The role of inflammatory mediators in the synergistic toxicity of ozone and 1-nitronaphthalene in rat airways

Environmental Health Perspectives

Volumn 114, Issue 9, 2006, Pages 1354-1360

  Schmelzer, Kara R ^a   Wheelock, Åsa M ^a   Dettmer, Katja ^a   Morin, Dexter ^a   Hammock, Bruce D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

1 nitronaphthalene; Arachidonic acid; Cyclooxygenase; Inflammatory mediators; Linoleic acid; Lipoxygenase; Ozone

Indexed keywords

1 NITRONAPHTHALENE; ARACHIDONIC ACID; AUTACOID; CHEMOKINE; CILIARY NEUROTROPHIC FACTOR; CYTOKINE; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; FRACTALKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; LEPTIN; LINOLEIC ACID; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; NERVE GROWTH FACTOR BETA SUBUNIT; PEPTIDOLEUKOTRIENE; SODIUM PEROXIDE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; VASCULOTROPIN;

AIR POLLUTION; AMBIENT AIR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOCHEMISTRY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIESEL ENGINE; DISEASE PREDISPOSITION; ENVIRONMENTAL EXPOSURE; EXHAUST GAS; IMMUNE RESPONSE; LUNG INJURY; LUNG LAVAGE; MALE; METABOLOMICS; NONHUMAN; PARTICULATE MATTER; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; RESPIRATORY TRACT DISEASE; TH1 CELL; TH2 CELL; TIME;

ADMINISTRATION, INHALATION; AIR POLLUTANTS; ANIMALS; CHEMOKINES; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; INFLAMMATION MEDIATORS; INHALATION EXPOSURE; LUNG; MALE; NAPHTHALENES; OZONE; PULMONARY CIRCULATION; RATS; RATS, SPRAGUE-DAWLEY; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 33748207355     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.8373     Document Type: Article

References (68)

1. Atkinson R, Arey J. 1994. Atmospheric chemistry of gas-phase polycyclic aromatic hydrocarbons: formation of atmospheric mutagens. Environ Health Perspect 102(suppl 4):117-126.
2. Balmes JR, Aris RM, Chen LL, Scannell C, Tager IB, Finkbeiner W, et al. 1997. Effects of ozone on normal and potentially sensitive human subjects. Part I: airway inflammation and responsiveness to ozone in normal and asthmatic subjects. Res Rep Health Eff Inst(78):1-37.
3. Barnes NC, Piper PJ, Costello JF. 1984. Comparative effects of inhaled leukotriene C4, leukotriene D4, and histamine in normal human subjects, Thorax 39(7):500-504.
4. Barr BC, Hyde DM, Plopper CG, Dungworth DL. 1990. A comparison of terminal airway remodeling in chronic daily versus episodic ozone exposure. Toxicol Appl Pharmacol 106:384-407.
5. Bosson J, Stenfors N, Bucht A, Helleday R, Pourazar J, Holgate ST, et al. 2003. Ozone-induced bronchial epithelial cytokine expression differs between healthy and asthmatic subjects. Clin Exp Allergy 33(6):777-782.
6. Bradding P, Redington AE, Djukanovic R, Conrad DJ, and Holgate ST. 1995. 15-Lipoxygenase immunoreactivity in normal and in asthmatic airways. Am J Respir Crit Care Med 151:1201-1204.
7. Braun A, Appel E, Baruch R, Herz U, Botchkarev V, Paus R, et al. 1998. Role of nerve growth factor in a mouse model of allergic airway inflammation and asthma. Eur J lmmunol 28(10):3240-3251.
8. Chang LY, Huang Y, Stockstill BL, Graham JA, Grose EC, Menache MG, et al. 1992. Epithelial injury and interstitial fibrosis in the proximal alveolar regions of rats chronically exposed to a simulated pattern of urban ambient ozone. Toxicol Appl Pharmacol 115(2):241-252.
9. Coffey MJ, Wheeler CS, Gross KB, Eschenbacher WL, Sporn PH, Peters-Golden M. 1996, Increased 5-lipoxygenase metabolism in the lungs of human subjects exposed to ozone. Toxicology 114(3):187-197.
10. Connor LM, Ballinger CA, Albrecht TB, Postlethwait EM. 2004. Interfacial phospholipids inhibit ozone-reactive absorption-mediated cytotoxicity in vitro. Am J Physiol Lung Cell Mol Physiol 286(6):L1169-1178.
11. Crivello JV. 1981. Nitrations and oxidations with inorganic nitrate salts in trifluoroacetic anhydride. J Org Chem 46:3056-3062.
12. Devlin RB, McDonnell WF, Becker S, Madden MC, McGee MP, Perez R, et al. 1996. Time-dependent changes of inflammatory mediators in the lungs of humans exposed to 0.4 ppm ozone for 2 hr: a comparison of mediators found in broncho-alveolar lavage fluid 1 and 18 hr after exposure. Toxicol Appl Pharmacol 138(1):176-185.
13. de Waai, Mareiyt R, Abrams J, Bennen B. Figdor CG, de Vries JE. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 174:1209-1220.
14. Draper W. 1986. Quantitation of nitro- and dinitropolycyclic aromatic hydrocarbons in diesel exhaust particulate matter. Chemosphere 15:437-447.
15. Drazen JM, Austen KF, Lewis RA, Clark DA, Goto G, Marfat A, et al. 1980. Comparative airway and vascular activities of leukotrienes C-1 and D in vivo and in vitro. Proc Natl Acad Sci USA 77(7):4354-4358.
16. Driscoll KE, Simpson L, Carter J, Hassenbein D, Leikauf GD. 1993. Ozone inhalation stimulates expression of a neutrophil chemotactic protein, macrophage inflammatory protein 2. Toxicol Appl Pharmacol 119(2):306-309.
17. Duan X, Buckpitt AR, Pinkerton KE, Ji C, Plopper CG. 1996. Ozone-induced alterations in glutathione in lung subcompartments of rats and monkeys. Am J Respir Cell Mol Biol 14(1):70-75.
18. Dudda A, Spiteller G, Kobelt F. 1996. Lipid oxidation products in ischemic porcine heart tissue. Chem Phys Lipids 82:39-51.
19. Gauderman WJ, Avol E, Gilliland F, Vora H, Thomas D, Berhane K, et al. 2004. The effect of air pollution on lung development from 10 to 18 years of age. N Engl J Med 351(11):1057-1067.
20. Gershwin LJ, Osebold JW, Zee YC. 1981. Immunoglobulin E-containing cells in mouse lung following allergen inhalation and ozone exposure. Int Arch Allergy Appl Immunol 65(3):266-277.
21. Harkerna JR, Plopper CG, Hyde DM, St George JA, Wilson DW, Dungworth DL. 1987. Response of the macaque nasal epithelium to ambient levels of ozone. A morphologic and morphometric study of the transitional and respiratory epithelium. Am J Pathol 128(1):29-44.
22. Hayakawa M, Kosaka K, Sugiyama S, Yokoo K, Aoyama H, lzawa Y, at al. 1990. Proposal of leukotoxin, 9,10-epoxy-12-octadecenoate, as a burn toxin. Biochem Int 21(3):573-579.
23. Hiltermann TJ, Peters EA, Alberts B, Kwikkers K, Borggreven PA, Hiemstra PS, et al. 1998. Ozone-induced airway hyperresponsiveness in patients with asthma: role of neutrophil-derived serine proteinases. Free Radic Biol Med 24(6):952-958.
24. Howard M. 1992. Biological properties of interleukin 10. J Clin Immunol 12:239-247.
25. Institute of Laboratory Animal Resources. 1996. Guide for the Care and Use of Laboratory Animals. 7th ed. Washington, DC:National Academy Press.
26. Ishihara Y, Kagawa J. 2003. Chronic diesel exhaust exposures of rats demonstrate concentration and time-dependent effects on pulmonary inflammation. Inhal Toxicol 15:473-492.
27. Ishii Y, Yang H, Sakamoto T, Nomura A, Hasegawa S, Hirata F, et al. 1997. Rat alveolar macrophage cytokine production and regulation of neutrophil recruitment following acute ozone exposure. Toxicol Appl Pharmacol 147(2):214-223.
28. Ishizaki T, Shigemori K, Ameshim S, Nakai T, Miyabo S, Hayakawa M, et al. 1996. Protective effects of BO-123, an ETA receptor antagonist, against leukotoxin-induced injury in rat lungs. Am J Physiol 271:L459-L463.
29. Joad JP, McDonald RJ, Gin SN, Bric JM. 1994. Ozone effects on mechanics and arachidonic acid metabolite concentrations in isolated rat lungs. Environ Res 66(2):186-197.
30. Kelly FJ, Mudway l, Krishna MT, Holgate ST. 1995. The free radical basis of air pollution: focus an ozone. Respir Mod 89(10):647-656.
31. Kim IH, Morisseau C, Watanabe T, Hammock BD. 2004. Design, synthesis, and biological activity of 1,3-disubstituted ureas as potent inhibitors of the soluble epoxide hydrolase of increased water solubility. J Med Chem 47(8):2110-2122.
32. Kishi N, Mano N, Asakawa N. 2001. Direct injection method for quantitation of endogenous leukotriene E4 in human urine by liquid chromatography/electrospray ionization tandem mass spectrometry with a column-switching technique. Anal Sci 17(6):709-713.
33. Kleeberger SR, Ohtsuka Y, Zhang LY, Longphre M. 2001. Airway responses to chronic ozone exposure are partially mediated through mast cells. J Appl Physiol 90(2):713-723.
34. Kuhn H. 1996. Biosynthesis, metabolization and biological importance of the primary 15-lipoxygenase metabolites 15-hydro(pero)XY-5Z,8Z,11Z,13E-eicosatetraenoic acid and 13-hydro(pero)XY-9Z, 11E-octadecadienoic acid. Prog Lipid Res 35(3):203-226.
35. Maggi E, Parronchi P, Manetti R, Simonelli C, Piccinni MP, Rugiu FS, et al. 1992. Reciprocal regulatory effects of IFN-γ and IL-1 on the in vitro development of human Th1 and Th2 clones. J Immunol 148(7):2142-2147.
36. Marom Z, Shelhamer JH, Bach MK, Morton DR, Kaliner M. 1982. Slow-reacting substances, leukotrienes C4 and D4, increase the release of mucus from human airways in vitro. Am Rev Respir Dis 126(3):449-451.
37. Marom Z, Shelhamer JH, Sun F, Kaliner M. 1983. Human airway monohydroxyeicosatetraenoic acid generation and mucus release. J Clin Invest 72(1):122-127.
38. Newman JW, Watanabe T, Hammock ED. 2002. The simultaneous quantification of cytochrome P450 dependent linoleate and arachidonate metabolites in urine by HPLC-MS/MS. J Lipid Res 43 (9):1563-1578.
39. Ozawa T, Sugiyama S, Hayakawa M, Satake T, Taki F, lwata M, et al. 1988. Existence of leukotoxin 9,10-epoxy-12-octadecenoate in lung lavage from rats breathing pure oxygen and from patients with the adult respiratory distress syndrome Am Rev Respir Dis 137(3):535-540.
40. Paige RC, Plopper CG. 1999. Acute and chronic effects of ozone in animal models. In: Air Pollution and Health (Holgate ST, Samet JM, Koren HS, Maynard RL, eds). London:Academic Press, 531-557.
41. Paige RC, Royce FH, Plopper CG, Buckpitt AR. 2000a. Long-term exposure to ozone increases acute pulmonary centriacinar injury by 1-nitronaphthalene: I. Region-specific enzyme activity. J Pharmacol Exp Ther 295(3):934-941.
42. Paige RC, Wong V, Plopper CG. 1997. Dose-related airway-selective epithelial toxicity of 1-nitronaphthalene in rats. Toxicol Appl Pharmacol 147(2):224-233.
43. Paige RC, Wong V, Plopper CG. 2000b. Long-term exposure to ozone increases acute pulmonary centriacinar injury by 1-nitronaphthalone: II. Quantitative histopathology. J Pharmacol Exp Ther 295 (3):942-950.
44. Pinkerton KE, Dodge DE, Cederdahl-Demmler J, Wong VJ, Peake J, Haselton CJ, et al. 1993. Differentiated bronchiolar epithelium in alveolar ducts of rats exposed to ozone for 20 months. Am J Pathol 142(3):947-956.
45. Plopper CG, Chu FP, Haselton CJ, Peake J, Wu J, Pinkerton KE. 1994a. Dose-dependent tolerance to ozone. I. Tracheo-bronchial epithelial reorganization in rats after 20 months' exposure. Am J Pathol 144(2):404-420.
46. Plopper CG, Duan X, Buckpitt AR, Pinkerton KE. 1994b. Dose-dependent tolerance to ozone. IV. Site-specific elevation in antioxidant enzymes in the lungs of rats exposed for 90 days or 20 months. Toxicol Appl Pharmacol 127:124-131.
47. Pryor WA. 1994. Mechanisms of radical formation from reactions of ozone with target molecules in the lung. Free Radic Biol Med 17(5):451-465.
48. Pulfer MK, Taube C, Gelfand E, Murphy RC. 2005. Ozone exposure in vivo and formation of biologically active oxysterols in the lung. J Pharmacol Exp Ther 312(1):256-264.
49. Putman E, van Golde LM, Haagsman HP. 1997. Toxic oxidant species and their impact on the pulmonary surfactant system. Lung 175(2):75-103.
50. Quarcoo D, Schulte-Herbruggen O, Lommatzsch M, Schierhorn K, Hoyle GW, Renz H, et al. 2004. Nerve growth factor induces increased airway inflammation via a neuropeptide-dependent mechanism in a transgenic animal model of allergic airway inflammation. Clin Exp Allergy 34(7): 146-1151.
51. Sanico AM, Stanisz AM, Gleeson TD, Bora S, Proud D, Bienenstock J, et al. 2000 Nerve growth factor expression and release in allergic inflammatory disease of the upper airways. Am J Respir Crit Care Med 161(5):1631-1635.
52. Sauer JM, Eversole RR, Lehmann CL, Johnson DE, Beuving LJ. 1997. An ultrastructural evaluation of acute 1-nitronaphthalene induced hepatic and pulmonary toxicity in the rat. Toxicol Lett 90(1):19-27.
53. Schlesinger RB, Driscoll KE, Gunnison AF, Zelikoff JT. 1990. Pulmonary arachidonic acid metabolism following acute exposures to ozone and nitrogen dioxide. J Toxicol Environ Health 31(4):275-290.
54. Schmelzer KR, Kubala L, Newman JW, Kim IH, Eiserich JP, Hammock BD. 2005. Soluble epoxide hydrolase is a therapeutic target for acute inflammation. Proc Natl Acad Sci USA 102(28):9772-9777.
55. Spanbroek R, Hildner M, Steinhilber D, Fusenig N, Yoneda K, Radmark O, at al. 2000. 5-Lipoxygenase expression in dendritic cells generated from CD34(+) hematopoietic progenitors and in lymphoid organs. Blood 96(12):3B57-3865.
56. Stankova J, Rola-Pleszczynski M, Dubois CM. 1995. Granulocytemacrophage colony-stimulating factor increases 5-lipoxygenase gene transcription and protein expression in human neutrophils. Blood 85(12):3719-3726.
57. Stockstill BL, Chang LY, Menache MG, Mellick PW, Mercer RR, Crapo JD. 1995. Bronchiolarized metaplasia and interstitial fibrosis in rat lungs chronically exposed to high ambient levels of ozone. Toxicol Appl Pharmacol 134(2):251-263.
58. U.S. Environmental Protection Agency (EPA). 2000. Air Quality and Emission Trends Report. Research Triangle Park, NC:U.S. Environmental Protection Agency.
59. van Bree L, Dormans JA, Boere AJ, Rombout PJ. 2001. Time study on development and repair of lung injury following ozone exposure in rats. Inhal Toxicol 13(8):703-718.
60. Van Scott MR, McIntire MR, Henke DC. 199D. Arachidonic acid metabolism and regulation of ion transport in rabbit Clara cells. Am J Physiol 259(4 Pt 1):L213-L221.
61. Verschoyle RD, Carthew P, Wolf CR, Dinsdale D. 1993. 1-Nitronaphthalene toxicity in rat lung and liver: effects of inhibiting and inducing cytochrome P450 activity. Toxicol Appl Pharmacol 122:208-213.
62. Verschoyle RD, Dinsdale D. 1990. Protection against chemical-induced lung injury by inhibition of pulmonary cytochrome P-450. Environ Health Perspect 85:95-100.
63. Warren DL, Brown DL Jr, Buckpitt AR. 1982. Evidence for cytochrome P-450 mediated metabolism in the bronchiolar damage by naphthalene. Chem Biol Interact 40:287-303.
64. Watanabe T, Morisseau C, Newman JW, Hammock BD. 2003. In vitro metabolism of the mammalian soluble opoxide hydrolase inhibitor, 1-cyclohexyl-3-dodecyl-urea. Drug Metab Dispos 31(7): 846-853.
65. Watt KC, Morin DM, Kurth MJ, Mercer RS, Plopper CG, Buckpitt AR. 1999. Glutathione conjugation of electrophilic metabolites of 1-nitronaphthalene in rat tracheobronchial airways and liver: identification by mass spectrometry and proton nuclear magnetic resonance spectroscopy. Chem Res Toxicol 12:831-839.
66. West JA, Pakehham G, Morin D, Fleschner CA, Buckpitt AR, Plopper CG. 2001. Inhaled naphthalene causes dose dependent Clara cell cytotoxicity in mice but not in rats. Toxicol Appl Pharmacol 173:114-119.
67. Wheelock AM, Boland BC, Isbell M, Morin D, Wegesser TC, Plopper CG, Buckpitt AR. 2005. In vivo effects of ozone exposure on protein adduct formation by 1-nitronaphthalene in rat lung. Am J Respir Cell Vol Biol 33(2):130-137.
68. Wheelock AM, Zhang L, Tran MU, Morin D, Penn S, Buckpitt AR, et al. 2004. Isolation of rodent airway epithelial cell proteins facilitates in vivo proteomics studies of lung toxicity. Am J Physiol Lung Cell Mol Physiol 286(2):L399-L410.