Pulmonary ozone exposure induces vascular dysfunction, mitochondrial damage, and atherogenesis

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 297, Issue 2, 2009, Pages

  Chuang, Gin C ^a,b   Yang, Zhen ^a,b   Westbrook, David G ^a   Pompilius, Melissa ^a   Ballinger, Carol A ^b   White, C Roger ^b,c   Krzywanski, David M ^a,b   Postlethwait, Edward M ^b   Ballinger, Scott W ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

Atherosclerosis; Environmental oxidants; Lung; Mice; Mitochondria; Mitochondrial DNA damage; Nitric oxide; Nonhuman primates; Oxidative stress

Indexed keywords

MITOCHONDRIAL DNA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OZONE;

AIR QUALITY CONTROL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; ENVIRONMENTAL EXPOSURE; HOSPITAL ADMISSION; MALE; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; VASCULAR DISEASE;

AIR POLLUTANTS; ANIMALS; AORTA; ATHEROSCLEROSIS; BLOOD PRESSURE; DNA DAMAGE; DNA, MITOCHONDRIAL; HEART RATE; LUNG DISEASES; MACACA MULATTA; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL DISEASES; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; NITRITES; OXIDANTS; OXIDATIVE STRESS; OZONE; SUPEROXIDE DISMUTASE; TYROSINE;

EID: 67651205332     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00102.2009     Document Type: Article

References (50)

1. Alink GM, de Boer RM, Mol J, Temmink JH. Toxic effects of ozone on human cells in vitro, exposed by gas diffusion through teflon film. Toxicology 17: 209-218, 1980.
2. Anderson HR, Ponce de Leon A, Bland JM, Bower JS, Strachan DP. Air pollution and daily mortality in London: 1987-92. BMJ 312: 665-669, 1996.
3. Ballinger CA, Cueto R, Squadrito G, Coffin JF, Velsor LW, Pryor WA, Postlethwait EM. Antioxidant-mediated augmentation of ozone-induced membrane oxidation. Free Radic Biol Med 38: 515-526, 2005.
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. Borja-Aburto VH, Castillejos M, Gold DR, Bierzwinski S, Loomis D. Mortality and ambient fine particles in southwest Mexico City, 1993-1995. Environ Health Perspect 106: 849-855, 1998.
6. Brook RD, Brook JR, Urch B, Vincent R, Rajagopalan S, Silverman F. Inhalation of fine particulate air pollution and ozone causes acute arterial vasoconstriction in healthy adults. Circulation 105: 1534-1536, 2002.
7. Brook RD, Franklin B, Cascio W, Hong Y, Howard G, Lipsett M, Luepker R, Mittleman M, Samet J, Smith SC Jr, Tager I. Air pollution and cardiovascular disease: a statement for healthcare professionals from the Expert Panel on Population and Prevention Science of the American Heart Association. Circulation 109: 2655-2671, 2004.
8. Bullock BC, Lehner ND, Clarkson TB, Feldner MA, Wagner WD, Lofland HB. Comparative primate atherosclerosis. I. Tissue cholesterol concentration and pathologic anatomy. Exp Mol Pathol 22: 151-175, 1975.
9. Chen C, Korshunov VA, Massett MP, Yan C, Berk BC. Impaired vasorelaxation in inbred mice is associated with alterations in both nitric oxide and super oxide pathways. J Vasc Res 44: 504-512, 2007.
10. Cho HY, Morgan DL, Bauer AK, Kleeberger SR. Signal transduction pathways of tumor necrosis factor-mediated lung injury induced by ozone in mice. Am J Respir Crit Care Med 175: 829-839, 2007.
11. Choi JH, Xu QS, Park SY, Kim JH, Hwang SS, Lee KH, Lee HJ, Hong YC. Seasonal variation of effect of air pollution on blood pressure. J Epidemiol Community Health 61: 314-318, 2007.
12. Dubick MA, Keen CL. Tissue trace elements and lung superoxide dismutase activity in mice exposed to ozone. Toxicol Lett 17: 355-360, 1983.
13. Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA, Halliwell B, van der Vliet A. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 391: 393-397, 1998.
14. Federal Register of March 27 2008. National Ambient Air Quality Standards for Ozone; Final Rule. EPA-HQ-OAR-2005-0172-7205 at http://www.regulations.gov. [April 19, 2009.]
15. Funabashi H, Shima M, Kuwaki T, Hiroshima K, Kuriyama T. Effects of repeated ozone exposure on pulmonary function and bronchial responsiveness in mice sensitized with ovalbumin. Toxicology 204: 75-83, 2004.
16. Gao X, Xu X, Belmadani S, Park Y, Tang Z, Feldman AM, Chilian WM, Zhang C. TNF-alpha contributes to endothelial dysfunction by upregulating arginase in ischemia/reperfusion injury. Arterioscler Thromb Vasc Biol 27: 1269-1275, 2007.
17. Gong H Jr, Wong R, Sarma RJ, Linn WS, Sullivan ED, Shamoo DA, Anderson KR, Prasad SB. Cardiovascular effects of ozone exposure in human volunteers. Am J Respir Crit Care Med 158: 538-546, 1998.
18. Goodwin BL, Pendleton LC, Levy MM, Solomonson LP, Eichler DC. Tumor necrosis factor-α reduces argininosuccinate synthase expression and nitric oxide production in aortic endothelial cells. Am J Physiol Heart Circ Physiol 293: H1115-H1121, 2007.
19. Goossens V, Grooten J, De Vos K, Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. PNAS USA 92: 8115-8119, 1995.
20. Hausladen A, Fridovich I. Measuring nitric oxide and superoxide: rate constants for aconitase reactivity. Methods Enzymol 269: 37-41, 1996.
21. Kafoury RM, Pryor WA, Squadrito GL, Salgo MG, Zou X, Friedman M. Induction of inflammatory mediators in human airway epithelial cells by lipid ozonation products. Am J Respir Crit Care Med 160: 1934-1942, 1999.
22. Kafoury RM, Pryor WA, Squadrito GL, Salgo MG, Zou X, Friedman M. Lipid ozonation products activate phospholipases A2, C, and D. Toxicol Appl Pharmacol 150: 338-349, 1998.
23. Knight-Lozano CA, Young CG, Burow DL, Hu ZY, Uyeminami D, Pinkerton KE, Ischiropoulos H, Ballinger SW. Cigarette smoke exposure and hypercholesterolemia increase mitochondrial damage in cardiovascular tissues. Circulation 105: 849-854, 2002.
24. Kojda G, Laursen JB, Ramasamy S, Kent JD, Kurz S, Burchfield J, Shesely EG, Harrison DG. Protein expression, vascular reactivity and soluble guanylate cyclase activity in mice lacking the endothelial cell nitric oxide synthase: contributions of NOS isoforms to blood pressure and heart rate control. Cardiovasc Res 42: 206-213, 1999.
25. Langford SD, Bidani A, Postlethwait EM. Ozone-reactive absorption by pulmonary epithelial lining fluid constituents. Toxicol Appl Pharmacol 132: 122-130, 1995.
26. Laskin DL, Fakhrzadeh L, Laskin JD. Nitric oxide and peroxynitrite in ozone-induced lung injury. Adv Exp Med Biol 500: 183-190, 2001.
27. Last JA, Gohil K, Mathrani VC, Kenyon NJ. Systemic responses to inhaled ozone in mice: cachexia and down-regulation of liver xenobiotic metabolizing genes. Toxicol Appl Pharmacol 208: 117-126, 2005.
28. Li Q, Verma IM. NF-kappaB regulation in the immune system. Nature Rev 2: 725-734, 2002.
29. Lippmann M, Frampton M, Schwartz J, Dockery D, Schlesinger R, Koutrakis P, Froines J, Nel A, Finkelstein J, Godleski J, Kaufman J, Koenig J, Larson T, Luchtel D, Liu LJ, Oberdorster G, Peters A, Sarnat J, Sioutas C, Suh H, Sullivan J, Utell M, Wichmann E, Zelikoff J. The U.S. Environmental Protection Agency Particulate Matter Health Effects Research Centers Program: a midcourse report of status, progress, and plans. Environ Health Perspect 111: 1074-1092, 2003.
30. Mills NL, Robinson SD, Fokkens PH, Leseman DL, Miller MR, Anderson D, Freney EJ, Heal MR, Donovan RJ, Blomberg A, Sandstrom T, MacNee W, Boon NA, Donaldson K, Newby DE, Cassee FR. Exposure to concentrated ambient particles does not affect vascular function in patients with coronary heart disease. Environ Health Perspect 116: 709-715, 2008.
31. Morrow JD, Harris TM, Roberts LJ 2nd. Noncyclooxygenase oxidative formation of a series of novel prostaglandins: analytical ramifications for measurement of eicosanoids. Anal Biochem 184: 1-10, 1990.
32. Penn A, Snyder CA. 1,3 Butadiene, a vapor phase component of environmental tobacco smoke, accelerates arteriosclerotic plaque development. Circulation 93: 552-557, 1996.
33. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and athero-sclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71: 343-353, 1992.
34. 3-induced formation of bioactive lipids: estimated surface concentrations and lining layer effects. Am J Physiol Lung Cell Mol Physiol 274: L1006-L1016, 1998.
35. Pryor WA, Squadrito GL, Friedman M. The cascade mechanism to explain ozone toxicity: the role of lipid ozonation products. Free Radic Biol Med 19: 935-941, 1995.
36. Rahman I, Clerch LB, Massaro D. Rat lung antioxidant enzyme induction by ozone. Am J Physiol Lung Cell Mol Physiol 260: L412-L418, 1991.
37. Rodriguez-Iturbe B, Sepassi L, Quiroz Y, Ni Z, Wallace DC, Vaziri ND. Association of mitochondrial SOD deficiency with salt-sensitive hypertension and accelerated renal senescence. J Appl Physiol 102: 255-260, 2007.
38. Ruidavets JB, Cassadou S, Cournot M, Bataille V, Meybeck M, Ferrieres J. Increased resting heart rate with pollutants in a population based study. J Epidemiol Community Health 59: 685-693, 2005.
39. 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.
40. 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.
41. Schulze-Osthoff K, Beyaert R, Vandevoorde V, Haegeman G, Fiers W. Depletion of the mitochondrial electron transport abrogates the cyto-toxic and gene-inductive effects of TNF. EMBO J 12: 3095-3104, 1993.
42. U.S. Environmental Protection Agency. Air Quality Criteria for Ozone and Related Photochemical Oxidants (Final). U. S. Environmental Protection Agency, Washington, D.C., EPA/600/R-05/004aF-cF, 2006.
43. Urch B, Silverman F, Corey P, Brook JR, Lukic KZ, Rajagopalan S, Brook RD. Acute blood pressure responses in healthy adults during controlled air pollution exposures. Environ Health Perspect 113: 1052-1055, 2005.
44. Valerio A, Cardile A, Cozzi V, Bracale R, Tedesco L, Pisconti A, Palomba L, Cantoni O, Clementi E, Moncada S, Carruba MO, Nisoli E. TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 116: 2791-2798, 2006.
45. Weller BL, Crapo JD, Slot J, Posthuma G, Plopper CG, Pinkerton KE. Site- and cell-specific alteration of lung copper/zinc and manganese superoxide dismutases by chronic ozone exposure. Am J Respir Cell Mol Biol 17: 552-560, 1997.
46. Wilson DW, Plopper CG, Dungworth DL. The response of the macaque tracheobronchial epithelium to acute ozone injury. A quantitative ultra-structural and autoradiographic study. Am J Pathol 116: 193-206, 1984.
47. Wong GH, Elwell JH, Oberley LW, Goeddel DV. Manganous super-oxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell 58: 923-931, 1989.
48. 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.
49. Yan G, You B, Chen SP, Liao JK, Sun J. Tumor necrosis factor-alpha downregulates endothelial nitric oxide synthase mRNA stability via translation elongation factor 1-alpha 1. Circ Res 103: 591-597, 2008.
50. Zhang C, Patel R, Eiserich JP, Zhou F, Kelpke S, Ma W, Parks DA, Darley-Usmar V, White CR. Endothelial dysfunction is induced by proinflammatory oxidant hypochlorous acid. Am J Physiol Heart Circ Physiol 281: H1469-H1475, 2001.