tachykinins in nonnociceptive vagal afferent neurons during respiratory viral infection in guinea pigs. Am J Respir Crit Care Med 165: 1071-1075, 2002.
13. Carr MJ, Hunter DD, and Undem BJ. Neurotrophins and asthma. Curr Opin Pulm Med 7: 1-7, 2001.
14. Carr MJ, Kollarik M, Meeker SN, and Undem BJ. A role for TRPV1 in bradykinin-induced excitation of vagal airway afferent nerve terminals. J Pharmacol Exp Ther 304: 1275-1279, 2003.
15. Carr MJ and Undem BJ. Bronchopulmonary afferent nerves. Respirology 8: 291-301, 2003.
16. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997.
17. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, and Julius D. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411: 957-962, 2001.
18. Chuaychoo B, Hunter DD, Myers AC, Kollarik M, and Undem BJ. Allergen-induced substance P synthesis in large-diameter sensory neurons innervating the lungs. J Allergy Clin Immunol 116: 325-331, 2005.
19. Chuaychoo B, Lee MG, Kollarik M, and Undem BJ. Effect of 5-hydroxytryptamine on vagal C-fiber subtypes in guinea pig lungs. Pulm Pharmacol Ther 18: 269-276, 2005.
20. Cockayne DA, Dunn PM, Zhong Y, Rong W, Hamilton SG, Knight GE, Ruan HZ, Ma B, Yip P, Nunn P, McMahon SB, Burnstock G, and Ford AP. P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J Physiol 567: 621-639, 2005.
21. Coleridge JC and Coleridge HM. Afferent vagal C fibre innervation of the lungs and airways and its functional significance. Rev Physiol Biochem Pharmacol 99: 1-110, 1984.
22. Curtis R and DiStefano PS. Neurotropic factors, retrograde axonal transport and cell signalling. Trends Cell Biol 4: 383-386, 1994.
23. Davies RO and Kubin L. Projection of pulmonary rapidly adapting receptors to the medulla of the cat: an antidromic mapping study. J Physiol 373: 63-86, 1986.
24. Davies RO, Kubin L, and Pack AI. Pulmonary stretch receptor relay neurones of the cat: location and contralateral medullary projections. J Physiol 383: 571-585, 1987.
25. Delpire E. Cation-chloride cotransporters in neuronal communication. News Physiol Sci 15: 309-312, 2000.
26. Dinh QT, Groneberg DA, Peiser C, Springer J, Joachim RA, Arck PC, Klapp BF, and Fischer A. Nerve growth factor-induced substance P in capsaicin-insensitive vagal neurons innervating the lower mouse airway. Clin Exp Allergy 34: 1474-1479, 2004.
27. Drummond HA, Abboud FM, and Welsh MJ. Localization of beta and gamma subunits of ENaC in sensory nerve endings in the rat foot pad. Brain Res 884: 1-12, 2000.
28. Drummond HA, Price MP, Welsh MJ, and Abboud FM. A molecular component of the arterial baroreceptor mechanotransducer. Neuron 21: 1435-1441, 1998.
29. Eccles R, Griffiths DH, Newton CG, and Tolley NS. The effects of D and L isomers of menthol upon nasal sensation of airflow. J Laryngol Otol 102: 506-508, 1988.
30. Evans AR, Vasko MR, and Nicol GD. The cAMP transduction cascade mediates the PGE2-induced inhibition of potassium currents in rat sensory neurones. J Physiol 516: 163-178, 1999.
31. Finger TE, Bottger B, Hansen A, Anderson KT, Alimohammadi H, and Silver WL. Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc Natl Acad Sci USA 100: 8981-8986, 2003.
32. Fox AJ, Barnes PJ, and Dray A. Stimulation of guinea-pig tracheal afferent fibres by non-isosmotic and low-chloride stimuli and the effect of frusemide. J Physiol 482: 179-187, 1995.
33. + channels and stomatin are expressed in rat trigeminal mechanosensory neurons. Cell Tissue Res 299: 327-334, 2000.
34. Glazebrook PA, Ramirez AN, Schild JH, Shieh CC, Doan T, Wible BA, and Kunze DL. Potassium channels Kv1.1, Kv1.2 and Kv1.6 influence excitability of rat visceral sensory neurons. J Physiol 541: 467-482, 2002.
35. Gold MS, Zhang L, Wrigley DL, and Traub RJ. Prostaglandin E2 modulates TTX-R INa in rat colonic sensory neurons. J Neurophysiol 88: 1512-1522, 2002.
36. Goodman MB, Lumpkin EA, Ricci A, Tracey WD, Kernan M, and Nicolson T. Molecules and mechanisms of mechanotransduction. J Neurosci 24: 9220-9222, 2004.
37. Grigg P. Biophysical studies of mechanoreceptors. J Appl Physiol 60: 1107-1115, 1986.
38. Haas M and Forbush B 3rd. The Na-K-Cl cotransporters. J Bioenerg Biomembr 30: 161-172, 1998.
39. Harper AA. Similarities between some properties of the soma and sensory receptors of primary afferent neurones. Exp Physiol 76: 369-377, 1991.
40. Helke CJ, Adryan KM, Fedorowicz J, Zhuo H, Park JS, Curtis R, Radley HE, and Distefano PS. Axonal transport of neurotrophins by visceral afferent and efferent neurons of the vagus nerve of the rat. J Comp Neurol 393: 102-117, 1998.
41. Ho CY, Gu Q, Lin YS, and Lee LY. Sensitivity of vagal afferent endings to chemical irritants in the rat lung. Respir Physiol 127: 113-124, 2001.
42. Hong JL, Ho CY, Kwong K, and Lee LY. Activation of pulmonary C fibres by adenosine in anaesthetized rats: role of adenosine A1 receptors. J Physiol 508: 109-118, 1998.
43. Howe CL and Mobley WC. Long-distance retrograde neurotrophic signaling. Curr Opin Neurobiol 15: 40-48, 2005.
44. Hoyle GW, Graham RM, Finkelstein JB, Nguyen KP, Gozal D, and Friedman M. Hyperinnervation of the airways in transgenic mice overexpressing nerve growth factor. Am J Respir Cell Mol Biol 18: 149-157, 1998.
45. Hunter DD, Myers AC, and Undem BJ. Nerve growth factor-induced phenotypic switch in guinea pig airway sensory neurons. Am J Respir Crit Care Med 161: 1985-1990, 2000.
46. Hurt CM, Wang L, Xu J, Sterious W, and Pelleg A. Electrophysiological- anatomic correlates of ATP-triggered vagal reflex in dogs. II. Vagal afferent traffic. Am J Physiol Heart Circ Physiol 267: H1093-H1097, 1994.
47. Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, Cho S, Min KH, Suh YG, Kim D, and Oh U. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci USA 97: 6155-6160, 2000.
48. Ichinose M, Belvisi MG, and Barnes PJ. Bradykinin-induced bronchoconstriction in guinea pig in vivo: role of neural mechanisms. J Pharmacol Exp Ther 253: 594-599, 1990.
49. Ingram SL and Williams JT. Modulation of the hyperpolarization-activated current (Ih) by cyclic nucleotides in guinea-pig primary afferent neurons. J Physiol 492: 97-106, 1996.
50. Jafri MS, Moore KA, Taylor GE, and Weinreich D. Histamine H1 receptor activation blocks two classes of potassium current, IK(rest) and IAHP, to excite ferret vagal afferents. J Physiol 503: 533-546, 1997.
51. Jia Y, Wang X, Aponte SI, Rivelli MA, Yang R, Rizzo CA, Corboz MR, Priestley T, and Hey JA. Nociceptin/orphanin FQ inhibits capsaicin-induced guinea-pig airway contraction through an inward-rectifier potassium channel. Br J Pharmacol 135: 764-770, 2002.
52. Jones RC 3rd, Xu L, and Gebhart GF. The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3. J Neurosci 25: 10981-10989, 2005.
53. Klein JP, Tendi EA, Dib-Hajj SD, Fields RD, and Waxman SG. Patterned electrical activity modulates sodium channel expression in sensory neurons. J Neurosci Res 74: 192-198, 2003.
54. Knight GE, Bodin P, De Groat WC, and Burnstock G. ATP is released from guinea pig ureter epithelium on distension. Am J Physiol Renal Physiol 282: F281-F288, 2002.
55. Kollarik M and Undem BJ. Activation of bronchopulmonary vagal afferent nerves with bradykinin, acid and vanilloid receptor agonists in wild-type and TRPV1-/- mice. J Physiol 555: 115-123, 2004.
56. Kollarik M and Undem BJ. Mechanisms of acid-induced activation of airway afferent nerve fibres in guinea-pig. J Physiol 543: 591-600, 2002.
57. Kou YR, Frazier DT, and Lee LY. The stimulatory effect of nicotine on vagal pulmonary C-fibers in dogs. Respir Physiol 76: 347-356, 1989.
58. Kwong K and Lee LY. Prostaglandin E2 potentiates a TTX-resistant sodium current in rat capsaicin-sensitive vagal pulmonary sensory neurones. J Physiol 564: 437-450, 2005.
59. Lai YL. Role of the axon reflex in capsaicin-induced bronchoconstriction in guinea pigs. Respir Physiol 83: 35-46, 1991.
60. Lee LY and Morton RF. Histamine enhances vagal pulmonary C-fiber responses to capsaicin and lung inflation. Respir Physiol 93: 83-96, 1993.
61. Lee LY, Morton RF, and Kou YR. Acute effects of cigarette smoke on breathing in rats: vagal and nonvagal mechanisms. J Appl Physiol 68: 955-961, 1990.
62. Lee LY, Morton RF, and Lundberg JM. Pulmonary chemoreflexes elicited by intravenous injection of lactic acid in anesthetized rats. J Appl Physiol 81: 2349-2357, 1996.
63. Lee MG, Macglashan DW Jr, and Undem BJ. Role of chloride channels in bradykinin-induced guinea pig airway vagal C-fibre activation. J Physiol 566: 205-212, 2005.
64. Lee MG, Undem BJ, Brown C, and Carr MJ. Effect of nociceptin in acid-evoked cough and airway sensory nerve activation in guinea pigs. Am J Respir Crit Care Med 173: 271-275, 2006.
65. Lee P, Zhuo H, and Helke CJ. Axotomy alters neurotrophin and neurotrophin receptor mRNAs in the vagus nerve and nodose ganglion of the rat. Brain Res Mol Brain Res 87: 31-41, 2001.
66. Lin SY and Corey DP. TRP channels in mechanosensation. Curr Opin Neurobiol 15: 350-357, 2005.
67. Loewenstein WR and Mendelson M. Components of receptor adaptation in a pacinian corpuscle. J Physiol 177: 377-397, 1965.
68. Lu SH, Yamagata T, Atsuki K, Sun L, Smith CP, Yoshimura N, Chancellor MB, and de Groat WC. Effect of KW-7158, a putative afferent nerve inhibitor, on bladder and vesico-vascular reflexes in rats. Brain Res 946: 72-78, 2002.
69. Lumpkin EA and Bautista DM. Feeling the pressure in mammalian somatosensation. Curr Opin Neurobiol 15: 382-388, 2005.
70. McAlexander MA, Myers AC, and Undem BJ. Adaptation of guinea-pig vagal airway afferent neurones to mechanical stimulation. J Physiol 521: 239-247, 1999.
71. McLeod RL, Parra LE, Mutter JC, Erickson CH, Carey GJ, Tulshian DB, Fawzi AB, Smith-Torhan A, Egan RW, Cuss FM, and Hey JA. Nociceptin inhibits cough in the guinea-pig by activation of ORL(1) receptors. Br J Pharmacol 132: 1175-1178, 2001.
72. Mohapatra DP and Nau C. Desensitization of capsaicin-activated currents in the vanilloid receptor TRPV1 is decreased by the cyclic AMP-dependent protein kinase pathway. J Biol Chem 278: 50080-50090, 2003.
73. Naeini RS, Witty MF, Seguela P, and Bourque CW. An N-terminal variant of Trpv1 channel is required for osmosensory transduction. Nat Neurosci 9: 93-98, 2006.
74. Nakajima S and Onodera K. Adaptation of the generator potential in the crayfish stretch receptors under constant length and constant tension. J Physiol 200: 187-204, 1969.
75. Nault MA, Vincent SG, and Fisher JT. Mechanisms of capsaicin- and lactic acid-induced bronchoconstriction in the newborn dog. J Physiol 515: 567-578, 1999.
76. Nealen ML, Gold MS, Thut PD, and Caterina MJ. TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 90: 515-520, 2003.
77. Nockher WA and Renz H. Neurotrophins and asthma: novel insight into neuroimmune interaction. J Allergy Clin Immunol 117: 67-71, 2006.
78. Oh EJ and Weinreich D. Bradykinin decreases K(+) and increases Cl(-) conductances in vagal afferent neurones of the guinea pig. J Physiol 558: 513-526, 2004.
79. Pan J, Copland I, Post M, Yeger H, and Cutz E. Mechanical stretch-induced serotonin release from pulmonary neuroendocrine cells: implications for lung development. Am J Physiol Lung Cell Mol Physiol 290: L185-L193, 2006.
80. Pedersen KE, Meeker SN, Riccio MM, and Undem BJ. Selective stimulation of jugular ganglion afferent neurons in guinea pig airways by hypertonic saline. J Appl Physiol 84: 499-506, 1998.
81. Pisarri TE, Jonzon A, Coleridge JC, and Coleridge HM. Rapidly adapting receptors monitor lung compliance in spontaneously breathing dogs. J Appl Physiol 68: 1997-2005, 1990.
82. Reisert J, Lai J, Yau KW, and Bradley J. Mechanism of the excitatory Cl- response in mouse olfactory receptor neurons. Neuron 45: 553-561, 2005.
83. Ricci A, Felici L, Mariotta S, Mannino F, Schmid G, Terzano C, Cardillo G, Amenta F, and Bronzetti E. Neurotrophin and neurotrophin receptor protein expression in the human lung. Am J Respir Cell Mol Biol 30: 12-19, 2004.
84. Ricco MM, Kummer W, Biglari B, Myers AC, and Undem BJ. Interganglionic segregation of distinct vagal afferent fibre phenotypes in guinea-pig airways. J Physiol 496: 521-530, 1996.
85. Roberts AM, Bhattacharya J, Schultz HD, Coleridge HM, and Coleridge JC. Stimulation of pulmonary vagal afferent C-fibers by lung edema in dogs. Circ Res 58: 512-522, 1986.
86. Ruan T, Lin YS, Lin KS, and Kou YR. Sensory transduction of pulmonary reactive oxygen species by capsaicin-sensitive vagal lung afferent fibres in rats. J Physiol 565: 563-578, 2005.
87. Sant'Ambrogio FB, Anderson JW, and Sant'Ambrogio G. Effect of L-menthol on laryngeal receptors. J Appl Physiol 70: 788-793, 1991.
88. Sant'Ambrogio FB, Sant'Ambrogio G, and Anderson JW. Effect of furosemide on the response of laryngeal receptors to low-chloride solutions. Eur Respir J 6: 1151-1155, 1993.
89. 2+ waves are propagated via ATP release and purinergic receptor activation. Am J Physiol Cell Physiol 279: C295-C307, 2000.
90. Schild JH, Alfrey KD, and Li BY. Voltage-gated ion channels in vagal afferent neurons. In: Advances in Vagal Afferent Neurobiology, edited by Undem BJ and Weinreich D. Boca Raton, FL: CRC, 2005, p. 77-100.
91. Sekizawa SI and Tsubone H. Nasal receptors responding to noxious chemical irritants. Respir Physiol 96: 37-48, 1994.
92. Shin J, Cho H, Hwang SW, Jung J, Shin CY, Lee SY, Kim SH, Lee MG, Choi YH, Kim J, Haber NA, Reichling DB, Khasar S, Levine JD, and Oh U. Bradykinin-12-lipoxygenase-VR1 signaling pathway for inflammatory hyperalgesia. Proc Natl Acad Sci USA 99: 10150-10155, 2002.
93. Springall DR, Cadieux A, Oliveira H, Su H, Royston D, and Polak JM. Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J Auton Nerv Syst 20: 155-166, 1987.
94. Sutherland SP, Benson CJ, Adelman JP, and McCleskey EW. Acid-sensing ion channel 3 matches the acid-gated current in cardiac ischemia-sensing neurons. Proc Natl Acad Sci USA 98: 711-716, 2001.
95. Syntichaki P and Tavernarakis N. Genetic models of mechanotransduction: the nematode Caenorhabditis elegans. Physiol Rev 84: 1097-1153, 2004.
96. Taylor-Clark TE, Kollarik M, MacGlashan DW Jr, and Undem BJ. Nasal sensory nerve populations responding to histamine and capsaicin. J Allergy Clin Immunol 116: 1282-1288, 2005.
97. Tominaga M and Caterina MJ. Thermosensation and pain. J Neurobiol 61: 3-12, 2004.
98. Tortorolo L, Langer A, Polidori G, Vento G, Stampachiacchere B, Aloe L, and Piedimonte G. Neurotrophin overexpression in lower airways of infants with respiratory syncytial virus infection. Am J Respir Crit Care Med 172: 233-237, 2005.
99. Undem BJ, Chuaychoo B, Lee MG, Weinreich D, Myers AC, and Kollarik M. Subtypes of vagal afferent C-fibres in guinea-pig lungs. J Physiol 556: 905-917, 2004.
100. Van Genechten J, Brouns I, Burnstock G, Timmermans JP, and Adriaensen D. Quantification of neuroepithelial bodies and their innervation in fawn-hooded and Wistar rat lungs. Am J Respir Cell Mol Biol 30: 20-30, 2004.
101. Weinreich D and Wonderlin WF. Inhibition of calcium-dependent spike after-hyperpolarization increases excitability of rabbit visceral sensory neurones. J Physiol 394: 415-427, 1987.
102. Widdicombe JG. Afferent receptors in the airways and cough. Respir Physiol 114: 5-15, 1998.
103. Widdicombe JG. Pulmonary and respiratory tract receptors. J Exp Biol 100: 41-57, 1982.
104. Yoshihara S, Morimoto H, Yamada Y, Abe T, and Arisaka O. Cannabinoid receptor agonists inhibit sensory nerve activation in guinea pig airways. Am J Respir Crit Care Med 170: 941-946, 2004.
105. Yu J, Zhang J, Wang Y, Fan F, and Yu A. Neuroepithelial bodies not connected to pulmonary slowly adapting stretch receptors. Respir Physiol Neurobiol 144: 1-14, 2004.
106. Zhang L, Jones S, Brody K, Costa M, and Brookes SJ. Thermosensitive transient receptor potential channels in vagal afferent neurons of the mouse. Am J Physiol Gastrointest Liver Physiol 286: G983-G991, 2004.
107. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, and Hogestatt ED. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400: 452-457, 1999.