Three days after a single exposure to ozone, the mechanism of airway hyperreactivity is dependent on substance P and nerve growth factor

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 300, Issue 2, 2011, Pages

  Verhein, Kirsten C ^a   Hazari, Mehdi S ^c   Moulton, Bart C ^b   Jacoby, Isabella W ^b   Jacoby, David B ^a,b,c   Fryer, Allison D ^a,b,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Neural plasticity; Pollution; Tachykinin receptors

Indexed keywords

CP 96 345; IMMUNOGLOBULIN G; INTERLEUKIN 1BETA; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR ANTIBODY; NEUROKININ 1 RECEPTOR ANTAGONIST; NOLPITANTIUM; OZONE; SAREDUTANT; SUBSTANCE P; UNCLASSIFIED DRUG;

AIRWAY HYPERREACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; EOSINOPHIL; FEMALE; GUINEA PIG; LUNG DISEASE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; VAGOTOMY;

AIR POLLUTANTS; ANIMALS; BRONCHIAL HYPERREACTIVITY; BRONCHOCONSTRICTION; DISEASE MODELS, ANIMAL; FEMALE; GUINEA PIGS; HUMANS; LUNG; MALE; MODELS, BIOLOGICAL; NERVE GROWTH FACTOR; OZONE; RECEPTORS, NEUROKININ-1; RECEPTORS, NEUROKININ-2; SUBSTANCE P; TIME FACTORS; VAGUS NERVE;

EID: 79551524023     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00060.2010     Document Type: Article

References (67)

1. Baluk P, Nigel W, McDonald B, McDonald DM. Localization of tachykinin NK1, NK2, and NK3 receptors in airways by immunohistochemistry (Abstract). Am J Respir Crit Care Med 153: A161, 1996.
2. Barker J, Wu Z, Dey R. Interleukin (IL)-1 regulates ozone-induced nerve growth factor (NGF) release in bronchoalveolar lavage fluid (BALF) in mice (Abstract). FASEB J 23: 1009.6, 2009.
3. Beckett WS, McDonnell WF, Horstman DH, House DE. Role of the parasympathetic nervous system in acute lung response to ozone. J Appl Physiol 59: 1879-1885, 1985.
4. Bell ML, McDermott A, Zeger SL, Samet JM, Dominici F. Ozone and short-term mortality in 95 US urban communities, 1987-2000. JAMA 292: 2372-2378, 2004.
5. Belmonte KE, Fryer AD, Costello RW. Role of insulin in antigeninduced airway eosinophilia and neuronal M2 muscarinic receptor dysfunction. J Appl Physiol 85: 1708-1718, 1998.
6. Biyah K, Molimard M, Emonds-Alt X, Advenier C. SR 140333 prevents potentiation by citric acid of plasma exudation induced by histamine in airways. Eur J Pharmacol 308: 325-328, 1996.
7. Canning BJ, Reynolds SM, Anukwu LU, Kajekar R, Myers AC. Endogenous neurokinins facilitate synaptic transmission in guinea pig airway parasympathetic ganglia. Am J Physiol Regul Integr Comp Physiol 283: R320-R330, 2002.
8. Carr MJ, Hunter DD, Jacoby DB, 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.
9. Chuang KJ, Chan CC, Su TC, Lee CT, Tang CS. The effect of urban air pollution on inflammation, oxidative stress, coagulation, and autonomic dysfunction in young adults. Am J Respir Crit Care Med 176: 370-376, 2007.
10. Chuaychoo B, Hunter DD, Myers AC, Kollarik M, Undem BJ. Allergen-induced substance P synthesis in large-diameter sensory neurons innervating the lungs. J Allergy Clin Immunol 116: 325-331, 2005.
11. Coleridge JC, Coleridge HM, Schelegle ES, Green JF. Acute inhalation of ozone stimulates bronchial C-fibers and rapidly adapting receptors in dogs. J Appl Physiol 74: 2345-2352, 1993.
12. Desqueyroux H, Pujet JC, Prosper M, Le Moullec Y, Momas I. Effects of air pollution on adults with chronic obstructive pulmonary disease. Arch Environ Health 57: 554-560, 2002.
13. Evans CM, Belmonte KE, Costello RW, Jacoby DB, Gleich GJ, Fryer AD. Substance P-induced airway hyperreactivity is mediated by neuronal M2 receptor dysfunction. Am J Physiol Lung Cell Mol Physiol 279: L477-L486, 2000.
14. Evans CM, Fryer AD, Jacoby DB, Gleich GJ, Costello RW. Pretreatment with antibody to eosinophil major basic protein prevents hyperresponsiveness by protecting neuronal M2 muscarinic receptors in antigen-challenged guinea pigs. J Clin Invest 100: 2254-2262, 1997.
15. Foster WM, Brown RH, Macri K, Mitchell CS. Bronchial reactivity of healthy subjects: 18-20 h postexposure to ozone. J Appl Physiol 89: 1804-1810, 2000.
16. Frossard N, Naline E, Olgart Hoglund C, Georges O, Advenier C. Nerve growth factor is released by IL-1beta and induces hyperresponsiveness of the human isolated bronchus. Eur Respir J 26: 15-20, 2005.
17. 2 muscarinic receptors in antigen-challenged guinea pigs is restored by heparin and poly-L-glutamate. J Clin Invest 90: 2292-2298, 1992.
18. Girard V, Yavo JC, Emonds-Alt X, Advenier C. The tachykinin NK2 receptor antagonist SR 48968 inhibits citric acid-induced airway hyperresponsiveness in guinea pigs. Am J Respir Crit Care Med 153: 1496-1502, 1996.
19. Golden JA, Nadel JA, Boushey HA. Bronchial hyperirritability in healthy subjects after exposure to ozone. Am Rev Respir Dis 118: 287-294, 1978.
20. Gordon T, Taylor BF, Amdur MO. Ozone inhibition of tissue cholinesterase in guinea pigs. Arch Environ Health 36: 284-288, 1981.
21. Green C. Animal Anesthesia. London: Laboratory Animals, 1982.
22. Grumann-Junior A, Dias MA, Alves RV, Boteon JE, Calixto JB. Mechanisms mediating substance P-induced contraction in the rat iris in vitro. Invest Ophthalmol Vis Sci 41: 1861-1870, 2000.
23. Gryparis A, Forsberg B, Katsouyanni K, Analitis A, Touloumi G, Schwartz J, Samoli E, Medina S, Anderson HR, Niciu EM, Wichmann HE, Kriz B, Kosnik M, Skorkovsky J, Vonk JM, Dortbudak Z. Acute effects of ozone on mortality from the "air pollution and health: a European approach" project. Am J Respir Crit Care Med 170: 1080-1087, 2004.
24. Guard S, Watson SP. Tachykinin receptor types: classification and membrane signalling mechanisms. Neurochem Int 18: 149-165, 1991.
25. Hall AK, Barnes PJ, Meldrum LA, Maclagan J. Facilitation by tachykinins of neurotransmission in guinea-pig pulmonary parasympathetic nerves. Br J Pharmacol 97: 274-280, 1989.
26. Hazari MS, Pan JH, Myers AC. Nerve growth factor acutely potentiates synaptic transmission in vitro and induces dendritic growth in vivo on adult neurons in airway parasympathetic ganglia. Am J Physiol Lung Cell Mol Physiol 292: L992-L1001, 2007.
27. 2 alpha in the airways of human subjects. Am J Respir Cell Mol Biol 9: 568-572, 1993.
28. Hey JA, Danko G, del Prado M, Chapman RW. Augmentation of neurally evoked cholinergic bronchoconstrictor responses by prejunctional NK2 receptors in the guinea-pig. J Auton Pharmacol 16: 41-48, 1996.
29. Holtzman MJ, McNamara MP, Sheppard D, Fabbri LM, Hahn HL, Graf PD, Nadel JA. Intravenous versus inhaled atropine for inhibiting bronchoconstrictor responses in dogs. J Appl Physiol 54: 134-139, 1983.
30. Hoyle GW, Graham RM, Finkelstein JB, Nguyen KP, Gozal D, Friedman M. Hyperinnervation of the airways in transgenic mice overexpressing nerve growth factor. Am J Respir Cell Mol Biol 18: 149-157, 1998.
31. Hurst SM, Stanisz AM, Sharkey KA, Collins SM. Interleukin 1 beta-induced increase in substance P in rat myenteric plexus. Gastroenterology 105: 1754-1760, 1993.
32. Jerrett M, Burnett RT, Pope CA 3rd, Ito K, Thurston G, Krewski D, Shi Y, Calle E, Thun M. Long-term ozone exposure and mortality. N Engl J Med 360: 1085-1095, 2009.
33. Jimba M, Skornik WA, Killingsworth CR, Long NC, Brain JD, Shore SA. Role of C fibers in physiological responses to ozone in rats. J Appl Physiol 78: 1757-1763, 1995.
34. Larsen GL, Loader J, Nguyen DD, Fratelli C, Dakhama A, Colasurdo GN. Mechanisms determining cholinergic neural responses in airways of young and mature rabbits. Pediatr Pulmonol 38: 97-106, 2004.
35. 2 muscarinic receptor dysfunction. Am J Physiol Lung Cell Mol Physiol 286: L1255-L1259, 2004.
36. Lee LY, Bleecker ER, Nadel JA. Effect of ozone on bronchomotor response to inhaled histamine aerosol in dogs. J Appl Physiol 43: 626-631, 1977.
37. Lisabeth LD, Escobar JD, Dvonch JT, Sanchez BN, Majersik JJ, Brown DL, Smith MA, Morgenstern LB. Ambient air pollution and risk for ischemic stroke and transient ischemic attack. Ann Neurol 64: 53-59, 2008.
38. Maggi CA. Tachykinin receptors and airway pathophysiology. Eur Respir J 6: 735-742, 1993.
39. Mapp CE, Miotto D, Braccioni F, Saetta M, Turato G, Maestrelli P, Krause JE, Karpitskiy V, Boyd N, Geppetti P, Fabbri LM. The distribution of neurokinin-1 and neurokinin-2 receptors in human central airways. Am J Respir Crit Care Med 161: 207-215, 2000.
40. Mitchell HW, Adcock J. Vagal mechanisms and the effect of indomethacin on bronchoconstrictor stimuli in the guinea-pig. Br J Pharmacol 94: 522-527, 1988.
41. Moore KA, Undem BJ, Weinreich D. Antigen inhalation unmasks NK-2 tachykinin receptor-mediated responses in vagal afferents. Am J Respir Crit Care Med 161: 232-236, 2000.
42. Myers AC, Undem BJ. Electrophysiological effects of tachykinins and capsaicin on guinea-pig bronchial parasympathetic ganglion neurones. J Physiol 470: 665-679, 1993.
43. Nakanishi S. Mammalian tachykinin receptors. Annu Rev Neurosci 14: 123-136, 1991.
44. Peden DB. Pollutants and asthma: role of air toxics. Environ Health Perspect 110, Suppl 4: 565-568, 2002.
45. Rice AJ, Reynolds PN, Reynolds AM, Holmes MD, Scicchitano R. Tachykinin-induced bronchoconstriction in sheep is NK-1 receptor mediated and exhibits tachyphylaxis. Respirology 6: 113-123, 2001.
46. Rich DQ, Schwartz J, Mittleman MA, Link M, Luttmann-Gibson H, Catalano PJ, Speizer FE, Dockery DW. Association of short-term ambient air pollution concentrations and ventricular arrhythmias. Am J Epidemiol 161: 1123-1132, 2005.
47. Ruidavets JB, Cournot M, Cassadou S, Giroux M, Meybeck M, Ferrieres J. Ozone air pollution is associated with acute myocardial infarction. Circulation 111: 563-569, 2005.
48. Schierhorn K, Hanf G, Fischer A, Umland B, Olze H, Kunkel G. Ozone-induced release of neuropeptides from human nasal mucosa cells. Int Arch Allergy Immunol 129: 145-151, 2002.
49. Schultheis AH, Bassett DJ, Fryer AD. Ozone-induced airway hyperresponsiveness and loss of neuronal M2 muscarinic receptor function. J Appl Physiol 76: 1088-1097, 1994.
50. Shore SA, Schwartzman IN, Le Blanc B, Murthy GG, Doerschuk CM. Tumor necrosis factor receptor 2 contributes to ozone-induced airway hyperresponsiveness in mice. Am J Respir Crit Care Med 164: 602-607, 2001.
51. Taylor-Clark TE, Undem BJ. Ozone activates airway nerves via the selective stimulation of TRPA1 ion channels. J Physiol 588: 423-433.
52. Tramontana M, Patacchini R, Giuliani S, Lippi A, Lecci A, Santicioli P, Criscuoli M, Maggi CA. Characterization of the antibronchoconstrictor activity of MEN 11420, a tachykinin NK2 receptor antagonist, in guinea-pigs. Eur J Pharmacol 352: 279-288, 1998.
53. Undem BJ, Hunter DD, Liu M, Haak-Frendscho M, Oakragly A, Fischer A. Allergen-induced sensory neuroplasticity in airways. Int Arch Allergy Immunol 118: 150-153, 1999.
54. van Hoof HJ, den Hartog GJ, Voss HP, van Bree L, Bast A. Capsaicin treatment induces muscarinic hyperreactivity in guinea pig trachea: a warning. Eur J Pharmacol 347: 261-264, 1998.
55. Vedder H, Affolter HU, Otten U. Nerve growth factor (NGF) regulates tachykinin gene expression and biosynthesis in rat sensory neurons during early postnatal development. Neuropeptides 24: 351-357, 1993.
56. Verhein KC, Jacoby DB, Fryer AD. IL-1 receptors mediate persistent, but not acute, airway hyperreactivity to ozone in guinea pigs. Am J Respir Cell Mol Biol 39: 730-738, 2008.
57. Wagner EM, Jacoby DB. Methacholine causes reflex bronchoconstriction. J Appl Physiol 86: 294-297, 1999.
58. Weinreich D, Moore KA, Taylor GE. Allergic inflammation in isolated vagal sensory ganglia unmasks silent NK-2 tachykinin receptors. J Neurosci 17: 7683-7693, 1997.
59. White SR, Ohno S, Munoz NM, Gleich GJ, Abrahams C, Solway J, Leff AR. Epithelium-dependent contraction of airway smooth muscle caused by eosinophil MBP. Am J Physiol Lung Cell Mol Physiol 259: L294-L303, 1990.
60. Wu ZX, Dey RD. Nerve growth factor-enhanced airway responsiveness involves substance P in ferret intrinsic airway neurons. Am J Physiol Lung Cell Mol Physiol 291: L111-L118, 2006.
61. Wu ZX, Maize DF Jr, Satterfield BE, Frazer DG, Fedan JS, Dey RD. Role of intrinsic airway neurons in ozone-induced airway hyperresponsiveness in ferret trachea. J Appl Physiol 91: 371-378, 2001.
62. Wu ZX, Satterfield BE, Dey RD. Substance P released from intrinsic airway neurons contributes to ozone-enhanced airway hyperresponsiveness in ferret trachea. J Appl Physiol 95: 742-750, 2003.
63. Wu ZX, Satterfield BE, Fedan JS, Dey RD. Interleukin-1β-induced airway hyperresponsiveness enhances substance P in intrinsic neurons of ferret airway. Am J Physiol Lung Cell Mol Physiol 283: L909-L917, 2002.
64. Yeadon M, Wilkinson D, Darley-Usmar V, O'Leary VJ, Payne AN. Mechanisms contributing to ozone-induced bronchial hyperreactivity in guinea-pigs. Pulm Pharmacol 5: 39-50, 1992.
65. 2 muscarinic receptors by eosinophil major basic protein. J Appl Physiol 87: 1272-1278, 1999.
66. Yost BL, Gleich GJ, Jacoby DB, Fryer AD. The changing role of eosinophils in long-term hyperreactivity following a single ozone exposure. Am J Physiol Lung Cell Mol Physiol 289: L627-L635, 2005.
67. Yuan L, Burcher E, Nail B. Tachykinin receptors and non-cholinergic bronchoconstriction in the anaesthetized guinea-pig. Clin Exp Pharmacol Physiol 23: 119-124, 1996.