Persistent rhinitis and epithelial remodeling induced by cyclic ozone exposure in the nasal airways of infant monkeys

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 300, Issue 2, 2011, Pages

  Carey, Stephan A ^a   Ballinger, Carol A ^b   Plopper, Charles G ^c,d   McDonald, Ruth J ^d   Bartolucci, Alfred A ^b   Postlethwait, Edward M ^b   Harkema, Jack R ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c School of Veterinary Medicine   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Air pollution; Children; Epithelial hyperplasia; Glutathione; Nasal epithelium; Squamous metaplasia

Indexed keywords

ASCORBIC ACID; GLUTATHIONE; GLUTATHIONE DISULFIDE; OZONE; URIC ACID;

AIRWAY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CORRELATION ANALYSIS; EPITHELIUM CELL; EPITHELIUM HYPERPLASIA; EXPOSURE; HISTOPATHOLOGY; MALE; MORPHOMETRICS; NONHUMAN; NOSE MUCOSA; PRIORITY JOURNAL; RHESUS MONKEY; RHINITIS; SQUAMOUS CELL METAPLASIA;

AIR POLLUTANTS; ANIMALS; ANTIOXIDANTS; CHILD; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; HUMANS; MACACA MULATTA; MALE; METAPLASIA; NASAL MUCOSA; NEUTROPHILS; OZONE; RHINITIS; RNA, MESSENGER;

EID: 79551557257     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00177.2010     Document Type: Article

References (73)

1. Abel K, Rocke DM, Chohan B, Fritts L, Miller CJ. Temporal and anatomic relationship between virus replication and cytokine gene expression after vaginal simian immunodeficiency virus infection. J Virol 79: 12164-12172, 2005.
2. Air Resources Board. Review of the California Ambient Air Quality Standard for Ozone. Sacramento, CA: Air Resources Board, 2005.
3. Akguner M, Barutcu A, Karaca C. Adolescent growth patterns of the bony and cartilaginous framework of the nose: a cephalometric study. Ann Plast Surg 41: 66-69, 1998.
4. Bateson TF, Schwartz J. Children's response to air pollutants. J Toxicol Environ Health A 71: 238-243, 2008.
5. Brain JD. The uptake of inhaled gases by the nose. Ann Otol Rhinol Laryngol 79: 529-539, 1970.
6. Calderon-Garciduenas L, Osorno-Velazquez A, Bravo-Alvarez H, Delgado-Chavez R, Barrios-Marquez R. Histopathologic changes of the nasal mucosa in southwest Metropolitan Mexico City inhabitants. Am J Pathol 140: 225-232, 1992.
7. Calderon-Garciduenas L, Rodriguez-Alcaraz A, Garcia R, Sanchez G, Barragan G, Camacho R, Ramirez L. Human nasal mucosal changes after exposure to urban pollution. Environ Health Perspect 102: 1074-1080, 1994.
8. Calderon-Garciduenas L, Rodriguez-Alcaraz A, Valencia-Salazar G, Mora-Tascareno A, Garcia R, Osnaya N, Villarreal-Calderon A, Devlin RB, Van Dyke T. Nasal biopsies of children exposed to air pollutants. Toxicol Pathol 29: 558-564, 2001.
9. Calderon-Garciduenas L, Valencia-Salazar G, Rodriguez-Alcaraz A, Gambling TM, Garcia R, Osnaya N, Villarreal-Calderon A, Devlin RB, Carson JL. Ultrastructural nasal pathology in children chronically and sequentially exposed to air pollutants. Am J Respir Cell Mol Biol 24: 132-138, 2001.
10. Carey SA, Garcia GJ, Minard KR, Einstein DR, Ballinger CA, Wagner JG, Plopper CG, Corley RA, Postlethwait EM, Kimbell JS, Harkema JR. Use of magnetic resonance (MR) imaging, light microscopy, and three-dimensional (3D) reconstruction in epithelial mapping of the nasal airways of infant rhesus monkeys (Abstract). Am J Respir Crit Care Med 175: A1357, 2007.
11. Carey SA, Minard KR, Trease LL, Wagner JG, Garcia GJ, Ballinger CA, Kimbell JS, Plopper C, Corley RA, Postlethwait EM, Harkema JR. Three-dimensional mapping of ozone-induced injury in the nasal airways of monkeys using magnetic resonance imaging and morphometric techniques. Toxicol Pathol 35: 27-40, 2007.
12. Carey SA, Wagner JG, Plopper CG, Postlethwait EM, Harkema JR. Acute and episodic ozone exposures induce similar epithelial lesions in the anterior nasal airways of infant rhesus monkeys (Abstract). Proc Am Thorac Soc 3: A388, 2006.
13. Castleman WL, Dungworth DL, Schwartz LW, Tyler WS. Acute respiratory bronchiolitis: an ultrastructural and autoradiographic study of epithelial cell injury and renewal in rhesus monkeys exposed to ozone. Am J Pathol 98: 811-840, 1980.
14. Cavanagh DG, Morris JB. Mucus protection and airway peroxidation following nitrogen dioxide exposure in the rat. J Toxicol Environ Health 22: 313-328, 1987.
15. Cho HY, Hotchkiss JA, Harkema JR. Inflammatory and epithelial responses during the development of ozone-induced mucous cell metaplasia in the nasal epithelium of rats. Toxicol Sci 51: 135-145, 1999.
16. Ciencewicki J, Jaspers I. Air pollution and respiratory viral infection. Inhal Toxicol 19: 1135-1146, 2007.
17. Cross CE, Halliwell B, Allen A. Antioxidant protection: a function of tracheobronchial and gastrointestinal mucus. Lancet 1: 1328-1330, 1984.
18. Cross CE, van der Vliet A, O'Neill CA, Louie S, Halliwell B. Oxidants, antioxidants, and respiratory tract lining fluids. Environ Health Perspect 102, Suppl 10: 185-191, 1994.
19. Dibbert B, Weber M, Nikolaizik WH, Vogt P, Schoni MH, Blaser K, Simon HU. Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. Proc Natl Acad Sci USA 96: 13330-13335, 1999.
20. Duan X, Buckpitt AR, Pinkerton KE, Ji C, Plopper CG. Ozone-induced alterations in glutathione in lung subcompartments of rats and monkeys. Am J Respir Cell Mol Biol 14: 70-75, 1996.
21. Fievez L, Kirschvink N, Dogne S, Jaspar F, Merville MP, Bours V, Lekeux P, Bureau F. Impaired accumulation of granulocytes in the lung during ozone adaptation. Free Radic Biol Med 31: 633-641, 2001.
22. Fusco D, Forastiere F, Michelozzi P, Spadea T, Ostro B, Arca M, Perucci CA. Air pollution and hospital admissions for respiratory conditions in Rome, Italy. Eur Respir J 17: 1143-1150, 2001.
23. Garcia GJ, Schroeter JD, Segal RA, Stanek J, Foureman GL, Kimbell JS. Dosimetry of nasal uptake of water-soluble and reactive gases: a first study of interhuman variability. Inhal Toxicol 21: 607-618, 2009.
24. Gore F, Regondi I, Schratz A, Solmi F. Children's Environmental Health Indicators: Presenting Regional Successes, Learning for the Future. Geneva: World Health Organization, 2009, p. 1-24.
25. Graham D, Henderson F, House D. Neutrophil influx measured in nasal lavages of humans exposed to ozone. Arch Environ Health 43: 228-233, 1988.
26. Graham DE, Koren HS. Biomarkers of inflammation in ozone-exposed humans. Comparison of the nasal and bronchoalveolar lavage. Am Rev Respir Dis 142: 152-156, 1990.
27. Harkema JR, Carey SA, Wagner JG. The nose revisited: a brief review of the comparative structure, function, and toxicologic pathology of the nasal epithelium. Toxicol Pathol 34: 252-269, 2006.
28. Harkema JR, Hotchkiss JA. In vivo effects of endotoxin on nasal epithelial mucosubstances: quantitative histochemistry. Exp Lung Res 17: 743-761, 1991.
29. Harkema JR, Hotchkiss JA, Henderson RF. Effects of 0.12 and 0.80 ppm ozone on rat nasal and nasopharyngeal epithelial mucosubstances: quantitative histochemistry. Toxicol Pathol 17: 525-535, 1989.
30. Harkema JR, Plopper CG, Hyde DM, St George JA, Dungworth DL. Effects of an ambient level of ozone on primate nasal epithelial mucosubstances. Quantitative histochemistry. Am J Pathol 127: 90-96, 1987.
31. Harkema JR, Plopper CG, Hyde DM, St George JA, Wilson DW, Dungworth DL. 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: 29-44, 1987.
32. Hellings PW, Hens G. Rhinosinusitis and the lower airways. Immunol Allergy Clin North Am 29: 733-740, 2009.
33. Hotchkiss JA, Hilaski R, Cho H, Regan K, Spencer P, Slack K, Harkema JR. Fluticasone propionate attenuates ozone-induced rhinitis and mucous cell metaplasia in rat nasal airway epithelium. Am J Respir Cell Mol Biol 18: 91-99, 1998.
34. Hubal EA, Kimbell JS, Fedkiw PS. Incorporation of nasal-lining mass-transfer resistance into a CFD model for prediction of ozone dosimetry in the upper respiratory tract. Inhal Toxicol 8: 831-857, 1996.
35. Hyde DM, Magliano DJ, Plopper CG. Morphometric assessment of pulmonary toxicity in the rodent lung. Toxicol Pathol 19: 428-446, 1991.
36. Hyde DM, Plopper C, St George JA, Harkema JR. Morphometric cell biology of airspace epithelium. In: Electron Microscopy of the Lung, edited by Schraufnagel DE. New York: Dekker, 1990, p. 1-120.
37. Jany B, Gallup M, Tsuda T, Basbaum C. Mucin gene expression in rat airways following infection and irritation. Biochem Biophys Res Commun 181: 1-8, 1991.
38. Jiang XZ, Morgan KT, Beauchamp RW. Histopathology of acute and subacute nasal toxicity. In: Toxicology of the Nasal Passages, edited by Barrow CS. New York: Hemisphere, 1986, p. 51-66.
39. Kepler GM, Joyner DR, Fleishman A, Richardson RB, Gross EA, Morgan KT, Godo MN, Kimbell JS. Method for obtaining accurate geometrical coordinates on nasal airways for computer dosimetry modeling and lesion mapping. Inhal Toxicol 7: 1207-1224, 1995.
40. Kim JJ. Ambient air pollution: health hazards to children. Pediatrics 114: 1699-1707, 2004.
41. Kimball RE, Reddy K, Peirce TH, Schwartz LW, Mustafa MG, Cross CE. Oxygen toxicity: augmentation of antioxidant defense mechanisms in rat lung. Am J Physiol 230: 1425-1431, 1976.
42. Kimbell JS. Nasal dosimetry of inhaled gases and particles: where do inhaled agents go in the nose? Toxicol Pathol 34: 270-273, 2006.
43. Kimbell JS, Gross EA, Richardson RB, Conolly RB, Morgan KT. Correlation of regional formaldehyde flux predictions with the distribution of formaldehyde-induced squamous metaplasia in F344 rat nasal passages. Mutat Res 380: 143-154, 1997.
44. Kimbell JS, Overton JH, Subramaniam RP, Schlosser PM, Morgan KT, Conolly RB, Miller FJ. Dosimetry modeling of inhaled formaldehyde: binning nasal flux predictions for quantitative risk assessment. Toxicol Sci 64: 111-121, 2001.
45. Kleeberger SR. Genetic aspects of susceptibility to air pollution. Eur Respir J Suppl 21: 52S-56S, 2003.
46. Kleeberger SR, Bassett DJ, Jakab GJ, Levitt RC. A genetic model for evaluation of susceptibility to ozone-induced inflammation. Am J Physiol Lung Cell Mol Physiol 258: L313-L320, 1990.
47. Kopp MV, Ulmer C, Ihorst G, Seydewitz HH, Frischer T, Forster J, Kuehr J. Upper airway inflammation in children exposed to ambient ozone and potential signs of adaptation. Eur Respir J 14: 854-861, 1999.
48. Koren HS, Hatch GE, Graham DE. Nasal lavage as a tool in assessing acute inflammation in response to inhaled pollutants. Toxicology 60: 15-25, 1990.
49. Luppi F, Aarbiou J, van Wetering S, Rahman I, de Boer WI, Rabe KF, Hiemstra PS. Effects of cigarette smoke condensate on proliferation and wound closure of bronchial epithelial cells in vitro: role of glutathione. Respir Res 6: 140, 2005.
50. Maples KR, Nikula KJ, Chen BT, Finch GL, Griffith WC, Harkema JR. Effects of cigarette smoke on the glutathione status of the upper and lower respiratory tract of rats. Inhal Toxicol 5: 389-401, 1993.
51. Markovic J, Borras C, Ortega A, Sastre J, Vina J, Pallardo FV. Glutathione is recruited into the nucleus in early phases of cell proliferation. J Biol Chem 282: 20416-20424, 2007.
52. Marraccini P, Brass DM, Hollingsworth JW, Maruoka S, Garantziotis S, Schwartz DA. Bakery flour dust exposure causes non-allergic inflammation and enhances allergic airway inflammation in mice. Clin Exp Allergy 38: 1526-1535, 2008.
53. Monn C. Exposure assessment of air pollutants: a review on spatial heterogeneity and indoor/outdoor/personal exposure to suspended particulate matter, nitrogen dioxide and ozone. In: Developments in Environmental Sciences, edited by Austin J, Brimblecombe P, and Sturges W. Oxford, UK: Elsevier Science, 2002, chapt. 4, p. 117-182.
54. Morgan M, Frank R. Uptake of pollutant gases by the respiratory system. In: Respiratory Defense Mechanisms, edited by Brain JD, Proctor DF, and Reid LM. New York: Dekker, 1977.
55. Nikula KJ, Wilson DW, Giri SN, Plopper CG, Dungworth DL. The response of the rat tracheal epithelium to ozone exposure. Injury, adaptation, and repair. Am J Pathol 131: 373-384, 1988.
56. Parker JD, Akinbami LJ, Woodruff TJ. Air pollution and childhood respiratory allergies in the United States. Environ Health Perspect 117: 140-147, 2009.
57. Plopper CG, Hatch GE, Wong V, Duan X, Weir AJ, Tarkington BK, Devlin RB, Becker S, Buckpitt AR. Relationship of inhaled ozone concentration to acute tracheobronchial epithelial injury, site-specific ozone dose, and glutathione depletion in rhesus monkeys. Am J Respir Cell Mol Biol 19: 387-399, 1998. (Pubitemid 128354208)
58. Puchelle E, Zahm JM, Tournier JM, Coraux C. Airway epithelial repair, regeneration, and remodeling after injury in chronic obstructive pulmonary disease. Proc Am Thorac Soc 3: 726-733, 2006. (Pubitemid 44788232)
59. Reddy NM, Kleeberger SR, Cho HY, Yamamoto M, Kensler TW, Biswal S, Reddy SP. Deficiency in Nrf2-GSH signaling impairs type II cell growth and enhances sensitivity to oxidants. Am J Respir Cell Mol Biol 37: 3-8, 2007. (Pubitemid 46999531)
60. Rogers DF, Jeffery PK. Inhibition of cigarette smoke-induced airway secretory cell hyperplasia by indomethacin, dexamethasone, prednisolone, or hydrocortisone in the rat. Exp Lung Res 10: 285-298, 1986.
61. Rosen CL. Maturation of breathing during sleep. In: Lung Biology in Health and Disease, Sleep and Breathing in Children: A Developmental Approach, edited by Lenfant C. New York: Dekker, 2008.
62. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108, 2008. (Pubitemid 351818697)
63. Sheldon LS. Overview of comorbid associations of allergic rhinitis. J Allergy Clin Immunol 99: S773-S780, 1997.
64. Sly PD, Flack F. Susceptibility of children to environmental pollutants. Ann NY Acad Sci 1140: 163-183, 2008.
65. Sram RJ, Benes I, Binkova B, Dejmek J, Horstman D, Kotesovec F, Otto D, Perreault SD, Rubes J, Selevan SG, Skalik I, Stevens RK, Lewtas J. Teplice program-the impact of air pollution on human health. Environ Health Perspect 104, Suppl 4: 699-714, 1996.
66. Thelander L, Reichard P. Reduction of ribonucleotides. Annu Rev Biochem 48: 133-158, 1979.
67. Wagner JG, Hotchkiss JA, Harkema JR. Effects of ozone and endotoxin coexposure on rat airway epithelium: potentiation of toxicantinduced alterations. Environ Health Perspect 109, Suppl 4: 591-598, 2001.
68. Wagner JG, Hotchkiss JA, Harkema JR. Enhancement of nasal inflammatory and epithelial responses after ozone and allergen coexposure in Brown Norway rats. Toxicol Sci 67: 284-294, 2002.
69. Wang Y, Abel K, Lantz K, Krieg AM, McChesney MB, Miller CJ. The Toll-like receptor 7 (TLR7) agonist, imiquimod, and the TLR9 agonist, CpG ODN, induce antiviral cytokines and chemokines but do not prevent vaginal transmission of simian immunodeficiency virus when applied intravaginally to rhesus macaques. J Virol 79: 14355-14370, 2005.
70. West JA, Buckpitt AR, Plopper CG. Elevated airway GSH resynthesis confers protection to Clara cells from naphthalene injury in mice made tolerant by repeated exposures. J Pharmacol Exp Ther 294: 516-523, 2000.
71. 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 116: 193-206, 1984.
72. Woodruff TJ, Axelrad DA, Kyle AD, Nweke O, Miller GG. America's Children and the Environment. Washington, DC: United States Environmental Protection Agency, 2007, p. 1-176.
73. Zavala M, Lei W, Molina MJ, Molina LT. Modeled and observed ozone sensitivity to mobile-source emissions in Mexico City. Atmos Chem Phys 9: 39-55, 2009.