Allergen and ozone exacerbate serotonin-induced increases in airway smooth muscle contraction in a model of childhood asthma

Respiration

Volumn 83, Issue 6, 2012, Pages 529-542

  Moore, Brian D ^a   Hyde, Dallas ^a   Miller, Lisa ^a   Wong, Emily ^a   Frelinger, Jessica ^a   Schelegle, Edward S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Air pollution; Airway hyperresponsiveness; Childhood asthma; House dust mite allergen; Rhesus monkeys; Serotonin

Indexed keywords

HOUSE DUST ALLERGEN; OZONE; SEROTONIN; SEROTONIN 1 RECEPTOR; SEROTONIN 2 RECEPTOR; SEROTONIN 3 RECEPTOR; SEROTONIN 4 RECEPTOR;

AIR POLLUTANT; ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREATHING MUSCLE; CHILDHOOD DISEASE; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; ELECTROSTIMULATION; ENVIRONMENTAL EXPOSURE; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; SMOOTH MUSCLE CONTRACTION;

ALLERGENS; ANIMALS; ASTHMA; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; INTRADERMAL TESTS; MACACA MULATTA; MUSCLE CONTRACTION; MUSCLE, SMOOTH; OZONE; PYROGLYPHIDAE; SEROTONIN; SEROTONIN ANTAGONISTS;

EID: 84862771013     PISSN: 00257931     EISSN: 14230356     Source Type: Journal    
DOI: 10.1159/000336835     Document Type: Article

References (80)

1. Akinbami LJ, Moorman JE, Garbe PL, Sondik EJ: Status of childhood asthma in the United States, 1980-2007. Pediatrics 2009; 123(suppl 3):S131-S145.
2. Prevention CfDCa: National hospital discharge survey, 2000; in Branch HCS (ed): Scientific Data Documentation. Hyattsville, Centers for Disease Control and Prevention, 2000.
3. Bloom B, Cohen RA, Freeman G: Summary Health Statistics for U.S. Children: national health interview survey, 2009. Vital Health Stat 2010; 247: 1-82.
4. Weiss KB, Sullivan SD: The health economics of asthma and rhinitis. I. Assessing the economic impact. J Allergy Clin Immunol 2001; 107: 3-8.
5. Platts-Mills TA: Dust mite allergens and asthma - a worldwide problem. J Allergy Clin Immunol 1989; 83: 416-427.
6. Hoshino M, Ohtawa J: Effects of adding omalizumab, an anti-immunoglobulin E antibody, on airway wall thickening in asthma. Respiration 2012;83:520-528.
7. Khatri SB, Holguin FC, Ryan PB, Mannino D, Erzurum SC, Teague WG: Association of ambient ozone exposure with airway inflammation and allergy in adults with asthma. J Asthma 2009; 46: 777-785.
8. McConnell R, Berhane K, Gilliland F, London SJ, Islam T, Gauderman WJ, Avol E, Margolis HG, Peters JM: Asthma in exercising children exposed to ozone: a cohort study. Lancet 2002; 359: 386-391.
9. State of the Air 2011. Washington, American Lung Association, 2011, pp 175.
10. Gauderman WJ, Avol E, Gilliland F, Vora H, Thomas D, Berhane K, McConnell R, Kuenzli N, Lurmann F, Rappaport E, Margolis H, Bates D, Peters J: The effect of air pollution on lung development from 10 to 18 years of age. N Engl J Med 2004; 351: 1057-1067.
11. Plopper CG, Smiley-Jewell SM, Miller LA, Fanucchi MV, Evans MJ, Buckpitt AR, Avdalovic M, Gershwin LJ, Joad JP, Kajekar R, Larson S, Pinkerton KE, Van Winkle LS, Schelegle ES, Pieczarka EM, Wu R, Hyde DM: Asthma/allergic airways disease: does postnatal exposure to environmental toxicants promote airway pathobiology? Toxicol Pathol 2007; 35: 97-110.
12. Schelegle ES, Miller LA, Gershwin LJ, Fanucchi MV, Van Winkle LS, Gerriets JE, Walby WF, Mitchell V, Tarkington BK, Wong VJ, Baker GL, Pantle LM, Joad JP, Pinkerton KE, Wu R, Evans MJ, Hyde DM, Plopper CG: Repeated episodes of ozone inhalation amplifies the effects of allergen sensitization and inhalation on airway immune and structural development in rhesus monkeys. Toxicol Appl Pharmacol 2003; 191: 74-85.
13. Kajekar R, Pieczarka EM, Smiley-Jewell SM, Schelegle ES, Fanucchi MV, Plopper CG: Early postnatal exposure to allergen and ozone leads to hyperinnervation of the pulmonary epithelium. Respir Physiol Neurobiol 2007; 155: 55-63.
14. Larson SD, Schelegle ES, Walby WF, Gershwin LJ, Fanuccihi MV, Evans MJ, Joad JP, Tarkington BK, Hyde DM, Plopper CG: Postnatal remodeling of the neural components of the epithelial-mesenchymal trophic unit in the proximal airways of infant rhesus monkeys exposed to ozone and allergen. Toxicol Appl Pharmacol 2004; 194: 211-220.
15. Evans MJ, Fanucchi MV, Baker GL, Van Winkle LS, Pantle LM, Nishio SJ, Schelegle ES, Gershwin LJ, Miller LA, Hyde DM, Sannes PL, Plopper CG: Atypical development of the tracheal basement membrane zone of infant rhesus monkeys exposed to ozone and allergen. Am J Physiol Lung Cell Mol Physiol 2003; 285:L931-L939.
16. Evans MJ, Fanucchi MV, Baker GL, Van Winkle LS, Pantle LM, Nishio SJ, Schelegle ES, Gershwin LJ, Miller LA, Hyde DM, Plopper CG: The remodelled tracheal basement membrane zone of infant rhesus monkeys after 6 months of recovery. Clin Exp Allergy 2004; 34: 1131-1136.
17. Fink KB, Gothert M: 5-HT receptor regulation of neurotransmitter release. Pharmacol Rev 2007; 59: 360-417.
18. Davenport TE, Stevens SR, Baroni K, Van Ness M, Snell CR: Diagnostic accuracy of symptoms characterising chronic fatigue syndrome. Disabil Rehabil 2011; 33: 1768-1775.
19. Cazzola I, Matera MG: 5-HT modifiers as a potential treatment of asthma. Trends Pharmacol Sci 2000; 21: 13-16.
20. Takahashi T, Ward JK, Tadjkarimi S, Yacoub MH, Barnes PJ, Belvisi MG: 5-hydroxytryptamine facilitates cholinergic bronchoconstriction in human and guinea pig airways. Am J Respir Crit Care Med 1995; 152: 377-380.
21. Szarek JL, Zhang JZ, Gruetter CA: Mechanisms of 5-hydroxytryptamine- induced contraction of isolated rat intrapulmonary bronchi. Pulm Pharmacol 1995; 8: 273-281.
22. Dupont L, Pype J, Demedts M, De Leyn P, Deneffe G, Verleden G: The effects of 5-HT on cholinergic contraction in human airways in vitro. Eur Respir J 1999; 14: 642-649.
23. Cazzola M, Matera MG, D'Amato G, Rossi F: Effects of serotonin on airways: recent developments. Allergy 1995; 50: 1-10.
24. Aizawa H, Takata S, Shigyo M, Matsumoto K, Inoue H, Hara N: N-omega-nitro-L-arginine methyl ester increases airway responsiveness to serotonin but not to acetylcholine in cats in vivo. Respiration 2001; 68: 286-291.
25. Yoshida M, Aizawa H, Hara N: Effect of endothelin-1 on the serotonin-induced contraction of smooth muscle in the guinea pig trachea. Respiration 1999; 66: 59-64.
26. Abdullah NA, Hirata M, Matsumoto K, Aizawa H, Inoue R, Hamano S, Ikeda S, Xie Z, Hara N, Ito Y: Contraction and depolarization induced by fetal bovine serum in airway smooth muscle. Am J Physiol 1994; 266:L528-L535.
27. Albu G, Petak F, Fontao F, Biton C, Pache JC, Habre W: Mechanisms of airway hyper-responsiveness after coronary ischemia. Respir Physiol Neurobiol 2008; 162: 176-183.
28. Almirall JJ, Dolman CS, Eidelman DH: Furosemide-induced bronchodilation in the rat bronchus: evidence of a role for prostaglandins. Lung 1997; 175: 155-163.
29. Atzori L, Bannenberg G, Corriga AM, Congiu L, Lundberg JM, Moldeus P, Ryrfeldt A: Sodium metabisulfite and citric acid induce bronchoconstriction via a sulfite-sensitive pathway in the isolated guinea pig lung. Respiration 1997; 64: 145-151.
30. Lechin F, van der Dijs B, Orozco B, Lechin M, Lechin AE: Increased levels of free serotonin in plasma of symptomatic asthmatic patients. Ann Allergy Asthma Immunol 1996; 77: 245-253.
31. Lechin F, van der Dijs B, Lechin A, Orozco B, Lechin M, Baez S, Rada I, Leon G, Acosta E: Plasma neurotransmitters and cortisol in chronic illness: role of stress. J Med 1994; 25: 181-192.
32. Lechin F, van der Dijs B, Orozco B, Jara H, Rada I, Lechin ME, Lechin AE: Neuropharmacologic treatment of bronchial asthma with the antidepressant tianeptine: a double-blind, crossover placebo-controlled study. Clin Pharmacol Ther 1998; 64: 223-232.
33. Dupont LJ, Pype JL, Demedts MG, De Leyn P, Deneffe G, Verleden GM: The effects of 8-hydroxy-2-(di-n-propylamino)tetralin on the cholinergic contraction in guinea pig and human airways in vitro. Am J Respir Crit Care Med 1998; 158: 1479-1486.
34. Dupont L, Pype J, Meade C, DeLeyn P, Deneffe G, Demedts M, Verleden G: Epinastine (WAL 801CL) inhibits the electrical field stimulation-induced cholinergic contraction in guinea pig and human airways in vitro. Eur Respir J 1999; 14: 1068-1075.
35. Evans MJ, Fanucchi MV, Plopper CG, Hyde DM: Postnatal development of the lamina reticularis in primate airways. Anat Rec 2010; 293: 947-954.
36. Plopper CG, Heidsiek JG, Weir AJ, George JA, Hyde DM: Tracheobronchial epithelium in the adult rhesus monkey: a quantitative histochemical and ultrastructural study. Am J Anat 1989; 184: 31-40.
37. Plopper CG, Alley JL, Weir AJ: Differentiation of tracheal epithelium during fetal lung maturation in the rhesus monkey Macaca mulatta . Am J Anat 1986; 175: 59-71.
38. Plopper C, St George J, Cardoso W, Wu R, Pinkerton K, Buckpitt A: Development of airway epithelium. Patterns of expression for markers of differentiation. Chest 1992; 101: 2S-5S.
39. Plopper CG, Weir AJ, Nishio SJ, Cranz DL, St George JA: Tracheal submucosal gland development in the rhesus monkey, Macaca mulatta : ultrastructure and histochemistry. Anat Embryol 1986; 174: 167-178.
40. Miller LA, Plopper CG, Hyde DM, Gerriets JE, Pieczarka EM, Tyler NK, Evans MJ, Gershwin LJ, Schelegle ES, Van Winkle LS: Immune and airway effects of house dust mite aeroallergen exposures during postnatal development of the infant rhesus monkey. Clin Exp Allergy 2003; 33: 1686-1694.
41. Schelegle ES, Gershwin LJ, Miller LAC, Fanucchi MV, Van Winkle LS, Gerriets JP, Walby WF, Omlor AM, Buckpitt AR, Tarkington BK, Wong VJ, Joad JP, Pinkerton KB, Wu R, Evans MJ, Hyde DM, Plopper CG: Allergic asthma induced in rhesus monkeys by house dust mite (Dermatophagoides farinae) . Am J Pathol 2001; 158: 333-341.
42. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals: Guide for the Care and Use of Laboratory Animals, ed 8. Washington, National Academies Press, 2011.
43. Wilson DW, Plopper CG, Dungworth DL: The response of the macaque tracheobronchial epithelium to acute ozone injury. A quantitative ultrastructural and autoradiographic study. Am J Pathol 1984; 116: 193-206.
44. Arvidsson LE, Hacksell U, Nilsson JL, Hjorth S, Carlsson A, Lindberg P, Sanchez D, Wikstrom H: 8-hydroxy-2-(di-n-propylamino) tetralin, a new centrally acting 5-hydroxytryptamine receptor agonist. J Med Chem 1981; 24: 921-923.
45. Middlemiss DN, Fozard JR: 8-hydroxy-2-(di-n-propylamino)-tetralin discriminates between subtypes of the 5-HT1 recognition site. Eur J Pharmacol 1983; 90: 151-153.
46. Peroutka SJ: Pharmacological differentiation and characterization of 5-HT1A, 5-HT1B, and 5-HT1C binding sites in rat frontal cortex. J Neurochem 1986; 47: 529-540.
47. Leung GP, Dun SL, Dun NJ, Wong PY: Serotonin via 5-HT1B and 5-HT2B receptors stimulates anion secretion in the rat epididymal epithelium. J Physiol 1999; 519: 657-667.
48. Feldman PD: Effects of serotonin-1 and serotonin-2 receptor agonists on neuronal activity in the nucleus tractus solitarius. J Auton Nerv Syst 1995; 56: 119-124.
49. Ismaiel AM, Titeler M, Miller KJ, Smith TS, Glennon RA: 5-HT1 and 5-HT2 binding profiles of the serotonergic agents alpha-methylserotonin and 2-methylserotonin. J Med Chem 1990; 33: 755-758.
50. Wilson H, Coffman WJ, Cohen ML: 5-hydroxytryptamine3 receptors mediate tachycardia in conscious instrumented dogs. J Pharmacol Exp Ther 1990; 252: 683-688.
51. Craig DA, Eglen RM, Walsh LK, Perkins LA, Whiting RL, Clarke DE: 5-methoxytryptamine and 2-methyl-5-hydroxytryptamine-induced desensitization as a discriminative tool for the 5-HT3 and putative 5-HT4 receptors in guinea pig ileum. Naunyn Schmiedebergs Arch Pharmacol 1990; 342: 9-16.
52. Glennon RA, Lee M, Rangisetty JB, Dukat M, Roth BL, Savage JE, McBride A, Rauser L, Hufeisen S, Lee DK: 2-substituted tryptamines: agents with selectivity for 5-HT(6) serotonin receptors. J Med Chem 2000; 43: 1011-1018.
53. Yang D, Soulier JL, Sicsic S, Mathe-Allainmat M, Bremont B, Croci T, Cardamone R, Aureggi G, Langlois M: New esters of 4-amino-5-chloro-2- methoxybenzoic acid as potent agonists and antagonists for 5-HT4 receptors. J Med Chem 1997; 40: 608-621.
54. De Ponti F, Crema F, Moro E, Nardelli G, Croci T, Frigo GM: Intestinal motor stimulation by the 5-HT4 receptor agonist ml10302: differential involvement of tachykininergic pathways in the canine small bowel and colon. Neurogastroenterol Motil 2001; 13: 543-553.
55. Soulier JL, Russo O, Giner M, Rivail L, Berthouze M, Ongeri S, Maigret B, Fischmeister R, Lezoualc'h F, Sicsic S, Berque-Bestel I: Design and synthesis of specific probes for human 5-HT4 receptor dimerization studies. J Med Chem 2005; 48: 6220-6228.
56. Frishman WH, Grewall P: Serotonin and the heart. Ann Med 2000; 32: 195-209.
57. Ju JM, Hwang JH, Piao LH, Park HW, Park JS, Shin DH, Cho JG, Kim KK, Kim JH: Ketanserin, a 5-HT2 antagonist, directly inhibits the ATP-sensitive potassium channel in mouse ventricular myocytes. J Cardiovasc Pharmacol 2006; 47: 96-102.
58. Ye JH, Ponnudurai R, Schaefer R: Ondansetron: A selective 5-HT(3) receptor antagonist and its applications in CNS-related disorders. CNS Drug Rev 2001; 7: 199-213.
59. Youssefyeh RD, Campbell HF, Klein S, Airey JE, Darkes P, Powers M, Schnapper M, Neuenschwander K, Fitzpatrick LR, Pendley CE, et al: Development of high-affinity 5-HT3 receptor antagonists. 1. Initial structure-activity relationship of novel benzamides. J Med Chem 1992; 35: 895-903.
60. Tuladhar BR, Costall B, Naylor RJ: Modulation of 5-HT4 receptor function in the rat isolated ileum by fluoxetine: the involvement of endogenous 5-hydroxytryptamine. Br J Pharmacol 2002; 136: 150-156.
61. Pindon A, van Hecke G, van Gompel P, Lesage AS, Leysen JE, Jurzak M: Differences in signal transduction of two 5-HT4 receptor splice variants: compound specificity and dual coupling with galphas- and galphai/ o-proteins. Mol Pharmacol 2002; 61: 85-96.
62. Gale JD, Grossman CJ, Whitehead JW, Oxford AW, Bunce KT, Humphrey PP: Gr113808: a novel, selective antagonist with high affinity at the 5-HT4 receptor. Br J Pharmacol 1994; 111: 332-338.
63. Matera MG, De Santis D, D'Agostino B, Pallotta M, Vacca C, Cazzola M, Rossi F: Role of 5-hydroxytryptamine in mediating adenosine-induced airway contraction. Immunopharmacology 1995; 29: 73-78.
64. Rizzo CA, Kreutner W, Chapman RW: 5-HT3 receptors augment neuronal, cholinergic contractions in guinea pig trachea. Eur J Pharmacol 1993; 234: 109-112.
65. Cazzola M, D'Amato G, Lobefalo G, Guillaro B, Sepe J, Assogna G, Pietroletti R, Lauria D: Ketanserin, a new blocking agent of serotonin S2-receptors. Respiratory functional effects in chronic obstruction of the airways. Chest 1987; 92: 863-866.
66. Lechin F, van der Dijs B, Lechin AE: Treatment of bronchial asthma with tianeptine. Methods Find Exp Clin Pharmacol 2004; 26: 697-701.
67. Lechin F, van der Dijs B, Lechin AE: Tianeptine: a new exploratory therapy for asthma. Chest 2004; 125: 348-349.
68. Bateson TF, Schwartz J: Children's response to air pollutants. J Toxicol Environ Health A 2008; 71: 238-243.
69. House-dust mite allergen and asthma. N Engl J Med 1991; 324: 337-338.
70. Bertelsen RJ, Carlsen KC, Carlsen KH, Granum B, Doekes G, Haland G, Mowinckel P, Lovik M: Childhood asthma and early life exposure to indoor allergens, endotoxin and beta(1,3)-glucans. Clin Exp Allergy;40: 307-316.
71. Brookes KA, Adams WC, Schelegle ES: O.35 ppm O3 exposure induces hyperresponsiveness on 24-h reexposure to 0.20 ppm O3. J Appl Physiol 1989; 66: 2756-2762.
72. Fanucchi MV, Plopper CG, Evans MJ, Hyde DM, Van Winkle LS, Gershwin LJ, Schelegle ES: Cyclic exposure to ozone alters distal airway development in infant rhesus monkeys. Am J Physiol Lung Cell Mol Physiol 2006; 291:L644-L650.
73. Gent JF, Triche EW, Holford TR, Belanger K, Bracken MB, Beckett WS, Leaderer BP: Association of low-level ozone and fine particles with respiratory symptoms in children with asthma. JAMA 2003; 290: 1859-1867.
74. Joad JP, Kott KS, Bric JM, Peake JL, Plopper CG, Schelegle ES, Gershwin LJ, Pinkerton KE: Structural and functional localization of airway effects from episodic exposure of infant monkeys to allergen and/or ozone. Toxicol Appl Pharmacol 2006; 214: 237-243.
75. Koren HS: Associations between criteria air pollutants and asthma. Environ Health Perspect 1995; 103 Suppl 6: 235-242.
76. Moore K, Neugebauer R, Lurmann F, Hall J, Brajer V, Alcorn S, Tager I: Ambient ozone concentrations cause increased hospitalizations for asthma in children: an 18-year study in southern California. Environ Health Perspect 2008; 116: 1063-1070.
77. Schelegle ES, Adams WC, Giri SN, Siefkin AD: Acute ozone exposure increases plasma prostaglandin f2 alpha in ozone-sensitive human subjects. Am Rev Respir Dis 1989; 140: 211-216.
78. Schelegle ES, Adams WC: Reduced exercise time in competitive simulations consequent to low level ozone exposure. Med Sci Sports Exerc 1986; 18: 408-414.
79. Moura CT, Bezerra FC, de Moraes IM, Magalhaes PJ, Capaz FR: Increased responsiveness to 5-hydroxytryptamine after antigenic challenge is inhibited by nifedipine and niflumic acid in rat trachea in vitro. Clin Exp Pharmacol Physiol 2005; 32: 1119-1123.
80. Avdalovic MV, Putney LF, Schelegle ES, Miller L, Usachenko JL, Tyler NK, Plopper CG, Gershwin LJ, Hyde DM: Vascular remodeling is airway generation-specific in a primate model of chronic asthma. Am J Respir Crit Care Med 2006; 174: 1069-1076.