Postnatal episodic ozone results in persistent attenuation of pulmonary and peripheral blood responses to LPS challenge

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 300, Issue 3, 2011, Pages

  Maniar Hew, Kinjal ^a   Postlethwait, Edward M ^b   Fanucchi, Michelle V ^b   Ballinger, Carol A ^b   Evans, Michael J ^a,c   Harkema, Jack R ^d   Carey, Stephan A ^d   Mcdonald, Ruth J ^e   Bartolucci, Alfred A ^b   Miller, Lisa A ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Infant; Lipopolysaccharide; Toll like receptor

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; INTERLEUKIN 6; INTERLEUKIN 8; OZONE;

AIR POLLUTION; AMBIENT AIR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CYTOKINE RELEASE; EOSINOPHIL COUNT; INNATE IMMUNITY; LEUKOCYTE COUNT; LUNG DEVELOPMENT; LUNG LAVAGE; MALE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PNEUMONIA; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RHESUS MONKEY;

AGING; ANIMALS; ANIMALS, NEWBORN; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; INFLAMMATION; INHALATION EXPOSURE; LEUKOCYTE COUNT; LEUKOCYTES; LIPOPOLYSACCHARIDES; LUNG; MACACA MULATTA; MALE; OZONE;

EID: 79955030552     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00254.2010     Document Type: Article

References (62)

1. Akinbami LJ, Lynch CD, Parker JD, Woodruff TJ. The association between childhood asthma prevalence and monitored air pollutants in metropolitan areas, United States, 2001-2004. Environ Res 110: 294-301, 2010.
2. Auten RL, Potts EN, Mason SN, Fischer B, Huang Y, Foster WM. Maternal exposure to particulate matter increases postnatal ozone-induced airway hyperreactivity in juvenile mice. Am J Respir Crit Care Med 180: 1218-1226, 2009.
3. Balinotti JE, Tiller CJ, Llapur CJ, Jones MH, Kimmel RN, Coates CE, Katz BP, Nguyen JT, Tepper RS. Growth of the lung parenchyma early in life. Am J Respir Crit Care Med 179: 134-137, 2009.
4. Bateson TF, Schwartz J. Children's response to air pollutants. J Toxicol Environ Health A 71: 238-243, 2008.
5. Becker S, Madden MC, Newman SL, Devlin RB, Koren HS. Modulation of human alveolar macrophage properties by ozone exposure in vitro. Toxicol Appl Pharmacol 110: 403-415, 1991.
6. Carey MA, Card JW, Voltz JW, Arbes SJ Jr, Germolec DR, Korach KS, Zeldin DC. It's all about sex: gender, lung development and lung disease. Trends Endocrinol Metab 18: 308-313, 2007.
7. Ciencewicki J, Jaspers I. Air pollution and respiratory viral infection. Inhal Toxicol 19: 1135-1146, 2007.
8. Comans-Bitter WM, de Groot R, van den Beemd R, Neijens HJ, Hop WC, Groeneveld K, Hooijkaas H, van Dongen JJ. Immunophenotyping of blood lymphocytes in childhood. Reference values for lymphocyte subpopulations. J Pediatr 130: 388-393, 1997.
9. El Gazzar M, McCall CE. MicroRNAs distinguish translational from transcriptional silencing during endotoxin tolerance. J Biol Chem 285: 20940-20951, 2010.
10. Ellis S, Mouihate A, Pittman QJ. Early life immune challenge alters innate immune responses to lipopolysaccharide: implications for host defense as adults. FASEB J 19: 1519-1521, 2005.
11. Eustis SL, Schwartz LW, Kosch PC, Dungworth DL. Chronic bron-chiolitis in nonhuman primates after prolonged ozone exposure. Am J Pathol 105: 121-137, 1981.
12. Fedulov AV, Leme A, Yang Z, Dahl M, Lim R, Mariani TJ, Kobzik L. Pulmonary exposure to particles during pregnancy causes increased neonatal asthma susceptibility. Am J Respir Cell Mol Biol 38: 57-67, 2008.
13. Fleisher B, Kulovich MV, Hallman M, Gluck L. Lung profile: sex differences in normal pregnancy. Obstet Gynecol 66: 327-330, 1985.
14. Frischer T, Studnicka M, Halmerbauer G, Horak F Jr, Gartner C, Tauber E, Koller DY.Ambient ozone exposure is associated with eosin-ophil activation in healthy children. Clin Exp Allergy 31: 1213-1219, 2001.
15. 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 351: 1057-1067, 2004.
16. Gauderman WJ, Vora H, McConnell R, Berhane K, Gilliland F, Thomas D, Lurmann F, Avol E, Kunzli N, Jerrett M, Peters J. Effect of exposure to traffic on lung development from 10 to 18 years of age: a cohort study. Lancet 369: 571-577, 2007.
17. Gilmour MI, Hmieleski RR, Stafford EA, Jakab GJ. Suppression and recovery of the alveolar macrophage phagocytic system during continuous exposure to 0.5 ppm ozone. Exp Lung Res 17: 547-558, 1991.
18. Gilmour MI, Park P, Doerfler D, Selgrade MK. Factors that influence the suppression of pulmonary antibacterial defenses in mice exposed to ozone. Exp Lung Res 19: 299-314, 1993.
19. Gilmour MI, Park P, Selgrade MK. Ozone-enhanced pulmonary infection with Streptococcus zooepidemicus in mice. The role of alveolar macrophage function and capsular virulence factors. Am Rev Respir Dis 147: 753-760, 1993.
20. Gold DR, Bloomberg GR, Cruikshank WW, Visness CM, Schwarz J, Kattan M, O'Connor GT, Wood RA, Burger MS, Wright RJ, Witter F, Lee-Parritz A, Sperling R, Sadovsky Y, Togias A, Gern JE. Parental characteristics, somatic fetal growth, and season of birth influence innate and adaptive cord blood cytokine responses. J Allergy Clin Immunol 124: 1078-1087, 2009.
21. Hamada K, Suzaki Y, Leme A, Ito T, Miyamoto K, Kobzik L, Kimura H. Exposure of pregnant mice to an air pollutant aerosol increases asthma susceptibility in offspring. J Toxicol Environ Health A 70: 688-695, 2007.
22. Hicks A, Kourteva G, Hilton H, Li H, Lin TA, Liao W, Li Y, Wei X, March T, Benson J, Renzetti LM. Cellular and molecular characterization of ozone-induced pulmonary inflammation in the cynomolgus monkey. Inflammation 33: 144-156, 2009.
23. Hoffstein V. Relationship between lung volume, maximal expiratory flow, forced expiratory volume in one second, and tracheal area in normal men and women. Am Rev Respir Dis 134: 956-961, 1986.
24. Hollingsworth JW 2nd, Cook DN, Brass DM, Walker JK, Morgan DL, Foster WM, Schwartz DA. The role of Toll-like receptor 4 in environmental airway injury in mice. Am J Respir Crit Care Med 170: 126-132, 2004.
25. Hollingsworth JW, Free ME, Li Z, Andrews LN, Nakano H, Cook D, Ozone activates pulmonary dendritic cells and promotes allergic sensitization through a Toll-like receptor 4-dependent mechanism. J Allergy Clin Immunol 125: 1167-1170, 2010.
26. Hollingsworth JW, Kleeberger SR, Foster WM. Ozone and pulmonary innate immunity. Proc Am Thorac Soc 4: 240-246, 2007.
27. Hollingsworth JW, Maruoka S, Li Z, Potts EN, Brass DM, Garant-ziotis S, Fong A, Foster WM, Schwartz DA. Ambient ozone primes pulmonary innate immunity in mice. J Immunol 179: 4367-4375, 2007.
28. Holt PG, Jones CA. The development of the immune system during pregnancy and early life. Allergy 55: 688-697, 2000.
29. Hyde DM, Hubbard WC, Wong V, Wu R, Pinkerton K, Plopper CG. Ozone-induced acute tracheobronchial epithelial injury: relationship to granulocyte emigration in the lung. Am J Respir Cell Mol Biol 6: 481-497, 1992.
30. John G, Yildirim AO, Rubin BK, Gruenert DC, Henke MO. TLR-4-mediated innate immunity is reduced in cystic fibrosis airway cells. Am J Respir Cell Mol Biol 42: 424-431, 2010.
31. Johnston CJ, Holm BA, Finkelstein JN. Sequential exposures to ozone and lipopolysaccharide in postnatal lung enhance or inhibit cytokine responses. Exp Lung Res 31: 431-447, 2005.
32. Kleeberger SR, Levitt RC, Zhang LY, Longphre M, Harkema J, Jedlicka A, Eleff SM, DiSilvestre D, Holroyd KJ. Linkage analysis of susceptibility to ozone-induced lung inflammation in inbred mice. Nat Genet 17: 475-478, 1997.
33. Koike E, Kobayashi T. Ozone exposure enhances antigen-presenting activity of interstitial lung cells in rats. Toxicology 196: 217-227, 2004.
34. Kopp MV, Bohnet W, Frischer T, Ulmer C, Studnicka M, Ihorst G, Gardner C, Forster J, Urbanek R, Kuehr J. Effects of ambient ozone on lung function in children over a two-summer period. Eur Respir J 16: 893-900, 2000.
35. 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.
36. La Pine TR, Joyner JL, Augustine NH, Kwak SD, Hill HR. Defective production of IL-18 and IL-12 by cord blood mononuclear cells influences the T helper-1 interferon gamma response to group B Streptococci. Pediatr Res 54: 276-281, 2003.
37. Lay JC, Alexis NE, Kleeberger SR, Roubey RA, Harris BD, Bromberg PA, Hazucha MJ, Devlin RB, Peden DB. Ozone enhances markers of innate immunity and antigen presentation on airway monocytes in healthy individuals. J Allergy Clin Immunol 120: 719-722, 2007.
38. Lin S, Liu X, Le LH, Hwang SA. Chronic exposure to ambient ozone and asthma hospital admissions among children. Environ Health Perspect 116: 1725-1730, 2008.
39. Lu YC, Yeh WC, Ohashi PS. LPS/TLR4 signal transduction pathway. Cytokine 42: 145-151, 2008.
40. + cells in infant rhesus monkeys. Toxicol Appl Pharmacol 236: 39-48, 2009.
41. Miller S, Ehrlich R. Susceptibility to respiratory infections of animals exposed to ozone. I. Susceptibility to Klebsiella pneumoniae. J Infect Dis 103: 145-149, 1958.
42. Mouihate A, Galic MA, Ellis SL, Spencer SJ, Tsutsui S, Pittman QJ. Early life activation of toll-like receptor 4 reprograms neural anti-inflammatory pathways. J Neurosci 30: 7975-7983, 2010.
43. Nguyen M, Leuridan E, Zhang T, De Wit D, Willems F, Van Damme P, Goldman M, Goriely S. Acquisition of adult-like TLR4 and TLR9 responses during the first year of life. PLos One 5: e10407, 2010.
44. Parker JD, Akinbami LJ, Woodruff TJ. Air pollution and childhood respiratory allergies in the United States. Environ Health Perspect 117: 140-147, 2009.
45. Prows DR, Shertzer HG, Daly MJ, Sidman CL, Leikauf GD. Genetic analysis of ozone-induced acute lung injury in sensitive and resistant strains of mice. Nat Genet 17: 471-474, 1997.
46. Rojas-Martinez R, Perez-Padilla R, Olaiz-Fernandez G, Mendoza-Alvarado L, Moreno-Macias H, Fortoul T, McDonnell W, Loomis D, Romieu I. Lung function growth in children with long-term exposure to air pollutants in Mexico City. Am J Respir Crit Care Med 176: 377-384, 2007.
47. Rusznak C, Devalia J, Sapsford R, Davies R. Ozone-induced mediator release from human bronchial epithelial cells in vitro and the influence of nedocromil sodium. Eur Respir J 9: 2298-2305, 1996.
48. Schaub B, Bellou A, Gibbons FK, Velasco G, Campo M, He H, Liang Y, Gillman MW, Gold D, Weiss ST, Perkins DL, Finn PW. TLR2 and TLR4 stimulation differentially induce cytokine secretion in human neo-natal, adult, and murine mononuclear cells. J Interferon Cytokine Res 24: 543-552, 2004.
49. 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 191: 74 -85, 2003.
50. Schwartz J. PM10, ozone, and hospital admissions for the elderly in Min-neapolis-St. Paul, Minnesota. Arch Environ Health 49: 366 -374, 1994.
51. Shore SA, Schwartzman IN, Le Blanc B, Murthy GG, Doerschuk CM. Tumor necrosis factor receptor 2 contributes to ozone-induced airway hyper-responsiveness in mice. Am J Respir Crit Care Med 164: 602-607, 2001.
52. Thomas GB, Fenters JD, Ehrlich R, Gardner DE. Effects of exposure to ozone on susceptibility to experimental tuberculosis. Toxicol Lett 9: 11-17, 1981.
53. Van Loveren H, Rombout PJ, Wagenaar SS, Walvoort HC, Vos JG. Effects of ozone on the defense to a respiratory Listeria monocytogenes infection in the rat. Suppression of macrophage function and cellular immunity and aggravation of histopathology in lung and liver during infection. Toxicol Appl Pharmacol 94: 374-393, 1988.
54. 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.
55. Whitelaw DM. Observations on human monocyte kinetics after pulse labeling. Cell Tissue Kinet 5: 311-317, 1972.
56. Williams AS, Leung SY, Nath P, Khorasani NM, Bhavsar P, Issa R, Mitchell JA, Adcock IM, Chung KF. Role of TLR2, TLR4, and MyD88 in murine ozone-induced airway hyperresponsiveness and neutrophilia. J Appl Physiol 103: 1189-1195, 2007.
57. Wong TW, Lau TS, Yu TS, Neller A, Wong SL, Tam W, Pang SW. Air pollution and hospital admissions for respiratory and cardiovascular diseases in Hong Kong. Occup Environ Med 56: 679-683, 1999.
58. Xia HJ, Zhang GH, Wang RR, Zheng YT. The influence of age and sex on the cell counts of peripheral blood leukocyte subpopulations in Chinese rhesus macaques. Cell Mol Immunol 6: 433-440, 2009.
59. Yerkovich ST, Wikstrom ME, Suriyaarachchi D, Prescott SL, Upham JW, Holt PG. Postnatal development of monocyte cytokine responses to bacterial lipopolysaccharide. Pediatr Res 62: 547-552, 2007.
60. 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.
61. Zeltner TB, Burri PH. The postnatal development and growth of the human lung. II. Morphology. Respir Physiol 67: 269-282, 1987.
62. Zhao Q, Simpson LG, Driscoll KE, Leikauf GD. Chemokine regulation of ozone-induced neutrophil and monocyte inflammation. Am J Physiol Lung Cell Mol Physiol 274: L39-L46, 1998.