Oxidative Stress, the Paradigm of Ozone Toxicity in Plants and Animals
- 628 Downloads
- 53 Citations
Abstract
Tropospheric ozone represents a relevant atmospheric pollutant, because of its strong oxidizing potential. The risk for animal (human) and plant health, at molecular and cellular level, arises from the oxidative damage to lipids, proteins and nucleic acids, depending on the dose. Therefore, ozone concentration and exposure time determine the chronic or acute toxicity and, consequently, the severity of injury at biochemical and physiological level. In living organisms, reactive oxygen species (ROS), directly or indirectly derived from ozone exposure, are scavenged by enzymatic and non-enzymatic antioxidant defensive mechanisms, overall deputed to preserve cell structures and biomacromolecules from the oxidative damage. These defences are essentially those also involved in detoxifying the ROS inevitably produced by the metabolism of organisms living in oxygenic atmosphere.
Keywords
Atmospheric pollution Tropospheric ozone Reactive oxygen species Antioxidant defencesNotes
Acknowledgements
We are grateful to Dr. Giovanni Lodi for providing Fig. 7. This research was partially supported by Progetto INFOGESO, Regione Lombardia, Piano per la Ricerca e lo Sviluppo 2004.
References
- Alscher, R. G. (1989). Biosynthesis and antioxidant function of glutathione in plants. Physiologia Plantarum, 93, 196–205.Google Scholar
- Apel, K., & Hirt, H. (2004). Reactive oxygen species: Metabolism, oxidative stress and signal transduction. Annual Reviews of Plant biology, 55, 373–399.Google Scholar
- Aris, R. M., Christian, D., Hearne, P. Q., Finkbeiner, W. E., & Balmes, J. R. (1993). Ozone-induced airway inflammation in human subjects as determined by airway lavage and biopsy. American Reviews of Respiratory Diseases, 148, 1363–1372.Google Scholar
- Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology, 141, 391–396.Google Scholar
- Balmes, J. R., Chen, L. L., Scannell, C., Tager, I., Christian, D., & Hearne, P. Q., et al. (1996). Ozone-induced decrements in FEV1 and FVC do not correlate with measures of inflammation. American Journal of Respiratory Critical Care and Medicine, 153, 904–909.Google Scholar
- Baumbach, G., & Vogt, U. (2003). Influence of inversion layers on the distribution of air pollutants in urban areas. Water, Air and Soil Pollution: Focus, 3, 67–87.Google Scholar
- Barr, B. C., Hyde, D. M., Plopper, C. G., & Dungworth, C. L. (1988). Distal airway remodelling in rats chronically exposed to ozone. American Reviews of Respiratory Diseases, 137, 924–938.Google Scholar
- Bayram, H., Sapsford, R. J., Abdelaziz, M. M., & Khair, O. A. (2001). Effect of ozone and nitrogen dioxide on the release of proinflammatory mediators from bronchial epithelial cell of non-atopic non-asthmatic subjects and atopic asthmatic patients in vivo. Journal of Allergy and Clinical Immunology, 107, 287–294.Google Scholar
- Bergmann, E., Bender, J., & Weigel, J. (1999). Ozone threshold doses and exposure–response relationships for the development of ozone injury symptoms in wild plant species. New Phytologist, 144, 423–435.Google Scholar
- Black, V. J., Black, C. R., Roberts, J. A., & Stewart, C. A. (2000). Impact of ozone on the reproductive development of plants. New Phytologist, 147, 421–447.Google Scholar
- Blatt, M. R. (2000). Cellular signaling and volume control in stomatal movements in plants. Annual Reviews of Cell and Development Biology, 16, 221–241.Google Scholar
- Blundell, R. (2006). The biology of small airway epithelium. International Journal of Molecular Medicine and Advanced Science, 2, 354–359.Google Scholar
- Boorman, G. A., Schwartz, L. W., & Dungworth, C. L. (1980). Pulmonary effects of prolonged ozone insult in rats: Morphometric analysis of central acinus. Laboratory Investigation, 43, 108–115.Google Scholar
- Borrell, A., Carbonell, L., Farràs, R., Puig-Parellada, P., & Tiburcio, A. F. (1997). Polyamines inhibit lipid peroxidation in senescing oat leaves. Physiologia Plantarum, 99, 385–390.Google Scholar
- Bors, W., Langebartels, C., Michel, C., & Sandermann, H. (1989). Polyamines as radical scavengers and protectans against ozone damage. Phytochemistry, 28, 1589–1595.Google Scholar
- Bosson, J., Stenfors, N., Bucht, A., Helleday, R., Pourazar, J., & Holgate, S. T., et al. (2003). Ozone-induced bronchial epithelial cytochine expression differs between health and asthmatic subjects. Clinical and Experimental Allergy, 33, 777–782.Google Scholar
- Bouchereau, A., Aziz, A., Larher, F., & Martin-Tanguy, J. (1999). Polyamines and environmental challenges: Recent development. Plant Science, 140, 103–125.Google Scholar
- Bowler, C., Van Camp, W., Van Montagu, M., & Inzé, D. (1994). Superoxide dismutase in plants. Critical Reviews in Plant Science, 13, 199–218.Google Scholar
- Bromberg, P. A., & Koren, H. S. (1995). Ozone-induced human respiratory dysfunction and disease. Toxicology Letters, 82/83, 307–316.Google Scholar
- Bruce, N. A., Catchart, R., Schwiers, E., & Hochstein, P. (1981). Uric acid provides an antioxidant defense in human against oxidant- and radical-caused aging and cancer: A hypothesis. Proceedings of the National Academy of Sciences of United States of America, 78, 6858–6862.Google Scholar
- Brunekreef, B. (1997). Air pollution and life expectancy: Is there a relation? Occupational and Environmental Medicine, 54, 781–784.CrossRefGoogle Scholar
- Carrasco-Rodriguez, J. L., Asensi-Fabado, A., & Del Valle-Tascon, S. (2005). Effects of tropospheric ozone on potato plants protected by the antioxidant diphenylamine (DPA). Water, Air, and Soil Pollution, 161, 229–312.Google Scholar
- Cho, H. Y., Hotchkiss, J. A., & Harkema, J. R. (1999). Inflammatory and epithelial responses during the development of ozone-induced mucous cell metaplasia in the nasal epithelium of rats. Toxicological Sciences, 51, 135–145.Google Scholar
- Christian, D. L., Chen, L. L., Scannell, C. H., Ferrando, R. E., Welch, B. S., & Balmes, J. R. (1998). Ozone-induced inflammation is attenuated with multiday exposure. American Journal of Respiratory Critical Care and Medicine, 158, 532–537.Google Scholar
- Coleridge, J. C. G., Coleridge, H. M., Schelegle, E. S., & Green, J. F. (1993). Acute inhalation of ozone stimulates bronchial C-fibers and rapidly adapting receptors in dogs. Journal of Applied Physiology, 74, 2345–2352.Google Scholar
- Comhair, S. A. A., & Erzurum, S. C. (2002). Antioxidant responses to oxidant mediated lung disease. American Journal of Physiology, 283, L246–L255.Google Scholar
- Creelman, R. A., & Mullet, J. E. (1997). Biosynthesis and action of jasmonates in plants. Annual Reviews of Plant Physiology and Plant Molecular Biology, 48, 355–381.Google Scholar
- Criegee, R. (1957). The course of ozonation of unsaturated compounds. Record of Chemical Progress, 18, 110–120.Google Scholar
- Cross, C. E., van der Vliet, A., O’Neill, C. A., Louie, S., & Halliwell, B. (1998a). Oxidants, antioxidants and respiratory tract lining fluids. Environmental Health Perspectives, 102, 185–191.Google Scholar
- Cross, C. E., van der Vliet, A., Louie, S., Thiele, J. J., & Halliwell, B. (1998b). Oxidative stress and antioxidants at biosurfaces: Plants, skin and respiratory tract surfaces. Environmental Health Perspectives, 106, 1241–1251.Google Scholar
- Cross, C. E., Valacchi, G., Schock, B., Wilson, M., Weber, S., & Eiserich, J. (2002). Environmental oxidant pollutant effects on biological systems. American Journal of Respiratory Critical Care and Medicine, 166, 44–50.Google Scholar
- Crutzen, P. J., & Lelieveld, J. (2001). Human impacts on atmospheric chemistry. Annual Review of Earth and Planetary Sciences, 29, 17–45.Google Scholar
- Cutler, R. G. (1984). Urate and ascorbate: Their possible roles as antioxidants in determining longevity of mammalian species. Archives of Gerontology and Geriatrics, 3, 321–348.Google Scholar
- Dahlgren, C., & Karlsson, A. (1999). Respiratory burst in human neutrophils. Journal of Immunological Methods, 232, 3–14.Google Scholar
- Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzé, D., & Van Breusegem, F. (2000). Dual action of active oxygen species durino plant stress responses. Cellular and Molecular Life Science, 57, 779–795.Google Scholar
- Davies, K. J., Sevanian, A., Muakkassah-Kelly, S. F., & Hochstein, P. (1986). Uric acid–iron complexes. A new aspect of the antioxidant functions of uric acid. Biochemical Journal, 235, 747–754.Google Scholar
- Della Penna, D., & Pogson, B. J. (2006). Vitamin synthesis in plants: Tocopherols and carotenoids. Annual Reviews in Plant Biology, 57, 711–738.Google Scholar
- DeLorme, M. P., Yang, H., Elbon-Copp, C., Gao, X., Barraclough-Mitchell, H., & Basset, D. J. P. (2002). Hyperresponsive airways correlate with lung tissue inflammatory cell changes in ozone-exposed rats. Journal of Toxicology and Environmental Health, 65, 1453–1470.Google Scholar
- Devlin, R. B., McDonnel, W. F., Mann, R., Becker, S., House, D. E., & Schreinemachers, D. (1991). Exposure to humans to ambient levels of ozone for 6.6 hours causes cellular and biochemical changes in the lung. American Journal of Respiratory Cell and Molecular Biology, 4, 72–81.Google Scholar
- Devlin, R. B., McKinnon, K. P., Noah, T., Becker, S., & Koren, H. S. (1994). Ozone-induced release of cytokines and fibronectine by alveolar macrophages and airway epithelial cells. American Journal of Physiology, 266, L612–L619.Google Scholar
- Domitrović, R. (2006). Vitamin C in disease prevention and therapy. Biochemia Medica, 16, 107–125.Google Scholar
- Duneclift, S., Wells, U., & Widdicombe, J. (1997). Estimation of thickness of airway surface liquid in ferret trachea in vitro. American Journal of Physiology, 83, 761–767.Google Scholar
- Dubbels, R., Reiter, R. J., Klenke, E., Goebel, A., Schnakenberg, E., & Ehlers, C. (1995). Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectroscopy. Journal of Pineal Research, 18, 28–31.Google Scholar
- Dutsch, H. V. (1978). Vertical ozone distribution on a global scale. Pure and Applied Geophysics, 116, 511–529.Google Scholar
- Enyedi, A. J., Eckardt, N. A., & Pell, E. J. (1992). Activity of ribulose bisphosphate carboxylase/oxygenase from potato cultivars with differential response to ozone stress. New Phytologist, 122, 493–500.Google Scholar
- Eshdat, Y., Holland, D., Faltin, Z., & Ben-Hayyim, G. (1997). Plant glutathione peroxidases. Physiologia Plantarum, 100, 234–240.Google Scholar
- Faoro, F., & Iriti, M. (2005). Cell death behind invisible symptoms: Early diagnosis of ozone injury. Biologia Plantarum, 49, 585–592.Google Scholar
- Felle, H. H., Herrmann, A., Hückelhoven, R., & Kogel, K.-H. (2005). Root-to-shoot signalling: Apoplastic alkalinization, a general stress response and defence factor in barley (Hordeum vulgare). Protoplasma, 227, 17–24.Google Scholar
- Foyer, C. H., & Halliwell, B. (1976). The presence of glutathione and glutathione in chloroplasts: A proposed role in ascorbic acid metabolism. Planta, 133, 21–25.Google Scholar
- Foyer, C. H., & Lelandais, M. (1996). A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaf mesophyll cells. Journal of Plant Physiology, 148, 391–398.Google Scholar
- Foyer, C. H., & Noctor, G. (2005). Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell, 17, 1866–1875.Google Scholar
- Fowler, D., Cape, J. N., Coyle, M., Smith, R. I., Hjellbrekke, A.-G., & Simpson, D. (1999). Modelling photochemical oxidant formation, transport, deposition and exposure of terrestrial ecosystems. Environmental Pollution, 100, 43–55.Google Scholar
- Frank, R., Liu, M. C., Spannhake, E. W., Mlynarek, S., Macri, K., & Weinmann, G. G. (2001). Repetitive ozone exposure of young adults. American Journal of Respiratory Critical Care and Medicine, 164, 1253–1260.Google Scholar
- Freeman, B. A., & Mudd, J. B. (1981). Reaction of ozone with sulfhydryls of human erythrocytes. Archives of Biochemistry and Biophysics, 208, 212–220.Google Scholar
- Gechev, T. S., Van Breusegem, F., Stone, J. M., Denev, I., & Laloi, C. (2006). Reactive oxygen species as signals that modulate plant responses and programmed cell death. BioEssays, 28, 1091–1101.Google Scholar
- Gilmour, M. I., Park, P., & Selgrade, M. K. (1993). Ozone-enhanced pulmonary infection with Streptococcus zooepidemicus in mice. American Reviews of Respiratory Diseases, 147, 753–760.Google Scholar
- Halliwell, B. (2006). Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology, 141, 312–322.Google Scholar
- Hassan, I. A. (2006). Physiological and biochemical response of potato (Solanum tuberosum L. Cv. Kara) to O3 and antioxidant chemicals: Possible roles of antioxidant enzymes. Annals of Applied Biology, 148, 197–206.Google Scholar
- Hazbun, M. E., Hamilton, R., Holian, A., & Eschenbacher, W. L. (1993). Ozone induced increases in substance P and 8-epi-prostaglandin F2. a. in the airways of human subjects. American Journal of Respiratory Cell and Molecular Biology, 9, 568–572.Google Scholar
- Ho, C. Y., & Lee, L. Y. (1998). Ozone enhances excitabilities of pulmonary C fibers to chemical and mechanical stimuli in anesthetized rats. Journal of Applied Physiology, 85, 1509–1515.Google Scholar
- Hoet, P. H. M., & Nemery, B. (2000). Polyamines in the lung: Polyamine uptake and polyamine-linked pathological or toxicological conditions. American Journal of Physiology, 278, L417–L433.Google Scholar
- Höppe, P., Praml, G., Rabe, G., Linder, J., Fruhmann, G., & Kessel, R. (1995). Environmental ozone field study on pulmonary and subjective responses of assumed risk groups. Environmental Research, 71, 109–121.Google Scholar
- Housley, D. G., Mudway, I., Kelly, F. J., Eccles, R., & Richards, R. J. (1995). Depletion of urate in human nasal lavage following in vitro ozone exposure. International Journal of Biochemistry and Cell Biology, 27, 1153–1159.Google Scholar
- Hussain, M. Z., Mustafa, M. G., Ghani, Q. P., & Bhatnagar, R. S. (1985). Stimulation of poly(ADP-ribose) synthetase activity in the lungs of mice exposed to a low level of ozone. Archives of Biochemistry and Biophysics, 241, 477–485.Google Scholar
- Hyde, D. G., Hubbard, W. C., Wong, V., Wu, R., Pinkerton, K., & Plopper, C. G. (1992). Ozone-induced acute tracheobronchial epithelial injury: Relationship to granulocyte emigration in the lung. American Journal of Respiratory Cell and Molecular Biology, 6, 481–497.Google Scholar
- Hyde, D. G., Miller, L. A., McDonald, R. J., Stovall, M. W., Wong, V., & Pinkerton, K. (1999). Neutrophils enhance clearance of necrotic cells in ozone-induced lung injury in rhesus monkeys. America Journal of Physiology, 277, L1190–L1198.Google Scholar
- Ignatenko, A. V., Cherenkevich, S. N., & Komyak, A. I. (1984). Chromatographic and spectroscopic investigation of the products of oxidation of tyrosine with ozone. Journal of Applied Spectroscopy, 41, 159–164.Google Scholar
- Iriti, M., & Faoro, F. (2004). Plant defence and human nutrition: The phenylpropanoids on the menù. Current Topics in Nutraceutical Research, 2, 47–65.Google Scholar
- Iriti, M., & Faoro, F. (2006). Grape phytochemicals: A bouquet of old and new nutraceuticals for human health. Medical Hypoteses, 67, 833–838.Google Scholar
- Iriti, M., Rabotti, G., de Ascensao, A. R., & Faoro, F. (2003). Benzothiadiazole-induced resistance modulates ozone tolerance. Journal of Agricultural and Food Chemistry, 51, 4308–4314.Google Scholar
- Iriti, M., Sironi, M., Gomarasca, S., Casazza, A. P., Soave, C., & Faoro, F. (2006). Cell death-mediated antiviral effect of chitosan in tabacco. Plant Physiology and Biochemistry, 44, 893–900.Google Scholar
- Jones, D. P. (2006). Redefining oxidative stress. Antioxidants & Redox Signaling, 8, 1865–1879.Google Scholar
- Jörres, R. A., Holz, O., Zachgo, W., Timm, P., Koschyk, S., Müller, B., & Grimminger, F. (2000). The effect of repeated ozone exposure on inflammatory markers in bronchoalveolar lavage fluid and mucosal biopsies. American Journal of Respiratory Critical Care and Medicine, 161, 1855–1861.Google Scholar
- Kanofsky, J. R., & Simall, P. (1990). Singlet oxygen production from the reactions of ozone with biological molecules. The Journal of Biological Chemistry, 266, 9039–9042.Google Scholar
- Kehrl, H. R., Vincent, L. M., Kowalsky, R. J., Horstman, D. H., O’Neill, J., & McCartney, W. H. (1987). Ozone exposure increases respiratory epithelial permeability in humans. American Reviews of Respiratory Diseases, 135, 1124–1128.Google Scholar
- Kelly, F. J. (2004). Dietary antioxidant and environmental stress. Proceedings of the Nutrition Society, 63, 579–585.Google Scholar
- Kelly, F. J., Dunster, C., & Mudway, I. (2003). Air pollution and the elderly: Oxidant/antioxidant issues worth consideration. European Respiration Journal, 21, 70s–75s.Google Scholar
- Kelly, F. J., Mudway, I., Krishna, M. T., & Holgate, S. T. (1995). The free radical basis of air pollution: Focus on ozone. Respiratory Medicine, 89, 647–656.Google Scholar
- Kerr, J. B., & McElroy, C. T. (1993). Evidence for large trend of ultraviolet-B radiation linked to ozone depletion. Science, 262, 1032–1034.Google Scholar
- Kerstiens, G., & Lendzian, K. J. (1989). Interactions between ozone and plant cuticles. I. Ozone deposition and permeability. New Phytologist, 112, 13–19.Google Scholar
- Kinnula, V. L., & Crapo, J. D. (2003). Superoxide dismutases in the lung and human lung diseases. Journal of Respiratory Critical Care and Medicine, 167, 1600–1619.Google Scholar
- Kley, D., Kleinmann, M., Sandermann, H., & Krupa, S. (1999). Photochemical oxidants: State of the science. Environmental Pollution, 100, 19–42.Google Scholar
- Kluchová, Z., & Tkáĉová, R. (2006). The role of oxidative stress in lung injury induced by cigarette smoke. Biologia, 61, 643–650.Google Scholar
- Koch, J. R., Creelman, R. A., Eshita, S. M., Seskar, M., Mullet, J. E., & Davis, K. R. (2000). Ozone sensitivity in hybrid poplar correlates with insensitivity to both salicylic acid and jasmonic acid: The role of programmed cell death in lesion formation. Plant Physiology, 123, 1–10.Google Scholar
- Koto, H., Aizawa, H., Takata, S., Inoue, H., & Hara, N. (1995). An important role of tachykinin in ozone-induced airway hyperresponsiveness. American Journal of Respiratory Critical Care and Medicine, 151, 1763–1769.Google Scholar
- Krishna, M. T., Springall, D., Meng, Q.-H., Withers, N., Biscione, G., & Frew, A. (1997). Effects of ozone on epithelium and sensory nerves in the bronchial mucosa of healthy humans. American Journal of Respiratory Critical Care and Medicine, 156, 943–950.Google Scholar
- Krupa, S., McGrath, M. T., Andersen, C. P., Booker, F., Burkey, K. O., & Chappelka, A. H. (2000). Ambient ozone and plant health. Plant Disease, 85, 4–12.Google Scholar
- Langebartels, C., Kerner, K., Leonardi, S., Schraudner, M., Trost, M., Heller, W., & Sandermann, H. (2002). Biochemical plant responses to ozone. I. Differential induction of polyamine and ethylene biosynthesis in tobacco. Plant Physiology, 95, 882–889.Google Scholar
- Langebartels, C., Wohlgemuth, H., Kschieschan, S., Grun, S., & Sandermann, H. (1991). Oxidative burst and cell death in ozone-exposed plants. Plant Physiology and Biochemistry, 40, 567–575.Google Scholar
- Langford, S. D., Bidani, A., & Postlethwait, E. M. (1995). Ozone-reactive absorption by pulmonary epithelial lining fluid constituents. Toxicology and Applied Pharmacology, 132, 122–130.Google Scholar
- Law, M. Y., Charles, S. A., & Halliwell, B. (1983). Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. Biochemical Journal, 210, 899–903.Google Scholar
- Lippman, M., & Schlesinger, R. B. (2000). Toxicological bases for the setting of health-related air pollution standards. Annual Reviews of Public Health, 21, 309–333.Google Scholar
- Logan, J. A. (1985). Tropospheric ozone: Seasonal behaviour, trends and anthropogenic influences. Journal of Geophysical Research, 90, 10463–10482.Google Scholar
- Luwe, M. W. F., Takahama, U., & Heber, U. (1993). Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacia oleracia, L.) leaves. Plant Physiology, 101, 969–976.Google Scholar
- Manning, W. J., Flgler, R. B., & Frekel, A. M. (2003). Assessing plant response to ambient O3: Growth of O3-sensitive loblolly pine seedlings treated with EDU and sodium erythorbate. Environmental Pollution, 126, 73–81.Google Scholar
- Marrs, K. A. (1996). The function and regulation of glutathione S-transferases in plants. Annual Reviews of Plant Physiology and Plant Molecular Biology, 47, 127–158.Google Scholar
- Mauzerall, D. L., & Wang, X. (2001). Protecting agricultural crops from the effects of tropospheric ozone exposure: Reconciling science and standard setting in the United States, Europe, and Asia. Annual Reviews of Energy and Environment, 26, 237–268.Google Scholar
- McDonnell, W. F., Stewart, P. W., Smith, M. V., Pan, W. K., & Pan, J. (1999). Ozone-induced respiratory symptoms: Exposure–response models and association with lung function. European Respiratory Journal, 14, 845–853.Google Scholar
- McKinnon, K. P., Madden, M. C., Noah, T. L., & Devlin, R. B. (1993). In vitro ozone exposure increases release of arachidonic acid products from a human bronchial epithelial cell line. Toxicology and Applied Pharmacology, 118, 215–223.Google Scholar
- Mehlhorn, H., O’Shea, J. M., & Wellburn, A. R. (1991). Atmospheric ozone interacts with stress ethylene formation by plants to cause visible plant injury. Plant, Cell and Environment, 13, 971–976.Google Scholar
- Meyer, A., Buhl, R., Kampf, S., & Magnussen, H. (1995). Intravenous N-acetylcysteine and lung glutathione of patients with pulmonary fibrosis and normals. American Journal of Respiratory Critical Care and Medicine, 152, 1055–1060.Google Scholar
- Möller, I. M. (2001). Plant mitochondria and oxidative stress: Electron transport, NADPH turnover and metabolism of reactive oxygen species. Annual Reviews of Plant Physiology and Plant Molecular Biology, 52, 561–591.Google Scholar
- Mudd, J. B., Leavitt, R., Ongun, A., & McManus, T. T. (1969). Reaction of ozone with amino acids and proteins. Atmospheric Environment, 3, 669–682.Google Scholar
- Mudway, I. S., & Kelly, F. J. (2000). Ozone and the lung: A sensitive issue. Molecular Aspects of Medicine, 21, 1–48.Google Scholar
- Mudway, I. S., & Kelly, F. J. (2004). An investigation of inhaled ozone dose and the magnitude of airway inflammation in healthy adults. American Journal of Respiratory Critical Care and Medicine, 169, 1089–1095.Google Scholar
- Müller, C., & Riederer, M. (2005). Plant surface in chemical ecology. Journal of Chemical Ecology, 31, 2621–2651.Google Scholar
- Mustafa, M. G. (1990). Biochemical basis of ozone toxicity. Free Radicals in Biology and Medicine, 9, 245–265.Google Scholar
- Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant, Cell and Physiology, 22, 867–880.Google Scholar
- Nali, C., Paoletti, E., Marabottini, R., Della Rocca, G., Lorenzini, G., & Paolacci, A. R., et al. (2004). Ecophysiological and biochemical strategies of response to ozone in Mediterranean evergreen broadleaf species. Atmospheric Environment, 38, 2247–2257.Google Scholar
- Noctor, G., & Foyer, C. H. (1998). Ascorbate and glutathione: Keeping active oxygen under control. Annual Reviews of Plant Physiology and Plant Molecular Biology, 49, 249–279.Google Scholar
- Ormrod, D. P., & Beckerson, D. W. (1986). Polyamines as antiozonant for tomato. Horticoltural Science, 21, 1070–1071.Google Scholar
- Padh, H. (1990). Cellular functions of ascorbic acid. Biochemistry and Cell Biology, 68, 1166–1173.CrossRefGoogle Scholar
- Paoletti, E. (2006). Impact of ozone on Mediterranean forests: A review. Environmental Pollution, 144, 463–474.Google Scholar
- Passannante, A. N., Hazucha, M. J., Bromberg, P. A., Seal, E., Folinsbee, L., & Koch, G. (1998). Nociceptive mechanisms modulate ozone-induced human lung function decrements. Journal of Applied Physiology, 85, 1863–1870.Google Scholar
- Peden, D. B., Hohman, R., Brown, M. E., Mason, R. T., Berkebile, C., & Fales, H. M. (1990). Uric acid is a major antioxidant in human nasal airway secretions. Proceedings of the National Academy of Sciences of the United States of America, 87, 7638–7642.Google Scholar
- Pell, E. J., Eckardt, N., & Glick, R. E. (1994). Biochemical and molecular basis fort he impairment of photosynthetic potential. Photosynthesis Research, 39, 453–462.Google Scholar
- Platt, U., & Hönninger, G. (2003). The role of halogen species in the troposphere. Chemosphere, 52, 325–338.Google Scholar
- Pryor, W. A. (1992). How far does ozone penetrate into the pulmonary air/tissue boundary before it reacts? Free Radicals in Biology and Medicine, 12, 83–88.Google Scholar
- Pryor, W. A. (1993). Ozone in all reactive splendour. Journal of Laboratory and Clinical Medicine, 122, 483–486.Google Scholar
- Pryor, W. A. (1994). Mechanisms of radical formation from reactions of ozone with target molecules in the lung. Free Radicals in Biology and Medicine, 17, 451–465.Google Scholar
- Pryor, W. A., Das, B., & Church, D. F. (1991). The ozonation of unsaturated fatty acids: Aldehydes and hydrogen peroxide as products and possible mediators of ozone toxicity. Chemical Research and Toxicology, 4, 341–348.Google Scholar
- Quinton, P. M. (1979). Composition and control of secretions from tracheal bronchial submucosal glands. Nature, 279, 551–552.Google Scholar
- Rahman, Q., Abidi, P., Afaq, F., Schiffmann, D., Mossman, B. T., & Kamp, D. V. (1999). Glutathione redox system in oxidative lung injury. Critical Reviews in Toxicology, 29, 543–568.Google Scholar
- Rao, M. V., & Davis, K. R. (1999). Ozone-induced cell death occurs via two distinct mechanisms. The role of salicylic acid. Plant Journal, 16, 603–614.Google Scholar
- Rao, M. V., & Davis, K. R. (2001). The physiology of ozone induced cell death. Planta, 213, 682–690.Google Scholar
- Rao, M. V., Koch, J. R., & Davis, K. R. (2000a). Ozone, a tool for probing programmed cell death in plants. Plant Molecular Biology, 44, 345–358.Google Scholar
- Rao, M. V., Lee, H.-L., & Davis, K. R. (2002). Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. Plant Journal, 32, 447–456.Google Scholar
- Rao, M. V., Lee, H.-L., Creelman, R. A., Mullet, J. E., & Davis, K. R. (2000b). Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell, 12, 1633–1646.Google Scholar
- Rauser, W. E. (1995). Phytochelatines and related peptides. Structure, biosynthesis and function. Plant Physiology, 109, 1141–1149.Google Scholar
- Rautenkranz, A. A. F., Li, L., Mächler, F., Märinoia, E., & Oertli, J. J. (1994). Transport of ascorbic and dehydroascorbic acids across protoplast and vacuole membranes isolated from barley (Hordeum vulgare L. cv Gerbel). Plant Physiology, 106, 187–193.Google Scholar
- Rawlings, A. V. (2006). Ethnic skin types: Are there differences in skin structure and function? International Journal of Cosmetic Science, 28, 79–83.Google Scholar
- Reddy, G. N., Arteca, R. N., Dai, Y. R., Flores, H. E., Negram, F. B., & Pell, E. J. (1994). Changes in ethylene and polyamines in relation to mRNA levels of the large and small subunits of ribulose bisphosphate oxygenase in ozone stressed potato foliage. Plant, Cell and Environment, 120, 819–826.Google Scholar
- Romieu, I., Sienra-Monge, J. J., Ramírez-Anguilar, M., Téllez-Rojo, M. M., Moreno-Marcías, H., & Reyes-Ruiz, N. I. (2002). Antioxidant supplementation and lung functions among children with asthma exposed to high levels of air pollutants. Journal of Respiratory Critical Care and Medicine, 166, 703–709.Google Scholar
- Rowland-Bamford, A. J., Borland, A. M., Lea, P. J., & Mansfield, T. A. (1989). The role of arginine decarboxylase in modulating the sensitivity of barley to ozone. Environmental Pollution, 61, 95–106.Google Scholar
- Royce, F. H., & Plopper, C. G. (1997). Effect of chronic daily ozone exposure on Clara cell secretory protein mRNA expression in the adult rat lung. Experimental Lung Research, 23, 51–64.Google Scholar
- Rustow, B., Haupt, R., Stevens, R. A., & Kinze, D. (1993). Type II pneumocytes secrete vitamin D together with surfactant lipids. American Journal of Physiology, 265, L133–L139.Google Scholar
- Samet, J. M., Hatch, G. E., Horstman, D., Steck-Scott, S., Arab, L., & Bromberg, P. A. (2001). Effect of antioxidant supplementation on ozone-induced lung injury in human subjects. Journal of Respiratory Critical Care and Medicine, 164, 819–825.Google Scholar
- Sandermann, H., Ernst, D., Heller, W., & Langebartels, C. (1998). Ozone: An abiotic elicitor of plant defence reactions. Trends in Plant Science, 3, 47–50.Google Scholar
- Sarnat, J. A., & Holguin, F. (2007). Asthma and air quality. Current Opinion in Pulmonary Medicine, 13, 63–66.Google Scholar
- Schelegle, E. S., Siefkin, A. D., & McDonald, R. J. (1991). Time course of ozone-induced neutrophilia in normal humans. American Reviews in Respiratory Medicine, 143, 1353–1358.Google Scholar
- Schuler, M. A. (1996). Plant cytochrome P450 monooxygenases. Critical Reviews in Plant Science, 15, 235–284.Google Scholar
- Sharma, Y. K., Leon, J., Raskin, I., & Davis, K. R. (1996). Ozone-induced expression of stress-related genes in Arabidopsis thaliana: The role of salicylic acid in the accumulation of defence-related transcripts and induced resistance. Proceedings of the National Academy of Sciences of the United States of America, 93, 5099–5104.Google Scholar
- Smirnoff, N., & Pallanca, J. E. (1995). Ascorbate metabolism in relation to oxidative stress. Biochemical Society Transactions, 24, 472–478.Google Scholar
- Sterner-Kock, A., Kock, M., Braun, R., & Hyde, D. M. (2000). Ozone-induced epithelial injury in the ferret is similar in nonhuman primates. American Journal of Respiratory Critical Care and Medicine, 162, 1152–1156.Google Scholar
- Tabor, C. W., & Tabor, H. (1984). Polyamines. Annual Reviews of Biochemistry, 53, 749–790.Google Scholar
- Takahashi, N., Yu, X., Schofield, B. H., Kleeberger, S. R., Scott, A. L., & Hasegawa, S. (1995). Expression of ICAM-1 in airway epithelium after acute ozone exposure in the mouse. Journal of Applied Physiology, 79, 1753–1761.Google Scholar
- Tepper, J. S., Costa, D. L., Fitzgerald, L., Doerfler, D. L., & Bromberg, P. A. (1993). Role of tachykinins in ozone-induced acute lung injury in guinea pigs. Journal of Applied Physiology, 75, 1404–1411.Google Scholar
- Tingey, D. T., & Hogsett, W. E. (1985). Water stress reduces ozone injury via a stomatal mechanism. Plant Physiology, 77, 944–947.Google Scholar
- Torsethaugen, G., Pell, E. J., & Assmann, S. M. (1999). Ozone inhibits guard cell K + channels implicated in stomatal opening. Proceedings of the National Academy of Sciences of the United States of America, 96, 13577–13582.Google Scholar
- Tuominen, H., Overmyer, K., Keinanen, M., Kollist, H., & Kangasjarvi, J. (2004). Mutual antagonism of ethylene and jasmonic acid regulates ozone-induced spreading cell death in Arabidopsis. Plant Journal, 39, 59–69.Google Scholar
- Van der Vliet, A., O’Neill, C. A., Cross, C. E., Koostra, J. M., Volz, W. G., Halliwell, B., & Louie, S. (1999). Determination of low-molecular-mass antioxidant concentrations in human respiratory tract lining fluids. American Journal of Physiology, 276, L289–L296.Google Scholar
- Van der Vliet, A., & Cross, C. E. (2000). Oxidants, nitrosants and the lungs. American Journal of Medicine, 109, 398–421.Google Scholar
- Violini, G., Maffi, D., Conti, G. G., Faoro, F., & Tornagli, R. (1992). Damage by ambient zone to bean leaves. Histological, histochemical and ultrastructural observations. Rivista Italiana di Patologia Vegetale, 2, 91–110.Google Scholar
- Wang, W.-C., Liang, X.-Z., Dudek, M. P., Pollard, D., & Thompson, S. L. (1995). Atmospheric ozone as climate gas. Atmospheric Research, 37, 247–256.Google Scholar
- Weinmann, G. G., Liu, M. C., Proud, D., Weidenbach-Gerbase, M., Hubbard, W., & Frank, R. (1995). Ozone exposure in humans: Inflammatory, small and peripheral airway responses. American Journal of Respiratory Critical Care and Medicine, 152, 1175–1182.Google Scholar
- Widdicombe, J. (1997). Airway and alveolar permeability and surface liquid thickness: Theory. American Journal of Physiology, 82, 3–12.Google Scholar
- Willekens, H., Inzé, D., Van Montagu, M., & Van Camp, W. (1995). Catalases in plants. Molecular Breeding, 1, 207–228.Google Scholar
- Wojtaszek, P. (1997). Oxidative burst: An early plant response to pathogen infection. Biochemical Journal, 322, 681–692.Google Scholar
- Yu, B. P. (1994). Cellular defenses against damage from reactive oxygen species. Physiological Reviews, 74, 139–162.Google Scholar